Intraperitoneal administration of tumor-targeting Salmonella typhimurium A1-R inhibits disseminated human ovarian cancer and extends survival in nude mice

Oncotarget

Volumn 6, Issue 13, 2015, Pages 11369-11377

  Matsumoto, Yasunori ^a,b,c   Miwa, Shinji ^a,b,d   Zhang, Yong ^a   Zhao, Ming ^a   Yano, Shuya ^a,b   Uehara, Fuminari ^a,b   Yamamoto, Mako ^a,b   Hiroshima, Yukihiko ^a,b   Toneri, Makoto ^a,b   Bouvet, Michael ^b   Matsubara, Hisahiro ^c   Tsuchiya, Hiroyuki ^d   Hoffman, Robert M ^a,b  

^a ANTICANCER INC   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c CHIBA UNIVERSITY   (Japan)

^d KANAZAWA UNIVERSITY   (Japan)

Author keywords

Bacterial therapy; Mouse model; Orthotopic; Ovarian cancer; Salmonella typhimurium A1 R

Indexed keywords

ANTINEOPLASTIC AGENT; SALMONELLA TYPHIMURIUM A1 R; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER SURVIVAL; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; OVARY CANCER; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SURVIVAL RATE; ANIMAL; BACTERIAL LOAD; BIOLOGICAL THERAPY; COMPARATIVE STUDY; DRUG SCREENING; GROWTH, DEVELOPMENT AND AGING; INTRAPERITONEAL DRUG ADMINISTRATION; INTRAVENOUS DRUG ADMINISTRATION; MICROBIOLOGY; NUDE MOUSE; OVARIAN NEOPLASMS; PATHOGENICITY; PATHOLOGY; PERITONEAL NEOPLASMS; PROCEDURES; TIME FACTOR; TUMOR CELL LINE; VIRULENCE;

ANIMALS; BACTERIAL LOAD; BIOLOGICAL THERAPY; CELL LINE, TUMOR; FEMALE; HUMANS; INJECTIONS, INTRAPERITONEAL; INJECTIONS, INTRAVENOUS; MICE, NUDE; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; SALMONELLA TYPHIMURIUM; TIME FACTORS; VIRULENCE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84929649278     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3607     Document Type: Article

References (37)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics. 2013. CA Cancer J Clin 2013;63:11-30.
2. Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA, editors. SEER Cancer Statistics Review, 1975-2010, National Cancer Institute, Bethesda, MD, http://seer.cancer. gov/csr/1975_2010/, based on November 2012 SEER data submission, posted to the SEER web site, April 2013.
3. American Cancer Society. 2013. [http://www.cancer.org/].
4. Cannistra SA, Bast RC, Jr, Berek JS. Progress in the management of gynecologic cancer: Consensus summary statement. J Clin Oncol 2003;21:129s-32s.
5. William Coley. Available at: http://en.wikipedia.org/wiki/ William_Coley [last accessed 12 December 2013].
6. Hoffman RM. The preclinical discovery of bacterial therapy for the treatment of metastatic cancer with unique advantages. Expert Opin Drug Discov 2012;7:73-83.
7. Forbes NS. Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer 2010;10:785-94.
8. Yazawa K, Fujimori M, Nakamura T, Sasaki T, Amano J, Kano Y, Taniguchi S. Bifidobacterium longum as a delivery system for gene therapy of chemically induced rat mammary tumors. Breast Cancer Res Treat 2001;66:165-70.
9. Dang LH, Bettegowda C, Huso DL, Kinzler KW, Vogelstein B. Combination bacteriolytic therapy for the treatment of experimental tumors. Proc Natl Acad Sci USA 2001;98:15155-60.
10. Roberts NJ, Zhang L, Janku F, Collins A, Bai RY, Staedtke V, Rusk AW, Tung D, Miller M, Roix J, Khanna KV, Murthy R, Benjamin RS, Helgason T, Szvalb AD, Bird JE, Roy-Chowdhuri S, Zhang HH, Qiao Y, Karim B, McDaniel J, Elpiner A, Sahora A, Lachowicz J, Phillips B, Turner A, Klein MK, Post G, Diaz LA Jr, Riggins GJ, Papadopoulos N, Kinzler KW, Vogelstein B, Bettegowda C, Huso DL, Varterasian M, Saha S, Zhou S. Intratumoral injection of Clostridium novyi-NT spores induces antitumor responses. Sci Transl Med 2014;6:249ra111.
11. Pawelek JM, Low KB, Bermudes D. Bacteria as tumourtargeting vectors. Lancet Oncol 2003;4:548-56.
12. Toso JF, Gill VJ, Hwu P, Marincola FM, Restifo NP, Schwartzentruber DJ, Sherry RM, Topalian SL, Yang JC, Stock F, Freezer LJ, Morton KE, Seipp C, Haworth L, Mavroukakis S, White D, MacDonald S, Mao J, Sznol M, Rosenberg SA. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma. J Clin Oncol 2002;20:142-52.
13. Zhang Y, Zhang N, Hoffman RM, Zhao M. Comparision of the selective targeting efficacy of S. typhimurium A1-R and VNP20009 on the lewis lung carcinoma in nude mice. Oncotarget 2015:Epub ahead of print.
14. Zhao M, Yang Y, Li XM, Jiang P, Baranov E, Li S, Xu M, Penman S, Hoffman RM. Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proc Natl Acad Sci USA 2005;102:755-60.
15. Zhao M, Yang M, Ma H, Li X, Tan X, Li S, Yang Z, Hoffman RM. Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice. Cancer Res 2006;66:7647-52.
16. Zhao M, Geller J, Ma H, Yang M, Penman S, Hoffman RM. Monotherapy with a tumor-targeting mutant of Salmonella typhimurium cures orthotopic metastatic mouse models of human prostate cancer. Proc Natl Acad Sci USA 2007;104:10170-4.
17. Hayashi K, Zhao M, Yamauchi K, Yamamoto N, Tsuchiya H, Tomita K, Kishimoto H, Bouvet M, Hoffman RM . Systemic targeting of primary bone tumor and lung metastasis of high-grade osteosarcoma in nude mice with a tumor-selective strain of Salmonella typhimurium. Cell Cycle 2009;8:870-5.
18. Nagakura C, Hayashi K, Zhao M, Yamauchi K, Yamamoto N, Tsuchiya H, Tomita K, Bouvet M, Hoffman RM. Efficacy of a genetically-modified Salmonella typhimuriumin an orthotopic human pancreatic cancer in nude mice. Anticancer Res 2009;29:1873-8.
19. Kimura H, Zhang L, Zhao M, Hayashi K, Tsuchiya H, Tomita K, Bouvet M, Wessels J, Hoffman RM. Targeted therapy of spinal cord glioma with a genetically-modified Salmonella typhimurium. Cell Prolif 2010;43:41-8.
20. Yam C, Zhao M, Hayashi K, Ma H, Kishimoto H, McElroy M, Bouvet M, Hoffman RM . Monotherapy with a tumortargeting mutant of Salmonella typhimurium controls liver metastasis in a mouse model of pancreatic cancer. J Surg Res 2010;164:248-55.
21. Momiyama M, Zhao M, Kimura H, Tran B, Chishima T, Bouvet M, Endo I, Hoffman RM. 2012. Inhibition and eradication of human glioma with tumor targeting Salmonella typhimurium in an orthotopic nude-mouse model. Cell Cycle 2012;11:628-32.
22. Uchugonova A, Zhao M, Zhang Y, Weinigel M, König K, Hoffman RM. Cancer-cell killing by engineered Salmonella imaged by multiphoton tomography in live mice. Anticancer Res 2012;32:4331-38.
23. Leschner S, Westphal K, Dietrich N, Viegas N, Jablonska J, Lyszkiewicz M, Lienenklaus S, Falk W, Gekara N, Loessner H, Weiss S. Tumor invasion of Salmonella enterica serovar Typhimurium is accompanied by strong hemorrhage promoted by TNFa. PLoS ONE 2009;4:e6692.
24. Liu F, Zhang L, Hoffman RM, Zhao M. Vessel destruction by tumor targeting Salmonella typhimurium A1-R is enhanced by high tumor vascularity. Cell Cycle 2010;9:4518-24.
25. Hiroshima Y, Zhao M, Zhang Y, Maawy A, Hassanein MK, Uehara F, Miwa S, Yano S, Momiyama M, Suetsugu A, Chishima T, Tanaka K, Bouvet M, Endo I, Hoffman RM. Comparison of efficacy of Salmonella typhimurium A1-R and chemotherapy on stem-like and non-stem human pancreatic cancer cells. Cell Cycle 2013;12:2774-80.
26. Hiroshima Y, Zhao M, Maawy A, Zhang Y, Katz MH, Fleming JB, Uehara F, Miwa S, Yano S, Momiyama M, Suetsugu A, Chishima T, Tanaka K, Bouvet M, Endo I, Hoffman RM. Efficacy of Salmonella typhimurium A1-R versus chemotherapy on a pancreatic cancer patientderived orthotopic xenograft (PDOX). J Cell Biochem 2014;115:1254-61.
27. Matsumoto Y, Miwa S, Zhang Y, Hiroshima Y, Yano S, Uehara F, Yamamoto M, Toneri M, Bouvet M, Matsubara H, Hoffman RM, Zhao M. Efficacy of tumor-targeting Salmonella typhimurium A1-R on nude mouse models of metastatic and disseminated human ovarian Cancer, J. Cell. Biochem 2014;115:1996-2003.
28. Blagosklonny MV. How cancer could be cured by 2015. Cell Cycle 2005;4:269-78.
29. Blagosklonny MV. Tissue-selective therapy of cancer. Br J Cancer 2003;89:1147-51.
30. Blagosklonny MV. Matching targets for selective cancer therapy. Drug Discov Today 2003;8:1104-7.
31. Blagosklonny MV. "Targeting the absence" and therapeutic engineering for cancer therapy.Cell Cycle 2008;7:1307-12.
32. Blagosklonny MV. Teratogens as anti-cancer drugs. Cell Cycle 2005;4:1518-21.
33. Blagosklonny MV. Treatment with inhibitors of caspases, that are substrates of drug transporters, selectively permits chemotherapy-induced apoptosis in multidrug-resistant cells but protects normal cells. Leukemia 2001;15:936-41.
34. Blagosklonny MV. Target for cancer therapy: proliferating cells or stem cells. Leukemia 2006;20:385-91.
35. Blagosklonny MV. Cancer stem cell and cancer stemloids:from biology to therapy. Cancer Biol Ther 2007;6:1684-90.
36. Buick RN, Pullano R, Trent JM. Comparative properties of five human ovarian adenocarcinoma cell lines. Cancer Res 1985;45:3668-76.
37. Yamauchi K, Yang M, Jiang P, Xu M, Yamamoto N, Tsuchiya H, Tomita K, Moossa AR, Bouvet M, Hoffman RM. Development of real-time subcellular dynamic multicolor imaging of cancer-cell trafficking in live mice with a variable-magnification whole-mouse imaging system. Cancer Res 2006;66:4208-14.