Adipose Tissue Immunometabolism and Apoptotic Cell Clearance
Abstract
:1. Introduction: The Impact of Apoptotic Cell Clearance in Fat Depots
2. Adipocyte Apoptosis Ignites Inflammation
3. Metabolites of Apoptotic Cells and Their Effect on Macrophages
3.1. Nuclear Receptor Ligands
3.2. Arginine and Polyamines
3.3. Lactate
3.4. Creatine
3.5. ATP and Nucleic Acids
4. Summary and Perspective
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Poon, I.; Lucas, C.; Rossi, A.G.; Ravichandran, K. Apoptotic cell clearance: Basic biology and therapeutic potential. Nat. Rev. Immunol. 2014, 14, 166–180. [Google Scholar] [CrossRef] [Green Version]
- Kourtzelis, I.; Hajishengallis, G.; Chavakis, T. Phagocytosis of Apoptotic Cells in Resolution of Inflammation. Front. Immunol. 2020, 11, 553. [Google Scholar] [CrossRef]
- Röszer, T. Transcriptional control of apoptotic cell clearance by macrophage nuclear receptors. Apoptosis 2016, 22, 284–294. [Google Scholar] [CrossRef] [PubMed]
- Röszer, T. Signal Mechanisms of M2 Macrophage Activation. In The M2 Macrophage; Springer International Publishing: Cham, Switzerland, 2020; pp. 73–97. [Google Scholar] [CrossRef]
- Zizzo, G.; Hilliard, B.A.; Monestier, M.; Cohen, P.L. Efficient Clearance of Early Apoptotic Cells by Human Macrophages Requires M2c Polarization and MerTK Induction. J. Immunol. 2012, 189, 3508–3520. [Google Scholar] [CrossRef] [Green Version]
- Lindhorst, A.; Raulien, N.; Wieghofer, P.; Eilers, J.; Rossi, F.M.V.; Bechmann, I.; Gericke, M. Adipocyte death triggers a pro-inflammatory response and induces metabolic activation of resident macrophages. Cell Death Dis. 2021, 12, 1–15. [Google Scholar] [CrossRef]
- Hahn, P.; Novak, M. Development of brown and white adipose tissue. J. Lipid Res. 1975, 16, 79–91. [Google Scholar] [CrossRef]
- Hull, D. The structure and function of brown adipose tissue. Br. Med. Bull. 1966, 22, 92–96. [Google Scholar] [CrossRef] [PubMed]
- Rosen, E.D.; Spiegelman, B.M. What We Talk About When We Talk About Fat. Cell 2014, 156, 20–44. [Google Scholar] [CrossRef] [Green Version]
- Harms, M.; Seale, P. Brown and beige fat: Development, function and therapeutic potential. Nat. Med. 2013, 19, 1252–1263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bartelt, A.; Heeren, J. Adipose tissue browning and metabolic health. Nat. Rev. Endocrinol. 2013, 10, 24–36. [Google Scholar] [CrossRef]
- Boutens, L.; Stienstra, R. Adipose tissue macrophages: Going off track during obesity. Diabetologia 2016, 59, 879–894. [Google Scholar] [CrossRef] [Green Version]
- Sorisky, A.; Magun, R.; Gagnon, A. Adipose cell apoptosis: Death in the energy depot. Int. J. Obes. 2000, 24, S3–S7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirsch, J.; Faust, I.M.; Johnson, P.R. What’s New in Obesity: Current Understanding of Adipose Tissue. Morphology 1979, 385–399. [Google Scholar] [CrossRef]
- Nisoli, E.; Cardile, A.; Bulbarelli, A.; Tedesco, L.; Bracale, R.; Cozzi, V.; Morroni, M.; Cinti, S.; Valerio, A.; Carruba, M.O. White adipocytes are less prone to apoptotic stimuli than brown adipocytes in rodent. Cell Death Differ. 2006, 13, 2154–2156. [Google Scholar] [CrossRef]
- Song, C.-X.; Chen, J.-Y.; Li, N.; Guo, Y. CTRP9 Enhances Efferocytosis in Macrophages via MAPK/Drp1-Mediated Mitochondrial Fission and AdipoR1-Induced Immunometabolism. J. Inflamm. Res. 2021, 14, 1007–1017. [Google Scholar] [CrossRef]
- Kuroda, M.; Sakaue, H. Adipocyte Death and Chronic Inflammation in Obesity. J. Med. Investig. 2017, 64, 193–196. [Google Scholar] [CrossRef] [Green Version]
- McLaughlin, T.; Craig, C.; Liu, L.-F.; Perelman, D.; Allister, C.; Spielman, D.; Cushman, S.W. Adipose Cell Size and Regional Fat Deposition as Predictors of Metabolic Response to Overfeeding in Insulin-Resistant and Insulin-Sensitive Humans. Diabetes 2016, 65, 1245–1254. [Google Scholar] [CrossRef] [Green Version]
- Björntorp, P.; Sjöström, L. The Composition and Metabolism in Vitro of Adipose Tissue Fat Cells of Different Sizes. Eur. J. Clin. Investig. 1972, 2, 78–84. [Google Scholar] [CrossRef] [PubMed]
- Boulton, T.J.C.; Dunlop, M.; Court, J.M. Adipocyte growth in the first 2 years of life. J. Paediatr. Child. Health 2008, 10, 301–305. [Google Scholar] [CrossRef]
- Dauncey, M.J.; Gairdner, D. Size of adipose cells in infancy. Arch. Dis. Child. 1975, 50, 286–290. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Waqas, S.F.H.; Hoang, A.C.; Lin, Y.-T.; Ampem, G.; Azegrouz, H.; Balogh, L.; Thuróczy, J.; Chen, J.-C.; Gerling, I.C.; Nam, S.; et al. Neuropeptide FF increases M2 activation and self-renewal of adipose tissue macrophages. J. Clin. Investig. 2017, 127, 2842–2854. [Google Scholar] [CrossRef]
- Yu, H.; Dilbaz, S.; Coßmann, J.; Hoang, A.C.; Diedrich, V.; Herwig, A.; Harauma, A.; Hoshi, Y.; Moriguchi, T.; Landgraf, K.; et al. Breast milk alkylglycerols sustain beige adipocytes through adipose tissue macrophages. J. Clin. Investig. 2019, 129, 2485–2499. [Google Scholar] [CrossRef] [Green Version]
- Vogel, P.; Read, R.; Hansen, G.; Wingert, J.; Dacosta, C.M.; Buhring, L.M.; Shadoan, M. Pathology of congenital generalized lipodystrophy in Agpat2-/- mice. Vet. Pathol. 2011, 48, 642–654. [Google Scholar] [CrossRef] [Green Version]
- Birk, R.Z.; Rubinstein, M. IFN-α induces apoptosis of adipose tissue cells. Biochem. Biophys. Res. Commun. 2006, 345, 669–674. [Google Scholar] [CrossRef]
- Domingo, P.; Matias-Guiu, X.; Pujol, R.M.; Francia, E.; Lagarda, E.; Sambeat, M.A.; Vázquez, G. Subcutaneous adipocyte apoptosis in HIV-1 protease inhibitor-associated lipodystrophy. AIDS 1999, 13, 2261–2267. [Google Scholar] [CrossRef] [PubMed]
- Alcalá, M.; Calderon-Dominguez, M.; Bustos, E.; Ramos, P.; Casals, N.; Serra, D.; Viana, M.; Herrero, L. Increased inflammation, oxidative stress and mitochondrial respiration in brown adipose tissue from obese mice. Sci. Rep. 2017, 7, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.H.; Kumar, S.; Barnett, A.H.; Eggo, M.C. Dexamethasone inhibits tumor necrosis factor-alpha-induced apoptosis and interleukin-1 beta release in human subcutaneous adipocytes and preadipocytes. J. Clin. Endocrinol. Metab. 2001, 86, 2817–2825. [Google Scholar] [PubMed] [Green Version]
- Tchkonia, T.; Tchoukalova, Y.D.; Giorgadze, N.; Pirtskhalava, T.; Karagiannides, I.; Forse, R.A.; Koo, A.; Stevenson, M.; Chinnappan, D.; Cartwright, A.; et al. Abundance of two human preadipocyte subtypes with distinct capacities for replication, adipogenesis, and apoptosis varies among fat depots. Am. J. Physiol. Metab. 2005, 288, E267–E277. [Google Scholar] [CrossRef]
- Prieur, X.; Rőszer, T.; Ricote, M. Lipotoxicity in macrophages: Evidence from diseases associated with the metabolic syndrome. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2010, 1801, 327–337. [Google Scholar] [CrossRef] [PubMed]
- Qian, S.; Pan, J.; Su, Y.; Tang, Y.; Wang, Y.; Zou, Y.; Zhao, Y.; Ma, H.; Zhang, Y.; Liu, Y.; et al. BMPR2 promotes fatty acid oxidation and protects white adipocytes from cell death in mice. Commun. Biol. 2020, 3, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Osuga, J.-I.; Ishibashi, S.; Oka, T.; Yagyu, H.; Tozawa, R.; Fujimoto, A.; Shionoiri, F.; Yahagi, N.; Kraemer, F.; Tsutsumi, O.; et al. Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity. Proc. Natl. Acad. Sci. USA 2000, 97, 787–792. [Google Scholar] [CrossRef] [Green Version]
- Guo, W.; Pirtskhalava, T.; Tchkonia, T.; Xie, W.; Thomou, T.; Han, J.; Wang, T.; Wong, S.; Cartwright, A.; Hegardt, F.G.; et al. Aging results in paradoxical susceptibility of fat cell progenitors to lipotoxicity. Am. J. Physiol. Metab. 2007, 292, E1041–E1051. [Google Scholar] [CrossRef] [PubMed]
- West, M. Dead adipocytes and metabolic dysfunction: Recent progress. Curr. Opin. Endocrinol. Diabetes Obes. 2009, 16, 178–182. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.; Barnes, G.T.; Yang, Q.; Tan, G.; Yang, D.; Chou, C.J.; Sole, J.; Nichols, A.; Ross, J.S.; Chen, H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Investig. 2003, 112, 1821–1830. [Google Scholar] [CrossRef]
- Cinti, S.; Mitchell, G.; Barbatelli, G.; Murano, I.; Ceresi, E.; Faloia, E.; Wang, S.; Fortier, M.; Greenberg, A.S.; Obin, M.S. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 2005, 46, 2347–2355. [Google Scholar] [CrossRef] [Green Version]
- Lumeng, C.N.; Bodzin, J.L.; Saltiel, A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Investig. 2007, 117, 175–184. [Google Scholar] [CrossRef] [Green Version]
- Braune, J.; Lindhorst, A.; Fröba, J.; Hobusch, C.; Kovacs, P.; Blüher, M.; Eilers, J.; Bechmann, I.; Gericke, M. Multinucleated Giant Cells in Adipose Tissue Are Specialized in Adipocyte Degradation. Diabetes 2020, 70, 538–548. [Google Scholar] [CrossRef]
- Strissel, K.J.; Stancheva, Z.; Miyoshi, H.; Perfield, J.W.; DeFuria, J.; Jick, Z.; Greenberg, A.S.; Obin, M.S. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 2007, 56, 2910–2918. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dai, L.; Bhargava, P.; Stanya, K.J.; Alexander, R.K.; Liou, Y.-H.; Jacobi, D.; Knudsen, N.H.; Hyde, A.; Gangl, M.R.; Liu, S.; et al. Macrophage alternative activation confers protection against lipotoxicity-induced cell death. Mol. Metab. 2017, 6, 1186–1197. [Google Scholar] [CrossRef]
- Nagareddy, P.; Kraakman, M.; Masters, S.; Stirzaker, R.A.; Gorman, D.J.; Grant, R.; Dragoljevic, D.; Hong, E.S.; Abdel-Latif, A.; Smyth, S.S.; et al. Adipose Tissue Macrophages Promote Myelopoiesis and Monocytosis in Obesity. Cell Metab. 2014, 19, 821–835. [Google Scholar] [CrossRef] [Green Version]
- Ravichandran, K.S. Find-me and eat-me signals in apoptotic cell clearance: Progress and conundrums. J. Exp. Med. 2010, 207, 1807–1817. [Google Scholar] [CrossRef]
- Benoit, M.E.; Clarke, E.; Morgado, P.; Fraser, D.A.; Tenner, A.J. Complement Protein C1q Directs Macrophage Polarization and Limits Inflammasome Activity during the Uptake of Apoptotic Cells. J. Immunol. 2012, 188, 5682–5693. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fischer-Posovszky, P.; Wang, Q.; Asterholm, I.W.; Rutkowski, J.; Scherer, P.E. Targeted Deletion of Adipocytes by Apoptosis Leads to Adipose Tissue Recruitment of Alternatively Activated M2 Macrophages. Endocrinology 2011, 152, 3074–3081. [Google Scholar] [CrossRef] [PubMed]
- Shaul, M.E.; Bennett, G.; Strissel, K.J.; Greenberg, A.S.; Obin, M.S. Dynamic, M2-Like Remodeling Phenotypes of CD11c+ Adipose Tissue Macrophages During High-Fat Diet-Induced Obesity in Mice. Diabetes 2010, 59, 1171–1181. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, B.; Wang, Z.; Zhang, Z.-Y.; Shen, Z.; Zhang, Z. The deficiency of macrophage erythropoietin signaling contributes to delayed acute inflammation resolution in diet-induced obese mice. Biochim. Biophys. Acta (BBA)—Mol. Basis Dis. 2018, 1865, 339–349. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Ye, J. Regulation of energy balance by inflammation: Common theme in physiology and pathology. Rev. Endocr. Metab. Disord. 2014, 16, 47–54. [Google Scholar] [CrossRef] [Green Version]
- Wieser, V.; Adolph, T.E.; Grander, C.; Grabherr, F.; Enrich, B.; Moser, P.; Moschen, A.R.; Kaser, S.; Tilg, H. Adipose type I interferon signalling protects against metabolic dysfunction. Gut 2016, 67, 157–165. [Google Scholar] [CrossRef] [Green Version]
- Derecka, M.; Gornicka, A.; Koralov, S.B.; Szczepanek, K.; Morgan, M.; Raje, V.; Sisler, J.; Zhang, Q.; Otero, D.; Cichy, J.; et al. Tyk2 and Stat3 Regulate Brown Adipose Tissue Differentiation and Obesity. Cell Metab. 2012, 16, 814–824. [Google Scholar] [CrossRef] [Green Version]
- Kristóf, E.; Klusóczki, A.; Veress, R.; Shaw, A.; Combi, Z.S.; Varga, K.; Győry, F.; Balajthy, Z.; Bai, P.; Bacso, Z.; et al. Interleukin-6 released from differentiating human beige adipocytes improves browning. Exp. Cell Res. 2019, 377, 47–55. [Google Scholar] [CrossRef]
- Alsaggar, M.; Mills, M.; Liu, D. Interferon beta overexpression attenuates adipose tissue inflammation and high-fat diet-induced obesity and maintains glucose homeostasis. Gene Ther. 2016, 24, 60–66. [Google Scholar] [CrossRef] [Green Version]
- Babaei, R.; Schuster, M.; Meln, I.; Lerch, S.; Ghandour, R.A.; Pisani, D.F.; Bayindir-Buchhalter, I.; Marx, J.; Wu, S.; Schoiswohl, G.; et al. Jak-TGFβ cross-talk links transient adipose tissue inflammation to beige adipogenesis. Sci. Signal. 2018, 11, eaai7838. [Google Scholar] [CrossRef] [Green Version]
- Asterholm, I.W.; Tao, C.; Morley, T.S.; Wang, Q.; Delgado-Lopez, F.; Wang, Z.; Scherer, P.E. Adipocyte Inflammation Is Essential for Healthy Adipose Tissue Expansion and Remodeling. Cell Metab. 2014, 20, 103–118. [Google Scholar] [CrossRef] [Green Version]
- Waqas, S.F.H.; Noble, A.; Hoang, A.C.; Ampem, G.; Popp, M.; Strauß, S.; Guille, M.; Röszer, T. Adipose tissue macrophages develop from bone marrow–independent progenitors in Xenopus laevis and mouse. J. Leukoc. Biol. 2017, 102, 845–855. [Google Scholar] [CrossRef] [Green Version]
- Peterson, K.R.; Flaherty, D.K.; Hasty, A.H. Obesity Alters B Cell and Macrophage Populations in Brown Adipose Tissue. Obesity 2017, 25, 1881–1884. [Google Scholar] [CrossRef] [Green Version]
- Han, C.Z.; Ravichandran, K.S. Metabolic Connections during Apoptotic Cell Engulfment. Cell 2011, 147, 1442–1445. [Google Scholar] [CrossRef] [Green Version]
- Yurdagul, A., Jr. Metabolic consequences of efferocytosis and its impact on atherosclerosis. Immunometabolism 2021, 3, e210017. [Google Scholar] [PubMed]
- Röszer, T.; Menéndez-Gutiérrez, M.P.; Cedenilla, M.; Ricote, M. Retinoid X receptors in macrophage biology. Trends Endocrinol. Metab. 2013, 24, 460–468. [Google Scholar] [CrossRef]
- Vasina, E.M.; Cauwenberghs, S.; Feijge, M.A.H.; Heemskerk, J.W.M.; Weber, C.; Koenen, R.R. Microparticles from apoptotic platelets promote resident macrophage differentiation. Cell Death Dis. 2011, 2, e211. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rigamonti, E.; Chinetti-Gbaguidi, G.; Staels, B. Regulation of macrophage functions by PPAR-alpha, PPAR-gamma, and LXRs in mice and men. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 1050–1059. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gonzalez, N.A.; Bensinger, S.J.; Hong, C.; Beceiro, S.; Bradley, M.N.; Zelcer, N.; Deniz, J.; Ramirez, C.; Díaz, M.; Castrillo, A. Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 2009, 31, 245–258. [Google Scholar] [CrossRef] [Green Version]
- Mukundan, L.; Odegaard, J.I.; Morel, C.R.; Heredia, J.E.; Mwangi, J.W.; Ricardo-Gonzalez, R.R.; Goh, Y.P.S.; Eagle, A.R.; Dunn, S.E.; Chawla, A.; et al. PPAR-delta senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat. Med. 2009, 15, 1266–1272. [Google Scholar] [CrossRef] [PubMed]
- Röszer, T.; Menéndez-Gutiérrez, M.P.; Lefterova, M.I.; Alameda, D.; Núñez, V.; Lazar, M.A.; Fischer, T.; Ricote, M. Autoimmune kidney disease and impaired engulfment of apoptotic cells in mice with macrophage peroxisome proliferator-activated receptor gamma or retinoid X receptor alpha deficiency. J. Immunol. 2011, 186, 621–631. [Google Scholar] [CrossRef] [PubMed]
- Yoon, Y.S.; Kim, S.-Y.; Kim, M.-J.; Lim, J.-H.; Cho, M.-S.; Kang, J.L. PPARgamma activation following apoptotic cell instillation promotes resolution of lung inflammation and fibrosis via regulation of efferocytosis and proresolving cytokines. Mucosal. Immunol. 2015, 8, 1031–1046. [Google Scholar] [CrossRef] [PubMed]
- Kato, Y.; Park, J.; Takamatsu, H.; Konaka, H.; Aoki, W.; Aburaya, S.; Ueda, M.; Nishide, M.; Koyama, S.; Kumanogoh, A.; et al. Apoptosis-derived membrane vesicles drive the cGAS-STING pathway and enhance type I IFN production in systemic lupus erythematosus. Ann. Rheum. Dis. 2018, 77, 1507–1515. [Google Scholar] [CrossRef] [Green Version]
- Zhu, M.; Barbas, A.S.; Lin, L.; Scheuermann, U.; Bishawi, M.; Brennan, T.V. Mitochondria Released by Apoptotic Cell Death Initiate Innate Immune Responses. ImmunoHorizons 2018, 2, 384–397. [Google Scholar] [CrossRef]
- Penberthy, K.; Ravichandran, K.S. Apoptotic cell recognition receptors and scavenger receptors. Immunol. Rev. 2015, 269, 44–59. [Google Scholar] [CrossRef] [Green Version]
- Garabuczi, E.; Kiss, B.; Felszeghy, S.B.; Tsay, G.J.; Fésüs, L.; Szondy, Z. Retinoids produced by macrophages engulfing apoptotic cells contribute to the appearance of transglutaminase 2 in apoptotic thymocytes. Amino Acids 2011, 44, 235–244. [Google Scholar] [CrossRef]
- Sarang, Z.; Garabuczi, É.; Joós, G.; Kiss, B.; Tóth, K.; Rühl, R.; Szondy, Z. Macrophages engulfing apoptotic thymocytes produce retinoids to promote selection, differentiation, removal and replacement of double positive thymocytes. Immunobiology 2013, 218, 1354–1360. [Google Scholar] [CrossRef] [PubMed]
- Rébé, C.; Raveneau, M.; Chevriaux, A.; Lakomy, D.; Sberna, A.-L.; Costa, A.; Bessède, G.; Athias, A.; Steinmetz, E.; Lobaccaro, J.M.A.; et al. Induction of Transglutaminase 2 by a Liver X Receptor/Retinoic Acid Receptor α Pathway Increases the Clearance of Apoptotic Cells by Human Macrophages. Circ. Res. 2009, 105, 393–401. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tóth, B.; Garabuczi, É.; Sarang, Z.; Vereb, G.; Vámosi, G.; Aeschlimann, D.; Blaskó, B.; Bécsi, B.; Erdõdi, F.; Lacy-Hulbert, A.; et al. Transglutaminase 2 Is Needed for the Formation of an Efficient Phagocyte Portal in Macrophages Engulfing Apoptotic Cells. J. Immunol. 2009, 182, 2084–2092. [Google Scholar] [CrossRef] [PubMed]
- Sarang, Z.; Joós, G.; Garabuczi, É.; Rühl, R.; Gregory, C.D.; Szondy, Z. Macrophages Engulfing Apoptotic Cells Produce Nonclassical Retinoids To Enhance Their Phagocytic Capacity. J. Immunol. 2014, 192, 5730–5738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Flajollet, S.; Staels, B.; Lefebvre, P. Retinoids and nuclear retinoid receptors in white and brown adipose tissues: Physiopathologic aspects. Horm. Mol. Biol. Clin. Investig. 2013, 14, 75–86. [Google Scholar] [CrossRef]
- Teruel, T.; Hernandez, R.; Benito, M.; Lorenzo, M. Rosiglitazone and Retinoic Acid Induce Uncoupling Protein-1 (UCP-1) in a p38 Mitogen-activated Protein Kinase-dependent Manner in Fetal Primary Brown Adipocytes. J. Biol. Chem. 2003, 278, 263–269. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mercader, J.; Ribot, J.; Murano, I.; Felipe, F.; Cinti, S.; Bonet, M.L.; Palou, A. Remodeling of White Adipose Tissue after Retinoic Acid Administration in Mice. Endocrinology 2006, 147, 5325–5332. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeyakumar, S.M.; Vajreswari, A.; Giridharan, N.V. Chronic Dietary Vitamin A Supplementation Regulates Obesity in an Obese Mutant WNIN/Ob Rat Model. Obesity 2006, 14, 52–59. [Google Scholar] [CrossRef] [PubMed]
- Tan, L.; Zhang, Y.; Crowe-White, K.M.; Senkus, K.E.; Erwin, M.E.; Wang, H. Vitamin A supplementation during suckling and postweaning periods attenuates the adverse metabolic effects of maternal high-fat diet consumption in Sprague-Dawley Rats. Curr. Dev. Nutr. 2020, 4, nzaa111. [Google Scholar] [CrossRef]
- Sidossis, L.; Kajimura, S. Brown and beige fat in humans: Thermogenic adipocytes that control energy and glucose homeostasis. J. Clin. Investig. 2015, 125, 478–486. [Google Scholar] [CrossRef]
- Murholm, M.; Isidor, M.S.; Basse, A.L.; Winther, S.; Sørensen, C.; Skovgaard-Petersen, J.; Nielsen, M.M.; Hansen, A.S.; Quistorff, B.; Hansen, J.B. Retinoic acid has different effects on UCP1 expression in mouse and human adipocytes. BMC Cell Biol. 2013, 14, 41. [Google Scholar] [CrossRef] [Green Version]
- Schweich, L.D.C.; De Oliveira, E.J.T.; Pesarini, J.R.; Hermeto, L.C.; Camassola, M.; Nardi, N.B.; Brochado, T.M.M.; Antoniolli-Silva, A.C.M.B.; Oliveira, R.J. All-trans retinoic acid induces mitochondria-mediated apoptosis of human adipose-derived stem cells and affects the balance of the adipogenic differentiation. Biomed. Pharmacother. 2017, 96, 1267–1274. [Google Scholar] [CrossRef]
- Jeyakumar, S.M.; Vajreswari, A.; Sesikeran, B.; Giridharan, N.V. Vitamin A supplementation induces adipose tissue loss through apoptosis in lean but not in obese rats of the WNIN/Ob strain. J. Mol. Endocrinol. 2005, 35, 391–398. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Landrier, J.-F.; Marcotorchino, J.; Tourniaire, F. Lipophilic Micronutrients and Adipose Tissue Biology. Nutrients 2012, 4, 1622–1649. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sergeev, I.N. Vitamin D-mediated apoptosis in cancer and obesity. Horm. Mol. Biol. Clin. Investig. 2014, 20. [Google Scholar] [CrossRef] [PubMed]
- Sergeev, I.N.; Song, Q. High vitamin D and calcium intakes reduce diet-induced obesity in mice by increasing adipose tissue apoptosis. Mol. Nutr. Food Res. 2014, 58, 1342–1348. [Google Scholar] [CrossRef]
- De Oliveira, L.F.; de Azevedo, L.G.; da Mota Santana, J.; de Sales, L.P.C.; Pereira-Santos, M. Obesity and overweight decreases the effect of vitamin D supplementation in adults: Systematic review and meta-analysis of randomized controlled trials. Rev. Endocr. Metab. Dis. 2020, 21, 67–76. [Google Scholar] [CrossRef]
- Pramono, A.; Jocken, J.W.; Blaak, E.E. Vitamin D deficiency in the aetiology of obesity-related insulin resistance. Diabetes/Metabolism Res. Rev. 2019, 35, e3146. [Google Scholar] [CrossRef] [PubMed]
- Fan, Y.; Futawaka, K.; Koyama, R.; Fukuda, Y.; Hayashi, M.; Imamoto, M.; Miyawaki, T.; Kasahara, M.; Tagami, T.; Moriyama, K. Vitamin D3/VDR resists diet-induced obesity by modulating UCP3 expression in muscles. J. Biomed. Sci. 2016, 23, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Narvaez, C.J.; Matthews, D.; Broun, E.; Chan, M.; Welsh, J. Lean Phenotype and Resistance to Diet-Induced Obesity in Vitamin D Receptor Knockout Mice Correlates with Induction of Uncoupling Protein-1 in White Adipose Tissue. Endocrinology 2009, 150, 651–661. [Google Scholar] [CrossRef] [PubMed]
- Diedrich, V.; Haugg, E.; Dreier, C.; Herwig, A. What can seasonal models teach us about energy balance? J. Endocrinol. 2020, 244, R17–R32. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wattie, N.; Ardern, C.I.; Baker, J. Season of birth and prevalence of overweight and obesity in Canada. Early Hum. Dev. 2008, 84, 539–547. [Google Scholar] [CrossRef]
- Phillips, D.; Young, J. Birth weight, climate at birth and the risk of obesity in adult life. Int. J. Obes. 2000, 24, 281–287. [Google Scholar] [CrossRef] [Green Version]
- Wasnik, S.; Rundle, C.H.; Baylink, D.J.; Yazdi, M.S.; Carreon, E.E.; Xu, Y.; Qin, X.; Lau, K.-H.W.; Tang, X. 1,25-Dihydroxyvitamin D suppresses M1 macrophages and promotes M2 differentiation at bone injury sites. JCI Insight 2018, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Das, L.M.; Binko, A.M.; Traylor, Z.P.; Peng, H.; Lu, K.Q. Vitamin D improves sunburns by increasing autophagy in M2 macrophages. Autophagy 2019, 15, 813–826. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Y.; Leung, D.Y.M.; Richers, B.N.; Liu, Y.; Remigio, L.K.; Riches, D.W.; Goleva, E. Vitamin D Inhibits Monocyte/Macrophage Proinflammatory Cytokine Production by Targeting MAPK Phosphatase-1. J. Immunol. 2012, 188, 2127–2135. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gunasekar, P.; Swier, V.J.; Fleegel, J.P.; Boosani, C.; Radwan, M.M.; Agrawal, D.K. Vitamin D and macrophage polarization in epicardial adipose tissue of atherosclerotic swine. PLoS ONE 2018, 13, e0199411. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, L.-J.; Guerrero-Juarez, C.F.; Hata, T.; Bapat, S.P.; Ramos, R.; Plikus, M.V.; Gallo, R.L. Dermal adipocytes protect against invasive Staphylococcus aureus skin infection. Science 2015, 347, 67–71. [Google Scholar] [CrossRef] [Green Version]
- Fernández, Á.F.; Bárcena, C.; Martínez-García, G.G.; Tamargo-Gómez, I.; Suárez, M.F.; Pietrocola, F.; Mariño, G. Autophagy couteracts weight gain, lipotoxicity and pancreatic β-cell death upon hypercaloric pro-diabetic regimens. Cell Death Dis. 2017, 8, e2970. [Google Scholar] [CrossRef] [PubMed]
- Rosa-Caldwell, M.E.; Brown, J.L.; Lee, D.E.; Blackwell, T.A.; Turner, K.W.; Brown, L.A.; Perry, R.A., Jr.; Haynie, W.S.; Washington, T.A.; Greene, N.P. Autophagy activation, not peroxisome proliferator-activated receptor γ coactivator 1α, may mediate exercise-induced improvements in glucose handling during diet-induced obesity. Exp. Physiol. 2017, 102, 1194–1207. [Google Scholar] [CrossRef]
- Chekeni, F.B.; Elliott, M.; Sandilos, J.K.; Walk, S.F.; Kinchen, J.; Lazarowski, E.R.; Armstrong, A.J.; Penuela, S.; Laird, D.W.; Salvesen, G.S.; et al. Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature 2010, 467, 863–867. [Google Scholar] [CrossRef] [Green Version]
- Medina, C.B.; Mehrotra, P.; Arandjelovic, S.; Perry, J.S.A.; Guo, Y.; Morioka, S.; Barron, B.; Walk, S.F.; Ghesquière, B.; Krupnick, A.S.; et al. Metabolites released from apoptotic cells act as tissue messengers. Nature 2020, 580, 130–135. [Google Scholar] [CrossRef]
- Barra, V.; Kuhn, A.-M.; Von Knethen, A.; Weigert, A.; Brüne, B. Apoptotic cell-derived factors induce arginase II expression in murine macrophages by activating ERK5/CREB. Cell. Mol. Life Sci. 2010, 68, 1815–1827. [Google Scholar] [CrossRef]
- Herr, D.R.; Reolo, M.J.Y.; Peh, Y.X.; Wang, W.; Lee, C.-W.; Rivera, R.; Paterson, I.C.; Chun, J. Sphingosine 1-phosphate receptor 2 (S1P2) attenuates reactive oxygen species formation and inhibits cell death: Implications for otoprotective therapy. Sci. Rep. 2016, 6, 24541. [Google Scholar] [CrossRef] [Green Version]
- Röszer, T. What Is an M2 Macrophage? Historical Overview of the Macrophage Polarization Model. The Th1/Th2 and M1/M2 Paradigm, the Arginine Fork. In The M2 Macrophage; Röszer, T., Ed.; Springer International Publishing: Cham, Schwitzerland, 2020; pp. 3–25. [Google Scholar] [CrossRef]
- Rőszer, T. Understanding the Mysterious M2 Macrophage through Activation Markers and Effector Mechanisms. Mediat. Inflammation 2015, 2015, 816460. [Google Scholar] [CrossRef] [Green Version]
- Yurdagul, A.; Subramanian, M.; Wang, X.; Crown, S.B.; Ilkayeva, O.R.; Darville, L.; Kolluru, G.K.; Rymond, C.C.; Gerlach, B.D.; Zheng, Z.; et al. Macrophage Metabolism of Apoptotic Cell-Derived Arginine Promotes Continual Efferocytosis and Resolution of Injury. Cell Metab. 2020, 31, 518–533.e10. [Google Scholar] [CrossRef]
- Moon, M.H.; Jeong, J.K.; Park, S.Y. Activation of S1P2 receptor, a possible mechanism of inhibition of adipogenic differentiation by sphingosine 1-phosphate. Mol. Med. Rep. 2015, 11, 1031–1036. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kitada, Y.; Kajita, K.; Taguchi, K.; Mori, I.; Yamauchi, M.; Ikeda, T.; Kawashima, M.; Asano, M.; Kajita, T.; Ishizuka, T.; et al. Blockade of Sphingosine 1-Phosphate Receptor 2 Signaling Attenuates High-Fat Diet-Induced Adipocyte Hypertrophy and Systemic Glucose Intolerance in Mice. Endocrinology 2016, 157, 1839–1851. [Google Scholar] [CrossRef] [PubMed]
- Iacomino, G.; Picariello, G.; D’Agostino, L. DNA and nuclear aggregates of polyamines. Biochim. Biophys. Acta (BBA)—Mol. Cell Res. 2012, 1823, 1745–1755. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maeda, Y.; Rachez, C.; Hawel, L., III; Byus, C.V.; Freedman, L.P.; Sladek, F.M. Polyamines Modulate the Interaction between Nuclear Receptors and Vitamin D Receptor-Interacting Protein 205. Mol. Endocrinol. 2002, 16, 1502–1510. [Google Scholar] [CrossRef] [PubMed]
- Rabinowitz, J.D.; Enerbäck, S. Lactate: The ugly duckling of energy metabolism. Nat. Metab. 2020, 2, 566–571. [Google Scholar] [CrossRef] [PubMed]
- Krycer, J.R.; Quek, L.-E.; Francis, D.; Fazakerley, D.J.; Elkington, S.D.; Diaz-Vegas, A.; Cooke, K.C.; Weiss, F.C.; Duan, X.; Kurdyukov, S.; et al. Lactate production is a prioritized feature of adipocyte metabolism. J. Biol. Chem. 2020, 295, 83–98. [Google Scholar] [CrossRef]
- DiGirolamo, M.; Newby, F.D.; Lovejoy, J. Lactate production in adipose tissue; a regulated function with extra-adipose implications. FASEB J. 1992, 6, 2405–2412. [Google Scholar] [CrossRef]
- Muñoz, S.; Franckhauser, S.; Elias, I.; Ferre, T.; Hidalgo, A.; Monteys, A.M.; Molas, M.; Cerdan, S.; Pujol, A.; Ruberte, J.; et al. Chronically increased glucose uptake by adipose tissue leads to lactate production and improved insulin sensitivity rather than obesity in the mouse. Diabetologia 2010, 53, 2417–2430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carrière, A.; Jeanson, Y.; Berger-Müller, S.; André, M.; Chenouard, V.; Arnaud, E.; Barreau, C.; Walther, R.; Galinier, A.; Wdziekonski, B.; et al. Browning of White Adipose Cells by Intermediate Metabolites: An Adaptive Mechanism to Alleviate Redox Pressure. Diabetes 2014, 63, 3253–3265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cai, T.-Q.; Ren, N.; Jin, L.; Cheng, K.; Kash, S.; Chen, R.; Wright, S.D.; Taggart, A.K.; Waters, M.G. Role of GPR81 in lactate-mediated reduction of adipose lipolysis. Biochem. Biophys. Res. Commun. 2008, 377, 987–991. [Google Scholar] [CrossRef]
- Tiefenthaler, M.; Amberger, A.; Bacher, N.; Hartmann, B.L.; Margreiter, R.; Kofler, R.; Konwalinka, G. Increased lactate production follows loss of mitochondrial membrane potential during apoptosis of human leukaemia cells. Br. J. Haematol. 2001, 114, 574–580. [Google Scholar] [CrossRef] [PubMed]
- Morioka, S.; Perry, J.S.A.; Raymond, M.H.; Medina, C.B.; Zhu, Y.; Zhao, L.; Serbulea, V.; Onengut-Gumuscu, S.; Leitinger, N.; Kucenas, S.; et al. Efferocytosis induces a novel SLC program to promote glucose uptake and lactate release. Nature 2018, 563, 714–718. [Google Scholar] [CrossRef]
- Colegio, O.; Chu, N.-Q.; Szabo, A.L.; Chu, T.; Rhebergen, A.M.; Jairam, V.; Cyrus, N.; Brokowski, C.E.; Eisenbarth, S.; Phillips, G.M.; et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 2014, 513, 559–563. [Google Scholar] [CrossRef]
- Selleri, S.; Bifsha, P.; Civini, S.; Pacelli, C.; Dieng, M.M.; Lemieux, W.; Jin, P.; Bazin, R.; Patey, N.; Marincola, F.M.; et al. Human mesenchymal stromal cell-secreted lactate induces M2-macrophage differentiation by metabolic reprogramming. Oncotarget 2016, 7, 30193–30210. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peter, K.; Rehli, M.; Singer, K.; Renner-Sattler, K.; Kreutz, M. Lactic acid delays the inflammatory response of human monocytes. Biochem. Biophys. Res. Commun. 2015, 457, 412–418. [Google Scholar] [CrossRef]
- Caslin, H.; Abebayehu, D.; Qayum, A.A.; Haque, T.T.; Taruselli, M.; Paez, P.A.; Pondicherry, N.; Barnstein, B.O.; Hoeferlin, L.A.; Chalfant, C.E.; et al. Lactic Acid Inhibits Lipopolysaccharide-Induced Mast Cell Function by Limiting Glycolysis and ATP Availability. J. Immunol. 2019, 203, 453–464. [Google Scholar] [CrossRef]
- Dietl, K.; Renner, K.; Dettmer, K.; Timischl, B.; Eberhart, K.; Dorn, C.; Hellerbrand, C.; Kastenberger, M.; Kunz-Schughart, L.; Oefner, P.J.; et al. Lactic Acid and Acidification Inhibit TNF Secretion and Glycolysis of Human Monocytes. J. Immunol. 2009, 184, 1200–1209. [Google Scholar] [CrossRef]
- Yang, K.; Xu, J.; Fan, M.; Tu, F.; Wang, X.; Ha, T.; Williams, D.L.; Li, C. Lactate Suppresses Macrophage Pro-Inflammatory Response to LPS Stimulation by Inhibition of YAP and NF-κB Activation via GPR81-Mediated Signaling. Front. Immunol. 2020, 38, 990–1002. [Google Scholar] [CrossRef]
- Hoque, R.; Farooq, A.; Ghani, A.; Gorelick, F.; Mehal, W.Z. Lactate Reduces Liver and Pancreatic Injury in Toll-Like Receptor—And Inflammasome-Mediated Inflammation via GPR81-Mediated Suppression of Innate Immunity. Gastroenterology 2014, 146, 1763–1774. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, H.-C.; Yan, X.-Y.; Yu, W.-W.; Liang, X.-Q.; Du, X.-Y.; Liu, Z.-C.; Long, J.-P.; Zhao, G.-H.; Liu, H.-B. Lactic acid in macrophage polarization: The significant role in inflammation and cancer. Int. Rev. Immunol. 2021, 1–15. [Google Scholar] [CrossRef]
- Feingold, K.R.; Moser, A.; Shigenaga, J.K.; Grunfeld, C. Inflammation inhibits GPR81 expression in adipose tissue. Inflamm. Res. 2011, 60, 991–995. [Google Scholar] [CrossRef] [PubMed]
- Ji, L.; Zhao, X.; Zhang, B.; Kang, L.; Song, W.; Zhao, B.; Xie, W.; Chen, L.; Hu, X. Slc6a8-Mediated Creatine Uptake and Accumulation Reprogram Macrophage Polarization via Regulating Cytokine Responses. Immunity 2019, 51, 272–284.e7. [Google Scholar] [CrossRef] [PubMed]
- Ji, L.; Zhao, X.; Zhang, B.; Kang, L.; Song, W.; Zhao, B.; Xie, W.; Hu, X. Creatine shapes macrophage polarization by reprogramming L-arginine metabolism. J. Immunol. 2019, 202 (Suppl. 1), 58. [Google Scholar]
- Riesberg, L.A.; McDonald, T.L.; Wang, Y.; Chen, X.-M.; Holzmer, S.W.; Tracy, S.M.; Drescher, K.M. Creatinine downregulates TNF-α in macrophage and T cell lines. Cytokine 2018, 110, 29–38. [Google Scholar] [CrossRef]
- Leland, K.M.; McDonald, T.L.; Drescher, K.M. Effect of creatine, creatinine, and creatine ethyl ester on TLR expression in macrophages. Int. Immunopharmacol. 2011, 11, 1341–1347. [Google Scholar] [CrossRef] [Green Version]
- Kazak, L.; Rahbani, J.; Samborska, B.; Lu, G.Z.; Jedrychowski, M.P.; Lajoie, M.; Zhang, S.; Ramsay, L.; Dou, F.; Tenen, D.; et al. Ablation of adipocyte creatine transport impairs thermogenesis and causes diet-induced obesity. Nat. Metab. 2019, 1, 360–370. [Google Scholar] [CrossRef]
- Kazak, L.; Chouchani, E.T.; Jedrychowski, M.P.; Erickson, B.; Shinoda, K.; Cohen, P.; Vetrivelan, R.; Lu, G.Z.; Laznik-Bogoslavski, D.; Hasenfuss, S.C.; et al. A Creatine-Driven Substrate Cycle Enhances Energy Expenditure and Thermogenesis in Beige Fat. Cell 2015, 163, 643–655. [Google Scholar] [CrossRef] [Green Version]
- Forbes, S.C.; Candow, D.G.; Krentz, J.R.; Roberts, M.D.; Young, K.C. Changes in Fat Mass Following Creatine Supplementation and Resistance Training in Adults ≥50 Years of Age: A Meta-Analysis. J. Funct. Morphol. Kinesiol. 2019, 4, 62. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oliveira, C.L.; Antunes, B.D.M.M.; Gomes, A.C.; Lira, F.S.; Pimentel, G.D.; Boulé, N.G.; Mota, J.F. Creatine supplementation does not promote additional effects on inflammation and insulin resistance in older adults: A pilot randomized, double-blind, placebo-controlled trial. Clin. Nutr. ESPEN 2020, 38, 94–98. [Google Scholar] [CrossRef]
- Zamaraeva, M.; Sabirov, R.Z.; Maeno, E.; Ando-Akatsuka, Y.; Bessonova, S.V.; Okada, Y. Cells die with increased cytosolic ATP during apoptosis: A bioluminescence study with intracellular luciferase. Cell Death Differ. 2005, 12, 1390–1397. [Google Scholar] [CrossRef]
- Qu, Y.; Misaghi, S.; Newton, K.; Gilmour, L.L.; Louie, S.; Cupp, J.E.; Dubyak, G.; Hackos, D.; Dixit, V.M. Pannexin-1 Is Required for ATP Release during Apoptosis but Not for Inflammasome Activation. J. Immunol. 2011, 186, 6553–6561. [Google Scholar] [CrossRef] [Green Version]
- Scemes, E.; Spray, D.C.; Meda, P. Connexins, pannexins, innexins: Novel roles of “hemi-channels”. Pflugers Archiv Eur. J. Physiol. 2009, 457, 1207–1226. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Samuels, S.E.; Lipitz, J.B.; Wang, J.; Dahl, G.; Muller, K.J. Arachidonic acid closes innexin/pannexin channels and thereby inhibits microglia cell movement to a nerve injury. Dev. Neurobiol. 2013, 73, 621–631. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kawamura, H.; Kawamura, T.; Kanda, Y.; Kobayashi, T.; Abo, T. Extracellular ATP-stimulated macrophages produce macrophage inflammatory protein-2 which is important for neutrophil migration. Immunology 2012, 136, 448–458. [Google Scholar] [CrossRef] [PubMed]
- Zha, Q.-B.; Wei, H.-X.; Li, C.-G.; Liang, Y.-D.; Xu, L.-H.; Bai, W.-J.; Pan, H.; He, X.-H.; Ouyang, D.-Y. ATP-Induced Inflammasome Activation and Pyroptosis Is Regulated by AMP-Activated Protein Kinase in Macrophages. Front. Immunol. 2016, 7, 597. [Google Scholar] [CrossRef] [Green Version]
- Sakaki, H.; Tsukimoto, M.; Harada, H.; Moriyama, Y.; Kojima, S. Autocrine Regulation of Macrophage Activation via Exocytosis of ATP and Activation of P2Y11 Receptor. PLoS ONE 2013, 8, e59778. [Google Scholar] [CrossRef] [Green Version]
- Lee, A.H.; Ledderose, C.; Li, X.; Slubowski, C.J.; Sueyoshi, K.; Staudenmaier, L.; Bao, Y.; Zhang, J.; Junger, W.G. Adenosine Triphosphate Release is Required for Toll-Like Receptor-Induced Monocyte/Macrophage Activation, Inflammasome Signaling, Interleukin-1β Production, and the Host Immune Response to Infection. Crit. Care Med. 2018, 46, e1183–e1189. [Google Scholar] [CrossRef]
- McArthur, K.; Whitehead, L.W.; Heddleston, J.M.; Li, L.; Padman, B.S.; Oorschot, V.; Geoghegan, N.D.; Chappaz, S.; Davidson, S.; Chin, H.S.; et al. BAK/BAX macropores facilitate mitochondrial herniation and mtDNA efflux during apoptosis. Science 2018, 359, eaao6047. [Google Scholar] [CrossRef] [Green Version]
- Hauser, P.; Wang, S.; Didenko, V.V. Apoptotic Bodies: Selective Detection in Extracellular Vesicles. In Signal Transduction Immunohistochemistry; Kalyuzhny, A., Ed.; Methods in Molecular Biology; Humana Press: New York, NY, USA, 2017; Volume 1554. [Google Scholar] [CrossRef]
- Minton, K. Anti-inflammatory effect of mitophagy. Nat. Rev. Immunol. 2016, 16, 206. [Google Scholar] [CrossRef]
- Harris, J.; Deen, N.; Zamani, S.; Hasnat, A. Mitophagy and the release of inflammatory cytokines. Mitochondrion 2018, 41, 2–8. [Google Scholar] [CrossRef]
- Bahat, A.; MacVicar, T.; Langer, T. Metabolism and Innate Immunity Meet at the Mitochondria. Front. Cell Dev. Biol. 2021, 9. [Google Scholar] [CrossRef] [PubMed]
- Dhir, A.; Dhir, S.; Borowski, L.; Jimenez, L.; Teitell, M.; Rötig, A.; Crow, Y.J.; Rice, G.I.; Duffy, D.; Tamby, C.; et al. Mitochondrial double-stranded RNA triggers antiviral signalling in humans. Nature 2018, 560, 238–242. [Google Scholar] [CrossRef] [PubMed]
- Jiang, L.; Paone, S.; Caruso, S.; Atkin-Smith, G.K.; Phan, T.K.; Hulett, M.; Poon, I.K.H. Determining the contents and cell origins of apoptotic bodies by flow cytometry. Sci. Rep. 2017, 7, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kalluri, R.; LeBleu, V.S. Discovery of Double-Stranded Genomic DNA in Circulating Exosomes. Cold Spring Harb. Symp. Quant. Biol. 2016, 81, 275–280. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Munoz, L.; Lauber, K.; Schiller, M.; Manfredi, A.A.; Herrmann, M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol. 2010, 6, 280–289. [Google Scholar] [CrossRef]
- Gupta, S.; Kaplan, M.J. Bite of the wolf: Innate immune responses propagate autoimmunity in lupus. J. Clin. Investig. 2021, 131, e144918. [Google Scholar] [CrossRef]
- Sule, S.; Rosen, A.; Petri, M.; Akhter, E.; Andrade, F. Abnormal Production of Pro- and Anti-Inflammatory Cytokines by Lupus Monocytes in Response to Apoptotic Cells. PLoS ONE 2011, 6, e17495. [Google Scholar] [CrossRef]
- Li, T.; Chen, Z.J. The cGAS–cGAMP–STING pathway connects DNA damage to inflammation, senescence, and cancer. J. Exp. Med. 2018, 215, 1287–1299. [Google Scholar] [CrossRef] [PubMed]
- Röszer, T. (Ed.) M2 Macrophages in the Metabolic Organs and in the Neuroendocrine System. In The M2, Macrophage; Springer International Publishing: Cham, Schwitzerland, 2020; pp. 171–187. [Google Scholar] [CrossRef]
- Chobot, A.; Górowska-Kowolik, K.; Sokołowska, M.; Jarosz-Chobot, P. Obesity and diabetes-Not only a simple link between two epidemics. Diabetes/Metab. Res. Rev. 2018, 34, e3042. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, K.; Gao, Z.; Kolonin, M.G. Transient inflammatory signaling promotes beige adipogenesis. Sci. Signal. 2018, 11, eaat3192. [Google Scholar] [CrossRef] [PubMed]
- Geserick, M.; Vogel, M.; Gausche, R.; Lipek, T.; Spielau, U.; Keller, E.; Pfäffle, R.; Kiess, W.; Körner, A. Acceleration of BMI in Early Childhood and Risk of Sustained Obesity. N. Engl. J. Med. 2018, 379, 1303–1312. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Röszer, T. Adipose Tissue Immunometabolism and Apoptotic Cell Clearance. Cells 2021, 10, 2288. https://doi.org/10.3390/cells10092288
Röszer T. Adipose Tissue Immunometabolism and Apoptotic Cell Clearance. Cells. 2021; 10(9):2288. https://doi.org/10.3390/cells10092288
Chicago/Turabian StyleRöszer, Tamás. 2021. "Adipose Tissue Immunometabolism and Apoptotic Cell Clearance" Cells 10, no. 9: 2288. https://doi.org/10.3390/cells10092288