Reciprocal cellular cross-talk within the tumor microenvironment promotes oncolytic virus activity

Nature Medicine

Volumn 21, Issue 5, 2015, Pages 530-536

  Ilkow, Carolina S ^a,b   Marguerie, Monique ^a,b   Batenchuk, Cory ^a,b   Mayer, Justin ^a   Ben Neriah, Daniela ^a   Cousineau, Sophie ^a   Falls, Theresa ^a   Jennings, Victoria A ^a   Boileau, Meaghan ^a   Bellamy, David ^a   Bastin, Donald ^a   De Souza, Christiano Tanese ^a   Alkayyal, Almohanad ^a,c   Zhang, Jiqing ^a,d   Le Boeuf, Fabrice ^a,b   Arulanandam, Rozanne ^a,b   Stubbert, Lawton ^a,b   Sampath, Padma ^e,f,g   Thorne, Steve H ^e,f,g   Paramanthan, Piriya ^h   Chatterjee, Avijit ^h   Strieter, Robert M ⁱ   Burdick, Marie ^j   Addison, Christina L ^a,b   Stojdl, David F ^b,k   Atkins, Harold L ^a   Auer, Rebecca C ^a   Diallo, Jean Simon ^a   Lichty, Brian D ^l   Bell, John C ^a,b   more..

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF TABUK   (Saudi Arabia)

^d THE SECOND HOSPITAL OF SHANDONG UNIVERSITY   (China)

^e UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^f UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^g UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF OTTAWA   (Canada)

ⁱ NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^j UNIVERSITY OF VIRGINIA   (United States)

^k CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

^l MCMASTER UNIVERSITY   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEIN; ONCOLYTIC VIRUS; TRANSFORMING GROWTH FACTOR BETA;

AGED; ANIMAL; CANCER TRANSPLANTATION; CHEMISTRY; CHLOROCEBUS AETHIOPS; COCULTURE; FEMALE; FIBROBLAST; FLUORESCENCE MICROSCOPY; HUMAN; LUNG TUMOR; MALE; METABOLISM; MIDDLE AGED; MOUSE; ONCOLYTIC VIROTHERAPY; OVARY TUMOR; PROCEDURES; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; VERO CELL LINE;

AGED; ANIMALS; ANTIVIRAL AGENTS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COCULTURE TECHNIQUES; FEMALE; FIBROBLAST GROWTH FACTOR 2; FIBROBLASTS; GREEN FLUORESCENT PROTEINS; HUMANS; LUNG NEOPLASMS; MALE; MICE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; NEOPLASM TRANSPLANTATION; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; OVARIAN NEOPLASMS; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA; TUMOR MICROENVIRONMENT; VERO CELLS;

EID: 84929146994     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3848     Document Type: Article

References (46)

1. Hanahan, D. & Coussens, L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21, 309-322 (2012).
2. Chung, A.S. et al. An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy. Nat. Med. 19, 1114-1123 (2013).
3. Hwang, R.F. et al. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 68, 918-926 (2008).
4. Lisanti, M.P., Martinez-Outschoorn, U.E. & Sotgia, F. Oncogenes induce the cancer-associated fibroblast phenotype: Metabolic symbiosis and "fibroblast addiction" are new therapeutic targets for drug discovery. Cell Cycle 12, 2723-2732 (2013).
5. Nakasone, E.S. et al. Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 21, 488-503 (2012).
6. Straussman, R. et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504 (2012).
7. Sun, Y. et al. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat. Med. 18, 1359-1368 (2012).
8. Wilson, T.R. et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 487, 505-509 (2012).
9. Breitbach, C.J. et al. Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans. Nature 477, 99-102 (2011).
10. Heo, J. et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat. Med. 19, 329-336 (2013).
11. Kalluri, R. & Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401 (2006).
12. Löhr, M. et al. Transforming growth factor-β1 induces desmoplasia in an experimental model of human pancreatic carcinoma. Cancer Res. 61, 550-555 (2001).
13. Rønnov-Jessen, L. & Petersen, O.W. Induction of αα-smooth muscle actin by transforming growth factor-β1 in quiescent human breast gland fibroblasts. Implications for myofibroblast generation in breast neoplasia. Lab. Invest. 68, 696-707 (1993).
14. Sobol, P.T. et al. Adaptive antiviral immunity is a determinant of the therapeutic success of oncolytic virotherapy. Mol. Ther. 19, 335-344 (2011).
15. Stojdl, D.F. et al. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4, 263-275 (2003).
16. Brun, J. et al. Identification of genetically modified Maraba virus as an oncolytic rhabdovirus. Mol. Ther. 18, 1440-1449 (2010).
17. Azzarone, B. et al. Abnormal properties of skin fibroblasts from patients with breast cancer. Int. J. Cancer. 33, 759-764 (1984).
18. Brouty-Boyé, D. et al. Fetal myofibroblast-like cells isolated from post-radiation fibrosis in human breast cancer. Int. J. Cancer. 47, 697-702 (1991).
19. Schor, S.L., Schor, A.M. & Rushton, G. Fibroblasts from cancer patients display a mixture of both foetal and adult-like phenotypic characteristics. J. Cell Sci. 90, 401-407 (1988).
20. Cirri, P. & Chiarugi, P. Cancer associated fibroblasts: the dark side of the coin. Am. J. Cancer Res. 1, 482-497 (2011).
21. Erez, N., Truitt, M., Olson, P., Arron, S.T. & Hanahan, D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-κB-dependent manner. Cancer Cell 17, 135-147 (2010).
22. Franco, O.E., Shaw, A.K., Strand, D.W. & Hayward, S.W. Cancer associated fibroblasts in cancer pathogenesis. Semin. Cell Dev. Biol. 21, 33-39 (2010).
23. Orimo, A. et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121, 335-348 (2005).
24. Räsänen, K. & Vaheri, A. Activation of fibroblasts in cancer stroma. Exp. Cell Res. 316, 2713-2722 (2010).
25. Spaeth, E.L. et al. Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PLoS ONE 4, e4992 (2009).
26. Ablasser, A. et al. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III - transcribed RNA intermediate. Nat. Immunol. 10, 1065-1072 (2009).
27. Chiu, Y.H., Macmillan, J.B. & Chen, Z.J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138, 576-591 (2009).
28. Yoneyama, M. et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5, 730-737 (2004).
29. Altomonte, J. & Ebert, O. Sorting out Pandora's box: discerning the dynamic roles of liver microenvironment in oncolytic virus therapy for hepatocellular carcinoma. Front. Oncol. 4, 85 (2014).
30. Kurozumi, K. et al. Effect of tumor microenvironment modulation on the efficacy of oncolytic virus therapy. J. Natl. Cancer Inst. 99, 1768-1781 (2007).
31. Stanford, M.M., Breitbach, C.J., Bell, J.C. & McFadden, G. Innate immunity, tumor microenvironment and oncolytic virus therapy: friends or foes? Curr. Opin. Mol. Ther. 10, 32-37 (2008).
32. Kim, R., Emi, M. & Tanabe, K. Cancer immunoediting from immune surveillance to immune escape. Immunology 121, 1-14 (2007).
33. Lichty, B.D., Breitbach, C.J., Stojdl, D.F. & Bell, J.C. Going viral with cancer immunotherapy. Nat. Rev. Cancer 14, 559-567 (2014).
34. Erkan, M. et al. The role of stroma in pancreatic cancer: diagnostic and therapeutic implications. Nat Rev Gastroenterol. Hepatol. 9, 454-467 (2012).
35. Erkan, M. et al. The impact of the activated stroma on pancreatic ductal adenocarcinoma biology and therapy resistance. Curr. Mol. Med. 12, 288-303 (2012).
36. Sanfilippo, C.M. & Blaho, J.A. ICP0 gene expression is a herpes simplex virus type 1 apoptotic trigger. J. Virol. 80, 6810-6821 (2006).
37. Dayer, A.G. et al. Expression of FGF-2 in neural progenitor cells enhances their potential for cellular brain repair in the rodent cortex. Brain 130, 2962-2976 (2007).
38. Kim, J.H. et al. Systemic armed oncolytic and immunologic therapy for cancer with JX-594, a targeted poxvirus expressing GM-CSF. Mol. Ther. 14, 361-370 (2006).
39. Breitbach, C.J. et al. Targeting tumor vasculature with an oncolytic virus. Mol. Ther. 19, 886-894 (2011).
40. Emig, D. et al. AltAnalyze and DomainGraph: analyzing and visualizing exon expression data. Nucleic Acids Res. 38, W755-W762 (2010).
41. Eden, E., Navon, R., Steinfeld, I., Lipson, D. & Yakhini, Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10, 48 (2009).
42. Samarajiwa, S.A., Forster, S., Auchettl, K. & Hertzog, P.J. INTERFEROME: the database of interferon regulated genes. Nucleic Acids Res. 37, D852-D857 (2009).
43. Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001).
44. Östman, A. & Augsten, M. Cancer-associated fibroblasts and tumor growth-bystanders turning into key players. Curr. Opin. Genet. Dev. 19, 67-73 (2009).
45. Tomayko, M.M. & Reynolds, C.P. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother. Pharmacol. 24, 148-154 (1989).
46. Dell, R.B., Holleran, S. & Ramakrishnan, R. Sample size determination. ILAR J 43, 207-213 (2002).