High efficacy of tumor-targeting Salmonella typhimurium A1-R on a doxorubicin- and dactolisib-resistant follicular dendritic-cell sarcoma in a patient-derived orthotopic xenograft PDOX nude mouse model

Oncotarget

Volumn 7, Issue 22, 2016, Pages 33046-33054

  Kiyuna, Tasuku ^a,b,c   Murakami, Takashi ^a,b   Tome, Yasunori ^c   Kawaguchi, Kei ^a,b   Igarashi, Kentaro ^a,b   Zhang, Yong ^a   Zhao, Ming ^a   Li, Yunfeng ^d   Bouvet, Michael ^b   Kanaya, Fuminori ^c   Singh, Arun ^d   Dry, Sarah ^d   Eilber, Fritz C ^d   Hoffman, Robert M ^a,b,e  

^a ANTICANCER INC   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF THE RYUKYUS   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e PDOX LLC   (United States)

Author keywords

Doxorubicin; GFP; Nude mice; PDOX; Salmonella typhimurium A1 R; Sarcoma; Soft tissue; Tumor targeting

Indexed keywords

A1 R; ANTINEOPLASTIC AGENT; DACTOLISIB; DOXORUBICIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; IMIDAZOLE DERIVATIVE; QUINOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; DRUG TARGETING; FEMALE; FOLLICULAR DENDRITIC CELL SARCOMA; HUMAN; HUMAN TISSUE; MOUSE; NONHUMAN; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TREATMENT RESPONSE; TUMOR VOLUME; ANIMAL; DRUG RESISTANCE; DRUG SCREENING; MICROBIOLOGY; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; SALMONELLOSIS; TUMOR CELL LINE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CELL LINE, TUMOR; DENDRITIC CELL SARCOMA, FOLLICULAR; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; IMIDAZOLES; MICE; MICE, NUDE; QUINOLINES; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84973560540     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8848     Document Type: Article

References (40)

1. Conry RM. Response of follicular dendritic cell sarcoma to gemcitabine and docetaxel: report of two cases and literature review. Clin Sarcoma Res 2014;4:6.
2. Khalid T, Folman R: Symptoms in cancer patients and an unusual tumor: Case 3. Follicular dendritic cell sarcoma. J Clin Oncol 2005;23:9425-9426.
3. Choi BS, Baek JH, Shin YM, Kim JH, Kim HW, Lee SJ, Cha HJ. Follicular dendritic cell sarcoma: a case report and review of the literature. Cancer Res Treat 2010;42:121-124.
4. Zhang Y, Zhang N, Zhao M, Hoffman RM. Comparison of the selective targeting efficacy of Salmonella typhimurium A1-R and VNP20009 on the Lewis lung carcinoma in nude mice. Oncotarget 2015;6:14625-14631. doi: 10.18632/ oncotarget.3342.
5. Hoffman, R.M., editor. Bacterial Therapy of Cancer: Methods and Protocols. Methods in Molecular Biology 1409. Walker, John M., series ed. Humana Press (Springer Science+Business Media New York), 2016.
6. Zhao M, Yang M, 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;102:755-760.
7. 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;104:10170-10174.
8. 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;66:7647-7652.
9. Zhang Y, Tome Y, Suetsugu A, Zhang L, Zhang N, Hoffman RM, Zhao M. Determination of the optimal route of administration of Salmonella typhimurium A1-R to target breast cancer in nude mice. Anticancer Res 2012;32:2501-2508.
10. Zhang Y, Miwa S, Zhang N, Hoffman RM, Zhao M. Tumor-targeting Salmonella typhimurium A1-R arrests growth of breast-cancer brain metastasis. Oncotarget 2015;6:2615-2622. doi: 10.18632/oncotarget.2811.
11. 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;32:4331-4339.
12. 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;9:4518-4524.
13. Nagakura C, Hayashi K, Zhao M, Yamauchi K, Yamamoto N, Tsuchiya H, Tomita K , Bouvet M, Hoffman RM. Efficacy of a genetically-modified Salmonella typhimurium in an orthotopic human pancreatic cancer in nude mice. Anticancer Res 2009;29:1873-1878.
14. Yam C, Zhao M, Hayashi K, Ma H, Kishimoto H, McElroy M, Bouvet M, Hoffman RM. Monotherapy with a tumortargeting mutant of S. typhimurium inhibits liver metastasis in a mouse model of pancreatic cancer. J Surg Res 2010;164:248-255.
15. 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;12:2774-2780.
16. 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;115:1254-1261.
17. Hiroshima Y, Zhang Y, Murakami T, Maawy AA, Miwa S, Yamamoto M, Yano S, Sato S, Momiyama M, Mori R, Matsuyama R, Chishima T, Tanaka K, et al. Efficacy of tumor-targeting Salmonella typhimurium A1-R in combination with anti-angiogenesis therapy on a pancreatic cancer patient-derived orthotopic xenograph (PDOX) and cell line mouse models. Oncotarget 2014;5:12346-12357. doi: 10.18632/oncotarget.2641.
18. 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.
19. Matsumoto Y, Miwa S, Zhang Y, Zhao M, Yano S, Uehara F, Yamamoto M, Hiroshima Y, Toneri M, Bouvet M, Matsubara H, Tsuchiya H, Hoffman RM. Intraperitoneal administration of tumor-targeting Salmonella typhimurium A1-R inhibits disseminated human ovarian cancer and extends survival in nude mice. Oncotarget 2015;6:11369-11377. doi: 10.18632/oncotarget.3607.
20. Yano S, Zhang Y, Zhao M, Hiroshima Y, Miwa S, Uehara F, Kishimoto H, Tazawa H, Bouvet M, Fujiwara T, and Hoffman RM. Tumor-targeting Salmonella typhimurium A1-R decoys quiescent cancer cells to cycle as visualized by FUCCI imaging and become sensitive to chemotherapy. Cell Cycle 2014;13:3958-3963.
21. Hiroshima Y, Zhang Y, Zhao M, Zhang N, Murakami T, Maawy A, Mii S, Uehara F, Yamamoto M, Miwa S, Yano S, Momiyama M, Mori R, Matsuyama R, Chishima T, Tanaka K, Ichikawa Y, Bouvet M, Endo I, Hoffman RM. Tumor-targeting Salmonella typhimurium A1-R in combination with Trastuzumab eradicates HER-2-positive cervical cancer cells in patient-derived mouse models. PLoS One 2015;10:e0120358.
22. Hayashi K, Zhao M, Yamauchi K, Yamamoto N, Tsuchiya H, Tomita K, Hoffman RM. Cancer metastasis directly eradicated by targeted therapy with a modified Salmonella typhimurium. J Cell Biochem 2009;106:992-998.
23. 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;8:870-875.
24. Miwa S, Zhang Y, Baek K-E, Uehara F, Yano S, Yamamoto M, Hiroshima Y, Matsumoto Y, Kimura H, Hayashi K, Yamamoto N, Bouvet M, Tsuchiya H, Hoffman RM, Zhao M. Inhibition of spontaneous and experimental lung metastasis of soft-tissue sarcoma by tumor-targeting Salmonella typhimurium A1-R. Oncotarget 2014;5:12849-12861. doi: 10.18632/oncotarget.2561.
25. Murakami T, DeLong J, Eilber FC, Zhao M, Zhang Y, Zhang N, Singh A, Russell T, Deng S, Reynoso J, Quan C, Hiroshima Y, Matsuyama R, Chishima T, Tanaka K, Bouvet M, Chawla S, Endo I, Hoffman RM. Tumortargeting Salmonella typhimurium A1-R in combination with doxorubicin eradicate soft tissue sarcoma in a patientderived orthotopic xenograft PDOX model. Oncotarget, Epub ahead of print. DOI: 10.18632/oncotarget.7226.
26. Hoffman, R.M., editor. Bacterial Therapy of Cancer: Methods and Protocols. Methods in Molecular Biology 1409. Walker, John M., series ed. Humana Press (Springer Science+Business Media New York), 2016.
27. Momiyama M, Zhao M, Kimura H, Tran B, Chishima T, Bouvet M, Endo I, Hoffman RM. Inhibition and eradication of human glioma with tumor-targeting Salmonella typhimurium in an orthotopic nude-mouse model. Cell Cycle 2012;11:628-632.
28. Hiroshima Y, Zhao M, Zhang Y, Zhang N, Maawy A, Murakami T, Mii S, Uehara F, Yamamoto M, Miwa S, Yano S, Momiyama M, Mori R,Matsuyama R, Chishima T, Tanaka K, Ichikawa Y, Bouvet M, Endo I, Hoffman RM. Tumor-targeting Salmonella typhimurium A1-R arrests a chemo-resistant patient soft-tissue sarcoma in nude mice. PLoS One 2015;10: e0134324.
29. Manara MC, Nicoletti G, Zambelli D, Ventura S, Guerzoni C, Landuzzi L, Lollini PL, Maira SM, García-Echeverría C, Mercuri M, Picci P, Scotlandi K. NVP-BEZ235 as a new therapeutic option for sarcomas. Clin Cancer Res 2010;16:530-540.
30. Mita MM, Poplin E, Britten CD, Tap WD, Rubin EH, Scott BB, Berk L, Rivera VM, Loewy JW, Dodion P, Haluska F, Sarantopoulos J, Mita A, Tolcher A. Phase I/IIa trial of the mammalian target of rapamycin inhibitor ridaforolimus (AP23573; MK-8669) administered orally in patients with refractory or advanced malignancies and sarcoma. Ann Oncol 2013;24:1104-1111.
31. 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, RoyChowdhuri 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.
32. 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.
33. Blagosklonny MV. Matching targets for selective cancer therapy. Drug Discov Today 2003;8:1104-7.
34. Blagosklonny MV. Teratogens as anti-cancer drugs. Cell Cycle 2005;4:1518-21.
35. 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.
36. Blagosklonny MV. Target for cancer therapy: proliferating cells or stem cells. Leukemia 2006;20:385-91.
37. Apontes P, Leontieva OV, Demidenko ZN, Li F, Blagosklonny MV. Exploring long-term protection of normal human fibroblasts and epithelial cells from chemotherapy in cell culture. Oncotarget 2011;2:222-33. doi: 10.18632/oncotarget.248.
38. Blagosklonny MV. Tissue-selective therapy of cancer. Br J Cancer 2003;89:1147-51.
39. Uchugonova A, Duong J, Zhang N, König K, Hoffman RM. The bulge area is the origin of nestin-expressing pluripotent stem cells of the hair follicle. J Cell Biochem 2011;112:2046-2050.
40. 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;66:4208-4214.