ICOS regulates the generation and function of human CD4+ Treg in a CTLA-4 dependent manner

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Zheng, Jian ^a   Chan, Ping Lung ^a   Liu, Yinping ^a   Qin, Gang ^a   Xiang, Zheng ^a   Lam, Kwok Tai ^a   Lewis, David B ^b   Lau, Yu Lung ^a   Tu, Wenwei ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CELL PROTEIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOGLOBULIN; LIGAND; PEPSTATIN; PROTEIN E64; PROTEIN ICOS; REGULATOR PROTEIN; UNCLASSIFIED DRUG; HYBRID PROTEIN; ICOSLG PROTEIN, HUMAN; INDUCIBLE T CELL COSTIMULATOR; INDUCIBLE T CELL COSTIMULATOR LIGAND;

ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL DAMAGE; CELL EXPANSION; CELL SURFACE; CONTROLLED STUDY; EXOCYTOSIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; 3T3 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL PROLIFERATION; DRUG EFFECTS; FLOW CYTOMETRY; GENETICS; METABOLISM; MOUSE; REGULATORY T LYMPHOCYTE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; CTLA-4 ANTIGEN; FLOW CYTOMETRY; HUMANS; INDUCIBLE T-CELL CO-STIMULATOR LIGAND; INDUCIBLE T-CELL CO-STIMULATOR PROTEIN; MICE; NIH 3T3 CELLS; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES, REGULATORY;

EID: 84891607732     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082203     Document Type: Article

References (50)

1. Beier KC, Hutloff A, Dittrich AM, Heuck C, Rauch A et al. (2000) Induction, binding specificity and function of human ICOS. Eur J Immunol 30: 3707-3717. doi:10.1002/1521-4141(200012)30:12. PubMed: 11169414.
2. Linterman MA, Rigby RJ, Wong R, Silva D, Withers D et al. (2009) Roquin Differentiates the Specialized Functions of Duplicated T Cell Costimulatory Receptor Genes Cd28 and Icos. Immunity 30: 228-241. doi:10.1016/j.immuni.2008. 12.015. PubMed: 19217324.
3. Watanabe M, Hara Y, Tanabe K, Toma H, Abe R (2005) A distinct role for ICOS-mediated co-stimulatory signaling in CD4+ and CD8+ T cell subsets. Int Immunol 17: 269-278. doi:10.1093/intimm/dxh206. PubMed: 15668466.
4. Bertram EM, Tafuri A, Shahinian A, Chan VS, Hunziker L et al. (2002) Role of ICOS versus CD28 in antiviral immunity. Eur J Immunol 32: 3376-3385. doi:10.1002/1521-4141(200212)32:12. PubMed: 12432568.
5. Currie AJ, Prosser A, McDonnell A, Cleaver AL, Robinson BW et al. (2009) Dual Control of Antitumor CD8 T Cells through the Programmed Death-1/Programmed Death-Ligand 1 Pathway and Immunosuppressive CD4 T Cells: Regulation and Counterregulation. J Immunol 183: 7898-7908. doi:10.4049/jimmunol.0901060. PubMed: 20007574.
6. Harada H, Salama AD, Sho M, Izawa A, Sandner SE et al. (2003) The role of the ICOS-B7h T cell costimulatory pathway in transplantation immunity. J Clin Invest 112: 234-243. doi:10.1172/JCI200317008. PubMed: 12865411.
7. Taylor PA, Panoskaltsis-Mortari A, Freeman GJ, Sharpe AH, Noelle RJ et al. (2005) Targeting of inducible costimulator (ICOS) expressed on alloreactive T cells down-regulates graft-versus-host disease (GVHD) and facilitates engraftment of allogeneic bone marrow (BM). Blood 105: 3372-3380. doi:10.1182/blood-2004-10-3869. PubMed: 15618467.
8. Maeda S, Fujimoto M, Matsushita T, Hamaguchi Y, Takehara K et al. (2011) Inducible costimulator (ICOS) and ICOS ligand signaling has pivotal roles in skin wound healing via cytokine production. Am J Pathol 179: 2360-2369. doi:10.1016/j.ajpath.2011.07.048. PubMed: 21925472.
9. Hodgson R, Christiansen D, Ziolkowski A, Mouhtouris E, Simeonovic CJ et al. (2011) Prolonged xenograft survival induced by inducible costimulator-Ig is associated with increased forkhead box p3+ cells. Transplantation 91: 1090-1097. doi:10.1097/TP.0b013e31821774e0. PubMed: 21544030.
10. Dong C, Juedes AE, Temann UA, Shresta S, Allison JP et al. (2001) ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 409: 97-101. doi:10.1038/35051100. PubMed: 11343121.
11. Moore TV, Clay BS, Cannon JL, Histed A, Shilling RA et al. (2011) Inducible costimulator controls migration of T cells to the lungs via down-regulation of CCR7 and CD62L. Am J Respir Cell Mol Biol 45: 843-850. doi:10.1165/rcmb.2010-0466OC. PubMed: 21421907.
12. Clay BS, Shilling RA, Bandukwala HS, Moore TV, Cannon JL et al. (2009) Inducible costimulator expression regulates the magnitude of Th2-mediated airway inflammation by regulating the number of Th2 cells. PLOS ONE 4: e7525. doi:10.1371/journal.pone.0007525. PubMed: 19888475.
13. McAdam AJ, Chang TT, Lumelsky AE, Greenfield EA, Boussiotis VA et al. (2000) Mouse inducible costimulatory molecule (ICOS) expression is enhanced by CD28 costimulation and regulates differentiation of CD4+ T cells. J Immunol 165: 5035-5040. PubMed: 11046032.
14. Bauquet AT, Jin H, Paterson AM, Mitsdoerffer M, Ho IC et al. (2009) The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat Immunol 10: 167-175. doi:10.1038/ni.1690. PubMed: 19098919.
15. Galicia G, Kasran A, Uyttenhove C, De Swert K, Van Snick J et al. (2009) ICOS Deficiency Results in Exacerbated IL-17 Mediated Experimental Autoimmune Encephalomyelitis. J Clin Immunol 29: 426-433. doi:10.1007/s10875-009-9287-7. PubMed: 19291374.
16. Smith KM, Brewer JM, Webb P, Coyle AJ, Gutierrez-Ramos C et al. (2003) Inducible costimulatory molecule-B7-related protein 1 interactions are important for the clonal expansion and B cell helper functions of naive, Th1, and Th2 T cells. J Immunol 170: 2310-2315. PubMed: 12594252.
17. Yong PF, Salzer U, Grimbacher B (2009) The role of costimulation in antibody deficiencies: ICOS and common variable immunodeficiency. Immunol Rev 229: 101-113. doi:10.1111/j.1600-065X.2009.00764.x. PubMed: 19426217.
18. Grinberg-Bleyer Y, Baeyens A, You S, Elhage R, Fourcade G et al. (2010) IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatory T cells. J Exp Med 207: 1871-1878. doi:10.1084/jem. 20100209. PubMed: 20679400.
19. Gomez de Agüero M, Vocanson M, Hacini-Rachinel F, Taillardet M, Sparwasser T et al. (2012) Langerhans cells protect from allergic contact dermatitis in mice by tolerizing CD8+ T cells and activating Foxp3+ regulatory T cells. J Clin Invest 122: 1700-1711. doi:10.1172/JCI59725. PubMed: 22523067.
20. Lischke T, Hegemann A, Gurka S, Vu Van D, Burmeister Y et al. (2012) Comprehensive Analysis of CD4+ T Cells in the Decision between Tolerance and Immunity In Vivo Reveals a Pivotal Role for ICOS. J Immunol 189: 234-244. doi:10.4049/jimmunol.1102034. PubMed: 22661090.
21. Chen Y, Shen S, Gorentla BK, Gao J, Zhong XP (2012) Murine Regulatory T Cells Contain Hyperproliferative and Death-Prone Subsets with Differential ICOS Expression. Journal of Immunology 188: 1698-1707. doi:10.4049/jimmunol.1102448.
22. Prevot N, Briet C, Lassmann H, Tardivel I, Roy E et al. (2010) Abrogation of icos/icosl costimulation in nod mice results in autoimmune deviation towards the neuromuscular system. Eur J Immunol 40: 2267-2276. doi:10.1002/eji. 201040416. PubMed: 20544729.
23. Burmeister Y, Lischke T, Dahler AC, Mages HW, Lam KP et al. (2008) ICOS controls the pool size of effector-memory and regulatory T cells. J Immunol 180: 774-782. PubMed: 18178815.
24. Kornete M, Sgouroudis E, Piccirillo CA (2012) ICOS-Dependent Homeostasis and Function of Foxp3+ Regulatory T Cells in Islets of Nonobese Diabetic Mice. J Immunol 188: 1064-1074. doi:10.4049/jimmunol.1101303. PubMed: 22227569.
25. Whitehead GS, Wilson RH, Nakano K, Burch LH, Nakano H, et al. (2012) IL-35 production by inducible costimulator (ICOS)-positive regulatory T cells reverses established IL-17-dependent allergic airways disease. The Journal of Allergy and Clinical Immunology 129: 207-15.e1-5.
26. Ito T, Hanabuchi S, Wang YH, Park WR, Arima K et al. (2008) Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 28: 870-880. doi:10.1016/j.immuni.2008.03.018. PubMed: 18513999.
27. Conrad C, Gregorio J, Wang YH, Ito T, Meller S et al. (2012) Plasmacytoid dendritic cells promote immunosuppression in ovarian cancer via ICOS co-stimulation of Foxp3+ T regulatory cells. Cancer Res 72: 5240-5249. doi:10.1158/0008-5472.CAN-12-2271. PubMed: 22850422.
28. Martin-Orozco N, Li Y, Wang Y, Liu S, Hwu P et al. (2010) Melanoma Cells Express ICOS Ligand to Promote the Activation and Expansion of T-Regulatory Cells. Cancer Res 70: 9581-9590. doi: 10.1158/0008-5472.CAN-10-1379. PubMed: 21098714.
29. Strauss L, Bergmann C, Szczepanski MJ, Lang S, Kirkwood JM et al. (2008) Expression of ICOS on human melanoma-infiltrating CD4+CD25highFoxp3+ T regulatory cells: implications and impact on tumor-mediated immune suppression. J Immunol 180: 2967-2980. PubMed: 18292519.
30. Tuettenberg A, Huter E, Hubo M, Horn J, Knop J et al. (2009) The Role of ICOS in Directing T Cell Responses: ICOS-Dependent Induction of T Cell Anergy by Tolerogenic Dendritic Cells. J Immunol 182: 3349-3356. doi:10.4049/jimmunol. 0802733. PubMed: 19265111.
31. Uchida K, Kusuda T, Koyabu M, Miyoshi H, Fukata N, et al. (2012) Regulatory T cells in type 1 autoimmune pancreatitis. International Journal of Rheumatology 2012: 795026.
32. Rudd CE, Taylor A, Schneider H (2009) CD28 and CTLA-4 coreceptor expression and signal transduction. Immunol Rev 229: 12-26. doi: 10.1111/j.1600-065X.2009.00770.x. PubMed: 19426212.
33. Tu W, Lau YL, Zheng J, Liu Y, Chan PL et al. (2008) Efficient generation of human alloantigen-specific CD4+ regulatory T cells from naive precursors by CD40-activated B cells. Blood 112: 2554-2562. doi: 10.1182/blood-2008-04-152041. PubMed: 18599794.
34. Zheng J, Liu Y, Qin G, Chan PL, Mao H et al. (2009) Efficient induction and expansion of human alloantigen-specific CD8 regulatory T cells from naive precursors by CD40-activated B cells. J Immunol 183: 3742-3750. doi:10.4049/jimmunol.0901329. PubMed: 19684082.
35. Takahashi N, Matsumoto K, Saito H, Nanki T, Miyasaka N et al. (2009) Impaired CD4 and CD8 Effector Function and Decreased Memory T Cell Populations in ICOS-Deficient Patients. J Immunol 182: 5515-5527. doi:10.4049/jimmunol. 0803256. PubMed: 19380800.
36. Ono M, Yaguchi H, Ohkura N, Kitabayashi I, Nagamura Y et al. (2007) Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 446: 685-689. doi:10.1038/nature05673. PubMed: 17377532.
37. Alegre ML, Frauwirth KA, Thompson CB (2001) T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol 1: 220-228. doi: 10.1038/35105024. PubMed: 11905831.
38. Egen JG, Kuhns MS, Allison JP (2002) CTLA-4: new insights into its biological function and use in tumor immunotherapy. Nat Immunol 3: 611-618. doi:10.1038/ni0702-611. PubMed: 12087419.
39. Read S, Malmström V, Powrie F (2000) Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J Exp Med 192: 295-302. doi:10.1084/jem.192.2.295. PubMed: 10899916.
40. Takahashi T, Tagami T, Yamazaki S, Uede T, Shimizu J et al. (2000) Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 192: 303-310. doi:10.1084/jem.192.2.303. PubMed: 10899917.
41. Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M et al. (2008) CTLA-4 control over Foxp3+ regulatory T cell function. Science 322: 271-275. doi:10.1126/science.1160062. PubMed: 18845758.
42. Wu J, Tang JL, Wu SJ, Lio HY, Yang YC (2009) Functional polymorphism of CTLA-4 and ICOS genes in allogeneic hematopoietic stem cell transplantation. Clin Chim Acta 403: 229-233. doi:10.1016/j.cca.2009.03.037. PubMed: 19332044.
43. Chen H, Liakou CI, Kamat A, Pettaway C, Ward JF et al. (2009) Anti-CTLA-4 therapy results in higher CD4+ICOShi T cell frequency and IFN-{gamma} levels in both nonmalignant and malignant prostate tissues. Proc Natl Acad Sci U S A 106: 2729-2734. doi:10.1073/pnas.0813175106. PubMed: 19202079.
44. Liakou CI, Kamat A, Tang DN, Chen H, Sun J et al. (2008) CTLA-4 blockade increases IFN{gamma}-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients. Proc Natl Acad Sci U S A 105: 14987-14992. doi:10.1073/pnas.0806075105. PubMed: 18818309.
45. Chuang E, Alegre ML, Duckett CS, Noel PJ, Vander Heiden MG et al. (1997) Interaction of CTLA-4 with the clathrin-associated protein AP50 results in ligand-independent endocytosis that limits cell surface expression. J Immunol 159: 144-151. PubMed: 9200449.
46. Gigoux M, Shang J, Pak Y, Xu M, Choe J et al. (2009) Inducible costimulator promotes helper T-cell differentiation through phosphoinositide 3-kinase. Proc Natl Acad Sci U S A 106: 20371-20376. doi:10.1073/pnas. 0911573106. PubMed: 19915142.
47. Koguchi Y, Thauland TJ, Slifka MK, Parker DC (2007) Preformed CD40 ligand exists in secretory lysosomes in effector and memory CD4+ T cells and is quickly expressed on the cell surface in an antigen-specific manner. Blood 110: 2520-2527. doi:10.1182/blood-2007-03-081299. PubMed: 17595332.
48. Mead KI, Zheng Y, Manzotti CN, Perry LC, Liu MK et al. (2005) Exocytosis of CTLA-4 is dependent on phospholipase D and ADP ribosylation factor-1 and stimulated during activation of regulatory T cells. J Immunol 174: 4803-4811. PubMed: 15814706.
49. Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD et al. (2006) FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 126: 375-387. doi:10.1016/j.cell.2006.05.042. PubMed: 16873067.
50. Zheng Y, Josefowicz SZ, Kas A, Chu TT, Gavin MA et al. (2007) Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445: 936-940. doi:10.1038/nature05563. PubMed: 17237761.