The deubiquitylase Ataxin-3 restricts PTEN transcription in lung cancer cells

Oncogene

Volumn 33, Issue 33, 2014, Pages 4265-4272

  Sacco, J J ^a   Yau, T Y ^a   Darling, S ^a   Patel, V ^a,b   Liu, H ^a,c   Urbe S ^a   Clague, M J ^a   Coulson, J M ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

ATXN3; ceRNA; deubiquitinase; MJD; phosphatase and tensin homolog; PTENP1

Indexed keywords

ATAXIN 3; ATAXIN 3 LIKE PROTEIN; DEUBIQUITINASE; HISTONE DEACETYLASE 3; JOSEPHIN DOMAIN CONTAINING 1 PROTEIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VORINOSTAT;

ARTICLE; CELL COUNT; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOLIC FRACTION; DRUG EXPOSURE; ENZYME PHOSPHORYLATION; HALF LIFE TIME; HUMAN; LUNG CANCER CELL LINE; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UBIQUITINATION;

CELL LINE, TUMOR; CELL SURVIVAL; DOWN-REGULATION; ENZYME STABILITY; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HUMANS; LUNG NEOPLASMS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PTEN PHOSPHOHYDROLASE; REPRESSOR PROTEINS; RNA STABILITY; UBIQUITINATION;

EID: 84906235090     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.512     Document Type: Article

References (55)

1. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 1998; 273: 13375-13378. (Pubitemid 28268370)
2. Salmena L, Carracedo A, Pandolfi PP. Tenets of PTEN tumor suppression. Cell 2008; 133: 403-414. (Pubitemid 351622014)
3. Song MS, Salmena L, Pandolfi PP. The functions and regulation of the PTEN tumor suppressor. Nat Rev Mol Cell Biol 2012; 13: 283-296.
4. Di Cristofano A, De Acetis M, Koff A, Cordon-Cardo C, Pandolfi PP. Pten and p27KIP1 cooperate in prostate cancer tumor suppression in the mouse. Nat Genet 2001; 27: 222-224. (Pubitemid 32157454)
5. Di Cristofano A, Kotsi P, Peng YF, Cordon-Cardo C, Elkon KB, Pandolfi PP. Impaired Fas response and autoimmunity in Pten+/- mice. Science 1999; 285: 2122-2125. (Pubitemid 29451429)
6. Alimonti A, Carracedo A, Clohessy JG, Trotman LC, Nardella C, Egia A et al. Subtle variations in Pten dose determine cancer susceptibility. Nat Genet 2010; 42: 454-458.
7. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast and prostate cancer. Science 1997; 275: 1943-1947. (Pubitemid 27148818)
8. Steck PA, Pershouse MA, Jasser SA, Yung WK, Lin H, Ligon AH et al. Identification of a candidate tumor suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet 1997; 15: 356-362. (Pubitemid 27147102)
9. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP. Pten is essential for embryonic development and tumor suppression. Nat Genet 1998; 19: 348-355. (Pubitemid 28357906)
10. Suzuki A, de la Pompa JL, Stambolic V, Elia AJ, Sasaki T, del Barco Barrantes I et al. High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Curr biol 1998; 8: 1169-1178. (Pubitemid 28494715)
11. Podsypanina K, Ellenson LH, Nemes A, Gu J, Tamura M, Yamada KM et al. Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems. Proc Natl Acad Sci USA 1999; 96: 1563-1568. (Pubitemid 29098491)
12. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T et al. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 1998; 95: 29-39. (Pubitemid 28458022)
13. Sun H, Lesche R, Li DM, Liliental J, Zhang H, Gao J et al. PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway. Proc Natl Acad Sci USA 1999; 96: 6199-6204. (Pubitemid 29256643)
14. Leslie NR, Foti M. Non-genomic loss of PTEN function in cancer: not in my genes. Trends pharmacol sci 2011; 32: 131-140.
15. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG et al. In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 2011; 147: 382-395.
16. Tay Y, Kats L, Salmena L, Weiss D, Tan SM, Ala U et al. Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 2011; 147: 344-357.
17. Jin G, Kim MJ, Jeon HS, Choi JE, Kim DS, Lee EB et al. PTEN mutations and relationship to EGFR, ERBB2, KRAS and TP53 mutations in non-small cell lung cancers. Lung Cancer 2010; 69: 279-283.
18. Soria JC, Lee HY, Lee JI, Wang L, Issa JP, Kemp BL et al. Lack of PTEN expression in non-small cell lung cancer could be related to promoter methylation. Clin Cancer Res 2002; 8: 1178-1184. (Pubitemid 34517656)
19. Cai J, Fang L, Huang Y, Li R, Yuan J, Yang Y et al. miR-205 targets PTEN and PHLPP2 to augment AKT signaling and drive malignant phenotypes in non-small cell lung cancer. Cancer Res 2013; 73: 5402-5415.
20. Sacco JJ, Coulson JM, Clague MJ, Urbe S. Emerging roles of deubiquitinases in cancer-associated pathways. IUBMB Life 2010; 62: 140-157.
21. Clague MJ, Coulson JM, Urbé S. Cellular functions of the DUBs. J Cell Sci 2012; 125: 277-286.
22. Clague MJ, Barsukov I, Coulson JM, Liu H, Rigden DJ, Urbe S. Deubiquitylases from genes to organism. Physiol rev 2013; 93: 1289-1315.
23. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 2005; 123: 773-786. (Pubitemid 41721026)
24. Reyes-Turcu FE, Ventii KH, Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 2009; 78: 363-397.
25. Amodio N, Scrima M, Palaia L, Salman AN, Quintiero A, Franco R et al. Oncogenic role of the E3 ubiquitin ligase NEDD4-1, a PTEN negative regulator, in non-smallcell lung carcinomas. Am J Pathol 2010; 177: 2622-2634.
26. Maddika S, Kavela S, Rani N, Palicharla VR, Pokorny JL, Sarkaria JN et al. WWP2 is an E3 ubiquitin ligase for PTEN. Nat cell biol 2011; 13: 728-733.
27. Van Themsche C, Leblanc V, Parent S, Asselin E. X-linked inhibitor of apoptosis protein (XIAP) regulates PTEN ubiquitination, content and compartmentalization. J Biol Chem 2009; 284: 20462-20466.
28. Song MS, Salmena L, Carracedo A, Egia A, Lo-Coco F, Teruya-Feldstein J et al. The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature 2008; 455: 813-817.
29. Omerovic J, Clague MJ, Prior IA. Phosphatome profiling reveals PTPN2, PTPRJ and PTEN as potent negative regulators of PKB/Akt activation in Ras-mutated cancer cells. Biochem J 2010; 426: 65-72.
30. Rodriguez-Lebron E, Costa MD, Luna-Cancalon K, Peron TM, Fischer S, Boudreau RL et al. Silencing mutant ATXN3 expression resolves molecular phenotypes in SCA3 transgenic mice. Mol ther 2013; 21: 1909-1918.
31. Vazquez F, Ramaswamy S, Nakamura N, Sellers WR. Phosphorylation of the PTEN tail regulates protein stability and function. Mol Cell Biol 2000; 20: 5010-5018. (Pubitemid 30431555)
32. Wu X, Hepner K, Castelino-Prabhu S, Do D, Kaye MB, Yuan XJ et al. Evidence for regulation of the PTEN tumor suppressor by a membrane-localized multi-PDZ domain containing scaffold protein MAGI-2. Proc Natl Acad Sci USA 2000; 97: 4233-4238. (Pubitemid 30226116)
33. Mao JH, Kim IJ, Wu D, Climent J, Kang HC, DelRosario R et al. FBXW7 targets mTOR for degradation and cooperates with PTEN in tumor suppression. Science 2008; 321: 1499-1502.
34. Yim EK, Peng G, Dai H, Hu R, Li K, Lu Y et al. Rak functions as a tumor suppressor by regulating PTEN protein stability and function. Cancer Cell 2009; 15: 304-314.
35. Yang Y, Zhou F, Fang Z, Wang L, Li Z, Sun L et al. Post-transcriptional and posttranslational regulation of PTEN by transforming growth factor-beta1. J Cell Biochem 2009; 106: 1102-1112.
36. Song EJ, Werner SL, Neubauer J, Stegmeier F, Aspden J, Rio D et al. The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev 2010; 24: 1434-1447.
37. Sowa ME, Bennett EJ, Gygi SP, Harper JW. Defining the human deubiquitinating enzyme interaction landscape. Cell 2009; 138: 389-403.
38. Evert BO, Araujo J, Vieira-Saecker AM, De Vos RA, Harendza S, Klockgether T et al. Ataxin-3 represses transcription via chromatin binding, interaction with histone deacetylase3 and histone deacetylation. J Neurosci 2006; 26: 11474-11486. (Pubitemid 44772178)
39. Li F, Macfarlan T, Pittman RN, Chakravarti D. Ataxin-3 is a histone-binding protein with two independent transcriptional corepressor activities. J Biol Chem 2002; 277: 45004-45012. (Pubitemid 36159099)
40. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta stone of a hidden RNA language? Cell 2011; 146: 353-358.
41. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP. A codingindependent function of gene and pseudogene mRNAs regulates tumor biology. Nature 2010; 465: 1033-1038.
42. Gan YH, Zhang S. PTEN/AKT pathway involved in histone deacetylases inhibitor induced cell growth inhibition and apoptosis of oral squamous cell carcinoma cells. Oral Oncol 2009; 45: e150-e154.
43. Pan L, Lu J, Wang X, Han L, Zhang Y, Han S et al. Histone deacetylase inhibitor trichostatin a potentiates doxorubicin-induced apoptosis by up-regulating PTEN expression. Cancer 2007; 109: 1676-1688. (Pubitemid 46595705)
44. Marks PA. Discovery and development of SAHA as an anticancer agent. Oncogene 2007; 26: 1351-1356. (Pubitemid 46328465)
45. Moss AC, Jacobson GM, Walker LE, Blake NW, Marshall E, Coulson JM. SCG3 transcript in peripheral blood is a prognostic biomarker for REST-deficient small cell lung cancer. Clin Cancer Res 2009; 15: 274-283.
46. Seki T, Gong L, Williams AJ, Sakai N, Todi SV, Paulson HL. JosD1, a membrane-targeted deubiquitinating enzyme, is activated by ubiquitination and regulates membrane dynamics, cell motility and endocytosis. J Biol Chem 2013; 288: 17145-17155.
47. Buus R, Faronato M, Hammond DE, Urbe S, Clague MJ. Deubiquitinase activities required for hepatocyte growth factor-induced scattering of epithelial cells. Curr Biol 2009; 19: 1463-1466.
48. Weeks SD, Grasty KC, Hernandez-Cuebas L, Loll PJ. Crystal structure of a Josephinubiquitin complex: evolutionary restraints on ataxin-3 deubiquitinating activity. J Biol Chem 2011; 286: 4555-4565.
49. Winborn BJ, Travis SM, Todi SV, Scaglione KM, Xu P, Williams AJ et al. The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J Biol Chem 2008; 283: 26436-26443.
50. Todi SV, Winborn BJ, Scaglione KM, Blount JR, Travis SM, Paulson HL. Ubiquitination directly enhances activity of the deubiquitinating enzyme ataxin-3. EMBO J 2009; 28: 372-382.
51. Gorski JJ, Pathak S, Panov K, Kasciukovic T, Panova T, Russell J et al. A novel TBPassociated factor of SL1 functions in RNA polymerase I transcription. EMBO J 2007; 26: 1560-1568. (Pubitemid 46480930)
52. Vasudevan KM, Gurumurthy S, Rangnekar VM. Suppression of PTEN expression by NF-kappa B prevents apoptosis. Mol Cell Biol 2004; 24: 1007-1021. (Pubitemid 38112166)
53. Andersen CL, Asmar F, Klausen T, Hasselbalch H, Gronbaek K. Somatic mutations of the CREBBP and EP300 genes affect response to histone deacetylase inhibition in malignant DLBCL clones. Leukemia Res Reports 2013; 2: 1-3.
54. Ikeda H, Yamaguchi M, Sugai S, Aze Y, Narumiya S, Kakizuka A. Expanded polyglutamine in the Machado-Joseph disease protein induces cell death in vitro and in vivo. Nat Genet 1996; 13: 196-202. (Pubitemid 26000440)
55. Wang HL, Hu SH, Chou AH, Wang SS, Weng YH, Yeh TH. H1152 promotes the degradation of polyglutamine-expanded ataxin-3 or ataxin-7 independently of its ROCK-inhibiting effect and ameliorates mutant ataxin-3-induced neurodegeneration in the SCA3 transgenic mouse. Neuropharmacology 2013; 70: 1-11.