Anti-CD4 treatment inhibits autoimmunity in scurfy mice through theattenuation of co-stimulatory signals

Journal of Autoimmunity

Volumn 50, Issue , 2014, Pages 23-32

  Mayer, C T ^a   Tian, L ^b,c   Hesse, C ^a   Kuhl A A ^d   Swallow, M ^a   Kruse, F ^a   Thiele, M ^a   Gershwin, M E ^e   Liston, A ^b,c   Sparwasser, T ^a  

^a INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anti CD4; Autoimmunity; Foxp3; IPEX; Scurfy; YTS177.9

Indexed keywords

CD134 ANTIGEN; CD30 ANTIGEN; CD4 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; LYMPHOCYTE ANTIBODY; TNFRSF4 PROTEIN, MOUSE;

ANIMAL; AUTOIMMUNITY; CELL SURVIVAL; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETIC DISEASES, X-LINKED; GENETICS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; MOUSE; PATHOLOGY; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD30; ANTIGENS, CD4; ANTILYMPHOCYTE SERUM; AUTOIMMUNITY; CELL SURVIVAL; DISEASE MODELS, ANIMAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENETIC DISEASES, X-LINKED; HUMANS; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, TRANSGENIC; RECEPTORS, OX40; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84899111478     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2013.08.010     Document Type: Article

References (47)

1. Klein L., Hinterberger M., Wirnsberger G., Kyewski B. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat Rev Immunol 2009, 9:833-844.
2. Mueller D.L. Mechanisms maintaining peripheral tolerance. Nat Immunol 2010, 11:21-27.
3. Bennett C.L., Christie J., Ramsdell F., Brunkow M.E., Ferguson P.J., Whitesell L., et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001, 27:20-21.
4. Barzaghi F., Passerini L., Bacchetta R. Immune dysregulation, polyendocrinopathy, enteropathy, x-linked syndrome: a paradigm of immunodeficiency with autoimmunity. Front Immunol 2012, 3:211.
5. d'Hennezel E., Bin Dhuban K., Torgerson T., Piccirillo C.A. The immunogenetics of immune dysregulation, polyendocrinopathy, enteropathy, X linked (IPEX) syndrome. JMed Genet 2012, 49:291-302.
6. Buckner J.H. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat Rev Immunol 2010, 10:849-859.
7. Brunkow M.E., Jeffery E.W., Hjerrild K.A., Paeper B., Clark L.B., Yasayko S.A., et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001, 27:68-73.
8. Lahl K., Loddenkemper C., Drouin C., Freyer J., Arnason J., Eberl G., et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. JExp Med 2007, 204:57-63.
9. Klages K., Mayer C.T., Lahl K., Loddenkemper C., Teng M.W., Ngiow S.F., et al. Selective depletion of Foxp3+ regulatory T cells improves effective therapeutic vaccination against established melanoma. Cancer Res 2010, 70:7788-7799.
10. Kim J.M., Rasmussen J.P., Rudensky A.Y. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 2007, 8:191-197.
11. Mayer C.T., Kuhl A.A., Loddenkemper C., Sparwasser T. Lack of Foxp3+ macrophages in both untreated and B16 melanoma-bearing mice. Blood 2012, 119:1314-1315.
12. Liston A., Farr A.G., Chen Z., Benoist C., Mathis D., Manley N.R., et al. Lack of Foxp3 function and expression in the thymic epithelium. JExp Med 2007, 204:475-480.
13. Kim J., Lahl K., Hori S., Loddenkemper C., Chaudhry A., deRoos P., et al. Cutting edge: depletion of Foxp3+ cells leads to induction of autoimmunity by specific ablation of regulatory T cells in genetically targeted mice. JImmunol 2009, 183:7631-7634.
14. Mayer C.T., Floess S., Baru A.M., Lahl K., Huehn J., Sparwasser T. CD8+ Foxp3+ T cells share developmental and phenotypic features with classical CD4+ Foxp3+ regulatory T cells but lack potent suppressive activity. Eur J Immunol 2011, 41:716-725.
15. Watts T.H. TNF/TNFR family members in costimulation of T cell responses. Annu Rev Immunol 2005, 23:23-68.
16. Blair P.J., Bultman S.J., Haas J.C., Rouse B.T., Wilkinson J.E., Godfrey V.L. CD4+CD8- T cells are the effector cells in disease pathogenesis in the scurfy (sf) mouse. JImmunol 1994, 153:3764-3774.
17. Gaspal F.M., Kim M.Y., McConnell F.M., Raykundalia C., Bekiaris V., Lane P.J. Mice deficient in OX40 and CD30 signals lack memory antibody responses because of deficient CD4 T cell memory. JImmunol 2005, 174:3891-3896.
18. Gaspal F., Withers D., Saini M., Bekiaris V., McConnell F.M., White A., et al. Abrogation of CD30 and OX40 signals prevents autoimmune disease in FoxP3-deficient mice. JExp Med 2011, 208:1579-1584.
19. Sugamura K., Ishii N., Weinberg A.D. Therapeutic targeting of the effector T-cell co-stimulatory molecule OX40. Nat Rev Immunol 2004, 4:420-431.
20. Mayer C.T., Berod L., Sparwasser T. Layers of dendritic cell-mediated T cell tolerance, their regulation and the prevention of autoimmunity. Front Immunol 2012, 3:183.
21. Li L., Crowley M., Nguyen A., Lo D. Ability of a nondepleting anti-CD4 antibody to inhibit Th2 responses and allergic lung inflammation is independent of coreceptor function. JImmunol 1999, 163:6557-6566.
22. Qin S.X., Wise M., Cobbold S.P., Leong L., Kong Y.C., Parnes J.R., et al. Induction of tolerance in peripheral T cells with monoclonal antibodies. Eur J Immunol 1990, 20:2737-2745.
23. Liu E., Moriyama H., Paronen J., Abiru N., Miao D., Yu L., et al. Nondepleting anti-CD4 monoclonal antibody prevents diabetes and blocks induction of insulin autoantibodies following insulin peptide B:9-23 immunization in the NOD mouse. JAutoimmun 2003, 21:213-219.
24. Waldmann H., Cobbold S. How do monoclonal antibodies induce tolerance? A role for infectious tolerance?. Annu Rev Immunol 1998, 16:619-644.
25. Becker C., Bopp T., Jonuleit H. Boosting regulatory T cell function by CD4 stimulation enters the clinic. Front Immunol 2012, 3:164.
26. Duarte J., Agua-Doce A., Oliveira V.G., Fonseca J.E., Graca L. Modulation of IL-17 and Foxp3 expression in the prevention of autoimmune arthritis in mice. PLoS One 2010, 5:e10558.
27. Kendal A.R., Chen Y., Regateiro F.S., Ma J., Adams E., Cobbold S.P., et al. Sustained suppression by Foxp3+ regulatory T cells is vital for infectious transplantation tolerance. JExp Med 2011, 208:2043-2053.
28. Junqueira L.C., Bignolas G., Brentani R.R. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochemical J 1979, 11:447-455.
29. Zhang W., Sharma R., Ju S.T., He X.S., Tao Y., Tsuneyama K., et al. Deficiency in regulatory T cells results in development of antimitochondrial antibodies and autoimmune cholangitis. Hepatology 2009, 49:545-552.
30. Lahl K., Mayer C.T., Bopp T., Huehn J., Loddenkemper C., Eberl G., et al. Nonfunctional regulatory T cells and defective control of Th2 cytokine production in natural scurfy mutant mice. JImmunol 2009, 183:5662-5672.
31. Kanangat S., Blair P., Reddy R., Daheshia M., Godfrey V., Rouse B.T., et al. Disease in the scurfy (sf) mouse is associated with overexpression of cytokine genes. Eur J Immunol 1996, 26:161-165.
32. Suscovich T.J., Perdue N.R., Campbell D.J. Type-1 immunity drives early lethality in scurfy mice. Eur J Immunol 2012.
33. Roncarolo M.G., Gregori S., Battaglia M., Bacchetta R., Fleischhauer K., Levings M.K. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006, 212:28-50.
34. Tanaka A., Miyakawa H., Luketic V.A., Kaplan M., Storch W.B., Gershwin M.E. The diagnostic value of anti-mitochondrial antibodies, especially in primary biliary cirrhosis. Cell Mol Biol (Noisy-le-grand) 2002, 48:295-299.
35. Sharma R., Jarjour W.N., Zheng L., Gaskin F., Fu S.M., Ju S.T. Large functional repertoire of regulatory T-cell suppressible autoimmune T cells in scurfy mice. JAutoimmun 2007, 29:10-19.
36. Nishimura H., Nose M., Hiai H., Minato N., Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999, 11:141-151.
37. Freeman G.J., Long A.J., Iwai Y., Bourque K., Chernova T., Nishimura H., et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. JExp Med 2000, 192:1027-1034.
38. Greenwald R.J., Boussiotis V.A., Lorsbach R.B., Abbas A.K., Sharpe A.H. CTLA-4 regulates induction of anergy invivo. Immunity 2001, 14:145-155.
39. Tanaka H., Leung P.S., Kenny T.P., Gershwin M.E., Bowlus C.L. Immunological orchestration of liver fibrosis. Clin Rev Allergy Immunol 2012, 43:220-229.
40. Oliveira V.G., Agua-Doce A., Curotto de Lafaille M.A., Lafaille J.J., Graca L. Adjuvant facilitates tolerance induction to factor VIII in hemophilic mice through a Foxp3-independent mechanism that relies on IL-10. Blood 2013, 121:3936-3945.
41. Waldmann H. Reprogramming the immune system. Clin Transpl 2008, 351-362.
42. Riewaldt J., Duber S., Boernert M., Krey M., Dembinski M., Weiss S., et al. Severe developmental B lymphopoietic defects in foxp3-deficient mice are refractory to adoptive regulatory t cell therapy. Front Immunol 2012, 3:141.
43. Huter E.N., Natarajan K., Torgerson T.R., Glass D.D., Shevach E.M. Autoantibodies in scurfy mice and IPEX patients recognize keratin 14. JInvest Dermatol 2010, 130:1391-1399.
44. Pillai S., Mattoo H., Cariappa A. Bcells and autoimmunity. Curr Opin Immunol 2011, 23:721-731.
45. Hiepe F., Dorner T., Hauser A.E., Hoyer B.F., Mei H., Radbruch A. Long-lived autoreactive plasma cells drive persistent autoimmune inflammation. Nat Rev Rheumatol 2011, 7:170-178.
46. Fehervari Z., Cooke A., Brett S., Turner J. Perturbation of naive TCR transgenic T cell functional responses and upstream activation events by anti-CD4 monoclonal antibodies. Eur J Immunol 2002, 32:333-340.
47. Tanaka S., Maeda S., Hashimoto M., Fujimori C., Ito Y., Teradaira S., et al. Graded attenuation of TCR signaling elicits distinct autoimmune diseases by altering thymic T cell selection and regulatory T cell function. JImmunol 2010, 185:2295-2305.