Altered Ca2+ Homeostasis in Immune Cells during Aging: Role of Ion Channels
Abstract
:1. Introduction
2. Altered T Cell Function during Aging
3. Orai/STIM
4. TRP Channels
5. Potassium Channels
6. CaV Channels, Voltage Gated Channels
7. Purinergic Receptors
8. Perspectives
Funding
Acknowledgments
Conflicts of Interest
References
- Grubeck-Loebenstein, B.; Berger, P.; Saurwein-Teissl, M.; Zisterer, K.; Wick, G. No immunity for the elderly. Nat. Med. 1998, 4, 870. [Google Scholar] [CrossRef]
- Weinberger, B.; Herndler-Brandstetter, D.; Schwanninger, A.; Weiskopf, D.; Grubeck-Loebenstein, B. Biology of immune responses to vaccines in elderly persons. Clin. Infect. Dis. 2008, 46, 1078–1084. [Google Scholar] [CrossRef]
- Nikolich-Zugich, J. The twilight of immunity: Emerging concepts in aging of the immune system. Nat. Immunol. 2018, 19, 10–19. [Google Scholar] [CrossRef]
- Goodwin, K.; Viboud, C.; Simonsen, L. Antibody response to influenza vaccination in the elderly: A quantitative review. Vaccine 2006, 24, 1159–1169. [Google Scholar] [CrossRef] [PubMed]
- Goronzy, J.J.; Weyand, C.M. Immune aging and autoimmunity. Cell Mol. Life Sci. 2012, 69, 1615–1623. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miller, R.A. Effect of aging on T lymphocyte activation. Vaccine 2000, 18, 1654–1660. [Google Scholar] [CrossRef]
- Haynes, L.; Swain, S.L. Aged-related shifts in T cell homeostasis lead to intrinsic T cell defects. Semin. Immunol. 2012, 24, 350–355. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nikolich-Zugich, J.; Li, G.; Uhrlaub, J.L.; Renkema, K.R.; Smithey, M.J. Age-related changes in CD8 T cell homeostasis and immunity to infection. Semin. Immunol. 2012, 24, 356–364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feske, S.; Wulff, H.; Skolnik, E.Y. Ion channels in innate and adaptive immunity. Annu. Rev. Immunol. 2015, 33, 291–353. [Google Scholar] [CrossRef] [Green Version]
- Trebak, M.; Kinet, J.P. Calcium signalling in T cells. Nat. Rev. Immunol. 2019, 19, 154–169. [Google Scholar] [CrossRef]
- Srikanth, S.; Woo, J.S.; Sun, Z.; Gwack, Y. Immunological Disorders: Regulation of Ca(2+) Signaling in T Lymphocytes. Adv. Exp. Med. Biol. 2017, 993, 397–424. [Google Scholar] [CrossRef] [PubMed]
- Feske, S.; Skolnik, E.Y.; Prakriya, M. Ion channels and transporters in lymphocyte function and immunity. Nat. Rev. Immunol. 2012, 12, 532–547. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oh-Hora, M.; Rao, A. Calcium signaling in lymphocytes. Curr. Opin. Immunol. 2008, 20, 250–258. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hale, J.S.; Boursalian, T.E.; Turk, G.L.; Fink, P.J. Thymic output in aged mice. Proc. Natl. Acad. Sci. USA 2006, 103, 8447–8452. [Google Scholar] [CrossRef] [Green Version]
- Rezzani, R.; Nardo, L.; Favero, G.; Peroni, M.; Rodella, L.F. Thymus and aging: Morphological, radiological, and functional overview. Age 2014, 36, 313–351. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Palmer, D.B. The effect of age on thymic function. Front. Immunol. 2013, 4, 316. [Google Scholar] [CrossRef] [Green Version]
- Li, M.; Yao, D.; Zeng, X.; Kasakovski, D.; Zhang, Y.; Chen, S.; Zha, X.; Li, Y.; Xu, L. Age related human T cell subset evolution and senescence. Immun. Ageing 2019, 16, 24. [Google Scholar] [CrossRef] [Green Version]
- Qi, Q.; Liu, Y.; Cheng, Y.; Glanville, J.; Zhang, D.; Lee, J.Y.; Olshen, R.A.; Weyand, C.M.; Boyd, S.D.; Goronzy, J.J. Diversity and clonal selection in the human T-cell repertoire. Proc. Natl. Acad. Sci. USA 2014, 111, 13139–13144. [Google Scholar] [CrossRef] [Green Version]
- Egorov, E.S.; Kasatskaya, S.A.; Zubov, V.N.; Izraelson, M.; Nakonechnaya, T.O.; Staroverov, D.B.; Angius, A.; Cucca, F.; Mamedov, I.Z.; Rosati, E.; et al. The Changing Landscape of Naive T Cell Receptor Repertoire With Human Aging. Front. Immunol. 2018, 9, 1618. [Google Scholar] [CrossRef] [Green Version]
- Britanova, O.V.; Putintseva, E.V.; Shugay, M.; Merzlyak, E.M.; Turchaninova, M.A.; Staroverov, D.B.; Bolotin, D.A.; Lukyanov, S.; Bogdanova, E.A.; Mamedov, I.Z.; et al. Age-related decrease in TCR repertoire diversity measured with deep and normalized sequence profiling. J. Immunol. 2014, 192, 2689–2698. [Google Scholar] [CrossRef] [Green Version]
- Schwartz, M.D.; Emerson, S.G.; Punt, J.; Goff, W.D. Decreased Naive T-cell Production Leading to Cytokine Storm as Cause of Increased COVID-19 Severity with Comorbidities. Aging Dis. 2020, 11, 742–745. [Google Scholar] [CrossRef] [PubMed]
- Smith, N.L.; Patel, R.K.; Reynaldi, A.; Grenier, J.K.; Wang, J.; Watson, N.B.; Nzingha, K.; Yee Mon, K.J.; Peng, S.A.; Grimson, A.; et al. Developmental Origin Governs CD8(+) T Cell Fate Decisions during Infection. Cell 2018, 174, 117–130.e114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reynaldi, A.; Smith, N.L.; Schlub, T.E.; Tabilas, C.; Venturi, V.; Rudd, B.D.; Davenport, M.P. Fate mapping reveals the age structure of the peripheral T cell compartment. Proc. Natl. Acad. Sci. USA 2019, 116, 3974–3981. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moskowitz, D.M.; Zhang, D.W.; Hu, B.; Le Saux, S.; Yanes, R.E.; Ye, Z.; Buenrostro, J.D.; Weyand, C.M.; Greenleaf, W.J.; Goronzy, J.J. Epigenomics of human CD8 T cell differentiation and aging. Sci. Immunol. 2017, 2, eaag0192. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rane, S.; Hogan, T.; Seddon, B.; Yates, A.J. Age is not just a number: Naive T cells increase their ability to persist in the circulation over time. PLoS Biol. 2018, 16, e2003949. [Google Scholar] [CrossRef]
- Hu, B.; Li, G.; Ye, Z.; Gustafson, C.E.; Tian, L.; Weyand, C.M.; Goronzy, J.J. Transcription factor networks in aged naive CD4 T cells bias lineage differentiation. Aging Cell 2019, 18, e12957. [Google Scholar] [CrossRef] [PubMed]
- Quinn, K.M.; Fox, A.; Harland, K.L.; Russ, B.E.; Li, J.; Nguyen, T.H.O.; Loh, L.; Olshanksy, M.; Naeem, H.; Tsyganov, K.; et al. Age-Related Decline in Primary CD8(+) T Cell Responses Is Associated with the Development of Senescence in Virtual Memory CD8(+) T Cells. Cell Rep. 2018, 23, 3512–3524. [Google Scholar] [CrossRef]
- White, J.T.; Cross, E.W.; Burchill, M.A.; Danhorn, T.; McCarter, M.D.; Rosen, H.R.; O’Connor, B.; Kedl, R.M. Virtual memory T cells develop and mediate bystander protective immunity in an IL-15-dependent manner. Nat. Commun. 2016, 7, 11291. [Google Scholar] [CrossRef] [Green Version]
- Li, G.; Yu, M.; Lee, W.W.; Tsang, M.; Krishnan, E.; Weyand, C.M.; Goronzy, J.J. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat. Med. 2012, 18, 1518–1524. [Google Scholar] [CrossRef]
- Ye, Z.; Li, G.; Kim, C.; Hu, B.; Jadhav, R.R.; Weyand, C.M.; Goronzy, J.J. Regulation of miR-181a expression in T cell aging. Nat. Commun. 2018, 9, 3060. [Google Scholar] [CrossRef]
- Gustafson, C.E.; Cavanagh, M.M.; Jin, J.; Weyand, C.M.; Goronzy, J.J. Functional pathways regulated by microRNA networks in CD8 T-cell aging. Aging Cell 2019, 18, e12879. [Google Scholar] [CrossRef] [PubMed]
- Kim, C.; Jadhav, R.R.; Gustafson, C.E.; Smithey, M.J.; Hirsch, A.J.; Uhrlaub, J.L.; Hildebrand, W.H.; Nikolich-Zugich, J.; Weyand, C.M.; Goronzy, J.J. Defects in Antiviral T Cell Responses Inflicted by Aging-Associated miR-181a Deficiency. Cell Rep. 2019, 29, 2202–2216.e5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, C.; Hu, B.; Jadhav, R.R.; Jin, J.; Zhang, H.; Cavanagh, M.M.; Akondy, R.S.; Ahmed, R.; Weyand, C.M.; Goronzy, J.J. Activation of miR-21-Regulated Pathways in Immune Aging Selects against Signatures Characteristic of Memory T Cells. Cell Rep. 2018, 25, 2148–2162.e5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fukushima, Y.; Minato, N.; Hattori, M. The impact of senescence-associated T cells on immunosenescence and age-related disorders. Inflamm. Regen. 2018, 38, 24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Goronzy, J.J.; Weyand, C.M. Understanding immunosenescence to improve responses to vaccines. Nat. Immunol. 2013, 14, 428–436. [Google Scholar] [CrossRef] [Green Version]
- Luz Correa, B.; Ornaghi, A.P.; Cerutti Muller, G.; Engroff, P.; Pestana Lopes, R.; Gomes da Silva Filho, I.; Bosch, J.A.; Bonorino, C.; Bauer, M.E. The inverted CD4:CD8 ratio is associated with cytomegalovirus, poor cognitive and functional states in older adults. Neuroimmunomodulation 2014, 21, 206–212. [Google Scholar] [CrossRef]
- McBride, J.A.; Striker, R. Imbalance in the game of T cells: What can the CD4/CD8 T-cell ratio tell us about HIV and health? PLoS Pathog. 2017, 13, e1006624. [Google Scholar] [CrossRef] [Green Version]
- Lu, W.; Mehraj, V.; Vyboh, K.; Cao, W.; Li, T.; Routy, J.P. CD4:CD8 ratio as a frontier marker for clinical outcome, immune dysfunction and viral reservoir size in virologically suppressed HIV-positive patients. J. Int AIDS Soc. 2015, 18, 20052. [Google Scholar] [CrossRef]
- Czesnikiewicz-Guzik, M.; Lee, W.W.; Cui, D.; Hiruma, Y.; Lamar, D.L.; Yang, Z.Z.; Ouslander, J.G.; Weyand, C.M.; Goronzy, J.J. T cell subset-specific susceptibility to aging. Clin. Immunol. 2008, 127, 107–118. [Google Scholar] [CrossRef] [Green Version]
- Huang, M.C.; Liao, J.J.; Bonasera, S.; Longo, D.L.; Goetzl, E.J. Nuclear factor-kappaB-dependent reversal of aging-induced alterations in T cell cytokines. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2008, 22, 2142–2150. [Google Scholar] [CrossRef]
- Sakata-Kaneko, S.; Wakatsuki, Y.; Matsunaga, Y.; Usui, T.; Kita, T. Altered Th1/Th2 commitment in human CD4+ T cells with ageing. Clin. Exp. Immunol. 2000, 120, 267–273. [Google Scholar] [CrossRef] [PubMed]
- Dayan, M.; Segal, R.; Globerson, A.; Habut, B.; Shearer, G.M.; Mozes, E. Effect of aging on cytokine production in normal and experimental systemic lupus erythematosus-afflicted mice. Exp. Gerontol. 2000, 35, 225–236. [Google Scholar] [CrossRef]
- Haynes, L.; Maue, A.C. Effects of aging on T cell function. Curr. Opin. Immunol. 2009, 21, 414–417. [Google Scholar] [CrossRef] [PubMed]
- Schmitt, V.; Rink, L.; Uciechowski, P. The Th17/Treg balance is disturbed during aging. Exp. Gerontol. 2013, 48, 1379–1386. [Google Scholar] [CrossRef] [PubMed]
- Schindowski, K.; Frohlich, L.; Maurer, K.; Muller, W.E.; Eckert, A. Age-related impairment of human T lymphocytes’ activation: Specific differences between CD4(+) and CD8(+) subsets. Mech. Ageing Dev. 2002, 123, 375–390. [Google Scholar] [CrossRef] [Green Version]
- Gardner, E.M.; Murasko, D.M. Age-related changes in Type 1 and Type 2 cytokine production in humans. Biogerontology 2002, 3, 271–290. [Google Scholar] [CrossRef] [PubMed]
- Zanni, F.; Vescovini, R.; Biasini, C.; Fagnoni, F.; Zanlari, L.; Telera, A.; Di Pede, P.; Passeri, G.; Pedrazzoni, M.; Passeri, M.; et al. Marked increase with age of type 1 cytokines within memory and effector/cytotoxic CD8+ T cells in humans: A contribution to understand the relationship between inflammation and immunosenescence. Exp. Gerontol. 2003, 38, 981–987. [Google Scholar] [CrossRef]
- Engwerda, C.R.; Fox, B.S.; Handwerger, B.S. Cytokine production by T lymphocytes from young and aged mice. J. Immunol. 1996, 156, 3621–3630. [Google Scholar]
- Ernst, D.N.; Weigle, W.O.; Noonan, D.J.; McQuitty, D.N.; Hobbs, M.V. The age-associated increase in IFN-gamma synthesis by mouse CD8+ T cells correlates with shifts in the frequencies of cell subsets defined by membrane CD44, CD45RB, 3G11, and MEL-14 expression. J. Immunol. 1993, 151, 575–587. [Google Scholar]
- Haynes, L.; Linton, P.J.; Eaton, S.M.; Tonkonogy, S.L.; Swain, S.L. Interleukin 2, but not other common gamma chain-binding cytokines, can reverse the defect in generation of CD4 effector T cells from naive T cells of aged mice. J. Exp. Med. 1999, 190, 1013–1024. [Google Scholar] [CrossRef]
- Adolfsson, O.; Huber, B.T.; Meydani, S.N. Vitamin E-enhanced IL-2 production in old mice: Naive but not memory T cells show increased cell division cycling and IL-2-producing capacity. J. Immunol. 2001, 167, 3809–3817. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Whisler, R.L.; Beiqing, L.; Chen, M. Age-related decreases in IL-2 production by human T cells are associated with impaired activation of nuclear transcriptional factors AP-1 and NF-AT. Cell. Immunol. 1996, 169, 185–195. [Google Scholar] [CrossRef] [PubMed]
- Pieren, D.K.J.; Smits, N.A.M.; van de Garde, M.D.B.; Guichelaar, T. Response kinetics reveal novel features of ageing in murine T cells. Sci. Rep. 2019, 9, 5587. [Google Scholar] [CrossRef] [Green Version]
- Linton, P.J.; Haynes, L.; Klinman, N.R.; Swain, S.L. Antigen-independent changes in naive CD4 T cells with aging. J. Exp. Med. 1996, 184, 1891–1900. [Google Scholar] [CrossRef] [PubMed]
- Fulop, T., Jr.; Gagne, D.; Goulet, A.C.; Desgeorges, S.; Lacombe, G.; Arcand, M.; Dupuis, G. Age-related impairment of p56lck and ZAP-70 activities in human T lymphocytes activated through the TcR/CD3 complex. Exp. Gerontol. 1999, 34, 197–216. [Google Scholar] [CrossRef]
- Tamura, T.; Kunimatsu, T.; Yee, S.T.; Igarashi, O.; Utsuyama, M.; Tanaka, S.; Miyazaki, S.; Hirokawa, K.; Nariuchi, H. Molecular mechanism of the impairment in activation signal transduction in CD4(+) T cells from old mice. Int. Immunol. 2000, 12, 1205–1215. [Google Scholar] [CrossRef] [Green Version]
- Gearing, A.J.; Wadhwa, M.; Perris, A.D. Interleukin 2 stimulates T cell proliferation using a calcium flux. Immunol. Lett. 1985, 10, 297–302. [Google Scholar] [CrossRef]
- Hogan, P.G. Calcium-NFAT transcriptional signalling in T cell activation and T cell exhaustion. Cell Calcium 2017, 63, 66–69. [Google Scholar] [CrossRef] [Green Version]
- Feske, S. Calcium signalling in lymphocyte activation and disease. Nat. Rev. Immunol. 2007, 7, 690–702. [Google Scholar] [CrossRef]
- Fagnoni, F.F.; Vescovini, R.; Mazzola, M.; Bologna, G.; Nigro, E.; Lavagetto, G.; Franceschi, C.; Passeri, M.; Sansoni, P. Expansion of cytotoxic CD8+ CD28- T cells in healthy ageing people, including centenarians. Immunology 1996, 88, 501–507. [Google Scholar] [CrossRef]
- Herndler-Brandstetter, D.; Landgraf, K.; Tzankov, A.; Jenewein, B.; Brunauer, R.; Laschober, G.T.; Parson, W.; Kloss, F.; Gassner, R.; Lepperdinger, G.; et al. The impact of aging on memory T cell phenotype and function in the human bone marrow. J. Leukoc. Biol. 2012, 91, 197–205. [Google Scholar] [CrossRef]
- Westmeier, J.; Paniskaki, K.; Karakose, Z.; Werner, T.; Sutter, K.; Dolff, S.; Overbeck, M.; Limmer, A.; Liu, J.; Zheng, X.; et al. Impaired Cytotoxic CD8(+) T Cell Response in Elderly COVID-19 Patients. mBio 2020, 11. [Google Scholar] [CrossRef]
- Miller, R.A.; Berger, S.B.; Burke, D.T.; Galecki, A.; Garcia, G.G.; Harper, J.M.; Sadighi Akha, A.A. T cells in aging mice: Genetic, developmental, and biochemical analyses. Immunol. Rev. 2005, 205, 94–103. [Google Scholar] [CrossRef] [Green Version]
- Garcia, G.G.; Miller, R.A. Single-cell analyses reveal two defects in peptide-specific activation of naive T cells from aged mice. J. Immunol. 2001, 166, 3151–3157. [Google Scholar] [CrossRef] [Green Version]
- Garcia, G.G.; Miller, R.A. Age-related defects in CD4+ T cell activation reversed by glycoprotein endopeptidase. Eur. J. Immunol. 2003, 33, 3464–3472. [Google Scholar] [CrossRef]
- Angenendt, A.; Steiner, R.; Knorck, A.; Schwar, G.; Konrad, M.; Krause, E.; Lis, A. Orai, STIM, and PMCA contribute to reduced calcium signal generation in CD8(+) T cells of elderly mice. Aging 2020, 12, 3266. [Google Scholar] [CrossRef]
- Hartmann, H.; Eckert, A.; Forstl, H.; Muller, W.E. Similar age-related changes of free intracellular calcium in lymphocytes and central neurons: Effects of Alzheimer’s disease. Eur. Arch. Psychiatry Clin. Neurosci. 1994, 243, 218–223. [Google Scholar] [CrossRef]
- Miller, R.A.; Jacobson, B.; Weil, G.; Simons, E.R. Diminished calcium influx in lectin-stimulated T cells from old mice. J. Cell Physiol. 1987, 132, 337–342. [Google Scholar] [CrossRef]
- Grossmann, A.; Maggio-Price, L.; Jinneman, J.C.; Rabinovitch, P.S. Influence of aging on intracellular free calcium and proliferation of mouse T-cell subsets from various lymphoid organs. Cell Immunol. 1991, 135, 118–131. [Google Scholar] [CrossRef]
- Dobber, R.; Tielemans, M.; de Weerd, H.; Nagelkerken, L. Mel14+ CD4+ T cells from aged mice display functional and phenotypic characteristics of memory cells. Int. Immunol. 1994, 6, 1227–1234. [Google Scholar] [CrossRef]
- Rajasekar, R.; Augustin, A. Antigen-dependent selection of T cells that are able to efficiently regulate free cytoplasmic Ca2+ levels. J. Immunol. 1994, 153, 1037–1045. [Google Scholar]
- Fulop, T., Jr.; Seres, I. Age-related changes in signal transduction. Implications for neuronal transmission and potential for drug intervention. Drugs Aging 1994, 5, 366–390. [Google Scholar] [CrossRef]
- Gupta, S. Membrane signal transduction in T cells in aging humans. Ann. N. Y. Acad. Sci. 1989, 568, 277–282. [Google Scholar] [CrossRef]
- Proust, J.J.; Filburn, C.R.; Harrison, S.A.; Buchholz, M.A.; Nordin, A.A. Age-related defect in signal transduction during lectin activation of murine T lymphocytes. J. Immunol. 1987, 139, 1472–1478. [Google Scholar]
- Panov, A.V.; Gutekunst, C.A.; Leavitt, B.R.; Hayden, M.R.; Burke, J.R.; Strittmatter, W.J.; Greenamyre, J.T. Early mitochondrial calcium defects in Huntington’s disease are a direct effect of polyglutamines. Nat. Neurosci. 2002, 5, 731–736. [Google Scholar] [CrossRef]
- Walter, M.C.; Rossius, M.; Zitzelsberger, M.; Vorgerd, M.; Muller-Felber, W.; Ertl-Wagner, B.; Zhang, Y.; Brinkmeier, H.; Senderek, J.; Schoser, B. 50 years to diagnosis: Autosomal dominant tubular aggregate myopathy caused by a novel STIM1 mutation. Neuromuscul. Disord. 2015, 25, 577–584. [Google Scholar] [CrossRef]
- Nesin, V.; Wiley, G.; Kousi, M.; Ong, E.C.; Lehmann, T.; Nicholl, D.J.; Suri, M.; Shahrizaila, N.; Katsanis, N.; Gaffney, P.M.; et al. Activating mutations in STIM1 and ORAI1 cause overlapping syndromes of tubular myopathy and congenital miosis. Proc. Natl. Acad. Sci. USA 2014, 111, 4197–4202. [Google Scholar] [CrossRef] [Green Version]
- Schuhmann, M.K.; Stegner, D.; Berna-Erro, A.; Bittner, S.; Braun, A.; Kleinschnitz, C.; Stoll, G.; Wiendl, H.; Meuth, S.G.; Nieswandt, B. Stromal interaction molecules 1 and 2 are key regulators of autoreactive T cell activation in murine autoimmune central nervous system inflammation. J. Immunol. 2010, 184, 1536–1542. [Google Scholar] [CrossRef] [Green Version]
- Kaufmann, U.; Shaw, P.J.; Kozhaya, L.; Subramanian, R.; Gaida, K.; Unutmaz, D.; McBride, H.J.; Feske, S. Selective ORAI1 Inhibition Ameliorates Autoimmune Central Nervous System Inflammation by Suppressing Effector but Not Regulatory T Cell Function. J. Immunol. 2016, 196, 573–585. [Google Scholar] [CrossRef] [Green Version]
- Bose, T.; Cieslar-Pobuda, A.; Wiechec, E. Role of ion channels in regulating Ca(2)(+) homeostasis during the interplay between immune and cancer cells. Cell Death Dis. 2015, 6, e1648. [Google Scholar] [CrossRef] [Green Version]
- Putney, J.W., Jr. A model for receptor-regulated calcium entry. Cell Calcium 1986, 7, 1–12. [Google Scholar] [CrossRef]
- Hoth, M.; Penner, R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 1992, 355, 353–356. [Google Scholar] [CrossRef] [PubMed]
- Liou, J.; Kim, M.L.; Heo, W.D.; Jones, J.T.; Myers, J.W.; Ferrell, J.E., Jr.; Meyer, T. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr. Biol. 2005, 15, 1235–1241. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roos, J.; DiGregorio, P.J.; Yeromin, A.V.; Ohlsen, K.; Lioudyno, M.; Zhang, S.; Safrina, O.; Kozak, J.A.; Wagner, S.L.; Cahalan, M.D.; et al. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J. Cell Biol. 2005, 169, 435–445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prakriya, M.; Feske, S.; Gwack, Y.; Srikanth, S.; Rao, A.; Hogan, P.G. Orai1 is an essential pore subunit of the CRAC channel. Nature 2006, 443, 230–233. [Google Scholar] [CrossRef]
- Vig, M.; Peinelt, C.; Beck, A.; Koomoa, D.L.; Rabah, D.; Koblan-Huberson, M.; Kraft, S.; Turner, H.; Fleig, A.; Penner, R.; et al. CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 2006, 312, 1220–1223. [Google Scholar] [CrossRef] [Green Version]
- Zhang, S.L.; Yeromin, A.V.; Zhang, X.H.; Yu, Y.; Safrina, O.; Penna, A.; Roos, J.; Stauderman, K.A.; Cahalan, M.D. Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc. Natl. Acad. Sci. USA 2006, 103, 9357–9362. [Google Scholar] [CrossRef] [Green Version]
- DeHaven, W.I.; Smyth, J.T.; Boyles, R.R.; Putney, J.W., Jr. Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels. J. Biol. Chem. 2007, 282, 17548–17556. [Google Scholar] [CrossRef] [Green Version]
- Lis, A.; Peinelt, C.; Beck, A.; Parvez, S.; Monteilh-Zoller, M.; Fleig, A.; Penner, R. CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties. Curr. Biol. 2007, 17, 794–800. [Google Scholar] [CrossRef] [Green Version]
- Williams, R.T.; Manji, S.S.; Parker, N.J.; Hancock, M.S.; Van Stekelenburg, L.; Eid, J.P.; Senior, P.V.; Kazenwadel, J.S.; Shandala, T.; Saint, R.; et al. Identification and characterization of the STIM (stromal interaction molecule) gene family: Coding for a novel class of transmembrane proteins. Biochem. J. 2001, 357, 673–685. [Google Scholar] [CrossRef]
- Miederer, A.M.; Alansary, D.; Schwar, G.; Lee, P.H.; Jung, M.; Helms, V.; Niemeyer, B.A. A STIM2 splice variant negatively regulates store-operated calcium entry. Nat. Commun. 2015, 6, 6899. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Darbellay, B.; Arnaudeau, S.; Bader, C.R.; Konig, S.; Bernheim, L. STIM1L is a new actin-binding splice variant involved in fast repetitive Ca2+ release. J. Cell Biol. 2011, 194, 335–346. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rana, A.; Yen, M.; Sadaghiani, A.M.; Malmersjo, S.; Park, C.Y.; Dolmetsch, R.E.; Lewis, R.S. Alternative splicing converts STIM2 from an activator to an inhibitor of store-operated calcium channels. J. Cell Biol. 2015, 209, 653–669. [Google Scholar] [CrossRef] [Green Version]
- Bergmeier, W.; Weidinger, C.; Zee, I.; Feske, S. Emerging roles of store-operated Ca(2)(+) entry through STIM and ORAI proteins in immunity, hemostasis and cancer. Channels 2013, 7, 379–391. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schwarz, E.C.; Qu, B.; Hoth, M. Calcium, cancer and killing: The role of calcium in killing cancer cells by cytotoxic T lymphocytes and natural killer cells. Biochim. Biophys. Acta 2013, 1833, 1603–1611. [Google Scholar] [CrossRef] [Green Version]
- Prakriya, M.; Lewis, R.S. Store-Operated Calcium Channels. Physiol. Rev. 2015, 95, 1383–1436. [Google Scholar] [CrossRef] [Green Version]
- Lioudyno, M.I.; Kozak, J.A.; Penna, A.; Safrina, O.; Zhang, S.L.; Sen, D.; Roos, J.; Stauderman, K.A.; Cahalan, M.D. Orai1 and STIM1 move to the immunological synapse and are up-regulated during T cell activation. Proc. Natl. Acad. Sci. USA 2008, 105, 2011–2016. [Google Scholar] [CrossRef] [Green Version]
- Quintana, A.; Schwindling, C.; Wenning, A.S.; Becherer, U.; Rettig, J.; Schwarz, E.C.; Hoth, M. T cell activation requires mitochondrial translocation to the immunological synapse. Proc. Natl. Acad. Sci. USA 2007, 104, 14418–14423. [Google Scholar] [CrossRef] [Green Version]
- Quintana, A.; Pasche, M.; Junker, C.; Al-Ansary, D.; Rieger, H.; Kummerow, C.; Nunez, L.; Villalobos, C.; Meraner, P.; Becherer, U.; et al. Calcium microdomains at the immunological synapse: How ORAI channels, mitochondria and calcium pumps generate local calcium signals for efficient T-cell activation. Embo J. 2011, 30, 3895–3912. [Google Scholar] [CrossRef] [Green Version]
- Barr, V.A.; Bernot, K.M.; Srikanth, S.; Gwack, Y.; Balagopalan, L.; Regan, C.K.; Helman, D.J.; Sommers, C.L.; Oh-Hora, M.; Rao, A.; et al. Dynamic movement of the calcium sensor STIM1 and the calcium channel Orai1 in activated T-cells: Puncta and distal caps. Mol. Biol. Cell 2008, 19, 2802–2817. [Google Scholar] [CrossRef]
- Yen, M.; Lewis, R.S. Numbers count: How STIM and Orai stoichiometry affect store-operated calcium entry. Cell Calcium 2019, 79, 35–43. [Google Scholar] [CrossRef]
- Fahrner, M.; Schindl, R.; Romanin, C. Studies of Structure-Function and Subunit Composition of Orai/STIM Channel. In Calcium Entry Channels in Non-Excitable Cells; Kozak, J.A., Putney, J.W., Jr., Eds.; CRC Press/Taylor & Francis: Boca Raton, FL, USA, 2018; pp. 25–50. [Google Scholar] [CrossRef]
- Lewis, R.S. Store-Operated Calcium Channels: From Function to Structure and Back Again. Cold Spring Harb Perspect. Biol. 2020, 12, a035055. [Google Scholar] [CrossRef] [PubMed]
- Gwack, Y.; Srikanth, S.; Oh-Hora, M.; Hogan, P.G.; Lamperti, E.D.; Yamashita, M.; Gelinas, C.; Neems, D.S.; Sasaki, Y.; Feske, S.; et al. Hair loss and defective T- and B-cell function in mice lacking ORAI1. Mol. Cell Biol. 2008, 28, 5209–5222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oh-Hora, M.; Yamashita, M.; Hogan, P.G.; Sharma, S.; Lamperti, E.; Chung, W.; Prakriya, M.; Feske, S.; Rao, A. Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nat. Immunol. 2008, 9, 432–443. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, K.D.; Srikanth, S.; Yee, M.K.; Mock, D.C.; Lawson, G.W.; Gwack, Y. ORAI1 deficiency impairs activated T cell death and enhances T cell survival. J. Immunol. 2011, 187, 3620–3630. [Google Scholar] [CrossRef] [PubMed]
- Weidinger, C.; Shaw, P.J.; Feske, S. STIM1 and STIM2-mediated Ca(2+) influx regulates antitumour immunity by CD8(+) T cells. EMBO Mol. Med. 2013, 5, 1311–1321. [Google Scholar] [CrossRef] [PubMed]
- Shaw, P.J.; Weidinger, C.; Vaeth, M.; Luethy, K.; Kaech, S.M.; Feske, S. CD4(+) and CD8(+) T cell-dependent antiviral immunity requires STIM1 and STIM2. J. Clin. Investig. 2014, 124, 4549–4563. [Google Scholar] [CrossRef] [Green Version]
- Zhou, X.; Friedmann, K.S.; Lyrmann, H.; Zhou, Y.; Schoppmeyer, R.; Knorck, A.; Mang, S.; Hoxha, C.; Angenendt, A.; Backes, C.S.; et al. A calcium optimum for cytotoxic T lymphocyte and natural killer cell cytotoxicity. J. Physiol. 2018, 596, 2681–2698. [Google Scholar] [CrossRef] [Green Version]
- Hogan, P.G.; Chen, L.; Nardone, J.; Rao, A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 2003, 17, 2205–2232. [Google Scholar] [CrossRef] [Green Version]
- Oh-hora, M.; Rao, A. The calcium/NFAT pathway: Role in development and function of regulatory T cells. Microbes Infect. 2009, 11, 612–619. [Google Scholar] [CrossRef] [Green Version]
- Feske, S.; Gwack, Y.; Prakriya, M.; Srikanth, S.; Puppel, S.H.; Tanasa, B.; Hogan, P.G.; Lewis, R.S.; Daly, M.; Rao, A. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 2006, 441, 179–185. [Google Scholar] [CrossRef] [PubMed]
- Lacruz, R.S.; Feske, S. Diseases caused by mutations in ORAI1 and STIM1. Ann. N. Y. Acad. Sci. 2015, 1356, 45–79. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McCarl, C.A.; Picard, C.; Khalil, S.; Kawasaki, T.; Rother, J.; Papolos, A.; Kutok, J.; Hivroz, C.; Ledeist, F.; Plogmann, K.; et al. ORAI1 deficiency and lack of store-operated Ca2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J. Allergy Clin. Immunol. 2009, 124, 1311–1318.e7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fuchs, S.; Rensing-Ehl, A.; Speckmann, C.; Bengsch, B.; Schmitt-Graeff, A.; Bondzio, I.; Maul-Pavicic, A.; Bass, T.; Vraetz, T.; Strahm, B.; et al. Antiviral and regulatory T cell immunity in a patient with stromal interaction molecule 1 deficiency. J. Immunol. 2012, 188, 1523–1533. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feske, S. ORAI1 and STIM1 deficiency in human and mice: Roles of store-operated Ca2+ entry in the immune system and beyond. Immunol. Rev. 2009, 231, 189–209. [Google Scholar] [CrossRef]
- Vaeth, M.; Yang, J.; Yamashita, M.; Zee, I.; Eckstein, M.; Knosp, C.; Kaufmann, U.; Karoly Jani, P.; Lacruz, R.S.; Flockerzi, V.; et al. ORAI2 modulates store-operated calcium entry and T cell-mediated immunity. Nat. Commun. 2017, 8, 14714. [Google Scholar] [CrossRef] [Green Version]
- Kircher, S.; Merino-Wong, M.; Niemeyer, B.A.; Alansary, D. Profiling calcium signals of in vitro polarized human effector CD4(+) T cells. Biochim. Biophys. Acta Mol. Cell Res. 2018, 1865, 932–943. [Google Scholar] [CrossRef]
- Bertin, S.; Aoki-Nonaka, Y.; de Jong, P.R.; Nohara, L.L.; Xu, H.; Stanwood, S.R.; Srikanth, S.; Lee, J.; To, K.; Abramson, L.; et al. The ion channel TRPV1 regulates the activation and proinflammatory properties of CD4(+) T cells. Nat. Immunol. 2014, 15, 1055–1063. [Google Scholar] [CrossRef]
- Majhi, R.K.; Sahoo, S.S.; Yadav, M.; Pratheek, B.M.; Chattopadhyay, S.; Goswami, C. Functional expression of TRPV channels in T cells and their implications in immune regulation. FEBS J. 2015, 282, 2661–2681. [Google Scholar] [CrossRef]
- Ferioli, S.; Zierler, S.; Zaisserer, J.; Schredelseker, J.; Gudermann, T.; Chubanov, V. TRPM6 and TRPM7 differentially contribute to the relief of heteromeric TRPM6/7 channels from inhibition by cytosolic Mg(2+) and Mg.ATP. Sci. Rep. 2017, 7, 8806. [Google Scholar] [CrossRef]
- Li, M.; Jiang, J.; Yue, L. Functional characterization of homo- and heteromeric channel kinases TRPM6 and TRPM7. J. Gen. Physiol. 2006, 127, 525–537. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Philipp, S.; Strauss, B.; Hirnet, D.; Wissenbach, U.; Mery, L.; Flockerzi, V.; Hoth, M. TRPC3 mediates T-cell receptor-dependent calcium entry in human T-lymphocytes. J. Biol. Chem. 2003, 278, 26629–26638. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wenning, A.S.; Neblung, K.; Strauss, B.; Wolfs, M.J.; Sappok, A.; Hoth, M.; Schwarz, E.C. TRP expression pattern and the functional importance of TRPC3 in primary human T-cells. Biochim. Biophys. Acta 2011, 1813, 412–423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Lu, Z.H.; Gabius, H.J.; Rohowsky-Kochan, C.; Ledeen, R.W.; Wu, G. Cross-linking of GM1 ganglioside by galectin-1 mediates regulatory T cell activity involving TRPC5 channel activation: Possible role in suppressing experimental autoimmune encephalomyelitis. J. Immunol. 2009, 182, 4036–4045. [Google Scholar] [CrossRef] [Green Version]
- Syed Mortadza, S.A.; Wang, L.; Li, D.; Jiang, L.H. TRPM2 Channel-Mediated ROS-Sensitive Ca(2+) Signaling Mechanisms in Immune Cells. Front. Immunol. 2015, 6, 407. [Google Scholar] [CrossRef] [Green Version]
- Wehrhahn, J.; Kraft, R.; Harteneck, C.; Hauschildt, S. Transient receptor potential melastatin 2 is required for lipopolysaccharide-induced cytokine production in human monocytes. J. Immunol. 2010, 184, 2386–2393. [Google Scholar] [CrossRef] [Green Version]
- Beck, A.; Kolisek, M.; Bagley, L.A.; Fleig, A.; Penner, R. Nicotinic acid adenine dinucleotide phosphate and cyclic ADP-ribose regulate TRPM2 channels in T lymphocytes. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2006, 20, 962–964. [Google Scholar] [CrossRef] [Green Version]
- Guse, A.H.; da Silva, C.P.; Berg, I.; Skapenko, A.L.; Weber, K.; Heyer, P.; Hohenegger, M.; Ashamu, G.A.; Schulze-Koops, H.; Potter, B.V.; et al. Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature 1999, 398, 70–73. [Google Scholar] [CrossRef]
- Melzer, N.; Hicking, G.; Gobel, K.; Wiendl, H. TRPM2 cation channels modulate T cell effector functions and contribute to autoimmune CNS inflammation. PLoS ONE 2012, 7, e47617. [Google Scholar] [CrossRef]
- Yamamoto, S.; Shimizu, S.; Kiyonaka, S.; Takahashi, N.; Wajima, T.; Hara, Y.; Negoro, T.; Hiroi, T.; Kiuchi, Y.; Okada, T.; et al. TRPM2-mediated Ca2+influx induces chemokine production in monocytes that aggravates inflammatory neutrophil infiltration. Nat. Med. 2008, 14, 738–747. [Google Scholar] [CrossRef]
- Di, A.; Gao, X.P.; Qian, F.; Kawamura, T.; Han, J.; Hecquet, C.; Ye, R.D.; Vogel, S.M.; Malik, A.B. The redox-sensitive cation channel TRPM2 modulates phagocyte ROS production and inflammation. Nat. Immunol. 2011, 13, 29–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zuo, L.; Prather, E.R.; Stetskiv, M.; Garrison, D.E.; Meade, J.R.; Peace, T.I.; Zhou, T. Inflammaging and Oxidative Stress in Human Diseases: From Molecular Mechanisms to Novel Treatments. Int. J. Mol. Sci. 2019, 20, 4472. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kakae, M.; Miyanohara, J.; Morishima, M.; Nagayasu, K.; Mori, Y.; Shirakawa, H.; Kaneko, S. Pathophysiological Role of TRPM2 in Age-Related Cognitive Impairment in Mice. Neuroscience 2019, 408, 204–213. [Google Scholar] [CrossRef] [PubMed]
- Launay, P.; Cheng, H.; Srivatsan, S.; Penner, R.; Fleig, A.; Kinet, J.P. TRPM4 regulates calcium oscillations after T cell activation. Science 2004, 306, 1374–1377. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shimizu, T.; Owsianik, G.; Freichel, M.; Flockerzi, V.; Nilius, B.; Vennekens, R. TRPM4 regulates migration of mast cells in mice. Cell Calcium 2009, 45, 226–232. [Google Scholar] [CrossRef] [PubMed]
- Barbet, G.; Demion, M.; Moura, I.C.; Serafini, N.; Leger, T.; Vrtovsnik, F.; Monteiro, R.C.; Guinamard, R.; Kinet, J.P.; Launay, P. The calcium-activated nonselective cation channel TRPM4 is essential for the migration but not the maturation of dendritic cells. Nat. Immunol. 2008, 9, 1148–1156. [Google Scholar] [CrossRef] [Green Version]
- Launay, P.; Fleig, A.; Perraud, A.L.; Scharenberg, A.M.; Penner, R.; Kinet, J.P. TRPM4 is a Ca2+-activated nonselective cation channel mediating cell membrane depolarization. Cell 2002, 109, 397–407. [Google Scholar] [CrossRef] [Green Version]
- Weber, K.S.; Hildner, K.; Murphy, K.M.; Allen, P.M. Trpm4 differentially regulates Th1 and Th2 function by altering calcium signaling and NFAT localization. J. Immunol. 2010, 185, 2836–2846. [Google Scholar] [CrossRef]
- Zhang, X.; Brunner, T.; Carter, L.; Dutton, R.W.; Rogers, P.; Bradley, L.; Sato, T.; Reed, J.C.; Green, D.; Swain, S.L. Unequal death in T helper cell (Th)1 and Th2 effectors: Th1, but not Th2, effectors undergo rapid Fas/FasL-mediated apoptosis. J. Exp. Med. 1997, 185, 1837–1849. [Google Scholar] [CrossRef]
- Serafini, N.; Dahdah, A.; Barbet, G.; Demion, M.; Attout, T.; Gautier, G.; Arcos-Fajardo, M.; Souchet, H.; Jouvin, M.H.; Vrtovsnik, F.; et al. The TRPM4 channel controls monocyte and macrophage, but not neutrophil, function for survival in sepsis. J. Immunol. 2012, 189, 3689–3699. [Google Scholar] [CrossRef]
- Vennekens, R.; Olausson, J.; Meissner, M.; Bloch, W.; Mathar, I.; Philipp, S.E.; Schmitz, F.; Weissgerber, P.; Nilius, B.; Flockerzi, V.; et al. Increased IgE-dependent mast cell activation and anaphylactic responses in mice lacking the calcium-activated nonselective cation channel TRPM4. Nat. Immunol. 2007, 8, 312–320. [Google Scholar] [CrossRef] [Green Version]
- Rixecker, T.; Mathar, I.; Medert, R.; Mannebach, S.; Pfeifer, A.; Lipp, P.; Tsvilovskyy, V.; Freichel, M. TRPM4-mediated control of FcepsilonRI-evoked Ca(2+) elevation comprises enhanced plasmalemmal trafficking of TRPM4 channels in connective tissue type mast cells. Sci. Rep. 2016, 6, 32981. [Google Scholar] [CrossRef] [Green Version]
- Nadler, M.J.; Hermosura, M.C.; Inabe, K.; Perraud, A.L.; Zhu, Q.; Stokes, A.J.; Kurosaki, T.; Kinet, J.P.; Penner, R.; Scharenberg, A.M.; et al. LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 2001, 411, 590–595. [Google Scholar] [CrossRef] [PubMed]
- Runnels, L.W.; Yue, L.; Clapham, D.E. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 2001, 291, 1043–1047. [Google Scholar] [CrossRef] [PubMed]
- Schmitz, C.; Perraud, A.L.; Johnson, C.O.; Inabe, K.; Smith, M.K.; Penner, R.; Kurosaki, T.; Fleig, A.; Scharenberg, A.M. Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 2003, 114, 191–200. [Google Scholar] [CrossRef] [Green Version]
- Chubanov, V.; Mittermeier, L.; Gudermann, T. Role of kinase-coupled TRP channels in mineral homeostasis. Pharm. Ther. 2018, 184, 159–176. [Google Scholar] [CrossRef]
- Abumaria, N.; Li, W.; Liu, Y. TRPM7 functions in non-neuronal and neuronal systems: Perspectives on its role in the adult brain. Behav. Brain Res. 2018, 340, 81–86. [Google Scholar] [CrossRef] [PubMed]
- Nadolni, W.; Zierler, S. The Channel-Kinase TRPM7 as Novel Regulator of Immune System Homeostasis. Cells 2018, 7, 109. [Google Scholar] [CrossRef] [Green Version]
- Sun, H.S. Role of TRPM7 in cerebral ischaemia and hypoxia. J. Physiol. 2017, 595, 3077–3083. [Google Scholar] [CrossRef] [Green Version]
- Komiya, Y.; Runnels, L.W. TRPM channels and magnesium in early embryonic development. Int. J. Dev. Biol. 2015, 59, 281–288. [Google Scholar] [CrossRef]
- Fleig, A.; Chubanov, V. Trpm7. Handb. Exp. Pharmacol. 2014, 222, 521–546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schmitz, C.; Brandao, K.; Perraud, A.L. The channel-kinase TRPM7, revealing the untold story of Mg(2+) in cellular signaling. Magnes Res. 2014, 27, 9–15. [Google Scholar] [CrossRef] [PubMed]
- Jin, J.; Desai, B.N.; Navarro, B.; Donovan, A.; Andrews, N.C.; Clapham, D.E. Deletion of Trpm7 disrupts embryonic development and thymopoiesis without altering Mg2+ homeostasis. Science 2008, 322, 756–760. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beesetty, P.; Wieczerzak, K.B.; Gibson, J.N.; Kaitsuka, T.; Luu, C.T.; Matsushita, M.; Kozak, J.A. Inactivation of TRPM7 kinase in mice results in enlarged spleens, reduced T-cell proliferation and diminished store-operated calcium entry. Sci. Rep. 2018, 8, 3023. [Google Scholar] [CrossRef] [PubMed]
- Romagnani, A.; Vettore, V.; Rezzonico-Jost, T.; Hampe, S.; Rottoli, E.; Nadolni, W.; Perotti, M.; Meier, M.A.; Hermanns, C.; Geiger, S.; et al. TRPM7 kinase activity is essential for T cell colonization and alloreactivity in the gut. Nat. Commun. 2017, 8, 1917. [Google Scholar] [CrossRef] [PubMed]
- Desai, B.N.; Krapivinsky, G.; Navarro, B.; Krapivinsky, L.; Carter, B.C.; Febvay, S.; Delling, M.; Penumaka, A.; Ramsey, I.S.; Manasian, Y.; et al. Cleavage of TRPM7 releases the kinase domain from the ion channel and regulates its participation in Fas-induced apoptosis. Dev. Cell 2012, 22, 1149–1162. [Google Scholar] [CrossRef] [Green Version]
- Faouzi, M.; Kilch, T.; Horgen, F.D.; Fleig, A.; Penner, R. The TRPM7 channel kinase regulates store-operated calcium entry. J. Physiol. 2017, 595, 3165–3180. [Google Scholar] [CrossRef] [Green Version]
- Suzuki, S.; Lis, A.; Schmitz, C.; Penner, R.; Fleig, A. The TRPM7 kinase limits receptor-induced calcium release by regulating heterotrimeric G-proteins. Cell Mol. Life Sci. 2018, 75, 3069–3078. [Google Scholar] [CrossRef]
- Mangan, P.R.; Harrington, L.E.; O’Quinn, D.B.; Helms, W.S.; Bullard, D.C.; Elson, C.O.; Hatton, R.D.; Wahl, S.M.; Schoeb, T.R.; Weaver, C.T. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006, 441, 231–234. [Google Scholar] [CrossRef]
- Zheng, S.G.; Gray, J.D.; Ohtsuka, K.; Yamagiwa, S.; Horwitz, D.A. Generation ex vivo of TGF-beta-producing regulatory T cells from CD4+CD25- precursors. J. Immunol. 2002, 169, 4183–4189. [Google Scholar] [CrossRef] [Green Version]
- Veldhoen, M.; Hocking, R.J.; Atkins, C.J.; Locksley, R.M.; Stockinger, B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24, 179–189. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, L.; Kitani, A.; Fuss, I.; Strober, W. Cutting edge: Regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J. Immunol. 2007, 178, 6725–6729. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, H.; Li, Z.; Yang, X.O.; Chang, S.H.; Nurieva, R.; Wang, Y.H.; Wang, Y.; Hood, L.; Zhu, Z.; Tian, Q.; et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 2005, 6, 1133–1141. [Google Scholar] [CrossRef] [PubMed]
- Sakaguchi, S.; Sakaguchi, N.; Asano, M.; Itoh, M.; Toda, M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995, 155, 1151–1164. [Google Scholar] [PubMed]
- Lee, G.R. The Balance of Th17 versus Treg Cells in Autoimmunity. Int. J. Mol. Sci. 2018, 19, 730. [Google Scholar] [CrossRef] [Green Version]
- Franceschi, C.; Bonafe, M.; Valensin, S.; Olivieri, F.; De Luca, M.; Ottaviani, E.; De Benedictis, G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 2000, 908, 244–254. [Google Scholar] [CrossRef]
- Franceschi, C.; Capri, M.; Monti, D.; Giunta, S.; Olivieri, F.; Sevini, F.; Panourgia, M.P.; Invidia, L.; Celani, L.; Scurti, M.; et al. Inflammaging and anti-inflammaging: A systemic perspective on aging and longevity emerged from studies in humans. Mech. Ageing Dev. 2007, 128, 92–105. [Google Scholar] [CrossRef] [PubMed]
- Medzhitov, R. Origin and physiological roles of inflammation. Nature 2008, 454, 428–435. [Google Scholar] [CrossRef] [PubMed]
- Franceschi, C.; Campisi, J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69 (Suppl. 1), S4–S9. [Google Scholar] [CrossRef]
- Bettelli, E.; Carrier, Y.; Gao, W.; Korn, T.; Strom, T.B.; Oukka, M.; Weiner, H.L.; Kuchroo, V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441, 235–238. [Google Scholar] [CrossRef]
- van der Geest, K.S.; Abdulahad, W.H.; Tete, S.M.; Lorencetti, P.G.; Horst, G.; Bos, N.A.; Kroesen, B.J.; Brouwer, E.; Boots, A.M. Aging disturbs the balance between effector and regulatory CD4+ T cells. Exp. Gerontol. 2014, 60, 190–196. [Google Scholar] [CrossRef] [PubMed]
- Beeton, C.; Chandy, K.G. Potassium channels, memory T cells, and multiple sclerosis. Neuroscientist 2005, 11, 550–562. [Google Scholar] [CrossRef] [PubMed]
- Panyi, G. Biophysical and pharmacological aspects of K+ channels in T lymphocytes. Eur. Biophys. J. 2005, 34, 515–529. [Google Scholar] [CrossRef] [PubMed]
- Wulff, H.; Beeton, C.; Chandy, K.G. Potassium channels as therapeutic targets for autoimmune disorders. Curr. Opin. Drug Discov. Devel. 2003, 6, 640–647. [Google Scholar] [PubMed]
- Beeton, C.; Pennington, M.W.; Wulff, H.; Singh, S.; Nugent, D.; Crossley, G.; Khaytin, I.; Calabresi, P.A.; Chen, C.Y.; Gutman, G.A.; et al. Targeting effector memory T cells with a selective peptide inhibitor of Kv1.3 channels for therapy of autoimmune diseases. Mol. Pharmacol. 2005, 67, 1369–1381. [Google Scholar] [CrossRef] [PubMed]
- Beeton, C.; Wulff, H.; Standifer, N.E.; Azam, P.; Mullen, K.M.; Pennington, M.W.; Kolski-Andreaco, A.; Wei, E.; Grino, A.; Counts, D.R.; et al. Kv1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc. Natl. Acad. Sci. USA 2006, 103, 17414–17419. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ghanshani, S.; Wulff, H.; Miller, M.J.; Rohm, H.; Neben, A.; Gutman, G.A.; Cahalan, M.D.; Chandy, K.G. Up-regulation of the IKCa1 potassium channel during T-cell activation. Molecular mechanism and functional consequences. J. Biol. Chem. 2000, 275, 37137–37149. [Google Scholar] [CrossRef] [Green Version]
- Liu, Q.H.; Fleischmann, B.K.; Hondowicz, B.; Maier, C.C.; Turka, L.A.; Yui, K.; Kotlikoff, M.I.; Wells, A.D.; Freedman, B.D. Modulation of Kv channel expression and function by TCR and costimulatory signals during peripheral CD4(+) lymphocyte differentiation. J. Exp. Med. 2002, 196, 897–909. [Google Scholar] [CrossRef] [Green Version]
- Wulff, H.; Calabresi, P.A.; Allie, R.; Yun, S.; Pennington, M.; Beeton, C.; Chandy, K.G. The voltage-gated Kv1.3 K(+) channel in effector memory T cells as new target for MS. J. Clin. Investig. 2003, 111, 1703–1713. [Google Scholar] [CrossRef] [Green Version]
- Fanger, C.M.; Neben, A.L.; Cahalan, M.D. Differential Ca2+ influx, KCa channel activity, and Ca2+ clearance distinguish Th1 and Th2 lymphocytes. J. Immunol. 2000, 164, 1153–1160. [Google Scholar] [CrossRef] [Green Version]
- Di, L.; Srivastava, S.; Zhdanova, O.; Ding, Y.; Li, Z.; Wulff, H.; Lafaille, M.; Skolnik, E.Y. Inhibition of the K+ channel KCa3.1 ameliorates T cell-mediated colitis. Proc. Natl. Acad. Sci. USA 2010, 107, 1541–1546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pennington, M.W.; Beeton, C.; Galea, C.A.; Smith, B.J.; Chi, V.; Monaghan, K.P.; Garcia, A.; Rangaraju, S.; Giuffrida, A.; Plank, D.; et al. Engineering a stable and selective peptide blocker of the Kv1.3 channel in T lymphocytes. Mol. Pharmacol. 2009, 75, 762–773. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kalman, K.; Pennington, M.W.; Lanigan, M.D.; Nguyen, A.; Rauer, H.; Mahnir, V.; Paschetto, K.; Kem, W.R.; Grissmer, S.; Gutman, G.A.; et al. ShK-Dap22, a potent Kv1.3-specific immunosuppressive polypeptide. J. Biol. Chem. 1998, 273, 32697–32707. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wulff, H.; Miller, M.J.; Hansel, W.; Grissmer, S.; Cahalan, M.D.; Chandy, K.G. Design of a potent and selective inhibitor of the intermediate-conductance Ca2+-activated K+ channel, IKCa1: A potential immunosuppressant. Proc. Natl. Acad. Sci. USA 2000, 97, 8151–8156. [Google Scholar] [CrossRef] [Green Version]
- Mestas, J.; Hughes, C.C. Of mice and not men: Differences between mouse and human immunology. J. Immunol. 2004, 172, 2731–2738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Verheugen, J.A.; Le Deist, F.; Devignot, V.; Korn, H. Enhancement of calcium signaling and proliferation responses in activated human T lymphocytes. Inhibitory effects of K+ channel block by charybdotoxin depend on the T cell activation state. Cell Calcium 1997, 21, 1–17. [Google Scholar] [CrossRef]
- Hu, L.; Pennington, M.; Jiang, Q.; Whartenby, K.A.; Calabresi, P.A. Characterization of the functional properties of the voltage-gated potassium channel Kv1.3 in human CD4+ T lymphocytes. J. Immunol. 2007, 179, 4563–4570. [Google Scholar] [CrossRef] [Green Version]
- Koch Hansen, L.; Sevelsted-Moller, L.; Rabjerg, M.; Larsen, D.; Hansen, T.P.; Klinge, L.; Wulff, H.; Knudsen, T.; Kjeldsen, J.; Kohler, R. Expression of T-cell KV1.3 potassium channel correlates with pro-inflammatory cytokines and disease activity in ulcerative colitis. J. Crohns Colitis 2014, 8, 1378–1391. [Google Scholar] [CrossRef]
- Chandy, K.G.; Wulff, H.; Beeton, C.; Pennington, M.; Gutman, G.A.; Cahalan, M.D. K+ channels as targets for specific immunomodulation. Trends Pharmacol. Sci. 2004, 25, 280–289. [Google Scholar] [CrossRef] [Green Version]
- Matheu, M.P.; Beeton, C.; Garcia, A.; Chi, V.; Rangaraju, S.; Safrina, O.; Monaghan, K.; Uemura, M.I.; Li, D.; Pal, S.; et al. Imaging of effector memory T cells during a delayed-type hypersensitivity reaction and suppression by Kv1.3 channel block. Immunity 2008, 29, 602–614. [Google Scholar] [CrossRef] [Green Version]
- Hu, L.; Wang, T.; Gocke, A.R.; Nath, A.; Zhang, H.; Margolick, J.B.; Whartenby, K.A.; Calabresi, P.A. Blockade of Kv1.3 potassium channels inhibits differentiation and granzyme B secretion of human CD8+ T effector memory lymphocytes. PLoS ONE 2013, 8, e54267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Panyi, G.; Vamosi, G.; Bacso, Z.; Bagdany, M.; Bodnar, A.; Varga, Z.; Gaspar, R.; Matyus, L.; Damjanovich, S. Kv1.3 potassium channels are localized in the immunological synapse formed between cytotoxic and target cells. Proc. Natl. Acad. Sci. USA 2004, 101, 1285–1290. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, X.; McElhaney, J.E. Age-related changes in memory and effector T cells responding to influenza A/H3N2 and pandemic A/H1N1 strains in humans. Vaccine 2011, 29, 2169–2177. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kollar, S.; Berta, L.; Vasarhelyi, Z.E.; Balog, A.; Vasarhelyi, B.; Rigo, J., Jr.; Toldi, G. Impact of aging on calcium influx and potassium channel characteristics of T lymphocytes. Oncotarget 2015, 6, 13750–13756. [Google Scholar] [CrossRef] [Green Version]
- Eil, R.; Vodnala, S.K.; Clever, D.; Klebanoff, C.A.; Sukumar, M.; Pan, J.H.; Palmer, D.C.; Gros, A.; Yamamoto, T.N.; Patel, S.J.; et al. Ionic immune suppression within the tumour microenvironment limits T cell effector function. Nature 2016, 537, 539–543. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Zhang, X.; Xue, L.; Xing, J.; Jouvin, M.H.; Putney, J.W.; Anderson, M.P.; Trebak, M.; Kinet, J.P. Low-Voltage-Activated CaV3.1 Calcium Channels Shape T Helper Cell Cytokine Profiles. Immunity 2016, 44, 782–794. [Google Scholar] [CrossRef] [Green Version]
- Matza, D.; Badou, A.; Klemic, K.G.; Stein, J.; Govindarajulu, U.; Nadler, M.J.; Kinet, J.P.; Peled, A.; Shapira, O.M.; Kaczmarek, L.K.; et al. T Cell Receptor Mediated Calcium Entry Requires Alternatively Spliced Cav1.1 Channels. PLoS ONE 2016, 11, e0147379. [Google Scholar] [CrossRef] [Green Version]
- Badou, A.; Jha, M.K.; Matza, D.; Mehal, W.Z.; Freichel, M.; Flockerzi, V.; Flavell, R.A. Critical role for the beta regulatory subunits of Cav channels in T lymphocyte function. Proc. Natl. Acad. Sci. USA 2006, 103, 15529–15534. [Google Scholar] [CrossRef] [Green Version]
- Jha, M.K.; Badou, A.; Meissner, M.; McRory, J.E.; Freichel, M.; Flockerzi, V.; Flavell, R.A. Defective survival of naive CD8+ T lymphocytes in the absence of the beta3 regulatory subunit of voltage-gated calcium channels. Nat. Immunol. 2009, 10, 1275–1282. [Google Scholar] [CrossRef] [Green Version]
- Omilusik, K.; Priatel, J.J.; Chen, X.; Wang, Y.T.; Xu, H.; Choi, K.B.; Gopaul, R.; McIntyre-Smith, A.; Teh, H.S.; Tan, R.; et al. The Ca(v)1.4 calcium channel is a critical regulator of T cell receptor signaling and naive T cell homeostasis. Immunity 2011, 35, 349–360. [Google Scholar] [CrossRef] [Green Version]
- Robert, V.; Triffaux, E.; Paulet, P.E.; Guery, J.C.; Pelletier, L.; Savignac, M. Protein kinase C-dependent activation of CaV1.2 channels selectively controls human TH2-lymphocyte functions. J. Allergy Clin. Immunol. 2014, 133, 1175–1183. [Google Scholar] [CrossRef] [PubMed]
- Kotturi, M.F.; Carlow, D.A.; Lee, J.C.; Ziltener, H.J.; Jefferies, W.A. Identification and functional characterization of voltage-dependent calcium channels in T lymphocytes. J. Biol. Chem. 2003, 278, 46949–46960. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stokes, L.; Gordon, J.; Grafton, G. Non-voltage-gated L-type Ca2+ channels in human T cells: Pharmacology and molecular characterization of the major alpha pore-forming and auxiliary beta-subunits. J. Biol. Chem. 2004, 279, 19566–19573. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tan, G.M.; Yu, D.; Wang, J.; Soong, T.W. Alternative splicing at C terminus of Ca(V)1.4 calcium channel modulates calcium-dependent inactivation, activation potential, and current density. J. Biol. Chem. 2012, 287, 832–847. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cabral, M.D.; Paulet, P.E.; Robert, V.; Gomes, B.; Renoud, M.L.; Savignac, M.; Leclerc, C.; Moreau, M.; Lair, D.; Langelot, M.; et al. Knocking down Cav1 calcium channels implicated in Th2 cell activation prevents experimental asthma. Am. J. Respir. Crit. Care Med. 2010, 181, 1310–1317. [Google Scholar] [CrossRef]
- Di Virgilio, F.; Dal Ben, D.; Sarti, A.C.; Giuliani, A.L.; Falzoni, S. The P2X7 Receptor in Infection and Inflammation. Immunity 2017, 47, 15–31. [Google Scholar] [CrossRef] [Green Version]
- Savio, L.E.B.; de Andrade Mello, P.; da Silva, C.G.; Coutinho-Silva, R. The P2X7 Receptor in Inflammatory Diseases: Angel or Demon? Front. Pharmacol. 2018, 9, 52. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Virgilio, F.; Chiozzi, P.; Ferrari, D.; Falzoni, S.; Sanz, J.M.; Morelli, A.; Torboli, M.; Bolognesi, G.; Baricordi, O.R. Nucleotide receptors: An emerging family of regulatory molecules in blood cells. Blood 2001, 97, 587–600. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- North, R.A. Molecular physiology of P2X receptors. Physiol. Rev. 2002, 82, 1013–1067. [Google Scholar] [CrossRef] [PubMed]
- Yip, L.; Woehrle, T.; Corriden, R.; Hirsh, M.; Chen, Y.; Inoue, Y.; Ferrari, V.; Insel, P.A.; Junger, W.G. Autocrine regulation of T-cell activation by ATP release and P2X7 receptors. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2009, 23, 1685–1693. [Google Scholar] [CrossRef] [Green Version]
- Borges da Silva, H.; Beura, L.K.; Wang, H.; Hanse, E.A.; Gore, R.; Scott, M.C.; Walsh, D.A.; Block, K.E.; Fonseca, R.; Yan, Y.; et al. The purinergic receptor P2RX7 directs metabolic fitness of long-lived memory CD8(+) T cells. Nature 2018, 559, 264–268. [Google Scholar] [CrossRef] [PubMed]
- Schenk, U.; Westendorf, A.M.; Radaelli, E.; Casati, A.; Ferro, M.; Fumagalli, M.; Verderio, C.; Buer, J.; Scanziani, E.; Grassi, F. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 2008, 1, ra6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cekic, C.; Linden, J. Purinergic regulation of the immune system. Nat. Rev. Immunol. 2016, 16, 177–192. [Google Scholar] [CrossRef] [PubMed]
- Onnis, A.; Baldari, C.T. Orchestration of Immunological Synapse Assembly by Vesicular Trafficking. Front. Cell Dev. Biol. 2019, 7, 110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Woehrle, T.; Yip, L.; Elkhal, A.; Sumi, Y.; Chen, Y.; Yao, Y.; Insel, P.A.; Junger, W.G. Pannexin-1 hemichannel-mediated ATP release together with P2X1 and P2X4 receptors regulate T-cell activation at the immune synapse. Blood 2010, 116, 3475–3484. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Surprenant, A.; Rassendren, F.; Kawashima, E.; North, R.A.; Buell, G. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 1996, 272, 735–738. [Google Scholar] [CrossRef]
- Chessell, I.P.; Hatcher, J.P.; Bountra, C.; Michel, A.D.; Hughes, J.P.; Green, P.; Egerton, J.; Murfin, M.; Richardson, J.; Peck, W.L.; et al. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005, 114, 386–396. [Google Scholar] [CrossRef]
- Schenk, U.; Frascoli, M.; Proietti, M.; Geffers, R.; Traggiai, E.; Buer, J.; Ricordi, C.; Westendorf, A.M.; Grassi, F. ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Sci. Signal. 2011, 4, ra12. [Google Scholar] [CrossRef]
- Manohar, M.; Hirsh, M.I.; Chen, Y.; Woehrle, T.; Karande, A.A.; Junger, W.G. ATP release and autocrine signaling through P2X4 receptors regulate gammadelta T cell activation. J. Leukoc. Biol. 2012, 92, 787–794. [Google Scholar] [CrossRef] [Green Version]
- Frascoli, M.; Marcandalli, J.; Schenk, U.; Grassi, F. Purinergic P2X7 receptor drives T cell lineage choice and shapes peripheral gammadelta cells. J. Immunol. 2012, 189, 174–180. [Google Scholar] [CrossRef] [Green Version]
- Gu, B.; Bendall, L.J.; Wiley, J.S. Adenosine triphosphate-induced shedding of CD23 and L-selectin (CD62L) from lymphocytes is mediated by the same receptor but different metalloproteases. Blood 1998, 92, 946–951. [Google Scholar] [CrossRef] [PubMed]
- Garbers, C.; Janner, N.; Chalaris, A.; Moss, M.L.; Floss, D.M.; Meyer, D.; Koch-Nolte, F.; Rose-John, S.; Scheller, J. Species specificity of ADAM10 and ADAM17 proteins in interleukin-6 (IL-6) trans-signaling and novel role of ADAM10 in inducible IL-6 receptor shedding. J. Biol. Chem. 2011, 286, 14804–14811. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moon, H.; Na, H.Y.; Chong, K.H.; Kim, T.J. P2X7 receptor-dependent ATP-induced shedding of CD27 in mouse lymphocytes. Immunol. Lett. 2006, 102, 98–105. [Google Scholar] [CrossRef] [PubMed]
- Sluyter, R.; Wiley, J.S. P2X7 receptor activation induces CD62L shedding from human CD4+ and CD8+ T cells. Inflamm. Cell Signal. 2014, 1, 44–49. [Google Scholar] [CrossRef]
- Trabanelli, S.; Ocadlikova, D.; Gulinelli, S.; Curti, A.; Salvestrini, V.; Vieira, R.P.; Idzko, M.; Di Virgilio, F.; Ferrari, D.; Lemoli, R.M. Extracellular ATP exerts opposite effects on activated and regulatory CD4+ T cells via purinergic P2 receptor activation. J. Immunol. 2012, 189, 1303–1310. [Google Scholar] [CrossRef] [Green Version]
- Lepine, S.; Le Stunff, H.; Lakatos, B.; Sulpice, J.C.; Giraud, F. ATP-induced apoptosis of thymocytes is mediated by activation of P2 X 7 receptor and involves de novo ceramide synthesis and mitochondria. Biochim. Biophys. Acta 2006, 1761, 73–82. [Google Scholar] [CrossRef]
- Seman, M.; Adriouch, S.; Scheuplein, F.; Krebs, C.; Freese, D.; Glowacki, G.; Deterre, P.; Haag, F.; Koch-Nolte, F. NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 2003, 19, 571–582. [Google Scholar] [CrossRef] [Green Version]
- Wang, C.M.; Ploia, C.; Anselmi, F.; Sarukhan, A.; Viola, A. Adenosine triphosphate acts as a paracrine signaling molecule to reduce the motility of T cells. EMBO J. 2014, 33, 1354–1364. [Google Scholar] [CrossRef] [Green Version]
- Idzko, M.; Ferrari, D.; Eltzschig, H.K. Nucleotide signalling during inflammation. Nature 2014, 509, 310–317. [Google Scholar] [CrossRef] [Green Version]
- Chen, J.; Zhao, Y.; Liu, Y. The role of nucleotides and purinergic signaling in apoptotic cell clearance-implications for chronic inflammatory diseases. Front. Immunol. 2014, 5, 656. [Google Scholar] [CrossRef] [Green Version]
- Theatre, E.; Frederix, K.; Guilmain, W.; Delierneux, C.; Lecut, C.; Bettendorff, L.; Bours, V.; Oury, C. Overexpression of CD39 in mouse airways promotes bacteria-induced inflammation. J. Immunol. 2012, 189, 1966–1974. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gu, J.; Ni, X.; Pan, X.; Lu, H.; Lu, Y.; Zhao, J.; Guo Zheng, S.; Hippen, K.L.; Wang, X.; Lu, L. Human CD39(hi) regulatory T cells present stronger stability and function under inflammatory conditions. Cell Mol. Immunol. 2017, 14, 521–528. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nikolova, M.; Carriere, M.; Jenabian, M.A.; Limou, S.; Younas, M.; Kok, A.; Hue, S.; Seddiki, N.; Hulin, A.; Delaneau, O.; et al. CD39/adenosine pathway is involved in AIDS progression. PLoS Pathog. 2011, 7, e1002110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parodi, A.; Battaglia, F.; Kalli, F.; Ferrera, F.; Conteduca, G.; Tardito, S.; Stringara, S.; Ivaldi, F.; Negrini, S.; Borgonovo, G.; et al. CD39 is highly involved in mediating the suppression activity of tumor-infiltrating CD8+ T regulatory lymphocytes. Cancer Immunol. Immunother. 2013, 62, 851–862. [Google Scholar] [CrossRef]
- Aliagas, E.; Vidal, A.; Texido, L.; Ponce, J.; Condom, E.; Martin-Satue, M. High expression of ecto-nucleotidases CD39 and CD73 in human endometrial tumors. Mediat. Inflamm. 2014, 2014, 509027. [Google Scholar] [CrossRef] [Green Version]
- Perrot, I.; Michaud, H.A.; Giraudon-Paoli, M.; Augier, S.; Docquier, A.; Gros, L.; Courtois, R.; Dejou, C.; Jecko, D.; Becquart, O.; et al. Blocking Antibodies Targeting the CD39/CD73 Immunosuppressive Pathway Unleash Immune Responses in Combination Cancer Therapies. Cell Rep. 2019, 27, 2411–2425.e9. [Google Scholar] [CrossRef] [Green Version]
- la Sala, A.; Ferrari, D.; Di Virgilio, F.; Idzko, M.; Norgauer, J.; Girolomoni, G. Alerting and tuning the immune response by extracellular nucleotides. J. Leukoc. Biol. 2003, 73, 339–343. [Google Scholar] [CrossRef]
- Zhang, Y.; Li, H.; Jia, X.; Zhang, X.; Xia, Y.; Wang, Y.; Fu, L.; Xiao, C.; Geng, D. Increased expression of P2X7 receptor in peripheral blood mononuclear cells correlates with clinical severity and serum levels of Th17-related cytokines in patients with myasthenia gravis. Clin. Neurol. Neurosurg. 2017, 157, 88–94. [Google Scholar] [CrossRef]
- Atarashi, K.; Nishimura, J.; Shima, T.; Umesaki, Y.; Yamamoto, M.; Onoue, M.; Yagita, H.; Ishii, N.; Evans, R.; Honda, K.; et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008, 455, 808–812. [Google Scholar] [CrossRef]
- Antonioli, L.; Pacher, P.; Vizi, E.S.; Hasko, G. CD39 and CD73 in immunity and inflammation. Trends Mol. Med. 2013, 19, 355–367. [Google Scholar] [CrossRef] [Green Version]
- Fang, F.; Yu, M.; Cavanagh, M.M.; Hutter Saunders, J.; Qi, Q.; Ye, Z.; Le Saux, S.; Sultan, W.; Turgano, E.; Dekker, C.L.; et al. Expression of CD39 on Activated T Cells Impairs their Survival in Older Individuals. Cell Rep. 2016, 14, 1218–1231. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gupta, P.K.; Godec, J.; Wolski, D.; Adland, E.; Yates, K.; Pauken, K.E.; Cosgrove, C.; Ledderose, C.; Junger, W.G.; Robson, S.C.; et al. CD39 Expression Identifies Terminally Exhausted CD8+ T Cells. PLoS Pathog. 2015, 11, e1005177. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bai, A.; Moss, A.; Rothweiler, S.; Serena Longhi, M.; Wu, Y.; Junger, W.G.; Robson, S.C. NADH oxidase-dependent CD39 expression by CD8(+) T cells modulates interferon gamma responses via generation of adenosine. Nat. Commun. 2015, 6, 8819. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Deaglio, S.; Dwyer, K.M.; Gao, W.; Friedman, D.; Usheva, A.; Erat, A.; Chen, J.F.; Enjyoji, K.; Linden, J.; Oukka, M.; et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 2007, 204, 1257–1265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernandez, D.; Flores-Santibanez, F.; Neira, J.; Osorio-Barrios, F.; Tejon, G.; Nunez, S.; Hidalgo, Y.; Fuenzalida, M.J.; Meza, D.; Ureta, G.; et al. Purinergic Signaling as a Regulator of Th17 Cell Plasticity. PLoS ONE 2016, 11, e0157889. [Google Scholar] [CrossRef] [PubMed]
- Friedman, D.J.; Kunzli, B.M.; Yi, A.R.; Sevigny, J.; Berberat, P.O.; Enjyoji, K.; Csizmadia, E.; Friess, H.; Robson, S.C. From the Cover: CD39 deletion exacerbates experimental murine colitis and human polymorphisms increase susceptibility to inflammatory bowel disease. Proc. Natl. Acad. Sci. USA 2009, 106, 16788–16793. [Google Scholar] [CrossRef] [Green Version]
- Aswad, F.; Kawamura, H.; Dennert, G. High sensitivity of CD4+CD25+ regulatory T cells to extracellular metabolites nicotinamide adenine dinucleotide and ATP: A role for P2X7 receptors. J. Immunol. 2005, 175, 3075–3083. [Google Scholar] [CrossRef] [Green Version]
- Aswad, F.; Dennert, G. P2X7 receptor expression levels determine lethal effects of a purine based danger signal in T lymphocytes. Cell. Immunol. 2006, 243, 58–65. [Google Scholar] [CrossRef] [Green Version]
- Mellouk, A.; Bobe, P. CD8(+), but not CD4(+) effector/memory T cells, express the CD44(high)CD45RB(high) phenotype with aging, which displays reduced expression levels of P2X7 receptor and ATP-induced cellular responses. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2019, 33, 3225–3236. [Google Scholar] [CrossRef]
- Cauwels, A.; Rogge, E.; Vandendriessche, B.; Shiva, S.; Brouckaert, P. Extracellular ATP drives systemic inflammation, tissue damage and mortality. Cell Death Dis. 2014, 5, e1102. [Google Scholar] [CrossRef] [Green Version]
- Osterholm, M.T.; Kelley, N.S.; Sommer, A.; Belongia, E.A. Efficacy and effectiveness of influenza vaccines: A systematic review and meta-analysis. Lancet Infect. Dis. 2012, 12, 36–44. [Google Scholar] [CrossRef]
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Zöphel, D.; Hof, C.; Lis, A. Altered Ca2+ Homeostasis in Immune Cells during Aging: Role of Ion Channels. Int. J. Mol. Sci. 2021, 22, 110. https://doi.org/10.3390/ijms22010110
Zöphel D, Hof C, Lis A. Altered Ca2+ Homeostasis in Immune Cells during Aging: Role of Ion Channels. International Journal of Molecular Sciences. 2021; 22(1):110. https://doi.org/10.3390/ijms22010110
Chicago/Turabian StyleZöphel, Dorina, Chantal Hof, and Annette Lis. 2021. "Altered Ca2+ Homeostasis in Immune Cells during Aging: Role of Ion Channels" International Journal of Molecular Sciences 22, no. 1: 110. https://doi.org/10.3390/ijms22010110