Type i IFN gene delivery suppresses regulatory T cells within tumors

Cancer Gene Therapy

Volumn 21, Issue 12, 2014, Pages 532-541

  Hashimoto, H ^a   Ueda, R ^a   Narumi, K ^a   Heike, Y ^b   Yoshida, T ^a   Aoki, K ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b Clinical Trials Committee   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ALPHA INTERFERON; CD4 ANTIGEN; CD8 ANTIGEN; GLYCOPROTEIN P 15095; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; TRANSCRIPTION FACTOR FOXP3; INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; GENE EXPRESSION; GENE TRANSFER; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; VIRAL GENE DELIVERY SYSTEM; ADENOVIRIDAE; ADMINISTRATION AND DOSAGE; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE COURSE; GENE THERAPY; GENE VECTOR; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; LYMPHOCYTE COUNT; MALE; METABOLISM; NEOPLASMS; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALIA; MUS;

ADENOVIRIDAE; ANIMALS; CELL LINE, TUMOR; DISEASE PROGRESSION; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HUMANS; IMMUNOMODULATION; INTERFERON TYPE I; INTERFERON-ALPHA; INTERLEUKIN-6; LYMPHOCYTE COUNT; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICE; NEOPLASMS; RECEPTORS, INTERLEUKIN-6; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TUMOR BURDEN;

EID: 84925933497     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2014.60     Document Type: Article

References (47)

1. Gonzalez-Navajas JM, Lee J, David M, Raz E. Immunomodulatory functions of type I interferons. Nat Rev Immunol 2012; 12: 125-135.
2. Ferrantini M, Capone I, Belardelli F. Interferon-alpha and cancer: mechanisms of action and new perspectives of clinical use. Biochimie 2007; 89: 884-893.
3. Rizza P, Moretti F, Belardelli F. Recent advances on the immunomodulatory effects of IFN-alpha: implications for cancer immunotherapy and autoimmunity. Autoimmunity 2010; 43: 204-209.
4. Escobar G, Moi D, Ranghetti A, Ozkal-Baydin P, Squadrito ML, Kajaste-Rudnitski A et al. Genetic engineering of hematopoiesis for targeted IFN-alpha delivery inhibits breast cancer progression. Sci Transl Med 2014; 6: 217ra3.
5. Narumi K, Kondoh A, Udagawa T, Hara H, Goto N, Ikarashi Y et al. Administration route-dependent induction of antitumor immunity by interferon-alpha gene transfer. Cancer Sci 2010; 101: 1686-1694.
6. Ohashi M, Yoshida K, Kushida M, Miura Y, Ohnami S, Ikarashi Y et al. Adenovirusmediated interferon alpha gene transfer induces regional direct cytotoxicity and possible systemic immunity against pancreatic cancer. Bri J Cancer 2005; 93: 441-449.
7. Hatanaka K, Suzuki K, Miura Y, Yoshida K, Ohnami S, Kitade Y et al. Interferonalpha and antisense K-ras RNA combination gene therapy against pancreatic cancer. J Gene Med 2004; 6: 1139-1148.
8. Hara H, Kobayashi A, Yoshida K, Ohashi M, Ohnami S, Uchida E et al. Local interferon-alpha gene therapy elicits systemic immunity in a syngeneic pancreatic cancer model in hamster. Cancer Sci 2007; 98: 455-463.
9. Udagawa T, Narumi K, Goto N, Aida K, Suzuki K, Ochiya T et al. Syngeneic hematopoietic stem cell transplantation enhances the antitumor immunity of intratumoral type I interferon gene transfer for sarcoma. Hum Gene Ther 2012; 23: 173-186.
10. Belardelli F, Ferrantini M, Proietti E, Kirkwood JM. Interferon-alpha in tumor immunity and immunotherapy. Cytokine Growth Factor Rev 2002; 13: 119-134.
11. Burdick LM, Somani N, Somani AK. Type I IFNs and their role in the development of autoimmune diseases. Expert Opin Drug Saf 2009; 8: 459-472.
12. Santini SM, Lapenta C, Santodonato L, D'Agostino G, Belardelli F, Ferrantini M. IFNalpha in the generation of dendritic cells for cancer immunotherapy. Handb Exp Pharmacol 2009; 188: 295-317.
13. Kobayashi N, Hiraoka N, Yamagami W, Ojima H, Kanai Y, Kosuge T et al. FOXP3+ regulatory T cells affect the development and progression of hepatocarcinogenesis. Clin Cancer Res 2007; 13: 902-911.
14. Jacobs JF, Nierkens S, Figdor CG, de Vries IJ, Adema GJ. Regulatory T cells in melanoma: the final hurdle towards effective immunotherapy? Lancet Oncol 2012; 13: e32-e42.
15. Byrne WL, Mills KH, Lederer JA, O'Sullivan GC. Targeting regulatory T cells in cancer. Cancer Res 2011; 71: 6915-6920.
16. Lal G, Zhang N, van der Touw W, Ding Y, Ju W, Bottinger EP et al. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol 2009; 182: 259-273.
17. Cucak H, Yrlid U, Reizis B, Kalinke U, Johansson-Lindbom B. Type I interferon signaling in dendritic cells stimulates the development of lymph-node-resident T follicular helper cells. Immunity 2009; 31: 491-501.
18. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci USA 2005; 102: 18538-18543.
19. Gnerlich JL, Mitchem JB, Weir JS, Sankpal NV, Kashiwagi H, Belt BA et al. Induction of Th17 cells in the tumor microenvironment improves survival in a murine model of pancreatic cancer. J Immunol 2010; 185: 4063-4071.
20. Sharma MD, Hou DY, Liu Y, Koni PA, Metz R, Chandler P et al. Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumordraining lymph nodes. Blood 2009; 113: 6102-6111.
21. Bacher N, Raker V, Hofmann C, Graulich E, Schwenk M, Baumgrass R et al. Interferon-alpha suppresses cAMP to disarm human regulatory T cells. Cancer Res 2013; 73: 5647-5656.
22. Bacher N, Graulich E, Jonuleit H, Grabbe S, Steinbrink K. Interferon-alpha abrogates tolerance induction by human tolerogenic dendritic cells. PloS One 2011; 6: e22763.
23. Pace L, Vitale S, Dettori B, Palombi C, La Sorsa V, Belardelli F et al. APC activation by IFN-alpha decreases regulatory T cell and enhances Th cell functions. J Immunol 2010; 184: 5969-5979.
24. Dong C. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol 2008; 8: 337-348.
25. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006; 126: 1121-1133.
26. Yang XO, Pappu BP, Nurieva R, Akimzhanov A, Kang HS, Chung Y et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 2008; 28: 29-39.
27. Xu L, Kitani A, Fuss I, Strober W. Cutting edge: regulatory T cells induce CD4 +CD25-Foxp3-T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol 2007; 178: 6725-6729.
28. Yang XO, Nurieva R, Martinez GJ, Kang HS, Chung Y, Pappu BP et al. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 2008; 29: 44-56.
29. Zheng SG, Wang J, Horwitz DA. Cutting edge: Foxp3+CD4+CD25+ regulatory T cells induced by IL-2 and TGF-beta are resistant to Th17 conversion by IL-6. J Immunol 2008; 180: 7112-7116.
30. Bollrath J, Phesse TJ, von Burstin VA, Putoczki T, Bennecke M, Bateman T et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cellcycle progression during colitis-associated tumorigenesis. Cancer Cell 2009; 15: 91-102.
31. Grivennikov S, Karin M. Autocrine IL-6 signaling: a key event in tumorigenesis? Cancer Cell 2008; 13: 7-9.
32. Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009; 15: 103-113.
33. Naugler WE, Karin M. The wolf in sheep's clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol Med 2008; 14: 109-119.
34. Bromberg J, Wang TC. Inflammation and cancer: IL-6 and STAT3 complete the link. Cancer Cell 2009; 15: 79-80.
35. Anglesio MS, George J, Kulbe H, Friedlander M, Rischin D, Lemech C et al. IL6-STAT3-HIF signaling and therapeutic response to the angiogenesis inhibitor sunitinib in ovarian clear cell cancer. Clin Cancer Res 2011; 17: 2538-2548.
36. Kulbe H, Thompson R, Wilson JL, Robinson S, Hagemann T, Fatah R et al. The inflammatory cytokine tumor necrosis factor-alpha generates an autocrine tumorpromoting network in epithelial ovarian cancer cells. Cancer Res 2007; 67: 585-592.
37. Song L, Rawal B, Nemeth JA, Haura EB. JAK1 activates STAT3 activity in non-smallcell lung cancer cells and IL-6 neutralizing antibodies can suppress JAK1-STAT3 signaling. Mol Cancer Ther 2011; 10: 481-494.
38. Guo Y, Nemeth J, O'Brien C, Susa M, Liu X, Zhang Z et al. Effects of siltuximab on the IL-6-induced signaling pathway in ovarian cancer. Clin Cancer Res 2010; 16: 5759-5769.
39. Chari A, Pri-Chen H, Jagannath S. Complete remission achieved with single agent CNTO 328, an anti-IL-6 monoclonal antibody, in relapsed and refractory myeloma. Clin Lymphoma Myeloma Leukemia 2013; 13: 333-337.
40. Rossi JF, Negrier S, James ND, Kocak I, Hawkins R, Davis H et al. A phase I/II study of siltuximab (CNTO 328), an anti-interleukin-6 monoclonal antibody, in metastatic renal cell cancer. Bri J Cancer 2010; 103: 1154-1162.
41. Fizazi K, De Bono JS, Flechon A, Heidenreich A, Voog E, Davis NB et al. Randomised phase II study of siltuximab (CNTO 328), an anti-IL-6 monoclonal antibody, in combination with mitoxantrone/prednisone versus mitoxantrone/prednisone alone in metastatic castration-resistant prostate cancer. Eur J Cancer 2012; 48: 85-93.
42. Mule JJ, Custer MC, Travis WD, Rosenberg SA. Cellular mechanisms of the antitumor activity of recombinant IL-6 in mice. J Immunol 1992; 148: 2622-2629.
43. Mullen CA, Coale MM, Levy AT, Stetler-Stevenson WG, Liotta LA, Brandt S et al. Fibrosarcoma cells transduced with the IL-6 gene exhibited reduced tumorigenicity, increased immunogenicity, and decreased metastatic potential. Cancer Res 1992; 52: 6020-6024.
44. 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.
45. Fisher DT, Chen Q, Skitzki JJ, Muhitch JB, Zhou L, Appenheimer MM et al. IL-6 trans-signaling licenses mouse and human tumor microvascular gateways for trafficking of cytotoxic T cells. J Clin Invest 2011; 121: 3846-3859.
46. Wang L, Yi T, Kortylewski M, Pardoll DM, Zeng D, Yu H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med 2009; 206: 1457-1464.
47. Martin-Orozco N, Muranski P, Chung Y, Yang XO, Yamazaki T, Lu S et al. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 2009; 31: 787-798.