1,081
Views
15
CrossRef citations to date
0
Altmetric
Research Paper

Tumor targeting Salmonella typhimurium A1-R in combination with gemcitabine (GEM) regresses partially GEM-resistant pancreatic cancer patient-derived orthotopic xenograft (PDOX) nude mouse models

, , , , , , , , , & show all
Pages 2019-2026 | Received 21 Feb 2018, Accepted 17 May 2018, Published online: 19 Sep 2018

References

  • Burris HA 3rd, Moore MJ, Andersen J, et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol. 1997;15:2403–2413.
  • Jenks S. AACR highlights: promise for treating pancreatic cancer. J Natl Cancer Inst. 2011;103:786–787.
  • Conroy T, Desseigne F, Ychou M, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364:1817–1825.
  • Von Hoff DD, Ervin T, Arena FP, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med. 2013;369:1691–1703.
  • Fu X, Le P, Hoffma RM. A metastatic-orthotopic transplant nude-mouse model of human patient breast cancer. Anticancer Res. 1993;13:901–904.
  • Fu X, Hoffman RM. Human ovarian carcinoma metastatic models constructed in nude mice by orthotopic transplantation of histologically-intact patient specimens. Anticancer Res. 1993;13:283–286.
  • Wang X, Fu X, Hoffman RM. A new patient-like metastatic model of human lung cancer constructed orthotopically with intact tissue via thoracotomy in immunodeficient mice. Int J Cancer. 1992;51:992–995.
  • Hiroshima Y, Zhang Y, Zhang N, et al. Establishment of a patient-derived orthotopic xenograph (PDOX) model of HER-2-positive cervical cancer expressing the clinical metastatic pattern. PLoS One. 2015;10:e0117417.
  • Fu X, Besterman JM, Monosov A, et al. Models of human metastatic colon cancer in nude mice orthotopically constructed by using histologically intact patient specimens. Proc Natl Acad Sci USA. 1991;88:9345–9349.
  • Metildi CA, Kaushal S, Luiken GA, et al. Fluorescently-labeled chimeric anti-CEA antibody improves detection and resection of human colon cancer in a patient-derived orthotopic xenograft (PDOX) nude mouse model. J Surg Oncol. 2014;109:451–458.
  • Hiroshima Y, Maawy A, Metildi CA, et al. Successful fluorescence-guided surgery on human colon cancer patient-derived orthotopic xenograft mouse models using a fluorophore-conjugated anti-CEA antibody and a portable imaging system. J Laparoendosc Adv Surg Tech A. 2014;24:241–247.
  • Furukawa T, Kubota T, Watanabe M, et al. Orthotopic transplantation of histologically intact clinical specimens of stomach cancer to nude mice: correlation of metastatic sites in mouse and individual patient donors. Int J Cancer. 1993;53:608–612.
  • Murakami T, DeLong J, Eilber FC, et al. Tumor-targeting Salmonella typhimurium A1-R in combination with doxorubicin eradicate soft tissue sarcoma in a patient-derived orthotopic xenograft PDOX model. Oncotarget. 2016;7:12783–12790.
  • Hiroshima Y, Zhao M, Zhang Y, et al. Tumor-targeting Salmonella typhimurium A1-R arrests a chemo-resistant patient soft-tissue sarcoma in nude mice. PLoS One. 2015;10:e0134324.
  • Kiyuna T, Murakami T, Tome Y, et al. 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. 2016;7:33046–33054.
  • Murakami T, Singh AS, Kiyuna T, et al. Effective molecular targeting of CDK4/6 and IGF-1R in a rare FUS-ERG fusion CDKN2A-deletion doxorubicin-resistant Ewing’s sarcoma in a patient-derived orthotopic xenograft (PDOX) nude-mouse model. Oncotarget. 2016;7:47556–47564.
  • Hiroshima Y, Zhang Y, Zhang N, et al. Patient-derived orthotopic xenograft (PDOX) nude mouse model of soft-tissue sarcoma more closely mimics the patient behavior in contrast to the subcutaneous ectopic model. Anticancer Res. 2015;35:697–701.
  • Igarashi K, Murakami T, Kawaguchi K, et al. A patient-derived orthotopic xenograft (PDOX) mouse model of an cisplatinum-resistant osteosarcoma lung metastasis that was sensitive to temozolomide and trabectedin: implications for precision oncology. Oncotarget. 2017;8:62111–62119.
  • Igarashi K, Kawaguchi K, Kiyuna T, et al. Temozolomide combined with irinotecan caused regression in an adult pleomorphic rhabdomyosarcoma patient-derived orthotopic xenograft (PDOX) nude-mouse model. Oncotarget. 2017;8:75874–75880.
  • Igarashi K, Kawaguchi K, Murakami T, et al. Intra-arterial administration of tumor-targeting Salmonella typhimurium A1-R regresses a cisplatin-resistant relapsed osteosarcoma in a patient-derived orthotopic xenograft (PDOX) mouse model. Cell Cycle. 2017;16:1164–1170.
  • Murakami T, Kiyuna T, Kawaguchi K, et al. The irony of highly-effective bacterial therapy of a patient-derived orthotopic xenograft (PDOX) model of Ewing’s sarcoma, which was blocked by Ewing himself 80 years ago. Cell Cycle. 2017;16:1046–1052.
  • Igarashi K, Kawaguchi K, Murakami T, et al. High efficacy of pazopanib on an undifferentiated spindle-cell sarcoma resistant to first-line therapy is identified with a patient-derived orthotopic xenograft (PDOX) nude mouse model. J Cell Biochem. 2017;118:2739–3743.
  • Kiyuna T, Murakami T, Tome Y, et al. Analysis of stroma labeling during multiple passage of a sarcoma imageable patient-derived orthotopic xenograft (iPDOX) in red fluorescent protein transgenic nude mice. J Cell Biochem. 2017;118:3367–3371.
  • Igarashi K, Murakami T, Kawaguchi K, et al. A patient-derived orthotopic xenograft (PDOX) mouse model of an cisplatinum-resistant osteosarcoma lung metastasis that was sensitive to temozolomide and trabectedin: implications for precision oncology. Oncotarget. 2017;8:62111–62119.
  • Igarashi K, Kawaguchi K, Murakami T, et al. A novel anionic-phosphate-platinum complex effectively targets an undifferentiated pleomorphic sarcoma better than cisplatinum and doxorubicin in a patient-derived orthotopic xenograft (PDOX). Oncotarget. 2017;8:63353–63359.
  • Miyake K, Murakami T, Kiyuna T, et al. The combination of temozolomide-irinotecan regresses a doxorubicin-resistant patient-derived orthotopic xenograft (PDOX) nude-mouse model of recurrent Ewing’s sarcoma with a FUS-ERG fusion and CDKN2A deletion: direction for third-line patient therapy. Oncotarget. 2017;8:103129–103136.
  • Murakami T, Li S, Han Q, et al. Recombinant methioninase effectively targets a Ewing’s sarcoma in a patient-derived orthotopic xenograft (PDOX) nude-mouse model. Oncotarget. 2017;8:35630–35638.
  • Igarashi K, Li S, Han Q, et al. Growth of a doxorubicin-resistant undifferentiated spindle-cell sarcoma PDOX is arrested by metabolic targeting with recombinant methioninase. J Cell Biochem. Forthcoming.
  • Igarashi K, Kawaguchi K, Li S, et al. Recombinant methioninase in combination with DOX overcomes first-line DOX resistance in a patient-derived orthotopic xenograft nude-mouse model of undifferentiated spindle-cell sarcoma. Cancer Lett. submitted.
  • Igarashi K, Kawaguchi K, Kiyuna T, et al. Tumor-targeting Salmonella typhimurium A1-R combined with recombinant methioninase and cisplatinum eradicates an osteosarcoma cisplatinum-resistant lung metastasis in a patient-derived orthotopic xenograft (PDOX) mouse model: decoy, trap and kill chemotherapy moves toward the clinic. Cell Cycle. submitted.
  • Kawaguchi K, Igarashi K, Li S, et al. Combination treatment with recombinant methioninase enables temozolomide to arrest a BRAF V600E melanoma growth in a patient-derived orthotopic xenograft. Oncotarget. 2017;8:85516–85525.
  • Kawaguchi K, Igarashi K, Li S, et al. Recombinant methioninase (rMETase) is an effective therapeutic for BRAF-V600E-negative as well as -positive melanoma in patient-derived orthotopic xenograft (PDOX) mouse models. Oncotarget. 2018;9:915–923.
  • Kawaguchi K, Han Q, Li S, et al. Intra-tumor L-methionine level highly correlates with tumor size in both pancreatic cancer and melanoma patient-derived orthotopic xenograft (PDOX) nude-mouse models. Oncotarget. Forthcoming.
  • Kawaguchi K, Han Q, Li S, et al. Targeting methionine with oral recombinant methioninase (o-rMETase) arrests a patient-derived orthotopic xenograft (PDOX) model of BRAF-V600E mutant melanoma: implications for clinical cancer therapy and prevention. Cell Cycle. Forthcoming.
  • Kawaguchi K, Murakami T, Chmielowski B, et al. Vemurafenib-resistant BRAF-V600E mutated melanoma is regressed by MEK targeting drug trametinib, but not cobimetinib in a patient-derived orthotopic xenograft (PDOX) mouse model. Oncotarget. 2016;7:71737–71743.
  • Kawaguchi K, Igarashi K, Murakami T, et al. Tumor-targeting Salmonella typhimurium A1-R combined with temozolomide regresses malignant melanoma with a BRAF-V600 mutation in a patient-derived orthotopic xenograft (PDOX) model. Oncotarget. 2016;7:85929–85936.
  • Kawaguchi K, Igarashi K, Murakami T, et al. Tumor-targeting Salmonella typhimurium A1-R sensitizes melanoma with a BRAF-V600E mutation to vemurafenib in a patient-derived orthotopic xenograft (PDOX) nude mouse model. J Cell Biochem. 2017;118:2314–2319.
  • Yamamoto M, Zhao M, Hiroshima Y, et al. Efficacy of tumor-targeting Salmonella typhimurium A1-R on a melanoma patient-derived orthotopic xenograft (PDOX) nude-mouse model. PLoS One. 2016;11:e0160882.
  • Hiroshima Y, Zhang Y, Murakami T, 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.
  • Fu X, Guadagni F, Hoffman RM. A metastatic nude-mouse model of human pancreatic cancer constructed orthotopically with histologically intact patient specimens. Proc Natl Acad Sci USA. 1992;89:5645–5649.
  • Hiroshima Y, Maawy A, Zhang Y, et al. Metastatic recurrence in a pancreatic cancer patient derived orthotopic xenograft (PDOX) nude mouse model is inhibited by neoadjuvant chemotherapy in combination with fluorescence-guided surgery with an anti-CA 19–9-conjugated fluorophore. PLoS One. 2014;9:e114310.
  • Hiroshima Y, Maawy AA, Katz MH, et al. Selective efficacy of zoledronic acid on metastasis in a patient-derived orthotopic xenograph (PDOX) nude-mouse model of human pancreatic cancer. J Surg Oncol. 2015;111:311–315.
  • Hoffman RM. Patient-derived orthotopic xenografts: better mimic of metastasis than subcutaneous xenografts. Nat Rev Cancer. 2015;15:451–452.
  • Hoffman RM, Zhao M. Methods for the development of tumor-targeting bacteria. Expert Opin Drug Discov. 2014;9:741–750.
  • Hiroshima Y, Zhao M, Maawy A, et al. Efficacy of Salmonella typhimurium A1-R versus chemotherapy on a pancreatic cancer patient-derived orthotopic xenograft (PDOX). J Cell Biochem. 2014;115:1254–1261.
  • Hayashi K, Zhao M, Yamauchi K, et al. 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.
  • Murakami T, Igarashi K, Kawaguchi K, et al. Tumor-targeting Salmonella typhimurium A1-R regresses an osteosarcoma in a patient-derived xenograph model resistant to a molecular-targeting drug. Oncotarget. 2017;8:8035–8042.
  • Hoffman RM, editor. Bacterial therapy of cancer: methods and protocols. Methods in molecular biology 1409. Walker, John M., series ed. New York (NY): Humana Press (Springer Science+Business Media); 2016.
  • Zhao M, Yang M, Li X-M, et al. Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proc Natl Acad Sci USA. 2005;102:755–760.
  • Yano S, Zhang Y, Zhao M, et al. 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.
  • Yano S, Takehara K, Zhao M, et al. Tumor-specific cell-cycle decoy by Salmonella typhimurium A1-R combined with tumor-selective cell-cycle trap by methioninase overcome tumor intrinsic chemoresistance as visualized by FUCCI imaging. Cell Cycle. 2016;15:1715–1723.
  • Igarashi K, Kawaguchi K, Kiyuna T, et al. Tumor-targeting Salmonella typhimurium A1-R combined with recombinant methioninase and cisplatinum eradicates an osteosarcoma cisplatinum-resistant lung metastasis in a patient-derived orthotopic xenograft (PDOX) mouse model: decoy, trap and kill chemotherapy moves toward the clinic. Cell Cycle. Forthcoming.
  • Yano S, Tazawa H, Hashimoto Y, et al. A genetically engineered oncolytic adenovirus decoys and lethally traps quiescent cancer stem-like cells into S/G2/M phases. Clin Cancer Res. 2013;19:6495–6505.
  • Yano S, Zhang Y, Miwa S, et al. Spatial-temporal FUCCI imaging of each cell in a tumor demonstrates locational dependence of cell cycle dynamics and chemoresponsiveness. Cell Cycle. 2014;13:2110–2119.
  • Blagosklonny MV. Matching targets for selective cancer therapy. Drug Discov Today. 2003;8:1104–1107.
  • Blagosklonny MV. Teratogens as anti-cancer drugs. Cell Cycle. 2005;4:1518–1521.
  • 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;15:936–941.
  • Blagosklonny MV. Target for cancer therapy: proliferating cells or stem cells. Leukemia. 2006;20:385–391.
  • Apontes P, Leontieva OV, Demidenko ZN, et al. Exploring long-term protection of normal human fibroblasts and epithelial cells from chemotherapy in cell culture. Oncotarget. 2011;2:222–233.
  • Blagosklonny MV. Tissue-selective therapy of cancer. Br J Cancer. 2003;89:1147–1151.
  • Matsuo Y, Raimondo M, Woodward TA, et al. CXC-chemokine/CXCR2 biological axis promotes angiogenesis in vitro and in vivo in pancreatic cancer. Int J Cancer. 2009;125:1027–1037.
  • Zhao M, Yang M, Ma H, et al. Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice. Cancer Res. 2006;66:7647–7652.
  • Zhao M, Geller J, Ma H, et al. 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.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.