Ubiquitin-specific peptidase 22 functions and its involvement in disease

Oncotarget

Volumn 7, Issue 28, 2016, Pages 44848-44856

  Melo Cardenas, Johanna ^a   Zhang, Yusi ^a   Zhang, Donna D ^b   Fang, Deyu ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Ataxia; Cancer; Deubiquitylation; Oncogene; USP22

Indexed keywords

CYCLIN B1; CYCLOOXYGENASE 2; FAR UPSTREAM ELEMENT BINDING PROTEIN 1; MESSENGER RNA; MYC PROTEIN; PEPTIDES AND PROTEINS; REGULATOR OF CALCINEURIN 1; SIRTUIN 1; SUCROSE NONFERMENTING 1; TELOMERIC REPEAT BINDING FACTOR 1; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR NFAT; UBIQUITIN; UBIQUITIN SPECIFIC PEPTIDASE 22; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; THIOL ESTER HYDROLASE; USP22 PROTEIN, HUMAN;

ARTICLE; CELL CYCLE G0 PHASE; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME REGULATION; G1 PHASE CELL CYCLE CHECKPOINT; HISTONE METHYLATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; ANTAGONISTS AND INHIBITORS; CELL CYCLE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASM; NEUROLOGIC DISEASE; ONCOGENE; PROCEDURES; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; CELL CYCLE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS; NERVOUS SYSTEM DISEASES; ONCOGENES; SIGNAL TRANSDUCTION; THIOLESTER HYDROLASES;

EID: 84978730188     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8602     Document Type: Article

References (73)

1. Ciechanover A, Heller H, Elias S, Haas AL and Hershko A. ATP-dependent conjugation of reticulocyte proteins with the polypeptide required for protein degradation. Proc Natl Acad Sci U S A. 1980; 77:1365-1368.
2. Hershko A, Ciechanover A, Heller H, Haas AL and Rose IA. Proposed role of ATP in protein breakdown: conjugation of protein with multiple chains of the polypeptide of ATPdependent proteolysis. Proc Natl Acad Sci U S A. 1980; 77:1783-1786.
3. Glickman MH and Ciechanover A. The ubiquitinproteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev. 2002; 82:373-428.
4. Bach I and OstendorffHP. Orchestrating nuclear functions: ubiquitin sets the rhythm. Trends Biochem Sci. 2003; 28:189-195.
5. Tenno T, Fujiwara K, Tochio H, Iwai K, Morita EH, Hayashi H, Murata S, Hiroaki H, Sato M, Tanaka K and Shirakawa M. Structural basis for distinct roles of Lys63-and Lys48-linked polyubiquitin chains. Genes Cells. 2004; 9:865-875.
6. Tokunaga F, Sakata S, Saeki Y, Satomi Y, Kirisako T, Kamei K, Nakagawa T, Kato M, Murata S, Yamaoka S, Yamamoto M, Akira S, Takao T, Tanaka K and Iwai K. Involvement of linear polyubiquitylation of NEMO in NFkappaB activation. Nat Cell Biol. 2009; 11:123-132.
7. Reyes-Turcu FE, Ventii KH and Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem. 2009; 78:363-397.
8. Fraile JM, Quesada V, Rodriguez D, Freije JM and Lopez-Otin C. Deubiquitinases in cancer: new functions and therapeutic options. Oncogene. 2012; 31:2373-2388.
9. Kowalski JR and Juo P. The role of deubiquitinating enzymes in synaptic function and nervous system diseases. Neural Plast. 2012; 2012:892749.
10. Daniel JA and Grant PA. Multi-tasking on chromatin with the SAGA coactivator complexes. Mutat Res. 2007; 618:135-148.
11. Bonnet J, Romier C, Tora L and Devys D. Zinc-finger UBPs: regulators of deubiquitylation. Trends Biochem Sci. 2008; 33:369-375.
12. Kohler A, Zimmerman E, Schneider M, Hurt E and Zheng N. Structural basis for assembly and activation of the heterotetrameric SAGA histone H2B deubiquitinase module. Cell. 2010; 141:606-617.
13. Samara NL, Datta AB, Berndsen CE, Zhang X, Yao T, Cohen RE and Wolberger C. Structural insights into the assembly and function of the SAGA deubiquitinating module. Science. 2010; 328:1025-1029.
14. Koehler C, Bonnet J, Stierle M, Romier C, Devys D and Kieffer B. DNA binding by Sgf11 protein affects histone H2B deubiquitination by Spt-Ada-Gcn5-acetyltransferase (SAGA). J Biol Chem. 2014; 289:8989-8999.
15. Bonnet J, Wang YH, Spedale G, Atkinson RA, Romier C, Hamiche A, Pijnappel WW, Timmers HT, Tora L, Devys D and Kieffer B. The structural plasticity of SCA7 domains defines their differential nucleosome-binding properties. EMBO Rep. 2010; 11:612-618.
16. Lang G, Bonnet J, Umlauf D, Karmodiya K, Koffler J, Stierle M, Devys D and Tora L. The tightly controlled deubiquitination activity of the human SAGA complex differentially modifies distinct gene regulatory elements. Mol Cell Biol. 2011; 31:3734-3744.
17. Sowa ME, Bennett EJ, Gygi SP and Harper JW. Defining the human deubiquitinating enzyme interaction landscape. Cell. 2009; 138:389-403.
18. Gurskiy D, Orlova A, Vorobyeva N, Nabirochkina E, Krasnov A, Shidlovskii Y, Georgieva S and Kopytova D. The DUBm subunit Sgf11 is required for mRNA export and interacts with Cbp80 in Drosophila. Nucleic Acids Res. 2012; 40:10689-10700.
19. Lim S, Kwak J, Kim M and Lee D. Separation of a functional deubiquitylating module from the SAGA complex by the proteasome regulatory particle. Nat Commun. 2013; 4:2641.
20. Henry KW, Wyce A, Lo WS, Duggan LJ, Emre NC, Kao CF, Pillus L, Shilatifard A, Osley MA and Berger SL. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGAassociated Ubp8. Genes Dev. 2003; 17:2648-2663.
21. Henry KW and Berger SL. Trans-tail histone modifications: wedge or bridge? Nat Struct Biol. 2002; 9:565-566.
22. Wyce A, Xiao T, Whelan KA, Kosman C, Walter W, Eick D, Hughes TR, Krogan NJ, Strahl BD and Berger SL. H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGArelated complex. Mol Cell. 2007; 27:275-288.
23. Bonnet J, Wang CY, Baptista T, Vincent SD, Hsiao WC, Stierle M, Kao CF, Tora L and Devys D. The SAGA coactivator complex acts on the whole transcribed genome and is required for RNA polymerase II transcription. Genes Dev. 2014; 28:1999-2012.
24. Zhao Y, Lang G, Ito S, Bonnet J, Metzger E, Sawatsubashi S, Suzuki E, Le Guezennec X, Stunnenberg HG, Krasnov A, Georgieva SG, Schule R, Takeyama K, Kato S, Tora L and Devys D. A TFTC/STAGA module mediates histone H2A and H2B deubiquitination, coactivates nuclear receptors, and counteracts heterochromatin silencing. Mol Cell. 2008; 29:92-101.
25. Mao P, Meas R, Dorgan KM and Smerdon MJ. UV damage-induced RNA polymerase II stalling stimulates H2B deubiquitylation. Proc Natl Acad Sci U S A. 2014; 111:12811-12816.
26. Zhang XY, Pfeiffer HK, Thorne AW and McMahon SB. USP22, an hSAGA subunit and potential cancer stem cell marker, reverses the polycomb-catalyzed ubiquitylation of histone H2A. Cell Cycle. 2008; 7:1522-1524.
27. Muller J and Verrijzer P. Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr Opin Genet Dev. 2009; 19:150-158.
28. Poeck B, Fischer S, Gunning D, Zipursky SL and Salecker I. Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron. 2001; 29:99-113.
29. Atanassov BS, Evrard YA, Multani AS, Zhang Z, Tora L, Devys D, Chang S and Dent SY. Gcn5 and SAGA regulate shelterin protein turnover and telomere maintenance. Mol Cell. 2009; 35:352-364.
30. Lin Z, Yang H, Kong Q, Li J, Lee SM, Gao B, Dong H, Wei J, Song J, Zhang DD and Fang D. USP22 antagonizes p53 transcriptional activation by deubiquitinating Sirt1 to suppress cell apoptosis and is required for mouse embryonic development. Mol Cell. 2012; 46:484-494.
31. Li L, Osdal T, Ho Y, Chun S, McDonald T, Agarwal P, Lin A, Chu S, Qi J, Li L, Hsieh YT, Dos Santos C, Yuan H, Ha TQ, Popa M, Hovland R, et al. SIRT1 Activation by a c-MYC Oncogenic Network Promotes the Maintenance and Drug Resistance of Human FLT3-ITD Acute Myeloid Leukemia Stem Cells. Cell stem cell. 2014; 15:431-446.
32. Lin Z, Tan C, Qiu Q, Kong S, Yang H, Zhao F, Liu Z, Li J, Kong Q, Gao B, Barrett T, Yang GY, Zhang J and Fang D. Ubiquitin-specific protease 22 is a deubiquitinase of CCNB1. Cell Discovery. 2015; 1.
33. Atanassov BS and Dent SY. USP22 regulates cell proliferation by deubiquitinating the transcriptional regulator FBP1. EMBO Rep. 2011; 12:924-930.
34. Kobayashi T, Iwamoto Y, Takashima K, Isomura A, Kosodo Y, Kawakami K, Nishioka T, Kaibuchi K and Kageyama R. Deubiquitinating enzymes regulate Hes1 stability and neuronal differentiation. FEBS J. 2015; 282:2411-2423.
35. Hong A, Lee JE and Chung KC. Ubiquitin-specific protease 22 (USP22) positively regulates RCAN1 protein levels through RCAN1 de-ubiquitination. J Cell Physiol. 2015; 230:1651-1660.
36. Gao Y, Lin F, Xu P, Nie J, Chen Z, Su J, Tang J, Wu Q, Li Y, Guo Z, Gao Z, Li D, Shen J, Ge S, Tsun A and Li B. USP22 is a positive regulator of NFATc2 on promoting IL2 expression. FEBS letters. 2014; 588:878-883.
37. Xiao H, Tian Y, Yang Y, Hu F, Xie X, Mei J and Ding F. USP22 acts as an oncogene by regulating the stability of cyclooxygenase-2 in non-small cell lung cancer. Biochemical and biophysical research communications. 2015; 460:703-708.
38. Wilson MA, Koutelou E, Hirsch C, Akdemir K, Schibler A, Barton MC and Dent SY. Ubp8 and SAGA regulate Snf1 AMP kinase activity. Mol Cell Biol. 2011; 31:3126-3135.
39. Chipumuro E and Henriksen MA. The ubiquitin hydrolase USP22 contributes to 3'-end processing of JAK-STATinducible genes. FASEB J. 2012; 26:842-854.
40. Schrecengost RS, Dean JL, Goodwin JF, Schiewer MJ, Urban MW, Stanek TJ, Sussman RT, Hicks JL, Birbe RC, Draganova-Tacheva RA, Visakorpi T, Demarzo AM, McMahon SB and Knudsen KE. USP22 Regulates Oncogenic Signaling Pathways to Drive Lethal Cancer Progression. Cancer Res. 2014; 74:272-286.
41. Xiong J, Zhou X, Gong Z, Wang T, Zhang C, Xu X, Liu J and Li W. PKA/CREB regulates the constitutive promoter activity of the USP22 gene. Oncol Rep. 2015; 33:1505-1511.
42. Xiong J, Che X, Li X, Yu H, Gong Z and Li W. Cloning and characterization of the human USP22 gene promoter. PLoS One. 2012; 7:e52716.
43. Armour SM, Bennett EJ, Braun CR, Zhang XY, McMahon SB, Gygi SP, Harper JW and Sinclair DA. A highconfidence interaction map identifies SIRT1 as a mediator of acetylation of USP22 and the SAGA coactivator complex. Mol Cell Biol. 2013; 33:1487-1502.
44. McCormick MA, Mason AG, Guyenet SJ, Dang W, Garza RM, Ting MK, Moller RM, Berger SL, Kaeberlein M, Pillus L, La Spada AR and Kennedy BK. The SAGA histone deubiquitinase module controls yeast replicative lifespan via Sir2 interaction. Cell Rep. 2014; 8:477-486.
45. Daniel JA, Torok MS, Sun ZW, Schieltz D, Allis CD, Yates JR, 3rd and Grant PA. Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J Biol Chem. 2004; 279:1867-1871.
46. Game JC, Birrell GW, Brown JA, Shibata T, Baccari C, Chu AM, Williamson MS and Brown JM. Use of a genomewide approach to identify new genes that control resistance of Saccharomyces cerevisiae to ionizing radiation. Radiat Res. 2003; 160:14-24.
47. Ratnakumar S, Hesketh A, Gkargkas K, Wilson M, Rash BM, Hayes A, Tunnacliffe A and Oliver SG. Phenomic and transcriptomic analyses reveal that autophagy plays a major role in desiccation tolerance in Saccharomyces cerevisiae. Mol Biosyst. 2011; 7:139-149.
48. Weake VM, Lee KK, Guelman S, Lin CH, Seidel C, Abmayr SM and Workman JL. SAGA-mediated H2B deubiquitination controls the development of neuronal connectivity in the Drosophila visual system. EMBO J. 2008; 27:394-405.
49. Weake VM, Dyer JO, Seidel C, Box A, Swanson SK, Peak A, Florens L, Washburn MP, Abmayr SM and Workman JL. Post-transcription initiation function of the ubiquitous SAGA complex in tissue-specific gene activation. Genes Dev. 2011; 25:1499-1509.
50. Lee HJ, Kim MS, Shin JM, Park TJ, Chung HM and Baek KH. The expression patterns of deubiquitinating enzymes, USP22 and Usp22. Gene Expr Patterns. 2006; 6:277-284.
51. Kosinsky RL, Wegwitz F, Hellbach N, Dobbelstein M, Mansouri A, Vogel T, Begus-Nahrmann Y and Johnsen SA. Usp22 deficiency impairs intestinal epithelial lineage specification in vivo. Oncotarget. 2015; 6:37906-18. doi: 10.18632/oncotarget.5412.
52. Sussman RT, Stanek TJ, Esteso P, Gearhart JD, Knudsen KE and McMahon SB. The epigenetic modifier ubiquitinspecific protease 22 (USP22) regulates embryonic stem cell differentiation via transcriptional repression of sexdetermining region Y-box 2 (SOX2). J Biol Chem. 2013; 288:24234-24246.
53. Kobayashi T, Iwamoto Y, Takashima K, Isomura A, Kosodo Y, Kawakami K, Nishioka T, Kaibuchi K and Kageyama R. Deubiquitinating enzymes regulate Hes1 stability and neuronal differentiation. FEBS J. 2015; 282:2475-2487.
54. Glinsky GV, Berezovska O and Glinskii AB. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest. 2005; 115:1503-1521.
55. Piao S, Liu Y, Hu J, Guo F, Ma J, Sun Y and Zhang B. USP22 is useful as a novel molecular marker for predicting disease progression and patient prognosis of oral squamous cell carcinoma. PLoS One. 2012; 7:e42540.
56. Tang B, Tang F, Li B, Yuan S, Xu Q, Tomlinson S, Jin J, Hu W and He S. High USP22 expression indicates poor prognosis in hepatocellular carcinoma. Oncotarget. 2015; 6:12654-12667. doi: 10.18632/oncotarget.3705.
57. Hu J, Liu YL, Piao SL, Yang DD, Yang YM and Cai L. Expression patterns of USP22 and potential targets BMI-1, PTEN, p-AKT in non-small-cell lung cancer. Lung Cancer. 2012; 77:593-599.
58. Yang M, Liu YD, Wang YY, Liu TB, Ge TT and Lou G. Ubiquitin-specific protease 22: a novel molecular biomarker in cervical cancer prognosis and therapeutics. Tumour Biol. 2014; 35:929-34.
59. Zhang XY, Varthi M, Sykes SM, Phillips C, Warzecha C, Zhu W, Wyce A, Thorne AW, Berger SL and McMahon SB. The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. Mol Cell. 2008; 29:102-111.
60. Lv L, Xiao XY, Gu ZH, Zeng FQ, Huang LQ and Jiang GS. Silencing USP22 by asymmetric structure of interfering RNA inhibits proliferation and induces cell cycle arrest in bladder cancer cells. Mol Cell Biochem. 2011; 346:11-21.
61. Xu K, Shimelis H, Linn DE, Jiang R, Yang X, Sun F, Guo Z, Chen H, Li W, Kong X, Melamed J, Fang S, Xiao Z, Veenstra TD and Qiu Y. Regulation of androgen receptor transcriptional activity and specificity by RNF6-induced ubiquitination. Cancer Cell. 2009; 15:270-282.
62. David G, Abbas N, Stevanin G, Durr A, Yvert G, Cancel G, Weber C, Imbert G, Saudou F, Antoniou E, Drabkin H, Gemmill R, Giunti P, Benomar A, Wood N, Ruberg M, et al. Cloning of the SCA7 gene reveals a highly unstable CAG repeat expansion. Nat Genet. 1997; 17:65-70.
63. Palhan VB, Chen S, Peng GH, Tjernberg A, Gamper AM, Fan Y, Chait BT, La Spada AR and Roeder RG. Polyglutamine-expanded ataxin-7 inhibits STAGA histone acetyltransferase activity to produce retinal degeneration. Proc Natl Acad Sci U S A. 2005; 102:8472-8477.
64. Burke TL, Miller JL and Grant PA. Direct inhibition of Gcn5 protein catalytic activity by polyglutamine-expanded ataxin-7. J Biol Chem. 2013; 288:34266-34275.
65. Helmlinger D, Hardy S, Abou-Sleymane G, Eberlin A, Bowman AB, Gansmuller A, Picaud S, Zoghbi HY, Trottier Y, Tora L and Devys D. Glutamine-expanded ataxin-7 alters TFTC/STAGA recruitment and chromatin structure leading to photoreceptor dysfunction. PLoS Biol. 2006; 4:e67.
66. McMahon SJ, Pray-Grant MG, Schieltz D, Yates JR, 3rd and Grant PA. Polyglutamine-expanded spinocerebellar ataxia-7 protein disrupts normal SAGA and SLIK histone acetyltransferase activity. Proc Natl Acad Sci U S A. 2005; 102:8478-8482.
67. McCullough SD, Xu X, Dent SY, Bekiranov S, Roeder RG and Grant PA. Reelin is a target of polyglutamine expanded ataxin-7 in human spinocerebellar ataxia type 7 (SCA7) astrocytes. Proc Natl Acad Sci U S A. 2012; 109:21319-21324.
68. Lan X, Koutelou E, Schibler AC, Chen YC, Grant PA and Dent SY. Poly(Q) Expansions in ATXN7 Affect Solubility but Not Activity of the SAGA Deubiquitinating Module. Mol Cell Biol. 2015; 35:1777-1787.
69. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, Jia M, Shepherd R, Leung K, Menzies A, Teague JW, Campbell PJ, Stratton MR and Futreal PA. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 2011; 39:D945-950.
70. Sippl W, Collura V and Colland F. Ubiquitin-specific proteases as cancer drug targets. Future Oncol. 2011; 7:619-632.
71. Bedford L, Lowe J, Dick LR, Mayer RJ and Brownell JE. Ubiquitin-like protein conjugation and the ubiquitinproteasome system as drug targets. Nat Rev Drug Discov. 2011; 10:29-46.
72. Chauhan D, Tian Z, Nicholson B, Kumar KG, Zhou B, Carrasco R, McDermott JL, Leach CA, Fulcinniti M, Kodrasov MP, Weinstock J, Kingsbury WD, Hideshima T, Shah PK, Minvielle S, Altun M, et al. A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes bortezomib resistance. Cancer Cell. 2012; 22:345-358.
73. Wang F, Stanek TR, Biswas L, Kodrasov M, LaRocque J, Wu J, Sterner D, Weinstock J, Mattern M, McMahon SB and Kumar S. Abstract 5432: Discovery and characterization of USP22 inhibitors as novel anti-cancer agents. Proceedings: AACR 106th Annual Meeting 2015. 2015.