Sustained Rap1 activation in autoantigen-specific T lymphocytes attenuates experimental autoimmune encephalomyelitis

Journal of Neuroimmunology

Volumn 250, Issue 1-2, 2012, Pages 35-43

  Salinas, Gabriela Franco ^a   Krausz, Sarah ^a   Dontje, Wendy ^a   Evavold, Brian D ^b   Tak, Paul P ^a   Baeten, Dominique L ^a   Reedquist, Kris A ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmunity; Experimental autoimmune encephalitis; Rap1; T lymphocyte; Tolerance

Indexed keywords

AUTOANTIGEN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; RAP1 PROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SURVIVAL; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; AUTOANTIGENS; AUTOIMMUNITY; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME ACTIVATION; FLOW CYTOMETRY; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RAP1 GTP-BINDING PROTEINS; T-LYMPHOCYTES;

EID: 84864862321     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2012.05.012     Document Type: Article

References (50)

1. Abreu J.R., Grabiec A.M., Krausz S., Spijker R., Burakowski T., Maslinski W., Eldering E., Tak P.P., Reedquist K.A. The presumed hyporesponsive behavior of rheumatoid arthritis T lymphocytes can be attributed to spontaneous ex vivo apoptosis rather than defects in T cell receptor signaling. J. Immunol. 2009, 183:621-630.
2. Abreu J.R., Krausz S., Dontje W., Grabiec A.M., de L.D., Nolte M.A., Tak P.P., Reedquist K.A. Sustained T cell Rap1 signaling is protective in the collagen-induced arthritis model of rheumatoid arthritis. Arthritis Rheum. 2010, 62:3289-3299.
3. Amsen D., Kruisbeek A., Bos J.L., Reedquist K. Activation of the Ras-related GTPase Rap1 by thymocyte TCR engagement and during selection. Eur. J. Immunol. 2000, 30:2832-2841.
4. Anderson M.S., Bluestone J.A. The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 2005, 23:447-485.
5. 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, 197:1073-1081.
6. Bevaart L., Vervoordeldonk M.J., Tak P.P. Evaluation of therapeutic targets in animal models of arthritis: how does it relate to rheumatoid arthritis?. Arthritis Rheum. 2010, 62:2192-2205.
7. Bos J.L., de R.J., Reedquist K.A. Rap1 signalling: adhering to new models. Nat. Rev. Mol. Cell Biol. 2001, 2:369-377.
8. Boussiotis V.A., Freeman G.J., Berezovskaya A., Barber D.L., Nadler L.M. Maintenance of human T cell anergy: blocking of IL-2 gene transcription by activated Rap1. Science 1997, 278:124-128.
9. Brand D.D., Kang A.H., Rosloniec E.F. Immunopathogenesis of collagen arthritis. Springer Semin. Immunopathol. 2003, 25:3-18.
10. Burbach B.J., Medeiros R.B., Mueller K.L., Shimizu Y. T-cell receptor signaling to integrins. Immunol. Rev. 2007, 218:65-81.
11. Cantaert T., Brouard S., Thurlings R.M., Pallier A., Salinas G.F., Braud C., Klarenbeek P.L., de V.N., Zhang Y., Soulillou J.P., Tak P.P., Baeten D. Alterations of the synovial T cell repertoire in anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheum. 2009, 60:1944-1956.
12. Cedeno S., Cifarelli D.F., Blasini A.M., Paris M., Placeres F., Alonso G., Rodriguez M.A. Defective activity of ERK-1 and ERK-2 mitogen-activated protein kinases in peripheral blood T lymphocytes from patients with systemic lupus erythematosus: potential role of altered coupling of Ras guanine nucleotide exchange factor hSos to adapter protein Grb2 in lupus T cells. Clin. Immunol. 2003, 106:41-49.
13. Dal Canto R.A., Shaw M.K., Nolan G.P., Steinman L., Fathman C.G. Local delivery of TNF by retrovirus-transduced T lymphocytes exacerbates experimental autoimmune encephalomyelitis. Clin. Immunol. 1999, 90:10-14.
14. Dillon T.J., Carey K.D., Wetzel S.A., Parker D.C., Stork P.J. Regulation of the small GTPase Rap1 and extracellular signal-regulated kinases by the costimulatory molecule CTLA-4. Mol. Cell. Biol. 2005, 25:4117-4128.
15. Ebisuno Y., Katagiri K., Katakai T., Ueda Y., Nemoto T., Inada H., Nabekura J., Okada T., Kannagi R., Tanaka T., Miyasaka M., Hogg N., Kinashi T. Rap1 controls lymphocyte adhesion cascade and interstitial migration within lymph nodes in RAPL-dependent and -independent manners. Blood 2010, 115:804-814.
16. 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, 5:189-197.
17. Ellis C.N., Krueger G.G. Treatment of chronic plaque psoriasis by selective targeting of memory effector T lymphocytes. N. Engl. J. Med. 2001, 345:248-255.
18. Genot E., Cantrell D.A. Ras regulation and function in lymphocytes. Curr. Opin. Immunol. 2000, 12:289-294.
19. Green D.R., Droin N., Pinkoski M. Activation-induced cell death in T cells. Immunol. Rev. 2003, 193:70-81.
20. Gregersen P.K. Gaining insight into PTPN22 and autoimmunity. Nat. Genet. 2005, 37:1300-1302.
21. Ishida D., Yang H., Masuda K., Uesugi K., Kawamoto H., Hattori M., Minato N. Antigen-driven T cell anergy and defective memory T cell response via deregulated Rap1 activation in SPA-1-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10919-10924.
22. 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, 183:7169-7177.
23. Katagiri K., Hattori M., Minato N., Kinashi T. Rap1 functions as a key regulator of T-cell and antigen-presenting cell interactions and modulates T-cell responses. Mol. Cell. Biol. 2002, 22:1001-1015.
24. Katagiri K., Maeda A., Shimonaka M., Kinashi T. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat. Immunol. 2003, 4:741-748.
25. Katagiri K., Ohnishi N., Kabashima K., Iyoda T., Takeda N., Shinkai Y., Inaba K., Kinashi T. Crucial functions of the Rap1 effector molecule RAPL in lymphocyte and dendritic cell trafficking. Nat. Immunol. 2004, 5:1045-1051.
26. Katagiri K., Imamura M., Kinashi T. Spatiotemporal regulation of the kinase Mst1 by binding protein RAPL is critical for lymphocyte polarity and adhesion. Nat. Immunol. 2006, 7:919-928.
27. Kent S.C., Chen Y., Bregoli L., Clemmings S.M., Kenyon N.S., Ricordi C., Hering B.J., Hafler D.A. Expanded T cells from pancreatic lymph nodes of type 1 diabetic subjects recognize an insulin epitope. Nature 2005, 435:224-228.
28. Keymeulen B., Vandemeulebroucke E., Ziegler A.G., Mathieu C., Kaufman L., Hale G., Gorus F., Goldman M., Walter M., Candon S., Schandene L., Crenier L., De B.C., Seigneurin J.M., De P.P., Pierard D., Weets I., Rebello P., Bird P., Berrie E., Frewin M., Waldmann H., Bach J.F., Pipeleers D., Chatenoud L. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N. Engl. J. Med. 2005, 352:2598-2608.
29. Klinkert W.E., Kojima K., Lesslauer W., Rinner W., Lassmann H., Wekerle H. TNF-alpha receptor fusion protein prevents experimental auto-immune encephalomyelitis and demyelination in Lewis rats: an overview. J. Neuroimmunol. 1997, 72:163-168.
30. 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, 349:1907-1915.
31. Kuchroo V.K., Anderson A.C., Waldner H., Munder M., Bettelli E., Nicholson L.B. T cell response in experimental autoimmune encephalomyelitis (EAE): role of self and cross-reactive antigens in shaping, tuning, and regulating the autopathogenic T cell repertoire. Annu. Rev. Immunol. 2002, 20:101-123.
32. Layer K., Lin G., Nencioni A., Hu W., Schmucker A., Antov A.N., Li X., Takamatsu S., Chevassut T., Dower N.A., Stang S.L., Beier D., Buhlmann J., Bronson R.T., Elkon K.B., Stone J.C., Van P.L., Lim B. Autoimmunity as the consequence of a spontaneous mutation in Rasgrp1. Immunity 2003, 19:243-255.
33. Li L., Greenwald R.J., Lafuente E.M., Tzachanis D., Berezovskaya A., Freeman G.J., Sharpe A.H., Boussiotis V.A. Rap1-GTP is a negative regulator of Th cell function and promotes the generation of CD4+CD103+ regulatory T cells in vivo. J. Immunol. 2005, 175:3133-3139.
34. Liu J., Marino M.W., Wong G., Grail D., Dunn A., Bettadapura J., Slavin A.J., Old L., Bernard C.C. TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat. Med. 1998, 4:78-83.
35. Menasche G., Kliche S., Bezman N., Schraven B. Regulation of T-cell antigen receptor-mediated inside-out signaling by cytosolic adapter proteins and Rap1 effector molecules. Immunol. Rev. 2007, 218:82-91.
36. Minato N., Kometani K., Hattori M. Regulation of immune responses and hematopoiesis by the Rap1 signal. Adv. Immunol. 2007, 93:229-264.
37. Mueller K.L., Thomas M.S., Burbach B.J., Peterson E.J., Shimizu Y. Adhesion and degranulation-promoting adapter protein (ADAP) positively regulates T cell sensitivity to antigen and T cell survival. J. Immunol. 2007, 179:3559-3569.
38. Priatel J.J., Teh S.J., Dower N.A., Stone J.C., Teh H.S. RasGRP1 transduces low-grade TCR signals which are critical for T cell development, homeostasis, and differentiation. Immunity 2002, 17:617-627.
39. Priatel J.J., Chen X., Dhanji S., Abraham N., Teh H.S. RasGRP1 transmits prodifferentiation TCR signaling that is crucial for CD4 T cell development. J. Immunol. 2006, 177:1470-1480.
40. Priatel J.J., Chen X., Zenewicz L.A., Shen H., Harder K.W., Horwitz M.S., Teh H.S. Chronic immunodeficiency in mice lacking RasGRP1 results in CD4 T cell immune activation and exhaustion. J. Immunol. 2007, 179:2143-2152.
41. Raab M., Wang H., Lu Y., Smith X., Wu Z., Strebhardt K., Ladbury J.E., Rudd C.E. T cell receptor "inside-out" pathway via signaling module SKAP1-RapL regulates T cell motility and interactions in lymph nodes. Immunity 2010, 32:541-556.
42. Remans P.H., Gringhuis S.I., van Laar J.M., Sanders M.E., Papendrecht-van der Voort E.A., Zwartkruis F.J., Levarht E.W., Rosas M., Coffer P.J., Breedveld F.C., Bos J.L., Tak P.P., Verweij C.L., Reedquist K.A. Rap1 signaling is required for suppression of Ras-generated reactive oxygen species and protection against oxidative stress in T lymphocytes. J. Immunol. 2004, 173:920-931.
43. Remans P.H., Wijbrandts C.A., Sanders M.E., Toes R.E., Breedveld F.C., Tak P.P., van Laar J.M., Reedquist K.A. CTLA-4IG suppresses reactive oxygen species by preventing synovial adherent cell-induced inactivation of Rap1, a Ras family GTPASE mediator of oxidative stress in rheumatoid arthritis T cells. Arthritis Rheum. 2006, 54:3135-3143.
44. 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, 172:1193-1200.
45. Sabatino J.J., Shires J., Altman J.D., Ford M.L., Evavold B.D. Loss of IFN-gamma enables the expansion of autoreactive CD4+ T cells to induce experimental autoimmune encephalomyelitis by a nonencephalitogenic myelin variant antigen. J. Immunol. 2008, 180:4451-4457.
46. Sabatino J.J., Huang J., Zhu C., Evavold B.D. High prevalence of low affinity peptide-MHC II tetramer-negative effectors during polyclonal CD4+ T cell responses. J. Exp. Med. 2011, 208:81-90.
47. Sebzda E., Bracke M., Tugal T., Hogg N., Cantrell D.A. Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling. Nat. Immunol. 2002, 3:251-258.
48. Sinclair L.V., Finlay D., Feijoo C., Cornish G.H., Gray A., Ager A., Okkenhaug K., Hagenbeek T.J., Spits H., Cantrell D.A. Phosphatidylinositol-3-OH kinase and nutrient-sensing mTOR pathways control T lymphocyte trafficking. Nat. Immunol. 2008, 9:513-521.
49. Wherry E.J. T cell exhaustion. Nat. Immunol. 2011, 12:492-499.
50. Yasuda S., Stevens R.L., Terada T., Takeda M., Hashimoto T., Fukae J., Horita T., Kataoka H., Atsumi T., Koike T. Defective expression of Ras guanyl nucleotide-releasing protein 1 in a subset of patients with systemic lupus erythematosus. J. Immunol. 2007, 179:4890-4900.