Quiescent subpopulations of human CD34-positive hematopoietic stem cells are preferred targets for stable recombinant adeno-associated virus type 2 transduction

Human Gene Therapy

Volumn 18, Issue 7, 2007, Pages 614-626

  Paz, Helicia ^a   Wong, Christie A ^a   Li, Wei ^a   Santat, Leah ^a   Wong, K K ^a   Chatterjee, Saswati ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CD38 ANTIGEN; PARVOVIRUS VECTOR; TYRPHOSTIN;

ARTICLE; CD34 SELECTION; CELL SUBPOPULATION; CLONOGENESIS; CONTROLLED STUDY; EPISOME; GENETIC TRANSDUCTION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; TRANSGENE; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME; VIRUS RECOMBINANT;

ANTIGENS, CD34; BONE MARROW CELLS; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; DEPENDOVIRUS; G0 PHASE; GENE EXPRESSION; GENE THERAPY; GENETIC VECTORS; HEMATOPOIETIC STEM CELLS; HUMANS; RECOMBINANT PROTEINS; TRANSDUCTION, GENETIC; TRANSGENES;

ADENO-ASSOCIATED VIRUS - 2;

EID: 34547508637     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2006.188     Document Type: Article

References (69)

1. ARRUDA, V.R., SCHUETTRUMPF, J., HERZOG, R.W., NICHOLS, T.C., ROBINSON, N., LOTFI, Y., MINGOZZI, F., XIAO, W., COUTO, L.B., and HIGH, K.A. (2004). Safety and efficacy of factor IX gene transfer to skeletal muscle in murine and canine hemophilia B models by adeno-associated viral vector serotype 1. Blood 103, 85-92.
2. ARRUDA, V.R., STEDMAN, H.H., NICHOLS, T.C., HASKINS, M.E., NICHOLSON, M., HERZOG, R.W., COUTO, L.B., and HIGH, K.A. (2005). Regional intravascular delivery of AAV-2-F.IX to skeletal muscle achieves long-term correction of hemophilia B in a large animal model. Blood 105, 3458-3464.
3. BELL, P., WANG, L., LEBHERZ, C., FLIEDER, D.B., BOVE, M.S., WU, D., GAO, G.P., WILSON, J.M., and WIVEL, N.A. (2005). No evidence for tumorigenesis of AAV vectors in a large-scale study in mice. Mol. Ther. 12, 299-306.
4. S/S mice. Genes Dev. 16, 2237-2251.
5. BERNS, K.I., and GIRAUD, C. (1996). Biology of adeno-associated virus. Curr. Top. Microbiol. Immunol. 218, 1-23.
6. BERTONCELLO, I., and WILLIAMS, B. (2004). Hematopoietic stem cell characterization by Hoechst 33342 and rhodamine 123 staining. Methods Mol. Biol. 263, 181-200.
7. BRADFORD, G.B., WILLIAMS, B., ROSSI, R., and BERTON-CELLO, I. (1997). Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp. Hematol. 25, 445-453.
8. CALMELS, B., FERGUSON, C., LAUKKANEN, M.O. ADLER, R., FAULHABER, M., KIM, H.J., SELLERS, S., HEMATTI, P., SCHMIDT, M., VON KALLE, C., AKAGI, K., DONAHUE, R.E., and DUNBAR, C.E. (2005). Recurrent retroviral vector integration at the MdsI/Evi1 locus in nonhuman primate hematopoietic cells. Blood 106, 2530-2533.
9. CHATTERJEE, S., and WONG, K.K. (1993). Adeno-associated viral vectors for the delivery of antisense RNA. Methods 5, 51-59.
10. CHATTERJEE, S., and WONG, K.K. (2000). Adeno-associated viral vectors for the delivery of ribozymes. In Intracellular Ribozyme Applications: Principles and Protocols. J.J. Rossi and L. Couture, eds. (Horizon Scientific Press, Norwich, U.K.) pp. 189-215.
11. CHATTERJEE, S., JOHNSON, P.R., and WONG, K.K., Jr. (1992). Dual-target inhibition of HIV-1 in vitro by means of an adeno-associated virus antisense vector. Science 258, 1485-1488.
12. CHATTERJEE, S., LI, W., WONG, C.A., FISHER-ADAMS, G., LU, D., GUHA, M., MACER, J.A., FORMAN, S.J., and WONG, K.K., Jr. (1999). Transduction of primitive human marrow and cord blood-derived hematopoietic progenitor cells with adeno-associated virus vectors. Blood 93, 1882-1894.
13. DUAN, D., SHARMA, P., YANG, J., YUE, Y., DUDUS, L., ZHANG, Y., FISHER, K.J., and ENGELHARDT, J.F. (1998). Circular intermediates of recombinant adeno-associated virus have defined structural characteristics responsible for long-term episomal persistence in muscle tissue. J. Virol. 72, 8568-8577.
14. DUNBAR, C.E., COTTLER-FOX, M., O'SHAUGHNESSY, J.A., DOREN, S., CARTER, C., BERENSON, R., BROWN, S., MOEN, R.C., GREENBLATT, J., STEWART, F.M., LEITMAN, S.F., WILSON, W.H., COWAN, K., YOUNG, N.S., and NIENHUIS, A.W. (1995). Retrovirally marked CD34-enriched peripheral blood and bone marrow cells contribute to long-term engraftment after autologous transplantation. Blood 85, 3048-3057.
15. EINERHAND, M.P., ANTONIOU, M., ZOLUTUKHIN, S., MUZYCZKA, N., BERNS, K.I., GROSVELD, F., and VALERIO, D. (1995). Regulated high-level human β-globin gene expression in erythroid cells following recombinant adeno-associated virus-mediated gene transfer. Gene Ther. 2, 336-243.
16. FERRARI, F.K., SAMULSKI, T., SHENK, T., and SAMULSKI, R.J. (1996). Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J. Virol. 70, 3227-3234.
17. FISHER, K.J., GAO, G.P., WEITZMAN, M.D., DEMATTEO, R., BURDA, J.F., and WILSON, J.M. (1996). Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J. Virol. 70, 520-532.
18. + human hematopoietic progenitor cells after transduction. Blood 88, 492-504.
19. FLOTTE, T.R. (2005). Adeno-associated virus-based gene therapy for inherited disorders. Pediatr. Res. 58, 1143-1147.
20. FLOTTE, T.R., AFIONE, S.A., and ZEITLIN, P.L. (1994). Adeno-associated virus vector gene expression occurs in nondividing cells in the absence of vector DNA integration. Am. J. Respir. Cell Mol. Biol. 11, 517-521.
21. FURUKAWA, Y. (1998). Cell cycle regulation of hematopoietic stem cells. Hum. Cell 11, 81-92.
22. GAO, G., VANDENBERGHE, L.H., ALVIRA, M.R., LU, Y., CALCEDO, R., ZHOU, X., and WILSON, J.M. (2004). Clades of adenoassociated viruses are widely disseminated in human tissues. J. Virol. 78, 6381-6388.
23. + cells in non-obese diabetic/severe combined immune-deficient mice. Blood 92, 2641-2649.
24. GOUSSETIS, E., THEODOSAKI, M., PATERAKIS, G., STEFANAKI, K., TSECOURA, C., PAPASSARANDIS, C., and GRAPHAKOS, S. (2003). Kinetics of quiescent cord blood stem/progenitor cells with high proliferative potential in stem-cell expansion culture. Cytotherapy 5, 500-508.
25. HACEIN-BEY-ABINA, S., VON KALLE, C., SCHMIDT, M., McCORMACK, M.P., WULFFRAAT, N., LEBOULCH, P., LIM, A., OSBORNE, C.S., PAWLIUK, R., MORILLON, E., SORENSEN, R., FORSTER, A., FRASER, P., COHEN, J.I., DE SAINT, B.G., ALEXANDER, I., WINTERGERST, U., FREBOURG, T., AURIAS, A., STOPPA-LYONNET, D., ROMANA, S., RADFORDWEISS, I., GROSS, F., VALENSI, F., DELABESSE, E., MACINTYRE, E., SIGAUX, F., SOULIER, J., LEIVA, L.E., WISSLER, M., PRINZ, C., RABBITTS, T.H., LE DEIST, F., FISCHER, A., and CAVAZZANA-CALVO, M. (2003). LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302, 415-419.
26. HANSEN, J., QING, K., KWON, H.J., MAH, C., and SRIVASTAVA, A. (2000). Impaired intracellular trafficking of adeno-associated virus type 2 vectors limits efficient transduction of murine fibroblasts. J. Virol. 74, 992-996.
27. HANSEN, J., QING, K., and SRIVASTAVA, A. (2001). Adeno-associated virus type 2-mediated gene transfer: Altered endocytic processing enhances transduction efficiency in murine fibroblasts. J. Virol. 75, 4080-4090.
28. HAO, Q.L., THIEMANN, F.T., PETERSEN, D., SMOGORZEWSKA, E.M., and CROOKS, C.M. (1996). Extended long-term culture reveals a highly quiescent and primitive human hematopoietic progenitor population. Blood 88, 3306-3313.
29. HARDING, T.C., KOPRIVNIKAR, K.E., TU, G.H., ZAYEK, N., LEW, S., SUBRAMANIAN, A., SIVAKUMARAN, A., FREY, D., HO, K., VANROEY, M.J., NICHOLS, T.C., BELLINGER, D.A., YENDLURI, S., WAUGH, J., McARTHUR, J., VERES, G., and DONAHUE, B.A. (2004). Intravenous administration of an AAV-2 vector for the expression of factor IX in mice and a dog model of hemophilia B. Gene Ther. 11, 204-213.
30. HIRT, B. (1967). Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26, 365-369.
31. HU, X., MOSCINSKI, L.C., HILL, B.J., CHEN, Q., WU, J., FISHER, A.B., and ZUCKERMAN, K.S. (1998). Characterization of a unique factor-independent variant derived from human factor-dependent TF-1 cells: A transformed event. Leuk. Res. 22, 817-826.
32. lo/sp primitive hemopoietic stem cells revealed by pyronin Y. Exp. Hematol. 29, 1109-1116.
33. KESSLER, P.D., PODSAKOFF, C.M., CHEN, X., McQUISTON, S.A., COLOSI, P.C., MATELIS, L.A., KURTZMAN, G.J., and BYRNE, B.J. (1996). Gene delivery to skeletal muscle results in sustained expression and systemic delivery of a therapeutic protein. Proc. Natl. Acad. Sci. U.S.A. 93, 14082-14087.
34. KIM, S.J., NAM, Y.R., SHIN, O., CHOI, J., LEE, B., CHANG, J.W., KWON, Y.K., PARK, K., and LEE, H. (2005). Treatment with hydroxyurea and tyrophostin-1 significantly improves the transduction efficiency of recombinant adeno-associated viruses in human cancer cells. Oncol. Rep. 14, 1475-1479.
35. + cells from the bone marrow of human immunodeficiency virus-1-infected children. Blood 94, 368-371.
36. KOOTSTRA, N.A., ZWART, B.M., and SCHUITEMAKER, H. (2000). Diminished human immunodeficiency virus type 1 reverse transcription and nuclear transport in primary macrophages arrested in early d phase of the cell cycle. J. Virol. 74, 1712-1717.
37. 1b phase of the cell cycle is required for completion of human immunodeficiency virus type 1 reverse transcription in T cells. J. Virol. 72, 3161-3168.
38. 0 lymphocytes. J. Virol. 73, 6526-6532.
39. 0. Blood 90, 658-668.
40. LEEMHUIS, T., YODER, M.C., GRIGSBY, S., AGUERO, B., EDER, P., and SROUR, E.F. (1996). Isolation of primitive human bone marrow hematopoietic progenitor cells using Hoechst 33342 and Rhodamine 123. Exp. Hematol. 24, 1215-1224.
41. LEWIS, P.F., and EMERMAN, M. (1994). Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J. Virol. 68, 510-516.
42. MAH, C., QING, K., KHUNTIRAT, B., PONNAZHAGAN, S., WANG, X.S., KUBE, D.M., YODER, M.C., and SRIVASTAVA, A. (1998). Adeno-associated virus type 2-mediated gene transfer: role of epidermal growth factor receptor protein tyrosine kinase in transgene expression. J. Virol. 72, 9835-9843.
43. MAHMUD, N., DEVINE, S.M., WELLER, K.P., PARMAR, S., STURGEON, C., NELSON, M.C., HEWETT, T., and HOFFMAN, R. (2001). The relative quiescence of hematopoietic stem cells in nonhuman primates. Blood 97, 3061-3068.
44. McCARTY, D.M., YOUNG, S.M., Jr., and SAMULSKI, R.J. (2004). Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet. 38, 819-845.
45. McCORMACK, M.P., and RABBITTS, T.H. (2004). Activation of the T-cell oncogene LMO2 after gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 350, 913-922.
46. McKEON, C., and SAMULSKI, R.J. (1996). NIDDK workshop on AAV vectors: Gene transfer into quiescent cells. Hum. Gene Ther. 7, 1615-1619.
47. MILLER, D.G., ADAM, M.A., and MILLER, A.D. (1990). Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol. Cell. Biol. 10, 4239-4242.
48. MILLER, D.G., PETEK, L.M., and RUSSELL, D.W. (2003). Human gene targeting by adeno-associated virus vectors is enhanced by DNA double-strand breaks. Mol. Cell. Biol. 23, 3550-3557.
49. + versus. Mutat. Res. 425, 169-176.
50. PARK, Y., and GERSON, S.L. (2005). DNA repair defects in stem cell function and aging. Annu. Rev. Med. 56, 495-508.
51. PETERS, S.O., KITTLER, E.L., RAMSHAW, H.S., and QUESENBERRY, P.J. (1996). Ex vivo expansion of murine marrow cells with interleukin-3 (IL-3), IL-6, IL-11, and stem cell factor leads to impaired engraftment in irradiated hosts. Blood 87, 30-37.
52. PODSAKOFF, G., WONG, K.K., Jr., and CHATTERJEE, S. (1994). Efficient gene transfer into nondividing cells by adeno-associated virus-based vectors. J. Virol. 68, 5656-5666.
53. PONNAZHAGAN, S., YODER, M.C., and SRIVASTAVA, A. (1997). Adeno-associated virus type 2-mediated transduction of murine hematopoietic cells with long-term repopulating ability and sustained expression of a human globin gene in vivo. J. Virol. 71, 3098-3104.
54. RAJ, K., OGSTON, P., and BEARD, P. (2001). Virus-mediated killing of cells that lack p53 activity. Nature 412, 914-917.
55. RUSSELL, D.W., and KAY, M.A. (1999). Adeno-associated virus vectors and hematology. Blood 94, 864-874.
56. SANLIOGLU, S., BENSON, P., and ENGELHARDT, J.F. (2000). Loss of ATM function enhances recombinant adeno-associated virus transduction and integration through pathways similar to UV irradiation. Virology 268, 68-78.
57. SANTAT, L., PAZ, H., WONG, C., LI, L., MACER, J., FORMAN, S., WONG, K.K., and CHATTERJEE, S. (2005). Recombinant AAV2 transduction of primitive human hematopoietic stem cells capable of serial engraftment in immune-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 102, 11053-11058.
58. SONG, S., MORGAN, M., ELLIS, T., POIRIER, A., CHESNUT, K., WANG, J., BRANTLY, M., MUZYCZKA, N., BYRNE, B.J., ATKINSON, M., and FLOTTE, T.R. (1998). Sustained secretion of human α- 1-antitrypsin from murine muscle transduced with adeno-associated virus vectors. Proc. Natl. Acad. Sci. U.S.A. 95, 14384-14388.
59. SONG, S., LU, Y., CHOI, Y.K., HAN, Y., TANG, Q., ZHAO, C., BERNS, K.I., and FLOTTE, T.R. (2004). DNA-dependent PK inhibits adeno-associated virus DNA integration. Proc. Natl. Acad. Sci. U.S.A. 101, 2112-2116.
60. SRIVASTAVA, A. (2004). Gene delivery to human and murine primitive hematopoietic stem and progenitor cells by AAV2 vectors. Methods Mol. Biol. 246, 245-254.
61. SRIVASTAVA, A. (2005). Hematopoietic stem cell transduction by recombinant adeno-associated virus vectors: Problems and solutions. Hum. Gene Ther. 16, 792-798.
62. SUN, J.Y., ANAND-JAWA, V., CHATTERJEE, S., and WONG, K.K. (2003). Immune responses to adeno-associated virus and its recombinant vectors. Gene Ther. 10, 964-976.
63. THOMAS, C.E., STORM, T.A., HUANG, Z., and KAY, M.A. (2004). Rapid uncoating of vector genomes is the key to efficient liver transduction with pseudotyped adeno-associated virus vectors. J. Virol. 78, 3110-3122.
64. VAN DER LOO, J.C., and PLOEMACHER, R.E. (1995). Marrow- and spleen-seeding efficiencies of all murine hematopoietic stem cell subsets are decreased by preincubation with hematopoietic growth factors. Blood 85, 2598-2606.
65. VAN DER LOO, J.C., SLIEKER, W.A., and PLOEMACHER, R.E. (1995). Use of ER-MP12 as a positive marker for the isolation of murine long-term in vitro repopulating stem cells. Exp. Hematol. 23, 1002-1010.
66. YOUNG, J.C., VARMA, A., DIGIUSTO, D., and BACKER, M.P. (1996). Retention of quiescent hematopoietic cells with high proliferative potential during ex vivo stem cell culture. Blood 87, 545-556.
67. ZENTILIN, L., MARCELLO, A., and GIACCA, M. (2001). Involvement of cellular double-stranded DNA break binding proteins in processing of the recombinant adeno-associated virus genome. J. Virol. 75, 12279-12287.
68. ZHONG, L., LI, W., YANG, Z., CHEN, L., LI, Y., QING, K., WEIGEL-KELLEY, K.A., YODER, M.C., SHOU, W., and SRIVASTAVA, A. (2004a). Improved transduction of primary murine hepatocytes by recombinant adeno-associated virus 2 vectors in vivo. Gene Ther. 11, 1165-1169.
69. ZHONG, L., LI, W., YANG, Z., QING, K., TAN, M., HANSEN, J., LI, Y., CHEN, L., CHAN, R.J., BISCHOF, D., MAINA, N., WEIGEL-KELLEY, K.A., ZHAO, W., LARSEN, S.H., YODER, M.C., SHOU, W., and SRIVASTAVA, A. (2004b). Impaired nuclear transport and uncoating limit recombinant adeno-associated virus 2 vector-mediated transduction of primary murine hematopoietic cells. Hum. Gene Ther. 15, 1207-1218.