Transforming growth factor-β suppresses the ability of ski to inhibit tumor metastasis by inducing its degradation

Cancer Research

Volumn 68, Issue 9, 2008, Pages 3277-3285

  Le Scolan, Erwan ^a   Zhu, Qingwei ^a,b   Wang, Long ^c   Bandyopadhyay, Abhik ^c   Javelaud, Delphine ^d   Mauviel, Alain ^d   Sun, Luzhe ^c   Luo, Kunxin ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c Mays Cancer Center at UT Health San Antonio   (United States)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARKADIA; DNA BINDING PROTEIN; PROTEASOME; PROTEIN SKI; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN; UNCLASSIFIED DRUG; NUCLEAR PROTEIN; ONCOPROTEIN; RNF111 PROTEIN, HUMAN; SKI PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; CANCER CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG CANCER; METASTASIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; METABOLISM; MOUSE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROTEIN PROCESSING; TUMOR SUPPRESSOR GENE; XENOGRAFT;

ANIMALS; DNA-BINDING PROTEINS; FEMALE; GENES, TUMOR SUPPRESSOR; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM METASTASIS; NUCLEAR PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 44849143723     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-6793     Document Type: Article

References (50)

1. Li Y, Turck CM, Teumer JK, Stavnezer E. Unique sequence, ski, in Sloan-Kettering avian retroviruses with properties of a new cell-derived oncogene. J Virol 1986;57:1065-72.
2. Nomura N, Sasamoto S, Ishii S, Date T, Matsui M, Ishizaki R. Isolation of human cDNA clones of ski and the ski-related gene, sno. Nucleic Acids Res 1989;17:5489-500.
3. Colmenares C, Stavnezer E. The ski oncogene induces muscle differentiation in quail embryo cells. Cell 1989;59:293-303.
4. Reed JA, Bales E, Xu W, Okan NA, Bandyopadhyay D, Medrano EE. Cytoplasmic localization of the oncogenic protein Ski in human cutaneous melanomas in vivo: functional implications for transforming growth factor β signaling. Cancer Res 2001;61:8074-8.
5. Fukuchi M, Nakajima M, Fukai Y, et al. Increased expression of c-Ski as a co-repressor in transforming growth factor-β signaling correlates with progression of esophageal squamous cell carcinoma. Int J Cancer 2004;108:818-24.
6. Buess M, Terracciano L, Reuter J, et al. Amplification of SKI is a prognostic marker in early colorectal cancer. Neoplasia 2004;6:207-12.
7. Heider TR, Lyman S, Schoonhoven R, Behrns KE. Ski promotes tumor growth through abrogation of transforming growth factor-β signaling in pancreatic cancer. Ann Surg 2007;246:61-8.
8. Ritter M, Kattmann D, Teichler S, et al. Inhibition of retinoic acid receptor signaling by Ski in acute myeloid leukemia. Leukemia 2006;20:437-43.
9. Shinagawa T, Nomura T, Colmenares C, Ohira M, Nakagawara A, Ishii S. Increased susceptibility to tumorigenesis of ski-deficient heterozygous mice. Oncogene 2001;20:8100-8.
10. -/- mice. Nat Genet 2002;30:106-9.
11. Brodeur GM. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 2003;3:203-16.
12. Smedley D, Sidhar S, Birdsall S, et al. Characterization of chromosome 1 abnormalities in malignant melanomas. Genes Chromosomes Cancer 2000;28:121-5.
13. Zhu Q, Krakowski AR, Dunham EE, et al. Dual role of SnoN in mammalian tumorigenesis. Mol Cell Biol 2007;27:324-39.
14. Luo K. Ski and SnoN: negative regulators of TGF-β signaling. Curr Opin Genet Dev 2004;14:65-70.
15. Roberts AB, Flanders KC, Heine UI, et al. Transforming growth factor-β: multifunctional regulator of differentiation and development. Philos Trans R Soc Lond B Biol Sci 1990;327:145-54.
16. Derynck R, Akhurst RJ, Balmain A. TGF-β signaling in tumor suppression and cancer progression. Nat Genet 2001;29:117-29.
17. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-β in homeostasis and cancer. Nat Rev Cancer 2003;3:807-21.
18. Levy L, Hill CS. Alterations in components of the TGF-β superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev 2006;17:41-58.
19. Bierie B, Moses HL. TGF-β and cancer. Cytokine Growth Factor Rev 2006;17:29-40.
20. Shi Y, Massague J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003;113:685-700.
21. Feng XH, Derynck R. Specificity and versatility in TGF-β signaling through Smads. Annu Rev Cell Dev Biol 2005;21:659-93.
22. Grimes HL, Ambrose MR, Goodenow MM. C-ski transcripts with and without exon 2 are expressed in skeletal muscle and throughout chick embryogenesis. Oncogene 1993;8:2863-8.
23. Lyons GE, Micales BK, Herr MJ, et al. Protooncogene c-ski is expressed in both proliferating and postmitotic neuronal populations. Dev Dyn 1994;201:354-65.
24. Namciu S, Lyons GE, Micales BK, Heyman HC, Colmenares C, Stavnezer E. Enhanced expression of mouse c-ski accompanies terminal skeletal muscle differentiation in vivo and in vitro. Dev Dyn 1995;204:291-300.
25. Kaufman CD, Martinez-Rodriguez G, Hackett PB, Jr. Ectopic expression of c-ski disrupts gastrulation and neural patterning in zebrafish. Mech Dev 2000;95:147-62.
26. Amaravadi LS, Neff AW, Sleeman JP, Smith RC. Autonomous neural axis formation by ectopic expression of the protooncogene c-ski. Dev Biol 1997;192:392-404.
27. Berk M, Desai SY, Heyman HC, Colmenares C. Mice lacking the ski proto-oncogene have defects in neurulation, craniofacial, patterning, and skeletal muscle development. Genes Dev 1997;11:2029-39.
28. Fumagalli S, Doneda L, Nomura N, Larizza L. Expression of the c-ski proto-oncogene in human melanoma cell lines. Melanoma Res 1993;3:23-7.
29. Fukasawa H, Yamamoto T, Togawa A, et al. Ubiquitin-dependent degradation of SnoN and Ski is increased in renal fibrosis induced by obstructive injury. Kidney Int 2006;69:1733-40.
30. Macdonald M, Wan Y, Wang W, et al. Control of cell cycle-dependent degradation of c-Ski proto-oncoprotein by Cdc34. Oncogene 2004;23:5643-53.
31. Marcelain K, Hayman MJ. The Ski oncoprotein is upregulated and localized at the centrosomes and mitotic spindle during mitosis. Oncogene 2005;24:4321-9.
32. 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;27:6068-83.
33. Nagano Y, Mavrakis KJ, Lee KL, et al. Arkadia induces degradation of SnoN and c-Ski to enhance transforming growth factor-h signaling. J Biol Chem 2007;282:20492-501.
34. Sun Y, Liu X, Ng-Eaton E, Lodish HF, Weinberg RA. SnoN and Ski protooncoproteins are rapidly degraded in response to transforming growth factor β signaling. Proc Natl Acad Sci U S A 1999;96:12442-7.
35. Bonni S, Wang HR, Causing CG, et al. TGF-β induces assembly of a Smad2-Smurf2 ubiquitin ligase complex that targets SnoN for degradation. Nat Cell Biol 2001;3:587-95.
36. Stroschein SL, Bonni S, Wrana JL, Luo K. Smad3 recruits the anaphase-promoting complex for ubiquitination and degradation of SnoN. Genes Dev 2001;15:2822-36.
37. Wan Y, Liu X, Kirschner MW. The anaphase-promoting complex mediates TGF-β signaling by targeting SnoN for destruction. Mol Cell 2001;8:1027-39.
38. Baldwin RL, Tran H, Karlan BY. Loss of c-myc repression coincides with ovarian cancer resistance to transforming growth factor β growth arrest independent of transforming growth factor β/Smad signaling. Cancer Res 2003;63:1413-9.
39. Javelaud D, Mohammad KS, McKenna CR, et al. Stable overexpression of Smad7 in human melanoma cells impairs bone metastasis. Cancer Res 2007;67:2317-24.
40. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH, Moustakas A. Transforming growth factor-β employs HMGA2 to elicit epithelial- mesenchymal transition. J Cell Biol 2006;174:175-83.
41. Peinado H, Quintanilla M, Cano A. Transforming growth factor β-1 induces snail transcription factor in epithelial cell lines: mechanisms for epithelial mesenchymal transitions. J Biol Chem 2003;278:21113-23.
42. de Winter JP, Roelen BA, ten Dijke P, van der Burg B, van den Eijnden-van Raaij AJ. DPC4 (SMAD4) mediates transforming growth factor-β1 (TGF-β1) induced growth inhibition and transcriptional response in breast tumour cells. Oncogene 1997;14:1891-9.
43. Luo K, Stroschein SL, Wang W, et al. The Ski oncoprotein interacts with the Smad proteins to repress TGFβ signaling. Genes Dev 1999;13:2196-206.
44. Azuma H, Ehata S, Miyazaki H, et al. Effect of Smad7 expression on metastasis of mouse mammary carcinoma JygMC(A) cells. J Natl Cancer Inst 2005;97:1734-46.
45. Liu W, Rui H, Wang J, et al. Axin is a scaffold protein in TGF-β signaling that promotes degradation of Smad7 by Arkadia. EMBO J 2006;25:1646-58.
46. Koinuma D, Shinozaki M, Komuro A, et al. Arkadia amplifies TGF-β superfamily signalling through degradation of Smad7. EMBO J 2003;22:6458-70.
47. Mavrakis KJ, Andrew RL, Lee KL, et al. Arkadia enhances Nodal/TGF-β signaling by coupling phospho-Smad2/3 activity and turnover. PLoS Biol 2007;5:e67.
48. Niederlander C, Walsh JJ, Episkopou V, Jones CM. Arkadia enhances nodal-related signalling to induce mesendoderm. Nature 2001;410:830-4.
49. Episkopou V, Arkell R, Timmons PM, Walsh JJ, Andrew RL, Swan D. Induction of the mammalian node requires Arkadia function in the extraembryonic lineages. Nature 2001;410:825-30.
50. Liu FY, Li XZ, Peng YM, Liu H, Liu YH. Arkadia regulates TGF-β signaling during renal tubular epithelial to mesenchymal cell transition. Kidney Int 2008;73:588-94.