The potential role of ubiquitin c-terminal hydrolases in oncogenesis

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1806, Issue 1, 2010, Pages 1-6

  Fang, Ying ^a   Fu, Da ^a   Shen, Xi Zhong ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

DUBs; Oncogenesis; UCHs

Indexed keywords

BRCA1 ASSOCIATED PROTEIN 1; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN THIOLESTERASE; UBIQUITIN THIOLESTERASE 37; UBIQUITIN THIOLESTERASE L1; UBIQUITIN THIOLESTERASE L3; UNCLASSIFIED DRUG;

APOPTOSIS; CANCER GROWTH; CANCER INHIBITION; CANCER INVASION; CARCINOGENESIS; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; HUMAN; METASTASIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; TUMOR RECURRENCE; UBIQUITINATION; UPREGULATION;

ANIMALS; CARBOXYPEPTIDASES; CYSTEINE ENDOPEPTIDASES; HUMANS; NEOPLASMS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN THIOLESTERASE;

EID: 77953694906     PISSN: 0304419X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbcan.2010.03.001     Document Type: Review

References (70)

1. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67:425-479.
2. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
3. Finley D., Ciechanover A., Varshavsky A. Ubiquitin as a central cellular regulator. Cell 2004, 116(Suppl. 2):S29-S32. 2p following S32.
4. Sridhar V.V., Kapoor A., Zhang K., Zhu J., Zhou T., Hasegawa P.M., Bressan R.A., Zhu J.K. Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 2007, 477:735-738.
5. Liu H., Buus R., Clague M.J., Urbe S. Regulation of ErbB2 receptor status by the proteasomal DUB POH1. PLoS ONE 2009, 4:e5544.
6. Singhal S., Taylor M.C., Baker R.T. Deubiquitylating enzymes and disease. BMC Biochem. 2008, 9(Suppl. 1):S3.
7. Amerik A.Y., Hochstrasser M. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 2004, 1695:189-207.
8. Soboleva T.A., Baker R.T. Deubiquitinating enzymes: their functions and substrate specificity. Curr. Protein Pept. Sci. 2004, 5:191-200.
9. Nijman S.M., Luna-Vargas M.P., Velds A., Brummelkamp T.R., Dirac A.M., Sixma T.K., Bernards R. A genomic and functional inventory of deubiquitinating enzymes. Cell 2005, 123:773-786.
10. Yao T., Song L., Xu W., DeMartino G.N., Florens L., Swanson S.K., Washburn M.P., Conaway R.C., Conaway J.W., Cohen R.E. Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat. Cell Biol. 2006, 8:994-1002.
11. Jensen D.E., Proctor M., Marquis S.T., Gardner H.P., Ha S.I., Chodosh L.A., Ishov A.M., Tommerup N., Vissing H., Sekido Y., Minna J., Borodovsky A., Schultz D.C., Wilkinson K.D., Maul G.G., Barlev N., Berger S.L., Prendergast G.C., Rauscher F.J. BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 1998, 16:1097-1112.
12. Das C., Hoang Q.Q., Kreinbring C.A., Luchansky S.J., Meray R.K., Ray S.S., Lansbury P.T., Ringe D., Petsko G.A. Structural basis for conformational plasticity of the Parkinson's disease-associated ubiquitin hydrolase UCH-L1. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4675-4680.
13. Johnston S.C., Larsen C.N., Cook W.J., Wilkinson K.D., Hill C.P. Crystal structure of a deubiquitinating enzyme (human UCH-L3) at 1.8 A resolution. EMBO J. 1997, 16:3787-3796.
14. Nishio K., Kim S.W., Kawai K., Mizushima T., Yamane T., Hamazaki J., Murata S., Tanaka K., Morimoto Y. Crystal structure of the de-ubiquitinating enzyme UCH37 (human UCH-L5) catalytic domain. Biochem. Biophys. Res. Commun. 2009, 390:855-860.
15. Larsen C.N., Krantz B.A., Wilkinson K.D. Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases. Biochemistry 1998, 37:3358-3368.
16. Leroy E., Boyer R., Auburger G., Leube B., Ulm G., Mezey E., Harta G., Brownstein M.J., Jonnalagada S., Chernova T., Dehejia A., Lavedan C., Gasser T., Steinbach P.J., Wilkinson K.D., Polymeropoulos M.H. The ubiquitin pathway in Parkinson's disease. Nature 1998, 395:451-452.
17. Liu Y., Fallon L., Lashuel H.A., Liu Z., Lansbury P.T. The UCH-L1 gene encodes two opposing enzymatic activities that affect α-synuclein degradation and Parkinson's disease susceptibility. Cell 2002, 111:209-218.
18. Osaka H., Wang Y.L., Takada K., Takizawa S., Setsuie R., Li H., Sato Y., Nishikawa K., Sun Y.J., Sakurai M., Harada T., Hara Y., Kimura I., Chiba S., Namikawa K., Kiyama H., Noda M., Aoki S., Wada K. Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron. Hum. Mol. Genet. 2003, 12:1945-1958.
19. Setsuie R., Wada K. The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochem. Int. 2007, 51:105-111.
20. Choi J., Levey A.I., Weintraub S.T., Rees H.D., Gearing M., Chin L.S., Li L. Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J. Biol. Chem. 2004, 279:13256-13264.
21. Gong B., Cao Z., Zheng P., Vitolo O.V., Liu S., Staniszewski A., Moolman D., Zhang H., Shelanski M., Arancio O. Ubiquitin hydrolase Uch-L1 rescues β-amyloid-induced decreases in synaptic function and contextual memory. Cell 2006, 126:775-788.
22. Son O.L., Kim H.T., Ji M.H., Yoo K.W., Rhee M., Kim C.H. Cloning and expression analysis of a Parkinson's disease gene, Uch-L1, and its promoter in zebrafish. Biochem. Biophys. Res. Commun. 2003, 312:601-607.
23. Setsuie R., Wang Y.L., Mochizuki H., Osaka H., Hayakawa H., Ichihara N., Li H., Furuta A., Sano Y., Sun Y.J., Kwon J., Kabuta T., Yoshimi K., Aoki S., Mizuno Y., Noda M., Wada K. Dopaminergic neuronal loss in transgenic mice expressing the Parkinson's disease-associated UCH-L1 I93M mutant. Neurochem. Int. 2007, 50:119-129.
24. Tan E.K., Puong K.Y., Fook-Chong S., Chua E., Shen H., Yuen Y., Pavanni R., Wong M.C., Puvan K., Zhao Y. Case-control study of UCHL1 S18Y variant in Parkinson's disease. Mov. Disord. 2006, 21:1765-1768.
25. Carmine Belin A., Westerlund M., Bergman O., Nissbrandt H., Lind C., Sydow O., Galter D. S18Y in ubiquitin carboxy-terminal hydrolase L1 (UCH-L1) associated with decreased risk of Parkinson's disease in Sweden. Parkinsonism Relat. Disord. 2007, 13:295-298.
26. Meray R.K., Lansbury P.T. Reversible monoubiquitination regulates the Parkinson's disease-associated ubiquitin hydrolase UCH-L1. J. Biol. Chem. 2007, 282:10567-10575.
27. Hemelaar J., Borodovsky A., Kessler B.M., Reverter D., Cook J., Kolli N., Gan-Erdene T., Wilkinson K.D., Gill G., Lima C.D., Ploegh H.L., Ovaa H. Specific and covalent targeting of conjugating and deconjugating enzymes of ubiquitin-like proteins. Mol. Cell. Biol. 2004, 24:84-95.
28. Frickel E.M., Quesada V., Muething L., Gubbels M.J., Spooner E., Ploegh H., Artavanis-Tsakonas K. Apicomplexan UCHL3 retains dual specificity for ubiquitin and Nedd8 throughout evolution. Cell. Microbiol. 2007, 9:1601-1610.
29. Setsuie R., Sakurai M., Sakaguchi Y., Wada K. Ubiquitin dimers control the hydrolase activity of UCH-L3. Neurochem. Int. 2009, 54:314-321.
30. Voges D., Zwickl P., Baumeister W. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 1999, 68:1015-1068.
31. Leggett D.S., Hanna J., Borodovsky A., Crosas B., Schmidt M., Baker R.T., Walz T., Ploegh H., Finley D. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 2002, 10:495-507.
32. Hamazaki J., Iemura S., Natsume T., Yashiroda H., Tanaka K., Murata S. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J. 2006, 25:4524-4536.
33. Saeki Y., Tanaka K. Cell Biology: Two hands for degradation. Nature 2008, 453:460-461.
34. Schreiner P., Chen X., Husnjak K., Randles L., Zhang N., Elsasser S., Finley D., Dikic I., Walters K.J., Groll M. Ubiquitin docking at the proteasome through a novel pleckstrin-homology domain interaction. Nature 2008, 453:548-552.
35. Husnjak K., Elsasser S., Zhang N., Chen X., Randles L., Shi Y., Hofmann K., Walters K.J., Finley D., Dikic I. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008, 453:481-488.
36. Yao T., Song L., Jin J., Cai Y., Takahashi H., Swanson S.K., Washburn M.P., Florens L., Conaway R.C., Cohen R.E., Conaway J.W. Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin-remodeling complex. Mol. Cell 2008, 31:909-917.
37. Zediak V.P., Berger S.L. Hit and run: transient deubiquitylase activity in a chromatin-remodeling complex. Mol. Cell 2008, 31:773-774.
38. Cai Y., Jin J., Yao T., Gottschalk A.J., Swanson S.K., Wu S., Shi Y., Washburn M.P., Florens L., Conaway R.C., Conaway J.W. YY1 functions with INO80 to activate transcription. Nat. Struct. Mol. Biol. 2007, 14:872-874.
39. Ventii K.H., Devi N.S., Friedrich K.L., Chernova T.A., Tighiouart M., Van Meir E.G., Wilkinson K.D. BRCA1-associated protein 1 is a tumor suppressor that requires deubiquitinating activity and nuclear localization. Cancer Res. 2008, 68:6953-6962.
40. Mallery D.L., Vandenberg C.J., Hiom K. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J. 2002, 21:6755-6762.
41. Mohammad R.M., Maki A., Pettit G.R. A.M. al-Katib, Bryostatin 1 induces ubiquitin COOH-terminal hydrolase in acute lymphoblastic leukemia cells. Enzyme Protein 1996, 49:262-272.
42. Hibi K., Westra W.H., Borges M., Goodman S., Sidransky D., Jen J. PGP9.5 as a candidate tumor marker for non-small-cell lung cancer. Am. J. Pathol. 1999, 155:711-715.
43. Sasaki H., Yukiue H., Moriyama S., Kobayashi Y., Nakashima Y., Kaji M., Fukai I., Kiriyama M., Yamakawa Y., Fujii Y. Expression of the protein gene product 9.5, PGP9.5, is correlated with T-status in non-small cell lung cancer. Jpn. J. Clin. Oncol. 2001, 31:532-535.
44. Yanagisawa T.Y., Sasahara Y., Fujie H., Ohashi Y., Minegishi M., Itano M., Morita S., Tsuchiya S., Hayashi Y., Ohi R., Konno T. Detection of the PGP9.5 and tyrosine hydroxylase mRNAs for minimal residual neuroblastoma cells in bone marrow and peripheral blood, Tohoku. J. Exp. Med. 1998, 184:229-240.
45. Tezel E., Hibi K., Nagasaka T., Nakao A. PGP9.5 as a prognostic factor in pancreatic cancer. Clin. Cancer Res. 2000, 6:4764-4767.
46. Aumuller G., Renneberg H., Leonhardt M., Lilja H., Abrahamsson P.A. Localization of protein gene product 9.5 immunoreactivity in derivatives of the human Wolffian duct and in prostate cancer. Prostate 1999, 38:261-267.
47. Leiblich A., Cross S.S., Catto J.W., Pesce G., Hamdy F.C., Rehman I. Human prostate cancer cells express neuroendocrine cell markers PGP 9.5 and chromogranin A. Prostate 2007, 67:1761-1769.
48. Takano T., Miyauchi A., Matsuzuka F., Yoshida H., Nakata Y., Kuma K., Amino N. PGP9.5 mRNA could contribute to the molecular-based diagnosis of medullary thyroid carcinoma. Eur. J. Cancer 2004, 40:614-618.
49. Takase T., Hibi K., Yamazaki T., Nakayama H., Taguchi M., Kasai Y., Ito K., Akiyama S., Nagasaka T., Nakao A. PGP9.5 overexpression in esophageal squamous cell carcinoma. Hepatogastroenterology 2003, 50:1278-1280.
50. Mizukami H., Shirahata A., Goto T., Sakata M., Saito M., Ishibashi K., Kigawa G., Nemoto H., Sanada Y., Hibi K. PGP9.5 methylation as a marker for metastatic colorectal cancer. Anticancer Res. 2008, 28:2697-2700.
51. Seliger B., Fedorushchenko A., Brenner W., Ackermann A., Atkins D., Hanash S., Lichtenfels R. Ubiquitin COOH-terminal hydrolase 1: a biomarker of renal cell carcinoma associated with enhanced tumor cell proliferation and migration. Clin. Cancer Res. 2007, 13:27-37.
52. Rolen U., Kobzeva V., Gasparjan N., Ovaa H., Winberg G., Kisseljov F., Masucci M.G. Activity profiling of deubiquitinating enzymes in cervical carcinoma biopsies and cell lines. Mol. Carcinog. 2006, 45:260-269.
53. Kim H.J., Kim Y.M., Lim S., Nam Y.K., Jeong J., Kim H.J., Lee K.J. Ubiquitin C-terminal hydrolase-L1 is a key regulator of tumor cell invasion and metastasis. Oncogene 2009, 28:117-127.
54. Rolen U., Freda E., Xie J., Pfirmann T., Frisan T., Masucci M.G. The ubiquitin C-terminal hydrolase UCH-L1 regulates B-cell proliferation and integrin activation. J. Cell. Mol. Med. 2009, 13:1666-1678.
55. Miyoshi Y., Nakayama S., Torikoshi Y., Tanaka S., Ishihara H., Taguchi T., Tamaki Y., Noguchi S. High expression of ubiquitin carboxy-terminal hydrolase-L1 and -L3 mRNA predicts early recurrence in patients with invasive breast cancer. Cancer Sci. 2006, 97:523-529.
56. Jensen D.E., Rauscher F.J. Defining biochemical functions for the BRCA1 tumor suppressor protein: analysis of the BRCA1 binding protein BAP1. Cancer Lett. 1999, 143(Suppl. 1):S13-S17.
57. Coupier I., Cousin P.Y., Hughes D., Legoix-Ne P., Trehin A., Sinilnikova O.M., Stoppa-Lyonnet D. BAP1 and breast cancer risk. Fam. Cancer 2005, 4:273-277.
58. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480.
59. Bheda A., Yue W., Gullapalli A., Whitehurst C., Liu R., Pagano J.S., Shackelford J. Positive reciprocal regulation of ubiquitin C-terminal hydrolase L1 and β-catenin/TCF signaling. PLoS ONE 2009, 4:e5955.
60. Takami Y., Nakagami H., Morishita R., Katsuya T., Cui T.X., Ichikawa T., Saito Y., Hayashi H., Kikuchi Y., Nishikawa T., Baba Y., Yasuda O., Rakugi H., Ogihara T., Kaneda Y. Ubiquitin carboxyl-terminal hydrolase L1, a novel deubiquitinating enzyme in the vasculature, attenuates NF-ΚB activation. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2184-2190.
61. Strayhorn W.D., Wadzinski B.E. A novel in vitro assay for deubiquitination of IΚ Bα. Arch. Biochem. Biophys. 2002, 400:76-84.
62. Kip1. Oncogene 2002, 21:3003-3010.
63. Tomoda K., Kubota Y., Kato J. Degradation of the cyclin-dependent-kinase inhibitor p27Kip1 is instigated by Jab1. Nature 1999, 398:160-165.
64. Bheda A., Shackelford J., Pagano J.S. Expression and functional studies of ubiquitin C-terminal hydrolase L1 regulated genes. PLoS ONE 2009, 4:e6764.
65. Kwon J., Wang Y.L., Setsuie R., Sekiguchi S., Sato Y., Sakurai M., Noda M., Aoki S., Yoshikawa Y., Wada K. Two closely related ubiquitin C-terminal hydrolase isozymes function as reciprocal modulators of germ cell apoptosis in cryptorchid testis. Am. J. Pathol. 2004, 165:1367-1374.
66. Chiba T., Tanaka K. Cullin-based ubiquitin ligase and its control by NEDD8-conjugating system. Curr. Protein Pept. Sci. 2004, 5:177-184.
67. Wicks S.J., Haros K., Maillard M., Song L., Cohen R.E., Dijke P.T., Chantry A. The deubiquitinating enzyme UCH37 interacts with Smads and regulates TGF-β signalling. Oncogene 2005, 24:8080-8084.
68. Wicks S.J., Grocott T., Haros K., Maillard M., ten Dijke P., Chantry A. Reversible ubiquitination regulates the Smad/TGF-β signalling pathway. Biochem. Soc. Trans. 2006, 34:761-763.
69. Nishikawa H., Wu W., Koike A., Kojima R., Gomi H., Fukuda M., Ohta T. BRCA1-associated protein 1 interferes with BRCA1/BARD1 RING heterodimer activity. Cancer Res. 2009, 69:111-119.
70. Misaghi S., Ottosen S., Izrael-Tomasevic A., Arnott D., Lamkanfi M., Lee J., Liu J., O'Rourke K., Dixit V.M., Wilson A.C. Association of C-terminal ubiquitin hydrolase BRCA1-associated protein 1 with cell cycle regulator host cell factor 1. Mol. Cell. Biol. 2009, 29:2181-2192.