Hematopoietic-specific lentiviral vectors circumvent cellular toxicity due to ectopic expression of Wiskott-Aldrich syndrome protein

Human Gene Therapy

Volumn 19, Issue 2, 2008, Pages 179-197

  Toscano, Miguel G ^a,b   Frecha, Cecilia ^a   Benabdellah, Karim ^a   Cobo, Marien ^a   Blundell, Mike ^c   Thrasher, Adrian J ^c   García Olivares, Enrique ^b   Molina, Ignacio J ^b   Martin, Francisco ^a  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LENTIVIRUS VECTOR; WISKOTT ALDRICH SYNDROME PROTEIN;

ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; T LYMPHOCYTE;

ANIMALS; CELL DEATH; CELL LINE; CELL PROLIFERATION; CYTOSKELETON; GENE THERAPY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HEMATOPOIETIC SYSTEM; HUMANS; LENTIVIRUS; MICE; ORGAN SPECIFICITY; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC; WISKOTT-ALDRICH SYNDROME; WISKOTT-ALDRICH SYNDROME PROTEIN;

EID: 39449108039     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2007.098     Document Type: Article

References (54)

1. AIUTI, A., SLAVIN, S., AKER, M., FICARA, F., DEOLA, S., MORTELLARO, A., MORECKI, S., ANDOLFI, G., TABUCCHI, A., CARLUCCI, F., MARINELLO, E., CATTANEO, F., VAI, S., SERVIDA, P., MINIERO, R., RONCAROLO, M.G., and BORDIGNON, C. (2002). Correction of ADA-SCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 296, 2410-2413.
2. BADOLATO, R., SOZZANI, S., MALACARNE, F., BRESCIANI, S., FIORINI, M., BORSATTI, A., ALBERTINI, A., MANTOVANI, A., UGAZIO, A.G., and NOTARANGELO, L.D. (1998). Monocytes from Wiskott-Aldrich patients display reduced chemotaxis and lack of cell polarization in response to monocyte chemoattractant protein-1 and formyl-methionyl-leucyl-phenylalanine. J. Immunol. 161, 1026-1033.
3. BURNS, S., THRASHER, A.J., BLUNDELL, M.P., MACHESKY, L., and JONES, G.E. (2001). Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 98, 1142-1149.
4. CAVAZZANA-CALVO, M., HACEIN-BEY, S., DE SAINT BASILE, G., GROSS, F., YVON, E., NUSBAUM, P., SELZ, F., HUE, C., CERTAIN, S., CASANOVA, J.L., BOUSSO, P., DEIST, F.L., and FISCHER, A. (2000). Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288, 669-672.
5. CUI, Y., GOLOB, J., KELLEHER, E., YE, Z., PARDOLL, D., and CHENG, L. (2002). Targeting transgene expression to antigen-presenting cells derived from lentivirus-transduced engrafting human hematopoietic stem/progenitor cells. Blood 99, 399-408.
6. CHAN, R.J., and YODER, M.C. (2004). The multiple facets of hematopoietic stem cells. Curr. Neurovasc. Res. 1, 197-206.
7. CHARRIER, S., DUPRE, L., SCARAMUZZA, S., JEANSON-LEH, L., BLUNDELL, M.P., DANOS, O., CATTANEO, F., AIUTI, A., ECKENBERG, R., THRASHER, A.J., RONCAROLO, M.G., and GALY, A. (2006). Lentiviral vectors targeting WASp expression to hematopoietic cells, efficiently transduce and correct cells from WAS patients. Gene Ther. 14, 415-428.
8. DE LA FUENTE, M.A., SASAHARA, Y., CALAMITO, M., ANTON, I.M., ELKHAL, A., GALLEGO, M.D., SURESH, K., SIMINOVITCH, K., OCHS, H.D., ANDERSON, K.C., ROSEN, F.S., GEHA, R.S., and RAMESH, N. (2007). WIP is a chaperone for Wiskott-Aldrich syndrome protein (WASP). Proc. Natl. Acad. Sci. U.S.A. 104, 926-931.
9. DEMAISON, C., BROUNS, G., BLUNDELL, M.P., GOLDMAN, J.P., LEVINSKY, R.J., GREZ, M., KINNON, C., and THRASHER, A.J. (2000). 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. 11, 91-100.
10. DEMAISON, C., PARSLEY, K., BROUNS, G., SCHERR, M., BATTMER, K., KINNON, C., GREZ, M., and THRASHER, A.J. (2002). High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency [correction of imunodeficiency] virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum. Gene Ther. 13, 803-813.
11. DE NORONHA, S., HARDY, S., SINCLAIR, J., BLUNDELL, M.P., STRID, J., SCHULZ, O., ZWIRNER, J., JONES, G.E., KATZ, D.R., KINNON, C., and THRASHER, A.J. (2005). Impaired dendritic-cell homing in vivo in the absence of Wiskott-Aldrich syndrome protein. Blood 105, 1590-1597.
12. DUPRE, L., TRIFARI, S., FOLLENZI, A., MARANGONI, F., LAIN DE LERA, T., BERNAD, A., MARTINO, S., TSUCHIYA, S., BORDIGNON, C., NALDINI, L., AIUTI, A., and RONCAROLO, M.G. (2004). Lentiviral vector-mediated gene transfer in T cells from Wiskott-Aldrich syndrome patients leads to functional correction. Mol. Ther. 10, 903-915.
13. DUPRE, L., MARANGONI, F., SCARAMUZZA, S., TRIFARI, S., HERNANDEZ, R.J., AIUTI, A., NALDINI, L., and RONCAROLO, M.G. (2006). Efficacy of gene therapy for Wiskott-Aldrich syndrome using a WAS promoter/cDNA-containing lentiviral vector and nonlethal irradiation. Hum. Gene Ther. 17, 303-313.
14. FINAN, P.M., SOAMES, C.J., WILSON, L., NELSON, D.L., STEWART, D.M., TRUONG, O., HSUAN, J.J., and KELLIE, S. (1996). Identification of regions of the Wiskott-Aldrich syndrome protein responsible for association with selected Src homology 3 domains. J. Biol. Chem. 271, 26291-26295.
15. GALLEGO, M.D., SANTAMARIA, M., PENA, J., and MOLINA, I.J. (1997). Defective actin reorganization and polymerization of Wiskott-Aldrich T cells in response to CD3-mediated stimulation. Blood 90, 3089-3097.
16. GARCIA-PACHECO, J.M., OLIVER, C., KIMATRAI, M., BLANCO, F.J., and OLIVARES, E.G. (2001). Human decidual stromal cells express CD34 and STRO-1 and are related to bone marrow stromal precursors. Mol. Hum. Reprod. 7, 1151-1157.
17. GASPAR, H.B., PARSLEY, K.L., HOWE, S., KING, D., GILMOUR, K.C., SINCLAIR, J., BROUNS, G., SCHMIDT, M., VON KALLE, C., BARINGTON, T., JAKOBSEN, M.A., CHRISTENSEN, H.O., AL GHONAIUM, A., WHITE, H.N., SMITH, J.L., LEVINSKY, R.J., ALI, R.R., KINNON, C., and THRASHER, A.J. (2004). Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet 364, 2181-2187.
18. GISMONDI, A., CIFALDI, L., MAZZA, C., GILIANI, S., PAROLINI, S., MORRONE, S., JACOBELLI, J., BANDIERA, E., NOTARANGELO, L., and SANTONI, A. (2004). Impaired natural and CD16-mediated NK cell cytotoxicity in patients with WAS and XLT: Ability of IL-2 to correct NK cell functional defect. Blood 104, 436-443.
19. 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 BASILE, 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.
20. HUMBLET-BARON, S., SATHER, B., ANOVER, S., BECKER-HERMAN, S., KASPROWICZ, D.J., KHIM, S., NGUYEN, T., HUDKINS-LOYA, K., ALPERS, C.E., ZIEGLER, S.F., OCHS, H., TORGERSON, T., CAMPBELL, D.J., and RAWLINGS, D.J. (2007). Wiskott-Aldrich syndrome protein is required for regulatory T cell homeostasis. J. Clin. Invest. 117, 407-418.
21. KOLLURI, R., TOLIAS, K.F., CARPENTER, C.L., ROSEN, F.S., and KIRCHHAUSEN, T. (1996). Direct interaction of the Wiskott-Aldrich syndrome protein with the GTPase Cdc42. Proc. Natl. Acad. Sci. U.S.A. 93, 5615-5618.
22. KONNO, A., WADA, T., SCHURMAN, S.H., GARABEDIAN, E.K., KIRBY, M., ANDERSON, S.M., and CANDOTTI, F. (2004). Differential contribution of Wiskott-Aldrich syndrome protein to selective advantage in T- and B-cell lineages. Blood 103, 676-678.
23. KONNO, A., KIRBY, M., ANDERSON, S.A., SCHWARTZBERG, P.L., and CANDOTTI, F. (2007). The expression of Wiskott-Aldrich syndrome protein (WASP) is dependent on WASP-interacting protein (WIP). Int. Immunol. 19, 185-192.
24. LAGASSE, E., CONNORS, H., AL-DHALIMY, M., REITSMA, M., DOHSE, M., OSBORNE, L., WANG, X., FINEGOLD, M., WEISSMAN, I.L., and GROMPE, M. (2000). Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat. Med. 6, 1229-1234.
25. LEVERRIER, Y., LORENZI, R., BLUNDELL, M.P., BRICKELL, P., KINNON, C., RIDLEY, A.J., and THRASHER, A.J. (2001). Cutting edge: The Wiskott-Aldrich syndrome protein is required for efficient phagocytosis of apoptotic cells. J. Immunol. 166, 4831-4834.
26. LINDER, S., and AEPFELBACHER, M. (2003). Podosomes: Adhesion hot-spots of invasive cells. Trends Cell Biol. 13, 376-385.
27. LINDER, S., NELSON, D., WEISS, M., and AEPFELBACHER, M. (1999). Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. U.S.A. 96, 9648-9653.
28. MACHESKY, L.M., MULLINS, R.D., HIGGS, H.N., KAISER, D.A., BLANCHOIN, L., MAY, R.C., HALL, M.E., and POLLARD, T.D. (1999). Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. U.S.A. 96, 3739-3744.
29. + regulatory T cells. J. Exp. Med. 204, 381-391.
30. + natural regulatory T cells. J. Exp. Med. 204, 369-380.
31. MARTIN, F., TOSCANO, M.G., BLUNDELL, M., FRECHA, C., SRIVASTAVA, G.K., SANTAMARIA, M., THRASHER, A.J., and MOLINA, I.J. (2005). Lentiviral vectors transcriptionally targeted to hematopoietic cells by WASP gene proximal promoter sequences. Gene Ther. 12, 715-723.
32. MARX, J. (2006). Cell biology: Podosomes and invadopodia help mobile cells step lively. Science 312, 1868-1869.
33. MOLINA, I.J., KENNEY, D.M., ROSEN, F.S., and REMOLDO'DONNELL, E. (1992). T cell lines characterize events in the pathogenesis of the Wiskott-Aldrich syndrome. J. Exp. Med. 176, 867-874.
34. MOLINA, I.J., SANCHO, J., TERHORST, C., ROSEN, F.S., and REMOLD-O'DONNELL, E. (1993). T cells of patients with the Wiskott-Aldrich syndrome have a restricted defect in proliferative responses. J. Immunol. 151, 4383-4390.
35. MONTINI, E., CESANA, D., SCHMIDT, M., SANVITO, F., PONZONI, M., BARTHOLOMAE, C., SERGI, L.S., BENEDICENTI, F., AMBROSI, A., DI SERIO, C., DOGLIONI, C., VON KALLE, C., and NALDINI, L. (2006). Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat. Biotechnol. 24, 687-696.
36. MOREAU-GAUDRY, F., XIA, P., JIANG, G., PERELMAN, N.P., BAUER, G., ELLIS, J., SURINYA, K.H., MAVILIO, F., SHEN, C.K., and MALIK, P. (2001). High-level erythroid-specific gene expression in primary human and murine hematopoietic cells with self-inactivating lentiviral vectors. Blood 98, 2664-2672.
37. MOSMANN, T. (1983). Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
38. NALDINI, L., BLOMER, U., GALLAY, P., ORY, D., MULLIGAN, R., GAGE, F.H., 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.
39. NEIL, S., MARTIN, F., IKEDA, Y., and COLLINS, M. (2001). Post-entry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J. Virol. 75, 5448-5456.
40. OTT, M.G., SCHMIDT, M., SCHWARZWAELDER, K., STEIN, S., SILER, U., KOEHL, U., GLIMM, H., KUHLCKE, K., SCHILZ, A., KUNKEL, H., NAUNDORF, S., BRINKMANN, A., DEICHMANN, A., FISCHER, M., BALL, C., PILZ, I., DUNBAR, C., DU, Y., JENKINS, N.A., COPELAND, N.G., LUTHI, U., HASSAN, M., THRASHER, A.J., HOELZER, D., VON KALLE, C., SEGER, R., and GREZ, M. (2006). Correction of X-linked chronic granulomatous disease by gene therapy, augmented by insertional activation of MDS1-EVI1, PRDM16 or SETBP1. Nat. Med. 12, 401-409.
41. PAROLINI, O., BERARDELLI, S., RIEDL, E., BELLO-FERNANDEZ, C., STROBL, H., MAJDIC, O., and KNAPP, W. (1997). Expression of Wiskott-Aldrich syndrome protein (WASP) gene during hematopoietic differentiation. Blood 90, 70-75.
42. RAMESH, N., ANTON, I.M., HARTWIG, J.H., and GEHA, R.S. (1997). WIP, a protein associated with Wiskott-Aldrich syndrome protein, induces actin polymerization and redistribution in lymphoid cells. Proc. Natl. Acad. Sci. U.S.A. 94, 14671-14676.
43. SEMBA, S., IWAYA, K., MATSUBAYASHI, J., SERIZAWA, H., KATABA, H., HIRANO, T., KATO, H., MATSUOKA, T., and MUKAI, K. (2006). Coexpression of actin-related protein 2 and Wiskott-Aldrich syndrome family verproline-homologous protein 2 in adenocarcinoma of the lung. Clin. Cancer Res. 12, 2449-2454.
44. SNAPPER, S.B., TAKESHIMA, F., ANTON, I., LIU, C.H., THOMAS, S.M., NGUYEN, D., DUDLEY, D., FRASER, H., PURICH, D., LOPEZ-ILASACA, M., KLEIN, C., DAVIDSON, L., BRONSON, R., MULLIGAN, R.C., SOUTHWICK, F., GEHA, R., GOLDBERG, M.B., ROSEN, F.S., HARTWIG, J.H., and ALT, F.W. (2001). NWASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat. Cell Biol. 3, 897-904.
45. STEWART, D.M., TREIBER-HELD, S., KURMAN, C.C., FACCHETTI, F., NOTARANGELO, L.D., and NELSON, D.L. (1996). Studies of the expression of the Wiskott-Aldrich syndrome protein. J. Clin. Invest. 97, 2627-2634.
46. SYMONS, M., DERRY, J.M., KARLAK, B., JIANG, S., LEMAHIEU, V., MCCORMICK, F., FRANCKE, U., and ABO, A. (1996). Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell 84, 723-734.
47. TAKENAWA, T., and MIKI, H. (2001). WASP and WAVE family proteins: Key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114, 1801-1809.
48. THRASHER, A.J. (2002). WASp in immune-system organization and function. Nat. Rev. Immunol. 2, 635-646.
49. TOSCANO, M.G., FRECHA, C., ORTEGA, C., SANTAMARIA, M., MARTIN, F., and MOLINA, I.J. (2004). Efficient lentiviral transduction of herpesvirus saimiri immortalized T cells as a model for gene therapy in primary immunodeficiencies. Gene Ther. 11, 956-961.
50. VASSILOPOULOS, G., WANG, P.R., and RUSSELL, D.W. (2003). Transplanted bone marrow regenerates liver by cell fusion. Nature 422, 901-904.
51. YAMAGUCHI, H., and CONDEELIS, J. (2006). Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta 1773, 642-652.
52. YAMAZAKI, D., KURISU, S., and TAKENAWA, T. (2005). Regulation of cancer cell motility through actin reorganization. Cancer Sci. 96, 379-386.
53. YANG, L.Y., TAO, Y.M., OU, D.P., WANG, W., CHANG, Z.G., and WU, F. (2006). Increased expression of Wiskott-Aldrich syndrome protein family verprolin-homologous protein 2 correlated with poor prognosis of hepatocellular carcinoma. Clin. Cancer Res. 12, 5673-5679.
54. ZUFFEREY, R., DULL, T., MANDEL, R.J., BUKOVSKY, A., QUIROZ, D., NALDINI, L., and TRONO, D. (1998). Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol. 72, 9873-9880.