Transcriptional up-regulation of Sox9 by NF-κB in endometrial carcinoma cells, modulating cell proliferation through alteration in the p14ARF/p53/p21WAF1 pathway

American Journal of Pathology

Volumn 181, Issue 2, 2012, Pages 684-692

  Saegusa, Makoto ^a   Hashimura, Miki ^a   Suzuki, Erina ^a   Yoshida, Tsutomu ^a   Kuwata, Takeshi ^b  

^a KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NATIONAL CANCER CENTER HOSPITAL EAST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KI 67 ANTIGEN; P21 ACTIVATED KINASE; PROTEIN KINASE B; PROTEIN P53; TRANSCRIPTION FACTOR SOX9;

ARTICLE; CANCER CELL; CANCER GRADING; CELL GROWTH; CELL PROLIFERATION; ENDOMETRIUM; ENDOMETRIUM CARCINOMA; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; MENSTRUATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; TRANSCRIPTION REGULATION; UPREGULATION;

ADULT; AGED; AGED, 80 AND OVER; BASE SEQUENCE; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ENDOMETRIAL NEOPLASMS; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KINETICS; MIDDLE AGED; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-AKT; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P14ARF; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84864118494     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.05.008     Document Type: Article

References (47)

1. G.E. Schepers, R.D. Teasdale, P. Koopman Twenty pairs of Sox: extent, homology, and nomenclature of the mouse and human Sox transcription factor gene families Dev Cell 3 2002 167 170
2. V. Lefebvre, B. Dumitriu, A. Penzo-Mendez, Y. Han, B. Pallavi Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors Int J Biochem Cell Biol 39 2007 2195 2214
3. P. Dy, A. Penzo-Mendez, H. Wang, C.E. Pedraza, W.B. Macklin, V. Lefebvre The three SoxC proteins- Sox4, Sox11 and Sox12- exhibit overlapping expression patterns and molecular properties Nucleic Acids Res 36 2008 3101 3117
4. J. Bowles, G. Schepers, P. Koopman Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators Dev Biol 227 2000 239 255
5. J.C. Kiefer Back to basics: Sox genes Dev Dyn 236 2007 2356 2366
6. S. McDowall, A. Argentaro, S. Ranganathan, P. Weller, S. Mertin, S. Mansour, J. Tolmie, V. Harley Functional and structural studies of wild type Sox9 and mutations causing campomelic dysplasia J Biol Chem 274 1999 24023 24030
7. P. Sudbeck, M.L. Schmitz, P.A. Baeuerle, G. Scherer Sex reversal by loss of the C-terminal transactivation domain of human Sox9 Nat Genet 13 1996 230 232
8. J.W. Foster, M.A. Dominguez-Steglich, S. Guioli, C. Kwok, P.A. Weller, M. Stevanovic, J. Weissenbach, S. Mansour, I.D. Young, P.N. Goodfellow Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene Nature 372 1994 525 530
9. T. Wagner, J. Wirth, J. Meyer, B. Zabel, M. Held, J. Zimmer, J. Pasantes, F.D. Bricarelli, J. Keutel, E. Hustert, U. Wolf, N. Tommerup, W. Schempp, G. Scherer Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the Sry-related gene Sox9 Cell 79 1994 1111 1120
10. R.F. Spokony, Y. Aoki, N. Saint-Germain, E. Magner-Fink, J.P. Saint-Jeannet The transcription factor Sox9 is required for cranial neural crest development in Xenopus Development 129 2002 421 432
11. C.C. Stolt, S. Rehberg, M. Ader, P. Lommes, D. Riethmacher, M. Schachner, U. Bartsch, M. Wegner Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10 Genes Dev 16 2002 165 170
12. J.W. Foster Mutations in Sox9 cause both autosomal sex reversal and campomelic dysplasia Acta Paediatr Jpn 38 1996 405 411
13. K. Piper, S.G. Ball, J.W. Keeling, S. Mansoor, D.L. Wiloson, N.A. Hanley Novel Sox9 expression during human pancreas development correlates to abnormalities in campomelic dysplasia Mech Dev 116 2002 223 226
14. S.S. Jiang, W.-T. Fang, Y.-H. Hou, S.-F. Huang, B.L. Yen, J.-L. Chang, S.-M. Li, H.-P. Liu, Y.-L. Liu, C.-T. Huang, Y.-W. Li, T.-H. Jang, S.-H. Chan, S.J. Yang, C.A. Hsiung, C.-W. Wu, L.-H. Wang, I.-S. Chang Upregulation of Sox9 in lung adenocarcinoma and its involvement in the regulation of cell growth and tumorigenicity Clin Cancer Res 16 2010 4363 4373
15. M. Saegusa, M. Hashimura, T. Kuwata, M. Hamano, I. Okayasu β-Catenin simultaneously induces activation of the p53-p21WAF1 pathway and overexpression of cyclin D1 during squamous differentiation of endometrial carcinoma cells Am J Pathol 164 2004 1739 1749
16. M. Saegusa, M. Hashimura, T. Kuwata, M. Hamano, I. Okayasu Crosstalk between NF-κB/p65 and β-catenin/TCF4/p300 signalling pathways through alterations in GSK-3β expression during trans-differentiation of endometrial carcinoma cells J Pathol 213 2007 35 45
17. M. Saegusa, M. Hashimura, T. Kuwata, I. Okayasu Requirement of the Akt/b-catenin pathway for uterine carcinosarcoma genesis, modulating E-cadherin expression through the transactivation of Slug. Am J Pathol 174 2009 2107 2115
18. M. Saegusa, M. Hashimura, T. Kuwata, M. Hamano, J. Watanabe, M. Kawaguchi, I. Okayasu Transcription factor Egr1 acts as an upstream regulator of β-catenin signaling through up-regulation of TCF4 and p300 expression during trans-differentiation of endometrial carcinoma cells J Pathol 216 2008 521 532
19. M. Saegusa, M. Hashimura, T. Kuwata Pin1 acts as a modulator of cell proliferation through alteration in NF-κB but not β-catenin/TCF4 signaling in a subset of endometrial carcinoma cells J Pathol 222 2010 410 420
20. S.G. Silverberg, G.L. Mutter, R.J. Kurman, R.A. Kubik-Huch, F. Nogates, F.A. Tavassoli Tumours of the uterine corpus: epithelial tumours and related lesions F.A. Tavassoli, P. Devilee, World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of the Breast and Female Genital Organs, ch 4 2003 IARC Press Lyon 221 232
21. W.T. Creasman Announcement FIGO stages: 1988 revisions Gynecol Oncol 35 1989 125 127
22. G.L. Mutter, A. Ferenczy Anatomy and histology of the uterine corpus R.J. Kurman, Blaustein's Pathology of the Female Genital Tract 2002 Springer-Verlag New York pp 383 419
23. B. de Crombrugghe, V. Lefebvre, R.R. Behringer, W. Bi, S. Murakami, W. Huang Transcriptional mechanism of chondrocyte differentiation Matrix Biol 19 2000 389 394
24. S. Muller, S. Soder, A.M. Oliveira, C.Y. Inwards, T. Aigner Type II collagen as specific marker for mesenchymal chondrosarcomas compared to other small cell sarcomas of the skeleton Mod Pathol 18 2005 1088 1094
25. I.O. Baas, J.-W.R. Mulder, J.A. Offerhaus, B. Vogelstein, S.R. Hamilton An evaluation of six antibodies for immunohistochemistry of mutant p53 gene product in archival colorectal neoplasms J Pathol 172 1994 5 12
26. S. Yamamoto, H. Tsuda, M. Takano, K. Iwaya, S. Tamai, O. Matsubara PIK3CA mutation is an early event in the development of endometriosis-associated ovarian clear cell adenocarcinoma J Pathol 225 2011 189 194
27. M.L. Rudd, J.C. Price, S. Fogoros, A.K. Godwin, D.C. Sgroi, M.J. Merino, D.W. Bell A unique spectrum of somatic PIK3CA (p110α) mutations within primary endometrial carcinomas Clin Cancer Res 17 2011 1331 1340
28. D.W. Bartlett, M.E. Davis Insight into the kinetics of siRNA-mediated gene silencing from live-cell and live-animal bioluminescent image Nucleic Acids Res 34 2006 322 333
29. W.S. El-Deiry, T. Tokino, V.E. Velculescu, D.B. Levy, R. Parsons, J.M. Trent, D. Lin, W.E. Mercer, K.W. Kinzler, B. Vogelstein WAF1, a potential mediator of p53 tumor suppression Cell 75 1993 817 825
30. Y. Kamachi, M. Uchikawa, H. Kondoh Pairing Sox off: with partners in the regulation of embryonic development Trends Genet 16 2000 182 187
31. K. Robertson, P.A. Jones The human ARF cell cycle regulator gene promoter is a CpG island which can be silenced by DNA methylation and down-regulated by wild-type p53 Mol Cell Biol 18 1998 6457 6473
32. M. Ushita, T. Saito, T. Ikeda, F. Yano, A. Higashikawa, N. Ogata, U. Chung, K. Nakamura, H. Kawaguchi Transcriptional induction of Sox9 by NF-κB family member RelA in chondrogenic cells Osteoarthritis Cartilage 17 2009 1065 1075
33. R. Sitcheran, P.C. Cogswell, A.S. Baldwin Jr NF-κB mediates inhibition of mesenchymal differentiation through a posttranscriptional gene silencing mechanism Genes Dev 17 2003 2368 2373
34. J.A. Romashkova, S.S. Makarov NF-κB is a target of Akt in anti-apoptotic PDGF signaling Nature 401 1999 86 90
35. F. Meng, L. Liu, P.C. Chin, S.R. D'Mello Akt is a downstream target of NF-κB J Biol Chem 277 2002 29674 29680
36. F. Meng, S.R. D'Mello NF-κB stimulates Akt phosphorylation and gene expression by distinct signaling mechanisms Biochim Biophys Acta 1630 2003 35 40
37. K. Oda, D. Stokoe, Y. Taketani, F. McCormick High frequency of coexistent mutations of PIK3CA and PTEN genes in endometrial carcinoma Cancer Res 65 2005 10669 10673
38. A. Velasco, E. Bussaglia, J. Pallares, X. Dolcet, D. Llobet, M. Encinas, N. Llecha, J. Palacios, J. Prat, X. Matias-Guiu PIK3CA gene mutations in endometrial carcinoma: correlation with PTEN and K-RAS alterations Hum Pathol 37 2006 1465 1472
39. P. Blache, M. van de Wetering, I. Duluc, C. Domon, P. Berta, J.-N. Freund, H. Clevers, P. Jay Sox9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes J Cell Biol 166 2004 37 47
40. D.K. Panda, D. Miao, V. Lefebvre, G.N. Hendy, D. Goltzman The transcription factor Sox9 regulates cell cycle and differentiation genes in chondrocytic CFK2 cells J Biol Chem 276 2001 41229 41236
41. T. Passeron, J.C. Valencia, T. Namiki, W.D. Vieira, H. Passeron, Y. Miyamura, V.J. Hearing Upregulation of Sox9 inhibits the growth of human and mouse melanomas and restores their sensitivity to retinoic acid J Clin Invest 119 2009 954 963
42. S. Murakami, V. Lefebvre, B. de Crombrugghe Potent inhibition of the master chondrogenic factor Sox9 gene by interleukin-1 and tumor necrosis factor-α J Biol Chem 275 2000 3687 3692
43. S. Julien, I. Puig, E. Caretti, J. Bonaventure, L. Nelles, F. van Roy, C. Dargemont, A. Garcia de Herreros, A. Bellacosa, L. Larue Activation of NF-κB by Akt upregulates Snail expression and induces epithelial mesenchyme transition Oncogene 26 2007 7445 7456
44. A. Bellacosa, J.R. Testa, R. Moore, L. Larue A portrait of AKT kinases: human cancer and animal models depict a family with strong individualities Cancer Biol Ther 3 2004 268 275
45. P. Viatour, M.P. Merville, V. Bours, A. Chariot Phosphorylation of NF-κB and IκB proteins: implications in cancer and inflammation Trends Biochem Sci 30 2005 43 52
46. Q.J. Cao, M.H. Einstein, P.S. Anderson, C.D. Runowicz, R. Balan, J.G. Jones Expression of Cox-2 Ki-67, cyclin D1, and p21 in endometrial endometrioid carcinomas Int J Gynecol Pathol 21 2002 147 154
47. N. Horree, P.J. van Diest, P. van der Groep, D.M.D.S. Sie-Go, A.P.M. Heintz Progressive derailment of cell cycle regulators in endometrial carcinogenesis J Clin Pathol 61 2008 36 42