Introduction of a xenogeneic gene via hematopoietic stem cells leads to specific tolerance in a rhesus monkey model

Molecular Therapy

Volumn 1, Issue 6, 2000, Pages 533-544

  Heim, Dominik A ^a   Hanazono, Yutaka ^a   Giri, Neelam ^a   Wu, Tong ^a   Childs, Richard ^a   Sellers, Stephanie E ^a   Muul, Linda ^b   Agricola, Brian A ^a   Metzger, Mark E ^a   Donahue, Robert E ^a   Tisdale, John F ^c   Dunbar, Cynthia E ^a,d  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d NONE   (United States)

Author keywords

Gene therapy; Genetic vectors; Hematopoietic stem cell transplantation; Immune tolerance; Polymerase chain reaction

Indexed keywords

ANIMALIA; MACACA MULATTA;

KANAMYCIN KINASE; MESSENGER RNA; PRIMER DNA;

ANIMAL; ARTICLE; AUTOTRANSPLANTATION; BIOLOGICAL MODEL; BIOSYNTHESIS; BLOOD AUTOTRANSFUSION; GENE EXPRESSION; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE; LYMPHOCYTE TRANSFUSION; MACACA; METABOLISM; METHODOLOGY; NUCLEOTIDE SEQUENCE;

ANIMALS; BASE SEQUENCE; BLOOD TRANSFUSION, AUTOLOGOUS; DNA PRIMERS; GENE EXPRESSION; GENE THERAPY; GENETIC VECTORS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; IMMUNE TOLERANCE; KANAMYCIN KINASE; LYMPHOCYTE TRANSFUSION; LYMPHOCYTES; MACACA MULATTA; MODELS, BIOLOGICAL; RNA, MESSENGER; TRANSDUCTION, GENETIC; TRANSPLANTATION, AUTOLOGOUS;

EID: 0034199170     PISSN: 15250016     EISSN: None     Source Type: Journal    
DOI: 10.1006/mthe.2000.0072     Document Type: Article

References (50)

1. To, L. B., Haylock, D. N., Simmons, P. J., and Juttner, C. A. (1997). The biology and clinical uses of blood stem cells. Blood 89: 2233-2258.
2. Dunbar, C. E., and Emmons, R. V. B. (1994). Gene transfer into hematopoietic progenitor and stem cells: Progress and problems. Stem Cells 12: 563-576.
3. Naldini, L., Blömer, U., Gallay, P., Ory, D., Mulligan, R., Gage, R., Verma, I. M., and Trono, D. (1996). In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267.
4. Poeschla, E. M., Wong-Staal, F., and Looney, D. J. (1998). Efficient transduction of non-dividing human cells by feline immunodeficiency virus lentiviral vectors. Nat. Med. 4: 354-357.
5. Miyoshi, H., Smith, K. A., Mosier, D. E., Verma, I. M., and Torbett, B. E. (1999). Transduction of human CD34+ cells that mediate long-term engraftment of NOD/SCID mice by HIV vectors. Science 283: 682-686.
6. McCarthy, M. (1996). Gene therapy blocked by strong immune response. Lancet 347: 314.
7. Tripathy, S. K., Black, H. B., Goldwasser, E., and Leiden, J. M. (1996). Immune responses to transgene-encoded proteins limit the stability of gene expression after injection of replication-defective adenovirus vectors. Nat. Med. 2: 545-550.
8. Riddell, S. R., Elliott, M., Lewinsohn, D. A., Gilbert, M. J., Wilson, L., Manley, S. A., Lupton, S. D., Overell, R. W., Reynolds, T. C., Corey, L., and Greenberg, P. D. (1996). T-cell mediated rejection of gene-modified HIV-specific cytotoxic T lymphocytes in HIV-infected patients. Nat. Med. 2: 216-223.
9. Stripecke, R., del Carmen Villacres, M., Skelton, D. C., Satake, N., Halene, S., and Kohn, D. B. (1999). Immune response to green fluorescent protein: Implications for gene therapy. Gene Ther. 6: 1305-1312.
10. Sachs, D. H., Sykes, M., Greenstein, J. L., and Cosimi, A. B. (1995). Tolerance and xenograft survival. Nat. Med. 1: 969.
11. Nokolic, B., and Sykes, M. (1997). Bone marrow chimerism and transplantation tolerance. Curr. Opin. Immunol. 9: 634-640.
12. Hamawy, M. M., and Knechtle, S. J. (1998). Strategies for tolerance induction in non-human primates. Curr. Opin. Immunol. 10: 513-517.
13. Sykes, M., Sachs, D. H., Nienhuis, A. W., Pearson, D. A., Moulton, A. D., and Bodine, D. M. (1993). Specific prolongation of skin graft survival following retroviral transduction of bone marrow with an allogeneic major histocompatibility complex gene. Transplantation 55: 197-202.
14. Lim, B., Apperly, J. F., Orkin, S. H., and Williams, D. A. (1989). Long-term expression of human adenosine deaminase in mice transplanted with retrovirus-infected hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 86: 8892-8897.
15. Correll, P. H., Colilla, S., Dave, H. P., and Karlsson, S. (1992). High levels of human glucocerebrosidase activity in macrophages of long-term reconstituted mice after retroviral infection of hematopoietic stem cells. Blood 80: 331-336.
16. Correll, P. H., Kew, Y., Perry, L. K., Brady, R. O., Fink, J. K., and Karlsson, S. (1990). Expression of human glucocerebrosidase in long-term reconstituted mice following retroviral-mediated gene transfer into hematopoietic stem cells. Hum. Gene Ther. 1: 277-283.
17. Van Beusechem, V. W., Kukler, A., Heidt, P. J., and Valerio, D. (1992). Long-term expression of human adenosine deaminase in rhesus monkeys transplanted with retrovirus-infected bone-marrow cells. Proc. Natl. Acad. Sci. USA 89: 7640-7644.
18. Bodine, D. M., Moritz, T., Donahue, R. E., Luskey, B. D., Kessler, S. W., Martin, D. I. K., Orkin, S. H., Nienhuis, A. W., and Williams, D. A. (1993). Long term expression of a murine adenosine deaminase (ADA) gene in rhesus hematopoietic cells of multiple lineages following retroviral mediated gene transfer into CD34+ bone marrow cells. Blood 82: 1975-1980.
19. Xu, L. C., Karlsson, S., Byrne, E. R., Kluepfel-Stahl, S., Kessler, S. W., Agricola, B. A., Seller, S., Kirby, M., Dunbar, C. E., Brady, R. O., Nienhuis, A. W., and Donahue, R. E. (1995). Long-term in vivo expression of the human glucocerebrosidase gene in non-human primates using retroviral supernatant transduction protocols. Proc. Natl. Acad. Sci. USA 92: 4372-4376.
20. Lutzko, C., Kruth, S., Abrams-Ogg, A. C. G., Lau, K., Li, L., Clark, B. R., Ruedy, C., Nanji, S., Foster, R., Kohn, D., Shull, R., and Dubé, I. D. (1999). Genetically corrected autologous stem cells engraft, but host immune responses limit their utility in canine α-L-iduronidase deficiency. Blood 93: 1895-1905.
21. Van Beusechem, V. W., and Valerio, D. (1999). Gene transfer into hematopoietic stem cells of nonhuman primates. Hum. Gene Ther. 7: 1649-1668.
22. Pear, W. S., Nolan, G. P., Scott, M. L., and Baltimore, D. (1993). Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90: 8392-8396.
23. Migita, M., Medin, J. A., Pawliuk, R., Jacobson, S., Nagle, J. W., Anderson, S., Amiri, M., Humphries, R. K., and Karlsson, S. (1995). Selection of transduced CD34+ progenitors and enzymatic correction of cells from Gaucher patients, with bicistronic vectors. Proc. Natl. Acad. Sci. USA 92: 12075-12079.
24. Hanazono, Y., Dunbar, C. E., and Emmons, R. V. B. (1997). Green fluorescent protein retroviral vectors: Low titer and high recombination frequency suggest a selective disadvantage. Hum. Gene Ther. 8: 1313-1319.
25. Miller, A. D., and Buttimore, C. (1986). Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mot. Cell. Biol. 6: 2895-2902.
26. Cassel, A., Cottier-Fox, M., Doren, S., and Dunbar, C. E. (1993). Retroviral-mediated gene transfer into CD34-enriched human peripheral blood stem cells. Exp. Hematol. 21: 585-591.
27. Persons, D. A., Allay, J. A., Allay, E. R., Smeyne, R. J., Ashmun, R. A., Sorrentino, B. P., and Nienhuis, A. W. (1997). Retroviral-mediated transfer of the green fluorescent protein gene into murine hematopoietic cells facilitates scoring and selection of transduced pro-genitors in vitro and identification of genetically modified cells in vivo. Blood 90: 1777-1786.
28. Bunnell, B. A., Muul, L. M., Donahue, R. E., Blaese, R. M., and Morgan, R. A. (1995). High-efficiency retroviral-mediated gene transfer into human and nonhuman primate peripheral blood lymphocytes. Proc. Natl. Acad. Sci. USA 92: 7739-7743.
29. Donahue, R. E., Kirby, M. R., Metzger, M. E., Agricola, B. A., Sellers, S. E., and Cullis, H. M. (1996). Peripheral blood CD34+ cells differ from bone marrow CD34+ cells in Thy-1 expression and cell cycle status in nonhuman primates mobilized or nonmobilized with granulocyte colony-stimulating factor and/or stem cell factor. Blood 87: 1644-1653.
30. Tisdale, J. F., Hanazono, Y., Sellers, S. E., Agricola, B. A., Metzger, M. E., Donahue, R. E., and Dunbar, C. E. (1998). Ex vivo expansion of genetically marked rhesus peripheral blood progenitor cells results in diminished long-term repopulating ability. Blood 92: 1131-1141.
31. Wu, T., Kim, H. J., Sellers, S. E., Meade, K. E., Agricola, B. A., Metzger, M. E., Kato, I., Donahue, R. E., Dunbar, C. E., and Tisdale, J. F. (2000). Prolonged high-level detection of retrovirally marked hematopoietic cells in nonhuman primates after transduction of CD34+ progenitors using clinically feasible methods. Mol. Ther. 3: 285-293.
32. Hanenberg, H., Xiao, X. L., Dilloo, D., Hashino, K., Kato, I., and Williams, D. A. (1996). Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nat. Med. 2: 876-882.
33. Sellers, S., Tisdale, J. F., Bodine, D. M., Williams, D. A., Karlsson, S., Metzger, M., Donahue, R. E., and Dunbar, C. E. (1999). No discrepancy between in vivo gene marking efficiency assessed in peripheral blood populations compared to bone marrow progenitors or CD34+ cells. Hum. Gene Ther. 10: 633-640.
34. Hanazono, Y., Brown, K. E., Handa, A., Metzger, M. E., Heim, D., Kurtzman, G. J., Donahue, R. E., and Dunbar, C. E. (1999). In vivo marking of rhesus monkey lymphocytes by adeno-associated viral vectors: Direct comparison with retroviral vectors. Blood 94: 2263-2270.
35. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W., and Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science 263: 802-805.
36. Selvaggi, T. A., Walker, R. E., and Fleisher, T. A. (1997). Development of antibodies to fetal calf serum with arthus-like reactions in human immunodeficiency virus-infected patients given syngeneic lymphocyte infusions. Blood 89: 776-779.
37. Bunnell, B. A., Metzger, M., Byrne, E., Morgan, R. A., and Donahue, R. E. (1997). Efficient in vivo marking of primary CD4+ T lymphocytes in non-human primates using a gibbon ape leukemia virus-derived retroviral vector. Blood 89: 1987-1995.
38. Wu, T., Bloom, M. L., Yu, J.-M., Tisdale, J. F., and Dunbar, C. E. (1998). Murine bone marrow expressing the neomycin resistance gene has no competitive disadvantage assessed in vivo. Hum. Gene Ther. 9: 1157-1164.
39. Challita, P.-M., and Kohn, D. B. (1994). Lack of expression from a retroviral vector after transduction of murine hematopoietic stem cells is associated with methylation in vivo. Proc. Natl. Acad. Sci. USA 91: 2567-2571.
40. Robbins, P. B., Skelton, D. C., Yu, X. J., Halene, S., Leonard, E. H., and Kohn, D. B. (1998). Consistent, persistent expression from modified retroviral vectors in murine hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 95: 10182-10187.
41. Laker, C., Meyer, J., Schopen, A., Friel, J., Heberlein, C., Ostertag, W., and Stocking, C. (1999). Host cis-mediated extinction of a retrovirus permissive for expression in embryonal stem cells during differentiation, J. Virol. 72: 339-348.
42. Koopmann, J. O., Haemmerling, G. J., and Momburg, F. (1997). Generation, intracellular transport and loading of peptides associated with MHC class I molecules. Curr. Opin. Immunol. 9: 80-88.
43. Ramsdell, F., and Fowlkes, B. J. (1990). Clonal deletion versus clonal anergy: The role of the thymus in inducing self tolerance. Science 248: 1342-1348.
44. Sachs, D. H., Bodine, D. M., Moulton, A. D., Pearson, D. A., Nienhuis, A. W., and Sykes, M. (1993). Tolerance induction using autologous bone marrow modified with an allogeneic class I MHC gene. Transplant. Proc. 25: 348-349.
45. Ierino, F. L., Gojo, S., Banerjee, P. T., Giovini, M., Xu, X., Gere, J., Kaynor, C., Awwad, M., Monroy, R., Rembert, J., Hatch, T., Foley, A., Kozlowski, T., Yamada, K., Neethling, F. A., Fishman, J., Bailin, M., Spitzer, T. R., Cooper, D. K. C., Cosimi, A. B., LeGuerin, C., and Sachs, D. H. (1999). Transfer of swine major histocompatibility complex class II genes into autologous bone marrow cells of baboons for the induction of tolerance across xeno-geneic barriers. Transplantation 67: 1119-1128.
46. Kavanaugh, M. P., Miller, D. G., Zhang, W., Lawa, W., Kozak, S. L., Kabat, D., and Miller, A. D. (1994). Cell-surface receptors for gibbon ape leukemia virus and amphotropic murine retrovirus and inducible sodium-dependent phosphate symporters. Proc. Natl. Acad. Sci. USA 91: 7071-7075.
47. Hohaus, S., Horvath, C., Nierhoff, D., Voso, M. T., Golling, M., Klar, E., Mytilineos, J., Opelz, G., Ho, A. D., and Haas, R. (1998). Microchimerism in bone marrow-derived CD34+ cells of patients after liver transplantation. Blood 92 (Suppl. 1): 132a.
48. Taniguchi, H., Toyoshima, T., Fukao, K., and Nakauchi, H. (1996). Presence of hematopoietic stem cells in the adult liver. Nat. Med. 2: 198-203.
49. Rosenzweig, M., MacVittie, T. J., Harper, D., Hempel, D., Glickman, R. L., Johnson, R. P., Farese, A. M., Whiting-Theobald, N., Linton, G. F., Yamasaki, G., Jordan, C. T., and Malech, H. L. (1999). Efficient and durable gene marking of hematopoietic progenitor cells in nonhuman primates after nonablative conditioning. Blood 94: 2271-2286.
50. Huhn, R. D., Tisdale, J. F., Agricola, B., Metzger, M. E., Donahue, R. E., and Dunbar, C. E. (1999). Retroviral marking and transplantation of rhesus hematopoietic cells by non-myeloablative conditioning. Hum. Gene Ther. 10: 1783-1790.