Biology of Blood and Marrow Transplantation
Volume 15, Issue 6 , Pages 662-670 , June 2009

Effect of Ex Vivo Culture of CD34+ Bone Marrow Cells on Immune Reconstitution of XSCID Dogs Following Allogeneic Bone Marrow Transplantation

  • Douglas R. Kennedy

      Affiliations

    • Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104
  • ,
  • Kyle McLellan

      Affiliations

    • Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104
  • ,
  • Peter F. Moore

      Affiliations

    • Department of Veterinary Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, CA 95616
  • ,
  • Paula S. Henthorn

      Affiliations

    • Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104
  • ,
  • Peter J. Felsburg

      Affiliations

    • Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104
    • Corresponding Author InformationCorrespondence and reprint requests: Dr. Peter J. Felsburg, V.M.D., PhD., School of Veterinary Medicine, University of Pennsylvania, 3900 Delancey St. Philadelphia, PA 19104, Telephone: 215-898-3527, Fax:215-898-3662.

Received 10 November 2008 ,Accepted 10 March 2009.

References 

  1. Krause DS, Fackler MJ, Civin CI, et al. CD34: structure, biology, and clinical utility. [see comments] Blood. 1996;87:1–13
  2. Bensinger WI, Clift R, Martin P, et al. Allogeneic peripheral blood stem cell transplantation in patients with advanced hematologic malignancies: a retrospective comparison with marrow transplantation. Blood. 1996;88:2794–2800
  3. Morel F, Szilvassy SJ, Travis M, et al. Primitive hematopoietic cells in murine bone marrow express the CD34 antigen. Blood. 1996;88:3774–3784
  4. Berenson RJ, Andrews RG, Bensinger WI, et al. Antigen CD34+ marrow cells engraft lethally irradiated baboons. J Clin Invest. 1988;81:951–955
  5. Andrews RG, Bryant EM, Bartelmez SH, et al. CD34+ marrow cells, devoid of T and B lymphocytes, reconstitute stable lymphopoiesis and myelopoiesis in lethally irradiated allogeneic baboons. Blood. 1992;80:1693–1701
  6. McSweeney PA, Rouleau KA, Wallace PM, et al. Characterization of monoclonal antibodies that recognize canine CD34. Blood. 1998;91:1977–1986
  7. Bruno B, Nash RA, Wallace PM, et al. CD34+ selected bone marrow grafts are radioprotective and establish mixed chimerism in dogs given high dose total body irradiation. Transplantation. 1999;68:338–344
  8. Hartnett BJ, Yao DP, Suter SE, et al. Transplantation of X-linked severe combined immunodeficient dogs with CD34+ bone marrow cells. Biol. Blood Marrow Transpl. 2002;8:188–197
  9. Aiuti A, Slavin S, Aker M, et al. Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science. 2002;296:2410–2413
  10. Cavazzana-Calvo M, Hacein-Bey S, de Saint Basile G, et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science. 2000;288:669–672
  11. Chinen J, Davis J, De Ravin SS, et al. Gene therapy improves immune function in preadolescents with X-linked severe combined immunodeficiency. Blood. 2007;110:67–73
  12. Gaspar HB, Bjorkegren E, Parsley K, et al. Successful reconstitution of immunity in ADA-SCID by stem cell gene therapy following cessation of PEG-ADA and use of mild preconditioning. Mol Ther. 2006;14:505–513
  13. Gaspar HB, Parsley KL, Howe S, et al. Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet. 2004;364:2181–2187
  14. Ginn SL, Curtin JA, Kramer B, et al. Treatment of an infant with X-linked severe combined immunodeficiency (SCID-X1) by gene therapy in Australia. Med J Aust. 2005;182:458–463
  15. Ott MG, Schmidt M, Schwarzwaelder K, et al. Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat Med. 2006;12:401–409
  16. Chang AH, Sadelain M. The genetic engineering of hematopoietic stem cells: the rise of lentiviral vectors, the conundrum of the LTR, and the promise of lineage-restricted vectors. Mol Ther. 2007;15:445–456
  17. Zielske SP, Gerson SL. Cytokines, including stem cell factor alone, enhance lentiviral transduction in nondividing human LTCIC and NOD/SCID repopulating cells. Mol Ther. 2003;7:325–333
  18. Brugger W, Scheding S, Ziegler B, et al. Ex vivo manipulation of hematopoietic stem and progenitor cells. Semin Hematol. 2000;37:42–49
  19. Carlo-Stella C, Tabilio A, Regazzi E, et al. Effect of chemotherapy for acute myelogenous leukemia on hematopoietic and fibroblast marrow progenitors. Bone Marrow Transplant. 1997;20:465–471
  20. Galotto M, Berisso G, Delfino L, et al. Stromal damage as consequence of high-dose chemo/radiotherapy in bone marrow transplant recipients. Exp Hematol. 1999;27:1460–1466
  21. O'Flaherty E, Sparrow R, Szer J. Bone marrow stromal function from patients after bone marrow transplantation. Bone Marrow Transplant. 1995;15:207–212
  22. Plett PA, Frankovitz SM, Wolber FM, et al. Treatment of circulating CD34(+) cells with SDF-1alpha or anti-CXCR4 antibody enhances migration and NOD/SCID repopulating potential. Exp Hematol. 2002;30:1061–1069
  23. Peters SO, Kittler EL, Ramshaw HS, et al. Murine marrow cells expanded in culture with IL-3, IL-6, IL-11, and SCF acquire an engraftment defect in normal hosts. Exp Hematol. 1995;23:461–469
  24. Varas F, Bernard A, Bueren JA. Restrictions in the stem cell function of murine bone marrow grafts after ex vivo expansion of short-term repopulating progenitors. Exp Hematol. 1998;26:100–109
  25. Brandt JE, Bartholomew AM, Fortman JD, et al. Ex vivo expansion of autologous bone marrow CD34(+) cells with porcine microvascular endothelial cells results in a graft capable of rescuing lethally irradiated baboons. Blood. 1999;94:106–113
  26. Abkowitz JL, Taboada MR, Sabo KM, et al. The ex vivo expansion of feline marrow cells leads to increased numbers of BFU-E and CFU-GM but a loss of reconstituting ability. Stem Cells. 1998;16:288–293
  27. Goan SR, Schwarz K, von Harsdorf S, et al. Fibroblasts retrovirally transfected with the human IL-3 gene initiate and sustain multilineage human hematopoiesis in SCID mice: comparison of CD34-enriched vs CD34-enriched and in vitro expanded grafts. Bone Marrow Transplant. 1996;18:513–519
  28. Guenechea G, Segovia JC, Albella B, et al. Delayed engraftment of nonobese diabetic/severe combined immunodeficient mice transplanted with ex vivo-expanded human CD34(+) cord blood cells. Blood. 1999;93:1097–1105
  29. Rebel VI, Tanaka M, Lee JS, et al. One-day ex vivo culture allows effective gene transfer into human nonobese diabetic/severe combined immune-deficient repopulating cells using high-titer vesicular stomatitis virus G protein pseudotyped retrovirus. Blood. 1999;93:2217–2224
  30. Demaison C, Brouns G, Blundell MP, et al. A defined window for efficient gene marking of severe combined immunodeficient-repopulating cells using a gibbon ape leukemia virus-pseudotyped retroviral vector. Hum Gene Ther. 2000;11:91–100
  31. Xu R, Reems JA. Umbilical cord blood progeny cells that retain a CD34+ phenotype after ex vivo expansion have less engraftment potential than unexpanded CD34+ cells. Transfusion. 2001;41:213–218
  32. Hows JM. Status of umbilical cord blood transplantation in the year 2001. J Clin Pathol. 2001;54:428–434
  33. Glimm H, Schmidt M, Fischer M, et al. Evidence of similar effects of short-term culture on the initial repopulating activity of mobilized peripheral blood transplants assessed in NOD/SCID-beta2microglobulin(null) mice and in autografted patients. Exp Hematol. 2005;33:20–25
  34. Rosler ES, Brandt JE, Chute J, et al. An in vivo competitive repopulation assay for various sources of human hematopoietic stem cells. Blood. 2000;96:3414–3421
  35. Felsburg PJ, Somberg RL, Hartnett BJ, et al. Canine X-linked severe combined immunodeficiency. A model for investigating the requirement for the common gamma chain (gamma c) in human lymphocyte development and function. Immunol Res. 1998;17:63–73
  36. Felsburg PJ, Somberg RL, Hartnett BJ, et al. Full immunologic reconstitution following nonconditioned bone marrow transplantation for canine X-linked severe combined immunodeficiency. Blood. 1997;90:3214–3221
  37. Henthorn PS, Somberg RL, Fimiani VM, et al. IL-2R gamma gene microdeletion demonstrates that canine X-linked severe combined immunodeficiency is a homologue of the human disease. Genomics. 1994;23:69–74
  38. Wagner JL, Burnett RC, DeRose SA, et al. Histocompatibility testing of dog families with highly polymorphic microsatellite markers. Transplantation. 1996;62:876–877
  39. Sandmaier BM, Fukuda T, Gooley T, et al. Dog leukocyte antigen-haploidentical stem cell allografts after anti-CD44 therapy and reduced-intensity conditioning in a preclinical canine model. Exp Hematol. 2003;31:168–175
  40. Fukuda T, Kerbauy FR, Gooley T, et al. Dog leukocyte antigen-haploidentical stem cell allografts after anti-CD44 therapy and nonmyeloablative conditioning in a preclinical canine model. Transplantation. 2006;82:332–339
  41. Ting-De Ravin SS, Kennedy DR, Naumann N, et al. Correction of canine X-linked severe combined immunodeficiency by in vivo retroviral gene therapy. Blood. 2006;107:3091–3097
  42. Cobbold S, Metcalfe S. Monoclonal antibodies that define canine homologues of human CD antigens: summary of the First International Canine Leukocyte Antigen Workshop (CLAW). Tissue Antigens. 1994;43:137–154
  43. Moore PF, Rossitto PV, Olivry T. Development of monoclonal antibodies to canine T cell receptor-γδ (TCR-γδ) and their utilization in the diagnosis of epidermotropic cutaneous T cell lymphoma. Vet. Pathol. 1994;31:597
  44. Kohn DB. Gene therapy for genetic haematological disorders and immunodeficiencies. J Intern Med. 2001;249:379–390
  45. Devine SM, Lazarus HM, Emerson SG. Clinical application of hematopoietic progenitor cell expansion: current status and future prospects. Bone Marrow Transplant. 2003;31:241–252
  46. Greiner DL, Hesselton RA, Shultz LD. SCID mouse models of human stem cell engraftment. Stem Cells. 1998;16:166–177
  47. Kerre TC, De Smet G, De Smedt M, et al. Adapted NOD/SCID model supports development of phenotypically and functionally mature T cells from human umbilical cord blood CD34(+) cells. Blood. 2002;99:1620–1626
  48. Vernau W, Hartnett BJ, Kennedy DR, et al. T cell repertoire development in XSCID dogs following nonconditioned allogeneic bone marrow transplantation. Biol Blood Marrow Transplant. 2007;13:1005–1015
  49. Hacein-Bey-Abina S, Le Deist F, Carlier F, et al. Sustained correction of X-linked severe combined immunodeficiency by ex vivo gene therapy. N Engl J Med. 2002;346:1185–1193
  50. Fischer A, Le Deist F, Hacein-Bey-Abina S, et al. Severe combined immunodeficiency. A model disease for molecular immunology and therapy. Immunol Rev. 2005;203:98–109
  51. Schmidt M, Hacein-Bey-Abina S, Wissler M, et al. Clonal evidence for the transduction of CD34+ cells with lymphomyeloid differentiation potential and self-renewal capacity in the SCID-X1 gene therapy trial. Blood. 2005;105:2699–2706
  52. Schwarzwaelder K, Howe SJ, Schmidt M, et al. Gammaretrovirus-mediated correction of SCID-X1 is associated with skewed vector integration site distribution in vivo. J Clin Invest. 2007;117:2241–2249
  53. Ferrebee JW, Lochte HL, Jaretzki A, et al. Successful marrow homograft in the dog after radiation. Surgery. 1958;43:516–520
  54. Thomas ED, Lochte HL, Cannon JH, et al. Supralethal whole body irradiation and isologous marrow transplantation in man. J Clin Invest. 1959;38:1709–1716
  55. Deeg HJ, Storb R, Weiden PL, et al. Cyclosporin A and methotrexate in canine marrow transplantation: engraftment, graft-versus-host disease, and induction of intolerance. Transplantation. 1982;34:30–35
  56. Yu C, Seidel K, Nash RA, et al. Synergism between mycophenolate mofetil and cyclosporine in preventing graft-versus-host disease among lethally irradiated dogs given DLA-nonidentical unrelated marrow grafts. Blood. 1998;91:2581–2587
  57. Storb R, Yu C, Wagner JL, et al. Stable mixed hematopoietic chimerism in DLA-identical littermate dogs given sublethal total body irradiation before and pharmacological immunosuppression after marrow transplantation. Blood. 1997;89:3048–3054

 Financial disclosure: See Acknowledgments on page 669.

PII: S1083-8791(09)00134-7

doi: 10.1016/j.bbmt.2009.03.014

Biology of Blood and Marrow Transplantation
Volume 15, Issue 6 , Pages 662-670 , June 2009