Th17 expansion in MS patients is counterbalanced by an expanded CD39 + regulatory T cell population during remission but not during relapse

Journal of Neuroimmunology

Volumn 240-241, Issue , 2011, Pages 97-103

  Peelen, Evelyn ^a,b   Damoiseaux, Jan ^a   Smolders, Joost ^a,b   Knippenberg, Stephanie ^a,b   Menheere, Paul ^a   Tervaert, Jan Willem Cohen ^a   Hupperts, Raymond ^a,b   Thewissen, Mariëlle ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Zuyderland Medical Centre   (Netherlands)

Author keywords

CD39; Multiple sclerosis; Regulatory T cell; T helper 17 cell; Vitamin D

Indexed keywords

25 HYDROXYVITAMIN D; BETA1A INTERFERON; INTERFERON BETA SERINE; INTERLEUKIN 17; VITAMIN D;

ADULT; ARTICLE; CD39+ REGULATORY T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; HEALTH STATUS; HOMEOSTASIS; HUMAN; HUMAN CELL; LYMPHOCYTE COUNT; LYMPHOCYTE SUBPOPULATION; MALE; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RELAPSE; REMISSION; TH17 CELL; VITAMIN BLOOD LEVEL;

ADULT; ANTIGENS, CD; APYRASE; CELL DIFFERENTIATION; FEMALE; HUMANS; INTERLEUKIN-17; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; VITAMIN D;

EID: 83555178479     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2011.09.013     Document Type: Article

References (29)

1. Alam M.S., Kurtz C.C., Rowlett R.M., Reuter B.K., Wiznerowicz E., Das S., Linden J., Crowe S.E., Ernst P.B. CD73 is expressed by human regulatory T helper cells and suppresses proinflammatory cytokine production and Helicobacter felis-induced gastritis in mice. J. Infect. Dis. 2009, 199:494-504.
2. Ascherio A., Munger K.L., Simon K.C. Vitamin D and multiple sclerosis. Lancet Neurol. 2010, 9:599-612.
3. Borsellino G., Kleinewietfeld M., Di Mitri D., Sternjak A., Diamantini A., Giometto R., Hopner S., Centonze D., Bernardi G., Dell'Acqua M.L., Rossini P.M., Battistini L., Rotzschke O., Falk K. Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 2007, 110:1225-1232.
4. Bours M.J., Swennen E.L., Di Virgilio F., Cronstein B.N., Dagnelie P.C. Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 2006, 112:358-404.
5. Bryl E., Vallejo A.N., Weyand C.M., Goronzy J.J. Down-regulation of CD28 expression by TNF-alpha. J. Immunol. 2001, 167:3231-3238.
6. Chiacchio T., Casetti R., Butera O., Vanini V., Carrara S., Girardi E., Di Mitri D., Battistini L., Martini F., Borsellino G., Goletti D. Characterization of regulatory T cells identified as CD4(+)CD25(high)CD39(+) in patients with active tuberculosis. Clin. Exp. Immunol. 2009, 156:463-470.
7. Compston A., Coles A. Multiple sclerosis. Lancet 2008, 372:1502-1517.
8. Durelli L., Conti L., Clerico M., Boselli D., Contessa G., Ripellino P., Ferrero B., Eid P., Novelli F. T-helper 17 cells expand in multiple sclerosis and are inhibited by interferon-beta. Ann. Neurol. 2009, 65:499-509.
9. Dwyer K.M., Hanidziar D., Putheti P., Hill P.A., Pommey S., McRae J.L., Winterhalter A., Doherty G., Deaglio S., Koulmanda M., Gao W., Robson S.C., Strom T.B. Expression of CD39 by human peripheral blood CD4+ CD25+ T cells denotes a regulatory memory phenotype. Am. J. Transplant. 2010, 10:2410-2420.
10. Fletcher J.M., Lonergan R., Costelloe L., Kinsella K., Moran B., O'Farrelly C., Tubridy N., Mills K.H. CD39+Foxp3+ regulatory T cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J. Immunol. 2009, 183:7602-7610.
11. Haas J., Hug A., Viehover A., Fritzsching B., Falk C.S., Filser A., Vetter T., Milkova L., Korporal M., Fritz B., Storch-Hagenlocher B., Krammer P.H., Suri-Payer E., Wildemann B. Reduced suppressive effect of CD4+CD25 high 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.
12. Hilchey S.P., Kobie J.J., Cochran M.R., Secor-Socha S., Wang J.C., Hyrien O., Burack W.R., Mosmann T.R., Quataert S.A., Bernstein S.H. Human follicular lymphoma CD39+-infiltrating T cells contribute to adenosine-mediated T cell hyporesponsiveness. J. Immunol. 2009, 183:6157-6166.
13. Kebir H., Kreymborg K., Ifergan I., Dodelet-Devillers A., Cayrol R., Bernard M., Giuliani F., Arbour N., Becher B., Prat A. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 2007, 13:1173-1175.
14. Libera D.D., Mitri D.D., Bergami A., Centonze D., Gasperini C., Grasso M.G., Galgani S., Martinelli V., Comi G., Avolio C., Martino G., Borsellino G., Sallusto F., Battistini L., Furlan R. T regulatory cells are markers of disease activity in multiple sclerosis patients. PLoS One 2011, 6:e21386.
15. Liu W., Putnam A.L., Xu-Yu Z., Szot G.L., Lee M.R., Zhu S., Gottlieb P.A., Kapranov P., Gingeras T.R., de St Fazekas, Groth B., Clayberger C., Soper D.M., Ziegler S.F., Bluestone J.A. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 2006, 203:1701-1711.
16. Mandapathil M., Hilldorfer B., Szczepanski M.J., Czystowska M., Szajnik M., Ren J., Lang S., Jackson E.K., Gorelik E., Whiteside T.L. Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells. J. Biol. Chem. 2010, 285:7176-7186.
17. Peelen E., Knippenberg S., Muris A.H., Thewissen M., Smolders J., Tervaert J.W., Hupperts R., Damoiseaux J. Effects of vitamin D on the peripheral adaptive immune system: a review. Autoimmun. Rev. 2011, 10:733-743.
18. Polman C.H., Reingold S.C., Edan G., Filippi M., Hartung H.P., Kappos L., Lublin F.D., Metz L.M., McFarland H.F., O'Connor P.W., Sandberg-Wollheim M., Thompson A.J., Weinshenker B.G., Wolinsky J.S. Diagnostic criteria for multiple sclerosis: 2005 revisions to the " McDonald Criteria". Ann. Neurol. 2005, 58:840-846.
19. Prietl B., Pilz S., Wolf M., Tomaschitz A., Obermayer-Pietsch B., Graninger W., Pieber T.R. Vitamin D supplementation and regulatory T cells in apparently healthy subjects: vitamin D treatment for autoimmune diseases?. Isr. Med. Assoc. J. 2010, 12:136-139.
20. Schulze Zur Wiesch J., Thomssen A., Hartjen P., Toth I., Lehmann C., Meyer-Olson D., Colberg K., Frerk S., Babikir D., Schmiedel S., Degen O., Mauss S., Rockstroh J., Staszewski S., Khaykin P., Strasak A., Lohse A.W., Fatkenheuer G., Hauber J., van Lunzen J. Comprehensive analysis of frequency and phenotype of T regulatory cells in HIV infection: CD39 expression of FoxP3+ T regulatory cells correlates with progressive disease. J. Virol. 2011, 85:1287-1297.
21. Seddiki N., Santner-Nanan B., Martinson J., Zaunders J., Sasson S., Landay A., Solomon M., Selby W., Alexander S.I., Nanan R., Kelleher A., de St Fazekas, Groth B. Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J. Exp. Med. 2006, 203:1693-1700.
22. Smolders J., Peelen E., Thewissen M., Cohen Tervaert J.W., Menheere P., Hupperts R., Damoiseaux J. Safety and T cell modulating effects of high dose vitamin D3 supplementation in multiple sclerosis. PLoS One 2010, 5:e15235.
23. Smolders J., Thewissen M., Peelen E., Menheere P., Tervaert J.W., Damoiseaux J., Hupperts R. Vitamin D status is positively correlated with regulatory T cell function in patients with multiple sclerosis. PLoS One 2009, 4:e6635.
24. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat. Med. 2007, 13:139-145.
25. Venken K., Hellings N., Hensen K., Rummens J.L., Medaer R., D'Hooghe M.B., Dubois B., Raus J., Stinissen P. Secondary progressive in contrast to relapsing-remitting multiple sclerosis patients show a normal CD4+CD25+ regulatory T-cell function and FOXP3 expression. J. Neurosci. Res. 2006, 83:1432-1446.
26. 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.
27. Wilson J.M., Kurtz C.C., Black S.G., Ross W.G., Alam M.S., Linden J., Ernst P.B. The A2B adenosine receptor promotes Th17 differentiation via stimulation of dendritic cell IL-6. J. Immunol. 2011, 186(12):6746-6752.
28. Ye Z.J., Zhou Q., Du R.H., Li X., Huang B., Shi H.Z. The imbalance of Th 17 cells and regulatory T cells in tuberculous pleural effusion. Clin. Vaccine Immunol. 2011, 18:1608-1615.
29. Ye Z.J., Zhou Q., Zhang J.C., Li X., Wu C., Qin S.M., Xin J.B., Shi H.Z. CD39+ regulatory T cells suppress generation and differentiation of Th17 cells in human malignant pleural effusion via a LAP-dependent mechanism. Respir. Res. 2011, 12:77.