Strict requirement for vector-induced type I interferon in efficacious antitumor responses to virally encoded IL12

Cancer Research

Volumn 75, Issue 3, 2015, Pages 497-507

  Melero, Ignacio ^a   Quetglas, Jose I ^a   Reboredo, Mercedes ^b   Dubrot, Juan ^a   Rodriguez Madoz, Juan R ^a   Mancheño, Uxua ^a   Casales, Erkuden ^a   Riezu Boj, Jose I ^a   Ruiz Guillen, Marta ^a   Ochoa, Maria C ^a   Sanmamed, Miguel F ^a   Thieblemont, Nathalie ^c   Smerdou, Cristian ^a   Hervas Stubbs, Sandra ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY CLINIC OF NAVARRA   (Spain)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERFERON; INTERFERON RECEPTOR; INTERLEUKIN 2; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; VIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW STROMA CELL; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; DRUG RESPONSE; FEMALE; HEMATOPOIETIC CELL; INTERFERON PRODUCTION; MACROPHAGE; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEMLIKI FOREST ALPHAVIRUS; SIGNAL TRANSDUCTION; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; WILD TYPE;

EID: 84964306138     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3356     Document Type: Article

References (51)

1. Teng MW, Vesely MD, Duret H, McLaughlin N, Towne JE, Schreiber RD, et al. Opposing roles for IL-23 and IL-12 in maintaining occult cancer in an equilibrium state. Cancer Res 2012;72:3987-96.
2. Del Vecchio M, Bajetta E, Canova S, Lotze MT, Wesa A, Parmiani G, et al. Interleukin-12: Biological properties and clinical application. Clin Cancer Res 2007;13:4677-85.
3. Curtsinger JM, Lins DC, Mescher MF. Signal 3 determines tolerance versus full activation of naive CD8 T cells: Dissociating proliferation and development of effector function. J Exp Med 2003;197:1141-51.
4. Wesa A, Kalinski P, Kirkwood JM, Tatsumi T, Storkus WJ. Polarized type-1 dendritic cells (DC1) producing high levels of IL-12 family members rescue patient TH1-type antimelanoma CD4+T cell responses in vitro. J Immunother 2007;30:75-82.
5. Zilocchi C, Stoppacciaro A, Chiodoni C, Parenza M, Terrazzini N, Colombo MP. Interferon gamma-independent rejection of interleukin 12-transduced carcinoma cells requires CD4+ T cells and granulocyte/macrophage colony-stimulating factor. J Exp Med 1998;188:133-43.
6. Atkins MB, Robertson MJ, Gordon M, Lotze MT, DeCoste M, DuBois JS, et al. Phase I evaluation of intravenous recombinant human interleukin 12 in patients with advanced malignancies. Clin Cancer Res 1997;3:409-17.
7. Gollob JA, Veenstra KG, Mier JW, Atkins MB. Agranulocytosis and hemolytic anemia in patients with renal cell cancer treated with interleukin-12. J Immunother 2001;24:91-8.
8. Wadler S, Levy D, Frederickson HL, Falkson CI, Wang Y, Weller E, et al. A phase II trial of interleukin-12 in patients with advanced cervical cancer: Clinical and immunologic correlates. eastern cooperative oncology group study E1E96. Gynecol Oncol 2004;92:957-64.
9. Robertson MJ, Cameron C, Atkins MB, Gordon MS, Lotze MT, Sherman ML, et al. Immunological effects of interleukin 12 administered by bolus intravenous injection to patientswith cancer. Clin Cancer Res 1999;5:9-16.
10. Leonard JP, Sherman ML, Fisher GL, Buchanan LJ, Larsen G, Atkins MB, et al. Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-gamma production. Blood 1997;90:2541-8.
11. van Herpen CM, Looman M, Zonneveld M, Scharenborg N, de Wilde PC, vande Locht L, et al. Intratumoral administration of recombinant human interleukin 12 in head and neck squamous cell carcinoma patients elicits a T-helper 1 profile in the locoregional lymph nodes. Clin Cancer Res 2004;10:2626-35.
12. Sangro B, Melero I, Qian C, Prieto J. Gene therapy of cancer based on interleukin 12. Curr Gene Ther 2005;5:573-81.
13. Pegram HJ, Lee JC, Hayman EG, Imperato GH, Tedder TF, Sadelain M, et al. Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning. Blood 2012;119:4133-41.
14. Barajas M, Mazzolini G, Genove G, Bilbao R, Narvaiza I, Schmitz V, et al. Gene therapy of orthotopic hepatocellular carcinoma in rats using adenovirus coding for interleukin 12. Hepatology 2001;33:52-61.
15. Tahara H, Zitvogel L, Storkus WJ, Zeh HJ 3rd, McKinney TG, Schreiber RD, et al. Effective eradication of established murine tumors with IL-12 gene therapy using a polycistronic retroviral vector. J Immunol 1995;154:6466-74.
16. Quetglas JI, Ruiz-Guillen M, Aranda A, Casales E, Bezunartea J, Smerdou C. Alphavirus vectors for cancer therapy. Virus Res 2010;153:179-96.
17. Rodriguez-Madoz JR, Prieto J, Smerdou C. Semliki forest virus vectors engineered to express higher IL-12 levels induce efficient elimination of murine colon adenocarcinomas. Mol Ther 2005;12:153-63.
18. Guan M, Rodriguez-Madoz JR, Alzuguren P, Gomar C, Kramer MG, Kochanek S, et al. Increased efficacy and safety in the treatment of experimental liver cancer with a novel adenovirus-alphavirus hybrid vector. Cancer Res 2006;66:1620-9.
19. Liljestrom P, Garoff H. A new generation of animal cell expression vectors based on the Semliki forest virus replicon. Biotechnology (N Y) 1991;9:1356-61.
20. Rodriguez-Madoz JR, Liu KH, Quetglas JI, Ruiz-Guillen M, Otano I, Crettaz J, et al. Semliki forest virus expressing interleukin-12 induces antiviral and antitumoral responses in woodchucks with chronic viral hepatitis and hepatocellular carcinoma. J Virol 2009;83:12266-78.
21. Huarte E, Larrea E, Hernandez-Alcoceba R, Alfaro C, Murillo O, Arina A, et al. Recombinant adenoviral vectors turn on the type I interferon system without inhibition of transgene expression and viral replication. Mol Ther 2006;14:129-38.
22. Hervas-Stubbs S, Perez-Gracia JL, Rouzaut A, Fernandez de Sanmamed M, Le Bon A, Melero IJ. Direct effects of type I IFNs on cells of the immune system. Clin Cancer Res 2011;17:2619-27.
23. Bekisz J, Baron S, Balinsky C, Morrow A, Zoon KC. Antiproliferative properties of type I and type II interferon. Pharmaceuticals (Basel) 2010;3:994-1015.
24. Le Bon A, Etchart N, Rossmann C, Ashton M, Hou S, Gewert D, et al. Crosspriming of CD8+T cells stimulated by virus-induced type I interferon. Nat Immunol 2003;4:1009-15.
25. Trinchieri G, Santoli D, Granato D, Perussia B. Antagonistic effects of interferons on the cytotoxicity mediated by natural killer cells. Fed Proc 1981;40:2705-10.
26. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 2005;202:637-50.
27. Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J Immunol 2005;174:4465-9.
28. Gresser I, Belardelli F, Maury C, Maunoury MT, Tovey MG. Injection of mice with antibody to interferon enhances the growth of transplantable murine tumors. J Exp Med 1983;158:2095-107.
29. Dunn GP, Bruce AT, Sheehan KC, Shankaran V, Uppaluri R, Bui JD, et al. A critical function for type I interferons in cancer immunoediting. Nat Immunol 2005;6:722-9.
30. Neidhart JA, Gagen MM, Young D, Tuttle R, Melink TJ, Ziccarrelli A, et al. Interferon-alpha therapy of renal cancer. Cancer Res 1984;44:4140-3.
31. Motzer RJ, Bacik J, Murphy BA, Russo P, Mazumdar M. Interferon-alfa as a comparative treatment for clinical trials of new therapies against advanced renal cell carcinoma. J Clin Oncol 2002;20:289-96.
32. Sterman DH, Recio A, Haas AR, Vachani A, Katz SI, Gillespie CT, et al. A phase I trial of repeated intrapleural adenoviral-mediated interferon-beta gene transfer formesothelioma and metastatic pleural effusions. Mol Ther 2010;18:852-60.
33. Sterman DH, Haas A, Moon E, Recio A, Schwed D, Vachani A, et al. A trial of intrapleural adenoviral-mediated interferon-alpha2b gene transfer for malignant pleural mesothelioma. Am J Respir Crit Care Med 2011;184:1395-9.
34. Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011;208:1989-2003.
35. Fuertes MB, Kacha AK, Kline J, Woo SR, Kranz DM, Murphy KM, et al. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8{alpha}+ dendritic cells. J Exp Med 2011;208:2005-16.
36. Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, et al. The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res 2011;71:2488-96.
37. Alsharifi M, Lobigs M, Regner M, Lee E, Koskinen A, Mullbacher A. Type I interferons trigger systemic, partial lymphocyte activation in response to viral infection. J Immunol 2005;175:4635-40.
38. Kawasaki T, Kawai T, Akira S. Recognition of nucleic acids by pattern-recognition receptors and its relevance in autoimmunity. Immunol Rev 2011;243:61-73.
39. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011;34:637-50.
40. Blasius AL, Giurisato E, Cella M, Schreiber RD, Shaw AS, Colonna M. Bone marrow stromal cell antigen 2 is a speci fic marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J Immunol 2006;177:3260-5.
41. Zeisberger SM, Odermatt B, Marty C, Zehnder-Fjallman AH, Ballmer-Hofer K, Schwendener RA. Clodronate-liposome-mediated depletion of tumour-associated macrophages: Anew and highly effective antiangiogenic therapy approach. Br J Cancer 2006;95:272-81.
42. Hervas-Stubbs S, Riezu-Boj JI, Mancheno U, Rueda P, Lopez L, Alignani D, et al. Conventional but not plasmacytoid dendritic cells foster the systemic virus-induced type I IFN response needed for efficient CD8 T cell priming. J Immunol 2014;193:1151-61.
43. Quetglas JI, Dubrot J, Bezunartea J, Sanmamed MF, Hervas-Stubbs S, Smerdou C, et al. Immunotherapeutic synergy between anti-CD137 mAb and intratumoral administration of a cytopathic semliki forest virus encoding IL-12. Mol Ther 2012;20:1664-75.
44. Hidmark AS, Nordstrom EK, Dosenovic P, Forsell MN, Liljestrom P, Karlsson Hedestam GB. Humoral responses against coimmunized protein antigen but not against alphavirus-encoded antigens require alpha/beta interferon signaling. J Virol 2006;80:7100-10.
45. Diebold SS, Schulz O, Alexopoulou L, Leitner WW, Flavell RA, Reise Sousa C. Role of TLR3 in the immunogenicity of replicon plasmid-based vaccines. Gene Ther 2009;16:359-66.
46. Barchet W, Cella M, Odermatt B, Asselin-Paturel C, Colonna M, Kalinke U. Virus-induced interferon alpha production by a dendritic cell subset in the absence of feedback signaling in vivo. J Exp Med 2002;195:507-16.
47. Swann JB, Hayakawa Y, Zerafa N, Sheehan KC, Scott B, Schreiber RD, et al. Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J Immunol 2007;178:7540-9.
48. Mescher MF, Curtsinger JM, Agarwal P, Casey KA, Gerner M, Hammerbeck CD, et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev 2006;211:81-92.
49. Morales JK, Kmieciak M, Knutson KL, Bear HD, Manjili MH. GM-CSF is one of the main breast tumor-derived soluble factors involved in the differentiation of CD11b-Gr1-bone marrow progenitor cells into myeloidderived suppressor cells. Breast Cancer Res Treat 2010;123:39-49.
50. Bayne LJ, Beatty GL, Jhala N, Clark CE, Rhim AD, Stanger BZ, et al. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer Cell 2012;21:822-35.
51. Garrity T, Pandit R, Wright MA, Benefield J, Keni S, Young MR. Increased presence of CD34+ cells in the peripheral blood of head and neck cancer patients and their differentiation into dendritic cells. Int J Cancer 1997;73:663-9.