The role of pluripotency factors to drive stemness in gastrointestinal cancer

Stem Cell Research

Volumn 16, Issue 2, 2016, Pages 349-357

  Müller, Martin ^a   Hermann, Patrick C ^a   Liebau, Stefan ^b   Weidgang, Clair ^c   Seufferlein, Thomas ^a   Kleger, Alexander ^a   Perkhofer, Lukas ^a  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FETAL ANTIGEN; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; STAT3 PROTEIN; STEM CELL FACTOR; TRANSCRIPTION FACTOR SOX2; KRUPPEL LIKE FACTOR; TRANSCRIPTION FACTOR SOX;

CANCER CELL LINE; CANCER STEM CELL; CARCINOGENESIS; CELL DEDIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL PLASTICITY; CLINICAL FEATURE; DIGESTIVE SYSTEM CANCER; DYSPLASIA; EMBRYONIC STEM CELL; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; HUMAN; IN VIVO STUDY; NEPHROBLASTOMA; NONHUMAN; PANCREAS CANCER; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REVIEW; STEM CELL SELF-RENEWAL; CYTOLOGY; GASTROINTESTINAL TUMOR; GENETICS; METABOLISM; NUCLEAR REPROGRAMMING; PATHOLOGY; STEM CELL;

CARCINOGENESIS; CELLULAR REPROGRAMMING; EPITHELIAL-MESENCHYMAL TRANSITION; GASTROINTESTINAL NEOPLASMS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; OCTAMER TRANSCRIPTION FACTOR-3; PROTO-ONCOGENE PROTEINS C-MYC; SOXB1 TRANSCRIPTION FACTORS; STEM CELLS;

EID: 84958541521     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2016.02.005     Document Type: Review

References (137)

1. Abad M., Mosteiro L., Pantoja C., et al. Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 2013, 502:340-345.
2. Akita H., Marquardt J.U., Durkin M.E., et al. MYC activates stem-like cell potential in hepatocarcinoma by a p53-dependent mechanism. Cancer Res. 2014, 74:5903-5913.
3. Al-Marzoqee F.Y., Khoder G., Al-Awadhi H., et al. Upregulation and inhibition of the nuclear translocation of Oct4 during multistep gastric carcinogenesis. Int. J. Oncol. 2012, 41:1733-1743.
4. Arsic N., Gadea G., Lagerqvist E.L., et al. The p53 isoform Delta133p53beta promotes cancer stem cell potential. Stem Cell Rep. 2015, 4:531-540.
5. Avior Y., Biancotti J.C., Benvenisty N. TeratoScore: assessing the differentiation potential of human pluripotent stem cells by quantitative expression analysis of teratomas. Stem Cell Rep. 2015, 4:967-974.
6. Basu-Roy U., Seo E., Ramanathapuram L., et al. Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene 2012, 31:2270-2282.
7. Beroukhim R., Mermel C.H., Porter D., et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010, 463:899-905.
8. Bhave V.S., Paranjpe S., Bowen W.C., et al. Genes inducing iPS phenotype play a role in hepatocyte survival and proliferation in vitro and liver regeneration in vivo. Hepatology 2011, 54:1360-1370.
9. Brambrink T., Foreman R., Welstead G.G., et al. Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell 2008, 2:151-159.
10. Burrell R.A., McGranahan N., Bartek J., et al. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 2013, 501:338-345.
11. Chen X., Whitney E.M., Gao S.Y., et al. Transcriptional profiling of kruppel-like factor 4 reveals a function in cell cycle regulation and epithelial differentiation. J. Mol. Biol. 2003, 326:665-677.
12. Chen Z., Xu W.R., Qian H., et al. Oct4, a novel marker for human gastric cancer. J. Surg. Oncol. 2009, 99:414-419.
13. Chen X., Wang Y., Xia H., et al. Loss of E-cadherin promotes the growth, invasion and drug resistance of colorectal cancer cells and is associated with liver metastasis. Mol. Biol. Rep. 2012, 39:6707-6714.
14. Chen S., Xu Y., Chen Y., et al. SOX2 gene regulates the transcriptional network of oncogenes and affects tumorigenesis of human lung cancer cells. PLoS One 2012, 7.
15. Choi B.J., Cho Y.G., Song J.W., et al. Altered expression of the KLF4 in colorectal cancers. Pathol. Res. Pract. 2006, 202:585-589.
16. Christofori G. New signals from the invasive front. Nature 2006, 441:444-450.
17. Cioffi M., Trabulo S.M., Sanchez-Ripoll Y., et al. The miR-17-92 cluster counteracts quiescence and chemoresistance in a distinct subpopulation of pancreatic cancer stem cells. Gut 2015.
18. Clevers H. The cancer stem cell: premises, promises and challenges. Nat. Med. 2011, 17:313-319.
19. Comes S., Gagliardi M., Laprano N., et al. L-proline induces a mesenchymal-like invasive program in embryonic stem cells by remodeling H3K9 and H3K36 methylation. Stem Cell Rep. 2013, 1:307-321.
20. Conacci-Sorrell M., Simcha I., Ben-Yedidia T., et al. Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of beta-catenin signaling, slug, and MAPK. J. Cell Biol. 2003, 163:847-857.
21. Croce C.M. Oncogenes and cancer. N. Engl. J. Med. 2008, 358:502-511.
22. Cui J., Shi M., Quan M., et al. Regulation of EMT by KLF4 in gastrointestinal cancer. Curr. Cancer Drug Targets 2013, 13:986-995.
23. Curry E.L., Moad M., Robson C.N., et al. Using induced pluripotent stem cells as a tool for modelling carcinogenesis. World J. Stem Cells 2015, 7:461-469.
24. Cusulin C., Chesnelong C., Bose P., et al. Precursor states of brain tumor initiating cell lines are predictive of survival in xenografts and associated with glioblastoma subtypes. Stem Cell Rep. 2015, 5:1-9.
25. Dai X., Ge J., Wang X., et al. OCT4 regulates epithelial-mesenchymal transition and its knockdown inhibits colorectal cancer cell migration and invasion. Oncol. Rep. 2013, 29:155-160.
26. Dalerba P., Kalisky T., Sahoo D., et al. Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat. Biotechnol. 2011, 29:1120-1127.
27. Dang C.V. MYC on the path to cancer. Cell 2012, 149:22-35.
28. Dang D.T., Chen X., Feng J., et al. Overexpression of Kruppel-like factor 4 in the human colon cancer cell line RKO leads to reduced tumorigenecity. Oncogene 2003, 22:3424-3430.
29. Dean M., Fojo T., Bates S. Tumour stem cells and drug resistance. Nat. Rev. Cancer 2005, 5:275-284.
30. Dong Z., Zeng Q., Luo H., et al. Increased expression of OCT4 is associated with low differentiation and tumor recurrence in human hepatocellular carcinoma. Pathol. Res. Pract. 2012, 208:527-533.
31. Dunn S.J., Martello G., Yordanov B., et al. Defining an essential transcription factor program for naive pluripotency. Science 2014, 344:1156-1160.
32. Esch D., Vahokoski J., Groves M.R., et al. A unique Oct4 interface is crucial for reprogramming to pluripotency. Nat. Cell Biol. 2013, 15:295-301.
33. Fischer K.R., Durrans A., Lee S., et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature 2015, 527:472-476.
34. Frankenberg S.R., Frank D., Harland R., et al. The POU-er of gene nomenclature. Development 2014, 141:2921-2923.
35. Fujii Y., Yoshihashi K., Suzuki H., et al. CDX1 confers intestinal phenotype on gastric epithelial cells via induction of stemness-associated reprogramming factors SALL4 and KLF5. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:20584-20589.
36. Gabay M., Li Y., Felsher D.W. MYC activation is a hallmark of cancer initiation and maintenance. Cold Spring Harb. Perspect. Med. 2014, 4.
37. Gazouli M., Roubelakis M.G., Theodoropoulos G.E., et al. OCT4 spliced variant OCT4B1 is expressed in human colorectal cancer. Mol. Carcinog. 2012, 51:165-173.
38. Gen Y., Yasui K., Nishikawa T., et al. SOX2 promotes tumor growth of esophageal squamous cell carcinoma through the AKT/mammalian target of rapamycin complex 1 signaling pathway. Cancer Sci. 2013, 104:810-816.
39. Greenman C., Stephens P., Smith R., et al. Patterns of somatic mutation in human cancer genomes. Nature 2007, 446:153-158.
40. Gutierrez-Aranda I., Ramos-Mejia V., Bueno C., et al. Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem Cells 2010, 28:1568-1570.
41. Han X., Fang X., Lou X., et al. Silencing SOX2 induced mesenchymal-epithelial transition and its expression predicts liver and lymph node metastasis of CRC patients. PLoS One 2012, 7.
42. He C., Jiang H., Geng S., et al. Expression of c-myc and fas correlates with perineural invasion of pancreatic cancer. Int. J. Clin. Exp. Pathol. 2012, 5:339-346.
43. He C., Jiang H., Geng S., et al. Expression and prognostic value of c-myc and fas (CD95/APO1) in patients with pancreatic cancer. Int. J. Clin. Exp. Pathol. 2014, 7:742-750.
44. Hermann P.C., Huber S.L., Herrler T., et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1:313-323.
45. Hermann P.C., Trabulo S.M., Sainz B., et al. Multimodal treatment eliminates cancer stem cells and leads to long-term survival in primary human pancreatic cancer tissue xenografts. PLoS One 2013, 8.
46. Hermann P.C., Sancho P., Canamero M., et al. Nicotine promotes initiation and progression of KRAS-induced pancreatic cancer via Gata6-dependent dedifferentiation of acinar cells in mice. Gastroenterology 2014, 147. (1119-33.e4).
47. Herreros-Villanueva M., Zhang J.S., Koenig A., et al. SOX2 promotes dedifferentiation and imparts stem cell-like features to pancreatic cancer cells. Oncogenesis 2013, 2.
48. Hochedlinger K., Yamada Y., Beard C., et al. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 2005, 121:465-477.
49. Holczbauer A., Factor V.M., Andersen J.B., et al. Modeling pathogenesis of primary liver cancer in lineage-specific mouse cell types. Gastroenterology 2013, 145:221-231.
50. Honing J., Pavlov K.V., Meijer C., et al. Loss of CD44 and SOX2 expression is correlated with a poor prognosis in esophageal adenocarcinoma patients. Ann. Surg. Oncol. 2014, 21(Suppl. 4):S657-S664.
51. Hsu L.S., Chan C.P., Chen C.J., et al. Decreased Kruppel-like factor 4 (KLF4) expression may correlate with poor survival in gastric adenocarcinoma. Med. Oncol. 2013, 30:632.
52. Hu T., Liu S., Breiter D.R., et al. Octamer 4 small interfering RNA results in cancer stem cell-like cell apoptosis. Cancer Res. 2008, 68:6533-6540.
53. Jenkins T.D., Opitz O.G., Okano J., et al. Transactivation of the human keratin 4 and Epstein-Barr virus ED-L2 promoters by gut-enriched Kruppel-like factor. J. Biol. Chem. 1998, 273:10747-10754.
54. Jiang X.M., Zhang J.B., Xiong J., et al. Altered distribution and expression pattern of E-cadherin in hepatocellular carcinomas: correlations with prognosis and clinical features. Asian Pac. J. Cancer Prev. 2012, 13:6455-6461.
55. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
56. Kaposi-Novak P., Libbrecht L., Woo H.G., et al. Central role of c-myc during malignant conversion in human hepatocarcinogenesis. Cancer Res. 2009, 69:2775-2782.
57. Karayiannakis A.J., Syrigos K.N., Chatzigianni E., et al. Aberrant E-cadherin expression associated with loss of differentiation and advanced stage in human pancreatic cancer. Anticancer Res. 1998, 18:4177-4180.
58. Katz J.P., Perreault N., Goldstein B.G., et al. Loss of Klf4 in mice causes altered proliferation and differentiation and precancerous changes in the adult stomach. Gastroenterology 2005, 128:935-945.
59. Kim C.G., Choi I.J., Lee J.Y., et al. Biopsy site for detecting Helicobacter pylori infection in patients with gastric cancer. J. Gastroenterol. Hepatol. 2009, 24:469-474.
60. Kopp J.L., von Figura G., Mayes E., et al. Identification of Sox9-dependent acinar-to-ductal reprogramming as the principal mechanism for initiation of pancreatic ductal adenocarcinoma. Cancer Cell 2012, 22:737-750.
61. Kraft P., Yen Y.C., Stram D.O., et al. Exploiting gene-environment interaction to detect genetic associations. Hum. Hered. 2007, 63:111-119.
62. Lamouille S., Xu J., Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 2014, 15:178-196.
63. Lee H.Y., Ahn J.B., Rha S.Y., et al. High KLF4 level in normal tissue predicts poor survival in colorectal cancer patients. World J. Surg. Oncol. 2014, 12:232.
64. Leis O., Eguiara A., Lopez-Arribillaga E., et al. Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene 2012, 31:1354-1365.
65. Li X.L., Eishi Y., Bai Y.Q., et al. Expression of the SRY-related HMG box protein SOX2 in human gastric carcinoma. Int. J. Oncol. 2004, 24:257-263.
66. Li Q., Gao Y., Jia Z., et al. Dysregulated Kruppel-like factor 4 and vitamin D receptor signaling contribute to progression of hepatocellular carcinoma. Gastroenterology 2012, 143(799-810):e1-e2.
67. Li Y., Lv Z., He G., et al. The SOX17/miR-371-5p/SOX2 axis inhibits EMT, stem cell properties and metastasis in colorectal cancer. Oncotarget 2015, 6:9099-9112.
68. Lin F., Lin P., Zhao D., et al. Sox2 targets cyclinE, p27 and survivin to regulate androgen-independent human prostate cancer cell proliferation and apoptosis. Cell Prolif. 2012, 45:207-216.
69. Lin Z.S., Chu H.C., Yen Y.C., et al. Kruppel-like factor 4, a tumor suppressor in hepatocellular carcinoma cells reverts epithelial mesenchymal transition by suppressing slug expression. PLoS One 2012, 7.
70. Lin H., Sun L.H., Han W., et al. Knockdown of OCT4 suppresses the growth and invasion of pancreatic cancer cells through inhibition of the AKT pathway. Mol. Med. Rep. 2014, 10:1335-1342.
71. Lonardo E., Hermann P.C., Mueller M.T., et al. Nodal/activin signaling drives self-renewal and tumorigenicity of pancreatic cancer stem cells and provides a target for combined drug therapy. Cell Stem Cell 2011, 9:433-446.
72. Long K.B., Hornick J.L. SOX2 is highly expressed in squamous cell carcinomas of the gastrointestinal tract. Hum. Pathol. 2009, 40:1768-1773.
73. Lundberg I.V., Lofgren Burstrom A., Edin S., et al. SOX2 expression is regulated by BRAF and contributes to poor patient prognosis in colorectal cancer. PLoS One 2014, 9.
74. Ma M.Q., Zhang H.D., Tang P., et al. Association of Kruppel-like factor 4 expression with the prognosis of esophageal squamous cell carcinoma patients. Int. J. Clin. Exp. Pathol. 2014, 7:6679-6685.
75. Magnuson T., Epstein C.J., Silver L.M., et al. Pluripotent embryonic stem cell lines can be derived from tw5/tw5 blastocysts. Nature 1982, 298:750-753.
76. Maherali N., Sridharan R., Xie W., et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007, 1:55-70.
77. Mansukhani A., Ambrosetti D., Holmes G., et al. Sox2 induction by FGF and FGFR2 activating mutations inhibits wnt signaling and osteoblast differentiation. J. Cell Biol. 2005, 168:1065-1076.
78. Marte B. Tumour heterogeneity. Nature 2013, 501:327.
79. Martinelli P., Canamero M., del Pozo N., et al. Gata6 is required for complete acinar differentiation and maintenance of the exocrine pancreas in adult mice. Gut 2013, 62:1481-1488.
80. Matsuoka J., Yashiro M., Sakurai K., et al. Role of the stemness factors sox2, oct3/4, and nanog in gastric carcinoma. J. Surg. Res. 2012, 174:130-135.
81. Meacham C.E., Morrison S.J. Tumour heterogeneity and cancer cell plasticity. Nature 2013, 501:328-337.
82. Merlos-Suarez A., Barriga F.M., Jung P., et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 2011, 8:511-524.
83. Morrison R., Schleicher S.M., Sun Y., et al. Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. J. Oncol. 2011, 2011:941876.
84. Mueller M.T., Hermann P.C., Witthauer J., et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 2009, 137:1102-1113.
85. Nichols J., Zevnik B., Anastassiadis K., et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95:379-391.
86. Ohnishi K., Semi K., Yamamoto T., et al. Premature termination of reprogramming in vivo leads to cancer development through altered epigenetic regulation. Cell 2014, 156:663-677.
87. Otsubo T., Akiyama Y., Yanagihara K., et al. SOX2 is frequently downregulated in gastric cancers and inhibits cell growth through cell-cycle arrest and apoptosis. Br. J. Cancer 2008, 98:824-831.
88. Papatsenko D., Darr H., Kulakovskiy I.V., et al. Single-cell analyses of ESCs reveal alternative pluripotent cell states and molecular mechanisms that control self-renewal. Stem Cell Rep. 2015, 5:207-220.
89. Patel N.V., Ghaleb A.M., Nandan M.O., et al. Expression of the tumor suppressor Kruppel-like factor 4 as a prognostic predictor for colon cancer. Cancer Epidemiol. Biomark. Prev. 2010, 19:2631-2638.
90. Polo J.M., Anderssen E., Walsh R.M., et al. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell 2012, 151:1617-1632.
91. Polvani S., Tarocchi M., Tempesti S., et al. COUP-TFII in pancreatic adenocarcinoma: clinical implication for patient survival and tumor progression. Int. J. Cancer 2014, 134:1648-1658.
92. Rais Y., Zviran A., Geula S., et al. Deterministic direct reprogramming of somatic cells to pluripotency. Nature 2013, 502:65-70.
93. Rathinam R., Berrier A., SK Alahari Role of Rho GTPases and their regulators in cancer progression. Front. Biosci. (Landmark Ed) 2011, 16:2561-2571.
94. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115.
95. Saigusa S., Tanaka K., Toiyama Y., et al. Correlation of CD133, OCT4, and SOX2 in rectal cancer and their association with distant recurrence after chemoradiotherapy. Ann. Surg. Oncol. 2009, 16:3488-3498.
96. Saiki Y., Ishimaru S., Mimori K., et al. Comprehensive analysis of the clinical significance of inducing pluripotent stemness-related gene expression in colorectal cancer cells. Ann. Surg. Oncol. 2009, 16:2638-2644.
97. Sainz B., Alcala S., Garcia E., et al. Microenvironmental hCAP-18/LL-37 promotes pancreatic ductal adenocarcinoma by activating its cancer stem cell compartment. Gut 2015, 64:1921-1935.
98. Sanada Y., Yoshida K., Ohara M., et al. Histopathologic evaluation of stepwise progression of pancreatic carcinoma with immunohistochemical analysis of gastric epithelial transcription factor SOX2: comparison of expression patterns between invasive components and cancerous or nonneoplastic intraductal components. Pancreas 2006, 32:164-170.
99. Sarkar A., Hochedlinger K. The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell 2013, 12:15-30.
100. Secombe J., Pierce S.B., Eisenman R.N. Myc: a weapon of mass destruction. Cell 2004, 117:153-156.
101. Shachaf C.M., Kopelman A.M., Arvanitis C., et al. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature 2004, 431:1112-1117.
102. Shan Z.Z., Yan X.B., Yan L.L., et al. Overexpression of Tbx3 is correlated with epithelial-mesenchymal transition phenotype and predicts poor prognosis of colorectal cancer. Am. J. Cancer Res. 2015, 5:344-353.
103. Shukrun R., Pode-Shakked N., Pleniceanu O., et al. Wilms' tumor blastemal stem cells dedifferentiate to propagate the tumor bulk. Stem Cell Rep. 2014, 3:24-33.
104. Smith D.R., Goh H.S. Overexpression of the c-myc proto-oncogene in colorectal carcinoma is associated with a reduced mortality that is abrogated by point mutation of the p53 tumor suppressor gene. Clin. Cancer Res. 1996, 2:1049-1053.
105. Sterneckert J., Hoing S., Scholer H.R. Concise review: Oct4 and more: the reprogramming expressway. Stem Cells 2012, 30:15-21.
106. Sun C., Sun L., Li Y., et al. Sox2 expression predicts poor survival of hepatocellular carcinoma patients and it promotes liver cancer cell invasion by activating slug. Med. Oncol. 2013, 30:503.
107. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
108. Takahashi K., Okita K., Nakagawa M., et al. Induction of pluripotent stem cells from fibroblast cultures. Nat. Protoc. 2007, 2:3081-3089.
109. Tang B., Raviv A., Esposito D., et al. A flexible reporter system for direct observation and isolation of cancer stem cells. Stem Cell Rep. 2015, 4:155-169.
110. Todaro M., Alea M.P., Di Stefano A.B., et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007, 1:389-402.
111. Unternaehrer J.J., Zhao R., Kim K., et al. The epithelial-mesenchymal transition factor SNAIL paradoxically enhances reprogramming. Stem Cell Rep. 2014, 3:691-698.
112. Vermeulen L., Todaro M., de Sousa Mello F., et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13427-13432.
113. Waghray A., Saiz N., Jayaprakash A.D., et al. Tbx3 controls Dppa3 levels and exit from pluripotency toward mesoderm. Stem Cell Rep. 2015, 5:97-110.
114. Wang Q., He W., Lu C., et al. Oct3/4 and Sox2 are significantly associated with an unfavorable clinical outcome in human esophageal squamous cell carcinoma. Anticancer Res. 2009, 29:1233-1241.
115. Wang X.Q., Ongkeko W.M., Chen L., et al. Octamer 4 (Oct4) mediates chemotherapeutic drug resistance in liver cancer cells through a potential Oct4-AKT-ATP-binding cassette G2 pathway. Hepatology 2010, 52:528-539.
116. Wei D., Gong W., Kanai M., et al. Drastic down-regulation of Kruppel-like factor 4 expression is critical in human gastric cancer development and progression. Cancer Res. 2005, 65:2746-2754.
117. Wei D., Kanai M., Huang S., et al. Emerging role of KLF4 in human gastrointestinal cancer. Carcinogenesis 2006, 27:23-31.
118. Wei D., Kanai M., Jia Z., et al. Kruppel-like factor 4 induces p27Kip1 expression in and suppresses the growth and metastasis of human pancreatic cancer cells. Cancer Res. 2008, 68:4631-4639.
119. Wei D., Wang L., Kanai M., et al. KLF4alpha up-regulation promotes cell cycle progression and reduces survival time of patients with pancreatic cancer. Gastroenterology 2010, 139:2135-2145.
120. Weidgang C.E., Russell R., Tata P.R., et al. TBX3 directs cell-fate decision toward mesendoderm. Stem Cell Rep. 2013, 1:248-265.
121. Wen J., Park J.Y., Park K.H., et al. Oct4 and nanog expression is associated with early stages of pancreatic carcinogenesis. Pancreas 2010, 39:622-626.
122. Wen K., Fu Z., Wu X., et al. Oct-4 is required for an antiapoptotic behavior of chemoresistant colorectal cancer cells enriched for cancer stem cells: effects associated with STAT3/survivin. Cancer Lett. 2013, 333:56-65.
123. Xu J., Lu B., Xu F., et al. Dynamic down-regulation of Kruppel-like factor 4 in colorectal adenoma-carcinoma sequence. J. Cancer Res. Clin. Oncol. 2008, 134:891-898.
124. Xu X.L., Ling Z.Q., Chen S.Z., et al. The impact of E-cadherin expression on the prognosis of esophageal cancer: a meta-analysis. Dis. Esophagus 2014, 27:79-86.
125. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
126. Yang Y., Goldstein B.G., Chao H.H., et al. KLF4 and KLF5 regulate proliferation, apoptosis and invasion in esophageal cancer cells. Cancer Biol. Ther. 2005, 4:1216-1221.
127. Yang A.D., Fan F., Camp E.R., et al. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin. Cancer Res. 2006, 12:4147-4153.
128. Yin X., Li Y.W., Zhang B.H., et al. Coexpression of stemness factors Oct4 and nanog predict liver resection. Ann. Surg. Oncol. 2012, 19:2877-2887.
129. Yin X., Li Y.W., Jin J.J., et al. The clinical and prognostic implications of pluripotent stem cell gene expression in hepatocellular carcinoma. Oncol. Lett. 2013, 5:1155-1162.
130. Yin X., Zhang B.H., Zheng S.S., et al. Coexpression of gene Oct4 and nanog initiates stem cell characteristics in hepatocellular carcinoma and promotes epithelial-mesenchymal transition through activation of Stat3/snail signaling. J. Hematol. Oncol. 2015, 8:23.
131. Zambon C.F., Basso D., Navaglia F., et al. Pro- and anti-inflammatory cytokines gene polymorphisms and helicobacter pylori infection: interactions influence outcome. Cytokine 2005, 29:141-152.
132. Zammarchi F., Morelli M., Menicagli M., et al. KLF4 is a novel candidate tumor suppressor gene in pancreatic ductal carcinoma. Am. J. Pathol. 2011, 178:361-372.
133. Zhang N., Zhang J., Wang Z.W., et al. Altered expression of Kruppel-like factor 4 and beta-catenin in human gastric cancer. Oncol. Lett. 2012, 3:1017-1022.
134. Zhang N., Zhang J., Shuai L., et al. Kruppel-like factor 4 negatively regulates beta-catenin expression and inhibits the proliferation, invasion and metastasis of gastric cancer. Int. J. Oncol. 2012, 40:2038-2048.
135. Zheng X., Carstens J.L., Kim J., et al. Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature 2015, 527:525-530.
136. Zhou X., Huang G.R., Hu P. Over-expression of Oct4 in human esophageal squamous cell carcinoma. Mol. Cell 2011, 32:39-45.
137. Zhu P., Wang Y., He L., et al. ZIC2-dependent OCT4 activation drives self-renewal of human liver cancer stem cells. J. Clin. Invest. 2015, 125:3795-3808.