Mesenchymal phenotype after chemotherapy is associated with chemoresistance and poor clinical outcome in esophageal cancer

Oncology Reports

Volumn 31, Issue 2, 2014, Pages 589-596

  Hara, Johji ^a   Miyata, Hiroshi ^a   Yamasaki, Makoto ^a   Sugimura, Keijiro ^a   Takahashi, Tsuyoshi ^a   Kurokawa, Yukinori ^a   Nakajima, Kiyokazu ^a   Takiguchi, Shuji ^a   Mori, Masaki ^a   Doki, Yuichiro ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Chemotherapy resistance; E cadherin; Epithelial mesenchymal transition; Esophageal cancer; Snail

Indexed keywords

BETA CATENIN; CISPLATIN; DOXORUBICIN; FLUOROURACIL; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR ZEB1; UVOMORULIN; VIMENTIN;

ADULT; ARTICLE; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER SURVIVAL; CONTINUOUS INFUSION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; ESOPHAGUS CANCER; ESOPHAGUS RESECTION; FEMALE; FOLLOW UP; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MULTIPLE CYCLE TREATMENT; PHENOTYPE; PREOPERATIVE CARE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL TIME; TREATMENT OUTCOME;

AGED; BETA CATENIN; CADHERINS; DRUG RESISTANCE, NEOPLASM; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; ESOPHAGEAL NEOPLASMS; ESOPHAGUS; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; MALE; MIDDLE AGED; TRANSCRIPTION FACTORS; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL; VIMENTIN;

EID: 84892380876     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2013.2876     Document Type: Article

References (38)

1. Medical Research Council Oesophageal Cancer Working Group, Surgical resection with or without preoperative chemotherapy in oesophageal cancer: a randomised controlled trial. Lancet 359: 1727-1733, 2002.
2. Kelsen DP, Ginsberg R, Pajak TF, Sheahan DG, Gunderson L, Mortimer J, Estes N, Haller DG, Ajani J, Kocha W, et al: Chemotherapy followed by surgery compared with surgery alone for localized esophageal cancer. N Engl J Med 339: 1979-1984, 1998.
3. Gebski V, Burmeister B, Smithers BM, Foo K, Zalcberg J and Simes J: Australasian Gastro-Intestinal Trials Group, Survival benefits from neoadjuvant chemoradiotherapy or chemotherapy in oesophageal carcinoma: a meta-analysis. Lancet Oncol 8: 226-234, 2007.
4. Law S, Fok M, Chow S, Chu KM and Wong J: Preoperative chemotherapy versus surgical therapy alone for squamous cell carcinoma of the esophagus: a prospective randomized trial. J Thorac Cardiovasc Surg 114: 210-217, 1997.
5. Ando N, Iizuka T, Ide H, Ishida K, Shinoda M, Nishimaki T, Takiyama W, Watanabe H, Isono K, Aoyama N, et al: Japan Clinical Oncology Group, Surgery plus chemotherapy compared with surgery alone for localized squamous cell carcinoma of the thoracic esophagus: a Japan Clinical Oncology Group Study - JCOG9204. J Clin Oncol 21: 4592-4596, 2003.
6. Yano M, Takachi K, Doki Y, Miyashiro I, Kishi K, Noura S, Eguchi H, Yamada T, Ohue M, Ohigashi H, et al: Preoperative chemotherapy for clinically node-positive patients with squamous cell carcinoma of the esophagus. Dis Esophagus 19: 158-163, 2006.
7. Tepper J, Krasna MJ, Niedzwiecki D, Hollis D, Reed CE, Goldberg R, Kiel K, Willett C, Sugarbaker D and Mayer R: Phase III trial of trimodality therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781. J Clin Oncol 26: 1086-1092, 2008.
8. Hilgenberg AD, Carey RW, Wilkins EW Jr, Choi NC, Mathisen DJ and Grillo HC: Preoperative chemotherapy, surgical resection, and selective postoperative therapy for squamous cell carcinoma of the esophagus. Ann Thorac Surg 45: 357-363, 1998.
9. Ancona E, Ruol A, Santi S, Merigliano S, Sileni VC, Koussis H, Zaninotto G, Bonavina L and Peracchia A: Only pathologic complete response to neoadjuvant chemotherapy improves significantly the long term survival of patients with resectable esophageal squamous cell carcinoma: final report of a randomized, controlled trial of preoperative chemotherapy versus surgery alone. Cancer 191: 2165-2174, 2001.
10. Urschel JD, Vasan H and Blewett CJ: A meta-analysis of randomized controlled trials that compared neoadjuvant chemotherapy and surgery to surgery alone for resectable esophageal cancer. Am J Surg 183: 274-279, 2002.
11. Kalluri R and Weinberg RA: The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428, 2009.
12. Zeisberg EM, Tarnavski O, Zeisberg M, Dorfman AL, McMullen JR, Gustafsson E, Chandraker A, Yuan X, Pu WT, Roberts AB, et al: Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 13: 952-961, 2007.
13. Zeisberg M, Yang C, Martino M, Duncan MB, Rieder F, Tanjore H and Kalluri R: Fibroblasts derive from hepatocytes in liver fibrosis via epithelial to mesenchymal transition. J Biol Chem 282: 23337-23347, 2007.
14. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D and Chapman HA: Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA 103: 13180-13185, 2006.
15. Thiery JP: Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454, 2002.
16. Yang J and Weinberg RA: Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14: 818-829, 2008.
17. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al: The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715, 2008.
18. Biddle A, Liang X, Gammon L, Fazil B, Harper LJ, Emich H, Costea DE and Mackenzie IC: Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res 71: 5317-5326, 2011.
19. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY and Bapat SA: Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 27: 2059-2068, 2009.
20. Eyler CE and Rich JN: Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 26: 2839-2845, 2008.
21. Baumann M, Krause M and Hill R: Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 8: 545-554, 2008.
22. Miyata H, Yoshioka A, Yamasaki M, Nushijima Y, Takiguchi S, Fujiwara Y, Nishida T, Mano M, Mori M and Doki Y: Tumor budding in tumor invasive front predicts prognosis and survival of patients with esophageal squamous cell carcinomas receiving neoadjuvant chemotherapy. Cancer 115: 3324-3334, 2009.
23. Usami Y, Chiba H, Nakayama F, Ueda J, Matsuda Y, Sawada N, Komori T, Ito A and Yokozaki H: Reduced expression of claudin-7 correlates with invasion and metastasis in squamous cell carcinoma of the esophagus. Hum Pathol 37: 569-577, 2006.
24. Miller AB, Hoogstraten B, Staquet M and Winkler A: Reporting results of cancer treatment. Cancer 47: 207-214, 1981.
25. Japan Esophageal Society: Japanese classification of esophageal cancer, tenth edition: parts II and III. Esophagus 6: 71-94, 2009.
26. Lombaerts M, van Wezel T, Philippo K, Dierssen JW, Zimmerman RM, Oosting J, van Eijk R, Eilers PH, van de Water B, Cornelisse CJ and Cleton-Jansen AM: E-cadherin transcriptional downregulation by promoter methylation but not mutation is related to epithelial-to-mesenchymal transition in breast cancer cell lines. Br J Cancer 94: 661-671, 2006.
27. Shiozaki H, Tahara H, Oka H, Miyata M, Kobayashi K, Tamura S, Iihara K, Doki Y, Hirano S, Takeichi M and Mori T: Expression of immunoreactive E-cadherin adhesion molecules in human cancers. Am J Pathol 139: 17-23, 1999.
28. Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R, Gray MJ, Cheng H, Hoff PM and Ellis LM: Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res 12: 4147-4153, 2006.
29. Kajiyama H, Shibata K, Terauchi M, Yamashita M, Ino K, Nawa A and Kikkawa F: Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. Int J Oncol 31: 277-283, 2007.
30. Shah AN, Summy JM, Zhang J, Park SI, Parikh NU and Gallick GE: Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann Surg Oncol 14: 3629-3637, 2007.
31. Arumugam T, Ramachandran V, Fournier KF, Wang H, Marquis L, Abbruzzese JL, Gallick GE, Logsdon CD, McConkey DJ and Choi W: Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res 69: 5820-5828, 2009.
32. Peinado H, Olmeda D and Cano A: Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7: 415-428, 2007.
33. Hsu DS, Lan HY, Huang CH, Tai SK, Chang SY, Tsai TL, Chang CC, Tzeng CH, Wu KJ, Kao JY and Yang MH: Regulation of excision repair cross-complementation group 1 by Snail contributes to cisplatin resistance in head and neck cancer. Clin Cancer Res 16: 4561-4571, 2010.
34. Hirohashi S and Kanai Y: Cell adhesion system and human cancer morphogenesis. Cell Sci 94: 575-581, 2003.
35. Nieto MA: The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3: 155-166, 2002.
36. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI, et al: Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 106: 13820-13825, 2009.
37. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, Basu D, Gimotty P, Vogt T and Herlyn M: A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141: 583-594, 2010.
38. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, et al: A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141: 69-80, 2010.