Gene-modified tumor vaccine secreting a designer cytokine Hyper-Interleukin-6 is an effective therapy in mice bearing orthotopic renal cell cancer

Cancer Gene Therapy

Volumn 17, Issue 7, 2010, Pages 465-475

  Wysocki, P J ^a,b   Kazimierczak, U ^a   Suchorska, W ^a   Kotlarski, M ^a   Malicki, J ^a   MacKiewicz, A ^a,b  

^a POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

^b BioContract Sp Z Oo   (Poland)

Author keywords

Gene modified vaccine; Hyper interleukin 6; Immunogene therapy; Renal cell cancer

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; RENCA H6 VACCINE; TRANSCRIPTION FACTOR FOXP3; TUMOR VACCINE; UNCLASSIFIED DRUG; CANCER VACCINE; CYTOKINE;

ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; GENE VECTOR; IMMUNE RESPONSE; KIDNEY CANCER; LENTIVIRINAE; MEMORY CELL; MODULATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; CARCINOMA, RENAL CELL; DISEASE MODEL; GENETICS; HUMAN; IMMUNOGENETICS; IMMUNOLOGY; KIDNEY NEOPLASMS; PATHOLOGY; SURVIVAL; TUMOR CELL LINE;

ANIMALS; CANCER VACCINES; CARCINOMA, RENAL CELL; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNOGENETICS; INTERLEUKIN-6; KIDNEY NEOPLASMS; MICE; MICE, INBRED BALB C; SURVIVAL ANALYSIS;

ANIMALIA; MURINAE; MUS;

EID: 77953699967     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2010.2     Document Type: Article

References (54)

1. Hudes G, Carducci M, Tomczak P, Dutcher J, Figlin R, Kapoor A et al. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N Engl J Med 2007; 356: 2271-2281.
2. Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Rixe O et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 2007; 356: 115-124.
3. Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebels M et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007; 356: 125-134.
4. Wysocki PJ, Zolnierek J, Szczylik C, Mackiewicz A. Targeted therapy of renal cell cancer. Curr Opin Investig Drugs 2008; 9: 570-575.
5. Motzer RJ, Rini BI, Bukowski RM, Curti BD, George DJ, Hudes GR et al. Sunitinib in patients with metastatic renal cell carcinoma. JAMA 2006; 295: 2516-2524.
6. Mach N, Dranoff G. Cytokine-secreting tumor cell vaccines. Curr Opin Immunol 2000; 12: 571-575.
7. Ward S, Casey D, Labarthe MC, Whelan M, Dalgleish A, Pandha H et al. Immunotherapeutic potential of whole tumour cells. Cancer Immunol Immunother 2002; 51: 351-357.
8. Scheffer SR, Nave H, Korangy F, Schlote K, Pabst R, Jaffee EM et al. Apoptotic, but not necrotic, tumor cell vaccines induce a potent immune response in vivo. Int J Cancer 2003; 103: 205-211.
9. Porgador A, Tzehoval E, Katz A, Vadai E, Revel M, Feldman M et al. Interleukin 6 gene transfection into Lewis lung carcinoma tumor cells suppresses the malignant phenotype and confers immunotherapeutic competence against parental metastatic cells. Cancer Res 1992; 52: 3679-3686.
10. Ledda MF, Adris S, Bravo AI, Bover L, Carbone C, Paleolog E et al. Tumor cells engineered to express interleukin-6 exhibit a reduced tumorigenicity depending on the tumor cell model. Cell Mol Biol (Noisy-le-grand) 1996; 42: 769-778.
11. Wysocki PJ, Kowalczyk DW, Izycki D, Grabarczyk P, Kwias Z, Mackiewicz A. IL-6 and GM-CSF in tumor rejection model of renal cell cancer. Adv Exp Med Biol 2001; 495: 379-383.
12. Taga T, Kishimoto T. Gp130 and the interleukin-6 family of cytokines. Annu Rev Immunol 1997; 15: 797-819.
13. Mackiewicz A, Schooltink H, Heinrich PC, Rose-John S. Complex of soluble human IL-6-receptor/IL-6 up-regulates expression of acute-phase proteins. J Immunol 1992; 149: 2021-2027.
14. Peters M, Blinn G, Solem F, Fischer M, Meyer zum Buschenfelde KH, Rose-John S. In vivo and in vitro activities of the gp130-stimulating designer cytokine Hyper-IL-6. J Immunol 1998; 161: 3575-3581.
15. Kowalczyk DW, Wlazlo AP, Shane S, Ertl HC. Vaccine regimen for prevention of sexually transmitted infections with human papillomavirus type 16. Vaccine 2001; 19: 3583-3590.
16. Weiss J, Zimmermann F. Tribromoethanol (Avertin) as an anaesthetic in mice. Lab Anim 1999; 33: 192-193.
17. Ahn KS, Jung YS, Kim J, Lee H, Yoon SS. Behavior of murine renal carcinoma cells grown in ectopic or orthotopic sites in syngeneic mice. Tumour Biol 2001; 22: 146-153.
18. Wysocki PJ, Kwiatkowska EP, Kazimierczak U, Suchorska W, Kowalczyk DW, Mackiewicz A. Captopril, an angioten-sin-converting enzyme inhibitor, promotes growth of immunogenic tumors in mice. Clin Cancer Res 2006; 12: 4095-4102.
19. Vieweg J, Heston WD, Gilboa E, Fair WR. An experimental model simulating local recurrence and pelvic lymph node metastasis following orthotopic induction of prostate cancer. Prostate 1994; 24: 291-298.
20. Tan MH, Holyoke ED, Goldrosen MH. Murine colon adenocarcinoma: syngeneic orthotopic transplantation and subsequent hepatic metastases. J Natl Cancer Inst 1977; 59: 1537-1544.
21. Ali SA, McLean CS, Boursnell ME, Martin G, Holmes CL, Reeder S et al. Preclinical evaluation of "whole" cell vaccines for prophylaxis and therapy using a disabled infectious single cycle-herpes simplex virus vector to transduce cytokine genes. Cancer Res 2000; 60: 1663-1670.
22. Wagner JR, Walther MM, Linehan WM, White DE, Rosenberg SA, Yang JC. Interleukin-2 based immunother-apy for metastatic renal cell carcinoma with the kidney in place. J Urol 1999; 162: 43-45.
23. Sella A, Swanson DA, Ro JY, Putnam Jr JB, Amato RJ, Markowitz AB et al. Surgery following response to inter-feron-alpha-based therapy for residual renal cell carcinoma. J Urol 1993; 149: 19-21; discussion 21-112
24. Hara I, Nagai H, Miyake H, Yamanaka K, Hara S, Micallef MJ et al. Effectiveness of cancer vaccine therapy using cells transduced with the interleukin-12 gene combined with systemic interleukin-18 administration. Cancer Gene Ther 2000; 7: 83-90.
25. Kausch I, Jiang H, Brocks C, Bruderek K, Kruger S, Sczakiel G et al. Ki-67-directed antisense therapy in an orthotopic renal cell carcinoma model. Eur Urol 2004; 46: 118-124; discussion 124-125.
26. Chagnon F, Thompson-Snipes L, Elhilali M, Tanguay S. Murine renal cell carcinoma: evaluation of a dendritic-cell tumour vaccine. BJU Int 2001; 88: 418-424.
27. Chagnon F, Tanguay S, Ozdal OL, Guan M, Ozen ZZ, Ripeau JS et al. Potentiation of a dendritic cell vaccine for murine renal cell carcinoma by CpG oligonucleotides. Clin Cancer Res 2005; 11: 1302-1311.
28. Wysocki PJ, Grabarczyk P, Mackiewicz-Wysocka M, Kowalczyk DW, Mackiewicz A. Genetically modified dendritic cells\a new, promising cancer treatment strategy? Expert Opin Biol Ther 2002; 2: 835-845.
29. Wysocki PJ, Karczewska-Dzionk A, Mackiewicz-Wysocka M, Mackiewicz A. Human cancer gene therapy with cytokine gene-modified cells. Expert Opin Biol Ther 2004; 4: 1595-1607.
30. Wysocki PJ, Zolnierek J, Szczylik C, Mackiewicz A. Recent developments in renal cell cancer immunotherapy. Expert Opin Biol Ther 2007; 7: 727-737.
31. Shibata J, Murakami K, Abe M, Hashimoto A, Utsugi T, Fukushima M et al. Life prolonging effect of antitumor agents on postoperative adjuvant therapy in the lung spontaneous metastasis model in mice. Anticancer Res 1998; 18: 1203-1209.
32. Medical Research Council Renal Cancer Collaborators. Interferon-alpha and survival in metastatic renal carcinoma: early results of a randomised controlled trial. Lancet 1999; 353: 14-17.
33. Levy DA, Slaton JW, Swanson DA, Dinney CP. Stage specific guidelines for surveillance after radical nephrectomy for local renal cell carcinoma. J Urol 1998; 159: 1163-1167.
34. Linehan WM, Shipley WU, Parkinson DR. Cancer of the kidney and urether. In: DeVita VT, Hellman S, Rosenberg SA (eds). Cancer: Principles and Practice of Oncology, 5th edn, Lippincott-Raven: Philadelphia, 1997, pp 858-911.
35. Ljungberg B, Alamdari FI, Rasmuson T, Roos G. Follow-up guidelines for nonmetastatic renal cell carcinoma based on the occurrence of metastases after radical nephrectomy. BJU Int 1999; 84: 405-411.
36. Salup RR, Back TC, Wiltrout RH. Successful treatment of advanced murine renal cell cancer by bicompartmental adoptive chemoimmunotherapy. J Immunol 1987; 138: 641-647.
37. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252.
38. Ozbek S, Peters M, Breuhahn K, Mann A, Blessing M, Fischer M et al. The designer cytokine hyper-IL-6 mediates growth inhibition and GM-CSF-dependent rejection of B16 melanoma cells. Oncogene 2001; 20: 972-979.
39. Drakesmith H, O'Neil D, Schneider SC, Binks M, Medd P, Sercarz E et al. In vivo priming of T cells against cryptic determinants by dendritic cells exposed to interleukin 6 and native antigen. Proc Natl Acad Sci USA 1998; 95: 14903-14908.
40. Shevach EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002; 2: 389-400.
41. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N et al. Conversion of peripheral CD4+CD25\naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. JExp Med2003; 198: 1875-1886.
42. Pyzik M, Piccirillo CA. TGF-beta1 modulates Foxp3 expression and regulatory activity in distinct CD4+ T cell subsets. J Leukoc Biol 2007; 82: 335-346.
43. Zhang Q, Rubenstein JN, Liu VC, Park I, Jang T, Lee C. Restoration of expression of transforming growth factor-beta type II receptor in murine renal cell carcinoma (renca) cells by 5-Aza-2'-deoxycytidine. Life Sci 2005; 76: 1159-1166.
44. Sonouchi K, Hamilton TA, Tannenbaum CS, Tubbs RR, Bukowski R, Finke JH. Chemokine gene expression in the murine renal cell carcinoma, RENCA, following treatment in vivo with interferon-alpha and interleukin-2. Am J Pathol 1994; 144: 747-755.
45. Chen X, Das R, Komorowski R, Beres A, Hessner MJ, Mihara M et al. Blockade of interleukin-6 signaling augments regulatory T-cell reconstitution and attenuates the severity of graft-versus-host disease. Blood 2009; 114: 891-900.
46. Dominitzki S, Fantini MC, Neufert C, Nikolaev A, Galle PR, Scheller J et al. Cutting edge: trans-signaling via the soluble IL-6R abrogates the induction of FoxP3 in naive CD4+CD25 T cells. J Immunol 2007; 179: 2041-2045.
47. Mendiratta SK, Quezada A, Matar M, Thull NM, Bishop JS, Nordstrom JL et al. Combination of interleukin 12 and interferon alpha gene therapy induces a synergistic antitumor response against colon and renal cell carcinoma. Hum Gene Ther 2000; 11: 1851-1862.
48. Izycki D, Nawrocki S, Laciak M, Gryska K, Baksalary-Izycka K, Mackiewicz A. Effect of cyclophosphamide on tumorogenesis of the IL-6 and Hyper-IL-6 gene modified murine melanoma cells. Wspolczesna Onkologia 2004; 8: 124-131.
49. Hillman GG, Younes E, Visscher D, Hamzavi F, Kim S, Lam JS et al. Inhibition of murine renal carcinoma pulmonary metastases by systemic administration of inter-feron gamma: mechanism of action and potential for combination with interleukin 4. Clin Cancer Res 1997; 3: 1799-1806.
50. Qin Z, Blankenstein T. CD4+ T cell\mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhemato-poietic cells. Immunity 2000; 12: 677-686.
51. Qin Z, Schwartzkopff J, Pradera F, Kammertoens T, Seliger B, Pircher H et al. A critical requirement of interferon gamma-mediated angiostasis for tumor rejection by CD8+ T cells. Cancer Res 2003; 63: 4095-4100.
52. Lefrancois L, Marzo AL. The descent of memory T-cell subsets. Nat Rev Immunol 2006; 6: 618-623.
53. Seder RA, Ahmed R. Similarities and differences in CD4+ and CD8+ effector and memory T cell generation. Nat Immunol 2003; 4: 835-842.
54. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003; 4: 225-234.