Tumor-suppressor role for the SPOP ubiquitin ligase in signal-dependent proteolysis of the oncogenic co-activator SRC-3/AIB1

Oncogene

Volumn 30, Issue 42, 2011, Pages 4350-4364

  Li, C ^a,b   Ao, J ^b   Fu, J ^a   Lee, D F ^c   Xu, J ^a   Lonard, D ^a   O'Malley, B W ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

breast cancer; SPOP; SRC 3 AIB1; steroid receptor co activator; tumor suppressor; ubiquitin ligase

Indexed keywords

CASEIN KINASE IEPSILON; CULLIN; CULLIN 3; PROTEIN RBX1; SHORT HAIRPIN RNA; SPECKLE TYPE POZ PROTEIN; STEROID RECEPTOR COACTIVATOR 3; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CARCINOGENESIS; CONTROLLED STUDY; GENE LOCUS; GENE OVEREXPRESSION; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; UBIQUITINATION;

ADENOCARCINOMA; ANIMALS; BREAST NEOPLASMS; CARRIER PROTEINS; CASEIN KINASE IEPSILON; CELL LINE, TUMOR; CULLIN PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, NUDE; NUCLEAR PROTEINS; NUCLEAR RECEPTOR COACTIVATOR 3; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 80054908957     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.151     Document Type: Article

References (70)

1. Anzick SL, Kononen J, Walker RL, Azorsa DO, Tanner MM, Guan XY et al. (1997). AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277: 965-968. (Pubitemid 27366683)
2. Belandia B, Parker MG. (2000). Functional interaction between the p160 coactivator proteins and the transcriptional enhancer factor family of transcription factors. J Biol Chem 275: 30801-30805.
3. Bennett EJ, Rush J, Gygi SP, Harper JW. (2010). Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 143: 951-965.
4. Bunce MW, Boronenkov IV, Anderson RA. (2008). Coordinated activation of the nuclear ubiquitin ligase Cul3-SPOP by the generation of phosphatidylinositol 5-phosphate. J Biol Chem 283: 8678-8686.
5. Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L et al. (1997). Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90: 569-580. (Pubitemid 27347246)
6. Chen MH, Wilson CW, Li YJ, Law KK, Lu CS, Gacayan R et al. (2009). Cilium-independent regulation of Gli protein function by Sufu in Hedgehog signaling is evolutionarily conserved. Genes Dev 23: 1910-1928.
7. Claiborn KC, Sachdeva MM, Cannon CE, Groff DN, Singer JD, Stoffers DA. (2010). Pcif1 modulates Pdx1 protein stability and pancreatic beta cell function and survival in mice. J Clin Invest 120: 3713-3721.
8. De Marchis L, Cropp C, Sheng ZM, Bargo S, Callahan R. (2004). Candidate target genes for loss of heterozygosity on human chromosome 17q21. Br J Cancer 90: 2384-2389. (Pubitemid 38961904)
9. Durocher F, Tonin P, Shattuck-Eidens D, Skolnick M, Narod SA, Simard J. (1996). Mutation analysis of the BRCA1 gene in 23 families with cases of cancer of the breast, ovary, and multiple other sites. J Med Genet 33: 814-819. (Pubitemid 26375787)
10. Eide EJ, Woolf MF, Kang H, Woolf P, Hurst W, Camacho F et al. (2005). Control of mammalian circadian rhythm by CKIepsilon-regulated proteasome-mediated PER2 degradation. Mol Cell Biol 25: 2795-2807. (Pubitemid 40381641)
11. Furukawa M, He YJ, Borchers C, Xiong Y. (2003). Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat Cell Biol 5: 1001-1007. (Pubitemid 37406914)
12. Geyer R, Wee S, Anderson S, Yates J, Wolf DA. (2003). BTB/POZ domain proteins are putative substrate adaptors for cullin 3 ubiquitin ligases. Mol Cell 12: 783-790. (Pubitemid 37222497)
13. Glass CK, Rosenfeld MG. (2000). The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev 14: 121-141. (Pubitemid 30070977)
14. Goel A, Janknecht R. (2004). Concerted activation of ETS protein ER81 by p160 coactivators, the acetyltransferase p300 and the receptor tyrosine kinase HER2/Neu. J Biol Chem 279: 14909-14916. (Pubitemid 38618881)
15. Halachmi S, Marden E, Martin G, MacKay H, Abbondanza C, Brown M. (1994). Estrogen receptor-associated proteins: possible mediators of hormone-induced transcription. Science 264: 1455-1458.
16. Hernandez-Munoz I, Lund AH, van der Stoop P, Boutsma E, Muijrers I, Verhoeven E et al. (2005). Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc Natl Acad Sci USA 102: 7635-7640. (Pubitemid 40741023)
17. Hershko A, Ciechanover A. (1998). The ubiquitin system. Annu Rev Biochem 67: 425-479. (Pubitemid 28411135)
18. Hong H, Kohli K, Trivedi A, Johnson DL, Stallcup MR. (1996). GRIP1, a novel mouse protein that serves as a transcriptional coactivator in yeast for the hormone binding domains of steroid receptors. Proc Natl Acad Sci USA 93: 4948-4952. (Pubitemid 26163504)
19. Jin J, Ang XL, Shirogane T, Wade Harper J. (2005). Identification of substrates for F-box proteins. Methods Enzymol 399: 287-309. (Pubitemid 41781941)
20. Jin J, Cardozo T, Lovering RC, Elledge SJ, Pagano M, Harper JW. (2004). Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev 18: 2573-2580. (Pubitemid 39453096)
21. Kajiro M, Hirota R, Nakajima Y, Kawanowa K, So-ma K, Ito I et al. (2009). The ubiquitin ligase CHIP acts as an upstream regulator of oncogenic pathways. Nat Cell Biol 11: 312-319.
22. Kuang SQ, Liao L, Zhang H, Lee AV, O'Malley BW, Xu J. (2004). AIB1/SRC-3 deficiency affects insulin-like growth factor I signaling pathway and suppresses v-Ha-ras-induced breast cancer initiation and progression in mice. Cancer Res 64: 1875-1885. (Pubitemid 38428714)
23. Kumar RPD, O'Malley BW. (2008). NR Coregulators and Human Diseases. World Scientific: Singapore; London, xi, 602 p.
24. Kwon JE, La M, Oh KH, Oh YM, Kim GR, Seol JH et al. (2006). BTB domain-containing speckle-type POZ protein (SPOP) serves as an adaptor of Daxx for ubiquitination by Cul3-based ubiquitin ligase. J Biol Chem 281: 12664-12672. (Pubitemid 43855356)
25. Lee DF, Kuo HP, Liu M, Chou CK, Xia W, Du Y et al. (2009). KEAP1 E3 Ligase-mediated downregulation of NF-kappaB signaling by targeting IKKbeta. Mol Cell 36: 131-140.
26. Lee SK, Kim HJ, Na SY, Kim TS, Choi HS, Im SY et al. (1998). Steroid receptor coactivator-1 coactivates activating protein-1-mediated transactivations through interaction with the c-Jun and c-Fos subunits. J Biol Chem 273: 16651-16654. (Pubitemid 28311685)
27. Lerebours F, Bertheau P, Bieche I, Driouch K, De The H, Hacene K et al. (2002). Evidence of chromosome regions and gene involvement in inflammatory breast cancer. Int J Cancer 102: 618-622. (Pubitemid 35334470)
28. Li C, Liang YY, Feng XH, Tsai SY, Tsai MJ, O'Malley BW. (2008a). Essential phosphatases and a phospho-degron are critical for regulation of SRC-3/AIB1 coactivator function and turnover. Mol Cell 31: 835-849.
29. Li C, Wu RC, Amazit L, Tsai SY, Tsai MJ, O'Malley BW. (2007a). Specific amino acid residues in the basic helix-loop-helix domain of SRC-3 are essential for its nuclear localization and proteasome-dependent turnover. Mol Cell Biol 27: 1296-1308. (Pubitemid 46239813)
30. Li H, Gomes PJ, Chen JD. (1997). RAC3, a steroid/nuclear receptor-associated coactivator that is related to SRC-1 and TIF2. Proc Natl Acad Sci USA 94: 8479-8484. (Pubitemid 27335064)
31. Li LB, Louie MC, Chen HW, Zou JX. (2008b). Proto-oncogene ACTR/AIB1 promotes cancer cell invasion by up-regulating specific matrix metalloproteinase expression. Cancer Lett 261: 64-73.
32. Li X, Amazit L, Long W, Lonard DM, Monaco JJ, O'Malley BW. (2007b). Ubiquitin-and ATP-independent proteolytic turnover of p21 by the REGgamma-proteasome pathway. Mol Cell 26: 831-842. (Pubitemid 46921009)
33. Li X, Lonard DM, Jung SY, Malovannaya A, Feng Q, Qin J et al. (2006). The SRC-3/AIB1 coactivator is degraded in a ubiquitin-and ATP-independent manner by the REGgamma proteasome. Cell 124: 381-392. (Pubitemid 43121985)
34. Liu J, Ghanim M, Xue L, Brown CD, Iossifov I, Angeletti C et al. (2009). Analysis of Drosophila segmentation network identifies a JNK pathway factor overexpressed in kidney cancer. Science 323: 1218-1222.
35. Louie MC, Zou JX, Rabinovich A, Chen HW. (2004). ACTR/AIB1 functions as an E2F1 coactivator to promote breast cancer cell proliferation and antiestrogen resistance. Mol Cell Biol 24: 5157-5171. (Pubitemid 38738153)
36. Luo W, Peterson A, Garcia BA, Coombs G, Kofahl B, Heinrich R et al. (2007). Protein phosphatase 1 regulates assembly and function of the beta-catenin degradation complex. EMBO J 26: 1511-1521. (Pubitemid 46480933)
37. McKenna NJ, Lanz RB, O'Malley BW. (1999). Nuclear receptor coregulators: cellular and molecular biology. Endocr Rev 20: 321-344. (Pubitemid 30649811)
38. McKenna NJ, O'Malley BW. (2002). Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108: 465-474. (Pubitemid 34260872)
39. Michaelson JS, Bader D, Kuo F, Kozak C, Leder P. (1999). Loss of Daxx, a promiscuously interacting protein, results in extensive apoptosis in early mouse development. Genes Dev 13: 1918-1923. (Pubitemid 29407359)
40. O'Malley BW, Kumar R. (2009). Nuclear receptor coregulators in cancer biology. Cancer Res 69: 8217-8222.
41. Onate SA, Tsai SY, Tsai MJ, O'Malley BW. (1995). Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 270: 1354-1357.
42. Orsetti B, Courjal F, Cuny M, Rodriguez C, Theillet C. (1999). 17q21-q25 aberrations in breast cancer: combined allelotyping and CGH analysis reveals 5 regions of allelic imbalance among which two correspond to DNA amplification. Oncogene 18: 6262-6270.
43. Osborne CK, Bardou V, Hopp TA, Chamness GC, Hilsenbeck SG, Fuqua SA et al. (2003). Role of the estrogen receptor coactivator AIB1 (SRC-3) and HER-2/neu in tamoxifen resistance in breast cancer. J Natl Cancer Inst 95: 353-361. (Pubitemid 36395255)
44. Petroski MD, Deshaies RJ. (2005). Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6: 9-20. (Pubitemid 40064895)
45. Pickart CM. (2001). Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533. (Pubitemid 32663902)
46. Pintard L, Willis JH, Willems A, Johnson JL, Srayko M, Kurz T et al. (2003). The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425: 311-316. (Pubitemid 37158408)
47. Planas-Silva MD, Shang Y, Donaher JL, Brown M, Weinberg RA. (2001). AIB1 enhances estrogen-dependent induction of cyclin D1 expression. Cancer Res 61: 3858-3862. (Pubitemid 32720941)
48. Qin L, Liao L, Redmond A, Young L, Yuan Y, Chen H et al. (2008). The AIB1 oncogene promotes breast cancer metastasis by activation of PEA3-mediated matrix metalloproteinase 2 (MMP2) and MMP9 expression. Mol Cell Biol 28: 5937-5950.
49. Radford DM, Fair KL, Phillips NJ, Ritter JH, Steinbrueck T, Holt MS et al. (1995). Allelotyping of ductal carcinoma in situ of the breast: deletion of loci on 8p, 13q, 16q, 17p and 17q. Cancer Res 55: 3399-3405.
50. Rivers A, Gietzen KF, Vielhaber E, Virshup DM. (1998). Regulation of casein kinase I epsilon and casein kinase I delta by an in vivo futile phosphorylation cycle. J Biol Chem 273: 15980-15984. (Pubitemid 28311363)
51. Sakanaka C. (2002). Phosphorylation and regulation of beta-catenin by casein kinase I epsilon. J Biochem 132: 697-703. (Pubitemid 35408491)
52. Shirogane T, Jin J, Ang XL, Harper JW. (2005). SCFbeta-TRCP controls clock-dependent transcription via casein kinase 1-depen-dent degradation of the mammalian period-1 (Per1) protein. J Biol Chem 280: 26863-26872. (Pubitemid 41040720)
53. Takeshita A, Cardona GR, Koibuchi N, Suen CS, Chin WW. (1997). TRAM-1, a novel 160-kDa thyroid hormone receptor activator molecule, exhibits distinct properties from steroid receptor coacti-vator-1. J Biol Chem 272: 27629-27634. (Pubitemid 27473556)
54. Tang J, Qu LK, Zhang J, Wang W, Michaelson JS, Degenhardt YY et al. (2006). Critical role for Daxx in regulating Mdm2. Nat Cell Biol 8: 855-862. (Pubitemid 44151589)
55. Torchia J, Rose DW, Inostroza J, Kamei Y, Westin S, Glass CK et al. (1997). The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature 387: 677-684. (Pubitemid 27270601)
56. Torres-Arzayus MI, Font de Mora J, Yuan J, Vazquez F, Bronson R, Rue M et al. (2004). High tumor incidence and activation of the PI3K/AKT pathway in transgenic mice define AIB1 as an oncogene. Cancer Cell 6: 263-274. (Pubitemid 39222039)
57. Voegel JJ, Heine MJ, Zechel C, Chambon P, Gronemeyer H. (1996). TIF2, a 160 kDa transcriptional mediator for the ligand-dependent activation function AF-2 of nuclear receptors. EMBO J 15: 3667-3675. (Pubitemid 26239779)
58. Wang Z, Rose DW, Hermanson O, Liu F, Herman T, Wu W et al. (2000). Regulation of somatic growth by the p160 coactivator p/CIP. Proc Natl Acad Sci USA 97: 13549-13554.
59. Welcker M, Clurman BE. (2008). FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 8: 83-93. (Pubitemid 351161321)
60. Werbajh S, Nojek I, Lanz R, Costas MA. (2000). RAC-3 is a NF-kappa B coactivator. FEBS Lett 485: 195-199.
61. Wu RC, Feng Q, Lonard DM, O'Malley BW. (2007). SRC-3 coactivator functional lifetime is regulated by a phospho-dependent ubiquitin time clock. Cell 129: 1125-1140. (Pubitemid 46891039)
62. Xu J, Liao L, Ning G, Yoshida-Komiya H, Deng C, O'Malley BW. (2000). The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM-1) is required for normal growth, puberty, female reproductive function, and mammary gland development. Proc Natl Acad Sci USA 97: 6379-6384. (Pubitemid 30412722)
63. Xu L, Wei Y, Reboul J, Vaglio P, Shin TH, Vidal M et al. (2003). BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425: 316-321. (Pubitemid 37158409)
64. Yan J, Erdem H, Li R, Cai Y, Ayala G, Ittmann M et al. (2008). Steroid receptor coactivator-3/AIB1 promotes cell migration and invasiveness through focal adhesion turnover and matrix metallo-proteinase expression. Cancer Res 68: 5460-5468.
65. Yan J, Yu CT, Ozen M, Ittmann M, Tsai SY, Tsai MJ. (2006). Steroid receptor coactivator-3 and activator protein-1 coordinately regulate the transcription of components of the insulin-like growth factor/AKT signaling pathway. Cancer Res 66: 11039-11046. (Pubitemid 44877004)
66. Yi P, Feng Q, Amazit L, Lonard DM, Tsai SY, Tsai MJ et al. (2008). Atypical protein kinase C regulates dual pathways for degradation of the oncogenic coactivator SRC-3/AIB1. Mol Cell 29: 465-476. (Pubitemid 351291678)
67. Yu C, York B, Wang S, Feng Q, Xu J, O'Malley BW. (2007). An essential function of the SRC-3 coactivator in suppression of cytokine mRNA translation and inflammatory response. Mol Cell 25: 765-778. (Pubitemid 46341916)
68. Zhou G, Hashimoto Y, Kwak I, Tsai SY, Tsai MJ. (2003). Role of the steroid receptor coactivator SRC-3 in cell growth. Mol Cell Biol 23: 7742-7755. (Pubitemid 37271472)
69. Zhou HJ, Yan J, Luo W, Ayala G, Lin SH, Erdem H et al. (2005). SRC-3 is required for prostate cancer cell proliferation and survival. Cancer Res 65: 7976-7983. (Pubitemid 41297277)
70. Zhuang M, Calabrese MF, Liu J, Waddell MB, Nourse A, Hammel M et al. (2009). Structures of SPOP-substrate complexes: insights into molecular architectures of BTB-Cul3 ubiquitin ligases. Mol Cell 36: 39-50.