Identification of acetylation-dependent regulatory mechanisms that govern the oncogenic functions of Skp2

Oncotarget

Volumn 3, Issue 11, 2012, Pages 1294-1300

  Wang, Zhiwei ^a   Inuzuka, Hiroyuki ^a   Zhong, Jiateng ^a,b   Liu, Pengda ^a   Sarkar, Fazlul H ^c   Sun, Yi ^d   Wei, Wenyi ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Basic Medical College   (China)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Acetylation; Cancer; Deacetylation; F box protein; Oncoprotein; Phosphorylation; SIRT3; Skp2; Therapy; Ubiquitination

Indexed keywords

CULLIN; CULLIN1; CYCLIN DEPENDENT KINASE INHIBITOR 1C; E1A ASSOCIATED P300 PROTEIN; F BOX PROTEIN; LYSINE; MYC PROTEIN; PEPTIDES AND PROTEINS; PROTEIN P21; PROTEIN P27; PROTEIN RBX1; PROTEIN TOB1; S PHASE KINASE ASSOCIATED PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 1; S PHASE KINASE ASSOCIATED PROTEIN 2; SIRTUIN 3; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; UVOMORULIN;

ACETYLATION; ARTICLE; BREAST TUMOR; CARCINOGENICITY; CELL MIGRATION; DEACETYLATION; HUMAN; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84872812301     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.740     Document Type: Article

References (63)

1. Frescas D and Pagano M. Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat Rev Cancer. 2008; 8(6):438-449.
2. Shi L, Wang S, Zangari M, Xu H, Cao TM, Xu C, Wu Y, Xiao F, Liu Y, Yang Y, Salama M, Li G, Tricot G and Zhan F. Over-expression of CKS1B activates both MEK/ERK and JAK/STAT3 signaling pathways and promotes myeloma cell drug-resistance. Oncotarget. 2010; 1(1):22-33.
3. Wang Z, Gao D, Fukushima H, Inuzuka H, Liu P, Wan L, Sarkar FH and Wei W. Skp2: a novel potential therapeutic target for prostate cancer. Biochim Biophys Acta. 2012; 1825(1):11-17.
4. Carrano AC, Eytan E, Hershko A and Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol. 1999; 1(4):193-199.
5. Sutterluty H, Chatelain E, Marti A, Wirbelauer C, Senften M, Muller U and Krek W. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol. 1999; 1(4):207-214.
6. Jonason JH, Gavrilova N, Wu M, Zhang H and Sun H. Regulation of SCF(SKP2) ubiquitin E3 ligase assembly and p27(KIP1) proteolysis by the PTEN pathway and cyclin D1. Cell Cycle. 2007; 6(8):951-961.
7. Zhang H. Skip the nucleus, AKT drives Skp2 and FOXO1 to the same place? Cell Cycle. 2010; 9(5):868-869.
8. Wang H, Cui J, Bauzon F and Zhu L. A comparison between Skp2 and FOXO1 for their cytoplasmic localization by Akt1. Cell Cycle. 2010; 9(5):1021-1022.
9. Huang H, Regan KM, Wang F, Wang D, Smith DI, van Deursen JM and Tindall DJ. Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci U S A. 2005; 102(5):1649-1654.
10. von der Lehr N, Johansson S and Larsson LG. Implication of the ubiquitin/proteasome system in Myc-regulated transcription. Cell Cycle. 2003; 2(5):403-407.
11. Cardozo T and Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol. 2004; 5(9):739-751.
12. Lim MS, Adamson A, Lin Z, Perez-Ordonez B, Jordan RC, Tripp S, Perkins SL and Elenitoba-Johnson KS. Expression of Skp2, a p27(Kip1) ubiquitin ligase, in malignant lymphoma: correlation with p27(Kip1) and proliferation index. Blood. 2002; 100(8):2950-2956.
13. Yang G, Ayala G, De Marzo A, Tian W, Frolov A, Wheeler TM, Thompson TC and Harper JW. Elevated Skp2 protein expression in human prostate cancer: association with loss of the cyclin-dependent kinase inhibitor p27 and PTEN and with reduced recurrence-free survival. Clin Cancer Res. 2002; 8(11):3419-3426.
14. Rose AE, Wang G, Hanniford D, Monni S, Tu T, Shapiro RL, Berman RS, Pavlick AC, Pagano M, Darvishian F, Mazumdar M, Hernando E and Osman I. Clinical relevance of SKP2 alterations in metastatic melanoma. Pigment Cell Melanoma Res. 2011; 24(1):197-206.
15. Xu HM, Liang Y, Chen Q, Wu QN, Guo YM, Shen GP, Zhang RH, He ZW, Zeng YX, Xie FY and Kang TB. Correlation of Skp2 overexpression to prognosis of patients with nasopharyngeal carcinoma from South China. Chin J Cancer. 2011; 30(3):204-212.
16. Schuler S, Diersch S, Hamacher R, Schmid RM, Saur D and Schneider G. SKP2 confers resistance of pancreatic cancer cells towards TRAIL-induced apoptosis. Int J Oncol. 2011; 38(1):219-225.
17. Radke S, Pirkmaier A and Germain D. Differential expression of the F-box proteins Skp2 and Skp2B in breast cancer. Oncogene. 2005; 24(21):3448-3458.
18. Zheng WQ, Zheng JM, Ma R, Meng FF and Ni CR. Relationship between levels of Skp2 and P27 in breast carcinomas and possible role of Skp2 as targeted therapy. Steroids. 2005; 70(11):770-774.
19. Lin HK, Chen Z, Wang G, Nardella C, Lee SW, Chan CH, Yang WL, Wang J, Egia A, Nakayama KI, Cordon-Cardo C, Teruya-Feldstein J and Pandolfi PP. Skp2 targeting suppresses tumorigenesis by Arf-p53-independent cellular senescence. Nature. 2010; 464(7287):374-379.
20. van Duijn PW and Trapman J. PI3K/Akt signaling regulates p27(kip1) expression via Skp2 in PC3 and DU145 prostate cancer cells, but is not a major factor in p27(kip1) regulation in LNCaP and PC346 cells. Prostate. 2006; 66(7):749-760.
21. Chuu CP, Kokontis JM, Hiipakka RA, Fukuchi J, Lin HP, Lin CY, Huo C, Su LC and Liao S. Androgen Suppresses Proliferation of Castration-Resistant LNCaP 104-R2 Prostate Cancer Cells via Androgen Receptor, Skp2, and c-Myc. Cancer Sci. 2011.
22. Wang S, Raven JF and Koromilas AE. STAT1 represses Skp2 gene transcription to promote p27Kip1 stabilization in Ras-transformed cells. Mol Cancer Res. 2010; 8(5):798-805.
23. Lin HK, Wang G, Chen Z, Teruya-Feldstein J, Liu Y, Chan CH, Yang WL, Erdjument-Bromage H, Nakayama KI, Nimer S, Tempst P and Pandolfi PP. Phosphorylation-dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB. Nat Cell Biol. 2009; 11(4):420-432.
24. Gao D, Inuzuka H, Tseng A, Chin RY, Toker A and Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat Cell Biol. 2009; 11(4):397-408.
25. Iyer NG, Ozdag H and Caldas C. p300/CBP and cancer. Oncogene. 2004; 23(24):4225-4231.
26. Yang XJ. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 2004; 32(3):959-976.
27. Huang WC and Chen CC. Akt phosphorylation of p300 at Ser-1834 is essential for its histone acetyltransferase and transcriptional activity. Mol Cell Biol. 2005; 25(15):6592-6602.
28. Kitagawa M, Lee SH and McCormick F. Skp2 suppresses p53-dependent apoptosis by inhibiting p300. Mol Cell. 2008; 29(2):217-231.
29. Inuzuka H, Gao D, Finley LW, Yang W, Wan L, Fukushima H, Chin YR, Zhai B, Shaik S, Lau AW, Wang Z, Gygi SP, Nakayama K, Teruya-Feldstein J, Toker A, Haigis MC, et al. Acetylation-dependent regulation of Skp2 function. Cell. 2012; 150(1):179-193.
30. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV and Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 2009; 325(5942):834-840.
31. Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T, Yao J, Zhou L, Zeng Y, Li H, Li Y, Shi J, An W, Hancock SM, He F, Qin L, et al. Regulation of cellular metabolism by protein lysine acetylation. Science. 2010; 327(5968):1000-1004.
32. Haigis MC and Sinclair DA. Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol. 2010; 5:253-295.
33. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004; 303(5666):2011-2015.
34. Motta MC, Divecha N, Lemieux M, Kamel C, Chen D, Gu W, Bultsma Y, McBurney M and Guarente L. Mammalian SIRT1 represses forkhead transcription factors. Cell. 2004; 116(4):551-563.
35. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, Leid M, McBurney MW and Guarente L. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature. 2004; 429(6993):771-776.
36. Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, Pandita TK, Guarente L and Weinberg RA. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell. 2001; 107(2):149-159.
37. Chen W. Accelerating cancer evolution: a dark side of SIRT1 in genome maintenance. Oncotarget. 2012; 3(4):363-364.
38. Herranz D, Iglesias G, Munoz-Martin M and Serrano M. Limited role of Sirt1 in cancer protection by dietary restriction. Cell Cycle. 2011; 10(13):2215-2217.
39. Inoue T, Hiratsuka M, Osaki M and Oshimura M. The molecular biology of mammalian SIRT proteins: SIRT2 in cell cycle regulation. Cell Cycle. 2007; 6(9):1011-1018.
40. Inoue T, Nakayama Y, Yamada H, Li YC, Yamaguchi S, Osaki M, Kurimasa A, Hiratsuka M, Katoh M and Oshimura M. SIRT2 downregulation confers resistance to microtubule inhibitors by prolonging chronic mitotic arrest. Cell Cycle. 2009; 8(8):1279-1291.
41. Sundaresan NR, Samant SA, Pillai VB, Rajamohan SB and Gupta MP. SIRT3 is a stress-responsive deacetylase in cardiomyocytes that protects cells from stress-mediated cell death by deacetylation of Ku70. Mol Cell Biol. 2008;28(20):6384-6401.
42. Scher MB, Vaquero A and Reinberg D. SirT3 is a nuclear NAD+-dependent histone deacetylase that translocates to the mitochondria upon cellular stress. Genes Dev. 2007; 21(8):920-928.
43. Haigis MC, Mostoslavsky R, Haigis KM, Fahie K, Christodoulou DC, Murphy AJ, Valenzuela DM, Yancopoulos GD, Karow M, Blander G, Wolberger C, Prolla TA, Weindruch R, Alt FW and Guarente L. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell. 2006; 126(5):941-954.
44. Jordan NV, Johnson GL and Abell AN. Tracking the intermediate stages of epithelial-mesenchymal transition in epithelial stem cells and cancer. Cell Cycle. 2011; 10(17):2865-2873.
45. Finley LW, Carracedo A, Lee J, Souza A, Egia A, Zhang J, Teruya-Feldstein J, Moreira PI, Cardoso SM, Clish CB, Pandolfi PP and Haigis MC. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell. 2011; 19(3):416-428.
46. Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, Pennington JD, van der Meer R, Nguyen P, Savage J, Owens KM, Vassilopoulos A, Ozden O, Park SH, Singh KK, Abdulkadir SA, Spitz DR, et al. SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell. 2010; 17(1):41-52.
47. Lindemann RK, Gabrielli B and Johnstone RW. Histone-deacetylase inhibitors for the treatment of cancer. Cell Cycle. 2004; 3(6):779-788.
48. Santos-Rosa H, Valls E, Kouzarides T and Martinez-Balbas M. Mechanisms of P/CAF auto-acetylation. Nucleic Acids Res. 2003; 31(15):4285-4292.
49. Dietschy T, Shevelev I, Pena-Diaz J, Huhn D, Kuenzle S, Mak R, Miah MF, Hess D, Fey M, Hottiger MO, Janscak P and Stagljar I. p300-mediated acetylation of the Rothmund-Thomson-syndrome gene product RECQL4 regulates its subcellular localization. J Cell Sci. 2009; 122(Pt 8):1258-1267.
50. Faiola F, Wu YT, Pan S, Zhang K, Farina A and Martinez E. Max is acetylated by p300 at several nuclear localization residues. Biochem J. 2007; 403(3):397-407.
51. di Bari MG, Ciuffini L, Mingardi M, Testi R, Soddu S and Barila D. c-Abl acetylation by histone acetyltransferases regulates its nuclear-cytoplasmic localization. EMBO Rep. 2006; 7(7):727-733.
52. Drobnjak M, Melamed J, Taneja S, Melzer K, Wieczorek R, Levinson B, Zeleniuch-Jacquotte A, Polsky D, Ferrara J, Perez-Soler R, Cordon-Cardo C, Pagano M and Osman I. Altered expression of p27 and Skp2 proteins in prostate cancer of African-American patients. Clin Cancer Res. 2003; 9(7):2613-2619.
53. Dowen SE, Scott A, Mukherjee G and Stanley MA. Overexpression of Skp2 in carcinoma of the cervix does not correlate inversely with p27 expression. Int J Cancer. 2003; 105(3):326-330.
54. Signoretti S, Di Marcotullio L, Richardson A, Ramaswamy S, Isaac B, Rue M, Monti F, Loda M and Pagano M. Oncogenic role of the ubiquitin ligase subunit Skp2 in human breast cancer. J Clin Invest. 2002; 110(5):633-641.
55. Traub F, Mengel M, Luck HJ, Kreipe HH and von Wasielewski R. Prognostic impact of Skp2 and p27 in human breast cancer. Breast Cancer Res Treat. 2006; 99(2):185-191.
56. Yokoi S, Yasui K, Mori M, Iizasa T, Fujisawa T and Inazawa J. Amplification and overexpression of SKP2 are associated with metastasis of non-small-cell lung cancers to lymph nodes. Am J Pathol. 2004; 165(1):175-180.
57. Li JQ, Wu F, Masaki T, Kubo A, Fujita J, Dixon DA, Beauchamp RD, Ishida T, Kuriyama S and Imaida K. Correlation of Skp2 with carcinogenesis, invasion, metastasis, and prognosis in colorectal tumors. Int J Oncol. 2004; 25(1):87-95.
58. Thiery JP, Acloque H, Huang RY and Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009; 139(5):871-890.
59. Grego-Bessa J, Diez J, Timmerman L and de la Pompa JL. Notch and epithelial-mesenchyme transition in development and tumor progression: another turn of the screw. Cell Cycle. 2004; 3(6):718-721.
60. Gregory PA, Bracken CP, Bert AG and Goodall GJ. MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle. 2008; 7(20):3112-3118.
61. Schmalhofer O, Brabletz S and Brabletz T. E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev. 2009; 28(1-2):151-166.
62. Giehl K and Menke A. Microenvironmental regulation of E-cadherin-mediated adherens junctions. Front Biosci. 2008; 13:3975-3985.
63. Huber MA, Kraut N and Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol. 2005; 17(5):548-558.