Reversal of autoimmune disease in lupus-prone New Zealand black/New Zealand white mice by nonmyeloablative transplantation of purified allogeneic hematopoietic stem cells

Blood

Volumn 110, Issue 4, 2007, Pages 1370-1378

  Smith Berdan, Stephanie ^a   Gille, Daphne ^a   Weissman, Irving L ^b   Christensen, Julie L ^a  

^a Cellerant Therapeutics   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CELL SURVIVAL; CHIMERA; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; FEMALE; FLOW CYTOMETRY; LUPUS LIKE SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEINURIA; THYMUS;

EID: 34548040947     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-03-081497     Document Type: Article

References (75)

1. Zampieri S, Iaccarino L, Ghirardello A, et al. Systemic lupus erythematosus, atherosclerosis, and autoantibodies. Ann N Y Acad Sci. 2005;1051:351-361.
2. Harley JB, Kelly JA. Genetic basis of systemic lupus erythematosus: a review of the unique genetic contributions in African Americans. J Natl Med Assoc. 2002;94:670-677.
3. Kelly JA, Moser KL, Harley JB. The genetics of systemic lupus erythematosus: putting the pieces together. Genes Immun. 2002;3(Suppl 1):S71-S85.
4. Tsao BP, Cantor RM, Grossman JM, et al. Linkage and interaction of loci on 1q23 and 16q12 may contribute to susceptibility to systemic lupus erythematosus. Arthritis Rheum. 2002;46:2928-2936.
5. James JA, Neas BR, Moser KL, et al. Systemic lupus erythematosus in adults is associated with previous Epstein-Barr virus exposure. Arthritis Rheum. 2001;44:1122-1126.
6. James JA, Harley JB, Scofield RH. Role of viruses in systemic lupus erythematosus and Sjögren syndrome. Curr Opin Rheumatol. 2001;13:370-376.
7. Mok CC, Lau CS. Pathogenesis of systemic lupus erythematosus. J Clin Pathol. 2003;56:481-490.
8. Gaipl US, Kuhn A, Sheriff A, et al. Clearance of apoptotic cells in human SLE. Curr Dir Autoimmun. 2006;9:173-187.
9. Agnello V. Association of systemic lupus erythematosus and SLE-like syndromes with hereditary and acquired complement deficiency states. Arthritis Rheum. 1978;21:S146-152.
10. Zonana-Nacach A, Barr SG, Magder LS, Petri M. Damage in systemic lupus erythematosus and its association with corticosteroids. Arthritis Rheum. 2000;43:1801-1808.
11. Brodsky RA, Petri M, Smith BD, et al. Immunoablative high-dose cyclophosphamide without stem-cell rescue for refractory, severe autoimmune disease. Ann Intern Med. 1998;129:1031-1035.
12. Burt RK, Traynor AE, Pope R, et al. Treatment of autoimmune disease by intense immunosuppressive conditioning and autologous hematopoietic stem cell transplantation. Blood. 1998;92:3505-3514.
13. Petri M, Jones RJ, Brodsky RA. High-dose cyclophosphamide without stem cell transplantation in systemic lupus erythematosus. Arthritis Rheum. 2003;48:166-173.
14. Tyndall A, Daikeler T. Autologous hematopoietic stem cell transplantation for autoimmune diseases. Acta Haematol. 2005;114:239-247.
15. Burt RK, Traynor A, Statkute L, et al. Nonmyeloablative hematopoietic stem cell transplantation for systemic lupus erythematosus. JAMA. 2006;295:527-535.
16. Marmont AM. Stem cell transplantation for autoimmune disorders. Coincidental autoimmune disease in patients transplanted for conventional indications. Best Pract Res Clin Haematol. 2004;17:223-232.
17. de Buys P, Khanna D, Furst DE. Hemopoietic stem cell transplantation in rheumatic diseases - an update. Autoimmun Rev. 2005;4:442-449.
18. Bowers E, Tamaki S, Coward A, Kaneshima H, Chao CC. Differing functional recovery of donor-derived immune cells after purified haploidentical and fully mismatched hematopoietic stem cell transplantation in mice. Exp Hematol. 2000;28:1481-1489.
19. Beilhack GF, Scheffold YC, Weissman IL, et al. Purified allogeneic hematopoietic stem cell transplantation blocks diabetes pathogenesis in NOD mice. Diabetes. 2003;52:59-68.
20. Beilhack GF, Landa RR, Masek MA, Shizuru JA. Prevention of type 1 diabetes with major histocompatibility complex-compatible and nonmarrow ablative hematopoietic stem cell transplants. Diabetes. 2005;54:1770-1779.
21. Shizuru JA, Jerabek L, Edwards CT, Weissman IL. Transplantation of purified hematopoietic stem cells: requirements for overcoming the barriers of allogeneic engraftment. Biol Blood Marrow Transplant. 1996;2:3-14.
22. Shizuru JA, Weissman IL, Kernoff R, Masek M, Scheffold YC. Purified hematopoietic stem cell grafts induce tolerance to alloantigens and can mediate positive and negative T cell selection. Proc Natl Acad Sci U S A. 2000;97:9555-9560.
23. Uchida N, Tsukamoto A, He D, Friera AM, Scollay R, Weissman IL. High doses of purified stem cells cause early hematopoietic recovery in syngeneic and allogeneic hosts. J Clin Invest. 1998;101:961-966.
24. Weissman IL. Translating stem and progenitor cell biology to the clinic: barriers and opportunities. Science. 2000;287:1442-1446.
25. Wang BY, Cherry El-Badri NS, Good RA. Prevention of development of autoimmune disease in BXSB mice by mixed bone marrow transplantation. Proc Natl Acad Sci U S A. 1997;94:12065-12069.
26. Karussis DM, Vourka-Karussis U, Lehmann D, et al. Prevention and reversal of adoptively transferred, chronic relapsing experimental autoimmune encephalomyelitis with a single high dose cytoreductive treatment followed by syngeneic bone marrow transplantation. J Clin Invest. 1993;92:765-772.
27. Guo Z, Wu T, Sozen H, et al. A substantial level of donor hematopoietic chimerism is required to protect donor-specific islet grafts in diabetic NOD mice. Transplantation. 2003;75:909-915.
28. Katagiri T, Cohen PL, Eisenberg RA. The lpr gene causes an intrinsic T cell abnormality that is required for hyperproliferation. J Exp Med. 1988;167:741-751.
29. Wang B, Yamamoto Y, El-Badri NS, Good RA. Effective treatment of autoimmune disease and progressive renal disease by mixed bone-marrow transplantation that establishes a stable mixed chimerism in BXSB recipient mice. Proc Natl Acad Sci U S A. 1999;96:3012-3016.
30. El-Badri NS, Wang BY, Steele A, et al. Successful prevention of autoimmune disease by transplantation of adequate number of fully allogeneic hematopoietic stem cells. Transplantation. 2000;70:870-877.
31. Jones OY, Steele A, Jones JM, et al. Nonmyeloablative bone marrow transplantation of BXSB lupus mice using fully matched allogeneic donor cells from green fluorescent protein transgenic mice. J Immunol. 2004;172:5415-5419.
32. Lambert PH, Dixon FJ. Pathogenesis of the glomerulonephritis of NZB/W mice. J Exp Med. 1968;127:507-522.
33. Andrews BS, Eisenberg RA, Theofilopoulos AN, et al. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med. 1978;148:1198-1215.
34. Yoshida S, Dorshkind K, Gershwin ME. Hemopoietic cell dysfunction in murine lupus. Clin Exp Rheumatol. 1987;5:79-87.
35. Kono DH, Burlingame RW, Owens DG, et al. Lupus susceptibility loci in New Zealand mice. Proc Natl Acad Sci U S A. 1994;91:10168-10172.
36. Vyse TJ, Kotzin BL. Genetic susceptibility to systemic lupus erythematosus. Annu Rev Immunol. 1998;16:261-292.
37. Tsao BP, Wallace DJ. Genetics of systemic lupus erythematosus. Curr Opin Rheumatol. 1997;9:377-379.
38. Tsao BP, Cantor RM, Kalunian KC, et al. Evidence for linkage of a candidate chromosome 1 region to human systemic lupus erythematosus. J Clin Invest. 1997;99:725-731.
39. Becker KG, Simon RM, Bailey-Wilson JE, et al. Clustering of non-major histocompatibility complex susceptibility candidate loci in human autoimmune diseases. Proc Natl Acad Sci U S A. 1998;95:9979-9984.
40. Reininger L, Winkler TH, Kalberer CP, Jourdan M, Melchers F, Rolink AG. Intrinsic B cell defects in NZB and NZW mice contribute to systemic lupus erythematosus in (NZB X NZW) F1 mice. J Exp Med. 1996;184:853-861.
41. Reininger L, Santiago ML, Takahashi S, Fossati L, Izui S. T helper cell subsets in the pathogenesis of systemic lupus erythematosus. Ann Med Interne (Paris). 1996;147:467-471.
42. Jongstra-Bilen J, Vukusic B, Boras K, Wither JE. Resting B cells from autoimmune lupus-prone New Zealand Black and (New Zealand black New Zealand white) F1 mice are hyper-responsive to T cell-derived stimuli. J Immunol. 1997;159:5810-5820.
43. Wang Y, Hu Q, Madri JA, Rollins SA, Chodera A, Matis LA. Amelioration of lupus-like autoimmune disease in NZB/WF1 mice after treatment with a blocking monoclonal antibody specific for complement component C5. Proc Natl Acad Sci U S A. 1996;93:8563-8568.
44. Wofsy D, Seaman WE. Successful treatment of autoimmunity in NZB/NZW F1 mice with monoclonal antibody to L3T4. J Exp Med. 1985;161:378-391.
45. Adkins B, Gandour D, Strober S, Weissman I. Total lymphoid irradiation leads to transient depletion of the mouse thymic medulla and persistent abnormalities among medullary stromal cells. J Immunol. 1988;140:3373-3379.
46. Ito T, Ishikawa S, Sato T, et al. Defective B1 cell homing to the peritoneal cavity and preferential recruitment of B1 cells in the target organs in a murine model for systemic lupus erythematosus. J Immunol. 2004;172:3628-3634.
47. Farinas MC, Adkins B, Stall AM, Weissman I, Strober S. B cell infiltration of the thymic medulla in New Zealand black, New Zealand white, and (New Zealand black X New Zealand white) F1 mice. Effect of total lymphoid irradiation. Arthritis Rheum. 1990;33:702-710.
48. Kaplan HS, Brown MB, Hirsch BB, Carnes WH. Indirect induction of lymphomas in irradiated mice. II. Factor of irradiation of the host. Cancer Res. 1956;16:426-428.
49. Lieberman M, Hansteen GA, McCune JM, Scott ML, White JH, Weissman IL. Indirect induction of radiation lymphomas in mice. Evidence for a novel, transmissible leukemogen. J Exp Med. 1987;166:1883-1893.
50. Theofilopoulos AN, Dixon FJ. Murine models of systemic lupus erythematosus. Adv Immunol. 1985;37:269-390.
51. Hayakawa K, Hardy RR, Herzenberg LA. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J Exp Med. 1985;161:1554-1568.
52. Hayakawa K, Hardy RR, Herzenberg LA. Peritoneal Ly-1 B cells: genetic control, autoantibody production, increased lambda light chain expression. Eur J Immunol. 1986;16:450-456.
53. Kantor AB, Stall AM, Adams S, Herzenberg LA. Differential development of progenitor activity for three B-cell lineages. Proc Natl Acad Sci U S A. 1992;89:3320-3324.
54. Mercolino TJ, Locke AL, Afshari A, et al. Restricted immunoglobulin variable region gene usage by normal Ly-1 (CD5+) B cells that recognize phosphatidyl choline. J Exp Med. 1989;169:1869-1877.
55. Hayakawa K, Hardy RR, Parks DR, Herzenberg LA. The 'Ly-1 B' cell subpopulation in normal immunodefective, and autoimmune mice. J Exp Med. 1983;157:202-218.
56. Pennell CA, Mercolino TJ, Grdina TA, Arnold LW, Haughton G, Clarke SH. Biased immunoglobulin variable region gene expression by Ly-1 B cells due to clonal selection. Eur J Immunol. 1989;19:1289-1295.
57. Murakami M, Yoshioka H, Shirai T, Tsubata T, Honjo T. Prevention of autoimmune symptoms in autoimmune-prone mice by elimination of B-1 cells. Int Immunol. 1995;7:877-882.
58. Ishikawa S, Sato T, Abe M, et al. Aberrant high expression of B lymphocyte chemokine (BLC/CXCL13) by C11b+CD11c+ dendritic cells in murine lupus and preferential chemotaxis of B1 cells towards BLC. J Exp Med. 2001;193:1393-1402.
59. Hoyer BF, Moser K, Hauser AE, et al. Short-lived plasmablasts and long-lived plasma cells contribute to chronic humoral autoimmunity in NZB/W mice. J Exp Med. 2004;199:1577-1584.
60. Tyndall A. Allogeneic bone marrow transplantation for autoimmune disease - the jury is still out. J Rheumatol. 2006;33:644-646.
61. Tyndall A, Saccardi R. Haematopoietic stem cell transplantation in the treatment of severe autoimmune disease: results from phase I/II studies, prospective randomized trials and future directions. Clin Exp Immunol. 2005;141:1-9.
62. Jayne D, Tyndall A. Autologous stem cell transplantation for systemic lupus erythematosus. Lupus. 2004;13:359-365.
63. Traynor AE, Barr WG, Rosa RM, et al. Hematopoietic stem cell transplantation for severe and refractory lupus. Analysis after five years and fifteen patients. Arthritis Rheum. 2002;46:2917-2923.
64. Burt RK, Fassas A, Snowden J, et al. Collection of hematopoietic stem cells from patients with autoimmune diseases. Bone Marrow Transplant. 2001;28:1-12.
65. Openshaw H, Stuve O, Antel JP, et al. Multiple sclerosis flares associated with recombinant granulocyte colony-stimulating factor. Neurology. 2000;54:2147-2150.
66. Statkute L, Verda L, Oyama Y, et al. Mobilization, harvesting and selection of peripheral blood stem cells in patients with autoimmune diseases undergoing autologous hematopoietic stem cell transplantation. Bone Marrow Transplant. 2007;39:317-329.
67. Burt RK, Marmont A, Oyama Y, et al. Randomized controlled trials of autologous hematopoietic stem cell transplantation for autoimmune diseases: the evolution from myeloablative to lymphoablative transplant regimens. Arthritis Rheum. 2006;54:3750-3760.
68. Weinberg K, Blazar BR, Wagner JE, et al. Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation. Blood. 2001;97:1458-1466.
69. Lapp WS, Ghayur T, Mendes M, Seddik M, Seemayer TA. The functional and histological basis for graft-versus-host-induced immunosuppression. Immunol Rev. 1985;88:107-133.
70. Seddik M, Seemayer TA, Lapp WS. The graft-versus-host reaction and immune function. I. T helper cell immunodeficiency associated with graft-versus-host-induced thymic epithelial cell damage. Transplantation. 1984;37:281-286.
71. Ghayur T, Seemayer TA, Xenocostas A, Lapp WS. Complete sequential regeneration of graft-vs-host-induced severely dysplastic thymuses. Implications for the pathogenesis of chronic graftvs-host disease. Am J Pathol. 1988;133:39-46.
72. Hollander GA, Widmer B, Burakoff SJ. Loss of normal thymic repertoire selection and persistence of autoreactive T cells in graft vs host disease. J Immunol. 1994;152:1609-1617.
73. van den Brink MR, Moore E, Ferrara JL, Burakoff SJ. Graft-versus-host- disease-associated thymic damage results in the appearance of T cell clones with antihost reactivity. Transplantation. 2000;69:446-449.
74. Tivol E, Komorowski R, Drobyski WR. Emergent autoimmunity in graft-versus-host disease. Blood. 2005;105:4885-4891.
75. Fukushi N, Arase H, Wang B, et al. Thymus: a direct target tissue in graft-versus-host reaction after allogeneic bone marrow transplantation that results in abrogation of induction of self-tolerance. Proc Natl Acad Sci U S A. 1990;87:6301-6305.