The systemic delivery of an oncolytic adenovirus expressing decorin inhibits bone metastasis in a mouse model of human prostate cancer

Gene Therapy

Volumn 22, Issue 3, 2015, Pages 247-256

  Xu, W ^a   Neill, T ^b   Yang, Y ^a   Hu, Z ^c   Cleveland, E ^d   Wu, Y ^e   Hutten, R ^e   Xiao, X ^f   Stock, S R ^g   Shevrin, D ^d   Kaul, K ^d   Brendler, C ^h   Iozzo, R V ^b   Seth, P ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c NATIONAL INSTITUTES FOR FOOD AND DRUG CONTROL   (China)

^d NorthShore University Research Institute   (United States)

^e EVANSTON NORTHWESTERN HEALTHCARE   (United States)

^f ARGONNE NATIONAL LABORATORY   (United States)

^g NORTHWESTERN UNIVERSITY   (United States)

^h NORTHSHORE UNIVERSITY HEALTHSYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; BETA CATENIN; DECORIN; MITOCHONDRIAL DNA; ONCOLYTIC ADENOVIRUS; OSTEOCALCIN; VASCULOTROPIN A; ONCOLYTIC VIRUS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BONE METASTASIS; CACHEXIA; CANCER GENE THERAPY; CANCER INHIBITION; CELL MIGRATION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME BLOOD LEVEL; GENE EXPRESSION; HEART LEFT VENTRICLE; HUMAN; HUMAN CELL; HYPERCALCEMIA; MALE; MICRO-COMPUTED TOMOGRAPHY; MIGRATION; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; TUMOR CELL; TUMOR VOLUME; VIRAL GENE DELIVERY SYSTEM; VIRUS REPLICATION; X RAY; ANIMAL; BONE NEOPLASMS; CELL MOTION; DISEASE MODEL; DRUG EFFECTS; GENE TRANSFER; GENETICS; METABOLISM; NUDE MOUSE; PROSTATIC NEOPLASMS; SECONDARY; TUMOR CELL LINE;

ADENOVIRIDAE; ANIMALIA; MUS; MUS MUSCULUS;

ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; DECORIN; DISEASE MODELS, ANIMAL; GENE TRANSFER TECHNIQUES; HUMANS; MALE; MICE, NUDE; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PROSTATIC NEOPLASMS;

EID: 84924628052     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2014.110     Document Type: Article

References (50)

1. Cancer Facts and Figures 2013. http://www.cancer.org/Research/cancer-facts-figures-2013.
2. Coleman RE. Metastatic bone disease: clinical features, pathophysiology and treatment strategies. Cancer Treat Rev 2001; 27: 165-176.
3. Sturge J, Caley MP, Waxman J. Bone metastasis in prostate cancer: emerging therapeutic strategies. Nat Rev Clin Oncol 2011; 8: 357-368.
4. Gartrell BA, Saad F. Managing bone metastases and reducing skeletal related events in prostate cancer. Nat Rev Clin Oncol 2014; 11: 335-345.
5. Deng X, He G, Liu J, Luo F, Peng X, Tang S et al. Recent advances in bone-targeted therapies of metastatic prostate cancer. Cancer Treat Rev 2014; 40: 730-738.
6. Camacho DF, Pienta KJ. A multi-targeted approach to treating bone metastases. Cancer Metastasis Rev 2014; 33: 545-553.
7. Suzman DL, Boikos SA, Carducci MA. Bone-targeting agents in prostate cancer. Cancer Metastasis Rev 2014; 33: 610-628.
8. Lee RJ, Smith MR. Targeting MET and vascular endothelial growth factor receptor signaling in castration-resistant prostate cancer. Cancer J 2013; 19: 90-98.
9. Lipton A, Balakumaran A. Denosumab for the treatment of cancer therapy-induced bone loss and prevention of skeletal-related events in patients with solid tumors. Expert Rev Clin Pharmacol 2012; 5: 359-371.
10. Fizazi K, Carducci M, Smith M, Damiao R, Brown J, Karsh L et al. Denosumab versus zoledronic acid for treatment of bone metastases in men with castration-resistant prostate cancer: a randomised, double-blind study. Lancet 2011; 377: 813-822.
11. Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M et al. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996; 274: 373-376.
12. Seth P (ed) Adenoviruses: Basic Biology to Gene Therapy . R G Landes Company: Austin, TX, USA, 1999.
13. Yamamoto M, Curiel DT. Current issues and future directions of oncolytic adenoviruses. Mol Ther 2010; 18: 243-250.
14. Choi IK, Yun CO. Recent developments in oncolytic adenovirus-based immunotherapeutic agents for use against metastatic cancers. Cancer Gene Ther 2013; 20: 70-76.
15. Schenk E, Essand M, Bangma CH, Barber C, Behr JP, Briggs S et al. Clinical adenoviral gene therapy for prostate cancer. Hum Gene Ther 2010; 21: 807-813.
16. Hu Z, Gupta J, Zhang Z, Gerseny H, Berg A, Chen YJ et al. Systemic delivery of oncolytic adenoviruses targeting transforming growth factor-beta inhibits established bone metastasis in a prostate cancer mouse model. Hum Gene Ther 2012; 23: 871-882.
17. Xu W, Zhang Z, Yang Y, Hu Z, Wang CH, Morgan M et al. Ad5/48 hexon oncolytic virus expressing sTGFbetaRIIFc produces reduced hepatic and systemic toxicities and inhibits prostate cancer bone metastases. Mol Ther 2014; 22: 1504-1517.
18. Edwards IJ. Proteoglycans in prostate cancer. Nat Rev Urol 2012; 9: 196-206.
19. Henke A, Grace OC, Ashley GR, Stewart GD, Riddick AC, Yeun H et al. Stromal expression of decorin, Semaphorin6D, SPARC, Sprouty1 and Tsukushi in developing prostate and decreased levels of decorin in prostate cancer. PLoS One 2012; 7: e42516.
20. Neill T, Schaefer L, Iozzo RV. Decorin: a guardian from the matrix. Am J Pathol 2012; 181: 380-387.
21. Sofeu Feugaing DD, Gotte M, Viola M. More than matrix: the multifaceted role of decorin in cancer. Eur J Cell Biol 2013; 92: 1-11.
22. Neill T, Painter H, Buraschi S, Owens RT, Lisanti MP, Schaefer L et al. Decorin antagonizes the angiogenic network: concurrent inhibition of Met, hypoxia inducible factor 1alpha, vascular endothelial growth factor A, and induction of thrombospondin-1 and TIMP3. J Biol Chem 2012; 287 : 5492-5506.
23. Buraschi S, Pal N, Tyler-Rubinstein N, Owens RT, Neill T, Iozzo RV. Decorin antagonizes Met receptor activity and down-regulates {beta}-catenin and Myc levels. J Biol Chem 2010; 285: 42075-42085.
24. Kypta RM, Waxman J. Wnt/beta-catenin signalling in prostate cancer. Nat Rev Urol 2012; 9: 418-428.
25. Cook LM, Shay G, Aruajo A, Lynch CC. Integrating new discoveries into the "vicious cycle" paradigm of prostate to bone metastases. Cancer Metastasis Rev 2014; 33: 511-525.
26. Varkaris A, Corn PG, Gaur S, Dayyani F, Logothetis CJ, Gallick GE. The role of HGF/c-Met signaling in prostate cancer progression and c-Met inhibitors in clinical trials. Expert Opin Investig Drugs 2011; 20: 1677-1684.
27. Zeng Y, Opeskin K, Goad J, Williams ED. Tumor-induced activation of lymphatic endothelial cells via vascular endothelial growth factor receptor-2 is critical for prostate cancer lymphatic metastasis. Cancer Res 2006; 66: 9566-9575.
28. Li X, Ling W, Khan S, Yaccoby S. Therapeutic effects of intrabone and systemic mesenchymal stem cell cytotherapy on myeloma bone disease and tumor growth. J Bone Miner Res 2012; 27: 1635-1648.
29. Li X, Pennisi A, Yaccoby S. Role of decorin in the antimyeloma effects of osteoblasts. Blood 2008; 112 : 159-168.
30. Reed CC, Gauldie J, Iozzo RV. Suppression of tumorigenicity by adenovirusmediated gene transfer of decorin. Oncogene 2002; 21: 3688-3695.
31. Goldoni S, Seidler DG, Heath J, Fassan M, Baffa R, Thakur ML et al. An antimetastatic role for decorin in breast cancer. Am J Pathol 2008; 173: 844-855.
32. Choi IK, Lee YS, Yoo JY, Yoon AR, Kim H, Kim DS et al. Effect of decorin on overcoming the extracellular matrix barrier for oncolytic virotherapy. Gene Ther 2010; 17 : 190-201.
33. Zhang Z, Krimmel J, Hu Z, Seth P. Systemic delivery of a novel liver-detargeted oncolytic adenovirus causes reduced liver toxicity but maintains the antitumor response in a breast cancer bone metastasis model. Hum Gene Ther 2011; 22: 1137-1142.
34. Aftab DT, McDonald DM. MET and VEGF: synergistic targets in castration-resistant prostate cancer. Clin Transl Oncol 2011; 13: 703-709.
35. Guise T. Examining the metastatic niche: targeting the microenvironment. Semin Oncol 2010; 37: S2-14.
36. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011; 331: 1559-1564.
37. Munesue S, Yoshitomi Y, Kusano Y, Koyama Y, Nishiyama A, Nakanishi H et al. A novel function of syndecan-2, suppression of matrix metalloproteinase-2 activation, which causes suppression of metastasis. J Biol Chem 2007; 282: 28164-28174.
38. Dagda RK, Cherra SJ 3rd, Kulich SM, Tandon A, Park D, Chu CT. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 2009; 284: 13843-13855.
39. Neill T, Torres A, Buraschi S, Owens RT, Hoek JB, Baffa R et al. Decorin induces mitophagy in breast carcinoma cells via peroxisome proliferator-activated receptor gamma coactivator-1alpha (PGC-1alpha) and mitostatin. J Biol Chem 2014; 289: 4952-4968.
40. Ma Y, Galluzzi L, Zitvogel L, Kroemer G. Autophagy and cellular immune responses. Immunity 2013; 39: 211-227.
41. Seth P, Wang ZG, Pister A, Zafar MB, Kim S, Guise T et al. Development of oncolytic adenovirus armed with a fusion of soluble transforming growth factorbeta receptor II and human immunoglobulin Fc for breast cancer therapy. Hum Gene Ther 2006; 17: 1152-1160.
42. Hu Z, Robbins JS, Pister A, Zafar MB, Zhang ZW, Gupta J et al. A modified hTERT promoter-directed oncolytic adenovirus replication with concurrent inhibition of TGFbeta signaling for breast cancer therapy. Cancer Gene Ther 2010; 17: 235-243.
43. Katayose D, Gudas J, Nguyen H, Srivastava S, Cowan KH, Seth P. Cytotoxic effects of adenovirus-mediated wild-type p53 protein expression in normal and tumor mammary epithelial cells. Clin Cancer Res 1995; 1: 889-897.
44. Hu Z, Zhang Z, Guise T, Seth P. Systemic delivery of an oncolytic adenovirus expressing soluble transforming growth factor-beta receptor II-Fc fusion protein can inhibit breast cancer bone metastasis in a mouse model. Hum Gene Ther 2010; 21: 1623-1629.
45. Zhang Z, Hu Z, Gupta J, Krimmel JD, Gerseny HM, Berg AF et al. Intravenous administration of adenoviruses targeting transforming growth factor beta signaling inhibits established bone metastases in 4T1 mouse mammary tumor model in an immunocompetent syngeneic host. Cancer Gene Ther 2012; 19: 630-636.
46. Goldoni S, Humphries A, Nystrom A, Sattar S, Owens RT, McQuillan DJ et al. Decorin is a novel antagonistic ligand of the Met receptor. J Cell Biol 2009; 185: 743-754.
47. Cory G. Scratch-wound assay. Methods Mol Biol 2011; 769: 25-30.
48. Hu Z, Gerseny H, Zhang Z, Chen YJ, Berg A, Stock S et al. Oncolytic adenovirus expressing soluble TGFbeta receptor II-Fc-mediated inhibition of established bone metastases: a safe and effective systemic therapeutic approach for breast cancer. Mol Ther 2011; 9: 1609-1618.
49. Wang YX, Carlo FD, Mancini DC, McNulty I, Tieman B, Bresnahan J et al. A high-throughput X-ray microtomography system at the Advanced Photon Source. Rev Sci Instrum 2001; 72: 2062-2068.
50. Schneider A, Kalikin LM, Mattos AC, Keller ET, Allen MJ, Pienta KJ et al. Bone turnover mediates preferential localization of prostate cancer in the skeleton. Endocrinology 2005; 146: 1727-1736.