Deubiquitylating enzymes and disease

Baker RT, Tobias JT, Varshavsky A: Ubiquitin-specific proteases of Saccharomyces cerevisiae. Cloning of UBP2 and UBP3, and functional analysis of the UBP gene family. J Biol Chem. 1992, 267: 23364-23375.

Matsui S, Sandberg AA, Negoro S, Seon BK, Goldstein G: Isopeptidase: a novel eukaryotic enzyme that cleaves isopeptide bonds. Proc Natl Acad Sci USA. 1982, 79: 1535-1539. 10.1073/pnas.79.5.1535.

Pickart CM, Rose IA: Ubiquitin carboxyl-terminal hydrolase acts on ubiquitin carboxyl-terminal amides. J Biol Chem. 1985, 260: 7903-7910.

Mayer AN, Wilkinson KD: Detection, resolution, and nomenclature of multiple ubiquitin carboxyl-terminal esterases from bovine calf thymus. Biochemistry. 1989, 28: 166-172. 10.1021/bi00427a024.

Amerik AY, Hochstrasser M: Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta. 2004, 1695: 189-207. 10.1016/j.bbamcr.2004.10.003.

Soboleva TA, Baker RT: Deubiquitinating enzymes: their functions and substrate specificity. Curr Protein Pept Sci. 2004, 5: 191-200. 10.2174/1389203043379765.

Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, Bernards R: A genomic and functional inventory of deubiquitinating enzymes. Cell. 2005, 123: 773-786. 10.1016/j.cell.2005.11.007.

Wilkinson KD: Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. Faseb J. 1997, 11: 1245-1256.

Onno M, Nakamura T, Mariage-Samson R, Hillova J, Hill M: Human TRE17 oncogene is generated from a family of homologous polymorphic sequences by single-base changes. DNA Cell Biol. 1993, 12: 107-118.

Papa FR, Hochstrasser M: The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature. 1993, 366: 313-319. 10.1038/366313a0.

Oliveira AM, Hsi BL, Weremowicz S, Rosenberg AE, Dal Cin P, Joseph N, Bridge JA, Perez-Atayde AR, Fletcher JA: USP6 (Tre2) fusion oncogenes in aneurysmal bone cyst. Cancer Res. 2004, 64: 1920-1923. 10.1158/0008-5472.CAN-03-2827.

Oliveira AM, Perez-Atayde AR, Inwards CY, Medeiros F, Derr V, Hsi BL, Gebhardt MC, Rosenberg AE, Fletcher JA: USP6 and CDH11 oncogenes identify the neoplastic cell in primary aneurysmal bone cysts and are absent in so-called secondary aneurysmal bone cysts. Am J Pathol. 2004, 165: 1773-1780.

Oliveira AM, Perez-Atayde AR, Dal Cin P, Gebhardt MC, Chen CJ, Neff JR, Demetri GD, Rosenberg AE, Bridge JA, Fletcher JA: Aneurysmal bone cyst variant translocations upregulate USP6 transcription by promoter swapping with the ZNF9, COL1A1, TRAP150, and OMD genes. Oncogene. 2005, 24: 3419-3426. 10.1038/sj.onc.1208506.

Martinu L, Masuda-Robens JM, Robertson SE, Santy LC, Casanova JE, Chou MM: The TBC (Tre-2/Bub2/Cdc16) domain protein TRE17 regulates plasma membrane-endosomal trafficking through activation of Arf6. Mol Cell Biol. 2004, 24: 9752-9762. 10.1128/MCB.24.22.9752-9762.2004.

Zapata JM, Pawlowski K, Haas E, Ware CF, Godzik A, Reed JC: A diverse family of proteins containing tumor necrosis factor receptor-associated factor domains. J Biol Chem. 2001, 276: 24242-24252. 10.1074/jbc.M100354200.

Li M, Chen D, Shiloh A, Luo J, Nikolaev AY, Qin J, Gu W: Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature. 2002, 416: 648-653. 10.1038/nature737.

Hu M, Li P, Li M, Li W, Yao T, Wu JW, Gu W, Cohen RE, Shi Y: Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell. 2002, 111: 1041-1054. 10.1016/S0092-8674(02)01199-6.

Sheng Y, Saridakis V, Sarkari F, Duan S, Wu T, Arrowsmith CH, Frappier L: Molecular recognition of p53 and MDM2 by USP7/HAUSP. Nat Struct Mol Biol. 2006, 13: 285-291. 10.1038/nsmb1067.

Li M, Brooks CL, Kon N, Gu W: A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol Cell. 2004, 13: 879-886. 10.1016/S1097-2765(04)00157-1.

Cummins JM, Vogelstein B: HAUSP is required for p53 destabilization. Cell Cycle. 2004, 3: 689-692.

Hu M, Gu L, Li M, Jeffrey PD, Gu W, Shi Y: Structural basis of competitive recognition of p53 and MDM2 by HAUSP/USP7: implications for the regulation of the p53-MDM2 pathway. PLoS Biol. 2006, 4 (2): e27-10.1371/journal.pbio.0040027.

Brooks CL, Gu W: p53 ubiquitination: Mdm2 and beyond. Mol Cell. 2006, 21: 307-315. 10.1016/j.molcel.2006.01.020.

Tang J, Qu LK, Zhang J, Wang W, Michaelson JS, Degenhardt YY, El-Deiry WS, Yang X: Critical role for Daxx in regulating Mdm2. Nat Cell Biol. 2006, 8: 855-862. 10.1038/ncb1442.

Masuya D, Huang C, Liu D, Nakashima T, Yokomise H, Ueno M, Nakashima N, Sumitomo S: The HAUSP gene plays an important role in non-small cell lung carcinogenesis through p53-dependent pathways. J Pathol. 2006, 208: 724-732. 10.1002/path.1931.

Boutell C, Everett RD: The herpes simplex virus type 1 (HSV-1) regulatory protein ICP0 interacts with and Ubiquitinates p53. J Biol Chem. 2003, 278: 36596-36602. 10.1074/jbc.M300776200.

Saridakis V, Sheng Y, Sarkari F, Holowaty MN, Shire K, Nguyen T, Zhang RG, Liao J, Lee W, Edwards AM, Arrowsmith CH, Frappier L: Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein-Barr nuclear antigen 1 implications for EBV-mediated immortalization. Mol Cell. 2005, 18: 25-36. 10.1016/j.molcel.2005.02.029.

Horst van der A, de Vries-Smits AM, Brenkman AB, van Triest MH, Broek van den N, Colland F, Maurice MM, Burgering BM: FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat Cell Biol. 2006, 8: 1064-1073. 10.1038/ncb1469.

Bignell GR, Warren W, Seal S, Takahashi M, Rapley E, Barfoot R, Green H, Brown C, Biggs PJ, Lakhani SR, et al.: Identification of the familial cylindromatosis tumour-suppressor gene. Nat Genet. 2000, 25: 160-165. 10.1038/76006.

Bowen S, Gill M, Lee DA, Fisher G, Geronemus RG, Vazquez ME, Celebi JT: Mutations in the CYLD gene in Brooke-Spiegler syndrome, familial cylindromatosis, and multiple familial trichoepithelioma: lack of genotype-phenotype correlation. J Invest Dermatol. 2005, 124: 919-920. 10.1111/j.0022-202X.2005.23688.x.

Kovalenko A, Chable-Bessia C, Cantarella G, Israel A, Wallach D, Courtois G: The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature. 2003, 424: 801-805. 10.1038/nature01802.

Brummelkamp TR, Nijman SM, Dirac AM, Bernards R: Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappaB. Nature. 2003, 424: 797-801. 10.1038/nature01811.

Trompouki E, Hatzivassiliou E, Tsichritzis T, Farmer H, Ashworth A, Mosialos G: CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature. 2003, 424: 793-796. 10.1038/nature01803.

Ikeda F, Dikic I: CYLD in ubiquitin signaling and tumor pathogenesis. Cell. 2006, 125: 643-645. 10.1016/j.cell.2006.05.003.

Reiley WW, Zhang M, Jin W, Losiewicz M, Donohue KB, Norbury CC, Sun SC: Regulation of T cell development by the deubiquitinating enzyme CYLD. Nat Immunol. 2006, 7: 411-417. 10.1038/ni1315.

Zhang J, Stirling B, Temmerman ST, Ma CA, Fuss IJ, Derry JM, Jain A: Impaired regulation of NF-kappaB and increased susceptibility to colitis-associated tumorigenesis in CYLD-deficient mice. J Clin Invest. 2006, 116: 3042-3049. 10.1172/JCI28746.

Evans PC, Smith TS, Lai MJ, Williams MG, Burke DF, Heyninck K, Kreike MM, Beyaert R, Blundell TL, Kilshaw PJ: A novel type of deubiquitinating enzyme. J Biol Chem. 2003, 278: 23180-23186. 10.1074/jbc.M301863200.

Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, Wu P, Wiesmann C, Baker R, Boone DL, Ma A, Koonin EV, Dixit VM: De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature. 2004, 430: 694-699. 10.1038/nature02794.

Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP, Ma A: Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science. 2000, 289: 2350-2354. 10.1126/science.289.5488.2350.

Chen ZJ: Ubiquitin signalling in the NF-kappaB pathway. Nat Cell Biol. 2005, 7: 758-765. 10.1038/ncb0805-758.

Krappmann D, Scheidereit C: A pervasive role of ubiquitin conjugation in activation and termination of IkappaB kinase pathways. EMBO Rep. 2005, 6: 321-326. 10.1038/sj.embor.7400380.

Sun L, Chen ZJ: The novel functions of ubiquitination in signaling. Curr Opin Cell Biol. 2004, 16: 119-126. 10.1016/j.ceb.2004.02.005.

Kaelin WG: Molecular basis of the VHL hereditary cancer syndrome. Nat Rev Cancer. 2002, 2: 673-682. 10.1038/nrc885.

Li Z, Na X, Wang D, Schoen SR, Messing EM, Wu G: Ubiquitination of a novel deubiquitinating enzyme requires direct binding to von Hippel-Lindau tumor suppressor protein. J Biol Chem. 2002, 277: 4656-4662. 10.1074/jbc.M108269200.

Li Z, Wang D, Na X, Schoen SR, Messing EM, Wu G: Identification of a deubiquitinating enzyme subfamily as substrates of the von Hippel-Lindau tumor suppressor. Biochem Biophys Res Commun. 2002, 294: 700-709. 10.1016/S0006-291X(02)00534-X.

Li Z, Wang D, Messing EM, Wu G: VHL protein-interacting deubiquitinating enzyme 2 deubiquitinates and stabilizes HIF-1alpha. EMBO Rep. 2005, 6: 373-378. 10.1038/sj.embor.7400377.

Semenza GL: Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 2003, 3: 721-732. 10.1038/nrc1187.

Leggett DS, Hanna J, Borodovsky A, Crosas B, Schmidt M, Baker RT, Walz T, Ploegh H, Finley D: Multiple associated proteins regulate proteasome structure and function. Mol Cell. 2002, 10: 495-507. 10.1016/S1097-2765(02)00638-X.

Hanna J, Hathaway NA, Tone Y, Crosas B, Elsasser S, Kirkpatrick DS, Leggett DS, Gygi SP, King RW, Finley D: Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation. Cell. 2006, 127: 99-111. 10.1016/j.cell.2006.07.038.

Crosas B, Hanna J, Kirkpatrick DS, Zhang DP, Tone Y, Hathaway NA, Buecker C, Leggett DS, Schmidt M, King RW, Gygi SP, Finley D: Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell. 2006, 127: 1401-1413. 10.1016/j.cell.2006.09.051.

Anderson C, Crimmins S, Wilson JA, Korbel GA, Ploegh HL, Wilson SM: Loss of Usp14 results in reduced levels of ubiquitin in ataxia mice. J Neurochem. 2005, 95: 724-731. 10.1111/j.1471-4159.2005.03409.x.

Wilson SM, Bhattacharyya B, Rachel RA, Coppola V, Tessarollo L, Householder DB, Fletcher CF, Miller RJ, Copeland NG, Jenkins NA: Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease. Nat Genet. 2002, 32: 420-425. 10.1038/ng1006.

Jackson P, Thompson RJ: The demonstration of new human brain-specific proteins by high-resolution two-dimensional polyacrylamide gel electrophoresis. J Neurol Sci. 1981, 49: 429-438. 10.1016/0022-510X(81)90032-0.

Ardley HC, Scott GB, Rose SA, Tan NG, Robinson PA: UCH-L1 aggresome formation in response to proteasome impairment indicates a role in inclusion formation in Parkinson's disease. J Neurochem. 2004, 90: 379-391. 10.1111/j.1471-4159.2004.02485.x.

Das C, Hoang QQ, Kreinbring CA, Luchansky SJ, Meray RK, Ray SS, Lansbury PT, Ringe D, Petsko GA: Structural basis for conformational plasticity of the Parkinson's disease-associated ubiquitin hydrolase UCH-L1. Proc Natl Acad Sci USA. 2006, 103: 4675-4680. 10.1073/pnas.0510403103.

Leroy E, Boyer R, Auburger G, Leube B, Ulm G, Mezey E, Harta G, Brownstein MJ, Jonnalagada S, Chernova T, et al.: The ubiquitin pathway in Parkinson's disease. Nature. 1998, 395: 451-452. 10.1038/26652.

McNaught KS, Jenner P: Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci Lett. 2001, 297: 191-194. 10.1016/S0304-3940(00)01701-8.

McNaught KS, Perl DP, Brownell AL, Olanow CW: Systemic exposure to proteasome inhibitors causes a progressive model of Parkinson's disease. Ann Neurol. 2004, 56: 149-162. 10.1002/ana.20186.

Lowe J, McDermott H, Landon M, Mayer RJ, Wilkinson KD: Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases. J Pathol. 1990, 161: 153-160. 10.1002/path.1711610210.

Elbaz A, Levecque C, Clavel J, Vidal JS, Richard F, Correze JR, Delemotte B, Amouyel P, Alperovitch A, Chartier-Harlin MC, et al.: S18Y polymorphism in the UCH-L1 gene and Parkinson's disease: evidence for an age-dependent relationship. Mov Disord. 2003, 18: 130-137. 10.1002/mds.10326.

Lincoln S, Vaughan J, Wood N, Baker M, Adamson J, Gwinn-Hardy K, Lynch T, Hardy J, Farrer M: Low frequency of pathogenic mutations in the ubiquitin carboxy-terminal hydrolase gene in familial Parkinson's disease. Neuroreport. 1999, 10: 427-429. 10.1097/00001756-199902050-00040.

Maraganore DM, Farrer MJ, Hardy JA, Lincoln SJ, McDonnell SK, Rocca WA: Case-control study of the ubiquitin carboxy-terminal hydrolase L1 gene in Parkinson's disease. Neurology. 1999, 53: 1858-1860.

Maraganore DM, Lesnick TG, Elbaz A, Chartier-Harlin MC, Gasser T, Kruger R, Hattori N, Mellick GD, Quattrone A, Satoh J, et al.: UCHL1 is a Parkinson's disease susceptibility gene. Ann Neurol. 2004, 55: 512-521. 10.1002/ana.20017.

Colomer Gould VF: Mouse models of Machado-Joseph disease and other polyglutamine spinocerebellar ataxias. NeuroRx. 2005, 2: 480-483. 10.1602/neurorx.2.3.480.

Perez MK, Paulson HL, Pittman RN: Ataxin-3 with an altered conformation that exposes the polyglutamine domain is associated with the nuclear matrix. Hum Mol Genet. 1999, 8: 2377-2385. 10.1093/hmg/8.13.2377.

Paulson HL, Das SS, Crino PB, Perez MK, Patel SC, Gotsdiner D, Fischbeck KH, Pittman RN: Machado-Joseph disease gene product is a cytoplasmic protein widely expressed in brain. Ann Neurol. 1997, 41: 453-462. 10.1002/ana.410410408.

Fujigasaki H, Uchihara T, Koyano S, Iwabuchi K, Yagishita S, Makifuchi T, Nakamura A, Ishida K, Toru S, Hirai S, et al.: Ataxin-3 is translocated into the nucleus for the formation of intranuclear inclusions in normal and Machado-Joseph disease brains. Exp Neurol. 2000, 165: 248-256. 10.1006/exnr.2000.7479.

Burnett B, Li F, Pittman RN: The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity. Hum Mol Genet. 2003, 12: 3195-3205. 10.1093/hmg/ddg344.

Chow MK, Mackay JP, Whisstock JC, Scanlon MJ, Bottomley SP: Structural and functional analysis of the Josephin domain of the polyglutamine protein ataxin-3. Biochem Biophys Res Commun. 2004, 322: 387-394. 10.1016/j.bbrc.2004.07.131.

Nijman SM, Huang TT, Dirac AM, Brummelkamp TR, Kerkhoven RM, D'Andrea AD, Bernards R: The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell. 2005, 17: 331-339. 10.1016/j.molcel.2005.01.008.

Jensen DE, Proctor M, Marquis ST, Gardner HP, Ha SI, Chodosh LA, Ishov AM, Tommerup N, Vissing H, Sekido Y, et al.: BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene. 1998, 16: 1097-1112. 10.1038/sj.onc.1201861.

Schoenfeld AR, Apgar S, Dolios G, Wang R, Aaronson SA: BRCA2 is ubiquitinated in vivo and interacts with USP11, a deubiquitinating enzyme that exhibits prosurvival function in the cellular response to DNA damage. Mol Cell Biol. 2004, 24: 7444-7455. 10.1128/MCB.24.17.7444-7455.2004.

Gray DA, Inazawa J, Gupta K, Wong A, Ueda R, Takahashi T: Elevated expression of Unph, a proto-oncogene at 3p21.3, in human lung tumors. Oncogene. 1995, 10: 2179-2183.

Blanchette P, Gilchrist CA, Baker RT, Gray DA: Association of UNP, a ubiquitin-specific protease, with the pocket proteins pRb, p107 and p130. Oncogene. 2001, 20: 5533-5537. 10.1038/sj.onc.1204823.

DeSalle LM, Latres E, Lin D, Graner E, Montagnoli A, Baker RT, Pagano M, Loda M: The de-ubiquitinating enzyme Unp interacts with the retinoblastoma protein. Oncogene. 2001, 20: 5538-5542. 10.1038/sj.onc.1204824.

Wada K, Kamitani T: UnpEL/Usp4 is ubiquitinated by Ro52 and deubiquitinated by itself. Biochem Biophys Res Commun. 2006, 342: 253-258. 10.1016/j.bbrc.2006.01.144.

Di Donato F, Chan EK, Askanase AD, Miranda-Carus M, Buyon JP: Interaction between 52 kDa SSA/Ro and deubiquitinating enzyme UnpEL: a clue to function. Int J Biochem Cell Biol. 2001, 33: 924-934. 10.1016/S1357-2725(01)00055-3.

Gesbert F, Malarde V, Dautry-Varsat A: Ubiquitination of the common cytokine receptor gammac and regulation of expression by an ubiquitination/deubiquitination machinery. Biochem Biophys Res Commun. 2005, 334: 474-480. 10.1016/j.bbrc.2005.06.121.

Graner E, Tang D, Rossi S, Baron A, Migita T, Weinstein LJ, Lechpammer M, Huesken D, Zimmermann J, Signoretti S, Loda M: The isopeptidase USP2a regulates the stability of fatty acid synthase in prostate cancer. Cancer Cell. 2004, 5: 253-261. 10.1016/S1535-6108(04)00055-8.

Priolo C, Tang D, Brahamandan M, Benassi B, Sicinska E, Ogino S, Farsetti A, Porrello A, Finn S, Zimmermann J, Febbo P, Loda M: The isopeptidase USP2a protects human prostate cancer from apoptosis. Cancer Res. 2006, 66: 8625-8632. 10.1158/0008-5472.CAN-06-1374.

Huang Y, Baker RT, Fischer-Vize JA: Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene. Science. 1995, 270: 1828-1831. 10.1126/science.270.5243.1828.

Chen X, Zhang B, Fischer JA: A specific protein substrate for a deubiquitinating enzyme: Liquid facets is the substrate of Fat facets. Genes Dev. 2002, 16: 289-294. 10.1101/gad.961502.

Dang LC, Melandri FD, Stein RL: Kinetic and mechanistic studies on the hydrolysis of ubiquitin C-terminal 7-amido-4-methylcoumarin by deubiquitinating enzymes. Biochemistry. 1998, 37: 1868-1879. 10.1021/bi9723360.

Russell NS, Wilkinson KD: Deubiquitinating enzyme purification, assay inhibitors, and characterization. Methods Mol Biol. 2005, 301: 207-219.

Pickart CM, Raasi S: Controlled synthesis of polyubiquitin chains. Methods Enzymol. 2005, 399: 21-36. 10.1016/S0076-6879(05)99002-2.

Saigoh K, Wang YL, Suh JG, Yamanishi T, Sakai Y, Kiyosawa H, Harada T, Ichihara N, Wakana S, Kikuchi T, Wada K: Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat Genet. 1999, 23: 47-51.

Sakurai M, Ayukawa K, Setsuie R, Nishikawa K, Hara Y, Ohashi H, Nishimoto M, Abe T, Kudo Y, Sekiguchi M, Sato Y, Aoki S, Noda M, Wada K: Ubiquitin C-terminal hydrolase L1 regulates the morphology of neural progenitor cells and modulates their differentiation. J Cell Sci. 2006, 119: 162-71. 10.1242/jcs.02716.

Ritchie KJ, Hahn CS, Kim KI, Yan M, Rosario D, Li L, de la Torre JC, Zhang DE: Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat Med. 2004, 10: 1374-1378. 10.1038/nm1133.

Mason DE, Ek J, Peters EC, Harris JL: Substrate profiling of deubiquitin hydrolases with a positional scanning library and mass spectrometry. Biochemistry. 2004, 43: 6535-6544. 10.1021/bi049722j.

Cheon KW, Baek KH: HAUSP as a therapeutic target for hematopoietic tumors (review). Int J Oncol. 2006, 28: 1209-1215.