Does lymphopenia preclude restoration of immune homeostasis? The particular case of type 1 diabetes

Autoimmunity Reviews

Volumn 9, Issue 10, 2010, Pages 687-690

  Askenasy, Enosh M ^a   Askenasy, Nadir ^b   Askenasy, Jean Jaques ^c  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Bone marrow transplantation; Hematopoietic chimerism; Homeostatic expansion; Lymphoablation; Lymphopenia induced proliferation; Type 1 diabetes

Indexed keywords

CYCLOPHOSPHAMIDE; THYMOCYTE ANTIBODY;

AUTOIMMUNITY; AUTOLOGOUS BONE MARROW TRANSPLANTATION; CELL PROLIFERATION; CYTOTOXIC T LYMPHOCYTE; DIABETOGENESIS; DRUG SENSITIVITY; EFFECTOR CELL; ENGRAFTMENT; GRAFT VERSUS HOST REACTION; HOMEOSTASIS; HUMAN; IMMUNE HOMEOSTASIS; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTOPENIA; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW;

ANIMALS; BONE MARROW TRANSPLANTATION; CYCLOPHOSPHAMIDE; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; DRUG RESISTANCE; HOMEOSTASIS; HUMANS; LYMPHOPENIA; MICE; MICE, INBRED NOD; RADIOTHERAPY; SELF TOLERANCE; T-LYMPHOCYTES; TRANSPLANTATION CONDITIONING;

EID: 77955235892     PISSN: 15689972     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.autrev.2010.05.019     Document Type: Review

References (49)

1. Alonso N., Soldevila B., Sanmartí A., Pujol-Borrell R., Martínez-Cáceres E. Regulatory T cells in diabetes and gastritis. Autoimmun Rev 2009, 8:659-662.
2. Borchers A.T., Uibo R., Gershwin M.E. The geoepidemiology of type 1 diabetes. Autoimmun Rev 2010, 9:A355-A365.
3. Ramanathan S., Bihoreau M.T., Paterson A.D., Marandi L., Gauguier D., Poussier P. Thymectomy and radiation-induced type 1 diabetes in nonlymphopenic BB rats. Diabetes 2002, 51:2975-2981.
4. King C., Ilic A., Koelsch K., Sarvetnick N. Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 2004, 117:265-277.
5. Dardenne M., Lepault F., Bendelac A., Bach J.F. Acceleration of the onset of diabetes in NOD mice by thymectomy at weaning. Eur J Immunol 1989, 19:889-895.
6. Gleeson P.A., Toh B.H., van Driel I.R. Organ-specific autoimmunity induced by lymphopenia. Immunol Rev 1996, 149:97-125.
7. Abbas A.K., Lohr J., Knoechel B. Balancing autoaggressive and protective T cell responses. J Autoimmun 2007, 28:59-61.
8. Serreze D.V., Hamaguchi K., Leiter E.H. Immunostimulation circumvents diabetes in NOD/Lt mice. J Autoimmun 1989, 2:759-776.
9. Setoguchi R., Hori S., Takahashi T., Sakaguchi S. Homeostatic maintenance of natural Foxp3+CD25+CD4+ regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 2005, 201:723-735.
10. Tang Q., Adams J.Y., Penaranda C., et al. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 2008, 28:687-697.
11. Burt R.K., Testori A., Craig R., Cohen B., Suffit R., Barr W. Hematopoietic stem cell transplantation for autoimmune diseases: what have we learned?. J Autoimmun 2008, 30:116-120.
12. Marmont A.M. Will hematopoietic stem cell transplantation cure human autoimmune diseases?. J Autoimmun 2008, 30:145-150.
13. Beilhack G.F., Scheffold Y.C., Weissman I.L., et al. Purified allogeneic hematopoietic stem cell transplantation blocks diabetes pathogenesis in NOD mice. Diabetes 2003, 52:59-68.
14. Kaminitz A., Iskovich S., Mizrahi K., et al. Low levels of allogeneic but not syngeneic hematopoietic chimerism reverse autoimmune insulitis in prediabetic NOD mice. J Autoimmun 2009, 33:83-91.
15. Yaniv I., Ash S., Farkas D.L., Askenasy N., Stein J. Consideration of strategies for hematopoietic cell transplantation. J Autoimmun 2009, 33:255-259.
16. Couri C.E., Oliveira M.C., Stracieri A.B., et al. C-peptide levels and insulin independence following autologous nonmyeloablative hematopoietic stem cell transplantation in newly diagnosed type 1 diabetes mellitus. JAMA 2009, 301:1573-1579.
17. Brode S., Raine T., Zaccone P., Cooke A. Cyclophosphamide-induced type-1 diabetes in the NOD mouse is associated with a reduction of CD4+CD25+Foxp3+ regulatory T cells. J Immunol 2006, 177:6603-6612.
18. Keymeulen B., Walter M., Mathieu C., et al. Four-year metabolic outcome of a randomised controlled CD3-antibody trial in recent-onset type 1 diabetic patients depends on their age and baseline residual beta cell mass. Diabetologia 2010, 53:614-623.
19. Goldrath A.W., Bogatzki L.Y., Bevan M.J. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J Exp Med 2000, 192:557-564.
20. Tanchot C., Le Campion A., Martin B., Léaument S., Dautigny N., Lucas B. Conversion of naive T cells to a memory-like phenotype in lymphopenic hosts is not related to a homeostatic mechanism that fills the peripheral naive T cell pool. J Immunol 2002, 168:5042-5046.
21. + regulatory T cells and memory T cells prevent lymphopenia-induced proliferation of naive T cells in transient states of lymphopenia. J Immunol 2006, 177:4558-4566.
22. Masopust D., Vezys V., Marzo A.L., Lefrancois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001, 291:2413-2417.
23. Colucci F., Cilio C.M., Lejon K., Goncalves C.P., Bergman M.L., Holmberg D. Programmed cell death in the pathogenesis of murine IDDM: resistance to apoptosis induced in lymphocytes by cyclophosphamide. J Autoimmun 1996, 9:271-276.
24. Yarkoni S., Kaminitz A., Sagiv Y., Askenasy N. Targeting of IL-2 receptor with a caspase fusion protein disrupts autoimmunity in prediabetic and diabetic NOD mice. Diabetologia 2010, 53:356-368.
25. Steptoe R.J., Stankovic S., Lopaticki S., Jones L.K., Harrison L.C., Morahan G. Persistence of recipient lymphocytes in NOD mice after irradiation and bone marrow transplantation. J Autoimmun 2004, 22:131-138.
26. Li H., Kaufman C.L., Boggs S.S., Johnson P.C., Patrene K.D., Ildstad S.T. Mixed allogeneic chimerism induced by a sublethal approach prevents autoimmune diabetes and reverses insulitis in non-obese diabetic (NOD) mice. J Immunol 1996, 156:380-388.
27. Le Campion A., Gagnerault M.C., Auffray C., et al. Lymphopenia-induced spontaneous T-cell proliferation as a cofactor for autoimmune disease development. Blood 2009, 114:1784-1793.
28. Shvets A., Chakrabarti R., Gonzalez-Quintial R., Baccala R., Theofilopoulos A.N., Prud'homme G.J. Impaired negative regulation of homeostatically proliferating T cells. Blood 2009, 113:622-625.
29. Shklovskaya E., Fazekas de St. Groth B. Severely impaired clonal deletion of CD4+ T cells in low-dose irradiated mice: role of T cell antigen receptor and IL-7 receptor signals. J Immunol 2006, 177:8320-8330.
30. Barthlott T., Kassiotis G., Stockinger B. T cell regulation as a side effect of homeostasis and competition. J Exp Med 2003, 197:451-460.
31. Troy A.E., Shen H. Cutting edge: homeostatic proliferation of peripheral T lymphocytes is regulated by clonal competition. J Immunol 2003, 170:672-676.
32. Knoechel B., Lohr J., Kahn E., Bluestone J.A., Abbas A.K. Sequential development of interleukin 2-dependent effector and regulatory T cells in response to endogenous systemic antigen. J Exp Med 2005, 202:1375-1386.
33. Min B., Yamane H., Hu-Li J., Paul W.E. Spontaneous and homeostatic proliferation of CD4 T cells are regulated by different mechanisms. J Immunol 2005, 174:6039-6044.
34. Bourgeois C., Hao Z., Rajewsky K., Potocnik A.J., Stockinger B. Ablation of thymic export causes accelerated decay of naive CD4 T cells in the periphery because of activation by environmental antigen. Proc Natl Acad Sci USA 2008, 105:8691-8696.
35. Larger E., Becourt C., Bach J.F., Boitard C. Pancreatic islet beta-cells drive T-cell immune responses in the nonobese diabetic mouse model. J Exp Med 1996, 181:1635-1642.
36. Kaminitz A., Stein J., Yaniv I., Askenasy N. The vicious cycle of apoptotic Β cell death in type 1 diabetes. Immunol Cell Biol 2007, 85:582-589.
37. La Gruta N.L., Driel I.R., Gleeson P.A. Peripheral T cell expansion in lymphopenic mice results in a restricted T cell repertoire. Eur J Immunol 2000, 30:3380-3386.
38. Surh C.D., Sprent J. Homeostatic T cell proliferation: how far can T cells be activated to self-ligands?. J Exp Med 2000, 21(192):F9-F14.
39. Schrum A.G., Turka L.A. The proliferative capacity of individual naive CD4(+) T cells is amplified by prolonged T cell antigen receptor triggering. J Exp Med 2002, 196:793-803.
40. Tang Q., Henriksen K.J., Bi M., et al. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 2004, 199:1455-1465.
41. Fehervari Z., Yamaguchi T., Sakaguchi S. The dichotomous role of IL-2: tolerance versus immunity. Trends Immunol 2006, 27:109-111.
42. Decallonne B., van Etten E., Giulietti A., et al. Defect in activation induced cell death in non-obese diabetic (NOD) T lymphocytes. J Autoimmun 2003, 20:219-226.
43. + regulatory T cells. J Immunol 2008, 181:7350-7355.
44. Elkin G., Prigozhina T.B., Slavin S. Prevention of diabetes in nonobese diabetic mice by nonmyeloablative allogeneic bone marrow transplantation. Exp Hematol 2004, 32:579-584.
45. Serreze D.V., Osborne M.A., Chen Y.G., et al. Partial versus full allogeneic hemopoietic chimerization is a preferential means to inhibit type 1 diabetes as the latter induces generalized immunosuppression. J Immunol 2006, 177:6675-6684.
46. Serreze D.V., Johnson E.A., Chapman H.D., et al. Autoreactive diabetogenic T-cells in NOD mice can efficiently expand from a greatly reduced precursor pool. Diabetes 2001, 50:1992-2000.
47. von Boehmer H., Melchers F. Checkpoints in lymphocyte development and autoimmune disease. Nat Immunol 2010, 11:14-20.
48. Haller M.J., Viener H.L., Wasserfall C., Brusko T., Atkinson M.A., Schatz D.A. Autologous umbilical cord blood infusion for type 1 diabetes. Exp Hematol 2008, 36:710-715.
49. Wu Z., Bensinger S.J., Zhang J., et al. Homeostatic proliferation is a barrier to transplantation tolerance. Nat Med 2004, 10:87-92.