Snail contributes to the maintenance of stem cell-like phenotype cells in human pancreatic cancer

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Zhou, Wei ^a   Lv, Ran ^a   Qi, Weilin ^a   Wu, Di ^a   Xu, Yunyun ^a   Liu, Wei ^a   Mou, Yiping ^a   Wang, Liewei ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX2; UVOMORULIN; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR XENOGRAFT;

ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS; PHENOTYPE; TRANSCRIPTION FACTORS; TUMOR BURDEN;

EID: 84900456721     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087409     Document Type: Article

References (40)

1. Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62: 10-29.
2. Magee CJ, Ghaneh P, Neoptolemos JP (2002) Surgical and medical therapy for pancreatic carcinoma. Best Pract Res Clin Gastroenterol 16: 435-455.
3. Jones RJ, Matsui WH, Smith BD (2004) Cancer stem cells: are we missing the target? J Natl Cancer Inst 96: 583-585. (Pubitemid 38584981)
4. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715. (Pubitemid 351636299)
5. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, et al. (2009) 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.
6. Polyak K, Weinberg RA (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273.
7. Nieto M.A (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3: 155-166.
8. Fan F, Samuel S, Evans KW, Lu J, Xia L, et al. (2012) Overexpression of Snail induces epithelial-mesenchymal transition and a cancer stem cell-like phenotype in human colorectal cancer cells. Cancer Med 1: 5-16.
9. Hotz B, Arndt M, Dullat S, Bhargava S, Buhr HJ, et al. (2007) Epithelial to mesenchymal transition: expression of the regulators snail, slug, and twist in pancreatic cancer. Clin Cancer Res 13: 4769-4776. (Pubitemid 47294783)
10. von Burstin J, Eser S, Paul MC, Seidler B, Brandl M, et al. (2009) E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex. Gastroenterology 137: 361-371, 371 e1-5.
11. Shin NR, Jeong EH, Choi CI, Moon HJ, Kwon CH, et al. (2012) Overexpression of Snail is associated with lymph node metastasis and poor prognosis in patients with gastric cancer. BMC Cancer 12: 521.
12. Kuo KT, Chou TY, Hsu HS, Chen WL, Wang LS (2012) Prognostic significance of NBS1 and Snail expression in esophageal squamous cell carcinoma. Ann Surg Oncol 19: Suppl 3, S549-557.
13. van Nes JG, de Kruijf EM, Putter H, Faratian D, Munro A, et al. (2012) Coexpression of SNAIL and TWIST determines prognosis in estrogen receptor-positive early breast cancer patients. Breast Cancer Res Treat 133: 49-59.
14. Shankar S, Nall D, Tang SN, Meeker D, Passarini J, et al. (2011) Resveratrol inhibits pancreatic cancer stem cell characteristics in human and KrasG12D transgenic mice by inhibiting pluripotency maintaining factors and epithelial-mesenchymal transition. PLoS One 6: e16530.
15. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, et al. (2008) Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 10: 295-305.
16. Nishioka R, Itoh S, Gui T, Gai Z, Oikawa K, et al. (2010) SNAIL induces epithelial-to-mesenchymal transition in a human pancreatic cancer cell line (BxPC3) and promotes distant metastasis and invasiveness in vivo. Exp Mol Pathol, 89, 149-157.
17. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323. (Pubitemid 47355323)
18. Zhu J, He J, Liu Y, Simeone DM, Lubman DM (2012) Identification of glycoprotein markers for pancreatic cancer CD24+CD44+ stem-like cells using nano-LC-MS/MS and tissue microarray. J Proteome Res 11: 2272-2281.
19. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037.
20. Rasheed ZA, Yang J, Wang Q, Kowalski J, Freed I, et al. (2010) Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst 102: 340-351.
21. Kim MP, Fleming JB, Wang H, Abbruzzese JL, Choi W, et al. (2011) ALDH activity selectively defines an enhanced tumor-initiating cell population relative to CD133 expression in human pancreatic adenocarcinoma. PLoS One 6: e20636.
22. Chen YC, Chen YW, Hsu HS, Tseng LM, Huang PI, et al. (2009) Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun 385: 307-313.
23. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
24. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, et al. (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17: 126-140. (Pubitemid 36062514)
25. Pesce M, Schöler HR (2001) Oct-4: gatekeeper in the beginnings of mammalian development. Stem Cells 19: 271-278. (Pubitemid 32721093)
26. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, et al. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113: 631-642. (Pubitemid 36694188)
27. Leis O, Eguiara A, Lopez-Arribillaga E, Alberdi MJ, Hernandez-Garcia S, et al. (2012) Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene 31: 1354-1365.
28. Kumar SM, Liu S, Lu H, Zhang H, Zhang PJ, et al. (2012) Acquired cancer stem cell phenotypes through Oct4-mediated dedifferentiation. Oncogene 31: 4898-4911.
29. Jeter CR, Liu B, Liu X, Chen X, Liu C, et al. (2011) NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation. Oncogene 30: 3833-3845.
30. Luo W, Li S, Peng B, Ye Y, Deng X, et al. (2013) Embryonic stem cells markers SOX2, OCT4 and Nanog expression and their correlations with epithelial-mesenchymal transition in nasopharyngeal carcinoma. PLoS One 8: e56324.
31. Chiou SH, Wang ML, Chou YT, Chen CJ, Hong CF, et al. (2010) Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation. Cancer Res 70: 10433-10444.
32. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, et al. (2012) EMT and dissemination precede pancreatic tumor formation. Cell 148: 349-361.
33. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T (2005) Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer 5: 744-749. (Pubitemid 41486367)
34. Chaffer CL, Weinberg RA (2011) A perspective on cancer cell metastasis. Science 331: 1559-1564.
35. Brabletz T (2012) To differentiate or not-routes towards metastasis. Nat Rev Cancer 12: 425-436.
36. Zhang L, Huang G, Li X, Zhang Y, Jiang Y, et al. (2013) Hypoxia induces epithelial-mesenchymal transition via activation of SNAI1 by hypoxia-inducible factor-1alpha in hepatocellular carcinoma. BMC Cancer 13: 108.
37. Wang H, Wang HS, Zhou BH, Li CL, Zhang F, et al. (2013) Epithelial-mesenchymal transition (EMT) induced by TNF-alpha requires AKT/GSK-3beta-mediated stabilization of snail in colorectal cancer. PLoS One 8: e56664.
38. Kim NH, Kim HS, Li XY, Lee I, Choi HS, et al. (2011) A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J Cell Biol 195: 417-433.
39. Siemens H, Jackstadt R, Hünten S, Kaller M, Menssen A, et al. (2011) miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 10: 4256-4271.
40. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, et al. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593-601. (Pubitemid 351627379)