Cancer-associated fibroblast-targeted strategy enhances antitumor immune responses in dendritic cell-based vaccine

Cancer Science

Volumn 106, Issue 2, 2015, Pages 134-142

  Ohshio, Yasuhiko ^a   Teramoto, Koji ^a   Hanaoka, Jun ^a   Tezuka, Noriaki ^a   Itoh, Yasushi ^a   Asai, Tohru ^a   Daigo, Yataro ^a   Ogasawara, Kazumasa ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Cancer associated fibroblasts; Dendritic cell based vaccine immunotherapy; Suppressor immune cells; Tranilast; Tumor microenvironment

Indexed keywords

DENDRITIC CELL VACCINE; PROSTAGLANDIN E2; STROMAL CELL DERIVED FACTOR 1; TRANILAST; TRANSFORMING GROWTH FACTOR BETA; ANTHRANILIC ACID DERIVATIVE; ANTINEOPLASTIC AGENT; CANCER VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; C57BL 6 MOUSE; CANCER ASSOCIATED FIBROBLAST; CANCER CELL; CANCER GROWTH; CANCER IMMUNIZATION; CANCER IMMUNOLOGY; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG INHIBITION; FEMALE; FIBROBLAST; HUMORAL IMMUNITY; IN VIVO STUDY; LYMPH NODE; LYMPHOCYTIC INFILTRATION; MOLECULARLY TARGETED THERAPY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SCID MOUSE; SUPPRESSOR CELL; T LYMPHOCYTE ACTIVATION; TUMOR DRAINING LYMPH NODE; TUMOR MICROENVIRONMENT; ANIMAL; C57BL MOUSE; DENDRITIC CELL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASMS; PROCEDURES; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DENDRITIC CELLS; FEMALE; FIBROBLASTS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNOTHERAPY; KILLER CELLS, NATURAL; LYMPH NODES; MICE; MICE, INBRED C57BL; MICE, SCID; NEOPLASMS; ORTHO-AMINOBENZOATES; T-LYMPHOCYTES, REGULATORY; TUMOR MICROENVIRONMENT;

EID: 84927685533     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12584     Document Type: Article

References (40)

1. Ding ZY, Zou XL, Wei YQ. Cancer microenvironment and cancer vaccine. Cancer Microenviron 2012; 5: 333-44.
2. Kobayashi N, Hiraoka N, Yamagami W et al. FOXP3+ regulatory T cells affect the development and progression of hepatocarcinogenesis. Clin Cancer Res 2007; 13: 902-11.
3. Karagöz B, Bilgi O, Gümüs M et al. CD8+CD28- cells and CD4+CD25+ regulatory T cells in the peripheral blood of advanced stage lung cancer patients. Med Oncol 2010; 27: 29-33.
4. Mandruzzato S, Solito S, Falisi E et al. IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J Immunol 2009; 182: 6562-8.
5. Curiel TJ, Coukos G, Zou L et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10: 942-9.
6. Hoechst B, Ormandy LA, Ballmaier M et al. A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology 2008; 135: 234-43.
7. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002; 196: 254-65.
8. Mueller MM, Fusenig NE. Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 2004; 4: 839-49.
9. Murata T, Mizushima H, Chinen I et al. HB-EGF and PDGF mediate reciprocal interactions of carcinoma cells with cancer-associated fibroblasts to support progression of uterine cervical cancers. Cancer Res 2011; 71: 6633-42.
10. Wu MH, Hong HC, Hong TM, Chiang WF, Jin YT, Chen YL. Targeting galectin-1 in carcinoma-associated fibroblasts inhibits oral squamous cell carcinoma metastasis by downregulating MCP-1/CCL2 expression. Clin Cancer Res 2011; 17: 1306-16.
11. Jedeszko C, Victor BC, Podgorski I, Sloane BF. Fibroblast hepatocyte growth factor promotes invasion of human mammary ductal carcinoma in situ. Cancer Res 2009; 69: 9148-55.
12. Orimo A, Gupta PB, Sgroi DC et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005; 121: 335-48.
13. Harper J, Sainson RC. Regulation of the anti-tumour immune response by cancer associated fibroblasts. Semin Cancer Biol 2014; 25: 69-77.
14. Hattori T, Wang PL. Inhibition by tranilast of nifedipine-induced proliferation of cultured human gingival fibroblasts. Eur J Pharmacol 2004; 498: 79-81.
15. Yasukawa T, Kimura H, Dong J et al. Effect of tranilast on proliferation, collagen gel contraction, and transforming growth factor beta secretion of retinal pigment epithelial cells and fibroblasts. Ophthalmic Res 2002; 34: 206-12.
16. Isaji M, Kikuchi S, Miyata H et al. Inhibitory effects of tranilast on the proliferation and functions of human pterygium-derived fibroblasts. Cornea 2000; 19: 364-8.
17. Oshima T, Kurosaka D, Kato K et al. Tranilast inhibits cell proliferation and collagen synthesis by rabbit corneal and Tenon's capsule fibroblasts. Curr Eye Res 2000; 20: 283-6.
18. Suzawa H, Kikuchi S, Arai N, Koda A. The mechanism involved in the inhibitory action of tranilast on collagen biosynthesis of keloid fibroblasts. Jpn J Pharmacol 1992; 60: 91-6.
19. Ohshio Y, Hanaoka J, Kontani K, Teramoto K. Tranilast inhibits the function of cancer-associated fibroblasts responsible for the induction of immune suppressor cell types. Scand J Immunol 2014; 80: 406-16.
20. Kontani K, Chano T, Ozaki Y et al. RB1CC1 suppresses cell cycle progression through RB1 expression in human neoplastic cells. Int J Mol Med 2003; 12: 767-9.
21. Teramoto K, Kontani K, Fujita T et al. Successful tumor eradication was achieved by collaboration of augmented cytotoxic activity and anti-angiogenic effects following therapeutic vaccines containing helper-activating analog-loaded dendritic cells and tumor antigen DNA. Cancer Immunol Immunother 2007; 56: 331-42.
22. Mandelboim O, Bar-Haim E, Vadai E, Fridkin M, Eisenbach L. Identification of shared tumor-associated antigen peptides between two spontaneous lung carcinomas. J Immunol 1997; 159: 6030-6.
23. Ito M, Minamiya Y, Kawai H et al. Tumor-derived TGFbeta-1 induces dendritic cell apoptosis in the sentinel lymph node. J Immunol 2006; 176: 5637-43.
24. Munn DH, Mellor AL. The tumor-draining lymph node as an immune-privileged site. Immunol Rev 2006; 213: 146-58.
25. Teramoto K, Kontani K, Ozaki Y et al. Deoxyribonucleic acid (DNA) encoding a pan-major histocompatibility complex class II peptide analogue augmented antigen-specific cellular immunity and suppressive effects on tumor growth elicited by DNA vaccine immunotherapy. Cancer Res 2003; 63: 7920-5.
26. Rogosnitzky M, Danks R, Kardash E. Therapeutic potential of tranilast, an anti-allergy drug, in proliferative disorders. Anticancer Res 2012; 32: 2471-8.
27. Tanaka K, Honda M, Kuramochi T, Morioka S. Prominent inhibitory effects of tranilast on migration and proliferation of and collagen synthesis by vascular smooth muscle cells. Atherosclerosis 1994; 107: 179-85.
28. Pan PY, Wang GX, Yin B et al. Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function. Blood 2008; 111: 219-28.
29. Yang L, Huang J, Ren X et al. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 2008; 13: 23-35.
30. Sinha P, Clements VK, Fulton AM, Ostrand-Rosenberg S. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 2007; 67: 4507-13.
31. Melani C, Sangaletti S, Barazzetta FM, Werb Z, Colombo MP. Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma. Cancer Res 2007; 67: 11438-46.
32. Kinoshita T, Ishii G, Hiraoka N et al. Forkhead box P3 regulatory T cells coexisting with cancer associated fibroblasts are correlated with a poor outcome in lung adenocarcinoma. Cancer Sci 2013; 104: 409-15.
33. Dürr C, Pfeifer D, Claus R et al. CXCL12 mediates immunosuppression in the lymphoma microenvironment after allogeneic transplantation of hematopoietic cells. Cancer Res 2010; 70: 10170-81.
34. Balsamo M, Scordamaglia F, Pietra G et al. Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity. Proc Natl Acad Sci USA 2009; 106: 20847-52.
35. Fujita T, Teramoto K, Ozaki Y et al. Inhibition of transforming growth factor-beta-mediated immunosuppression in tumor-draining lymph nodes augments antitumor responses by various immunologic cell types. Cancer Res 2009; 69: 5142-50.
36. Scanlan MJ, Raj BK, Calvo B et al. Molecular cloning of fibroblast activation protein alpha, a member of the serine protease family selectively expressed in stromal fibroblasts of epithelial cancers. Proc Natl Acad Sci USA 1994; 91: 5657-61.
37. Wen Y, Wang CT, Ma TT et al. Immunotherapy targeting fibroblast activation protein inhibits tumor growth and increases survival in a murine colon cancer model. Cancer Sci 2010; 101: 2325-32.
38. Loeffler M, Krüger JA, Niethammer AG, Reisfeld RA. Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest 2006; 116: 1955-62.
39. Liao D, Luo Y, Markowitz D, Xiang R, Reisfeld RA. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS One 2009; 4: e7965.
40. Lee J, Fassnacht M, Nair S, Boczkowski D, Gilboa E. Tumor immunotherapy targeting fibroblast activation protein, a product expressed in tumor-associated fibroblasts. Cancer Res 2005; 65: 11156-63.