Emerging evidence of coding mutations in the ubiquitin-proteasome system associated with cerebellar ataxias

Human Genome Variation

Volumn 1, Issue , 2014, Pages

  Ronnebaum, Sarah M ^a   Patterson, Cam ^b   Schisler, Jonathan C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; HSP70 INTERACTING PROTEIN; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG;

CEREBELLAR ATAXIA; GENE; GENE MUTATION; HUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; STUB1 GENE; WHOLE EXOME SEQUENCING;

EID: 84944511835     PISSN: None     EISSN: 2054345X     Source Type: Journal    
DOI: 10.1038/hgv.2014.18     Document Type: Review

References (59)

1. Sailer A, Houlden H. Recent advances in the genetics of cerebellar ataxias. Curr Neurol Neurosci Rep 2012; 12: 227-236.
2. Ward LD, Kellis M. Interpreting noncoding genetic variation in complex traits and human disease. Nat Biotechnol 2012; 30: 1095-1106.
3. Ng SY, Lin L, Soh BS, Stanton LW. Long noncoding RNAs in development and disease of the central nervous system. Trends Genet 2013; 29: 461-468.
4. Stenson PD, Mort M, Ball EV, Shaw K, Phillips A, Cooper DN. The Human Gene Mutation Database: building a comprehensive mutation repository for clinical and molecular genetics, diagnostic testing and personalized genomic medicine. Hum Genet 2014; 133: 1-9.
5. Ng SB, Buckingham KJ, Lee C, Bigham AW, Tabor HK, Dent KM et al. Exome sequencing identifies the cause of a mendelian disorder. Nat Genet 2010; 42: 30-35.
6. Hersheson J, Haworth A, Houlden H. The inherited ataxias: genetic heterogeneity, mutation databases, and future directions in research and clinical diagnostics. Hum Mutat 2012; 33: 1324-1332.
7. Bamshad MJ, Ng SB, Bigham AW, Tabor HK, Emond MJ, Nickerson DA et al. Exome sequencing as a tool for Mendelian disease gene discovery. Nat Rev Genet 2011; 12: 745-755.
8. Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, Handsaker RE et al. An integrated map of genetic variation from 1,092 human genomes. Nature 2012; 491: 56-65.
9. Shi CH, Schisler JC, Rubel CE, Tan S, Song B, McDonough H et al. Ataxia and hypogonadism caused by the loss of ubiquitin ligase activity of the U box protein CHIP. Hum Mol Genet 2014; 23: 1013-1024.
10. Connell P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, Höhfeld J et al. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol 2001; 3: 93-96.
11. Dai Q, Zhang C, Wu Y, McDonough H, Whaley RA, Godfrey V et al. CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J 2003; 22: 5446-5458.
12. Kampinga HH, Kanon B, Salomons FA, Kabakov AE, Patterson C. Overexpression of the cochaperone CHIP enhances Hsp70-dependent folding activity in mammalian cells. Mol Cell Biol 2003; 23: 4948-4958.
13. McDonough H, Charles PC, Hilliard EG, Qian SB, Min JN, Portbury A et al. Stress-dependent Daxx-CHIP interaction suppresses the p53 apoptotic program. J Biol Chem 2009; 284: 20649-20659.
14. Ronnebaum SM, Wu Y, McDonough H, Patterson C. The Ubiquitin Ligase CHIP Prevents SirT6 Degradation through Noncanonical Ubiquitination. Mol Cell Biol 2013; 33: 4461-4472.
15. Rosser MF, Washburn E, Muchowski PJ, Patterson C, Cyr DM. Chaperone functions of the E3 ubiquitin ligase CHIP. J Biol Chem 2007; 282: 22267-22277.
16. Schisler JC, Rubel CE, Zhang C, Lockyer P, Cyr DM, Patterson C. CHIP protects against cardiac pressure overload through regulation of AMPK. J Clin Invest 2013; 123: 3588-3599.
17. Min JN, Whaley RA, Sharpless NE, Lockyer P, Portbury AL, Patterson C. CHIP deficiency decreases longevity, with accelerated aging phenotypes accompanied by altered protein quality control. Mol Cell Biol 2008; 28: 4018-4025.
18. Shi Y, Wang J, Li JD, Ren H, Guan W, He M et al. Identification of CHIP as a novel causative gene for autosomal recessive cerebellar ataxia. PLoS ONE 2013; 8: e81884.
19. Depondt C, Donatello S, Simonis N, Rai M, van Heurck R, Abramowicz M et al. Autosomal recessive cerebellar ataxia of adult onset due to STUB1 mutations. Neurology 2014; 82: 1749-1750.
20. Synofzik M, Schüle R, Schulze M, Gburek-Augustat J, Schweizer R, Schirmacher A et al. Phenotype and frequency of STUB1 mutations: next-generation screenings in Caucasian ataxia and spastic paraplegia cohorts. Orphanet J Rare Dis 2014; 9: 57.
21. Cordoba M, Rodriguez-Quiroga S, Gatto EM, Alurralde A, Kauffman MA. Ataxia plus myoclonus in a 23-year-old patient due to STUB1 mutations. Neurology 2014; 83: 287-288.
22. Shin Y, Klucken J, Patterson C, Hyman BT, McLean PJ. The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J Biol Chem 2005; 280: 23727-23734.
23. Shimura H, Schwartz D, Gygi SP, Kosik KS. CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem 2004; 279: 4869-4876.
24. Tetzlaff JE, Putcha P, Outeiro TF, Ivanov A, Berezovska O, Hyman BT et al. CHIP targets toxic alpha-Synuclein oligomers for degradation. J Biol Chem 2008; 283: 17962-17968.
25. Ding X, Goldberg MS. Regulation of LRRK2 stability by the E3 ubiquitin ligase CHIP. PLoS ONE 2009; 4: e5949.
26. Ko HS, Bailey R, Smith WW, Liu Z, Shin JH, Lee YI et al. CHIP regulates leucine-rich repeat kinase-2 ubiquitination, degradation, and toxicity. Proc Natl Acad Sci USA 2009; 106: 2897-2902.
27. Jana NR, Dikshit P, Goswami A, Kotliarova S, Murata S, Tanaka K et al. Co-chaperone CHIP associates with expanded polyglutamine protein and promotes their degradation by proteasomes. J Biol Chem 2005; 280: 11635-11640.
28. Miller VM, Nelson RF, Gouvion CM, Williams A, Rodriguez-Lebron E, Harper SQ et al. CHIP suppresses polyglutamine aggregation and toxicity in vitro and in vivo. J Neurosci 2005; 25: 9152-9161.
29. Imai Y, Soda M, Hatakeyama S, Akagi T, Hashikawa T, Nakayama KI et al. CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Mol Cell 2002; 10: 55-67.
30. Al-Ramahi I, Lam YC, Chen HK, de Gouyon B, Zhang M, Pérez AM et al. CHIP protects from the neurotoxicity of expanded and wild-type ataxin-1 and promotes their ubiquitination and degradation. J Biol Chem 2006; 281: 26714-26724.
31. Scaglione KM, Zavodszky E, Todi SV, Patury S, Xu P, Rodríguez-Lebrón E et al. Ube2w and ataxin-3 coordinately regulate the ubiquitin ligase CHIP. Mol Cell 2011; 43: 599-612.
32. 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.
33. Winborn BJ, Travis SM, Todi SV, Scaglione KM, Xu P, Williams AJ et al. The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J Biol Chem 2008; 283: 26436-26443.
34. Kawaguchi Y, Okamoto T, Taniwaki M, Aizawa M, Inoue M, Katayama S et al. CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat Genet 1994; 8: 221-228.
35. Williams AJ, Knutson TM, Colomer Gould VF, Paulson HL. In vivo suppression of polyglutamine neurotoxicity by C-terminus of Hsp70-interacting protein (CHIP) supports an aggregation model of pathogenesis. Neurobiol Dis 2009; 33: 342-353.
36. Tsou WL, Burr AA, Ouyang M, Blount JR, Scaglione KM, Todi SV. Ubiquitination regulates the neuroprotective function of the deubiquitinase ataxin-3 in vivo. J Biol Chem 2013; 288: 34460-34469.
37. Nikolay R, Wiederkehr T, Rist W, Kramer G, Mayer MP, Bukau B. Dimerization of the human E3 ligase CHIP via a coiled-coil domain is essential for its activity. J Biol Chem 2004; 279: 2673-2678.
38. Qian SB, Waldron L, Choudhary N, Klevit RE, Chazin WJ, Patterson C. Engineering a ubiquitin ligase reveals conformational flexibility required for ubiquitin transfer. J Biol Chem 2009; 284: 26797-26802.
39. Margolin DH, Kousi M, Chan YM, Lim ET, Schmahmann JD, Hadjivassiliou M et al. Ataxia, dementia, and hypogonadotropism caused by disordered ubiquitination. N Engl J Med 2013; 368: 1992-2003.
40. Sawyer SL, Schwartzentruber J, Beaulieu CL, Dyment D, Smith A, Warman Chardon J et al. Exome sequencing as a diagnostic tool for pediatric-onset ataxia. Hum Mutat 2014; 35: 45-49.
41. Davies JE, Sarkar S, Rubinsztein DC. The ubiquitin proteasome system in Huntington's disease and the spinocerebellar ataxias. BMC Biochem 2007; 8(Suppl 1):S2.
42. Duenas AM, Goold R, Giunti P. Molecular pathogenesis of spinocerebellar ataxias. Brain 2006; 129: 1357-1370.
43. Evert BO, Wullner U, Klockgether T. Cell death in polyglutamine diseases. Cell Tissue Res 2000; 301: 189-204.
44. Orr HT. Beyond the Qs in the polyglutamine diseases. Genes Dev 2001; 15: 925-932.
45. Synofzik M, Gonzalez MA, Lourenco CM, Coutelier M, Haack TB, Rebelo A et al. PNPLA6 mutations cause Boucher-Neuhauser and Gordon Holmes syndromes as part of a broad neurodegenerative spectrum. Brain 2014; 137: 69-77.
46. Alves-Rodrigues A, Gregori L, Figueiredo-Pereira ME. Ubiquitin, cellular inclusions and their role in neurodegeneration. Trends Neurosci 1998; 21: 516-520.
47. Gong B, Cao Z, Zheng P, Vitolo OV, Liu S, Staniszewski A et al. Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 2006; 126: 775-788.
48. Leroy E, Boyer R, Auburger G, Leube B, Ulm G, Mezey E et al. The ubiquitin pathway in Parkinson's disease. Nature 1998; 395: 451-452.
49. Bilguvar K, Tyagi NK, Ozkara C, Tuysuz B, Bakircioglu M, Choi M et al. Recessive loss of function of the neuronal ubiquitin hydrolase UCHL1 leads to early-onset progressive neurodegeneration. Proc Natl Acad Sci USA 2013; 110: 3489-3494.
50. Chen F, Sugiura Y, Myers KG, Liu Y, Lin W. Ubiquitin carboxyl-terminal hydrolase L1 is required for maintaining the structure and function of the neuromuscular junction. Proc Natl Acad Sci USA 2010; 107: 1636-1641.
51. Saigoh K, Wang YL, Suh JG, Yamanishi T, Sakai Y, Kiyosawa H et al. Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat Genet 1999; 23: 47-51.
52. Yamazaki K, Wakasugi N, Tomita T, Kikuchi T, Mukoyama M, Ando K. Gracile axonal dystrophy (GAD), a new neurological mutant in the mouse. Proc Soc Exp Biol Med 1988; 187: 209-215.
53. Conroy J, McGettigan P, Murphy R, Webb D, Murphy SM, McCoy B et al. A novel locus for episodic ataxia:UBR4 the likely candidate. Eur J Hum Genet 2013; 22: 505-510.
54. Deng HX, Chen W, Hong ST, Boycott KM, Gorrie GH, Siddique N et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/ dementia. Nature 2011; 477: 211-215.
55. Williams KL, Warraich ST, Yang S, Solski JA, Fernando R, Rouleau GA et al. UBQLN2/ubiquilin 2 mutation and pathology in familial amyotrophic lateral sclerosis. Neurobiol Aging 2012; 33: 2527 e2523-2510.
56. Johnson JO, Mandrioli J, Benatar M, Abramzon Y, Van Deerlin VM, Trojanowski JQ et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 2010; 68: 857-864.
57. Flex E, Ciolfi A, Caputo V, Fodale V, Leoni C, Melis D et al. Loss of function of the E3 ubiquitin-protein ligase UBE3B causes Kaufman oculocerebrofacial syndrome. J Med Genet 2013; 50: 493-499.
58. Basel-Vanagaite L, Dallapiccola B, Ramirez-Solis R, Segref A, Thiele H, Edwards A et al. Deficiency for the ubiquitin ligase UBE3B in a blepharophimosis-ptosis-intellectual-disability syndrome. Am J Hum Genet 2012; 91: 998-1010.
59. Chahrour MH, Yu TW, Lim ET, Ataman B, Coulter ME, Hill RS et al. Whole-exome sequencing and homozygosity analysis implicate depolarization-regulated neuronal genes in autism. PLoS Genet 2012; 8: e1002635.