Regulation of T-cell activation and migration by the kinase TBK1 during neuroinflammation

Nature Communications

Volumn 6, Issue , 2015, Pages

  Yu, Jiayi ^a   Zhou, Xiaofei ^a   Chang, Mikyoung ^a   Nakaya, Mako ^a,b   Chang, Jae Hoon ^a,c   Xiao, Yichuan ^a   William Lindsey, J ^d   Dorta Estremera, Stephanie ^a,e   Cao, Wei ^a,e   Zal, Anna ^a   Zal, Tomasz ^a,e   Sun, Shao Cong ^a,e  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF FUKUI   (Japan)

^c Yeungnam University   (South Korea)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOTRANSFERASE; PROTEIN KINASE B; TBK1 KINASE; UNCLASSIFIED DRUG; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; PROTEIN SERINE THREONINE KINASE; TARGET OF RAPAMYCIN KINASE; TBK1 PROTEIN, HUMAN; TBK1 PROTEIN, MOUSE;

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; IMMUNE RESPONSE; IMMUNITY; INHIBITION; MOLECULAR ANALYSIS; NERVOUS SYSTEM DISORDER; NEUROLOGY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EFFECTOR CELL; LYMPHOCYTE MIGRATION; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UBIQUITINATION; ANIMAL; AUTOIMMUNITY; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MOTION; CELL SEPARATION; CENTRAL NERVOUS SYSTEM; CYTOLOGY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; JURKAT CELL LINE; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; MACROPHAGE; MALE; METABOLISM; ORTHOMYXOVIRIDAE; PHOSPHORYLATION; T LYMPHOCYTE;

MUS;

ANIMALS; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELL SEPARATION; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; ORTHOMYXOVIRIDAE; PHENOTYPE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TOR SERINE-THREONINE KINASES;

EID: 84949092447     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7074     Document Type: Article

References (51)

1. Ohashi, P. S. T-cell signalling and autoimmunity: molecular mechanisms of disease. Nat. Rev. Immunol. 2, 427-438 (2002).
2. Frohman, E. M., Racke, M. K. & Raine, C. S. Multiple sclerosis-the plaque and its pathogenesis. N. Engl. J. Med. 354, 942-955 (2006).
3. Simmons, S. B., Pierson, E. R., Lee, S. Y. & Goverman, J. M. Modeling the heterogeneity of multiple sclerosis in animals. Trends Immunol. 34, 410-422 (2013).
4. Goverman, J. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9, 393-407 (2009).
5. Sallusto, F. et al. T-cell trafficking in the central nervous system. Immunol. Rev. 248, 216-227 (2012).
6. Zhu, J., Yamane, H. & Paul, W. E. Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 28, 445-489 (2010).
7. Fitzgerald, K. A. et al. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4, 491-496 (2003).
8. Sharma, S. et al. Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151 (2003).
9. McWhirter, S. M. et al. IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl Acad. Sci. USA 101, 233-238 (2004).
10. Hemmi, H. et al. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199, 1641-1650 (2004).
11. Perry, A. K., Chow, E. K., Goodnough, J. B., Yeh, W. C. & Cheng, G. Differential requirement for TANK-binding kinase-1 in type I interferon responses to toll-like receptor activation and viral infection. J. Exp. Med. 199, 1651-1658 (2004).
12. Solt, L. A. & May, M. J. The IkappaB kinase complex: master regulator of NF-kappaB signaling. Immunol. Res. 42, 3-18 (2008).
13. Verhelst, K., Verstrepen, L., Carpentier, I. & Beyaert, R. IkappaB kinase epsilon (IKKepsilon): a therapeutic target in inflammation and cancer. Biochem. Pharmacol. 85, 873-880 (2013).
14. Hiscott, J. Convergence of the NF-kappaB and IRF pathways in the regulation of the innate antiviral response. Cytokine Growth Factor Rev. 18, 483-490 (2007).
15. Bonnard, M. et al. Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-kB-dependent gene transcription. EMBO J. 19, 4976-4985 (2000).
16. Gaide, O. et al. CARMA1 is a critical lipid raft-associated regulator of TCRinduced NF-kappa B activation. Nat. Immunol. 3, 836-843 (2002).
17. Wang, D. et al. A requirement for CARMA1 in TCR-induced NF-kappa B activation. Nat. Immunol. 3, 830-835 (2002).
18. Harhaj, E. W. et al. Somatic mutagenesis studies of NF-kappa B signaling in human T cells: evidence for an essential role of IKK gamma in NF-kappa B activation by T-cell costimulatory signals and HTLV-I Tax protein. Oncogene 19, 1386-1391 (2000).
19. Harp, J. R. & Onami, T. M. Naive T cells re-distribute to the lungs of selectin ligand deficient mice. PLoS ONE 5, e10973 (2010).
20. Arbones, M. L. et al. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity 1, 247-260 (1994).
21. Finlay, D. & Cantrell, D. A. Metabolism, migration and memory in cytotoxic T cells. Nat. Rev. Immunol. 11, 109-117 (2011).
22. Reboldi, A. et al. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 10, 514-523 (2009).
23. Sporici, R. & Issekutz, T. B. CXCR3 blockade inhibits T-cell migration into the CNS during EAE and prevents development of adoptively transferred, but not actively induced, disease. Eur. J. Immunol. 40, 2751-2761 (2010).
24. Odoardi, F. et al. T cells become licensed in the lung to enter the central nervous system. Nature 488, 675-679 (2012).
25. Fabre, S. et al. Stable activation of phosphatidylinositol 3-kinase in the T cell immunological synapse stimulates Akt signaling to FoxO1 nuclear exclusion and cell growth control. J. Immunol. 174, 4161-4171 (2005).
26. Chi, H. Regulation and function of mTOR signalling in T cell fate decisions. Nat. Rev. Immunol. 12, 325-338 (2012).
27. Sprent, J. & Surh, C. D. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat. Immunol. 12, 478-484 (2011).
28. Clark, K. et al. Novel cross-talk within the IKK family controls innate immunity. Biochem. J. 434, 93-104 (2011).
29. Joung, S. M. et al. Akt contributes to activation of the TRIF-dependent signaling pathways of TLRs by interacting with TANK-binding kinase 1. J. Immunol. 186, 499-507 (2011).
30. Pelletier, D. & Hafler, D. A. Fingolimod for multiple sclerosis. N. Engl. J. Med. 366, 339-347 (2012).
31. Groves, A., Kihara, Y. & Chun, J. Fingolimod: direct CNS effects of sphingosine 1-phosphate (S1P) receptor modulation and implications in multiple sclerosis therapy. J. Neurol. Sci. 328, 9-18 (2013).
32. Finlay, D. & Cantrell, D. Phosphoinositide 3-kinase and the mammalian target of rapamycin pathways control T cell migration. Ann. NY Acad. Sci. 1183, 149-157 (2010).
33. Kebir, H. et al. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 13, 1173-1175 (2007).
34. Zhang, F., Shi, Y., Wang, L. & Sriram, S. Role of HDAC3 on p53 expression and apoptosis in T cells of patients with multiple sclerosis. PLoS ONE 6, e16795 (2011).
35. Kemppinen, A. K., Kaprio, J., Palotie, A. & Saarela, J. Systematic review of genome-wide expression studies in multiple sclerosis. BMJ Open 1, e000053 (2011).
36. Reilly, S. M. et al. An inhibitor of the protein kinases TBK1 and IKK-varepsilon improves obesity-related metabolic dysfunctions in mice. Nat. Med. 19, 313-321 (2013).
37. Sebzda, E., Zou, Z., Lee, J. S., Wang, T. & Kahn, M. L. Transcription factor KLF2 regulates the migration of naive T cells by restricting chemokine receptor expression patterns. Nat. Immunol. 9, 292-300 (2008).
38. Kerdiles, Y. M. et al. Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat. Immunol. 10, 176-184 (2009).
39. Masopust, D. & Schenkel, J. M. The integration of T cell migration, differentiation and function. Nat. Rev. Immunol. 13, 309-320 (2013).
40. Pham, T. H., Okada, T., Matloubian, M., Lo, C. G. & Cyster, J. G. S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity 28, 122-133 (2008).
41. Carlson, C. M. et al. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature 442, 299-302 (2006).
42. Fabre, S. et al. FOXO1 regulates L-Selectin and a network of human T cell homing molecules downstream of phosphatidylinositol 3-kinase. J. Immunol. 181, 2980-2989 (2008).
43. Rougerie, P. et al. Fam65b is a new transcriptional target of FOXO1 that regulates RhoA signaling for T lymphocyte migration. J. Immunol. 190, 748-755 (2013).
44. Jin, J. et al. The kinase TBK1 controls IgA class switching by negatively regulating noncanonical NF-kappaB signaling. Nat. Immunol. 13, 1101-1109 (2012).
45. Xie, X. et al. I{kappa}B kinase {varepsilon} and TANK-binding kinase 1 activate AKT by direct phosphorylation. Proc. Natl Acad. Sci. USA 108, 6474-6479 (2011).
46. Hara, H. et al. The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18, 763-775 (2003).
47. Pasparakis, M. et al. TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature 417, 861-866 (2002).
48. Reiley, W., Zhang, M. & Sun, S.-C. Tumor suppressor negatively regulates JNK signaling pathway downstream of TNFR members. J. Biol. Chem. 279, 55161-55167 (2004).
49. Reiley, W. W. et al. Deubiquitinating enzyme CYLD negatively regulates the ubiquitin-dependent kinase Tak1 and prevents abnormal T cell responses. J. Exp. Med. 204, 1475-1485 (2007).
50. Cvijic, M. E., Xiao, G. & Sun, S. C. Study of T-cell signaling by somatic cell mutagenesis and complementation cloning. J. Immunol. Methods 278, 293-304 (2003).
51. Uhlik, M. et al. NF-kappaB-inducing kinase and IkappaB kinase participate in human T-cell leukemia virus I Tax-mediated NF-kappaB activation. J. Biol. Chem. 273, 21132-21136 (1998).