Neuroantigen-specific CD8+ regulatory T-cell function is deficient during acute exacerbation of multiple sclerosis

Journal of Autoimmunity

Volumn 36, Issue 2, 2011, Pages 115-124

  Baughman, Ethan J ^a   Mendoza, Jason P ^a   Ortega, Sterling B ^a   Ayers, Chris L ^a   Greenberg, Benjamin M ^a   Frohman, Elliot M ^a   Karandikar, Nitin J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

CD8; Exacerbation; Immune regulation; Multiple sclerosis; Suppressor; Treg

Indexed keywords

ANTIGEN; AUTOANTIGEN; NEUROANTIGEN; UNCLASSIFIED DRUG;

ADULT; AGED; ANTIGENICITY; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE EXACERBATION; FEMALE; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MALE; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ADULT; AGED; ANTIGENS; AUTOANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; FEMALE; FLOW CYTOMETRY; HUMANS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; T-LYMPHOCYTES, REGULATORY; YOUNG ADULT;

EID: 79951960075     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2010.12.003     Document Type: Article

References (54)

1. McFarland H.F., Martin R. Multiple sclerosis: a complicated picture of autoimmunity. Nat Immunol 2007, 8:913-919.
2. Arbour N., Holz A., Sipe J.C., Naniche D., Romine J.S., Zyroff J., et al. A new approach for evaluating antigen-specific T cell responses to myelin antigens during the course of multiple sclerosis. J Neuroimmunol 2003, 137:197-209.
3. Crawford M.P., Yan S.X., Ortega S.B., Mehta R.S., Hewitt R.E., Price D.A., et al. High prevalence of autoreactive, neuroantigen-specific CD8+ T cells in multiple sclerosis revealed by novel flow cytometric assay. Blood 2004, 103:4222-4231.
4. Babbe H., Roers A., Waisman A., Lassmann H., Goebels N., Hohlfeld R., et al. Clonal expansions of CD8(+) T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction. J Exp Med 2000, 192:393-404.
5. Huseby E.S., Liggitt D., Brabb T., Schnabel B., Ohlen C., Goverman J. A pathogenic role for myelin-specific CD8(+) T cells in a model for multiple sclerosis. J Exp Med 2001, 194:669-676.
6. Jacobsen M., Cepok S., Quak E., Happel M., Gaber R., Ziegler A., et al. Oligoclonal expansion of memory CD8+ T cells in cerebrospinal fluid from multiple sclerosis patients. Brain 2002, 125:538-550.
7. Skulina C., Schmidt S., Dornmair K., Babbe H., Roers A., Rajewsky K., et al. Multiple sclerosis: brain-infiltrating CD8+ T cells persist as clonal expansions in the cerebrospinal fluid and blood. Proc Natl Acad Sci U S A 2004, 101:2428-2433.
8. Jurewicz A., Biddison W.E., Antel J.P. MHC class I-restricted lysis of human oligodendrocytes by myelin basic protein peptide-specific CD8 T lymphocytes. J Immunol 1998, 160:3056-3059.
9. Niland B., Banki K., Biddison W.E., Perl A. CD8+ T cell-mediated HLA-A*0201-restricted cytotoxicity to transaldolase peptide 168-176 in patients with multiple sclerosis. J Immunol 2005, 175:8365-8378.
10. Chess L., Jiang H. Resurrecting CD8+ suppressor T cells. Nat Immunol 2004, 5:469-471.
11. Sarantopoulos S., Lu L., Cantor H. Qa-1 restriction of CD8+ suppressor T cells. J Clin Invest 2004, 114:1218-1221.
12. Smith T.R., Kumar V. Revival of CD8+ Treg-mediated suppression. Trends Immunol 2008, 29:337-342.
13. Tang Q., Henriksen K.J., Bi M., Finger E.B., Szot G., Ye J., et al. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 2004, 199:1455-1465.
14. Tennakoon D.K., Mehta R.S., Ortega S.B., Bhoj V., Racke M.K., Karandikar N.J. Therapeutic induction of regulatory, cytotoxic CD8+ T cells in multiple sclerosis. J Immunol 2006, 176:7119-7129.
15. York N.R., Mendoza J.P., Ortega S.B., Benagh A., Tyler A.F., Firan M., et al. Immune regulatory CNS-reactive CD8+T cells in experimental autoimmune encephalomyelitis. J Autoimmun 2010, 35:33-44.
16. Lee Y.H., Ishida Y., Rifa'i M., Shi Z., Isobe K., Suzuki H. Essential role of CD8+CD122+ regulatory T cells in the recovery from experimental autoimmune encephalomyelitis. J Immunol 2008, 180:825-832.
17. Hu D., Ikizawa K., Lu L., Sanchirico M.E., Shinohara M.L., Cantor H. Analysis of regulatory CD8 T cells in Qa-1-deficient mice. Nat Immunol 2004, 5:516-523.
18. Chen M.L., Yan B.S., Kozoriz D., Weiner H.L. Novel CD8+ Treg suppress EAE by TGF-beta- and IFN-gamma-dependent mechanisms. Eur J Immunol 2009, 39:3423-3435.
19. Chang X., Zheng P., Liu Y. FoxP3: a genetic link between immunodeficiency and autoimmune diseases. Autoimmun Rev 2006, 5:399-402.
20. Bonelli M., Smolen J.S., Scheinecker C. Treg and lupus. Ann Rheum Dis 2010, 69(Suppl. 1):i65-i66.
21. Brusko T., Atkinson M. Treg in type 1 diabetes. Cell Biochem Biophys 2007, 48:165-175.
22. Jaeckel E., Kretschmer K., Apostolou I., von Boehmer H. Instruction of Treg commitment in peripheral T cells is suited to reverse autoimmunity. Semin Immunol 2006, 18:89-92.
23. Viglietta V., Baecher-Allan C., Weiner H.L., Hafler D.A. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis. J Exp Med 2004, 199:971-979.
24. Haas J., Hug A., Viehover A., Fritzsching B., Falk C.S., Filser A., et al. Reduced suppressive effect of CD4+CD25high regulatory T cells on the T cell immune response against myelin oligodendrocyte glycoprotein in patients with multiple sclerosis. Eur J Immunol 2005, 35:3343-3352.
25. Venken K., Hellings N., Thewissen M., Somers V., Hensen K., Rummens J.L., et al. Compromised CD4+ CD25(high) regulatory T-cell function in patients with relapsing-remitting multiple sclerosis is correlated with a reduced frequency of FOXP3-positive cells and reduced FOXP3 expression at the single-cell level. Immunology 2008, 123:79-89.
26. Antel J., Bania M., Noronha A., Neely S. Defective suppressor cell function mediated by T8+ cell lines from patients with progressive multiple sclerosis. J Immunol 1986, 137:3436-3439.
27. Antel J., Brown M., Nicholas M.K., Blain M., Noronha A., Reder A. Activated suppressor cell function in multiple sclerosis-clinical correlations. J Neuroimmunol 1988, 17:323-330.
28. Karandikar N.J., Crawford M.P., Yan X., Ratts R.B., Brenchley J.M., Ambrozak D.R., et al. Glatiramer acetate (Copaxone) therapy induces CD8(+) T cell responses in patients with multiple sclerosis. J Clin Invest 2002, 109:641-649.
29. Yssel H., Spits H. Generation and maintenance of cloned human T cell lines. Curr Protoc Immunol 2002, Chapter 7: Unit 7.19.
30. Berger C., Jensen M.C., Lansdorp P.M., Gough M., Elliott C., Riddell S.R. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest 2008, 118:294-305.
31. Joosten S.A., van Meijgaarden K.E., Savage N.D., de Boer T., Triebel F., van der Wal A., et al. Identification of a human CD8+ regulatory T cell subset that mediates suppression through the chemokine CC chemokine ligand 4. Proc Natl Acad Sci U S A 2007, 104:8029-8034.
32. Herzenberg L.A., Tung J., Moore W.A., Herzenberg L.A., Parks D.R. Interpreting flow cytometry data: a guide for the perplexed. Nat Immunol 2006, 7:681-685.
33. Bach M.A., Phan-Dinh-Tuy F., Tournier E., Chatenoud L., Bach J.F., Martin C., et al. Deficit of suppressor T cells in active multiple sclerosis. Lancet 1980, 2:1221-1223.
34. Antel J.P., Bania M.B., Reder A., Cashman N. Activated suppressor cell dysfunction in progressive multiple sclerosis. J Immunol 1986, 137:137-141.
35. Kang H.K., Liu M., Datta S.K. Low-dose peptide tolerance therapy of lupus generates plasmacytoid dendritic cells that cause expansion of autoantigen-specific regulatory T cells and contraction of inflammatory Th17 cells. J Immunol 2007, 178:7849-7858.
36. James E.A., Kwok W.W. CD8+ suppressor-mediated regulation of human CD4+ T cell responses to glutamic acid decarboxylase 65. Eur J Immunol 2007, 37:78-86.
37. Tsai S., Shameli A., Yamanouchi J., Clemente-Casares X., Wang J., Serra P., et al. Reversal of autoimmunity by boosting memory-like autoregulatory T cells. Immunity 2010, 32:568-580.
38. Colovai A.I., Mirza M., Vlad G., Wang S., Ho E., Cortesini R., et al. Regulatory CD8+CD28- T cells in heart transplant recipients. Hum Immunol 2003, 64:31-37.
39. Filaci G., Fenoglio D., Fravega M., Ansaldo G., Borgonovo G., Traverso P., et al. CD8+ CD28- T regulatory lymphocytes inhibiting T cell proliferative and cytotoxic functions infiltrate human cancers. J Immunol 2007, 179:4323-4334.
40. Koide J., Engleman E.G. Differences in surface phenotype and mechanism of action between alloantigen-specific CD8+ cytotoxic and suppressor T cell clones. J Immunol 1990, 144:32-40.
41. Lin Y.X., Wang L.L., Yan L.N., Cai P., Li B., Wen T.F., et al. Analysis of CD8+CD28- T-suppressor cells in living donor liver transplant recipients. Hepatobiliary Pancreat Dis Int 2009, 8:241-246.
42. Sindhi R., Manavalan J.S., Magill A., Suciu-Foca N., Zeevi A. Reduced immunosuppression in pediatric liver-intestine transplant recipients with CD8+CD28- T-suppressor cells. Hum Immunol 2005, 66:252-257.
43. Suciu-Foca N., Manavalan J.S., Scotto L., Kim-Schulze S., Galluzzo S., Naiyer A.J., et al. Molecular characterization of allospecific T suppressor and tolerogenic dendritic cells: review. Int Immunopharmacol 2005, 5:7-11.
44. Trzonkowski P., Zilvetti M., Chapman S., Wieckiewicz J., Sutherland A., Friend P., et al. Homeostatic repopulation by CD28-CD8+ T cells in alemtuzumab-depleted kidney transplant recipients treated with reduced immunosuppression. Am J Transplant 2008, 8:338-347.
45. Peng G., Wang H.Y., Peng W., Kiniwa Y., Seo K.H., Wang R.F. Tumor-infiltrating gammadelta T cells suppress T and dendritic cell function via mechanisms controlled by a unique toll-like receptor signaling pathway. Immunity 2007, 27:334-348.
46. Mahic M., Henjum K., Yaqub S., Bjornbeth B.A., Torgersen K.M., Tasken K., et al. Generation of highly suppressive adaptive CD8(+)CD25(+)FOXP3(+) regulatory T cells by continuous antigen stimulation. Eur J Immunol 2008, 38:640-646.
47. Lu L., Yu Y., Li G., Pu L., Zhang F., Zheng S., et al. CD8(+)CD103(+) regulatory T cells in spontaneous tolerance of liver allografts. Int Immunopharmacol 2009, 9:546-548.
48. Uss E., Rowshani A.T., Hooibrink B., Lardy N.M., van Lier R.A., ten Berge I.J. CD103 is a marker for alloantigen-induced regulatory CD8+ T cells. J Immunol 2006, 177:2775-2783.
49. Izawa A., Yamaura K., Albin M.J., Jurewicz M., Tanaka K., Clarkson M.R., et al. A novel alloantigen-specific CD8+PD1+ regulatory T cell induced by ICOS-B7h blockade in vivo. J Immunol 2007, 179:786-796.
50. Bienvenu B., Martin B., Auffray C., Cordier C., Becourt C., Lucas B. Peripheral CD8+CD25+ T lymphocytes from MHC class II-deficient mice exhibit regulatory activity. J Immunol 2005, 175:246-253.
51. Kiniwa Y., Miyahara Y., Wang H.Y., Peng W., Peng G., Wheeler T.M., et al. CD8+ Foxp3+ regulatory T cells mediate immunosuppression in prostate cancer. Clin Cancer Res 2007, 13:6947-6958.
52. Manavalan J.S., Kim-Schulze S., Scotto L., Naiyer A.J., Vlad G., Colombo P.C., et al. Alloantigen specific CD8+CD28- FOXP3+ T suppressor cells induce ILT3+ ILT4+ tolerogenic endothelial cells, inhibiting alloreactivity. Int Immunol 2004, 16:1055-1068.
53. Meloni F., Cascina A., Paschetto E., Marone Bianco A., Morosini M., Pellegrini C., et al. Monocyte chemoattractant protein-1 levels in bronchoalveolar lavage fluid of lung-transplanted patients treated with tacrolimus as rescue treatment for refractory acute rejection. Transplant Proc 2003, 35:1523-1526.
54. Joosten S.A., Ottenhoff T.H. Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination. Hum Immunol 2008, 69:760-770.