SHIP limits immunoregulatory capacity in the T-cell compartment

Blood

Volumn 113, Issue 13, 2009, Pages 2934-2944

  Collazo, Michelle M ^a   Wood, Daniela ^a   Paraiso, Kim H T ^a   Lund, Erin ^a   Engelman, Robert W ^a   Le, Cam Tien ^b   Stauch, Diana ^b   Kotsch, Katja ^b   Kerr, William G ^a,c  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD134 ANTIGEN; CD16 ANTIGEN; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; PROTEIN TYROSINE PHOSPHATASE SHP 2; SH2 DOMAIN CONTAINING INOSITOL 5-PHOSPHATASE; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC GRAFT REJECTION; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; COLITIS; CONTROLLED STUDY; ENZYME DEFICIENCY; GRAFT VERSUS HOST REACTION; IMMUNOREGULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE;

EID: 63849121372     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-09-181164     Document Type: Article

References (46)

1. Saoudi A, Seddon B, Heath V, Fowell D, Mason D. The physiologic role of regulatory T cells in the prevention of autoimmunity: the function of the thymus in the generation of the regulatory T cell subset. Immunol Rev. 1996; 149:195-216.
2. Sakaguchi S, Fukuma K, Kuribayashi K, Masuda T. Organ-specific autoimmune diseases induced in mice by elimination of T cell subset: I. Evidence for the active participation of T cells in natural self-tolerance: deficit of a T cell subset as a possible cause of autoimmune disease. J Exp Med. 1985;161:72-87.
3. Edinger M, Hoffmann P, Ermann J, et al. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus- host disease after bone marrow transplantation. Nat Med. 2003;9:1144-1150.
4. Hoffmann P, Ermann J, Edinger M, Fathman CG, Strober S. Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J Exp Med. 2002;196:389-399.
5. Kingsley CI, Karim M, Bushell AR, Wood KJ. CD25+CD4+ regulatory T cells prevent graft rejection: CTLA-4- and IL-10-dependent immuno- regulation of alloresponses. J Immunol. 2002;168:1080-1086.
6. Wang JW, Howson JM, Ghansah T, et al. Influence of SHIP on the NK repertoire and allogeneic bone marrow transplantation. Science. 2002;295:2094-2097.
7. Paraiso KH, Ghansah T, Costello A, Engelman RW, Kerr WG. Induced SHIP deficiency expands myeloid regulatory cells and abrogates graft-versus-host disease. J Immunol. 2007;178:2893-2900.
8. Ghansah T, Paraiso KH, Highfill S, et al. Expansion of myeloid suppressor cells in SHIP-deficient mice represses allogeneic T cell responses. J Immunol. 2004;173:7324-7330.
9. Wahle JA, Paraiso KH, Costello AL, Goll EL, Sentman CL, Kerr WG. Cutting edge: dominance by an MHC-independent inhibitory receptor compromises NK killing of complex targets. J Immunol. 2006;176:7165-7169.
10. Taylor PA, Panoskaltsis-Mortari A, Swedin JM, et al. L-Selectin(hi) but not the L-selectin(lo) CD4+25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection. Blood. 2004; 104:3804-3812.
11. MacDonald KP, Rowe V, Clouston AD, et al. Cytokine expanded myeloid precursors function as regulatory antigen-presenting cells and promote tolerance through IL-10-producing regulatory T cells. J Immunol. 2005;174:1841-1850.
12. Huang B, Pan PY, Li Q, et al. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 2006;66:1123-1131.
13. Walsh PT, Buckler JL, Zhang J, et al. PTEN inhibits IL-2 receptor-mediated expansion of CD4+ CD25+ Tregs. J Clin Invest. 2006;116:25212531.
14. So T, Croft M. Cutting edge: OX40 inhibits TGF-beta- and antigen-driven conversion of naive CD4 T cells into CD25+ Foxp3+ T cells. J Immunol. 2007;179:1427-1430.
15. Mazzucchelli R, Hixon JA, Spolski R, et al. Development of regulatory T cells requires IL-7Ralpha stimulation by IL-7 or TSLP. Blood. 2008;112:3283-3292.
16. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25) breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol. 1995;155:1151-1164.
17. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4:330-336.
18. Lehmann J, Huehn J, de la Rosa M, et al. Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25- regu- latory T cells. Proc Natl Acad Sci USA. 2002;99:13031-13036.
19. Cepek KL, Shaw SK, Parker CM, et al. Adhesion between epithelial cells and Tlymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature. 1994;372:190-193.
20. So T, Lee SW, Croft M. Immune regulation and control of regulatory T cells by OX40 and 4-1BB. Cytokine Growth Factor Rev. 2008;19:253-262.
21. Kanamaru F, Youngnak P, Hashiguchi M, et al. Costimulation via glucocorticoid-induced TNF receptor in both conventional and CD25+ regulatory CD4+ T cells. J Immunol. 2004;172:7306-7314.
22. Nolte-'t Hoen EN, Wagenaar-Hilbers JP, Boot EP, et al. Identification of a CD4+CD25+ Tcell subset committed in vivo to suppress antigen-specific T cell responses without additional stimulation. Eur J Immunol. 2004;34:3016-3027.
23. Huehn J, Siegmund K, Lehmann JC, et al. Developmental stage, phenotype, and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J Exp Med. 2004;199:303-313.
24. Ono M, Shimizu J, Miyachi Y, Sakaguchi S. Control of autoimmune myocarditis and multiorgan inflammation by glucocorticoid-induced TNF receptor family-related protein(high), Foxp3-ex- pressing CD25+ and CD25- regulatory T cells. J Immunol. 2006;176:4748-4756.
25. Uraushihara K, Kanai T, Ko K, et al. Regulation of murine inflammatory bowel disease by CD25+ and CD25-CD4+ glucocorticoid-induced TNF receptor family-related gene+ regulatory T cells. J Immunol. 2003;171:708-716.
26. Karlsson MC, Guinamard R, Bolland S, Sankala M, Steinman RM, Ravetch JV. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J Exp Med. 2003;198:333-340.
27. Weijer K, Uittenbogaart CH, Voordouw A, et al. Intrathymic and extrathymic development of human plasmacytoid dendritic cell precursors invivo. Blood. 2002;99:2752-2759.
28. Desponts C, Hazen AL, Paraiso KH, Kerr WG. SHIP deficiency enhances HSC proliferation and survival but compromises homing and repopulation. Blood. 2006;107:4338-4345.
29. Corry RJ, Winn HJ, Russell PS. Heart transplantation in congenic strains of mice. Transplant Proc. 1973;5:733-735.
30. Hartigan-O'Connor DJ, Poon C, Sinclair E, McCune JM. Human CD4+ regulatory T cells express lower levels of the IL-7 receptor alpha chain (CD127), allowing consistent identification and sorting of live cells. J Immunol Methods. 2007;319:41-52.
31. Nimmerjahn F, Ravetch JV. Analyzing antibody-Fc-receptor interactions. Methods Mol Biol. 2008;415:151-162.
32. Tarasenko T, Kole HK, Chi AW, Mentink-Kane MM, Wynn TA, Bolland S. T cell-specific deletion of the inositol phosphatase SHIP reveals its role in regulating Th1/Th2 and cytotoxic responses. Proc Natl Acad Sci USA. 2007;104:11382-11387.
33. Kashiwada M, Cattoretti G, McKeag L, et al. Downstream of tyrosine kinases-1 and Src homology 2-containing inositol 5'-phosphatase are required for regulation of CD4+CD25+ T cell development. J Immunol. 2006;176:3958-3965.
34. Thornton AM, Shevach EM. Suppressor effector function of CD4+ CD25+ immunoregulatory T cells is antigen nonspecific. J Immunol. 2000;164:183-190.
35. Streeter PR, Zhang X, Tittle TV, Schon CN, Weinberg AD, Maziarz RT. CD25 expression distinguishes functionally distinct alloreactive CD4 CD134 (OX40) T-cell subsets in acute graft-ver-sus-host disease. Biol Blood Marrow Transplant. 2004;10:298-309.
36. Song J, So T, Cheng M, Tang X, Croft M. Sustained survivin expression from OX40 costimulatory signals drives T cell clonal expansion. Immunity. 2005;22:621-631.
37. Harnaha J, Machen J, Wright M, et al. Interleukin-7 is a survival factor for CD4+ CD25+ T-cells and is expressed by diabetes-suppressive dendritic cells. Diabetes. 2006;55:158-170.
38. Sarnacki S, Begue B, Buc H, Le Deist F, Cerf-Bensussan N. Enhancement of CD3-induced activation of human intestinal intraepithelial lymphocytes by stimulation of the beta 7-containing integrin defined by HML-1 monoclonal antibody. Eur J Immunol 1992;22:2887-2892
39. Yates J, Rovis F, Mitchell P, et al. The maintenance of human CD4+ CD25+ regulatory T cell function: IL-2, IL-4, IL-7 and IL-15 preserve optimal suppressive potency in vitro. Int Immunol.2007;19:785-799.
40. Galandrini R, Tassi I, Morrone S, et al. The adaptor protein shc is involved in the negative regulation of NK cell-mediated cytotoxicity. Eur J Immunol. 2001;31:2016-2025.
41. Ono M, Bolland S, Tempst P, Ravetch JV. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc-(gamma)RIIB. Nature. 1996;383:263-266.
42. Brauweiler A, Tamir I, Dal Porto J, et al. Differential regulation of B cell development, activation, and death by the src homology 2 domain-containing 5' inositol phosphatase (SHIP). J Exp Med. 2000;191:1545-1554.
43. Hazen AL, Smith MJ, Desponts C, Winter O, Moser K, Kerr WG. SHIP is required for a functional hematopoietic stem cell niche. Blood. 2009; 113:2924-2933.
44. Rutella S, Pierelli L, Bonanno G, et al. Role for granulocyte colony-stimulating factor in the generation of human T regulatory type 1 cells. Blood. 2002;100:2562-2571.
45. Morris ES, MacDonald KP, Rowe V, et al. Donor treatment with pegylated G-CSF augments the generation of IL-10-producing regulatory T cells and promotes transplantation tolerance. Blood. 2004;103:3573-3581.
46. Suri-Payer E, Amar AZ, Thornton AM, Shevach EM. CD4+CD25+ T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells. J Immunol. 1998;160:1212-1218.