Molecular Oncology
Volume 2, Issue 2 , Pages 164-181 , August 2008

Overexpression of SnoN/SkiL, amplified at the 3q26.2 locus, in ovarian cancers: A role in ovarian pathogenesis

  • Meera Nanjundan

      Affiliations

    • University of Texas, MD Anderson Cancer Center, Department of Systems Biology, 1515 Holcombe Boulevard, Box 950, Houston, TX, USA
    • University of South Florida, Division of Cell, Microbiology, and Molecular Biology, 4202 East Fowler Avenue, SCA110, Tampa, FL, USA
    • Corresponding Author InformationCorresponding author at: University of South Florida, Division of Cell, Microbiology, and Molecular Biology, 4202 East Fowler Avenue, SCA110, Tampa, FL 33620, USA. Tel.: +1 813 974 8133; fax: +1 813 974 1614.
    • ,
  • Kwai Wa Cheng

      Affiliations

    • University of Texas, MD Anderson Cancer Center, Department of Systems Biology, 1515 Holcombe Boulevard, Box 950, Houston, TX, USA
    • ,
  • Fan Zhang

      Affiliations

    • University of Texas, MD Anderson Cancer Center, Department of Systems Biology, 1515 Holcombe Boulevard, Box 950, Houston, TX, USA
    • ,
  • John Lahad

      Affiliations

    • University of Texas, MD Anderson Cancer Center, Department of Systems Biology, 1515 Holcombe Boulevard, Box 950, Houston, TX, USA
    • ,
  • Wen-Lin Kuo

      Affiliations

    • University of California San Francisco, Department of Laboratory Medicine and the Lawrence Berkeley National Laboratory, Berkeley, CA, USA
    • ,
  • Rosemarie Schmandt

      Affiliations

    • Department of Gynecologic Oncology, MD Anderson Cancer Center, Houston, TX, USA
    • ,
  • Karen Smith-McCune

      Affiliations

    • Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Francisco, CA, USA
    • ,
  • David Fishman

      Affiliations

    • New York University, New York, NY, USA
    • ,
  • Joe W. Gray

      Affiliations

    • University of California San Francisco, Department of Laboratory Medicine and the Lawrence Berkeley National Laboratory, Berkeley, CA, USA
    • ,
  • Gordon B. Mills

      Affiliations

    • University of Texas, MD Anderson Cancer Center, Department of Systems Biology, 1515 Holcombe Boulevard, Box 950, Houston, TX, USA

Received 8 December 2007 ,Revised 1 May 2008 ,Accepted 6 May 2008.

References 

  1. Baldwin RL, Tran H, Karlan BY. Loss of c-myc repression coincides with ovarian cancer resistance to transforming growth factor beta growth arrest independent of transforming growth factor beta/Smad signaling. Cancer Res. 2003;63:1413–1419
  2. Braig M, Schmitt CA. Oncogene-induced senescence: putting the brakes on tumor development. Cancer Res. 2006;66:2881–2884
  3. Buess M, Terracciano L, Reuter J, Ballabeni P, Boulay JL, Laffer U, et al. Amplification of SKI is a prognostic marker in early colorectal cancer. Neoplasia. 2004;6:207–212
  4. Chelbi-Alix MK, Pelicano L, Quignon F, Koken MH, Venturini L, Stadler M, et al. Induction of the PML protein by interferons in normal and APL cells. Leukemia. 1995;9:2027–2033
  5. Chen QM. Replicative senescence and oxidant-induced premature senescence. Beyond the control of cell cycle checkpoints. Ann. N.Y. Acad. Sci. 2000;908:111–125
  6. Chen T, Triplett J, Dehner B, Hurst B, Colligan B, Pemberton J, et al. Transforming growth factor-beta receptor type I gene is frequently mutated in ovarian carcinomas. Cancer Res. 2001;61:4679–4682
  7. Chia JA, Simms LA, Cozzi SJ, Young J, Jass JR, Walsh MD, et al. SnoN expression is differently regulated in microsatellite unstable compared with microsatellite stable colorectal cancers. BMC Cancer. 2006;6:252
  8. Coates PJ. Markers of senescence?. J. Pathol. 2002;196:371–373
  9. Dellaire G, Bazett-Jones DP. PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays. 2004;26:963–977
  10. Eder AM, Sui X, Rosen DG, Nolden LK, Cheng KW, Lahad JP, et al Atypical PKCiota contributes to poor prognosis through loss of apical-basal polarity and cyclin E overexpression in ovarian cancer. Proc. Natl. Acad. Sci. USA. 2005;102:12519–12524
  11. Edmiston JS, Yeudall WA, Chung TD, Lebman DA. Inability of transforming growth factor-beta to cause SnoN degradation leads to resistance to transforming growth factor-beta-induced growth arrest in esophageal cancer cells. Cancer Res. 2005;65:4782–4788
  12. Efeyan A, Collado M, Velasco-Miguel S, Serrano M. Genetic dissection of the role of p21(Cip1/Waf1) in p53-mediated tumour suppression. Oncogene. 2006;26:1645–1649
  13. Elliott RL, Blobe GC. Role of transforming growth factor Beta in human cancer. J. Clin. Oncol. 2005;23:2078–2093
  14. Fukuchi M, Nakajima M, Fukai Y, Miyazaki T, Masuda N, Sohda M, et al. Increased expression of c-Ski as a co-repressor in transforming growth factor-beta signaling correlates with progression of esophageal squamous cell carcinoma. Int. J. Cancer. 2004;108:818–824
  15. 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
  16. Hsu YH, Sarker KP, Pot I, Chan A, Netherton SJ, Bonni S. Sumoylated SnoN represses transcription in a promoter-specific manner. J. Biol. Chem. 2006;281:33008–33018
  17. Hurteau J, Rodriguez GC, Whitaker RS, Shah S, Mills G, Bast RC, et al. Transforming growth factor-beta inhibits proliferation of human ovarian cancer cells obtained from ascites. Cancer. 1994;74:93–99
  18. Imoto I, Pimkhaokham A, Fukuda Y, Yang ZQ, Shimada Y, Nomura N, et al. SNO is a probable target for gene amplification at 3q26 in squamous-cell carcinomas of the esophagus. Biochem. Biophys. Res. Commun. 2001;286:559–565
  19. Imoto I, Yuki Y, Sonoda I, Ito T, Shimada Y, Imamura M, et al. Identification of ZASC1 encoding a Kruppel-like zinc finger protein as a novel target for 3q26 amplification in esophageal squamous cell carcinomas. Cancer Res. 2003;63:5691–5696
  20. Krakowski AR, Laboureau J, Mauviel A, Bissell MJ, Luo K. Cytoplasmic SnoN in normal tissues and nonmalignant cells antagonizes TGF-beta signaling by sequestration of the Smad proteins. Proc. Natl. Acad. Sci. USA. 2005;102:12437–12442
  21. Kuhn W, Schmalfeldt B, Reuning U, Pache L, Berger U, Ulm K, et al Prognostic significance of urokinase (uPA) and its inhibitor PAI-1 for survival in advanced ovarian carcinoma stage FIGO IIIc. Br. J. Cancer. 1999;79:1746–1751
  22. Kutz SM, Hordines J, McKeown-Longo PJ, Higgins PJ. TGF-beta1-induced PAI-1 gene expression requires MEK activity and cell-to-substrate adhesion. J. Cell Sci. 2001;114:3905–3914
  23. Levy L, Howell M, Das D, Harkin S, Episkopou V, Hill CS. Arkadia activates Smad3/Smad4-dependent transcription by triggering signal-induced SnoN degradation. Mol. Cell. Biol. 2007;27:6068–6083
  24. Liu X, Sun Y, Weinberg RA, Lodish HF. Ski/Sno and TGF-beta signaling. Cytokine Growth Factor Rev. 2001;12:1–8
  25. Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature. 2005;436:720–724
  26. Muller S, Ledl A, Schmidt D. SUMO: a regulator of gene expression and genome integrity. Oncogene. 2004;23:1998–2008
  27. Nagano Y, Mavrakis KJ, Lee KL, Fujii T, Koinuma D, Sase H, et al Arkadia induces degradation of SnoN and c-Ski to enhance transforming growth factor-beta signaling. J. Biol. Chem. 2007;282:20492–20501
  28. Nanjundan M, Nakayama Y, Cheng KW, Lahad J, Liu J, Lu K, et al Amplification of MDS1/EVI1 and EVI1, located in the 3q26.2 amplicon, is associated with favorable patient prognosis in ovarian cancer. Cancer Res. 2007;67:3074–3084
  29. Reed JA, Lin Q, Chen D, Mian IS, Medrano EE. SKI pathways inducing progression of human melanoma. Cancer Metastasis Rev. 2005;24:265–272
  30. Riazimand SH, Welkoborsky HJ, Bernauer HS, Jacob R, Mann WJ. Investigations for fine mapping of amplifications in chromosome 3q26.3–28 frequently occurring in squamous cell carcinomas of the head and neck. Oncology. 2002;63:385–392
  31. Roninson IB. Tumor cell senescence in cancer treatment. Cancer Res. 2003;63:2705–2715
  32. Sarker KP, Wilson SM, Bonni S. SnoN is a cell type-specific mediator of transforming growth factor-beta responses. J. Biol. Chem. 2005;280:13037–13046
  33. Sattler HP, Rohde V, Bonkhoff H, Zwergel T, Wullich B. Comparative genomic hybridization reveals DNA copy number gains to frequently occur in human prostate cancer. Prostate. 1999;39:79–86
  34. Sattler HP, Lensch R, Rohde V, Zimmer E, Meese E, Bonkhoff H, et al Novel amplification unit at chromosome 3q25–q27 in human prostate cancer. Prostate. 2000;45:207–215
  35. Shayesteh L, Lu Y, Kuo WL, Baldocchi R, Godfrey T, Collins C, et al. PIK3CA is implicated as an oncogene in ovarian cancer. Nat. Genet. 1999;21:99–102
  36. Shinagawa T, Dong HD, Xu M, Maekawa T, Ishii S. The sno gene, which encodes a component of the histone deacetylase complex, acts as a tumor suppressor in mice. Embo J. 2000;19:2280–2291
  37. Shinagawa T, Nomura T, Colmenares C, Ohira M, Nakagawara A, Ishii S. Increased susceptibility to tumorigenesis of ski-deficient heterozygous mice. Oncogene. 2001;20:8100–8108
  38. Snijders AM, Nowak N, Segraves R, Blackwood S, Brown N, Conroy J, et al Assembly of microarrays for genome-wide measurement of DNA copy number. Nat. Genet. 2001;29:263–264
  39. Stroschein SL, Wang W, Zhou S, Zhou Q, Luo K. Negative feedback regulation of TGF-beta signaling by the SnoN oncoprotein. Science. 1999;286:771–774
  40. Stroschein SL, Bonni S, Wrana JL, Luo K. Smad3 recruits the anaphase-promoting complex for ubiquitination and degradation of SnoN. Genes Dev. 2001;15:2822–2836
  41. Sugita M, Tanaka N, Davidson S, Sekiya S, Varella-Garcia M, West J, et al. Molecular definition of a small amplification domain within 3q26 in tumors of cervix, ovary, and lung. Cancer Genet. Cytogenet. 2000;117:9–18
  42. Sunde JS, Donninger H, Wu K, Johnson ME, Pestell RG, Rose GS, et al. Expression profiling identifies altered expression of genes that contribute to the inhibition of transforming growth factor-{beta} signaling in ovarian cancer. Cancer Res. 2006;66:8404–8412
  43. Trost TM, Lausch EU, Fees SA, Schmitt S, Enklaar T, Reutzel D, et al Premature senescence is a primary fail-safe mechanism of ERBB2-driven tumorigenesis in breast carcinoma cells. Cancer Res. 2005;65:840–849
  44. Wang D, Kanuma T, Takama F, Mizumuma H, Ibuki Y, Wake N, et al. Mutation analysis of the Smad3 gene in human ovarian cancers. Int. J. Oncol. 1999;15:949–953
  45. Wang D, Kanuma T, Mizumuma H, Ibuki Y, Takenoshita S. Mutation analysis of the Smad6 and Smad7 gene in human ovarian cancers. Int. J. Oncol. 2000;17:1087–1091
  46. Weber-Mangal S, Sinn HP, Popp S, Klaes R, Emig R, Bentz M, et al. Breast cancer in young women (< or =35years): genomic aberrations detected by comparative genomic hybridization. Int. J. Cancer. 2003;107:583–592
  47. Weichert W, Gekeler V, Denkert C, Dietel M, Hauptmann S. Protein kinase C isoform expression in ovarian carcinoma correlates with indicators of poor prognosis. Int. J. Oncol. 2003;23:633–639
  48. Wessels LF, van Welsem T, Hart AA, van't Veer LJ, Reinders MJ, Nederlof PM. Molecular classification of breast carcinomas by comparative genomic hybridization: a specific somatic genetic profile for BRCA1 tumors. Cancer Res. 2002;62:7110–7117
  49. Whitley BR, Palmieri D, Twerdi CD, Church FC. Expression of active plasminogen activator inhibitor-1 reduces cell migration and invasion in breast and gynecological cancer cells. Exp. Cell Res. 2004;296:151–162
  50. Wilson JJ, Malakhova M, Zhang R, Joachimiak A, Hegde RS. Crystal structure of the dachshund homology domain of human SKI. Structure. 2004;12:785–792
  51. Zhang F, Monkkonen M, Roth S, Laiho M. Proteasomal activity modulates TGF-ss signaling in a gene-specific manner. FEBS Lett. 2002;527:58–62
  52. Zhang F, Lundin M, Ristimaki A, Heikkila P, Lundin J, Isola J, et al. Ski-related novel protein N (SnoN), a negative controller of transforming growth factor-beta signaling, is a prognostic marker in estrogen receptor-positive breast carcinomas. Cancer Res. 2003;63:5005–5010
  53. Zhang H, Cohen SN. Smurf2 up-regulation activates telomere-dependent senescence. Genes Dev. 2004;18:3028–3040
  54. Zhu Q, Pearson-White S, Luo K. Requirement for the SnoN oncoprotein in transforming growth factor beta-induced oncogenic transformation of fibroblast cells. Mol. Cell. Biol. 2005;25:10731–10744
  55. Zhu Q, Krakowski AR, Dunham EE, Wang L, Bandyopadhyay A, Berdeaux R, et al. Dual role of SnoN in mammalian tumorigenesis. Mol. Cell. Biol. 2007;27:324–339

PII: S1574-7891(08)00060-4

doi: 10.1016/j.molonc.2008.05.001

Molecular Oncology
Volume 2, Issue 2 , Pages 164-181 , August 2008

Article Tools

* Image Usage & Resolution