Hematopoietic stem cell gene therapy as a treatment for autoimmune diseases

Molecular Pharmaceutics

Volumn 8, Issue 5, 2011, Pages 1488-1494

  Alderuccio, Frank ^a   Nasa, Zeyad ^a   Chung, Jieyu ^a   Ko, Hyun Ja ^a   Chan, James ^a   Toh, Ban Hock ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

autoimmune disease; bone marrow transplantation; experimental autoimmune encephalomyelitis; gene therapy; immune tolerance

Indexed keywords

ALLERGIC ENCEPHALOMYELITIS; AUTOIMMUNE DISEASE; GENE THERAPY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENT DIABETES MELLITUS; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; AUTOIMMUNE DISEASES; CELLS, CULTURED; COMBINED MODALITY THERAPY; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE THERAPY; GENE TRANSFER TECHNIQUES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOSUPPRESSION; MICE;

EID: 80053510675     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp2001523     Document Type: Review

References (75)

1. Rose, N. R.; Mackay, I. R. The Autoimmune Diseases, 4 th ed.; Elsevier Academic Press: San Diego, CA, 2006.
2. Bach, J. F., Type 1 Diabetes. In The Autoimmune Diseases; Noel Rose, I. M., Ed.; Elsevier: Sydney, 2006; pp 483-500.
3. Hafler, D. A.; Slavik, J. M.; Anderson, D. E.; OConnor, K. C.; De Jager, P.; Baecher-Allan, C. Multiple sclerosis Immunol. Rev. 2005, 204, 208-231 (Pubitemid 40460504)
4. Compston, A.; Coles, A. Multiple sclerosis Lancet 2008, 372, 1502-1517
5. Arnett, P. A.; Strober, L. B. Cognitive and neurobehavioral features in multiple sclerosis Expert Rev. Neurother. 2011, 11, 411-424
6. Frohman, E. M.; Racke, M. K.; Raine, C. S. Multiple sclerosis-the plaque and its pathogenesis N. Engl. J. Med. 2006, 354, 942-955
7. Iwasaki, A.; Medzhitov, R. Regulation of adaptive immunity by the innate immune system Science 2010, 327, 291-295
8. Janeway, C. A., Jr.; Medzhitov, R. Innate immune recognition Annu. Rev. Immunol. 2002, 20, 197-216 (Pubitemid 34293424)
9. Murphy, K.; Travers, P.; Walter, P. Janeways Immunobiology, 7 th ed.; Garland Publishing: New York, 2008.
10. Goodnow, C. C.; Sprent, J.; de St Groth, B. F.; Vinuesa, C. G. Cellular and genetic mechanisms of self tolerance and autoimmunity Nature 2005, 435, 590-597 (Pubitemid 40825498)
11. Griesemer, A. D.; Sorenson, E. C.; Hardy, M. A. The role of the thymus in tolerance Transplantation 2010, 90, 465-474
12. Kronenberg, M.; Rudensky, A. Regulation of immunity by self-reactive T cells Nature 2005, 435, 598-604 (Pubitemid 40825499)
13. Kyewski, B.; Klein, L. A central role for central tolerance Annu. Rev. Immunol. 2006, 24, 571-606
14. Palmer, E. Negative selection-clearing out the bad apples from the T-cell repertoire Nat. Rev. Immunol. 2003, 3, 383-391 (Pubitemid 37323198)
15. Derbinski, J.; Kyewski, B. Linking signalling pathways, thymic stroma integrity and autoimmunity Trends Immunol. 2005, 26, 503-506 (Pubitemid 41297677)
16. Derbinski, J.; Pinto, S.; Rosch, S.; Hexel, K.; Kyewski, B. Promiscuous gene expression patterns in single medullary thymic epithelial cells argue for a stochastic mechanism Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 657-662 (Pubitemid 351171764)
17. Kyewski, B.; Taubert, R. How promiscuity promotes tolerance: the case of myasthenia gravis Ann. N.Y. Acad. Sci. 2008, 1132, 157-162 (Pubitemid 351841368)
18. Mathis, D.; Benoist, C. Aire Annu. Rev. Immunol. 2009, 27, 287-312
19. Gray, D.; Abramson, J.; Benoist, C.; Mathis, D. Proliferative arrest and rapid turnover of thymic epithelial cells expressing Aire J. Exp. Med. 2007, 204, 2521-2528 (Pubitemid 350044777)
20. Anderson, M. S.; Venanzi, E. S.; Klein, L.; Chen, Z.; Berzins, S. P.; Turley, S. J.; von Boehmer, H.; Bronson, R.; Dierich, A.; Benoist, C.; Mathis, D. Projection of an immunological self shadow within the thymus by the aire protein Science 2002, 298, 1395-1401 (Pubitemid 35346134)
21. Derbinski, J.; Gabler, J.; Brors, B.; Tierling, S.; Jonnakuty, S.; Hergenhahn, M.; Peltonen, L.; Walter, J.; Kyewski, B. Promiscuous gene expression in thymic epithelial cells is regulated at multiple levels.[see comment] J. Exp. Med. 2005, 202, 33-45 (Pubitemid 41002908)
22. Gotter, J.; Brors, B.; Hergenhahn, M.; Kyewski, B. Medullary Epithelial Cells of the Human Thymus Express a Highly Diverse Selection of Tissue-specific Genes Colocalized in Chromosomal Clusters J. Exp. Med. 2004, 199, 155-166 (Pubitemid 38139246)
23. Finnish-German APECED Consortium. An autoimmune disease, APECED, caused by mutations in a novel gene featuring two PHD-type zinc-finger domains. Nat. Genet. 1997, 17, 399-403.
24. Akirav, E. M.; Ruddle, N. H.; Herold, K. C. The role of AIRE in human autoimmune disease Nat. Rev. Endocrinol. 2011, 7, 25-33
25. Hubert, F. X.; Kinkel, S. A.; Crewther, P. E.; Cannon, P. Z.; Webster, K. E.; Link, M.; Uibo, R.; OBryan, M. K.; Meager, A.; Forehan, S. P.; Smyth, G. K.; Mittaz, L.; Antonarakis, S. E.; Peterson, P.; Heath, W. R.; Scott, H. S. Aire-deficient C57BL/6 mice mimicking the common human 13-base pair deletion mutation present with only a mild autoimmune phenotype J. Immunol. 2009, 182, 3902-3918
26. Kuroda, N.; Mitani, T.; Takeda, N.; Ishimaru, N.; Arakaki, R.; Hayashi, Y.; Bando, Y.; Izumi, K.; Takahashi, T.; Nomura, T.; Sakaguchi, S.; Ueno, T.; Takahama, Y.; Uchida, D.; Sun, S.; Kajiura, F.; Mouri, Y.; Han, H.; Matsushima, A.; Yamada, G.; Matsumoto, M. Development of autoimmunity against transcriptionally unrepressed target antigen in the thymus of Aire-deficient mice J. Immunol. 2005, 174, 1862-1870 (Pubitemid 40223925)
27. Allen, S.; Turner, S. J.; Bourges, D.; Gleeson, P. A.; van Driel, I. R. Shaping the T-cell repertoire in the periphery Immunol. Cell Biol. 2011, 89, 60-69
28. Mueller, D. L. Mechanisms maintaining peripheral tolerance Nat. Immunol. 2010, 11, 21-27
29. Wing, K.; Sakaguchi, S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity Nat. Immunol. 2010, 11, 7-13
30. Alderuccio, F.; Toh, B. H.; Tan, S. S.; Gleeson, P. A.; van Driel, I. R. An autoimmune disease with multiple molecular targets abrogated by the transgenic expression of a single autoantigen in the thymus J. Exp. Med. 1993, 178, 419-426 (Pubitemid 23218190)
31. French, M. B.; Allison, J.; Cram, D. S.; Thomas, H. E.; Dempsey-Collier, M.; Silva, A.; Georgiou, H. M.; Kay, T. W.; Harrison, L. C.; Lew, A. M. Transgenic expression of mouse proinsulin II prevents diabetes in nonobese diabetic mice [published erratum appears in Diabetes 1997 May;46(5):924] Diabetes 1997, 46, 34-39 (Pubitemid 27009946)
32. Jaeckel, E.; Lipes, M. A.; von Boehmer, H. Recessive tolerance to preproinsulin 2 reduces but does not abolish type 1 diabetes Nat. Immunol. 2004, 5, 1028-1035 (Pubitemid 41057722)
33. Xu, H.; Wawrousek, E. F.; Redmond, T. M.; Nickerson, J. M.; Wiggert, B.; Chan, C. C.; Caspi, R. R. Transgenic expression of an immunologically privileged retinal antigen extraocularly enhances self tolerance and abrogates susceptibility to autoimmune uveitis Eur. J. Immunol. 2000, 30, 272-278 (Pubitemid 30011789)
34. Billingham, R. E.; Brent, L.; Medawar, P. B. Activity acquired tolerance of foreign cells Nature 1953, 172, 603-606
35. Brocker, T.; Riedinger, M.; Karjalainen, K. Targeted expression of major histocompatibility complex (MHC) class II molecules demonstrates that dendritic cells can induce negative but not positive selection of thymocytes in vivo J. Exp. Med. 1997, 185, 541-550 (Pubitemid 27078372)
36. Ohnmacht, C.; Pullner, A.; King, S. B.; Drexler, I.; Meier, S.; Brocker, T.; Voehringer, D. Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity J. Exp. Med. 2009, 206, 549-559
37. Derbinski, J.; Kyewski, B. How thymic antigen presenting cells sample the bodys self-antigens Curr. Opin. Immunol. 2010, 22, 592-600
38. Murphy, K.; Biondo, M.; Toh, B. H.; Alderuccio, F. Tolerance established in autoimmune disease by mating or bone marrow transplantation that target autoantigen to thymus Int. Immunol. 2003, 15, 1-9
39. Steptoe, R. J.; Ritchie, J. M.; Harrison, L. C. Transfer of hematopoietic stem cells encoding autoantigen prevents autoimmune diabetes J. Clin. Invest. 2003, 111, 1357-1363 (Pubitemid 36554706)
40. Alderuccio, F.; Murphy, K.; Toh, B. H. Stem cells engineered to express self-antigen to treat autoimmunity Trends Immunol. 2003, 24, 176-180 (Pubitemid 36412104)
41. Chan, J.; Alderuccio, F.; Toh, B. H. Transplantation of Genetically Modified Haematopoietic Stem Cells to Induce Antigen-Specific Tolerance as a Cure for Autoimmune Diseases Curr. Stem Cell Res. Ther. 2011, 6 (1) 44-49
42. Alderuccio, F.; Chan, J.; Scott, D. W.; Toh, B. H. Gene therapy and bone marrow stem-cell transfer to treat autoimmune disease Trends Mol. Med. 2009, 15, 344-351
43. Siatskas, C.; Chan, J.; Field, J.; Murphy, K.; Nasa, Z.; Toh, B. H.; Alderuccio, F. Gene therapy strategies towards immune tolerance to treat the autoimmune diseases Curr. Gene Ther. 2006, 6, 45-58
44. Miller, S. D.; Karpus, W. J. Experimental autoimmune encepahlomeylitis. Curr. Protoc. Immunol. 2007, 15.11.11-15.11.18.
45. Gold, R.; Linington, C.; Lassmann, H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research Brain 2006, 129, 1953-1971 (Pubitemid 44289062)
46. Steinman, L.; Zamvil, S. S. How to successfully apply animal studies in experimental allergic encephalomyelitis to research on multiple sclerosis.[comment] Ann. Neurol. 2006, 60, 12-21
47. Fontoura, P.; Garren, H.; Steinman, L. Antigen-specific therapies in multiple sclerosis: going beyond proteins and peptides Int. Rev. Immunol. 2005, 24, 415-446 (Pubitemid 41755155)
48. Chan, J.; Ban, E. J.; Chun, K. H.; Wang, B.; Backstrom, B. T.; Bernard, C.; Toh, B. H.; Alderuccio, F. Transplantation of Bone Marrow Transduced to Express Self-Antigen Establishes Deletional Tolerance and Permanently Remits Autoimmune Disease J. Immmunol. 2008, 181, 7571-7580
49. Chan, J.; Ban, E. J.; Chun, K. H.; Wang, S.; McQualter, J.; Bernard, C.; Toh, B. H.; Alderuccio, F. Methylprednisolone induces reversible clinical and pathological remission and loss of lymphocyte reactivity to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis Autoimmunity 2008, 41, 405-413 (Pubitemid 351891202)
50. Blanco, Y.; Saiz, A.; Carreras, E.; Graus, F. Autologous haematopoietic-stem-cell transplantation for multiple sclerosis Lancet Neurol. 2005, 4, 54-63 (Pubitemid 40023236)
51. Burt, R. K.; Loh, Y.; Cohen, B.; Stefoski, D.; Balabanov, R.; Katsamakis, G.; Oyama, Y.; Russell, E. J.; Stern, J.; Muraro, P.; Rose, J.; Testori, A.; Bucha, J.; Jovanovic, B.; Milanetti, F.; Storek, J.; Voltarelli, J. C.; Burns, W. H. Autologous non-myeloablative haemopoietic stem cell transplantation in relapsing-remitting multiple sclerosis: a phase I/II study Lancet Neurol. 2009, 8, 244-253
52. Marmont, A. M. The origin of increasing utilization of hematopoietic stem cell transplantation (HSCT) for severe autoimmune diseases (SAD). Introduction Autoimmunity 2008, 41, 556-562
53. Couzin, J. Immunology. Gently soothing a savage immune system Science 2002, 296, 456-458 (Pubitemid 34408644)
54. Marmont, A. Will heamatopoietic stem cell transplantation cure human autoimmune diseases? J. Autoimmun. 2008, 30, 145-150
55. Kang, E. S.; Iacomini, J. Induction of central deletional T cell tolerance by gene therapy J. Immunol. 2002, 169, 1930-1935 (Pubitemid 34857656)
56. Chan, J.; Clements, W.; Field, J.; Lock, P.; Yap, F.; Toh, B. H.; 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)
57. Dresch, C.; Edelmann, S. L.; Marconi, P.; Brocker, T. Lentiviral-mediated transcriptional targeting of dendritic cells for induction of T cell tolerance in vivo J. Immunol. 2008, 181, 4495-4506
58. Ko, H.-J.; Chung, J. Y.; Nasa, Z.; Chan, J.; Siatskas, C.; Toh, B. H.; Alderuccio, F. Targeting MOG expression to dendritic cells delays onset of experimental autoimmune disease Autoimmunity 2011, 44 (3) 177-187
59. Chernajovsky, Y.; Gould, D. J.; Podhajcer, O. L. Gene therapy for autoimmune diseases: quo vadis? Nat. Rev. Immunol. 2004, 4, 800-811 (Pubitemid 39336296)
60. Skupsky, J.; Zhang, A. H.; Su, Y.; Scott, D. W. B-cell-delivered gene therapy induces functional T regulatory cells and leads to a loss of antigen-specific effector cells Mol. Ther. 2010, 18, 1527-1535
61. Han, G.; Li, Y.; Wang, J.; Wang, R.; Chen, G.; Song, L.; Xu, R.; Yu, M.; Wu, X.; Qian, J.; Shen, B. Active tolerance induction and prevention of autoimmune diabetes by immunogene therapy using recombinant adenoassociated virus expressing glutamic acid decarboxylase 65 peptide GAD(500-585) J. Immunol. 2005, 174, 4516-4524
62. Jaeckel, E.; von Boehmer, H.; Manns, M. P. Antigen-specific FoxP3-transduced T-cells can control established type 1 diabetes Diabetes 2005, 54, 306-310
63. Melo, M. E.; Qian, J.; El-Amine, M.; Agarwal, R. K.; Soukhareva, N.; Kang, Y.; Scott, D. W. Gene transfer of Ig-fusion proteins into B cells prevents and treats autoimmune diseases J. Immunol. 2002, 168, 4788-4795 (Pubitemid 34441388)
64. Dal Canto, R. A.; Costa, G.; Shaw, M. D.; Seroogy, C.; Nolan, G. P.; Fathman, C. G. Local delivery of cytokines by retrovirally transduced antigen-specific TCR+ hybridoma cells in experimental autoimmune encephalomyelitis Eur. Cytokine Network 1998, 9, 83-91 (Pubitemid 28508770)
65. Shaw, M. K.; Lorens, J. B.; Dhawan, A.; DalCanto, R.; Tse, H. Y.; Tran, A. B.; Bonpane, C.; Eswaran, S. L.; Brocke, S.; Sarvetnick, N.; Steinman, L.; Nolan, G. P.; Fathman, C. G. Local delivery of interleukin 4 by retrovirus-transduced T lymphocytes ameliorates experimental autoimmune encephalomyelitis J. Exp. Med. 1997, 185, 1711-1714 (Pubitemid 27203267)
66. Louie, K. A.; Weiner, L. P.; Du, J.; Kochounian, H. H.; Fling, S. P.; Wei, W.; McMillan, M. Cell-based gene therapy experiments in murine experimental autoimmune encephalomyelitis Gene Ther. 2005, 12, 1145-1153 (Pubitemid 41030620)
67. Xu, B.; Haviernik, P.; Wolfraim, L. A.; Bunting, K. D.; Scott, D. W. Bone marrow transplantation combined with gene therapy to induce antigen-specific tolerance and ameliorate EAE Mol. Ther. 2006, 13, 42-48 (Pubitemid 41763481)
68. Peters, T. R.; Bodine, D. M.; McDonagh, K. T.; Lovett-Racke, A.; McFarland, H. F.; McFarlin, D. E.; Nienhuis, A. W.; Racke, M. K. Retrovirus mediated gene transfer of the self antigen MBP into the bone marrow of mice alters resistance to experimental autoimmune encephalomyelitis J. Neuroimmunol. 2000, 103, 51-62 (Pubitemid 30058253)
69. Ally, B. A.; Hawley, T. S.; McKall-Faienza, K. J.; Kundig, T. M.; Oehen, S. U.; Pircher, H.; Hawley, R. G.; Ohashi, P. S. Prevention of autoimmune disease by retroviral-mediated gene therapy J. Immunol. 1995, 155, 5404-5408
70. Tian, C.; Bagley, J.; Kaye, J.; Iacomini, J. Induction of T cell tolerance to a protein expressed in the cytoplasm through retroviral-mediated gene transfer J. Gene Med. 2003, 5, 359-365 (Pubitemid 40309694)
71. 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)
72. Evans, G. L.; Morgan, R. A. Genetic induction of immune tolerance to human clotting factor VIII in a mouse model for hemophilia A Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 5734-5739 (Pubitemid 28224165)
73. Tian, C.; Bagley, J.; Cretin, N.; Seth, N.; Wucherpfennig, K. W.; Iacomini, J. Prevention of type 1 diabetes by gene therapy J. Clin. Invest. 2004, 114, 969-978 (Pubitemid 39578725)
74. Wong, W.; Billing, J. S.; Stranford, S. A.; Hyde, K.; Fry, J.; Morris, P. J.; Wood, K. J. Retroviral transfer of donor MHC class I or MHC class II genes into recipient bone marrow cells can induce operational tolerance to alloantigens in vivo Hum. Gene Ther. 2003, 14, 577-590 (Pubitemid 36438941)
75. Baranyi, U.; Linhart, B.; Pilat, N.; Gattringer, M.; Bagley, J.; Muehlbacher, F.; Iacomini, J.; Valenta, R.; Wekerle, T. Tolerization of a type 1 allergic response through transplantation of genetically modified hematopoietic stem cells J. Immunol. 2008, 180, 8168-8175