Suppression of pancreatic ductal adenocarcinoma growth by intratumoral delivery of attenuated Salmonella typhimurium using a dual fluorescent live tracking system

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015; 65:5-29; PMID:25559415; http://dx.doi.org/10.3322/caac.21254
   PubMed Web of Science ®Google Scholar
• Feig C, Gopinathan A, Neesse A, Chan DS, Cook N, Tuveson DA. The pancreas cancer microenvironment. Clin Cancer Res 2012; 18:4266-76; PMID:22896693; http://dx.doi.org/10.1158/1078-0432.CCR-11-3114
   PubMed Web of Science ®Google Scholar
• Matsuo Y, Ding Q, Desaki R, Maemura K, Mataki Y, Shinchi H, Natsugoe S, Takao S. Hypoxia inducible factor-1 alpha plays a pivotal role in hepatic metastasis of pancreatic cancer: an immunohistochemical study. J Hepatobiliary Pancreat Sci 2014; 21:105-12; PMID:23798470; http://dx.doi.org/10.1002/jhbp.6
   PubMed Web of Science ®Google Scholar
• 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 U S A 2005; 102:755-60; PMID:15644448; http://dx.doi.org/10.1073/pnas.0408422102
   PubMed Web of Science ®Google Scholar
• Roberts NJ, Zhang L, Janku F, Collins A, Bai RY, Staedtke V, Rusk AW, Tung D, Miller M, Roix J, et al. Intratumoral injection of Clostridium novyi-NT spores induces antitumor responses. Sci Transl Med 2014; 6:249ra111; PMID:25122639; http://dx.doi.org/10.1126/scitranslmed.3008982
   PubMed Web of Science ®Google Scholar
• Maletzki C, Linnebacher M, Kreikemeyer B, Emmrich J. Pancreatic cancer regression by intratumoural injection of live Streptococcus pyogenes in a syngeneic mouse model. Gut 2008; 57:483-91; PMID:18025068; http://dx.doi.org/10.1136/gut.2007.125419
   PubMed Web of Science ®Google Scholar
• Forbes NS. Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer; 10:785-94; PMID:20944664; http://dx.doi.org/10.1038/nrc2934
   PubMed Web of Science ®Google Scholar
• Hiroshima Y, Zhang Y, Murakami T, Maawy A, Miwa S, Yamamoto M, Yano S, Sato S, Momiyama M, Mori R, et al. Efficacy of tumor-targeting Salmonella typhimurium A1-R in combination with anti-angiogenesis therapy on a pancreatic cancer patient-derived orthotopic xenograft (PDOX) and cell line mouse models. Oncotarget 2014; 5:12346-57; PMID:25402324; http://dx.doi.org/10.18632/oncotarget.2641
   PubMed Web of Science ®Google Scholar
• 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; 29:1873-8; PMID:19528442
   PubMed Web of Science ®Google Scholar
• Low KB, Ittensohn M, Luo X, Zheng LM, King I, Pawelek JM, Bermudes D. Construction of VNP20009: a novel, genetically stable antibiotic-sensitive strain of tumor-targeting Salmonella for parenteral administration in humans. Method Mol Med 2004; 90:47-60; PMID:14657558
   PubMedGoogle Scholar
• Thamm DH, Kurzman ID, King I, Li Z, Sznol M, Dubielzig RR, Vail DM, MacEwen EG. Systemic administration of an attenuated, tumor-targeting Salmonella typhimurium to dogs with spontaneous neoplasia: phase I evaluation. Clin Cancer Res 2005; 11:4827-34; PMID:16000580; http://dx.doi.org/10.1158/1078-0432.CCR-04-2510
   PubMed Web of Science ®Google Scholar
• Friedlos F, Lehouritis P, Ogilvie L, Hedley D, Davies L, Bermudes D, King I, Martin J, Marais R, Springer CJ. Attenuated Salmonella targets prodrug activating enzyme carboxypeptidase G2 to mouse melanoma and human breast and colon carcinomas for effective suicide gene therapy. Clin Cancer Res 2008; 14:4259-66; PMID:18594008; http://dx.doi.org/10.1158/1078-0432.CCR-07-4800
   PubMed Web of Science ®Google Scholar
• Luo X, Li Z, Lin S, Le T, Ittensohn M, Bermudes D, Runyab JD, Shen SY, Chen J, King IC, et al. Antitumor effect of VNP20009, an attenuated Salmonella, in murine tumor models. Oncol Res 2001; 12:501-8; PMID:11939414; http://dx.doi.org/10.3727/096504001108747512
   PubMed Web of Science ®Google Scholar
• Cheng X, Zhang X, Zhou Y, Zhang C, Hua ZC. A Salmonella Typhimurium mutant strain capable of RNAi delivery: higher tumor-targeting and lower toxicity. Cancer Biol Ther 2014; 15:1068-76; PMID:24842165; http://dx.doi.org/10.4161/cbt.29185
   PubMed Web of Science ®Google Scholar
• Toso JF, Gill VJ, Hwu P, Marincola FM, Restifo NP, Schwartzentruber DJ, Sherry RM, Topalian SL, Yang JC, Stock F, et al. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma. J Clin Oncol 2002; 20:142-52; PMID:11773163; http://dx.doi.org/10.1200/JCO.20.1.142
   PubMed Web of Science ®Google Scholar
• Heimann DM, Rosenberg SA. Continuous intravenous administration of live genetically modified salmonella typhimurium in patients with metastatic melanoma. J Immunother (Hagerstown, Md : 1997) 2003; 26:179-80; PMID:12616110; http://dx.doi.org/10.1097/00002371-200303000-00011
   PubMed Web of Science ®Google Scholar
• Piatkevich KD, Hulit J, Subach OM, Wu B, Abdulla A, Segall JE, Verkhusha VV. Monomeric red fluorescent proteins with a large Stokes shift. Proc Natl Acad Sci U S A 2009; 107:5369-74; PMID:20212155; http://dx.doi.org/10.1073/pnas.0914365107
   Web of Science ®Google Scholar
• Vuletic I, Liu J, Wu H, Ding Y, Lei Y, Li C, Zhu D, Ren Q, Sun H, Li J. Establishment of an mKate2-Expressing Cell Line for Non-Invasive Real-Time Breast Cancer In Vivo Imaging. Mol Imaging Biol 2015; 17:811-8; PMID:25902968; http://dx.doi.org/10.1007/s11307-015-0853-5
   PubMed Web of Science ®Google Scholar
• Yu YA, Shabahang S, Timiryasova TM, Zhang Q, Beltz R, Gentschev I, Goebel W, Szalay AA. Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat Biotechnol 2004; 22:313-20; PMID:14990953; http://dx.doi.org/10.1038/nbt937
   PubMed Web of Science ®Google Scholar
• Contag CH, Contag PR, Mullins JI, Spilman SD, Stevenson DK, Benaron DA. Photonic detection of bacterial pathogens in living hosts. Mol Microbiol 1995; 18:593-603; PMID:8817482; http://dx.doi.org/10.1111/j.1365-2958.1995.mmi_18040593.x
   PubMed Web of Science ®Google Scholar
• O'Neill K, Lyons SK, Gallagher WM, Curran KM, Byrne AT. Bioluminescent imaging: a critical tool in pre-clinical oncology research. J Pathol 2010; 220:317-27; PMID:19967724; http://dx.doi.org/10.1002/path.2656
   PubMed Web of Science ®Google Scholar
• Shcherbo D, Murphy CS, Ermakova GV, Solovieva EA, Chepurnykh TV, Shcheglov AS, Verkhusha VV, Pletnev VZ, Hazelwood KL, Roche PM, et al. Far-red fluorescent tags for protein imaging in living tissues. Biochem J 2009; 418:567-74; PMID:19143658; http://dx.doi.org/10.1042/BJ20081949
   PubMed Web of Science ®Google Scholar
• Jiang SN, Park SH, Lee HJ, Zheng JH, Kim HS, Bom HS, Hong Y, Szardenings M, Shin MG, Kim SC, et al. Engineering of bacteria for the visualization of targeted delivery of a cytolytic anticancer agent. Mol Therapy 2013; 21:1985-95; PMID:23922014; http://dx.doi.org/10.1038/mt.2013.183
   PubMed Web of Science ®Google Scholar
• Nemunaitis J, Cunningham C, Senzer N, Kuhn J, Cramm J, Litz C, Cavagnolo R, Cahill A, Clairmont C, Sznol M. Pilot trial of genetically modified, attenuated Salmonella expressing the E. coli cytosine deaminase gene in refractory cancer patients. Cancer Gene Ther 2003; 10:737-44; PMID:14502226; http://dx.doi.org/10.1038/sj.cgt.7700634
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang N, Hoffman RM, Zhao M. Comparison of the selective targeting efficacy of Salmonella typhimurium A1-R and VNP20009 on the lewis lung carcinoma in nude mice. Oncotarget 2015; 6:14625-31; PMID:25714030; http://dx.doi.org/10.18632/oncotarget.3342
   Web of Science ®Google Scholar
• Chen J, Wei D, Zhuang H, Qiao Y, Tang B, Zhang X, Wei J, Fang S, Chen G, Du P, et al. Proteomic screening of anaerobically regulated promoters from Salmonella and its antitumor applications. Mol Cell Proteomics 2011; 10:M111 009399; PMID:21474796; http://dx.doi.org/10.1074/mcp.M111.009399
   PubMed Web of Science ®Google Scholar
• 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 U S A 2007; 104:10170-4; PMID:17548809; http://dx.doi.org/10.1073/pnas.0703867104
   PubMed Web of Science ®Google Scholar
• 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; 6:2615-22; PMID:25575815; http://dx.doi.org/10.18632/oncotarget.2811
   PubMed Web of Science ®Google Scholar
• Hiroshima Y, Zhao M, Maawy A, Zhang Y, Katz MH, Fleming JB, Uehara F, Miwa S, Yano S, Momiyama M, et al. Efficacy of Salmonella typhimurium A1-R versus chemotherapy on a pancreatic cancer patient-derived orthotopic xenograft (PDOX). J Cell Biochem 2014; 115:1254-61; PMID:24435915; http://dx.doi.org/10.1002/jcb.24769
   PubMed Web of Science ®Google Scholar
• Kong B, Cheng T, Wu W, Regel I, Raulefs S, Friess H, Erkan M, Esposito I, Kleeff J, Michalski CW. Hypoxia-induced endoplasmic reticulum stress characterizes a necrotic phenotype of pancreatic cancer. Oncotarget 2015; 6:32154-60; PMID:26452217; http://dx.doi.org/10.18632/oncotarget.5168
   PubMed Web of Science ®Google Scholar
• Matsuoka H, Shibamoto Y, Kubota T, Tsujitani M, Majima T. In vivo efficacy and pharmacokinetics of a new hypoxic cell radiosensitizer doranidazole in SUIT-2 human pancreatic cancer xenografted in mouse pancreas. Oncol Rep 2000; 7:23-6; PMID:10601585; http://dx.doi.org/10.3892/or.7.1.23
   PubMed Web of Science ®Google Scholar
• Yu B, Yang M, Shi L, Yao Y, Jiang Q, Li X, Tang LH, Zheng BJ, Yuen KY, Smith DK, et al. Explicit hypoxia targeting with tumor suppression by creating an “obligate” anaerobic Salmonella Typhimurium strain. Sci Rep 2012; 2:436; PMID:22666539; http://dx.doi.org/10.1038/srep00436
   PubMed Web of Science ®Google Scholar
• Avogadri F, Martinoli C, Petrovska L, Chiodoni C, Transidico P, Bronte V, Longhi R, Colombo MP, Dougan G, Rescigno M. Cancer immunotherapy based on killing of Salmonella-infected tumor cells. Cancer research 2005; 65:3920-7; PMID:15867392; http://dx.doi.org/10.1158/0008-5472.CAN-04-3002
   PubMed Web of Science ®Google Scholar
• Schoumacher RA, Ram J, Iannuzzi MC, Bradbury NA, Wallace RW, Hon CT, Kelly DR, Schmid SM, Gelder FB, Rado TA. A cystic fibrosis pancreatic adenocarcinoma cell line. Proc Natl Acad Sci U S A 1990; 87:4012-6; PMID:1692630; http://dx.doi.org/10.1073/pnas.87.10.4012
   PubMed Web of Science ®Google Scholar
• Pan J, Cheng L, Bi X, Zhang X, Liu S, Bai X, Li F, Zhao AZ. Elevation of omega-3 Polyunsaturated Fatty Acids Attenuates PTEN-deficiency Induced Endometrial Cancer Development through Regulation of COX-2 and PGE2 Production. Sci Rep 2015; 5:14958; PMID:26468779; http://dx.doi.org/10.1038/srep14958
   PubMed Web of Science ®Google Scholar
• Eisenstark A, Kazmierczak RA, Dino A, Khreis R, Newman D, Schatten H. Development of Salmonella strains as cancer therapy agents and testing in tumor cell lines. Methods Mol Biol (Clifton, NJ) 2007; 394:323-54; PMID:18363243; http://dx.doi.org/10.1007/978-1-59745-512-1_16
   PubMedGoogle Scholar