A simple and effective method to generate lentiviral vectors for ex vivo gene delivery to mature human peripheral blood lymphocytes

Human Gene Therapy Methods

Volumn 23, Issue 2, 2012, Pages 73-83

  Yang, Shicheng ^a,e   Karne, Neel K ^a,b   Goff, Stephanie L ^a,c   Black, Mary A ^a   Xu, Hui ^a   Bischof, Daniela ^d   Cornetta, Kenneth ^d   Rosenberg, Steven A ^a   Morgan, Richard A ^a   Feldman, Steven A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^c College of Physicicans and Surgeons ^*  (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LENTIVIRUS VECTOR; MELANOMA ANTIGEN; T LYMPHOCYTE RECEPTOR; DEOXYRIBONUCLEASE; GREEN FLUORESCENT PROTEIN; MELAN A; RIBONUCLEASE; SERRATIA MARCESCENS NUCLEASE;

ARTICLE; BIOSAFETY; COMPARATIVE STUDY; CONTROLLED STUDY; EX VIVO GENE TRANSFER; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MELANOMA CELL; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; RETROVIRUS; WOODCHUCK HEPATITIS VIRUS; ANALYSIS OF VARIANCE; BIOSYNTHESIS; FLOW CYTOMETRY; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; LENTIVIRINAE; LYMPHOCYTE; METABOLISM; METHODOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY SEQUENCE; TUMOR CELL LINE;

MURINAE; WOODCHUCK HEPATITIS VIRUS;

ANALYSIS OF VARIANCE; CELL LINE, TUMOR; ENDODEOXYRIBONUCLEASES; ENDORIBONUCLEASES; FLOW CYTOMETRY; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; LENTIVIRUS; LYMPHOCYTES; MART-1 ANTIGEN; REAL-TIME POLYMERASE CHAIN REACTION; REGULATORY ELEMENTS, TRANSCRIPTIONAL;

EID: 84870816149     PISSN: 19466536     EISSN: 19466544     Source Type: Journal    
DOI: 10.1089/hgtb.2011.199     Document Type: Article

References (56)

1. Aiuti, A., Shimon, S., Aker, M., et al. (2002). Correction of ADASCID by stem cell gene therapy combined with nonmyeloablative conditioning. Science 296, 2410-2413.
2. Ansorge, S., Lanthier, S., Transfiguracion, J., et al. (2009). Development of a scalable process for high-yield lentiviral vector production by transient transfection of HEK293 suspension cultures. J. Gene Med. 11, 868-876.
3. Blaese, R.M., Culver, K.W., Miller, A.D., et al. (1995). T lymphocyte-directed gene therapy for ADA-SCID: Initial trial results after 4 years. Science 270, 475-480.
4. Bouchard, M.J., and Schneider, R.J. (2004). The enigmatic X gene of hepatitis B virus. J. Virol. 78, 12725-12734.
5. Brentjens, R.J., Riviere, I., Park, J.H., et al. (2011). Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood 118, 4817-4828.
6. Cavalieri, S., Cazzaniga, S., Geuna, M., et al. (2003). Human T lymphocytes transduced by lentiviral vectors in the absence of TCR activation maintain an intact immune competence. Blood 102, 497-505.
7. Cavazzana-Calvo, M., Jacein-Bey, S., de Saint Basile, G., et al. (2000). Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288, 669-672.
8. Cavazzana-Calvo, M., Payen, E., Negre, O., et al. (2010). Transfusion independence and HMGA2 activation after gene therapy of human b-thalassaemia. Nature 467, 318-322.
9. Chang, A.H., and Sadelain, M. (2007). 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. 15, 445-456.
10. Charrier, S., Ferrand, M., Zerbato, M., et al. (2011). Quantification of lentiviral vector copy numbers in individual hematopoietic colony-forming cells shows vector dose-dependent effects on the frequency and level of transduction. Gene Ther. 18, 479-487.
11. Deglon, N., Tseng, J.L., Bensadoun, J.-C., et al. (2000). Selfinactivating lentiviral vectors with enhanced transgene expression as potential gene transfer system in Parkinson's disease. Hum. Gene Ther. 11, 179-190.
12. Dudley, M.E., Yang, J.C., Sherry, R., et al. (2008). Adoptive cell therapy for patients with metastatic melanoma: Evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 26, 5233-5239.
13. Dull, T., Zufferey, R., Kelly, M., et al. (1998). A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72, 8463-8471.
14. Feldman, S.A., Goff, S.L., Xu, H., et al. (2011). Rapid production of clinical-grade gammaretroviral vectors in expanded surface roller bottles using a ''modified'' step-filtration process for clearance of packaging cells. Hum. Gene Ther. 22, 107-115.
15. Gaspar, H.B., Parsley, K.L., Howe, S., et al. (2004). Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet 364, 2181-2187.
16. Goff, S., Johnson, L., Black, M., et al. (2010). Enhanced receptor expression and in vitro effector function of a murine-human hybrid MART-1-reactive T cell receptor following a rapid expansion. Cancer Immunol. Immunother. 59, 1551-1560.
17. Griffiths, E. (1997). WHO Expert Committee on Biological Standardization: Highlights of the meeting of October 1996. Biologicals 25, 359-362.
18. Hacein-Bey-Abina, S., von Kalle, C., Schmidt, M., et al. (2003). A serious adverse event after successful gene therapy for Xlinked severe combined immunodeficiency. N. Engl. J. Med. 348, 255-256.
19. Heslop, H.E., Ng, C.Y.C., Li, C., et al. (1996). Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat. Med. 2, 551-555.
20. Ikawa, M., Tanaka, M., Kao, W.W.-Y., and Verma, I.M. (2003). Generation of transgenic mice using lentiviral vectors: A novel preclinical assessment of lentiviral vectors for gene therapy. Mol. Ther. 8, 666-673.
21. Ikeda, Y., Takeuchi, Y., Martin, F., et al. (2003). Continuous hightiter HIV-1 vector production. Nat. Biotechnol. 21, 569-572.
22. Johnson, L.A., Heemskerk, B., Powell, D.J., Jr., et al. (2006). Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J. Immunol. 177, 6548-6559.
23. Johnson, L.A., Morgan, R.A., Dudley, M.E., et al. (2009). Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114, 535-546.
24. Jones, S., Peng, P.D., Yang, S., et al. (2009). Lentiviral vector design for optimal T cell receptor gene expression in the transduction of peripheral blood lymphocytes and tumorinfiltrating lymphocytes. Hum. Gene Ther. 20, 630-640.
25. Kafri, T., van Praag, H., Ouyang, L., et al. (1999). A packaging cell line for lentivirus vectors. J. Virol. 73, 576-584.
26. Kalos, M., Levine, B.L., Porter, D.L., et al. (2011). T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med. 3, 95ra73.
27. Kochenderfer J.N. Wilson W.H. Janik J.E. et al. (2010). Eradication of B-lineage cells regression of lymphoma in Patient Treated With Autologous T Cells Genetically Engineered To Recognize CD19. Blood 116 4099-4102
28. Kochenderfer, J.N., Dudley, M.E., Maric, I., et al. (2011). Dramatic regression of chronic lymphocytic leukemia in the first patient treated with donor-derived genetically-engineered anti-CD19-chimeric-antigen-receptor- expressing T cells after allogeneic hematopoietic stem cell transplantation. Biol. Blood Marrow Transplant. 17, S158-S158.
29. Lize'e, G., Aerts, J.L., Gonzales, M.I., et al. (2003). Real-time quantitative reverse transcriptase-polymerase chain reaction as a method for determining lentiviral vector titers and measuring transgene expression. Hum. Gene Ther. 14, 497-507.
30. Merten, O.-W., Charrier, S., Laroudie, N., et al. (2011). Largescale manufacture and characterization of a lentiviral vector produced for clinical ex vivo gene therapy application. Hum. Gene Ther. 22, 343-356.
31. Montini, E., Cesana, D., Schmidt, M., et al. (2006). Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat. Biotechnol. 24, 687-696.
32. Morgan, R.A., Dudley, M.E., Wunderlich, J.R., et al. (2006). Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314, 126-129.
33. Parkhurst, M.R., Yang, J.C., Langan, R.C., et al. (2011). T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol. Ther. 19, 620-626.
34. Pfeifer, A., Ikawa, M., Dayn, Y., and Verma, I.M. (2002). Transgenesis by lentiviral vectors: Lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. U.S.A. 99, 2140-2145.
35. Porter, D.L., Levine, B.L., Kalos, M., et al. (2011). Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365, 725-733.
36. Ramezani, A., Hawley, T.S., and Hawley, R.G. (2000). Lentiviral vectors for enhanced gene expression in human hematopoietic cells. Mol. Ther. 2, 458-469.
37. Robbins, P.F., Morgan, R.A., Feldman, S.A., et al. (2011). Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J. Clin. Oncol. 29, 917-924.
38. Rosenberg, S.A., Yang, J.C., Sherry, R.M., et al. (2011). Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 17, 4550-4557.
39. Sastry, L., Xu, Y., Cooper, R., et al. (2004). Evaluation of plasmid DNA removal from lentiviral vectors by Benzonase treatment. Hum. Gene Ther. 15, 221-226.
40. Savoldo, B., Ramos, C.A., Liu, E., et al. (2011). CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J. Clin. Invest. 121, 1822-1826.
41. Schambach, A., Bohne, J., Baum, C., et al. (2005). Woodchuck hepatitis virus post-transcriptional regulatory element deleted from X protein and promoter sequences enhances retroviral vector titer and expression. Gene Ther. 13, 641-645.
42. Schambach, A., Mueller, D., Galla, M., et al. (2006). Overcoming promoter competition in packaging cells improves production of self-inactivating retroviral vectors. Gene Ther. 13, 1524-1533.
43. Schweizer, M., and Merten, O.-W. (2010). Large-scale production means for the manufacturing of lentiviral vectors. Curr. Gene Ther. 10, 474-486.
44. Segura, M.M., Garnier, A., Durocher, Y., et al. (2010). New protocol for lentiviral vector mass production. In Lentivirus Gene Engineering Protocols. M. Federico, ed. (Humana Press, New York), pp. 39-52.
45. Segura, M.M., Kamen, A.A., and Garnier, A. (2011). Overview of Current Scalable Methods for Purification of Viral Vectors. In Viral Vectors for Gene Therapy, O.-W. Merten, and M. Al- Rubeai, eds. (Humana Press), pp. 89-116.
46. Shaw, K.L., and Kohn, D.B. (2011). A tale of two SCIDs. Sci. Transl. Med. 3, 97ps36.
47. Stewart, H.J., Fong-Wong, L., Strickland, I., et al. (2011). A stable producer cell line for the manufacture of a lentiviral vector for gene therapy of Parkinson's disease. Hum. Gene Ther. 22, 357-369.
48. Throm, R.E., Ouma, A.A., Zhou, S., et al. (2009). Efficient construction of producer cell lines for a SIN lentiviral vector for SCID-X1 gene therapy by concatemeric array transfection. Blood 113, 5104-5110.
49. Topalian, S., Solomon, D., and Rosenberg, S. (1989). Tumorspecific cytolysis by lymphocytes infiltrating human melanomas. J. Immunol. 142, 3714-3725.
50. Walter, E.A., Greenberg, P.D., Gilbert, M.J., et al. (1995). Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N. Engl. J. Med. 333, 1038-1044.
51. Wiznerowicz, M., and Trono,D. (2005).HarnessingHIVfor therapy: Basic research and biotechnology. Trends Biotechnol. 23, 42-47.
52. Woods, N.-B., Bottero, V., Schmidt, M., et al. (2006). Gene therapy: Therapeutic gene causing lymphoma. Nature 440, 1123-1123.
53. Wu, X., Li, Y., Crise, B., and Burgess, S.M. (2003). Transcription start regions in the human genome are favored targets for MLV integration. Science 300, 1749-1751.
54. Yang, S., Cohen, C.J., Peng, P.D., et al. (2008a). Development of optimal bicistronic lentiviral vectors facilitates high-level TCR gene expression and robust tumor cell recognition. Gene Ther. 15, 1411-1423.
55. Yang, S., Rosenberg, S.A., and Morgan, R.A. (2008b). Clinicalscale lentiviral vector transduction of PBL for TCR gene therapy and potential for expression in less-differentiated cells. J. Immunother. 31, 830-839.
56. Zufferey, R., Donello, J.E., Trono, D., and Hope, T.J. (1999). Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J. Virol. 73, 2886-2892.