Enhanced costimulation by CD70+ B cells aggravates experimental autoimmune encephalomyelitis in autoimmune mice

Journal of Neuroimmunology

Volumn 255, Issue 1-2, 2013, Pages 8-17

  FrancoSalinas, G ^a   Cantaert, T ^a,b   Nolte, M A ^c   Tak, P P ^a,d   van Lier, R A W ^c   Baeten, D L ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SANQUIN RESEARCH   (Netherlands)

^d GLAXOSMITHKLINE   (United Kingdom)

Author keywords

B lymphocyte; CD70; Costimulation; Experimental autoimmune encephalomyelitis; Regulatory T cell; T lymphocyte

Indexed keywords

CD70 ANTIGEN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DISEASE EXACERBATION; DISEASE SEVERITY; GENE OVEREXPRESSION; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD70; B-LYMPHOCYTE SUBSETS; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; IMMUNOPHENOTYPING; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; T-LYMPHOCYTES, REGULATORY;

EID: 84872654537     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2012.10.010     Document Type: Article

References (77)

1. Ait-Oufella H., Herbin O., Bouaziz J.D., Binder C.J., Uyttenhove C., Laurans L., Taleb S., Van V.E., Esposito B., Vilar J., Sirvent J., Van S.J., Tedgui A., Tedder T.F., Mallat Z. B cell depletion reduces the development of atherosclerosis in mice. J. Exp. Med. 2010, 207(8):1579-1587. (available from: PM:20603314).
2. Aramaki O., Shirasugi N., Akiyama Y., Takayama T., Shimazu M., Kitajima M., Ikeda Y., Niimi M. Induction of operational tolerance and generation of regulatory cells after intratracheal delivery of alloantigen combined with nondepleting anti-CD4 monoclonal antibody. Transplantation 2003, 76(9):1305-1314. (available from: PM:14627908).
3. Arbuckle M.R., McClain M.T., Rubertone M.V., Scofield R.H., Dennis G.J., James J.A., Harley J.B. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 2003, 349(16):1526-1533. (available from: PM:14561795).
4. Arechiga A.F., Habib T., He Y., Zhang X., Zhang Z.Y., Funk A., Buckner J.H. Cutting edge: the PTPN22 allelic variant associated with autoimmunity impairs B cell signaling. J. Immunol. 2009, 182(6):3343-3347. (available from: PM:19265110).
5. Arens R., Tesselaar K., Baars P.A., van Schijndel G.M., Hendriks J., Pals S.T., Krimpenfort P., Borst J., van Oers M.H., van Lier R.A. Constitutive CD27/CD70 interaction induces expansion of effector-type T cells and results in IFNgamma-mediated B cell depletion. Immunity 2001, 15(5):801-812. (available from: PM:11728341).
6. Arens R., Nolte M.A., Tesselaar K., Heemskerk B., Reedquist K.A., van Lier R.A., van Oers M.H. Signaling through CD70 regulates B cell activation and IgG production. J. Immunol. 2004, 173(6):3901-3908. (available from: PM:15356138).
7. Arens R., Schepers K., Nolte M.A., van Oosterwijk M.F., van Lier R.A., Schumacher T.N., van Oers M.H. Tumor rejection induced by CD70-mediated quantitative and qualitative effects on effector CD8+ T cell formation. J. Exp. Med. 2004, 199(11):1595-1605. (available from: PM:15184507).
8. Bettelli E., Pagany M., Weiner H.L., Linington C., Sobel R.A., Kuchroo V.K. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 2003, 197(9):1073-1081. (available from: PM:12732654).
9. Bettelli E., Baeten D., Jager A., Sobel R.A., Kuchroo V.K. Myelin oligodendrocyte glycoprotein-specific T and B cells cooperate to induce a Devic-like disease in mice. J. Clin. Invest. 2006, 116(9):2393-2402. (available from: PM:16955141).
10. Brand D.D., Kang A.H., Rosloniec E.F. Immunopathogenesis of collagen arthritis. Springer Semin. Immunopathol. 2003, 25(1):3-18. (available from: PM:12904888).
11. Camous L., Melander C., Vallet M., Squalli T., Knebelmann B., Noel L.H., Fakhouri F. Complete remission of lupus nephritis with rituximab and steroids for induction and rituximab alone for maintenance therapy. Am. J. Kidney Dis. 2008, 52(2):346-352. (available from: PM:18572292).
12. Carreno B.M., Collins M. The B7 family of ligands and its receptors: new pathways for costimulation and inhibition of immune responses. Annu. Rev. Immunol. 2002, 20:29-53. (available from: PM:11861596).
13. Carter N.A., Rosser E.C., Mauri C. IL-10 produced by B cells is crucial for the suppression of Th17/ Th1 responses, induction of Tr1 cells and reduction of collagen-induced arthritis. Arthritis Res. Ther. 2012, 14(1):R32. (available from: PM:22315945).
14. Cho Y.G., Cho M.L., Min S.Y., Kim H.Y. Type II collagen autoimmunity in a mouse model of human rheumatoid arthritis. Autoimmun. Rev. 2007, 7(1):65-70. (available from: PM:17967728).
15. Denoeud J., Moser M. Role of CD27/CD70 pathway of activation in immunity and tolerance. J. Leukoc. Biol. 2011, 89(2):195-203. (available from: PM:20699361).
16. Dorner T., Kinnman N., Tak P.P. Targeting B cells in immune-mediated inflammatory disease: a comprehensive review of mechanisms of action and identification of biomarkers. Pharmacol. Ther. 2010, 125(3):464-475. (available from: PM:20097226).
17. Edwards J.C., Szczepanski L., Szechinski J., Filipowicz-Sosnowska A., Emery P., Close D.R., Stevens R.M., Shaw T. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 2004, 350(25):2572-2581. (available from: PM:15201414).
18. El-behi M., Rostami A., Ciric B. Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. J. Neuroimmune Pharmacol. 2010, 5(2):189-197. (available from: PM:20107924).
19. Elgueta R., Benson M.J., de Vries V.C., Wasiuk A., Guo Y., Noelle R.J. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol. Rev. 2009, 229(1):152-172. (available from: PM:19426221).
20. Franciotta D., Salvetti M., Lolli F., Serafini B., Aloisi F. B cells and multiple sclerosis. Lancet Neurol. 2008, 7(9):852-858. (available from: PM:18703007).
21. Franssila R., Hedman K. Infection and musculoskeletal conditions: viral causes of arthritis. Best Pract. Res. Clin. Rheumatol. 2006, 20(6):1139-1157. (available from: PM:17127201).
22. Gausas J., Paterson P.Y., Day E.D., Dal Canto M.C. Intact B-cell activity is essential for complete expression of experimental allergic encephalomyelitis in Lewis rats. Cell. Immunol. 1982, 72(2):360-366. (available from: PM:6185236).
23. Genain C.P., Nguyen M.H., Letvin N.L., Pearl R., Davis R.L., Adelman M., Lees M.B., Linington C., Hauser S.L. Antibody facilitation of multiple sclerosis-like lesions in a nonhuman primate. J. Clin. Invest. 1995, 96(6):2966-2974. (available from: PM:8675668).
24. Grewal I.S., Flavell R.A. The role of CD40 ligand in costimulation and T-cell activation. Immunol. Rev. 1996, 153:85-106. (available from: PM:9010720).
25. Gunnarsson I., Sundelin B., Jonsdottir T., Jacobson S.H., Henriksson E.W., van Vollenhoven R.F. Histopathologic and clinical outcome of rituximab treatment in patients with cyclophosphamide-resistant proliferative lupus nephritis. Arthritis Rheum. 2007, 56(4):1263-1272. (available from: PM:17393458).
26. Habib T., Funk A., Rieck M., Brahmandam A., Dai X., Panigrahi A.K., Luning Prak E.T., Meyer-Bahlburg A., Sanda S., Greenbaum C., Rawlings D.J., Buckner J.H. Altered B cell homeostasis is associated with type I diabetes and carriers of the PTPN22 allelic variant. J. Immunol. 2012, 188(1):487-496. (available from: PM:22105996).
27. Harlan D.M., Hengartner H., Huang M.L., Kang Y.H., Abe R., Moreadith R.W., Pircher H., Gray G.S., Ohashi P.S., Freeman G.J. Mice expressing both B7-1 and viral glycoprotein on pancreatic beta cells along with glycoprotein-specific transgenic T cells develop diabetes due to a breakdown of T-lymphocyte unresponsiveness. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(8):3137-3141. (available from: PM:7512724).
28. Harley J.B., Alarcon-Riquelme M.E., Criswell L.A., Jacob C.O., Kimberly R.P., Moser K.L., Tsao B.P., Vyse T.J., Langefeld C.D., Nath S.K., Guthridge J.M., Cobb B.L., Mirel D.B., Marion M.C., Williams A.H., Divers J., Wang W., Frank S.G., Namjou B., Gabriel S.B., Lee A.T., Gregersen P.K., Behrens T.W., Taylor K.E., Fernando M., Zidovetzki R., Gaffney P.M., Edberg J.C., Rioux J.D., Ojwang J.O., James J.A., Merrill J.T., Gilkeson G.S., Seldin M.F., Yin H., Baechler E.C., Li Q.Z., Wakeland E.K., Bruner G.R., Kaufman K.M., Kelly J.A. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat. Genet. 2008, 40(2):204-210. (available from: PM:18204446).
29. Hauser S.L., Waubant E., Arnold D.L., Vollmer T., Antel J., Fox R.J., Bar-Or A., Panzara M., Sarkar N., Agarwal S., Langer-Gould A., Smith C.H. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. 2008, 358(7):676-688. (available from: PM:18272891).
30. Hendriks J., Xiao Y., Borst J. CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T cell pool. J. Exp. Med. 2003, 198(9):1369-1380. (available from: PM:14581610).
31. Jager A., Dardalhon V., Sobel R.A., Bettelli E., Kuchroo V.K. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 2009, 183(11):7169-7177. (available from: PM:19890056).
32. Jak M., Mous R., Remmerswaal E.B., Spijker R., Jaspers A., Yague A., Eldering E., van Lier R.A., van Oers M.H. Enhanced formation and survival of CD4+ CD25hi Foxp3+ T-cells in chronic lymphocytic leukemia. Leuk. Lymphoma 2009, 50(5):788-801. (available from: PM:19452318).
33. Kozyrev S.V., Abelson A.K., Wojcik J., Zaghlool A., Linga Reddy M.V., Sanchez E., Gunnarsson I., Svenungsson E., Sturfelt G., Jonsen A., Truedsson L., Pons-Estel B.A., Witte T., D'Alfonso S., Barizzone N., Danieli M.G., Gutierrez C., Suarez A., Junker P., Laustrup H., Gonzalez-Escribano M.F., Martin J., Abderrahim H., Alarcon-Riquelme M.E. Functional variants in the B-cell gene BANK1 are associated with systemic lupus erythematosus. Nat. Genet. 2008, 40(2):211-216. (available from: PM:18204447).
34. Kremer J.M., Westhovens R., Leon M., Di G.E., Alten R., Steinfeld S., Russell A., Dougados M., Emery P., Nuamah I.F., Williams G.R., Becker J.C., Hagerty D.T., Moreland L.W. Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N. Engl. J. Med. 2003, 349(20):1907-1915. (available from: PM:14614165).
35. Krishnamoorthy G., Lassmann H., Wekerle H., Holz A. Spontaneous opticospinal encephalomyelitis in a double-transgenic mouse model of autoimmune T cell/B cell cooperation. J. Clin. Invest. 2006, 116(9):2385-2392. (available from: PM:16955140).
36. LaGasse J.M., Brantley M.S., Leech N.J., Rowe R.E., Monks S., Palmer J.P., Nepom G.T., McCulloch D.K., Hagopian W.A. Successful prospective prediction of type 1 diabetes in schoolchildren through multiple defined autoantibodies: an 8-year follow-up of the Washington State Diabetes Prediction Study. Diabetes Care 2002, 25(3):505-511. (available from: PM:11874938).
37. Lee W.W., Yang Z.Z., Li G., Weyand C.M., Goronzy J.J. Unchecked CD70 expression on T cells lowers threshold for T cell activation in rheumatoid arthritis. J. Immunol. 2007, 179(4):2609-2615. (available from: PM:17675524).
38. Libregts S., van Olffen R.W., van der Sluijs K.F., van Lier R.A., Nolte M.A. Function of CD27 in helper T cell differentiation. Immunol. Lett. 2011, 136(2):177-186. (available from: PM:21277898).
39. Linington C., Bradl M., Lassmann H., Brunner C., Vass K. Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin/oligodendrocyte glycoprotein. Am. J. Pathol. 1988, 130(3):443-454. (available from: PM:2450462).
40. Litzenburger T., Fassler R., Bauer J., Lassmann H., Linington C., Wekerle H., Iglesias A. B lymphocytes producing demyelinating autoantibodies: development and function in gene-targeted transgenic mice. J. Exp. Med. 1998, 188(1):169-180. (available from: PM:9653093).
41. Looney R.J., Anolik J.H., Campbell D., Felgar R.E., Young F., Arend L.J., Sloand J.A., Rosenblatt J., Sanz I. B cell depletion as a novel treatment for systemic lupus erythematosus: a phase I/II dose-escalation trial of rituximab. Arthritis Rheum. 2004, 50(8):2580-2589. (available from: PM:15334472).
42. Lyons J.A., San M., Happ M.P., Cross A.H. B cells are critical to induction of experimental allergic encephalomyelitis by protein but not by a short encephalitogenic peptide. Eur. J. Immunol. 1999, 29(11):3432-3439. (available from: PM:10556797).
43. Manocha M., Rietdijk S., Laouar A., Liao G., Bhan A., Borst J., Terhorst C., Manjunath N. Blocking CD27-CD70 costimulatory pathway suppresses experimental colitis. J. Immunol. 2009, 183(1):270-276. (available from: PM:19525396).
44. Menard L., Saadoun D., Isnardi I., Ng Y.S., Meyers G., Massad C., Price C., Abraham C., Motaghedi R., Buckner J.H., Gregersen P.K., Meffre E. The PTPN22 allele encoding an R620W variant interferes with the removal of developing autoreactive B cells in humans. J. Clin. Invest. 2011, 121(9):3635-3644. (available from: PM:21804190).
45. Murata K., Nose M., Ndhlovu L.C., Sato T., Sugamura K., Ishii N. Constitutive OX40/OX40 ligand interaction induces autoimmune-like diseases. J. Immunol. 2002, 169(8):4628-4636. (available from: PM:12370402).
46. Nakajima A., Oshima H., Nohara C., Morimoto S., Yoshino S., Kobata T., Yagita H., Okumura K. Involvement of CD70-CD27 interactions in the induction of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2000, 109(2):188-196. (available from: PM:10996221).
47. Nielen M.M., van S.D., Reesink H.W., van de Stadt R.J., van der Horst-Bruinsma I.E., de Koning M.H., Habibuw M.R., Vandenbroucke J.P., Dijkmans B.A. Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum. 2004, 50(2):380-386. (available from: PM:14872479).
48. Nolte M.A., van Olffen R.W., van Gisbergen K.P., van Lier R.A. Timing and tuning of CD27-CD70 interactions: the impact of signal strength in setting the balance between adaptive responses and immunopathology. Immunol. Rev. 2009, 229(1):216-231. (available from: PM:19426224).
49. Nurieva R.I., Liu X., Dong C. Yin-Yang of costimulation: crucial controls of immune tolerance and function. Immunol. Rev. 2009, 229(1):88-100. (available from: PM:19426216).
50. Oelke K., Lu Q., Richardson D., Wu A., Deng C., Hanash S., Richardson B. Overexpression of CD70 and overstimulation of IgG synthesis by lupus T cells and T cells treated with DNA methylation inhibitors. Arthritis Rheum. 2004, 50(6):1850-1860. (available from: PM:15188362).
51. Pender M.P. Preventing and curing multiple sclerosis by controlling Epstein-Barr virus infection. Autoimmun. Rev. 2009, 8(7):563-568. (available from: PM:19254880).
52. Pender M.P. The essential role of Epstein-Barr virus in the pathogenesis of multiple sclerosis. Neuroscientist 2011, 17(4):351-367. (available from: PM:21075971).
53. Pescovitz M.D., Greenbaum C.J., Krause-Steinrauf H., Becker D.J., Gitelman S.E., Goland R., Gottlieb P.A., Marks J.B., McGee P.F., Moran A.M., Raskin P., Rodriguez H., Schatz D.A., Wherrett D., Wilson D.M., Lachin J.M., Skyler J.S. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med. 2009, 361(22):2143-2152. (available from: PM:19940299).
54. Poirier N., Azimzadeh A.M., Zhang T., Dilek N., Mary C., Nguyen B., Tillou X., Wu G., Reneaudin K., Hervouet J., Martinet B., Coulon F., Allain-Launay E., Karam G., Soulillou J.P., Pierson R.N., Blancho G., Vanhove B. Inducing CTLA-4-dependent immune regulation by selective CD28 blockade promotes regulatory T cells in organ transplantation. Sci. Transl. Med. 2010, 2(17):17ra10. (available from: PM:20371478).
55. Ruddle N.H., Bergman C.M., McGrath K.M., Lingenheld E.G., Grunnet M.L., Padula S.J., Clark R.B. An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J. Exp. Med. 1990, 172(4):1193-1200. (available from: PM:2212948).
56. Salomon B., Lenschow D.J., Rhee L., Ashourian N., Singh B., Sharpe A., Bluestone J.A. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 2000, 12(4):431-440. (available from: PM:10795741).
57. Salomon B., Rhee L., Bour-Jordan H., Hsin H., Montag A., Soliven B., Arcella J., Girvin A.M., Padilla J., Miller S.D., Bluestone J.A. Development of spontaneous autoimmune peripheral polyneuropathy in B7-2-deficient NOD mice. J. Exp. Med. 2001, 194(5):677-684. (available from: PM:11535635).
58. Sawada S., Takei M., Inomata H., Nozaki T., Shiraiwa H. What is after cytokine-blocking therapy, a novel therapeutic target--synovial Epstein-Barr virus for rheumatoid arthritis. Autoimmun. Rev. 2007, 6(3):126-130. (available from: PM:17289546).
59. Schluesener H.J., Sobel R.A., Linington C., Weiner H.L. A monoclonal antibody against a myelin oligodendrocyte glycoprotein induces relapses and demyelination in central nervous system autoimmune disease. J. Immunol. 1987, 139(12):4016-4021. (available from: PM:3500978).
60. Shilling R.A., Bandukwala H.S., Sperling A.I. Regulation of T:B cell interactions by the inducible costimulator molecule: does ICOS "induce" disease?. Clin. Immunol. 2006, 121(1):13-18. (available from: PM:16790364).
61. Simpson T.R., Quezada S.A., Allison J.P. Regulation of CD4 T cell activation and effector function by inducible costimulator (ICOS). Curr. Opin. Immunol. 2010, 22(3):326-332. (available from: PM:20116985).
62. Slavik J.M., Hutchcroft J.E., Bierer B.E. CD28/CTLA-4 and CD80/CD86 families: signaling and function. Immunol. Res. 1999, 19(1):1-24. (available from: PM:10374692).
63. Tak P.P., Hintzen R.Q., Teunissen J.J., Smeets T.J., Daha M.R., van Lier R.A., Kluin P.M., Meinders A.E., Swaak A.J., Breedveld F.C. Expression of the activation antigen CD27 in rheumatoid arthritis. Clin. Immunol. Immunopathol. 1996, 80(2):129-138. (available from: PM:8764557).
64. Tang Q., Henriksen K.J., Boden E.K., Tooley A.J., Ye J., Subudhi S.K., Zheng X.X., Strom T.B., Bluestone J.A. Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells. J. Immunol. 2003, 171(7):3348-3352. (available from: PM:14500627).
65. Tesselaar K., Arens R., van Schijndel G.M., Baars P.A., van der Valk M.A., Borst J., van Oers M.H., van Lier R.A. Lethal T cell immunodeficiency induced by chronic costimulation via CD27-CD70 interactions. Nat. Immunol. 2003, 4(1):49-54. (available from: PM:12469117).
66. Toussirot E., Roudier J. Pathophysiological links between rheumatoid arthritis and the Epstein-Barr virus: an update. Joint Bone Spine 2007, 74(5):418-426. (available from: PM:17625943).
67. Townsend M.J., Monroe J.G., Chan A.C. B-cell targeted therapies in human autoimmune diseases: an updated perspective. Immunol. Rev. 2010, 237(1):264-283. (available from: PM:20727041).
68. van Gisbergen K.P., Klarenbeek P.L., Kragten N.A., Unger P.P., Nieuwenhuis M.B., Wensveen F.M., ten B.A., Tak P.P., Eldering E., Nolte M.A., van Lier R.A. The costimulatory molecule CD27 maintains clonally diverse CD8(+) T cell responses of low antigen affinity to protect against viral variants. Immunity 2011, 35(1):97-108. (available from: PM:21763160).
69. van Olffen R.W., Koning N., van Gisbergen K.P., Wensveen F.M., Hoek R.M., Boon L., Hamann J., van Lier R.A., Nolte M.A. GITR triggering induces expansion of both effector and regulatory CD4+ T cells in vivo. J. Immunol. 2009, 182(12):7490-7500. (available from: PM:19494272).
70. van Vollenhoven R.F., Gunnarsson I., Welin-Henriksson E., Sundelin B., Osterborg A., Jacobson S.H., Klareskog L. Biopsy-verified response of severe lupus nephritis to treatment with rituximab (anti-CD20 monoclonal antibody) plus cyclophosphamide after biopsy-documented failure to respond to cyclophosphamide alone. Scand. J. Rheumatol. 2004, 33(6):423-427. (available from: PM:15794203).
71. Wang J., Lo J.C., Foster A., Yu P., Chen H.M., Wang Y., Tamada K., Chen L., Fu Y.X. The regulation of T cell homeostasis and autoimmunity by T cell-derived LIGHT. J. Clin. Invest. 2001, 108(12):1771-1780. (available from: PM:11748260).
72. Watts T.H. TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 2005, 23:23-68. (available from: PM:15771565).
73. Wolthers K.C., Otto S.A., Lens S.M., Kolbach D.N., van Lier R.A., Miedema F., Meyaard L. Increased expression of CD80, CD86 and CD70 on T cells from HIV-infected individuals upon activation in vitro: regulation by CD4+ T cells. Eur. J. Immunol. 1996, 26(8):1700-1706. (available from: PM:8765009).
74. Xiao X., Kroemer A., Gao W., Ishii N., Demirci G., Li X.C. OX40/OX40L costimulation affects induction of Foxp3+ regulatory T cells in part by expanding memory T cells in vivo. J. Immunol. 2008, 181(5):3193-3201. (available from: PM:18713990).
75. Yanagisawa S., Takeichi N., Kaneyama T., Yagita H., Taniguchi S., Kim B.S., Koh C.S. Effects of anti-CD70 mAb on Theiler's murine encephalomyelitis virus-induced demyelinating disease. Brain Res. 2010, 1317:236-245. (available from: PM:20045400).
76. Yang Z.Z., Novak A.J., Ziesmer S.C., Witzig T.E., Ansell S.M. CD70+ non-Hodgkin lymphoma B cells induce Foxp3 expression and regulatory function in intratumoral CD4+CD25 T cells. Blood 2007, 110(7):2537-2544. (available from: PM:17615291).
77. Yurasov S., Wardemann H., Hammersen J., Tsuiji M., Meffre E., Pascual V., Nussenzweig M.C. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 2005, 201(5):703-711. (available from: PM:15738055).