Transplantation of retrovirally transduced bone marrow prevents autoimmune disease in aged mice by peripheral tolerance mechanisms

Autoimmunity

Volumn 44, Issue 5, 2011, Pages 384-393

  Chen, Xiang T ^a   Chan, Siow T ^a   Hosseini, Hamid ^a   Layton, Daniel ^a   Boyd, Richard ^a   Alderuccio, Frank ^a   Toh, Ban Hock ^a   Chan, James ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Bone marrow stem cells; Experimental autoimmune encephalomyelitis; Gene therapy; Myelin oligodendrocyte glycoprotein; Tolerance

Indexed keywords

MYELIN OLIGODENDROCYTE GLYCOPROTEIN;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY DETECTION; ARTICLE; AUTOLOGOUS BONE MARROW TRANSPLANTATION; BONE MARROW TRANSPLANTATION; CASTRATION INDUCED THYMUS REGROWTH; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOLOGICAL TOLERANCE; INGUINAL LYMPH NODE; INTERMETHOD COMPARISON; MALE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN EXPRESSION; RADIATION DOSE; REGULATORY T LYMPHOCYTE; SHAM PROCEDURE; THYMUS DISEASE;

ANIMALS; AUTOANTIBODIES; AUTOIMMUNE DISEASES; BONE MARROW TRANSPLANTATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENETIC VECTORS; IMMUNE TOLERANCE; LYMPH NODES; MALE; MICE; MICE, INBRED C57BL; MYELIN-ASSOCIATED GLYCOPROTEIN; RETROVIRIDAE; SPINAL CORD; SPLEEN; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND; TRANSDUCTION, GENETIC; TRANSPLANTATION CHIMERA;

EID: 79960111421     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.3109/08916934.2010.541173     Document Type: Article

References (48)

1. Chan J, Siatskas C, Field J, Toh B-H, Alderuccio F. Mechanisms and applications of stem cell gene therapy in autoimmunity. Drug Discov Today Dis Mech 2006;3: 219-223 (Pubitemid 44356300)
2. Fassas A, Anagnostopoulos A, Kazis A, Kapinas K, Sakellari I, Kimiskidis V, Smias C, Eleftheriadis N, Tsimourtou V. Autologous stem cell transplantation in progressive multiple sclerosis-an interim analysis of efficacy. J Clin Immunol 2000;20:24-30 (Pubitemid 30210103)
3. Fassas A, Passweg JR, Anagnostopoulos A, Kazis A, Kozak T, Havrdova E, Carreras E, Graus F, Kashyap A, Openshaw H, Schipperus M, Deconinck E, Mancardi G, Marmont A, Hansz J, Rabusin M, Zuazu Nagore FJ, Besalduch J, Dentamaro T, Fouillard L, Hertenstein B. Hematopoietic stem cell transplantation for multiple sclerosis. A retrospective multicenter study. J Neurol 2002; 249:1088-1097 (Pubitemid 35002235)
4. Saiz A, Blanco Y, Berenguer J, Gomez M, Carreras E, Arbizu T, Graus F. Clinical outcome 6 years after autologous hematopoietic stem cell transplantation in multiple sclerosis.. Neurologia 2008;23:405-407
5. Gualandi F, Bruno B, Van Lint MT, Luchetti S, Uccelli A, Capello E, Mancardi GL, Bacigalupo A, Marmont A. Autologous stem cell transplantation for severe autoimmune diseases: A 10-year experience. Ann NY Acad Sci 2007;1110: 455-464 (Pubitemid 350043035)
6. Farge D, Labopin M, Tyndall A, Fassas A, Mancardi GL, Van Laar J, Ouyang J, Kozak T, Moore J, Kötter I, Chesnel V, Marmont A, Gratwohl A, Saccardi R. Autologous hematopoietic stem cell transplantation for autoimmune diseases: An observational study on 12 years? experience from the European Group for Blood and Marrow Transplantation Working Party on Autoimmune Diseases. Haematologica 2010;95:284-292
7. Chan J, Ban EJ, Chun KH, Wang S, Backstrom BT, Bernard CC, Toh B-H, Alderuccio F. Transplantation of bone marrow transduced to express self-antigen establishes deletional tolerance and permanently remits autoimmune disease. J Immunol 2008;181:7571-7580
8. Alderuccio F, Chan J, Scott DW, Toh BH. Gene therapy and bone marrow stem-cell transfer to treat autoimmune disease. Trends Mol Med 2009;15:344-351
9. Ally BA, Hawley TS, McKall-Faienza KJ, Kundig TM, Oehen SU, Pircher H, Hawley RG, Ohashi PS. Prevention of autoimmune disease by retroviral-mediated gene therapy. J Immunol 1995;155:5404-5408
10. Chan J, ClementsW, Field J, Nasa Z, Lock P, Yap F, Toh BH, Alderuccio F. Transplantation of bone marrow genetically engineered to express proinsulin II protects against autoimmune insulitis in NOD mice. J Gene Med 2006;8: 1281-1290 (Pubitemid 44782507)
11. Xu B, Haviernik P, Wolfraim LA, Bunting KD, Scott DW. Bone marrow transplantation combined with gene therapy to induce antigen-specific tolerance and ameliorate EAE. Mol Ther 2006;13:42-48 (Pubitemid 41763481)
12. Tian C, Bagley J, Cretin N, Seth N, Wucherpfennig KW, Iacomini J. Prevention of type 1 diabetes by gene therapy. J Clin Invest 2004;114:969-978 (Pubitemid 39578725)
13. Baranyi U, Linhart B, Pilat N, Gattringer M, Bagley J, Muehlbacher F, Iacomini J, Valenta R,Wekerle T. Tolerization of a type I allergic immune response through transplantation of genetically modified hematopoietic stem cells. J Immunol 2008;180:8168-8175
14. Anastasiadis K, Tratnatunga C. Changes with aging. The thymus gland. Berlin: Springer; 2007. p 9-11
15. Greenstein BD, Fitzpatrick FT, Adcock IM, Kendall MD, Wheeler MJ. Reappearance of the thymus in old rats after orchidectomy: Inhibition of regeneration by testosterone. J Endocrinol 1986;110:417-422 (Pubitemid 16052771)
16. Sutherland JS, Goldberg GL, Hammett MV, Uldrich AP, Berzins SP, Heng TS, Blazar BR, Millar JL, Malin MA, Chidgey AP, Boyd RL. Activation of thymic regeneration in mice and humans following androgen blockade. J Immunol 2005;175:2741-2753 (Pubitemid 41113891)
17. Seach N, Layton D, Lim J, Chidgey A, Boyd R. Thymic generation and regeneration: A new paradigm for establishing clinical tolerance of stem cell-based therapies. Curr Opin Biotechnol 2007;18:441-447 (Pubitemid 350119857)
18. Goldberg GL, Dudakov JA, Reiseger JJ, Seach N, Ueno T, Vlahos K, Hammett MV, Young LF, Heng TS, Boyd RL, Chidgey AP. Sex steroid ablation enhances immune reconstitution following cytotoxic antineoplastic therapy in young mice. J Immunol 2010;184:6014-6024
19. Fehervari Z, Sakaguchi S. CD4? Tregs and immune control. J Clin Invest 2004;114:1209-1217
20. Wing K, Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat Immunol 2010;11:7-13
21. McQualter JL, Darwiche R, Ewing C, Onuki M, Kay TW, Hamilton JA, Reid HH, Bernard CC. Granulocyte macrophage colony-stimulating factor: A new putative therapeutic target in multiple sclerosis. J Exp Med 2001; 194:873-882
22. Aiuti A, Cattaneo F, Galimberti S, Benninghoff U, Cassani B, Callegaro L, Scaramuzza S, Andolfi G, Mirolo M, Brigida I, Tabucchi A, Carlucci F, Eibl M, Aker M, Slavin S, Al-Mousa H, Al Ghonaium A, Ferster A, Duppenthaler A, Notarangelo L, Wintergerst U, Buckley RH, Bregni M, Marktel S, Valsecchi MG, Rossi P, Ciceri F, Miniero R, Bordignon C, Roncarolo MG. Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl JMed 2009;360:447-458
23. Chan JM, Villarreal G, Jin WW, Stepan T, Burstein H, Wahl SM. Intraarticular gene transfer of TNFR:Fc suppresses experimental arthritis with reduced systemic distribution of the gene product. Mol Ther 2002;6:727-736 (Pubitemid 36054306)
24. Doering CB, Spencer HT. Advancements in gene transferbased therapy for hemophilia A. Expert Rev Hematol 2009;2: 673-683
25. Gaspar HB, Parsley KL, Howe S, King D, Gilmour KC, Sinclair J, Brouns G, Schmidt M, Von Kalle C, Barington T, Jakobsen MA, Christensen HO, Al Ghonaium A, White HN, Smith JL, Levinsky RJ, Ali RR, Kinnon C, Thrasher AJ. Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet 2004;364: 218-217
26. Leung PS, Dhirapong A, Wu PY, Tao MH. Gene therapy in autoimmune diseases: Challenges and opportunities. Autoimmun Rev 2010;9:170-174
27. Bagley J, Tian C, Sachs DH, Iacomini J. Induction of T-cell tolerance to an MHC class I alloantigen by gene therapy. Blood 2002;99:4394-4399 (Pubitemid 34627206)
28. Eixarch H, Espejo C, Gomez A, Mansilla MJ, Castillo M, Mildner A, Vidal F, Gimeno R, Prinz M, Montalban X, Barquinero J. Tolerance induction in experimental autoimmune encephalomyelitis using non-myeloablative hematopoietic gene therapy with autoantigen. Mol Ther 2009;17:897-905
29. Kincade PW, Medina KL, Smithson G. Sex hormones as negative regulators of lymphopoiesis. Immunol Rev 1994;137: 119-134 (Pubitemid 24117120)
30. Berzins SP, Godfrey DI, Miller JF, Boyd RL. A central role for thymic emigrants in peripheral T cell homeostasis. Proc Natl Acad Sci USA 1999;96:9787-9791 (Pubitemid 29398810)
31. Naylor K, Li G, Vallejo AN, Lee WW, Koetz K, Bryl E, Witkowski J, Fulbright J, Weyand CM, Goronzy JJ. The influence of age on T cell generation and TCR diversity. J Immunol 2005;174:7446-7452 (Pubitemid 40705717)
32. Mackall CL, Fleisher TA, Brown MR, Andrich MP, Chen CC, Feuerstein IM, Horowitz ME, Magrath IT, Shad AT, Steinberg SM, Wexler LH, Gress RE. Age, thymopoiesis, and CD4? T-lymphocyte regeneration after intensive chemotherapy. N Engl J Med 1995;332:143-149
33. Tian C, Bagley J, Iacomini J. Expression of antigen on mature lymphocytes is required to induce T cell tolerance by gene therapy. J Immunol 2002;169:3771-3776
34. Tian C, Yuan X, Jindra PT, Bagley J, Sayegh MH, Iacomini J. Induction of transplantation tolerance to fully mismatched cardiac allografts by T cell mediated delivery of alloantigen in press Clin Immunol 2010;136:174-187
35. Melo ME, Qian J, El-Amine M, Agarwal RK, Soukhareva N, Kang Y, Scott DW, et al. Gene transfer of Ig-fusion proteins into B cells prevents and treats autoimmune diseases. J Immunol 2002;168:4788-4795 (Pubitemid 34441388)
36. Song L, Wang J, Wang R, Yu M, Sun Y, Han G, Li Y, Qian J, Scott DW, Kang Y, Soukhareva N, Shen B. Retroviral delivery of GAD-IgG fusion construct induces tolerance and modulates diabetes: A role for CD4? regulatory T cells and TGFbeta? Gene Ther 2004;11:1487-1496 (Pubitemid 39359456)
37. Werner-Klein M, Dresch C, Marconi P, Brocker T. Transcriptional targeting of B cells for induction of peripheral CD8 T cell tolerance. J Immunol 2007;178: 7738-7746 (Pubitemid 46898045)
38. Agarwal RK, Kang Y, Zambidis E, Scott DW, Chan CC, Caspi RR. Retroviral gene therapy with an immunoglobulin- antigen fusion construct protects from experimental autoimmune uveitis. J Clin Invest 2002;106:245-252 (Pubitemid 30483128)
39. Gallegos AM, Bevan MJ. Central tolerance to tissue-specific antigens mediated by direct and indirect antigen presentation. J Exp Med 2004;200:1039-1049 (Pubitemid 39431128)
40. Luckashenak N, Schroeder S, Endt K, SchmidtD, Mahnke K, Bachmann MF,Marconi P, Deeg CA, Brocker T. Constitutive crosspresentation of tissue antigens by dendritic cells controls CD8? T cell tolerance in vivo. Immunity 2008;28: 521-532
41. Liston A, Gray DH, Lesage S, Fletcher AL, Wilson J, Webster KE, Scott HS, Boyd RL, Peltonen L, Goodnow CC. Gene dosage-limiting role of Aire in thymic expression, clonal deletion, and organ-specific autoimmunity. J Exp Med 2004; 200:1015-1026 (Pubitemid 39431126)
42. Stephens LA, Gray D, Anderton SM. CD4?CD25? regulatory T cells limit the risk of autoimmune disease arising from T cell receptor crossreactivity. Proc Natl Acad Sci USA 2005; 102:17418-17423 (Pubitemid 41740881)
43. Akirav EM, Bergman CM, Hill M, Ruddle NH. Depletion of CD4?CD25? T cells exacerbates experimental autoimmune encephalomyelitis induced by mouse, but not rat, antigens. J Neurosci Res 2009;87:3511-3519
44. Liang Y, Van Zant G, Szilvassy SJ. Effects of aging on the homing and engraftment of murine hematopoietic stem and progenitor cells. Blood 2005;106:1479-1487 (Pubitemid 41129619)
45. Jing D, Fonseca AV, Alakel N, Fierro FA, Muller K, Bornhauser M, Ehninger G, Corbeil D, Ordemann R. Hematopoietic stem cells in co-culture with mesenchymal stromal cells-modeling the niche compartments in vitro. Haematologica 2010;95:542-550
46. Caplan AI. Why are MSCs therapeutic? New data: New insight. J Pathol 2009;217:318-324
47. Battiwalla M, Hematti P. Mesenchymal stem cells in hematopoietic stem cell transplantation. Cytotherapy 2009; 11:503-515
48. Gill J, Malin M, Hollander GA, Boyd R. Generation of a complete thymic microenvironment by MTS24? thymic epithelial cells. Nat Immunol 2002;3:635-642 (Pubitemid 34752472)