The basic helix-loop-helix transcription factor DEC2 inhibits TGF-β-induced tumor progression in human pancreatic cancer BxPC-3 cells

International Journal of Molecular Medicine

Volumn 30, Issue 3, 2012, Pages 495-501

  Sato, Fuyuki ^a   Kawamura, Haruka ^a   Wu, Yunyan ^a   Sato, Hiroyasu ^a   Jin, Daiki ^a   Bhawal, Ujjal Kumar ^b   Kawamoto, Takeshi ^c   Fujimoto, Katsumi ^c   Noshiro, Mitsuhide ^c   Seino, Hiroko ^a   Morohashi, Satomo ^a   Kato, Yukio ^c   Kijima, Hiroshi ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c HIROSHIMA UNIVERSITY   (Japan)

Author keywords

BxPC 3 cells; Differentiated embryo chondrocyte 2; Immunohistochemistry; Slug; Transforming growth factor

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR DEC2; CLAUDIN 1; CLAUDIN 4; NERVE CELL ADHESION MOLECULE; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ADULT; AGED; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER INVASION; CELL MIGRATION; CELL STRAIN BXPC 3; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; PANCREATIC NEOPLASMS; RNA INTERFERENCE; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84865170080     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2012.1037     Document Type: Article

References (37)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C and Thun MJ: Cancer statistics, 2006. CA Cancer J Clin 56: 106-130, 2006.
2. Yeo TP, Hruban RH, Leach SD, Wilentz RE, Sohn TA, Kern SE, Iacobuzio-Donahue CA, Maitra A, Goggins M, Canto MI, et al: Pancreatic cancer. Curr Probl Cancer Rev 26: 176-275, 2002.
3. Zavadil J and Böttinger EP: TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24: 5764-5774, 2005.
4. 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.
5. Kleeff J, Friess H, Simon P, Susmallian S, Büchler P, Zimmermann A, Büchler MW and Korc M: Overexpression of Smad2 and colocalization with TGF-beta1 in human pancreatic cancer. Dig Dis Sci 44: 1793-1802, 1999. (Pubitemid 29446842)
6. Friess H, Yamanaka Y, Büchler M, Ebert M, Beger HG, Gold LI and Korc M: Enhanced expression of transforming growth factor beta isoforms in pancreatic cancer correlates with decreased survival. Gastroenterology 105: 1846-1856, 1993. (Pubitemid 24002804)
7. Huber MA, Kraut N and Beug H: Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 17: 548-558, 2005. (Pubitemid 41267170)
8. Thiery JP and Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142, 2006. (Pubitemid 43278296)
9. Medici D, Hay ED and Olsen BR: Snail and Slug promote epithelial-mesenchymal transition through beta-catenin-T-cell factor-4-dependent expression of transforming growth factor-beta 3. Mol Biol Cell 19: 4875-4887, 2008.
10. Hahn SA, Schutte M, Hoque AT, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH and Kern SE: DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271: 350-353, 1996.
11. Bartsch D, Hahn SA, Danichevski KD, Ramaswamy A, Bastian D, Galehdari H, Barth P, Schmiegel W, Simon B and Rothmund M: Mutations of the DPC4/Smad4 gene in neuroendocrine pancreatic tumors. Oncogene 18: 2367-2371, 1999. (Pubitemid 29192714)
12. Miyazawa K, Shinozaki M, Hara T, Furuya T and Miyazono K: Two major Smad pathways in TGF-beta superfamily signalling. Genes Cells 7: 1191-1204, 2002. (Pubitemid 36024597)
13. Massagué J: How cells read TGF-beta signals. Nat Rev Mol Cell Biol 1: 169-178, 2000.
14. Zawel L, Dai JL, Buckhaults P, Zhou S, Kinzler KW, Vogelstein B and Kern SE: Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell 1: 611-617, 1998. (Pubitemid 128374697)
15. Sato F, Kawamoto T, Fujimoto K, Noshiro M, Honda KK, Honma S, Honma K and Kato Y: Functional analysis of the basic helix-loop-helix transcription factor DEC1 in circadian regulation. Interaction with BMAL1. Eur J Biochem 271: 4409-4419, 2004. (Pubitemid 39576558)
16. Sato F, Bhawal UK, Kawamoto T, Fujimoto K, Imaizumi T, Imanaka T, Kondo J, Koyanagi S, Noshiro M, Yoshida H, et al: Basic-helix-loop-helix (bHLH) transcription factor DEC2 negatively regulates vascular endothelial growth factor expression. Genes Cells 13: 131-144, 2008. (Pubitemid 351188984)
17. Wu Y, Sato F, Bhawal UK, Kawamoto T, Fujimoto K, Noshiro M, Morohashi S, Kato Y and Kijima H: 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.
18. Wu Y, Sato F, Bhawal UK, Kawamoto T, Fujimoto K, Noshiro M, Seino H, Morohashi S, Kato Y and Kijima H: BHLH transcription factor DEC2 regulates pro-apoptotic factor Bim in human oral cancer HSC-3 cells. Biomed Res 33: 75-82, 2012.
19. Imaizumi T, Sato F, Tanaka H, Matsumiya T, Yoshida H, Yashiro-Aizawa T, Tsuruga K, Hayakari R, Kijima H and Satoh K: Basic-helix-loop-helix transcription factor DEC2 constitutes negative feedback loop in IFN-β-mediated inflammatory responses in human mesangial cells. Immunol Lett 136: 37-43, 2011.
20. Liu Y, Sato F, Kawamoto T, Fujimoto K, Morohashi S, Akasaka H, Kondo J, Wu Y, Noshiro M, Kato Y and Kijima H: Anti-apoptotic effect of the basic helix-loop-helix (bHLH) transcription factor DEC2 in human breast cancer cells. Genes Cells 15: 315-325, 2010.
21. Bhawal UK, Sato F, Arakawa Y, Fujimoto K, Kawamoto T, Tanimoto K, Ito Y, Sasahira T, Sakurai T, Kobayashi M, et al: Basic helix-loop-helix transcription factor DEC1 negatively regulates cyclin D1. J Pathol 224: 420-429, 2011.
22. Sato F, Wu Y, Bhawal UK, Liu Y, Imaizumi T, Morohashi S, Kato Y and Kijima H: 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.
23. Choi SM, Cho HJ, Cho H, Kim KH, Kim JB and Park H: Stra13/DEC1 and DEC2 inhibit sterol regulatory element binding protein-1c in a hypoxia-inducible factor-dependent mechanism. Nucleic Acids Res 36: 6372-6385, 2008.
24. Nishioka R, Itoh S, Gui T, Gai Z, Oikawa K, Kawai M, Tani M, Yamaue H and Muragaki Y: 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, 2010.
25. Shah PP and Kakar SS: Pituitary tumor transforming gene induces epithelial to mesenchymal transition by regulation of twist, snail, slug, and E-cadherin. Cancer Lett 311: 66-76, 2011.
26. Takano S, Kanai F, Jazag A, Ijichi H, Yao J, Ogawa H, Enomoto N, Omata M and Nakao A: Smad4 is essential for down-regulation of E-cadherin induced by TGF-beta in pancreatic cancer cell line PANC-1. J Biochem 141: 345-351, 2007. (Pubitemid 46770387)
27. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH and Moustakas A: Transforming growth factor-beta employs HMGA2 to elicit epithelial- mesenchymal transition. J Cell Biol 174: 175-183, 2006. (Pubitemid 44079853)
28. Sánchez-Martín M, Rodríguez-García A, Pérez-Losada J, Sagrera A, Read AP and Sánchez-García I: SLUG (SNAI2) deletions in patients with Waardenburg disease. Hum Mol Genet 11: 3231-3236, 2002.
29. Grotegut S, von Schweinitz D, Christofori G and Lehembre F: Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J 25: 3534-3545, 2006. (Pubitemid 44264864)
30. Zhang K, Chen D, Jiao X, Zhang S, Liu X, Cao J, Wu L and Wang D: Slug enhances invasion ability of pancreatic cancer cells through upregulation of matrix metalloproteinase-9 and actin cytoskeleton remodeling. Lab Invest 91: 426-438, 2011.
31. Tang P, Yu Z, Zhang K, Wang Y, Ma Z, Zhang S, Chen D and Zhou Y: Slug down-regulation by RNA interference inhibits invasion growth in human esophageal squamous cell carcinoma. BMC Gastroenterol 11: 60, 2011.
32. Emadi Baygi M, Soheili ZS, Essmann F, Deezagi A, Engers R, Goering W and Schulz WA: Slug/SNAI2 regulates cell proliferation and invasiveness of metastatic prostate cancer cell lines. Tumour Biol 31: 297-307, 2010.
33. Kurrey NK, Amit K and Bapat SA: Snail and Slug are major determinants of ovarian cancer invasiveness at the transcription level. Gynecol Oncol 97: 155-165, 2005. (Pubitemid 40403688)
34. Kawamoto T, Noshiro M, Sato F, Maemura K, Takeda N, Nagai R, Iwata T, Fujimoto K, Furukawa M, Miyazaki K, et al: A novel autofeedback loop of Dec1 transcription involved in circadian rhythm regulation. Biochem Biophys Res Commun 2: 117-124, 2004. (Pubitemid 37524033)
35. Chakrabarti J, Turley H, Campo L, Han C, Harris AL, Gatter KC and Fox SB: 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. (Pubitemid 39273790)
36. Giatromanolaki A, Koukourakis MI, Sivridis E, Turley H, Wykoff CC, Gatter KC and Harris 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. (Pubitemid 36748031)
37. Li Y, Zhang H, Xie M, Hu M, Ge S, Yang D, Wan Y and Yan B: 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. (Pubitemid 35216815)