CD4+NKG2D+ T cells exhibit enhanced migratory and encephalitogenic properties in Neuroinflammation

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Ruck, Tobias ^a   Bittner, Stefan ^a,b   Gross, Catharina C ^a   Breuer, Johanna ^a   Albrecht, Stefanie ^a   Korr, Sabrina ^a   Göbel, Kerstin ^a   Pankratz, Susann ^a   Henschel, Christian M ^a   Schwab, Nicholas ^a   Staszewski, Ori ^c   Prinz, Marco ^c   Kuhlmann, Tanja ^a   Meuth, Sven G ^a   Wiendl, Heinz ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b Interdisciplinary Center for Clinical Research (IZKF)   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CORTICOSTEROID; GAMMA INTERFERON; INTERLEUKIN 17; NATURAL KILLER CELL RECEPTOR NKG2D;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CD4+NKG2D+ T LYMPHOCYTE; CEREBROSPINAL FLUID; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; DISEASE SEVERITY; ENDOTHELIUM CELL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; MALE; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OLIGODENDROGLIA; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BLOCKING; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

BLOOD-BRAIN BARRIER; CD4-POSITIVE T-LYMPHOCYTES; CHEMOTAXIS, LEUKOCYTE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MULTIPLE SCLEROSIS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; SIGNAL TRANSDUCTION;

EID: 84896734088     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081455     Document Type: Article

References (38)

1. Martin R, McFarland HF, McFarlin DE (1992) Immunological aspects of demyelinating diseases. Annu Rev Immunol 10: 153-187. doi:10.1146/ annurev.iy.10.040192.001101. PubMed: 1375472.
2. Hafler DA, Slavik JM, Anderson DE, O'Connor KC, De Jager P et al. (2005). Multiple Sclerosis - Immunol Rev 204: 208-231.
3. June CH, Bluestone JA, Nadler LM, Thompson CB (1994) The B7 and CD28 receptor families. Immunol Today 15: 321-331. doi: 10.1016/0167-5699(94)90080-9. PubMed: 7522010. (Pubitemid 24231747)
4. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR et al. (2001) Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2: 255-260. doi:10.1038/85321. PubMed: 11224526. (Pubitemid 33706003)
5. Ortler S, Leder C, Mittelbronn M, Zozulya AL, Knolle PA et al. (2008) B7-H1 restricts neuroantigen-specific T cell responses and confines inflammatory CNS damage: implications for the lesion pathogenesis of multiple sclerosis. Eur J Immunol 38: 1734-1744. doi:10.1002/eji.200738071. PubMed: 18421793.
6. Allez M, Tieng V, Nakazawa A, Treton X, Pacault V et al. (2007) CD4+NKG2D+ T cells in Crohn's disease mediate inflammatory and cytotoxic responses through MICA interactions. Gastroenterology 132: 2346-2358. doi:10.1053/j.gastro.2007.03.025. PubMed: 17570210. (Pubitemid 46890855)
7. Bauer S, Groh V, Wu J, Steinle A, Phillips JH et al. (1999) Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285: 727-729. doi:10.1126/science.285.5428.727. PubMed: 10426993.
8. Raulet DH (2003) Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 3: 781-790. doi:10.1038/nri1199. PubMed: 14523385.
9. Groh V, Smythe K, Dai Z, Spies T (2006) Fas-ligand-mediated paracrine T cell regulation by the receptor NKG2D in tumor immunity. Nat Immunol 7: 755-762. doi:10.1038/ni1350. PubMed: 16732291. (Pubitemid 43905875)
10. Groh V, Bruhl A, El-Gabalawy H, Nelson JL, Spies T (2003) Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc Natl Acad Sci U S A 100: 9452-9457. doi:10.1073/pnas.1632807100. PubMed: 12878725. (Pubitemid 37033949)
11. Ito Y, Kanai T, Totsuka T, Okamoto R, Tsuchiya K et al. (2008) Blockade of NKG2D signaling prevents the development of murine CD4+ T cell-mediated colitis. Am J Physiol Gastrointest Liver Physiol 294: G199-G207. PubMed: 17962357.
12. Andersson AK, Sumariwalla PF, McCann FE, Amjadi P, Chang C et al. (2011) Blockade of NKG2D ameliorates disease in mice with collagen-induced arthritis: a potential pathogenic role in chronic inflammatory arthritis. Arthritis Rheum 63: 2617-2629. doi:10.1002/art.30460. PubMed: 21618462.
13. Pariente B, Mocan I, Camus M, Dutertre CA, Ettersperger J, et al. (2011) Activation of the receptor NKG2D leads to production of Th17 cytokines in CD4+ T cells of patients with Crohn's disease. Gastroenterology 141: 217-226, e211-212
14. Dai Z, Turtle CJ, Booth GC, Riddell SR, Gooley TA et al. (2009) Normally occurring NKG2D+CD4+ T cells are immunosuppressive and inversely correlated with disease activity in juvenile-onset lupus. J Exp Med 206: 793-805. doi:10.1084/jem.20081648. PubMed: 19289577.
15. Steinle A, Li P, Morris DL, Groh V, Lanier LL et al. (2001) Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics 53: 279-287. doi: 10.1007/s002510100325. PubMed: 11491531. (Pubitemid 32678762)
16. Eagle RA, Traherne JA, Hair JR, Jafferji I, Trowsdale J (2009) ULBP6/ RAET1L is an additional human NKG2D ligand. Eur J Immunol 39: 3207-3216. doi:10.1002/eji.200939502. PubMed: 19658097.
17. Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR et al. (2002) The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17: 19-29. doi:10.1016/S1074-7613(02)00333-3. PubMed: 12150888. (Pubitemid 34874615)
18. Champsaur M, Lanier LL (2010) Effect of NKG2D ligand expression on host immune responses. Immunol Rev 235: 267-285. PubMed: 20536569.
19. Saikali P, Antel JP, Newcombe J, Chen Z, Freedman M et al. (2007) NKG2D-mediated cytotoxicity toward oligodendrocytes suggests a mechanism for tissue injury in multiple sclerosis. J Neurosci 27: 1220-1228. doi:10.1523/JNEUROSCI.4402-06.2007. PubMed: 17267578. (Pubitemid 46203331)
20. Ogasawara K, Hamerman JA, Ehrlich LR, Bour-Jordan H, Santamaria P et al. (2004) NKG2D blockade prevents autoimmune diabetes in NOD mice. Immunity 20: 757-767. doi:10.1016/j.immuni.2004.05.008. PubMed: 15189740. (Pubitemid 38757445)
21. Van Belle TL, Ling E, Haase C, Bresson D, Ursø B et al. (2013) NKG2D blockade facilitates diabetes prevention by antigen-specific Tregs in a virus-induced model of diabetes. J Autoimmun 40: 66-73. doi:10.1016/j.jaut.2012. 08.001. PubMed: 22944096.
22. Kjellev S, Haase C, Lundsgaard D, Ursø B, Tornehave D et al. (2007) Inhibition of NKG2D receptor function by antibody therapy attenuates transfer-induced colitis in SCID mice. Eur J Immunol 37: 1397-1406. doi:10.1002/eji.200636473. PubMed: 17407193. (Pubitemid 46925322)
23. Maccalli C, Scaramuzza S, Parmiani G (2009) TNK cells (NKG2D+ CD8+ or CD4+ T lymphocytes) in the control of human tumors. Cancer Immunol Immunother 58: 801-808. doi:10.1007/s00262-008-0635-x. PubMed: 19089424.
24. Tejada-Simon MV, Hong J, Rivera VM, Zhang JZ (2001) Reactivity pattern and cytokine profile of T cells primed by myelin peptides in multiple sclerosis and healthy individuals. Eur J Immunol 31: 907-917. doi:10.1002/1521- 4141(200103)31:3. PubMed: 11241296. (Pubitemid 32237127)
25. de Rosbo NK, Ben-Nun A (1998) T-cell responses to myelin antigens in multiple sclerosis; relevance of the predominant autoimmune reactivity to myelin oligodendrocyte glycoprotein. J Autoimmun 11: 287-299. doi: 10.1006/jaut.1998.0202. PubMed: 9776706.
26. Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D et al. (2009) 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. doi:10.1038/ni.1716. PubMed: 19305396.
27. Langer HF, Choi EY, Zhou H, Schleicher R, Chung KJ et al. (2012) Platelets contribute to the pathogenesis of experimental autoimmune encephalomyelitis. Circ Res 110: 1202-1210. doi:10.1161/CIRCRESAHA.111.256370. PubMed: 22456181.
28. Kopp HG, Placke T, Salih HR (2009) Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res 69: 7775-7783. doi: 10.1158/0008-5472.CAN-09- 2123. PubMed: 19738039.
29. Rentzos M, Cambouri C, Rombos A, Nikolaou C, Anagnostouli M et al. (2006) IL-15 is elevated in serum and cerebrospinal fluid of patients with multiple sclerosis. J Neurol Sci 241: 25-29. doi:10.1016/j.jns.2005.10.003. PubMed: 16316662. (Pubitemid 43112512)
30. Saikali P, Antel JP, Pittet CL, Newcombe J, Arbour N (2010) Contribution of astrocyte-derived IL-15 to CD8 T cell effector functions in multiple sclerosis. J Immunol 185: 5693-5703. doi:10.4049/jimmunol.1002188. PubMed: 20926794.
31. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP et al. (2001) Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 50: 121-127. doi:10.1002/ana.1032. PubMed: 11456302.
32. Feger U, Tolosa E, Huang YH, Waschbisch A, Biedermann T et al. (2007) HLA-G expression defines a novel regulatory T-cell subset present in human peripheral blood and sites of inflammation. Blood 110: 568-577. doi:10.1182/blood-2006-11-057125. PubMed: 17371944. (Pubitemid 47105395)
33. Huang YH, Zozulya AL, Weidenfeller C, Metz I, Buck D et al. (2009) Specific central nervous system recruitment of HLA-G(+) regulatory T cells in multiple sclerosis. Ann Neurol 66: 171-183. doi:10.1002/ana.21705. PubMed: 19705413.
34. Göbel K, Pankratz S, Schneider-Hohendorf T, Bittner S, Schuhmann MK et al. (2011) Blockade of the kinin receptor B1 protects from autoimmune CNS disease by reducing leukocyte trafficking. J Autoimmun, 36: 106-14. PubMed: 21216565.
35. Bittner S, Ruck T, Schuhmann MK, Herrmann AM, Maati HM et al. (2013) Endothelial TWIK-related potassium channel-1 (TREK1) regulates immune-cell trafficking into the CNS. Nat Med 19: 1161-1165. doi:10.1038/nm.3303. PubMed: 23933981.
36. Wong D, Dorovini-Zis K, Vincent SR (2004) Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier. Exp Neurol 190: 446-455. doi:10.1016/j.expneurol.2004.08.008. PubMed: 15530883. (Pubitemid 39504999)
37. Chen SH, Stins MF, Huang SH, Chen YH, Kwon-Chung KJ et al. (2003) Cryptococcus neoformans induces alterations in the cytoskeleton of human brain microvascular endothelial cells. J Med Microbiol 52: 961-970. doi:10.1099/jmm.0.05230-0. PubMed: 14532340. (Pubitemid 38648135)
38. Lanz TV, Becker S, Osswald M, Bittner S, Schuhmann MK et al. (2013) Protein kinase Cbeta as a therapeutic target stabilizing blood-brain barrier disruption in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 110: 14735-14740. doi:10.1073/pnas.1302569110. PubMed: 23959874.