Parkin-mediated K63-polyubiquitination targets ubiquitin C-terminal hydrolase L1 for degradation by the autophagy-lysosome system

Cellular and Molecular Life Sciences

Volumn 72, Issue 9, 2015, Pages 1811-1824

  McKeon, Jeanne E ^a   Sha, Di ^a   Li, Lian ^a   Chin, Lih Shen ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autophagy; Lysine 63 linked polyubiquitination; Lysosome; Parkinsonism; Ubiquitin

Indexed keywords

PARKIN; POLYUBIQUITIN; UBIQUITIN CARBOXYL-TERMINAL HYDROLASE L-1, MOUSE; UBIQUITIN PROTEIN LIGASE; UBIQUITIN THIOLESTERASE; UCHL1 PROTEIN, HUMAN;

ANIMAL; AUTOPHAGY; CELL LINE; GENETICS; HUMAN; KNOCKOUT MOUSE; LYSOSOME; METABOLISM; MOUSE; MUTATION; PARKINSON DISEASE; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

ANIMALS; AUTOPHAGY; CELL LINE; HUMANS; LYSOSOMES; MICE; MICE, KNOCKOUT; MUTATION; PARKINSON DISEASE; POLYUBIQUITIN; PROTEIN INTERACTION MAPS; PROTEOLYSIS; UBIQUITIN THIOLESTERASE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84939991427     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1781-2     Document Type: Article

References (78)

1. Satija YK, Bhardwaj A, Das S (2013) A portrayal of E3 ubiquitin ligases and deubiquitylases in cancer. Int J Cancer 133(12):2759-2768. doi: 10.1002/ijc.28129
2. McKinnon C, Tabrizi SJ (2014) The ubiquitin-proteasome system in neurodegeneration. Antioxid Redox Signal. doi: 10.1089/ars.2013.5802
3. Hussain S, Zhang Y, Galardy PJ (2009) DUBs and cancer: the role of deubiquitinating enzymes as oncogenes, non-oncogenes and tumor suppressors. Cell Cycle 8(11):1688-1697
4. Kowalski JR, Juo P (2012) The role of deubiquitinating enzymes in synaptic function and nervous system diseases. Neural Plast 2012:892749. doi: 10.1155/2012/892749
5. van Tijn P, Hol EM, van Leeuwen FW, Fischer DF (2008) The neuronal ubiquitin-proteasome system: murine models and their neurological phenotype. Prog Neurobiol 85(2):176-193. doi: 10.1016/j.pneurobio.2008.03.001
6. Pickart CM, Eddins MJ (2004) Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta 1695(1-3):55-72. doi: 10.1016/j.bbamcr.2004.09.019
7. Pickart CM, Fushman D (2004) Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 8(6):610-616. doi: 10.1016/j.cbpa.2004.09.009
8. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19(1):94-102. doi: 10.1093/emboj/19.1.94
9. Chen ZJ, Sun LJ (2009) Nonproteolytic functions of ubiquitin in cell signaling. Mol Cell 33(3):275-286. doi: 10.1016/j.molcel.2009.01.014
10. Olzmann JA, Chin LS (2008) Parkin-mediated K63-linked polyubiquitination: a signal for targeting misfolded proteins to the aggresome-autophagy pathway. Autophagy 4(1):85-87
11. Olzmann JA, Li L, Chudaev MV, Chen J, Perez FA, Palmiter RD, Chin LS (2007) Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. J Cell Biol 178(6):1025-1038. doi: 10.1083/jcb.200611128
12. Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78:363-397. doi: 10.1146/annurev.biochem.78.082307.091526
13. Eletr ZM, Wilkinson KD (2014) Regulation of proteolysis by human deubiquitinating enzymes. Biochim Biophys Acta 1843(1):114-128. doi: 10.1016/j.bbamcr.2013.06.027
14. Larsen CN, Krantz BA, Wilkinson KD (1998) Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases. Biochemistry 37(10):3358-3368. doi: 10.1021/bi972274d
15. Case A, Stein RL (2006) Mechanistic studies of ubiquitin C-terminal hydrolase L1. Biochemistry 45(7):2443-2452. doi: 10.1021/bi052135t
16. Wang YL, Takeda A, Osaka H, Hara Y, Furuta A, Setsuie R, Sun YJ, Kwon J, Sato Y, Sakurai M, Noda M, Yoshikawa Y, Wada K (2004) Accumulation of beta- and gamma-synucleins in the ubiquitin carboxyl-terminal hydrolase L1-deficient gad mouse. Brain Res 1019(1-2):1-9. doi: 10.1016/j.brainres.2004.05.023
17. Wilkinson KD, Lee KM, Deshpande S, Duerksen-Hughes P, Boss JM, Pohl J (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246(4930):670-673
18. Osaka H, Wang YL, Takada K, Takizawa S, Setsuie R, Li H, Sato Y, Nishikawa K, Sun YJ, Sakurai M, Harada T, Hara Y, Kimura I, Chiba S, Namikawa K, Kiyama H, Noda M, Aoki S, Wada K (2003) Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron. Hum Mol Genet 12(16):1945-1958
19. Leroy E, Boyer R, Auburger G, Leube B, Ulm G, Mezey E, Harta G, Brownstein MJ, Jonnalagada S, Chernova T, Dehejia A, Lavedan C, Gasser T, Steinbach PJ, Wilkinson KD, Polymeropoulos MH (1998) The ubiquitin pathway in Parkinson's disease. Nature 395(6701):451-452. doi: 10.1038/26652
20. Bilguvar K, Tyagi NK, Ozkara C, Tuysuz B, Bakircioglu M, Choi M, Delil S, Caglayan AO, Baranoski JF, Erturk O, Yalcinkaya C, Karacorlu M, Dincer A, Johnson MH, Mane S, Chandra SS, Louvi A, Boggon TJ, Lifton RP, Horwich AL, Gunel M (2013) Recessive loss of function of the neuronal ubiquitin hydrolase UCHL1 leads to early-onset progressive neurodegeneration. Proc Natl Acad Sci USA 110(9):3489-3494. doi: 10.1073/pnas.1222732110
21. Nishikawa K, Li H, Kawamura R, Osaka H, Wang YL, Hara Y, Hirokawa T, Manago Y, Amano T, Noda M, Aoki S, Wada K (2003) Alterations of structure and hydrolase activity of parkinsonism-associated human ubiquitin carboxyl-terminal hydrolase L1 variants. Biochem Biophys Res Commun 304(1):176-183
22. Choi J, Levey AI, Weintraub ST, Rees HD, Gearing M, Chin LS, Li L (2004) Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J Biol Chem 279(13):13256-13264. doi: 10.1074/jbc.M314124200
23. Saigoh K, Wang YL, Suh JG, Yamanishi T, Sakai Y, Kiyosawa H, Harada T, Ichihara N, Wakana S, Kikuchi T, Wada K (1999) Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat Genet 23(1):47-51. doi: 10.1038/12647
24. Walters BJ, Campbell SL, Chen PC, Taylor AP, Schroeder DG, Dobrunz LE, Artavanis-Tsakonas K, Ploegh HL, Wilson JA, Cox GA, Wilson SM (2008) Differential effects of Usp14 and Uch-L1 on the ubiquitin proteasome system and synaptic activity. Mol Cell Neurosci 39(4):539-548. doi: 10.1016/j.mcn.2008.07.028
25. Chen F, Sugiura Y, Myers KG, Liu Y, Lin W (2010) Ubiquitin carboxyl-terminal hydrolase L1 is required for maintaining the structure and function of the neuromuscular junction. Proc Natl Acad Sci USA 107(4):1636-1641. doi: 10.1073/pnas.0911516107
26. Yamazaki K, Wakasugi N, Tomita T, Kikuchi T, Mukoyama M, Ando K (1988) Gracile axonal dystrophy (GAD), a new neurological mutant in the mouse. Proc Soc Exp Biol Med 187(2):209-215
27. Doran JF, Jackson P, Kynoch PA, Thompson RJ (1983) Isolation of PGP 9.5, a new human neurone-specific protein detected by high-resolution two-dimensional electrophoresis. J Neurochem 40(6):1542-1547
28. Day IN, Thompson RJ (2010) UCHL1 (PGP 9.5): neuronal biomarker and ubiquitin system protein. Prog Neurobiol 90(3):327-362. doi: 10.1016/j.pneurobio.2009.10.020
29. Hurst-Kennedy J, Chin LS, Li L (2012) Ubiquitin C-terminal hydrolase l1 in tumorigenesis. Biochem Res Int 2012:123706. doi: 10.1155/2012/123706
30. Mastoraki A, Ioannidis E, Apostolaki A, Patsouris E, Aroni K (2009) PGP 9.5 and cyclin D1 coexpression in cutaneous squamous cell carcinomas. Int J Surg Pathol 17(6):413-420. doi: 10.1177/1066896909336018
31. Chen G, Gharib TG, Huang CC, Thomas DG, Shedden KA, Taylor JM, Kardia SL, Misek DE, Giordano TJ, Iannettoni MD, Orringer MB, Hanash SM, Beer DG (2002) Proteomic analysis of lung adenocarcinoma: identification of a highly expressed set of proteins in tumors. Clin Cancer Res 8(7):2298-2305
32. Tezel E, Hibi K, Nagasaka T, Nakao A (2000) PGP9.5 as a prognostic factor in pancreatic cancer. Clin Cancer Res 6(12):4764-4767
33. West AB, Maidment NT (2004) Genetics of parkin-linked disease. Hum Genet 114(4):327-336. doi: 10.1007/s00439-003-1074-6
34. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392(6676):605-608. doi: 10.1038/33416
35. Lucking CB, Durr A, Bonifati V, Vaughan J, De Michele G, Gasser T, Harhangi BS, Meco G, Denefle P, Wood NW, Agid Y, Brice A (2000) Association between early-onset Parkinson's disease and mutations in the parkin gene. N Engl J Med 342(21):1560-1567. doi: 10.1056/NEJM200005253422103
36. Cesari R, Martin ES, Calin GA, Pentimalli F, Bichi R, McAdams H, Trapasso F, Drusco A, Shimizu M, Masciullo V, D'Andrilli G, Scambia G, Picchio MC, Alder H, Godwin AK, Croce CM (2003) Parkin, a gene implicated in autosomal recessive juvenile parkinsonism, is a candidate tumor suppressor gene on chromosome 6q25-q27. Proc Natl Acad Sci USA 100(10):5956-5961. doi: 10.1073/pnas.0931262100
37. Picchio MC, Martin ES, Cesari R, Calin GA, Yendamuri S, Kuroki T, Pentimalli F, Sarti M, Yoder K, Kaiser LR, Fishel R, Croce CM (2004) Alterations of the tumor suppressor gene Parkin in non-small cell lung cancer. Clin Cancer Res 10(8):2720-2724
38. Poulogiannis G, McIntyre RE, Dimitriadi M, Apps JR, Wilson CH, Ichimura K, Luo F, Cantley LC, Wyllie AH, Adams DJ, Arends MJ (2010) PARK2 deletions occur frequently in sporadic colorectal cancer and accelerate adenoma development in Apc mutant mice. Proc Natl Acad Sci USA 107(34):15145-15150. doi: 10.1073/pnas.1009941107
39. Veeriah S, Taylor BS, Meng S, Fang F, Yilmaz E, Vivanco I, Janakiraman M, Schultz N, Hanrahan AJ, Pao W, Ladanyi M, Sander C, Heguy A, Holland EC, Paty PB, Mischel PS, Liau L, Cloughesy TF, Mellinghoff IK, Solit DB, Chan TA (2010) Somatic mutations of the Parkinson's disease-associated gene PARK2 in glioblastoma and other human malignancies. Nat Genet 42(1):77-82. doi: 10.1038/ng.491
40. Chin LS, Nugent RD, Raynor MC, Vavalle JP, Li L (2000) SNIP, a novel SNAP-25-interacting protein implicated in regulated exocytosis. J Biol Chem 275(2):1191-1200
41. Pridgeon JW, Olzmann JA, Chin LS, Li L (2007) PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol 5(7):e172. doi: 10.1371/journal.pbio.0050172
42. Sha D, Chin LS, Li L (2010) Phosphorylation of parkin by Parkinson disease-linked kinase PINK1 activates parkin E3 ligase function and NF-kappaB signaling. Hum Mol Genet 19(2):352-363. doi: 10.1093/hmg/ddp501
43. Giles LM, Li L, Chin LS (2009) Printor, a novel torsinA-interacting protein implicated in dystonia pathogenesis. J Biol Chem 284(32):21765-21775. doi: 10.1074/jbc.M109.004838
44. Hackbarth JS, Lee SH, Meng XW, Vroman BT, Kaufmann SH, Karnitz LM (2004) S-peptide epitope tagging for protein purification, expression monitoring, and localization in mammalian cells. Biotechniques 37(5):835-839
45. Lee SM, Chin LS, Li L (2012) Charcot-Marie-Tooth disease-linked protein SIMPLE functions with the ESCRT machinery in endosomal trafficking. J Cell Biol 199(5):799-816. doi: 10.1083/jcb.201204137
46. Li Y, Chin LS, Weigel C, Li L (2001) Spring, a novel RING finger protein that regulates synaptic vesicle exocytosis. J Biol Chem 276(44):40824-40833. doi: 10.1074/jbc.M106141200
47. Webber E, Li L, Chin LS (2008) Hypertonia-associated protein Trak1 is a novel regulator of endosome-to-lysosome trafficking. J Mol Biol 382(3):638-651. doi: 10.1016/j.jmb.2008.07.045
48. Lee SM, Olzmann JA, Chin LS, Li L (2011) Mutations associated with Charcot-Marie-Tooth disease cause SIMPLE protein mislocalization and degradation by the proteasome and aggresome-autophagy pathways. J Cell Sci 124(Pt 19):3319-3331. doi: 10.1242/jcs.087114
49. Perez FA, Palmiter RD (2005) Parkin-deficient mice are not a robust model of parkinsonism. Proc Natl Acad Sci USA 102(6):2174-2179. doi: 10.1073/pnas.0409598102
50. Perez FA, Curtis WR, Palmiter RD (2005) Parkin-deficient mice are not more sensitive to 6-hydroxydopamine or methamphetamine neurotoxicity. BMC Neurosci 6:71. doi: 10.1186/1471-2202-6-71
51. Hjerpe R, Aillet F, Lopitz-Otsoa F, Lang V, England P, Rodriguez MS (2009) Efficient protection and isolation of ubiquitylated proteins using tandem ubiquitin-binding entities. EMBO Rep 10(11):1250-1258. doi: 10.1038/embor.2009.192
52. Davison EJ, Pennington K, Hung CC, Peng J, Rafiq R, Ostareck-Lederer A, Ostareck DH, Ardley HC, Banks RE, Robinson PA (2009) Proteomic analysis of increased Parkin expression and its interactants provides evidence for a role in modulation of mitochondrial function. Proteomics 9(18):4284-4297. doi: 10.1002/pmic.200900126
53. Schlehe JS, Lutz AK, Pilsl A, Lammermann K, Grgur K, Henn IH, Tatzelt J, Winklhofer KF (2008) Aberrant folding of pathogenic Parkin mutants: aggregation versus degradation. J Biol Chem 283(20):13771-13779. doi: 10.1074/jbc.M707494200
54. Carmine Belin A, Westerlund M, Bergman O, Nissbrandt H, Lind C, Sydow O, Galter D (2007) S18Y in ubiquitin carboxy-terminal hydrolase L1 (UCH-L1) associated with decreased risk of Parkinson's disease in Sweden. Parkinsonism Relat Disord 13(5):295-298. doi: 10.1016/j.parkreldis.2006.12.002
55. Satoh J, Kuroda Y (2001) A polymorphic variation of serine to tyrosine at codon 18 in the ubiquitin C-terminal hydrolase-L1 gene is associated with a reduced risk of sporadic Parkinson's disease in a Japanese population. J Neurol Sci 189(1-2):113-117
56. Elbaz A, Levecque C, Clavel J, Vidal JS, Richard F, Correze JR, Delemotte B, Amouyel P, Alperovitch A, Chartier-Harlin MC, Tzourio C (2003) S18Y polymorphism in the UCH-L1 gene and Parkinson's disease: evidence for an age-dependent relationship. Mov Disord 18(2):130-137. doi: 10.1002/mds.10326
57. Maraganore DM, Lesnick TG, Elbaz A, Chartier-Harlin MC, Gasser T, Kruger R, Hattori N, Mellick GD, Quattrone A, Satoh J, Toda T, Wang J, Ioannidis JP, de Andrade M, Rocca WA (2004) UCHL1 is a Parkinson's disease susceptibility gene. Ann Neurol 55(4):512-521. doi: 10.1002/ana.20017
58. Wheeler TC, Chin LS, Li Y, Roudabush FL, Li L (2002) Regulation of synaptophysin degradation by mammalian homologues of seven in absentia. J Biol Chem 277(12):10273-10282. doi: 10.1074/jbc.M107857200
59. Lee JT, Wheeler TC, Li L, Chin LS (2008) Ubiquitination of alpha-synuclein by Siah-1 promotes alpha-synuclein aggregation and apoptotic cell death. Hum Mol Genet 17(6):906-917. doi: 10.1093/hmg/ddm363
60. Ciechanover A (2005) Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ 12(9):1178-1190. doi: 10.1038/sj.cdd.4401692
61. Rubinsztein DC (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443(7113):780-786. doi: 10.1038/nature05291
62. Meray RK, Lansbury PT Jr (2007) Reversible monoubiquitination regulates the Parkinson disease-associated ubiquitin hydrolase UCH-L1. J Biol Chem 282(14):10567-10575. doi: 10.1074/jbc.M611153200
63. Dawson TM, Dawson VL (2009) The role of parkin in familial and sporadic Parkinson's disease. Mov Disord 25(Suppl 1):9. doi: 10.1002/mds.22798
64. Chin LS, Olzmann JA, Li L (2010) Parkin-mediated ubiquitin signalling in aggresome formation and autophagy. Biochem Soc Trans 38(Pt 1):144-149. doi: 10.1042/BST0380144
65. Kirkin V, McEwan DG, Novak I, Dikic I (2009) A role for ubiquitin in selective autophagy. Mol Cell 34(3):259-269. doi: 10.1016/j.molcel.2009.04.026
66. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282(33):24131-24145. doi: 10.1074/jbc.M702824200
67. Wooten MW, Geetha T, Babu JR, Seibenhener ML, Peng J, Cox N, Diaz-Meco MT, Moscat J (2008) Essential role of sequestosome 1/p62 in regulating accumulation of Lys63-ubiquitinated proteins. J Biol Chem 283(11):6783-6789. doi: 10.1074/jbc.M709496200
68. Larsen CN, Price JS, Wilkinson KD (1996) Substrate binding and catalysis by ubiquitin C-terminal hydrolases: identification of two active site residues. Biochemistry 35(21):6735-6744. doi: 10.1021/bi960099f
69. Liu Y, Fallon L, Lashuel HA, Liu Z, Lansbury PT Jr (2002) The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Cell 111(2):209-218
70. Shulman JM, De Jager PL, Feany MB (2011) Parkinson's disease: genetics and pathogenesis. Annu Rev Pathol 6:193-222. doi: 10.1146/annurev-pathol-011110-130242
71. Mori H, Kondo T, Yokochi M, Matsumine H, Nakagawa-Hattori Y, Miyake T, Suda K, Mizuno Y (1998) Pathologic and biochemical studies of juvenile parkinsonism linked to chromosome 6q. Neurology 51(3):890-892
72. Takahashi H, Ohama E, Suzuki S, Horikawa Y, Ishikawa A, Morita T, Tsuji S, Ikuta F (1994) Familial juvenile parkinsonism: clinical and pathologic study in a family. Neurology 44(3 Pt 1):437-441
73. Goldberg MS, Fleming SM, Palacino JJ, Cepeda C, Lam HA, Bhatnagar A, Meloni EG, Wu N, Ackerson LC, Klapstein GJ, Gajendiran M, Roth BL, Chesselet MF, Maidment NT, Levine MS, Shen J (2003) Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J Biol Chem 278(44):43628-43635. doi: 10.1074/jbc.M308947200
74. Itier JM, Ibanez P, Mena MA, Abbas N, Cohen-Salmon C, Bohme GA, Laville M, Pratt J, Corti O, Pradier L, Ret G, Joubert C, Periquet M, Araujo F, Negroni J, Casarejos MJ, Canals S, Solano R, Serrano A, Gallego E, Sanchez M, Denefle P, Benavides J, Tremp G, Rooney TA, Brice A, Garcia de Yebenes J (2003) Parkin gene inactivation alters behaviour and dopamine neurotransmission in the mouse. Hum Mol Genet 12(18):2277-2291. doi: 10.1093/hmg/ddg239
75. Thao DT, An PN, Yamaguchi M, LinhThuoc T (2012) Overexpression of ubiquitin carboxyl terminal hydrolase impairs multiple pathways during eye development in Drosophila melanogaster. Cell Tissue Res 348(3):453-463. doi: 10.1007/s00441-012-1404-x
76. Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, Dawson VL, Dawson TM (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304(5675):1328-1331. doi: 10.1126/science.1093891
77. Yao D, Gu Z, Nakamura T, Shi ZQ, Ma Y, Gaston B, Palmer LA, Rockenstein EM, Zhang Z, Masliah E, Uehara T, Lipton SA (2004) Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci USA 101(29):10810-10814. doi: 10.1073/pnas.0404161101
78. Lowe J, McDermott H, Landon M, Mayer RJ, Wilkinson KD (1990) Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases. J Pathol 161(2):153-160. doi: 10.1002/path.1711610210