Direct regulation of FOXK1 by C-jun promotes proliferation, invasion and metastasis in gastric cancer cells

Cell Death and Disease

Volumn 7, Issue 11, 2016, Pages

  Peng, Ying ^a   Zhang, Pei ^a   Huang, Xiaoting ^a   Yan, Qingqing ^b,c   Wu, Meiyan ^a   Xie, Ruyi ^a   Wu, Yao ^a   Zhang, Mengnan ^a   Nan, Qingzhen ^a   Zhao, Jinjun ^a   Li, Aimin ^a   Xiong, Jing ^a   Ren, Yuexin ^a   Bai, Yang ^a   Chen, Ye ^a   Liu, Side ^a   Wang, Jide ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b GUANGZHOU MEDICAL UNIVERSITY   (China)

^c Central Hospital of Nansha   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOGLIN; FORKHEAD TRANSCRIPTION FACTOR; FOXK1 PROTEIN; GELATINASE A; GELATINASE B; KI 67 ANTIGEN; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN C JUN; PROTEIN KINASE B; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; FOXK1 PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; METASTASIS; METASTASIS POTENTIAL; MOUSE; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; STOMACH CANCER; STOMACH CARCINOGENESIS; TRANSCRIPTION INITIATION; TUMOR GROWTH; TUMOR INVASION; CARCINOGENESIS; CELL MOTION; DISEASE COURSE; DRUG EFFECTS; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROGNOSIS; STOMACH TUMOR; TUMOR CELL LINE;

BASE SEQUENCE; CARCINOGENESIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PHENOTYPE; PROGNOSIS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-JUN; STOMACH NEOPLASMS; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 85009855926     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2016.225     Document Type: Article

References (43)

1. Weigel D, Jäckle H. The fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell 1990; 63: 455–456.
2. Overdier DG, Porcella A, Costa RH. The DNA-binding specificity of the hepatocyte nuclear factor 3/forkhead domain is influenced by amino-acid residues adjacent to the recognition helix. Mol Cell Biol 1994; 14: 2755–2766.
3. Bassel-Duby R, Hernandez MD, Yang Q, Rochelle JM, Seldin MF, Williams RS. Myocyte nuclear factor, a novel winged-helix transcription factor under both developmental and neural regulation in striated myocytes. Mol Cell Biol 1994; 14: 4596–4605.
4. Wotton KR, Mazet F, Shimeld SM. Expression of FoxC, FoxF, FoxL1, and FoxQ1 genes in the dogfish Scyliorhinus canicula defines ancient and derived roles for Fox genes in vertebrate development. Dev Dyn 2008; 237: 1590–1603.
5. Leung TW, Lin SS, Tsang AC, Tong CS, Ching JC, Leung WY et al. Over-expression of FoxM1 stimulates cyclin B1 expression. FEBS Lett 2001; 507: 59–66.
6. Sturgill TW, Stoddard PB, Cohn SM, Mayo MW. The promoter for intestinal cell kinase is head-to-head with F-Box 9 and contains functional sites for TCF7L2 and FOXA factors. Mol Cancer 2010; 9: 104.
7. Sharma SK, Leinemann U, Ratke R, Oetjen E, Blume R, Dickel C et al. Characterization of a novel Foxa (hepatocyte nuclear factor-3) site in the glucagon promoter that is conserved between rodents and humans. Biochem J 2005; 389(Part 3): 831–841.
8. Fu W, Ma Q, Chen L, Li P, Zhang M, Ramamoorthy S et al. MDM2 acts downstream of p53 as an E3 ligase to promote FOXO ubiquitination and degradation. J Biol Chem 2009; 284: 13987–14000.
9. Jonsson H, Peng SL. Forkhead transcription factors in immunology. Cell Mol Life Sci 2005; 62: 397–409.
10. Wolf I, Bose S, Williamson EA, Miller CW, Karlan BY, Koeffler HP. FOXA1: growth inhibitor and a favorable prognostic factor in human breast cancer. Int J Cancer 2007; 120: 1013–1022.
11. Freyaldenhoven BS, Fried C, Wielckens K. FOXD4a and FOXD4b, two new winged helix transcription factors, are expressed in human leukemia cell lines. Gene 2002; 294: 131–140.
12. Teh MT, Wong ST, Neill GW, Ghali LR, Philpott MP, Quinn AG. FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res 2002; 62: 4773–4780.
13. Xia L, Huang W, Tian D, Zhang L, Qi X, Chen Z et al. Forkhead box Q1 promotes hepatocellular carcinoma metastasis by transactivating ZEB2 and VersicanV1 expression. Hepatology 2014; 59: 958–973.
14. Garry DJ, Meeson A, Elterman J, Zhao Y, Yang P, Bassel-Duby R et al. Myogenic stem cell function is impaired in mice lacking the forkhead/winged helix protein MNF. Proc Natl Acad Sci USA 2000; 97: 5416–5421.
15. Yang Q, Bassel-Duby R, Williams RS. Transient expression of a winged-helix protein MNF-beta, during myogenesis. Mol Cell Biol 1997; 17: 5236–5243.
16. Shi X, Seldin DC, Garry DJ. Foxk1 recruits the Sds3 complex and represses gene expression in myogenic progenitors. Biochem J 2012; 446: 349–357.
17. Yang Q, Bassel-Duby R, Williams RS. Transient expression of a winged-helix protein, MNF-beta, during myogenesis. Mol Cell Biol 1997; 17: 5236–5243.
18. Hawke TJ, Jiang N, Garry DJ. Absence of p21CIP rescues myogenic progenitor cell proliferative and regenerative capacity in Foxk1 null mice. J Biol Chem 2003; 278: 4015–4020.
19. Zhang Y, Shen WL, Shi ML, Zhang LZ, Zhang Z, Li P et al. Involvement of aberrant miR-139/ Jun feedback loop in human gastric cancer. Biochim Biophys Acta 2015; 1853: 481–488.
20. Meyer-ter-Vehn T, Covacci A, Kist M, Pahl HL. Helicobacter pylori activates mitogen-activated protein kinase cascades and induces expression of the proto-oncogenes c-fos and c-Jun. J Biol Chem 2000; 275: 16064–16072.
21. Katiyar S, Jiao X, Wagner E, Lisanti MP, Pestell RG. Somatic excision demonstrates that c-Jun induces cellular migration and invasion through induction of stem cell factor. Mol Cell Biol 2007; 27: 1356–1369.
22. Jiao X, Katiyar S, Willmarth NE, Liu M, Ma X, Flomenberg N et al. induces mammary epithelial cellular invasion and breast cancer stem cell expansion. J Biol Chem 2010; 285: 8218–8226.
23. Virolle T, Djabari Z, Ortonne JP, Aberdam D. DNA conformation driven by AP-1 triggers cell-specific expression via a strong epithelial enhancer. EMBO Rep 2000; 1: 328–333.
24. Zutter MM, Painter AD, Yang X. The megakaryocyte/platelet-specific enhancer of the alpha2beta1 integrin gene: two tandem AP1 sites and the mitogen-activated protein kinase signaling cascade. Blood 1999; 93: 1600–1611.
25. Wang J, Yang Y, Xia HH, Gu Q, Lin MC, Jiang B et al. Suppression of FHL2 expression induces cell differentiation and inhibits gastrointestinal carcinogenesis. Gastroenterology 2007; 132: 1066–1076.
26. Zhang W, Jiang B, Guo Z, Sardet C, Zou B, Lam CS et al. protein 2 promotes invasive potential and epithelial–mesenchymal transition in colon cancer. Carcinogenesis 2010; 31: 1220–1229.
27. Yan Q, Zhang W, Wu Y, Wu M, Zhang M, Shi X et al. KLF8 promotes tumorigenesis, invasion and metastasis of colorectal cancer cells by transcriptional activation of FHL2. Oncotarget 2015; 6: 25402–25417.
28. Shibata J, Murakami K, Aoyagi Y, Oie S, Hashimoto A, Suzuki K et al. The induction of apoptosis and inhibition of AP-1 activity by TAC-101 (4-[3,5-bis(trimethylsilyl) benzamido] benzoic acid) may result in life prolonging effect in animals bearing metastasizing cancer. Anticancer Res 2000; 20: 3583–3590.
29. Wang W, Li X, Lee M, Jun S, Aziz KE, Feng L et al. FOXKs promote Wnt/β-catenin signaling by translocating DVL into the nucleus. Dev Cell. 2015; 32: 707–718.
30. Han G, Lu SL, Li AG, He W, Corless CL, Kulesz-Martin M et al. Distinct mechanisms of TGF-beta1-mediated epithelial-to-mesenchymal transition and metastasis during skin carcinogenesis. J Clin Invest 2005; 115: 1714–1723.
31. Tang YN, Ding WQ, Guo XJ, Yuan XW, Wang DM, Song JG. Epigenetic regulation of Smad2 and Smad3 by profilin-2 promotes lung cancer growth and metastasis. Nat Commun 2015; 6: 8230.
32. He J, Tegen SB, Krawitz AR, Martin GS, Luo K. The transforming activity of Ski and SnoN is dependent on their ability to repress the activity of Smad proteins. J Biol Chem 2003; 278: 30540–30547.
33. Zhou Z, Zhang L, Xie B, Wang X, Yang X, Ding N et al. FOXC2 promotes chemoresistance in nasopharyngeal carcinomas via induction of epithelial mesenchymal transition. Cancer Lett 2015; 363: 137–145.
34. Zhang H, Meng F, Liu G, Zhang B, Zhu J, Wu F et al. Forkhead transcription factor foxq1 promotes epithelial–mesenchymal transition and breast cancer metastasis. Cancer Res 2011; 71: 1292–1301.
35. Angel P, Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta 1991; 1072: 129–57.
36. Blonska M, Zhu Y, Chuang HH, You MJ, Kunkalla K, Vega F et al. Jun-regulated genes promote interaction of diffuse large B-cell lymphoma with the microenvironment. Blood 2015; 125: 981–991.
37. Zhao C, Qiao Y, Jonsson P, Wang J, Xu L, Rouhi P et al. Genome-wide profiling of AP-1-regulated transcription provides insights into the invasiveness of triple-negative breast cancer. Cancer Res 2014; 74: 3983–3994.
38. Zabini D, Crnkovic S, Xu H, Tscherner M, Ghanim B, Klepetko W et al. High-mobility group box-1 induces vascular remodelling processes via c-Jun activation. J Cell Mol Med 2015; 19: 1151–1161.
39. Bae JA, Yoon S, Park SY, Lee JH, Hwang JE, Kim H et al. An unconventional KITENIN/ ErbB4-mediated downstream signal of EGF upregulates c-Jun and the invasiveness of colorectal cancer cells. Clin Cancer Res 2014; 20: 4115–4128.
40. Eferl R, Ricci R, Kenner L, Zenz R, David JP, Rath M et al. Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell 2003; 112: 181–192.
41. Leaner VD, Kinoshita I, Birrer MJ. AP-1 complexes containing cJun and JunB cause cellular transformation of Rat1a fibroblasts and share transcriptional targets. Oncogene 2003; 22: 5619–5629.
42. Smith LM, Wise SC, Hendricks DT, Sabichi AL, Bos T, Reddy P et al. c-Jun overexpression in MCF-7 breast cancer cells produces a tumorigenic, invasive and hormone resistant phenotype. Oncogene 1999; 18: 6063–6070.
43. Zhang W, Wang J, Zou B, Sardet C, Li J, Lam CS et al. Four and a half LIM protein 2 (FHL2) negatively regulates the transcription of E-cadherin through interaction with Snail1. Eur J Cancer 2011; 47: 121–130.