Cytokine gene therapy: Hopes and pitfalls

Annals of Oncology

Volumn 10, Issue 3, 1999, Pages 261-266

  Nanni, P ^a   Forni, G ^b   Lollini, P L ^a,c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c Istituto di Cancerologia   (Italy)

Author keywords

Cytokines; Gene therapy; Immune response

Indexed keywords

ALPHA INTERFERON; COLONY STIMULATING FACTOR 1; CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 7; TUMOR NECROSIS FACTOR ALPHA;

CANCER IMMUNOTHERAPY; CLINICAL PROTOCOL; GENE THERAPY; GENE TRANSFER; GENETIC TRANSDUCTION; HUMAN; IMMUNOTHERAPY; PRIORITY JOURNAL; REVIEW; TUMOR CELL; VACCINATION;

CLINICAL TRIALS; CYTOKINES; GENE THERAPY; HUMANS; NEOPLASMS; PROGNOSIS; TREATMENT OUTCOME;

EID: 0032915866     PISSN: 09237534     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1008304721889     Document Type: Review

References (86)

1. Forni G, Parmiani G, Guarini A, Foa R. Gene transfer in tumor therapy. Ann Oncol 1994; 5: 789-94.
2. Consalvo M, Mullen C, Modesti A et al. 5-Fluorocytosine induced eradication of murine adenocarcinomas engineered to express the cytosine deaminase suicide gene requires host immune competence and leaves an efficient memory. J Immunol 1995; 154: 5302-12.
3. Forni G, Foa R, Santoni A, Frati L (eds). Cytokine-Induced Tumor Immunogenicity. From Exogenous Molecules to Gene Therapy. London: Academic Press 1994.
4. Nanni P, De Giovanni C, Nicoletti G et al. The immune response elicited by mammary adenocarcinoma cells transduced with γ-interferon and cytosine deaminase genes cures lung metastases by parental cells. Human Gene Ther 1998; 9: 217-24.
5. Disis ML, Cheever MA. Oncogenic proteins as tumors antigens. Curr Opinion Immunol 1996; 8: 637-42.
6. Ryffel B (ed). Cytokine-induced pathology. Int Rev Exp Pathol 1993; 34.
7. Pardoll DM. Paracrine cytokine adjuvants in cancer immunotherapy. Annu Rev Immunol 1995; 13: 399-415.
8. Dranoff G, Mulligan R. Gene transfer as cancer therapy. Adv Immunol 1996; 58: 417-54.
9. Musiani P, Modesti A, Giovarelli M et al. Cytokines, tumour-cell death and immunogenicity: A question of choice. Immunol Today 1997; 18: 32-6.
10. Ogura H, Tani K, Ozawa K et al. Implantation of genetically manipulated fibroblasts into mice as antitumor α-interferon therapy. Cancer Res 1990; 50: 5102-6.
11. Restifo NP, Spiess PJ, Karp SE et al. A nonimmunogenic sarcoma transduced with the cDNA for interferon-γ elicits CD8+ T cells against the wild-type tumor: Correlation with antigen presentation capability. J Exp Med 1992; 175: 1423-31.
12. Cavallo F, Di Pierro F, Giovarelli M et al. Protective and curative potential of vaccination with interleukin-2-gene-transfected cells from a spontaneous mouse mammary adenocarcinoma. Cancer Res 1993; 53: 5067-70.
13. Dranoff G, Jaffee E, Lazenby A et al. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci USA 1993; 90: 3539-43.
14. Ferrantini M, Proietti E, Santodonato L et al. α-Interferon gene transfer into metastatic friend leukemia cells abrogated tumorigenicity in immunocompetent mice: Antitumor therapy by means of interferon-producing cells. Cancer Res 1993; 53: 1107-12.
15. Porgador A, Gansbacher B, Bannerji R et al. Anti-metastatic vaccination of tumor-bearing mice with IL-2-gene-inserted tumor cells. Int J Cancer 1993; 53: 471-7.
16. Porgador A, Tzehoval E, Vadai E et al. Immunotherapy via gene therapy: Comparison of the effects of tumor cells transduced with the interleukin-2, interleukin-6, or interferon-gamma genes. J Immunother 1993; 14: 191-201.
17. Shiloni E, Karp SE, Custer MC et al. Retroviral transduction of interferon-gamma cDNA into a nonimmunogenic murine fibro-sarcoma: Generation of T cells in draining lymph nodes capable of treating established parental metastatic tumor. Cancer Immunol Immunother 1993; 37: 286-92.
18. Allione A, Consalvo M, Nanni P et al. Immunizing and curative potential of replicating and nonreplicating murine mammary adenocarcinoma cells engineered with interleukin (IL)-2, IL-4, IL-6, IL-7, IL-10, TNF-α, GM-CSF, and IFN-γ gene or admixed with conventional adjuvant. Cancer Res 1994; 54: 6022-6.
19. Harada K, Yoshida J, Mizuno M et al. Growth inhibition of subcutaneously transplanted human glioma by transfection-induced tumor necrosis factor-α and augmentation of the effect by gamma-interferon. J Neurooncol 1994; 22: 221-5.
20. McBride WH, Dougherty GD, Wallis AE et al. Interleukin-3 in gene therapy of cancer. Folia Biol (Praha) 1994; 40: 62-73.
21. Nakamura Y, Wakimoto H, Abe J et al. Adoptive immunotherapy with murine tumor-specific T lymphocytes engineered to secrete interleukin-2. Cancer Res 1994; 54: 5757-60.
22. Saito S, Bannerji R, Gansbacher B et al. Immunotherapy of bladder cancer with cytokine gene-modified tumor vaccines. Cancer Res 1994; 54: 3516-20.
23. Vieweg J, Rosenthal FM, Bannerji R et al. Immunotherapy of prostate cancer in the Dunning rat model: Use of cytokine gene modified tumor vaccines. Cancer Res 1994; 54: 1760-5.
24. Vile RG, Hart IR. Targeting of cytokine gene expression to malignant melanoma cells using tissue specific promoter sequences. Ann Oncol 1994; 5 (Suppl 4): 59-65.
25. Addison CL, Braciak T, Ralston R et al. Intratumoral injection of an adenovirus expressing interleukin-2 induces regression and immunity in a murine breast cancer model. Proc Natl Acad Sci USA 1995; 92: 8522-6.
26. Cao X, Zhang W, Gu S et al. Induction of antitumor immunity and treatment of preestablished tumor by interleukin-6-gene-transfected melanoma cells combined with low-dose interleukin-2. J Cancer Res Clin Oncol 1995; 121: 721-8.
27. Cao X, Wang J, Zhang W et al. Treatment of human hepatocellular carcinoma by fibroblast-mediated human interferon-α gene therapy in combination with adoptive chemoimmunotherapy. J Cancer Res Clin Oncol 1995; 121: 457-62.
28. Hurford RKJr, Dranoff G, Mulligan RC, Tepper RI. Gene therapy of metastatic cancer by in vivo retroviral gene targeting. Nature Genet 1995; 10: 430-5.
29. Missol E, Sochanik A, Szala S. Introduction of murine IL-4 gene into B16(F10) melanoma tumors by direct gene transfer with DNA-liposome complexes. Cancer Lett 1995; 97:189-93.
30. Sun WH, Burkholder JK, Sun J et al. In vivo cytokine gene transfer by gene gun reduces tumor growth in mice. Proc Natl Acad Sci USA 1995; 92: 2889-93.
31. Tahara H, Zitvogel L, Storkus WJ et al. Effective eradication of established murine tumors with IL-12 gene therapy using a polycistronic retroviral vector. J Immunol 1995; 154: 6466-74.
32. Tjuvajev J, Gansbacher B, Desai R et al. RG-2 glioma growth attenuation and severe brain edema caused by local production of interleukin-2 and interferon-γ. Cancer Res 1995; 55:1902-10.
33. Zatloukal K, Schneeberger A, Berger M et al. Elicitation of a systemic and protective anti-melanoma immune response by an IL-2-based vaccine. J Immunol 1995; 154: 3406-19.
34. Abdel-Wahab Z, Dar MM, Hester D et al. Effect of irradiation on cytokine production. MHC antigen expression, and vaccine potential of interleukin-2 and interferon-γ gene-modified melanoma cells. Cell Immunol 1996; 171: 246-54.
35. Arca MJ, Krauss JC, Aruga A et al. Therapeutic efficacy of T cells derived from lymph nodes draining a poorly immunogenic tumor transduced to secrete granulocyte-macrophage colony-stimulating factor. Cancer Gene Ther 1996; 3: 39-47.
36. Bramson JL, Hitt M, Addison CL et al. Direct intratumoral injection of an adenovirus expressing interleukin-12 induces regression and long-lasting immunity that is associated with highly localized expression of interleukin-12. Hum Gene Ther 1996; 7: 1995-2002.
37. Coveney E, Clary B, Iacobucci M et al. Active immunotherapy with transiently transfected cytokine-secreting tumor cells inhibits breast cancer metastases in tumor-bearing animals. Surgery 1996; 120: 265-73.
38. Egilmez NK, Cuenca R, Yokota SJ et al. In vivo cytokine gene therapy of human tumor xenografts in SCID mice by liposome-mediated DNA delivery. Gene Ther 1996; 3: 607-14.
39. Parker SE, Khatibi S, Margalith M et al. Plasmid DNA gene therapy: Studies with the human interleukin-2 gene in tumor cells in vitro and in the murine B16 melanoma model in vivo. Cancer Gene Ther 1996; 3: 175-85.
40. Qin H, Chatterjee SK. Cancer gene therapy using tumor cells infected with recombinant vaccinia virus expressing GM-CSF. Hum Gene Ther 1996; 7: 1853-60.
41. Rakhmilevich AL, Turner J, Ford MJ et al. Gene gun-mediated skin transfection with interleukin-12 gene results in regression of established primary and metastatic murine tumors. Proc Natl Acad Sci USA 1996; 93: 6291-6.
42. Sampson JH, Archer GE, Ashley DM et al. Subcutaneous vaccination with irradiated, cytokine-producing tumor cells stimulates CD8+ cell-mediated immunity against tumors located in the 'immunologically priviliged' central nervous system. Proc Natl Acad Sci USA 1996; 93: 10399-404.
43. Vagliani M, Rodolfo M, Cavallo F et al. Interleukin-12 potentiates the curative effect of a vaccine based on interleukin 2-transduced tumor cells. Cancer Res 1996; 56: 467-70.
44. Wang J, Cao X, Zhang W et al. Treatment of leukemia with fibroblast-mediated interferon-α gene therapy alone or in combination with doxorubicin. Leuk Res 1996; 20: 379-84.
45. Zhang JF, Hu C, Geng Y et al. Gene therapy with an adeno-associated virus carrying an interferon gene results in tumor growth suppression and regression. Cancer Gene Ther 1996; 3: 31-8.
46. Aruga E, Aruga A, Area MJ et al. Immune responsiveness to a murine mammary carcinoma modified to express B7-1, interleukin-12, or GM-CSF. Cancer Gene Ther 1997; 4: 157-66.
47. Aruga A, Aruga E, Chang AE. Reduced efficacy of allogeneic versus syngeneic fibroblasts modified to secrete cytokines as a tumor vaccine adjuvant. Cancer Res 1997; 57: 3230-7.
48. Chen L, Chen D, Block E et al. Eradication of murine bladder carcinoma by intratumor injection of a bicistronic adenoviral vector carrying cDNAs for the IL-12 heterodimer and its inhibition by the IL-12p40 subunit homodimer. J Immunol 1997; 159: 351-9.
49. Heike Y, Takahashi M, Ohira T et al. Genetic immunotherapy by intrapleural, intraperitoneal and subcutaneous injection of IL-2 gene-modified Lewis lung carcinoma cells. Int J Cancer 1997; 73: 844-9.
50. Hsieh C-L, Pang VF, Chen D-S, Hwang L-H. Regression of established mouse leukemia by GM-CSF-transduced tumor vaccine: Implications for cytotoxic T-lymphocyte responses and tumor burdens. Hum Gene Ther 1997; 8: 1843-54.
51. Moriguchi Y, Kan N, Okino T et al. The effectiveness of active specific immunotherapy using interferon-γ-gene-transduced tumor cells in a murine tumor model. Surg Today 1997; 27: 571-3.
52. Rakhmilevich AL, Janssen K, Turner J et al. Cytokine gene therapy of cancer using gene gun technology: Superior antitumor activity of interleukin-12. Hum Gene Ther 1997; 8: 1303-11.
53. Yu JS, Burwick JA, Dranoff G, Breakefield XO. Gene therapy for metastatic brain tumors by vaccination with granulocyte-macrophage colony-stimulating factor-transduced tumor cells. Hum Gene Ther 1997; 8: 1065-72.
54. Nanni P, Rossi I, De Giovanni C et al. Interleukin-12 gene therapy of MHC-negative murine melanoma metastases. Cancer Res 1998; 58: 1225-30.
55. Abdel-Wahab Z, Weltz C, Hester D et al. A phase I clinical trial of immunotherapy with interferon-γ gene-modified autologous melanoma cells. Cancer 1997; 80: 401-12.
56. Simons J, Jaffee E, Weber C et al. Bioactivity of autologous irradiated renal cell carcinoma vaccines generated by ex vivo granulocyte-macrophage colony-stimulating factor gene transfer. Cancer Res 1997; 57: 1537-46.
57. Belli F, Arienti F, Sule'-Suso J et al. Active immunization of metastatic melanoma patients with interleukin-2-transduced allogeneic melanoma cells: Evaluation of efficacy and tolerability. Cancer Immunol Immunother 1997; 44: 197-203.
58. Parmiani G, Arienti f, Sule'-Suso J et al. Cytokine-based gene therapy of human tumors. An overview. Folia Biol (Praha) 1996; 42: 305-9.
59. Roth JA, Cristiano RJ. Gene therapy for cancer: What have we done and where are we going? J Natl Cancer Inst 1997; 89: 21-39.
60. Human gene marker/therapy clinical protocols (complete updated listings). Hum Gene Ther 1997; 8: 2301-38.
61. Connor J, Bannerji R, Saito S et al. Regression of bladder tumors in mice treated with interleukin-2 gene-modified tumor cells. J Exp Med 1993; 177: 1127-34.
62. Kim TS, Russel SJ, Collins MKL, Cohen EP. Immunization with interleukin-2-secreting allogeneic mouse fibroblasts expressing melanoma-associated antigens prolongs the survival of mice with melanoma. Int J Cancer 1993; 55: 865-72.
63. Ohe Y, Podack ER, Olsen KJ et al. Combination effect of vaccination with IL-2 and IL-4 cDNA transfected cells on the induction of a therapeutic immune response against Lewis lung carcinoma cells. Int J Cancer 1993; 53: 432-7.
64. Nishihara K, Barth RF, Wilkie N et al. Increased in vitro and in vivo tumoricidal activity of a macrophage cell line genetically engineered to express IFN-γ, IL-4, IL-6, or TNF-α. Cancer Gene Ther 1995; 2: 113-24.
65. Porgador A, Tzehoval E, Vadai E et al. Combined vaccination with major histocompatibility class 1 and interleukin-2 gene-transduced melanoma cells synergizes the cure of postsurgical established lung metastases. Cancer Res 1995; 55: 4941-9.
66. Abe J, Wakimoto H, Tsunoda R et al. In vivo antitumor effect of cytotoxic T lymphocytes engineered to produce interferon-γ by adenovirus-mediated genetic transduction. Biochem Biophys Res Comm 1996; 218: 164-70.
67. Bausero MA, Panoskaltsis-Mortari A, Blazar BR, Katsanis E. Effective immunization against neuroblastoma using double-transduced tumor cells secreting GM-CSF and interferon-γ. J Immunother Emphasis Tumor Immunol 1996; 19: 113-24.
68. Chen S-H, Kosai K-I, Xu B et al. Combination suicide and cytokine gene therapy for hepatic metastases of colon carcinoma: Sustained antitumor immunity prolongs animal survival. Cancer Res 1996; 56: 3758-62.
69. Clary BM, Coveney EC, Blazer DJ III et al. Active immunotherapy of pancreatic cancer with tumor cells genetically engineered to secrete multiple cytokines. Surgery 1996; 120: 174-81.
70. Hollingsworth SJ, Darling D, Gaken J et al. The effect of combined expression of interleukin-2 and interleukin-4 on the tumorigenicity and treatment of B16F10 melanoma. Br J Cancer 1996; 74: 6-15.
71. Levitsky HI, Montgomery J, Ahmadzadeh M et al. Immunization with granulocyte-macrophage colony-stimulating factor-transduced, but not B7-1-transduced, lymphoma cells primes idiotype-specific T cells and generates potent systemic antitumor immunity. J Immunol 1996; 156: 3858-65.
72. Mullen CA, Petropoulos D, Lowe RM. Treatment of microscopic pulmonary metastases with recombinant autologous tumor vaccine expressing interleukin-6 and Escherichia coli cytosine deaminase suicide genes. Cancer Res 1996; 56: 1361-6.
73. Okada H, Miyamura K, Itoh T et al. Gene therapy against an experimental glioma using adeno-associated virus vectors. Gene Ther 1996; 3: 957-64.
74. Wakimoto H, Abe J, Tsunoda R et al. Intensified antitumor immunity by a cancer vaccine that produces granulocyte-macrophage colony-stimulating factor plus interleukin-4. Cancer Res 1996; 56: 1828-33.
75. Abdel-Wahab Z, Dar M, Osanto S et al. Eradication of melanoma pulmonary metastases by immunotherapy with tumor cells engineered to secrete interleukin-2 or γ-interferon. Cancer Gene Ther 1997; 4: 33-41.
76. Coll JL, Mesnil M, Lefebvre M-F et al. Long-term survival of immunocompetent rats with intraperitoneal colon carcinoma tumors using herpes simplex thymidine kinase/ganciclovir and IL-2 treatments. Gene Ther 1997; 4: 1160-6.
77. Fallarino F, Ashikari A, Boon T, Gajewski TF. Antigen-specific regression of established tumors induced by active immunization with irradiated IL-12-but not B7-1-transfected tumor cells. Int Immunol 1997; 9: 1259-69.
78. Gaken JA, Hollingsworth SJ, Hirst WJR et al. Irradiated NC Adenocarcinoma cells transduced with both B7.1 and interleukin-2 induce CD4+-mediated rejection of established tumors. Hum Gene Ther 1997; 8: 477-88.
79. Kwong Y-L, Chen S-H, Kosai K et al. Combination therapy with suicide and cytokine genes for hepatic metastases of lung cancer. Chest 1997; 112: 1332-7.
80. Parney IF, Petruk KC, Zhang C et al. Granulocyte-macrophage colony-stimulating factor and B7-2 combination immunogene therapy in an allogeneic Hu-PBL-SCID/Beige mouse-human glioblastoma multiforme model. Hum Gene Ther 1997; 8: 1073-85.
81. Santodonato L, D'Agostino G, Santini SM et al. Local and systemic antitumor response after combined therapy of mouse metastatic tumors with tumor cells expressing IFN-α and HSVtk: Perspectives for the generation of cancer vaccines. Gene Ther 1997; 4: 1246-55.
82. Sharma S, Miller PW, Stolina M et al. Multicomponent gene therapy vaccines for lung cancer: Effective eradication of established murine tumors in vivo with interleukin-7/herpes simplex thymidine kinase-transduced autologous tumor and ex vivo activated dendritic cells. Gene Ther 1997; 4: 1361-70.
83. Rossi I, Nicoletti G, Landuzzi L et al. Inhibition of lung colonisation of a mouse mammary carcinoma by therapeutic vaccination with interferon-α gene-transduced tumor cells. Clin Exp Metas 1998; 16: 123-8.
84. Nanni P, De Giovanni C, Nicoletti G et al. The immune response elicited by mammary adenocarcinoma cells transduced with interferon-γ and cytosine deaminase genes cures lung metastases by parental cells. Hum Gene Ther 1998; 9: 217-24.
85. Lollini P-L, De Giovanni C, Landuzzi L et al. Transduction of genes coding for a histocompatibility (MHC) antigen and for its physiological inducer interferon-γ in the same cell: Efficient MHC expression and inhibition of tumor and metastasis growth. Hum Gene Ther 1995; 6: 743-52.
86. Lollini P-L, D'Errico A, De Giovanni C et al. Systemic effects of cytokines released by gene-transduced tumor cells: Marked hyperplasia induced in small bowel by γ-interferon transfectants through host's lymphocytes. Int J Cancer 1995; 61: 425-30.