The Immune Regulatory Role of Protein Kinase CK2 and Its Implications for Treatment of Cancer
Abstract
:1. Introduction
2. Protein Kinase CK2
2.1. CK2 Structure and Function
2.2. Signaling Pathways Regulated by CK2
2.3. CK2 Inhibitors
3. Role of the Immune System in Health and Disease
3.1. Innate Immune Cells
3.1.1. Neutrophils
3.1.2. Monocytes and Macrophages
3.1.3. Dendritic Cells
3.2. Adaptive Immune Cells
3.2.1. T-Cells
3.2.2. B-Cells
4. CK2 Regulates Immune Cell Function
4.1. Innate Immunity
4.1.1. CK2 Function in Neutrophils, Monocytes and Macrophages
4.1.2. CK2 Function in Dendritic Cells (DCs)
4.2. Adaptive Immunity
4.2.1. CK2 Function in CD4+ T-Cells
4.2.2. CK2 Function in B-Cells
5. Perspectives on the Use of CK2 Inhibitors for Cancer Therapy
Author Contributions
Funding
Conflicts of Interest
Abbreviations
B-ALL | B-cell acute lymphoblastic leukemia |
CX-4945 | (5-(3-chlorophenyl)amino)-benzo(c)-2,6-naphthyridine-8-carboxylic acid) |
CD | Crohn’s Disease |
DMAT | 2-dimethylamino-4,5,6,7-tetrabromo-1H-benzimidazole |
DCs | Dendritic Cells |
FO | Follicular |
IL-1β | Interleukin-1β |
IKK | IκB Kinase |
JAK | Janus Kinase |
MoDCs | Monocyte-derived DCs |
MZ | Marginal Zone |
mTOR | Mammalian Target of Rapamycin |
NF-κB | Nuclear Factor-κB |
PI3K | Phosphatidylinositol 3-Kinase |
PTPs | Protein Tyrosine Phosphatases |
PTEN | Phosphatase and Tensin Homolog deleted on Chromosome 10 |
STAT | Signal Transducers and Activators of Transcription |
SOCS | Suppressors of Cytokine Signaling |
TBB | 4,5,6,7-tetrabromo-1H-benzotriazole |
Th1 | T helper 1 |
Th17 | T helper 17 |
Tregs | T Regulatory Cells |
TAMs | Tumor Associated Macrophages |
References
- Borgo, C.; D’Amore, C.; Sarno, S.; Salvi, M.; Ruzzene, M. Protein kinase CK2: A potential therapeutic target for diverse human diseases. Signal Transduct. Target. Ther. 2021, 6, 183. [Google Scholar] [CrossRef] [PubMed]
- Burnett, G.; Kennedy, E.P. The enzymatic phosphorylation of proteins. J. Biol. Chem. 1954, 211, 969–980. [Google Scholar] [CrossRef]
- Husain, K.; Williamson, T.T.; Nelson, N.; Ghansah, T. Protein kinase 2 (CK2): A potential regulator of immune cell development and function in cancer. Immunol. Med. 2021, 44, 159–174. [Google Scholar] [CrossRef]
- Borgo, C.; Ruzzene, M. Role of protein kinase CK2 in antitumor drug resistance. J. Exp. Clin. Cancer Res. 2019, 38, 287. [Google Scholar] [CrossRef]
- Gibson, S.A.; Benveniste, E.N. Protein kinase CK2: An emerging regulator of immunity. Trends Immunol. 2018, 39, 82–85. [Google Scholar] [CrossRef] [PubMed]
- Pinna, L.A. Protein kinase CK2: A challenge to canons. J. Cell Sci. 2002, 115, 3873–3878. [Google Scholar] [CrossRef] [Green Version]
- Lozeman, F.J.; Litchfield, D.W.; Piening, C.; Takio, K.; Walsh, K.A.; Krebs, E.G. Isolation and characterization of human cDNA clones encoding the alpha and the alpha’ subunits of casein kinase II. Biochemistry 1990, 29, 8436–8447. [Google Scholar] [CrossRef] [PubMed]
- Allende, J.E.; Allende, C.C. Protein kinases. 4. Protein kinase CK2: An enzyme with multiple substrates and a puzzling regulation. FASEB J. 1995, 9, 313–323. [Google Scholar] [CrossRef]
- Litchfield, D.W.; Luscher, B. Casein kinase II in signal transduction and cell cycle regulation. Mol. Cell Biochem. 1993, 127–128, 187–199. [Google Scholar] [CrossRef] [PubMed]
- Bibby, A.C.; Litchfield, D.W. The multiple personalities of the regulatory subunit of protein kinase CK2: CK2 dependent and CK2 independent roles reveal a secret identity for CK2β. Int. J. Biol. Sci. 2005, 1, 67–79. [Google Scholar] [CrossRef]
- Gotz, C.; Montenarh, M. Protein kinase CK2 in development and differentiation. Biomed. Rep. 2017, 6, 127–133. [Google Scholar] [CrossRef]
- Rodriguez, F.A.; Contreras, C.; Bolanos-Garcia, V.; Allende, J.E. Protein kinase CK2 as an ectokinase: The role of the regulatory CK2β subunit. Proc. Natl. Acad. Sci. USA 2008, 105, 5693–5698. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meggio, F.; Pinna, L.A. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 2003, 17, 349–368. [Google Scholar] [CrossRef]
- Marin, O.; Meggio, F.; Draetta, G.; Pinna, L.A. The consensus sequences for cdc2 kinase and for casein kinase-2 are mutually incompatible. A study with peptides derived from the β-subunit of casein kinase-2. FEBS Lett. 1992, 301, 111–114. [Google Scholar] [CrossRef] [Green Version]
- Lou, D.Y.; Dominguez, I.; Toselli, P.; Landesman-Bollag, E.; O’Brien, C.; Seldin, D.C. The alpha catalytic subunit of protein kinase CK2 is required for mouse embryonic development. Mol. Cell Biol. 2008, 28, 131–139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dominguez, I.; Degano, I.R.; Chea, K.; Cha, J.; Toselli, P.; Seldin, D.C. CK2α is essential for embryonic morphogenesis. Mol. Cell Biochem. 2011, 356, 209–216. [Google Scholar] [CrossRef] [Green Version]
- Buchou, T.; Vernet, M.; Blond, O.; Jensen, H.H.; Pointu, H.; Olsen, B.B.; Cochet, C.; Issinger, O.G.; Boldyreff, B. Disruption of the regulatory β subunit of protein kinase CK2 in mice leads to a cell-autonomous defect and early embryonic lethality. Mol. Cell Biol. 2003, 23, 908–915. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nunez de Villavicencio-Diaz, T.; Rabalski, A.J.; Litchfield, D.W. Protein kinase CK2: Intricate relationships within regulatory cellular networks. Pharmaceuticals 2017, 10, 27. [Google Scholar] [CrossRef] [Green Version]
- Chua, M.M.; Ortega, C.E.; Sheikh, A.; Lee, M.; Abdul-Rassoul, H.; Hartshorn, K.L.; Dominguez, I. CK2 in cancer: Cellular and biochemical mechanisms and potential therapeutic target. Pharmaceuticals 2017, 10, 18. [Google Scholar] [CrossRef]
- Ersahin, T.; Tuncbag, N.; Cetin-Atalay, R. The PI3K/AKT/mTOR interactive pathway. Mol. Biosyst. 2015, 11, 1946–1954. [Google Scholar] [CrossRef]
- Porta, C.; Paglino, C.; Mosca, A. Targeting PI3K/Akt/mTOR signaling in cancer. Front. Oncol. 2014, 4, 64. [Google Scholar] [CrossRef] [Green Version]
- LoRusso, P.M. Inhibition of the PI3K/AKT/mTOR pathway in solid tumors. J. Clin. Oncol. 2016, 34, 3803–3815. [Google Scholar] [CrossRef]
- Liu, R.; Chen, Y.; Liu, G.; Li, C.; Song, Y.; Cao, Z.; Li, W.; Hu, J.; Lu, C.; Liu, Y. PI3K/AKT pathway as a key link modulates the multidrug resistance of cancers. Cell Death Dis. 2020, 11, 797. [Google Scholar] [CrossRef]
- Guerra, B. Protein kinase CK2 subunits are positive regulators of AKT kinase. Int. J. Oncol. 2006, 28, 685–693. [Google Scholar] [CrossRef] [Green Version]
- Di Maira, G.; Salvi, M.; Arrigoni, G.; Marin, O.; Sarno, S.; Brustolon, F.; Pinna, L.A.; Ruzzene, M. Protein kinase CK2 phosphorylates and upregulates Akt/PKB. Cell Death Differ. 2005, 12, 668–677. [Google Scholar] [CrossRef]
- Di Maira, G.; Brustolon, F.; Pinna, L.A.; Ruzzene, M. Dephosphorylation and inactivation of Akt/PKB is counteracted by protein kinase CK2 in HEK 293T cells. Cell Mol. Life Sci. 2009, 66, 3363–3373. [Google Scholar] [CrossRef] [PubMed]
- Torres, J.; Pulido, R. The tumor suppressor PTEN is phosphorylated by the protein kinase CK2 at its C terminus. Implications for PTEN stability to proteasome-mediated degradation. J. Biol. Chem. 2001, 276, 993–998. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miller, S.J.; Lou, D.Y.; Seldin, D.C.; Lane, W.S.; Neel, B.G. Direct identification of PTEN phosphorylation sites. FEBS Lett. 2002, 528, 145–153. [Google Scholar] [CrossRef] [Green Version]
- Vazquez, F.; Grossman, S.R.; Takahashi, Y.; Rokas, M.V.; Nakamura, N.; Sellers, W.R. Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J. Biol. Chem. 2001, 276, 48627–48630. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olsen, B.B.; Svenstrup, T.H.; Guerra, B. Downregulation of protein kinase CK2 induces autophagic cell death through modulation of the mTOR and MAPK signaling pathways in human glioblastoma cells. Int. J. Oncol. 2012, 41, 1967–1976. [Google Scholar] [CrossRef] [Green Version]
- Zheng, Y.; McFarland, B.C.; Drygin, D.; Yu, H.; Bellis, S.L.; Kim, H.; Bredel, M.; Benveniste, E.N. Targeting protein kinase CK2 suppresses prosurvival signaling pathways and growth of glioblastoma. Clin. Cancer Res. 2013, 19, 6484–6494. [Google Scholar] [CrossRef] [Green Version]
- Liu, T.; Zhang, L.; Joo, D.; Sun, S.C. NF-kappaB signaling in inflammation. Signal Transduct. Target. Ther. 2017, 2, 17023. [Google Scholar] [CrossRef] [Green Version]
- Taniguchi, K.; Karin, M. NF-kappaB, inflammation, immunity and cancer: Coming of age. Nat. Rev. Immunol. 2018, 18, 309–324. [Google Scholar] [CrossRef] [PubMed]
- Dominguez, I.; Sonenshein, G.E.; Seldin, D.C. Protein kinase CK2 in health and disease: CK2 and its role in Wnt and NF-kappaB signaling: Linking development and cancer. Cell Mol. Life. Sci. 2009, 66, 1850–1857. [Google Scholar] [CrossRef]
- Wang, D.; Westerheide, S.D.; Hanson, J.L.; Baldwin, A.S., Jr. Tumor necrosis factor alpha-induced phosphorylation of RelA/p65 on Ser529 is controlled by casein kinase II. J. Biol. Chem. 2000, 275, 32592–32597. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seif, F.; Khoshmirsafa, M.; Aazami, H.; Mohsenzadegan, M.; Sedighi, G.; Bahar, M. The role of JAK-STAT signaling pathway and its regulators in the fate of T helper cells. Cell Commun. Signal. 2017, 15, 23. [Google Scholar] [CrossRef] [Green Version]
- Rawlings, J.S.; Rosler, K.M.; Harrison, D.A. The JAK/STAT signaling pathway. J. Cell. Sci. 2004, 117, 1281–1283. [Google Scholar] [CrossRef] [Green Version]
- O’Shea, J.J.; Murray, P.J. Cytokine signaling modules in inflammatory responses. Immunity 2008, 28, 477–487. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liongue, C.; O’Sullivan, L.A.; Trengove, M.C.; Ward, A.C. Evolution of JAK-STAT pathway components: Mechanisms and role in immune system development. PLoS ONE 2012, 7, e32777. [Google Scholar] [CrossRef]
- Villarino, A.V.; Kanno, Y.; O’Shea, J.J. Mechanisms and consequences of Jak-STAT signaling in the immune system. Nat. Immunol. 2017, 18, 374–384. [Google Scholar] [CrossRef]
- Manni, S.; Brancalion, A.; Mandato, E.; Tubi, L.Q.; Colpo, A.; Pizzi, M.; Cappellesso, R.; Zaffino, F.; Di Maggio, S.A.; Cabrelle, A.; et al. Protein kinase CK2 inhibition down modulates the NF-κB and STAT3 survival pathways, enhances the cellular proteotoxic stress and synergistically boosts the cytotoxic effect of bortezomib on multiple myeloma and mantle cell lymphoma cells. PLoS ONE 2013, 8, e75280. [Google Scholar] [CrossRef] [Green Version]
- Zheng, Y.; Qin, H.; Frank, S.J.; Deng, L.; Litchfield, D.W.; Tefferi, A.; Pardanani, A.; Lin, F.T.; Li, J.; Sha, B.; et al. A CK2-dependent mechanism for activation of the JAK-STAT signaling pathway. Blood 2011, 118, 156–166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Battistutta, R.; De Moliner, E.; Sarno, S.; Zanotti, G.; Pinna, L.A. Structural features underlying selective inhibition of protein kinase CK2 by ATP site-directed tetrabromo-2-benzotriazole. Protein. Sci. 2001, 10, 2200–2206. [Google Scholar] [CrossRef] [Green Version]
- Borgo, C.; Ruzzene, M. Protein kinase CK2 inhibition as a pharmacological strategy. Adv. Protein. Chem. Struct. Biol. 2021, 124, 23–46. [Google Scholar] [CrossRef]
- Chen, X.; Li, C.; Wang, D.; Chen, Y.; Zhang, N. Recent advances in the discovery of CK2 allosteric inhibitors: From traditional screening to structure-based design. Molecules 2020, 25, 870. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Laudet, B.; Barette, C.; Dulery, V.; Renaudet, O.; Dumy, P.; Metz, A.; Prudent, R.; Deshiere, A.; Dideberg, O.; Filhol, O.; et al. Structure-based design of small peptide inhibitors of protein kinase CK2 subunit interaction. Biochem. J. 2007, 408, 363–373. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prudent, R.; Moucadel, V.; Laudet, B.; Barette, C.; Lafanechere, L.; Hasenknopf, B.; Li, J.; Bareyt, S.; Lacote, E.; Thorimbert, S.; et al. Identification of polyoxometalates as nanomolar noncompetitive inhibitors of protein kinase CK2. Chem. Biol. 2008, 15, 683–692. [Google Scholar] [CrossRef]
- Viht, K.; Saaver, S.; Vahter, J.; Enkvist, E.; Lavogina, D.; Sinijarv, H.; Raidaru, G.; Guerra, B.; Issinger, O.G.; Uri, A. Acetoxymethyl ester of tetrabromobenzimidazole-peptoid conjugate for inhibition of protein kinase CK2 in living cells. Bioconjug Chem. 2015, 26, 2324–2335. [Google Scholar] [CrossRef] [PubMed]
- Cozza, G.; Zanin, S.; Sarno, S.; Costa, E.; Girardi, C.; Ribaudo, G.; Salvi, M.; Zagotto, G.; Ruzzene, M.; Pinna, L.A. Design, validation and efficacy of bisubstrate inhibitors specifically affecting ecto-CK2 kinase activity. Biochem. J. 2015, 471, 415–430. [Google Scholar] [CrossRef]
- Rosales, M.; Perez, G.V.; Ramon, A.C.; Cruz, Y.; Rodriguez-Ulloa, A.; Besada, V.; Ramos, Y.; Vazquez-Blomquist, D.; Caballero, E.; Aguilar, D.; et al. Targeting of protein kinase CK2 in acute myeloid leukemia cells using the clinical-grade synthetic-peptide CIGB-300. Biomedicines 2021, 9, 766. [Google Scholar] [CrossRef] [PubMed]
- Chaplin, D.D. 1. Overview of the immune response. J. Allergy Clin. Immunol. 2003, 111, S442–S459. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vivier, E.; Malissen, B. Innate and adaptive immunity: Specificities and signaling hierarchies revisited. Nat. Immunol. 2005, 6, 17–21. [Google Scholar] [CrossRef]
- Gasteiger, G.; D’Osualdo, A.; Schubert, D.A.; Weber, A.; Bruscia, E.M.; Hartl, D. Cellular innate immunity: An old game with new players. J. Innate. Immun. 2017, 9, 111–125. [Google Scholar] [CrossRef]
- Cronkite, D.A.; Strutt, T.M. The regulation of inflammation by innate and adaptive lymphocytes. J. Immunol. Res. 2018, 2018, 1467538. [Google Scholar] [CrossRef] [PubMed]
- Mayadas, T.N.; Cullere, X.; Lowell, C.A. The multifaceted functions of neutrophils. Annu. Rev. Pathol. 2014, 9, 181–218. [Google Scholar] [CrossRef] [Green Version]
- Liew, P.X.; Kubes, P. The neutrophil’s role during health and disease. Physiol. Rev. 2019, 99, 1223–1248. [Google Scholar] [CrossRef]
- Borregaard, N. Neutrophils, from marrow to microbes. Immunity 2010, 33, 657–670. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Winterbourn, C.C.; Kettle, A.J.; Hampton, M.B. Reactive oxygen species and neutrophil function. Annu. Rev. Biochem. 2016, 85, 765–792. [Google Scholar] [CrossRef]
- Tecchio, C.; Micheletti, A.; Cassatella, M.A. Neutrophil-derived cytokines: Facts beyond expression. Front. Immunol. 2014, 5, 508. [Google Scholar] [CrossRef] [Green Version]
- Jakubzick, C.V.; Randolph, G.J.; Henson, P.M. Monocyte differentiation and antigen-presenting functions. Nat. Rev. Immunol. 2017, 17, 349–362. [Google Scholar] [CrossRef]
- Guilliams, M.; Mildner, A.; Yona, S. Developmental and functional heterogeneity of monocytes. Immunity 2018, 49, 595–613. [Google Scholar] [CrossRef] [Green Version]
- Gordon, S.; Taylor, P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5, 953–964. [Google Scholar] [CrossRef]
- Prinz, M.; Erny, D.; Hagemeyer, N. Ontogeny and homeostasis of CNS myeloid cells. Nat. Immunol. 2017, 18, 385–392. [Google Scholar] [CrossRef]
- Mantovani, A.; Sica, A.; Locati, M. New vistas on macrophage differentiation and activation. Eur. J. Immunol. 2007, 37, 14–16. [Google Scholar] [CrossRef]
- van der Does, A.M.; Beekhuizen, H.; Ravensbergen, B.; Vos, T.; Ottenhoff, T.H.; van Dissel, J.T.; Drijfhout, J.W.; Hiemstra, P.S.; Nibbering, P.H. LL-37 directs macrophage differentiation toward macrophages with a proinflammatory signature. J. Immunol. 2010, 185, 1442–1449. [Google Scholar] [CrossRef] [Green Version]
- Krausgruber, T.; Blazek, K.; Smallie, T.; Alzabin, S.; Lockstone, H.; Sahgal, N.; Hussell, T.; Feldmann, M.; Udalova, I.A. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat. Immunol. 2011, 12, 231–238. [Google Scholar] [CrossRef]
- Krzyszczyk, P.; Schloss, R.; Palmer, A.; Berthiaume, F. The role of macrophages in acute and chronic wound healing and interventions to promote pro-wound healing phenotypes. Front. Physiol. 2018, 9, 419. [Google Scholar] [CrossRef] [PubMed]
- Arango Duque, G.; Descoteaux, A. Macrophage cytokines: Involvement in immunity and infectious diseases. Front. Immunol. 2014, 5, 491. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Atri, C.; Guerfali, F.Z.; Laouini, D. Role of human macrophage polarization in inflammation during infectious diseases. Int. J. Mol. Sci. 2018, 19, 1801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duan, Z.; Luo, Y. Targeting macrophages in cancer immunotherapy. Signal Transduct. Target. Ther. 2021, 6, 127. [Google Scholar] [CrossRef]
- Cabeza-Cabrerizo, M.; Cardoso, A.; Minutti, C.M.; Pereira da Costa, M.; Reis, E.S.C. Dendritic cells revisited. Annu. Rev. Immunol. 2021, 39, 131–166. [Google Scholar] [CrossRef]
- Eisenbarth, S.C. Dendritic cell subsets in T cell programming: Location dictates function. Nat. Rev. Immunol. 2019, 19, 89–103. [Google Scholar] [CrossRef] [PubMed]
- Martin-Gayo, E.; Yu, X.G. Role of dendritic cells in natural immune control of HIV-1 infection. Front. Immunol. 2019, 10, 1306. [Google Scholar] [CrossRef]
- Kumar, B.V.; Connors, T.J.; Farber, D.L. Human T cell development, localization, and function throughout life. Immunity 2018, 48, 202–213. [Google Scholar] [CrossRef] [Green Version]
- Luckheeram, R.V.; Zhou, R.; Verma, A.D.; Xia, B. CD4(+)T cells: Differentiation and functions. Clin. Dev. Immunol. 2012, 2012, 925135. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dong, C. Cytokine regulation and function in T cells. Annu. Rev. Immunol. 2021, 39, 51–76. [Google Scholar] [CrossRef]
- Zhu, X.; Zhu, J. CD4 T helper cell subsets and related human immunological disorders. Int. J. Mol. Sci. 2020, 21, 8011. [Google Scholar] [CrossRef] [PubMed]
- Sun, B.; Zhang, Y. Overview of orchestration of CD4+ T cell subsets in immune responses. Adv. Exp. Med. Biol. 2014, 841, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Sanz, I.; Wei, C.; Jenks, S.A.; Cashman, K.S.; Tipton, C.; Woodruff, M.C.; Hom, J.; Lee, F.E. Challenges and opportunities for consistent classification of human B cell and plasma cell populations. Front. Immunol. 2019, 10, 2458. [Google Scholar] [CrossRef] [Green Version]
- Adler, L.N.; Jiang, W.; Bhamidipati, K.; Millican, M.; Macaubas, C.; Hung, S.C.; Mellins, E.D. The other function: Class II-restricted antigen presentation by B cells. Front. Immunol. 2017, 8, 319. [Google Scholar] [CrossRef] [Green Version]
- Petersone, L.; Edner, N.M.; Ovcinnikovs, V.; Heuts, F.; Ross, E.M.; Ntavli, E.; Wang, C.J.; Walker, L.S.K. T cell/B cell collaboration and autoimmunity: An intimate relationship. Front. Immunol. 2018, 9, 1941. [Google Scholar] [CrossRef] [PubMed]
- Lund, F.E. Cytokine-producing B lymphocytes-key regulators of immunity. Curr. Opin. Immunol. 2008, 20, 332–338. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pieper, K.; Grimbacher, B.; Eibel, H. B-cell biology and development. J. Allergy Clin. Immunol. 2013, 131, 959–971. [Google Scholar] [CrossRef] [PubMed]
- Allman, D.; Pillai, S. Peripheral B cell subsets. Curr. Opin. Immunol. 2008, 20, 149–157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoffman, W.; Lakkis, F.G.; Chalasani, G. B cells, antibodies, and more. Clin. J. Am. Soc. Nephrol. 2016, 11, 137–154. [Google Scholar] [CrossRef] [PubMed]
- Larson, S.R.; Bortell, N.; Illies, A.; Crisler, W.J.; Matsuda, J.L.; Lenz, L.L. Myeloid cell CK2 regulates inflammation and resistance to bacterial infection. Front. Immunol. 2020, 11, 590266. [Google Scholar] [CrossRef]
- Dinarello, C.A. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 2011, 117, 3720–3732. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liang, M.D.; Zhang, Y.; McDevit, D.; Marecki, S.; Nikolajczyk, B.S. The interleukin-1β gene is transcribed from a poised promoter architecture in monocytes. J. Biol. Chem. 2006, 281, 9227–9237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Y.; Saccani, S.; Shin, H.; Nikolajczyk, B.S. Dynamic protein associations define two phases of IL-1β transcriptional activation. J. Immunol. 2008, 181, 503–512. [Google Scholar] [CrossRef]
- Jung, D.H.; Park, H.J.; Byun, H.E.; Park, Y.M.; Kim, T.W.; Kim, B.O.; Um, S.H.; Pyo, S. Diosgenin inhibits macrophage-derived inflammatory mediators through downregulation of CK2, JNK, NF-κB and AP-1 activation. Int. Immunopharmacol. 2010, 10, 1047–1054. [Google Scholar] [CrossRef]
- Hashimoto, A.; Gao, C.; Mastio, J.; Kossenkov, A.; Abrams, S.I.; Purandare, A.V.; Desilva, H.; Wee, S.; Hunt, J.; Jure-Kunkel, M.; et al. Inhibition of casein kinase 2 disrupts differentiation of myeloid cells in cancer and enhances the efficacy of immunotherapy in mice. Cancer Res. 2018, 78, 5644–5655. [Google Scholar] [CrossRef] [Green Version]
- de Bourayne, M.; Gallais, Y.; El Ali, Z.; Rousseau, P.; Damiens, M.H.; Cochet, C.; Filhol, O.; Chollet-Martin, S.; Pallardy, M.; Kerdine-Romer, S. Protein kinase CK2 controls T-cell polarization through dendritic cell activation in response to contact sensitizers. J. Leukoc. Biol. 2017, 101, 703–715. [Google Scholar] [CrossRef] [PubMed]
- Reverendo, M.; Arguello, R.J.; Polte, C.; Valecka, J.; Camosseto, V.; Auphan-Anezin, N.; Ignatova, Z.; Gatti, E.; Pierre, P. Polymerase III transcription is necessary for T cell priming by dendritic cells. Proc. Natl. Acad. Sci. USA 2019, 116, 22721–22729. [Google Scholar] [CrossRef]
- Voisinne, G.; Gonzalez de Peredo, A.; Roncagalli, R. CD5, an undercover regulator of TCR signaling. Front. Immunol. 2018, 9, 2900. [Google Scholar] [CrossRef]
- Axtell, R.C.; Xu, L.; Barnum, S.R.; Raman, C. CD5-CK2 binding/activation-deficient mice are resistant to experimental autoimmune encephalomyelitis: Protection is associated with diminished populations of IL-17-expressing T cells in the central nervous system. J. Immunol. 2006, 177, 8542–8549. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sestero, C.M.; McGuire, D.J.; De Sarno, P.; Brantley, E.C.; Soldevila, G.; Axtell, R.C.; Raman, C. CD5-dependent CK2 activation pathway regulates threshold for T cell anergy. J. Immunol. 2012, 189, 2918–2930. [Google Scholar] [CrossRef] [Green Version]
- Ulges, A.; Klein, M.; Reuter, S.; Gerlitzki, B.; Hoffmann, M.; Grebe, N.; Staudt, V.; Stergiou, N.; Bohn, T.; Bruhl, T.J.; et al. Protein kinase CK2 enables regulatory T cells to suppress excessive TH2 responses in vivo. Nat. Immunol. 2015, 16, 267–275. [Google Scholar] [CrossRef]
- Gibson, S.A.; Yang, W.; Yan, Z.; Liu, Y.; Rowse, A.L.; Weinmann, A.S.; Qin, H.; Benveniste, E.N. Protein kinase CK2 controls the fate between Th17 cell and regulatory T cell differentiation. J. Immunol. 2017, 198, 4244–4254. [Google Scholar] [CrossRef]
- Ulges, A.; Witsch, E.J.; Pramanik, G.; Klein, M.; Birkner, K.; Buhler, U.; Wasser, B.; Luessi, F.; Stergiou, N.; Dietzen, S.; et al. Protein kinase CK2 governs the molecular decision between encephalitogenic TH17 cell and Treg cell development. Proc. Natl. Acad. Sci. USA 2016, 113, 10145–10150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gibson, S.A.; Yang, W.; Yan, Z.; Qin, H.; Benveniste, E.N. CK2 controls Th17 and regulatory T cell differentiation through inhibition of FoxO1. J. Immunol. 2018, 201, 383–392. [Google Scholar] [CrossRef] [Green Version]
- Yang, W.; Gibson, S.A.; Yan, Z.; Wei, H.; Tao, J.; Sha, B.; Qin, H.; Benveniste, E.N. Protein kinase 2 (CK2) controls CD4(+) T cell effector function in the pathogenesis of colitis. Mucosal. Immunol. 2020, 13, 788–798. [Google Scholar] [CrossRef] [PubMed]
- Wei, H.; Yang, W.; Hong, H.; Yan, Z.; Qin, H.; Benveniste, E.N. Protein kinase CK2 regulates B cell development and differentiation. J. Immunol. 2021, 207, 799–808. [Google Scholar] [CrossRef] [PubMed]
- Shimada, A. Hematological malignancies and molecular targeting therapy. Eur. J. Pharmacol. 2019, 862, 172641. [Google Scholar] [CrossRef] [PubMed]
- Phan-Dinh-Tuy, F.; Henry, J.; Boucheix, C.; Perrot, J.Y.; Rosenfeld, C.; Kahn, A. Protein kinases in human leukemic cells. Am. J. Hematol. 1985, 19, 209–218. [Google Scholar] [CrossRef]
- Roig, J.; Krehan, A.; Colomer, D.; Pyerin, W.; Itarte, E.; Plana, M. Multiple forms of protein kinase CK2 present in leukemic cells: In vitro study of its origin by proteolysis. Mol. Cell Biochem. 1999, 191, 229–234. [Google Scholar] [CrossRef]
- Piazza, F.A.; Ruzzene, M.; Gurrieri, C.; Montini, B.; Bonanni, L.; Chioetto, G.; Di Maira, G.; Barbon, F.; Cabrelle, A.; Zambello, R.; et al. Multiple myeloma cell survival relies on high activity of protein kinase CK2. Blood 2006, 108, 1698–1707. [Google Scholar] [CrossRef] [Green Version]
- Silva, A.; Yunes, J.A.; Cardoso, B.A.; Martins, L.R.; Jotta, P.Y.; Abecasis, M.; Nowill, A.E.; Leslie, N.R.; Cardoso, A.A.; Barata, J.T. PTEN posttranslational inactivation and hyperactivation of the PI3K/Akt pathway sustain primary T cell leukemia viability. J. Clin. Investig. 2008, 118, 3762–3774. [Google Scholar] [CrossRef] [Green Version]
- Pizzi, M.; Piazza, F.; Agostinelli, C.; Fuligni, F.; Benvenuti, P.; Mandato, E.; Casellato, A.; Rugge, M.; Semenzato, G.; Pileri, S.A. Protein kinase CK2 is widely expressed in follicular, Burkitt and diffuse large B-cell lymphomas and propels malignant B-cell growth. Oncotarget 2015, 6, 6544–6552. [Google Scholar] [CrossRef] [Green Version]
- Trembley, J.H.; Chen, Z.; Unger, G.; Slaton, J.; Kren, B.T.; Van Waes, C.; Ahmed, K. Emergence of protein kinase CK2 as a key target in cancer therapy. Biofactors 2010, 36, 187–195. [Google Scholar] [CrossRef] [Green Version]
- Shehata, M.; Schnabl, S.; Demirtas, D.; Hilgarth, M.; Hubmann, R.; Ponath, E.; Badrnya, S.; Lehner, C.; Hoelbl, A.; Duechler, M.; et al. Reconstitution of PTEN activity by CK2 inhibitors and interference with the PI3-K/Akt cascade counteract the antiapoptotic effect of human stromal cells in chronic lymphocytic leukemia. Blood 2010, 116, 2513–2521. [Google Scholar] [CrossRef]
- Mishra, S.; Reichert, A.; Cunnick, J.; Senadheera, D.; Hemmeryckx, B.; Heisterkamp, N.; Groffen, J. Protein kinase CKIIalpha interacts with the Bcr moiety of Bcr/Abl and mediates proliferation of Bcr/Abl-expressing cells. Oncogene 2003, 22, 8255–8262. [Google Scholar] [CrossRef] [Green Version]
- Mishra, S.; Pertz, V.; Zhang, B.; Kaur, P.; Shimada, H.; Groffen, J.; Kazimierczuk, Z.; Pinna, L.A.; Heisterkamp, N. Treatment of P190 Bcr/Abl lymphoblastic leukemia cells with inhibitors of the serine/threonine kinase CK2. Leukemia 2007, 21, 178–180. [Google Scholar] [CrossRef]
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gajewski, T.F.; Schreiber, H.; Fu, Y.X. Innate and adaptive immune cells in the tumor microenvironment. Nat. Immunol. 2013, 14, 1014–1022. [Google Scholar] [CrossRef] [Green Version]
- Veglia, F.; Gabrilovich, D.I. Dendritic cells in cancer: The role revisited. Curr. Opin. Immunol. 2017, 45, 43–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ohue, Y.; Nishikawa, H. Regulatory T (Treg) cells in cancer: Can Treg cells be a new therapeutic target? Cancer Sci. 2019, 110, 2080–2089. [Google Scholar] [CrossRef]
- Song, C.; Ge, Z.; Ding, Y.; Tan, B.H.; Desai, D.; Gowda, K.; Amin, S.; Gowda, R.; Robertson, G.P.; Yue, F.; et al. IKAROS and CK2 regulate expression of BCL-XL and chemosensitivity in high-risk B-cell acute lymphoblastic leukemia. Blood 2020, 136, 1520–1534. [Google Scholar] [CrossRef]
- Bernardi, C.; Maurer, G.; Ye, T.; Marchal, P.; Jost, B.; Wissler, M.; Maurer, U.; Kastner, P.; Chan, S.; Charvet, C. CD4(+) T cells require Ikaros to inhibit their differentiation toward a pathogenic cell fate. Proc. Natl. Acad. Sci. USA 2021, 118, e2023172118. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. 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
Hong, H.; Benveniste, E.N. The Immune Regulatory Role of Protein Kinase CK2 and Its Implications for Treatment of Cancer. Biomedicines 2021, 9, 1932. https://doi.org/10.3390/biomedicines9121932
Hong H, Benveniste EN. The Immune Regulatory Role of Protein Kinase CK2 and Its Implications for Treatment of Cancer. Biomedicines. 2021; 9(12):1932. https://doi.org/10.3390/biomedicines9121932
Chicago/Turabian StyleHong, Huixian, and Etty N. Benveniste. 2021. "The Immune Regulatory Role of Protein Kinase CK2 and Its Implications for Treatment of Cancer" Biomedicines 9, no. 12: 1932. https://doi.org/10.3390/biomedicines9121932