Clinical trials with retrovirus mediated gene therapy - What have we learned?

Journal of Neuro-Oncology

Volumn 65, Issue 3, 2003, Pages 227-236

  Rainov, Nikolai G ^a,b   Ren, Huan ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b WALTON CENTRE FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

Author keywords

Clinical trials; Gene therapy; Retrovirus; Thymidine kinase

Indexed keywords

ANTINEOPLASTIC AGENT; CYTOKINE; DOUBLE STRANDED DNA; GANCICLOVIR; GUANINE NUCLEOTIDE BINDING PROTEIN; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN; PA317 PROTEIN; PG13 PROTEIN; PRODRUG; PROTEIN; RETROVIRUS VECTOR; RNA DIRECTED DNA POLYMERASE; THYMIDINE KINASE; TRITIUM; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VIRUS DNA; VIRUS GLYCOPROTEIN; VIRUS PROTEIN; VIRUS RNA;

BRAIN ABSCESS; BRAIN TUMOR; BYSTANDER EFFECT; CANCER; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER SURVIVAL; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; DRUG SAFETY; DRUG TOXICITY; GENE TARGETING; GENETIC TRANSDUCTION; GLIOBLASTOMA; GLIOMA; GLIOMA CELL; HERPES SIMPLEX VIRUS; HUMAN; HYDROCEPHALUS; IN VIVO STUDY; INTRACRANIAL HYPERTENSION; NEUROLOGIC DISEASE; NONHUMAN; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PHASE 3 CLINICAL TRIAL; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL; RETROVIRUS; REVIEW; SEIZURE; TRANSGENE; TREATMENT FAILURE; TUMOR CELL; VIRAL GENE THERAPY; VIRUS GENOME; VIRUS REPLICATION;

ANIMALS; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CLINICAL TRIALS; GENE THERAPY; GENETIC ENGINEERING; GENETIC VECTORS; GLIOMA; HUMANS; IMMUNOTHERAPY; RETROVIRIDAE; TREATMENT OUTCOME;

EID: 0346873932     PISSN: 0167594X     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:NEON.0000003652.71665.f2     Document Type: Review

References (73)

1. Moolten FL: Tumor chemosensitivity conferred by inserted herpes thymidine kinase genes: Paradigm for a prospective cancer control strategy. Cancer Res 46: 5276-5281, 1986
2. Kramm CM, Sena-Esteves M, Barnett FH, Rainov NG, Schuback DE, Yu JS, Pechan PA, Paulus W, Chiocca EA, Breakfield XO: Gene therapy for brain tumors. Brain Pathol 5: 345-381, 1995
3. Rainov NG, Kramm CM: Vector delivery methods and targeting strategies for gene therapy of brain tumors. Curr Gene Ther 1: 367-383, 2001a
4. Lam PY, Breakefield XO: Potential of gene therapy for brain tumors. Hum Mol Genet 10: 777-787, 2001
5. Coffin JM: Retroviridae and Their Replication in 'Virology'. In: Coffin JM (ed) Raven Press, New York, 1990, pp 1437-1500
6. Albritton LM, Kim JW, Tseng L, Cunningham JM: Envelope-binding domain in the cationic amino acid transporter determines the host range of ecotropic murine retroviruses. J Virol 67: 2091-2096, 1993
7. Chu TH, Martinez I, Sheay WC, Dornburg R: Cell targeting with retroviral vector particles containing antibody-envelope fusion proteins. Gene Ther 1: 292-299, 1994
8. Uckert W and Walther W: Retrovirus-mediated gene transfer in cancer therapy. Pharmacol Ther 63: 323-347, 1994
9. Bowerman B, Brown PO, Bishop JM, Varmus HE: A nucleo-protein complex mediates the integration of retroviral DNA. Genes Dev 3: 469-478, 1989
10. Lewis PF, Emerman M: Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J Virol 68: 510-516, 1994
11. Lewis P, Hensel M, Emerman M: Human immunodeficiency virus infection of cells arrested in the cell cycle. Embo J 11: 3053-3058, 1992
12. Varmus HE, Swanstorm R: Replication of retroviruses. In Varmus HE, Swanstorm R (eds) RNA Tumor Viruses. Cold Spring Harbour, New York, 1990, pp 369-512
13. Chumakov I, Stuhlmann H, Harbers K, Jaenisch R: Cloning of two genetically transmitted Moloney leukemia proviral genomes: Correlation between biological activity of the cloned DNA and viral genome activation in the animal. J Virol 42: 1088-1098, 1982
14. Danos O, Mulligan RC: Safe and efficient generation of recombinant retroviruses with amphotropic and ecotropic host ranges. Proc Natl Acad Sci USA 85: 6460-6464, 1988
15. Markowitz D, Goff S, Bank A: Construction and use of a safe and efficient amphotropic packaging cell line. Virology 167: 400-406, 1988
16. Shapiro WR, Shapiro JR: Biology and treatment of malignant glioma. Oncology (Huntingt) 12:233-240; discussion 240, 246, 1998
17. Oldfield EH, Ram Z, Culver KW, Blaese RM, DeVroom HL, Anderson WF: Gene therapy for the treatment of brain tumors using intra-tumoral transduction with the thymidine kinase gene and intravenous ganciclovir. Hum Gene Ther 4: 39-69, 1993
18. Boviatsis EJ, Chase M, Wei MX, Tamiya T, Hurford RK Jr, Kowall NW, Tepper RI, Breakefield XO, Chiocca EA: Gene transfer into experimental brain tumors mediated by adenovirus, herpes simplex virus, and retrovirus vectors. Hum Gene Ther 5: 183-191, 1994
19. Tamiya T, Wei MX, Chase M, Ono Y, Lee F, Breakefield XO, Chiocca EA: Transgene inheritance and retroviral infection contribute to the efficiency of gene expression in solid tumors inoculated with retroviral vector producer cells. Gene Ther 2: 531-538, 1995
20. Ram Z, Kulver KW, Walbridge S, Blaese RM, Oldfield EH: In situ retroviral-mediated gene transfer for the treatment of brain tumors in rats. Cancer Res 53: 83-88, 1993
21. Ram Z, Culver KW, Walbridge S, Frank JA, Blaese RM, Oldfield EH: Toxicity studies of retroviral-mediated gene transfer for the treatment of brain tumors. J Neurosurg 79: 400-407, 1993
22. Long Z, Li LP, Grooms T, Lockey C, Nader K, Mychkovsky I, Mueller S, Burimski I, Ryan P, Kikuchi G, Ennist D, Marcus S, Otto E and McGarrity G: Biosafety monitoring of patients receiving intracerebral injections of murine retroviral vector producer cells. Hum Gene Ther 9: 1165-1172, 1998
23. Shand N, Weber F, Mariani L, Bernstein M, Gianella-Borradori A, Long Z, Sorensen AG, Barbier N: A phase 1-2 clinical trial of gene therapy for recurrent glioblastoma multiforme by tumor transduction with the herpes simplex thymidine kinase gene followed by ganciclovir. GLI328 European-Canadian Study Group. Hum Gene Ther 10: 2325-2335, 1999
24. Boris-Lawrie K, Temin HM: The retroviral vector. Replication cycle and safety considerations for retrovirus-mediated gene therapy. Ann NY Acad Sci 716: 59-70; discussion 71, 1994
25. Mann R, Mulligan RC, Baltimore D: Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell 33: 153-159, 1983
26. Lyons RM, Forry-Schaudies S, Otto E, Wey C, Patil-Koota V, Kaloss M, McGarrity GJ and Chiang YL: An improved retroviral vector encoding the herpes simplex virus thymidine kinase gene increases antitumor efficacy in vivo. Cancer Gene Ther 2: 273-280, 1995
27. Short MP, Choi BC, Lee JK, Malick A, Breakefield XO, Martuza RL: Gene delivery to glioma cells in rat brain by grafting of a retrovirus packaging cell line. J Neurosci Res 27: 427-439, 1990
28. Rainov NG, Kramm CM, Aboody-Guterman K, Chase M, Ueki K, Louis DN, Harsh GRt, Chiocca A, Breakefield XO: Retrovirus-mediated gene therapy of experimental brain neoplasms using the herpes simplex virus-thymidine kinase/ganciclovir paradigm. Cancer Gene Ther 3: 99-106, 1996
29. Kaloss M, Linscott M, Wey C, Lu P, Long Z, McGarrity GJ, Otto E, Lyons RM: Distribution of retroviral vectors and vector producer cells using two routes of administration in rats. Gene Ther 6: 1389-1396, 1999
30. Long Z, Lu P, Grooms T, Mychkovsky I, Westley T, Fitzgerald T, Sharma-Chibber S, Shand N, McGarrity G, Otto E: Molecular evaluation of biopsy and autopsy specimens from patients receiving in vivo retroviral gene therapy. Hum Gene Ther 10: 733-740, 1999
31. Rainov NG: A phase III clinical evaluation of herpes simplex virus type 1 thymidine kinase and ganciclovir gene therapy as an adjuvant to surgical resection and radiation in adults with previously untreated glioblastoma multiforme. Hum Gene Ther 11: 2389-2401, 2000b
32. Barba D, Hardin J, Sadelain M, Gage FH: Development of anti-tumor immunity following thymidine kinase-mediated killing of experimental brain tumors. Proc Natl Acad Sci USA 91: 4348-4352, 1994
33. Ram Z, Culver KW, Oshiro EM, Viola JJ, DeVroom HL, Otto E, Long Z, Chiang Y, McGarrity GJ, Muul LM, Katz D, Blaese RM, Oldfield EH: Therapy of malignant brain tumors by intratumoral implantation of retroviral vector-producing cells. Nat Med 3: 1354-1361, 1997
34. Puumalainen AM, Vapalahti M, Agrawal RS, Kossila M, Laukkanen J, Lehtolainen P, Vitta H, Paljarvi L, Vanninen R, Yla-Herttuala S: Beta-galactosidase gene transfer to human malignant glioma in vivo using replication-deficient retroviruses and adenoviruses. Hum Gene Ther 9: 1769-1774, 1998
35. Rainov NG, Kramm CM, Banning U, Riemann D, Holzhausen HJ, Heidecke V, Burger KJ, Burkert W, Korholz D: Immune response induced by retrovirus-mediated HSV-tk/GCV pharmacogene therapy in patients with glioblastoma multiforme. Gene Ther 7: 1853-1858, 2000a
36. Sena-Esteves M, Hampl JA, Camp SM, Breakefield XO: Generation of stable retrovirus packaging cell lines after transduction with herpes simplex virus hybrid amplicon vectorsdouble dagger. J Gene Med 4: 229-239, 2002
37. Ezzeddine ZD, Martuza RL, Platika D, Short MP, Malick A, Choi B, Breakefield XO: Selective killing of glioma cells in culture and in vivo by retrovirus transfer of the herpes simplex virus thymidine kinase gene. New Biol 3: 608-614, 1991
38. Takamiya Y, Short MP, Ezzeddine ZD, Moolten FL, Breakefield XO and Martuza RL: Gene therapy of malignant brain tumors: A rat glioma line bearing the herpes simplex virus type 1-thymidine kinase gene and wild type retrovirus kills other tumor cells. J Neurosci Res 33: 493-503, 1992
39. Bi WL, Parysek LM, Warnick R, Stambrook PJ: In vitro evidence that metabolic cooperation is responsible for the bystander effect observed with HSV tk retroviral gene therapy. Hum Gene Ther 4: 725-731, 1993
40. Freeman SM, Abboud CN, Whartenby KA, Packman CH, Koeplin DS, Moolten FL, Abraham GN: The 'bystander effect': Tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res 53: 5274-5283, 1993
41. Ishii-Morita H, Agbaria R, Mullen CA, Hirano H, Koeplin DA, Ram Z, Oldfield EH, Johns DG, Blaese RM: Mechanism of 'bystander effect' killing in the herpes simplex thymidine kinase gene therapy model of cancer treatment. Gene Ther 4: 244-251, 1997
42. Burrows FJ, Gore M, Smiley WR, Kanemitsu MY, Jolly DJ, Read SB, Nicholas T, Kruse CA: Purified herpes simplex virus thymidine kinase retroviral particles: III. Characterization of bystander killing mechanisms in transfected tumor cells. Cancer Gene Ther 9: 87-95, 2002
43. Tapscott SJ, Miller AD, Olson JM, Berger MS, Groudine M, Spence AM: Gene therapy of rat 9L gliosarcoma tumors by transduction with selectable genes does not require drug selection. Proc Natl Acad Sci USA 91: 8185-8189, 1994
44. Vile RG, Castleden S, Marshall J, Camplejohn R, Upton C, Chong H: Generation of an anti-tumour immune response in a non-immunogenic tumour: HSVtk killing in vivo stimulates a mononuclear cell infiltrate and a Th1-like profile of intratumoural cytokine expression. Int J Cancer 71: 267-274, 1997
45. Mullen CA, Anderson L, Woods K, Nishino M, Petropoulos D: Ganciclovir chemoablation of herpes thymidine kinase suicide gene- modified tumors produces tumor necrosis and induces systemic immune responses. Hum Gene Ther 9: 2019-2030, 1998
46. Culver KW, Ram Z, Wallbridge S, Ishii H, Oldfield EH, Blaese RM: In vivo gene transfer with retroviral vector-producer cells for treatment of experimental brain tumors. Science 256: 1550-1552, 1992
47. Barba D, Hardin J, Ray J, Gage FH: Thymidine kinase-mediated killing of rat brain tumors. J Neurosurg 79: 729-735, 1993
48. Lee H, Song JJ, Kim E, Yun CO, Choi J, Lee B, Kim J, Chang JW, Kim JH: Efficient gene transfer of VSV-G pseudotyped retroviral vector to human brain tumor. Gene Ther 8: 268-273, 2001
49. Tamura K, Tamura M, Ikenaka K, Yoshimatsu T, Miyao Y, Nanmoku K, Shimizu K: Eradication of murine brain tumors by direct inoculation of concentrated high titer-recombinant retrovirus harboring the herpes simplex virus thymidine kinase gene. Gene Ther 8: 215-222, 2001
50. Sandmair AM, Loimas S, Poptani H, Vainio P, Vanninen R, Turunen M, Tyynela K, Vapalahti M, Yla-Herttuala S: Low efficacy of gene therapy for rat BT4C malignant glioma using intra-tumoural transduction with thymidine kinase retrovirus packaging cell injections and ganciclovir treatment. Acta Neurochir 141: 867-872, 1999
51. Sandmair AM, Turunen M, Tyynela K, Loimas S, Vainio P, Vanninen R, Vapalahti M, Bjerkvig R, Janne J, Yla-Herttuala S: Herpes simplex virus thymidine kinase gene therapy in experimental rat BT4C glioma model: Effect of the percentage of thymidine kinase-positive glioma cells on treatment effect, survival time, and tissue reactions. Cancer Gene Ther 7: 413-421, 2000
52. Klatzmann D, Valery CA, Bensimon G, Marro B, Boyer O, Mokhtari K, Diquet B, Salzmann JL, Philippon J: A phase I/II study of herpes simplex virus type 1 thymidine kinase 'suicide' gene therapy for recurrent glioblastoma. Study Group on Gene Therapy for Glioblastoma. Hum Gene Ther 9: 2595-2604, 1998
53. Izquierdo M, Martin V, De Felipe P, Izquierdo JM, Perez-Higueras A, Cortes ML, Paz JF, Isla A, Blazquez MG: Human malignant brain tumor response to herpes simplex thymidine kinase (HSVtk)/ganciclovir gene therapy. Gene Ther 3: 491-495, 1996
54. Izquierdo M, Cortes ML, Martin V, De Felipe P, Izquierdo JM, Perrez-Higueras A, Paz JF, Isla A, Blazquez MG: Gene therapy in brain tumors: Implications of the size of glioblastoma on its curability. Acta Neurochir Supple (Wien) 68: 111-117, 1997
55. Packer RJ, Raffel C, Villablanca JG, Tonn JC, Burdach SE, Burger K, LaFond D, McComb JG, Cogen PH, Vezina G, Kapcala LP: Treatment of progressive or recurrent pediatric malignant supratentorial brain tumors with herpes simplex virus thymidine kinase gene vector-producer cells followed by intravenous ganciclovir administration. J Neurosurg 92: 249-254, 2000
56. Kramm CM, Korholz D, Rainov NG, Niehues T, Fischer U, Steffens S, Frank S, Banning U, Horneff G, Schroten H, Burdach S: Systemic activation of the immune system during ganciclovir treatment following intratumoral herpes simplex virus type 1 thymidine kinase gene transfer in an adolescent ependymoma patient. Neuropediatrics 33: 6-9, 2002
57. Palu G, Cavaggioni A, Calvi P, Franchin E, Pizzato M, Boschetto R, Parolin C, Chilosi M, Ferrini S, Zanusso A, Colombo F: Gene therapy of glioblastoma multiforme via combined expression of suicide and cytokine genes: A pilot study in humans. Gene Ther 6: 330-337, 1999
58. Boothman DA, Davis TW, Sahijdak WM: Enhanced expression of thymidine kinase in human cells following ionizing radiation. Int J Radiat Oncol Biol Phys 30: 391-398, 1994
59. Kim JH, Kim SH, Brown SL, Freytag SO: Selective enhancement by an antiviral agent of the radiation-induced cell killing of human glioma cells transduced with HSV-tk gene. Cancer Res 54: 6053-6056, 1994
60. Harsh GR, Deisboeck TS, Louis DN, Hilton J, Colvin M, Silver JS, Qureshi NH, Kracher J, Finkelstein D, Chiocca EA, Hochberg FH: Thymidine kinase activation of ganciclovir in recurrent malignant gliomas: A gene-marking and neuropathological study. J Neurosurg 92: 804-811, 2000
61. Kramer ED, Packer RJ, Ginsberg J, Goldman S, Thompson S, Bayer LA, Shen V, Harris R, Khan S, Finlay JL: Acute neurologic dysfunction associated with high-dose chemotherapy and autologous bone marrow rescue for primary malignant brain tumors. Pediatr Neurosurg 27: 230-237, 1997
62. Prados MD, Russo C: Chemotherapy of brain tumors. Semin Surg Oncol 14: 88-95, 1998
63. Sandmair AM, Loimas S, Puranen P, Immonen A, Kossila M, Puranen M, Hurskainen H, Tyynela K, Turunen M, Vanninen R, Lehtolainen P, Paljarvi L, Johansson R, Vapalahti M, Yla-Herttuala S: Thymidine kinase gene therapy for human malignant glioma, using replication-deficient retroviruses or adenoviruses. Hum Gene Ther 11: 2197-2205, 2000
64. Russell DW, Berger MS, Miller AD: The effects of human serum and cerebrospinal fluid on retroviral vectors and packaging cell lines. Hum Gene Ther 6: 635-641, 1995
65. Blasberg RG, Tjuvajev JG: Herpes simplex virus thymidine kinase as a marker/reporter gene for PET imaging of gene therapy. Q J Nucl Med 43: 163-169, 1999
66. Gambir SS, Herschman HR, Cherry SR, Barrio JR, Satyamurthy N, Toyokuni T, Phelps ME, Larson SM, Balatoni J, Finn R, Sadelain M, Tjuvajev J, Blasberg R: Imaging transgene expression with radionuclide imaging technologies. Neoplasia 2: 118-138, 2000
67. Rainov NG, Fels C, Droege JW, Schafer C, Kramm CM, Chou TC: Temozolomide enhances herpes simplex virus thymidine kinase/ganciclovir therapy of malignant glioma. Cancer Gene Ther 8: 662-668, 2001b
68. Inamura T, Nomura T, Bartus RT, Black KL: Intracarotid infusion of RMP-7, a bradykinin analog: A method for selective drug delivery to brain tumors. J Neurosurg 81: 752-758, 1994
69. LeMay DR, Kittaka M, Gordon EM, Gray B, Stins MF, McComb JG, Jovanovic S, Tabrizi P, Weiss MH, Bartus R, Anderson WF, Zlokovic BV: Intravenous RMP-7 increases delivery of ganciclovir into rat brain tumors and enhances the effects of herpes simplex virus thymidine kinase gene therapy. Hum Gene Ther 9: 989-995, 1998
70. Herrlinger U, Woiciechowski C, Sena-Esteves M, Aboody KS, Jacobs AH, Rainov NG, Snyder EY, Breakfield XO: Neural precursor cells for delivery of replication-conditional HSV-1 vectors to intracerebral gliomas. Mol Ther 1: 347-357, 2000
71. Lieberman DM, Laske DW, Morrison PF, Bankiewicz KS, Oldfield EH: Convection-enhanced distribution of large molecules in gray matter during interstitial drug infusion. J Neurosurg 82: 1021-1029, 1995
72. Parsa AT, Chi JH, Hurley PT, Jeyapalan SA, Bruce JN: Immunomodulation of glioma cells after gene therapy: Induction of major histocompatibility complex class I but not class II antigen in vitro. Neurosurgery 49: 681-688; discussion 688-689, 2001
73. DiMeco F, Rhines LD, Hanes J, Tyler BM, Brat D, Torchiana E, Guarnieni M, Colombo MP, Pardoll DM, Finocchiaro G, Brem H, Olivi A: Paracrine delivery of IL-12 against intracranial 9L gliosarcoma in rats. J Neurosurg 92: 419-427, 2000