The BHLH transcription factor DEC1 plays an important role in the epithelial-mesenchymal transition of pancreatic cancer

International Journal of Oncology

Volumn 41, Issue 4, 2012, Pages 1337-1346

  Wu, Yunyan ^a,b   Sato, Fuyuki ^a   Yamada, Toshiyuki ^a   Bhawal, Ujjal Kumar ^c   Kawamoto, Takeshi ^d   Fujimoto, Katsumi ^d   Noshiro, Mitsuhide ^d   Seino, Hiroko ^a   Morohashi, Satoko ^a   Hakamada, Kenichi ^a   Abiko, Yoshimitsu ^c   Kato, Yukio ^d   Kijima, Hiroshi ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b CHINA MEDICAL UNIVERSITY   (China)

^c NIHON UNIVERSITY   (Japan)

^d HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Differentiated embryonic chondrocyte gene 1; Epithelial mesenchymal transition; Human pancreatic cancer; Transforming growth factor

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR DEC1; CLAUDIN 4; NERVE CELL ADHESION MOLECULE; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER CELL; CANCER TISSUE; CELL INVASION; CELL MEMBRANE; CELL MIGRATION; CELL NUCLEUS; CELL STRUCTURE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; PANCREAS; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

APOPTOSIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CLAUDIN-4; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; PANCREATIC NEOPLASMS; RNA, SMALL INTERFERING; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEINS;

EID: 84866483661     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2012.1559     Document Type: Article

References (42)

1. Thiery JP and Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142, 2006.
2. Zavadil J and Böttinger EP: TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24: 5764-5774, 2005.
3. Miettinen PJ, Ebner R, Lopez AR and Derynck R: TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 127: 2021-2036, 1994.
4. Moustakas A and Heldin CH: Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 98: 1512-1520, 2007.
5. Miyazawa K, Shinozaki M, Hara T, et al: Two major Smad pathways in TGF-beta superfamily signalling. Genes Cells 7: 1191-1204, 2002.
6. Giehl K, Seidel B, Gierschik P, et al: TGFbeta1 represses proliferation of pancreatic carcinoma cells which correlates with Smad4-independent inhibition of ERK activation. Oncogene 19: 4531-4541, 2000.
7. Hahn SA, Schutte M, Hoque AT, et al: DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271: 350-353, 1996.
8. Bartsch D, Hahn SA, Danichevski KD, et al: Mutations of the DPC4/Smad4 gene in neuroendocrine pancreatic tumors. Oncogene 18: 2367-2371, 1999.
9. Massagué J: How cells read TGF-beta signals. Nat Rev Mol Cell Biol 1: 169-178, 2000.
10. Zawel L, Dai JL, Buckhaults P, et al: Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell 1: 611-617, 1998.
11. Ohashi S, Natsuizaka M, Naganuma S, et al: A NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors. Cancer Res 71: 6836-6847, 2011.
12. Dave N, Guaita-Esteruelas S, Gutarra S, et al: Functional cooperation between Snail1 and twist in the regulation of ZEB1 expression during epithelial to mesenchymal transition. J Biol Chem 286: 12024-12032, 2011.
13. Gregory PA, Bracken CP, Smith E, et al: An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell 22: 1686-1698, 2011.
14. Hong J, Zhou J, Fu J, et al: Phosphorylation of serine 68 of Twist1 by MAPKs stabilizes Twist1 protein and promotes breast cancer cell invasiveness. Cancer Res 71: 3980-3990, 2011.
15. Ikenouchi J, Matsuda M, Furuse M and Tsukita S: Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci 116: 1959-1967, 2003.
16. Ohkubo T and Ozawa M: The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J Cell Sci 117: 1675-1685, 2004.
17. Zavadil J, Cermak L, Soto-Nieves N, et al: Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J 23: 1155-1165, 2004.
18. Wu Y, Sato F, Bhawal UK, et al: Basic helix-loop-helix transcription factors DEC1 and DEC2 regulate the paclitaxel-induced apoptotic pathway of MCF-7 human breast cancer cells. Int J Mol Med 27: 491-495, 2011.
19. Liu Y, Sato F, Kawamoto T, et al: Anti-apoptotic effect of the basic helix-loop-helix (bHLH) transcription factor DEC2 in human breast cancer cells. Genes Cells 15: 315-325, 2010.
20. Bhawal UK, Sato F, Arakawa Y, et al: Basic helix-loop-helix transcription factor DEC1 negatively regulates cyclin D1. J Pathol 224: 420-429, 2011.
21. Li Y, Xie M, Yang J, et al: The expression of antiapoptotic protein survivin is transcriptionally upregulated by DEC1 primarily through multiple sp1 binding sites in the proximal promoter. Oncogene 25: 3296-3306, 2006.
22. Turley H, Wykoff CC, Troup S, et al: The hypoxia-regulated transcription factor DEC1 (Stra13, SHARP-2) and its expression in human tissues and tumours. J Pathol 203: 808-813, 2004.
23. Chakrabarti J, Turley H, Campo L, et al: The transcription factor DEC1 (stra13, SHARP2) is associated with the hypoxic response and high tumour grade in human breast cancers. Br J Cancer 91: 954-958, 2004.
24. Giatromanolaki A, Koukourakis MI, Sivridis E, et al: DEC1 (STRA13) protein expression relates to hypoxia- inducible factor 1-alpha and carbonic anhydrase-9 overexpression in non-small cell lung cancer. J Pathol 200: 222-228, 2003.
25. Kondo J, Sato F, Kusumi T, et al: Claudin-1 expression is induced by tumor necrosis factor-α in human pancreatic cancer cells. Int J Mol Med 22: 645-649, 2008.
26. Suzuki T, Sato F, Kondo J, et al: Period is involved in the proliferation of human pancreatic MIA-PaCa2 cancer cells by TNF-alpha. Biomed Res 29: 99-103, 2008.
27. Sato F, Wu Y, Bhawal UK, Liu Y, et al: PERIOD1 (PER1) has anti-apoptotic effects, and PER3 has pro-apoptotic effects during cisplatin (CDDP) treatment in human gingival cancer CA9-22 cells. Eur J Cancer 47: 1747-1758, 2011.
28. Li Y, Zhang H, Xie M, et al: Abundant expression of Dec1/stra13/sharp2 in colon carcinoma: its antagonizing role in serum deprivation-induced apoptosis and selective inhibition of procaspase activation. Biochem J 367: 413-422, 2002.
29. Wang W, Reiser-Erkan C, Michalski CW, et al: Hypoxia inducible BHLHB2 is a novel and independent prognostic marker in pancreatic ductal adenocarcinoma. Biochem Biophys Res Commun 401: 422-428, 2010.
30. Kon N, Hirota T, Kawamoto T, et al: Activation of TGF-beta/activin signalling resets the circadian clock through rapid induction of Dec1 transcripts. Nat Cell Biol 10: 1463-1469, 2008.
31. Nicolás FJ and Hill CS: Attenuation of the TGF-beta-Smad signaling pathway in pancreatic tumor cells confers resistance to TGF-beta-induced growth arrest. Oncogene 22: 3698-3711, 2003.
32. Sato F, Kawamoto T, Fujimoto K, et al: Functional analysis of the basic helix-loop-helix transcription factor DEC1 in circadian regulation. Interaction with BMAL1. Eur J Biochem 271: 4409-4419, 2004.
33. Kawamoto T, Noshiro M, Sato F, et al: A novel autofeedback loop of Dec1 transcription involved in circadian rhythm regulation. Biochem Biophys Res Commun 313: 117-124, 2004.
34. Bloom BB, Humphries DE, Kuang PP, et al: Structure and expression of the promoter for the R4/ALK5 human type I transforming growth factor-beta receptor: regulation by TGF-beta. Biochim Biophys Acta 1312: 243-248, 1996.
35. Mulder KM: Role of ras and Mapks in TGF-beta signaling. Cytokine Growth Factor Rev 11: 23-35, 2000.
36. Michl P, Barth C, Buchholz M, et al: Claudin-4 expression decreases invasiveness and metastatic potential of pancreatic cancer. Cancer Res 63: 6265-6271, 2003.
37. Turksen K and Troy TC: Junctions gone bad: Claudins and loss of the barrier in cancer. Biochim Biophys Acta 1816: 73-79, 2011.
38. Berx G and Van Roy F: The E-cadherin/catenin complex: an important gatekeeper in breast cancer tumorigenesis and malignant progression. Breast Cancer Res 3: 289-293, 2001.
39. Wells A, Yates C and Shepard CR: E-cadherin as an indicator of mesenchymal to epithelial reverting transitions during the metastatic seeding of disseminated carcinomas. Clin Exp Metastasis 25: 621-628, 2008.
40. Martínez-Estrada OM, Cullerés A, Soriano FX, et al: The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem J 394: 449-457, 2006.
41. Batlle E, Sancho E, Francí C, et al: The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2: 84-89, 2002.
42. Reka AK, Kurapati H, Narala VR, et al: Peroxisome proliferator-activated receptor-gamma activation inhibits tumor metastasis by antagonizing Smad3-mediated epithelial-mesenchymal transition. Mol Cancer Ther 9: 3221-3232, 2010.