Ubiquitin phosphorylation in Parkinson's disease: Implications for pathogenesis and treatment

Translational Neurodegeneration

Volumn 5, Issue 1, 2016, Pages

  Chin, Lih Shen ^a   Li, Lian ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mitochondrial quality control; Mitophagy; Parkin; Parkinson's disease; PINK1; Ubiquitin phosphorylation; Ubiquitin protein ligase

Indexed keywords

DEUBIQUITINASE; FARNOQUINONE; MITOCHONDRIAL DNA; PARKIN; PINK1 KINASE; PROTEIN SERINE THREONINE KINASE; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; URSODEOXYCHOLIC ACID;

ARTICLE; AUTOPHAGY; AUTOSOMAL RECESSIVE DISORDER; CONFORMATIONAL TRANSITION; DEPOLARIZATION; HOMOZYGOSITY; HUMAN; LOSS OF FUNCTION MUTATION; MITOCHONDRIAL MEMBRANE; MITOPHAGY; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; UBIQUITINATION;

EID: 84953236597     PISSN: None     EISSN: 20479158     Source Type: Journal    
DOI: 10.1186/s40035-015-0049-6     Document Type: Article

References (90)

1. Lang AE, Lozano AM. Parkinson's disease. First of two parts. N Engl J Med. 1998;339(15):1044-53.
2. Lang AE, Lozano AM. Parkinson's disease. Second of two parts. N Engl J Med. 1998;339(16):1130-43.
3. Savitt JM, Dawson VL, Dawson TM. Diagnosis and treatment of Parkinson disease: molecules to medicine. J Clin Invest. 2006;116(7):1744-54.
4. Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K. Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res. 2004;318(1):121-34.
5. Goedert M, Spillantini MG, Del Tredici K, Braak H. 100 years of Lewy pathology. Nat Rev Neurol. 2013;9(1):13-24.
6. Olanow CW, Schapira AH. Therapeutic prospects for Parkinson disease. Ann Neurol. 2013;74(3):337-47.
7. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science. 2004;304(5674):1158-60.
8. Bonifati V, Rohe CF, Breedveld GJ, Fabrizio E, De Mari M, Tassorelli C, et al. Early-onset parkinsonism associated with PINK1 mutations: frequency, genotypes, and phenotypes. Neurology. 2005;65(1):87-95.
9. Tan EK, Skipper LM. Pathogenic mutations in Parkinson disease. Hum Mutat. 2007;28(7):641-53.
10. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 1998;392(6676):605-8.
11. Hattori N, Mizuno Y. Pathogenetic mechanisms of parkin in Parkinson's disease. Lancet. 2004;364(9435):722-4.
12. Weissman AM. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol. 2001;2(3):169-78.
13. Olzmann JA, Li L, Chin LS. Aggresome formation and neurodegenerative diseases: therapeutic implications. Curr Med Chem. 2008;15(1):47-60.
14. Komander D, Rape M. The ubiquitin code. Annu Rev Biochem. 2012;81:203-29.
15. Reyes-Turcu FE, Ventii KH, Wilkinson KD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem. 2009;78:363-97.
16. Sharma K, D'Souza RC, Tyanova S, Schaab C, Wisniewski JR, Cox J, et al. Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Rep. 2014;8(5):1583-94.
17. Lundby A, Secher A, Lage K, Nordsborg NB, Dmytriyev A, Lundby C, et al. Quantitative maps of protein phosphorylation sites across 14 different rat organs and tissues. Nat Commun. 2012;3:876.
18. Swaney DL, Rodriguez-Mias RA, Villen J. Phosphorylation of ubiquitin at Ser65 affects its polymerization, targets, and proteome-wide turnover. EMBO Rep. 2015;16(9):1131-44.
19. McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol. 2006;16(14):R551-60.
20. Herrmann JM, Riemer J. The intermembrane space of mitochondria. Antioxid Redox Signal. 2010;13(9):1341-58.
21. Cookson MR, Bandmann O. Parkinson's disease: insights from pathways. Hum Mol Genet. 2010;19(R1):R21-7.
22. Schon EA, Przedborski S. Mitochondria: the next (neurode)generation. Neuron. 2011;70(6):1033-53.
23. Schapira AH. Mitochondrial dysfunction in Parkinson's disease. Cell Death Differ. 2007;14(7):1261-6.
24. Hatano Y, Li Y, Sato K, Asakawa S, Yamamura Y, Tomiyama H, et al. Novel PINK1 mutations in early-onset parkinsonism.[erratum appears in Ann Neurol. 2004 Oct;56(4):603]. Ann Neurol. 2004;56(3):424-7.
25. Zadikoff C, Rogaeva E, Djarmati A, Sato C, Salehi-Rad S, St George-Hyslop P, et al. Homozygous and heterozygous PINK1 mutations: considerations for diagnosis and care of Parkinson's disease patients. Mov Disord. 2006;21(6):875-9.
26. Hedrich K, Hagenah J, Djarmati A, Hiller A, Lohnau T, Lasek K, et al. Clinical spectrum of homozygous and heterozygous PINK1 mutations in a large German family with Parkinson disease: role of a single hit? Arch Neurol. 2006;63(6):833-8.
27. Toft M, Myhre R, Pielsticker L, White LR, Aasly JO, Farrer MJ. PINK1 mutation heterozygosity and the risk of Parkinson's disease. J Neurol Neurosurg Psychiatry. 2007;78(1):82-4.
28. Sim CH, Gabriel K, Mills RD, Culvenor JG, Cheng HC. Analysis of the regulatory and catalytic domains of PTEN-induced kinase-1 (PINK1). Hum Mutat. 2012;33(10):1408-22.
29. Lazarou M, Jin SM, Kane LA, Youle RJ. Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev Cell. 2012;22(2):320-33.
30. Jin SM, Lazarou M, Wang C, Kane LA, Narendra DP, Youle RJ. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol. 2010;191(5):933-42.
31. Greene AW, Grenier K, Aguileta MA, Muise S, Farazifard R, Haque ME, et al. Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep. 2012;13(4):378-85.
32. Deas E, Plun-Favreau H, Gandhi S, Desmond H, Kjaer S, Loh SH, et al. PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum Mol Genet. 2011;20(5):867-79.
33. Meissner C, Lorenz H, Weihofen A, Selkoe DJ, Lemberg MK. The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J Neurochem. 2011;117(5):856-67.
34. Yamano K, Youle RJ. PINK1 is degraded through the N-end rule pathway. Autophagy. 2013;9(11):1758-69.
35. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010;8(1), e1000298.
36. Becker D, Richter J, Tocilescu MA, Przedborski S, Voos W. Pink1 kinase and its membrane potential (Deltapsi)-dependent cleavage product both localize to outer mitochondrial membrane by unique targeting mode. J Biol Chem. 2012;287(27):22969-87.
37. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A. 2010;107(1):378-83.
38. Zhou C, Huang Y, Shao Y, May J, Prou D, Perier C, et al. The kinase domain of mitochondrial PINK1 faces the cytoplasm. Proc Natl Acad Sci U S A. 2008;105(33):12022-7.
39. Gandhi S, Muqit MM, Stanyer L, Healy DG, Abou-Sleiman PM, Hargreaves I, et al. PINK1 protein in normal human brain and Parkinson's disease. Brain. 2006;129(Pt 7):1720-31.
40. Pridgeon JW, Olzmann JA, Chin LS, Li L. PINK1 Protects against Oxidative Stress by Phosphorylating Mitochondrial Chaperone TRAP1. PLoS Biol. 2007;5:e172.
41. Mills RD, Sim CH, Mok SS, Mulhern TD, Culvenor JG, Cheng HC. Biochemical aspects of the neuroprotective mechanism of PTEN-induced kinase-1 (PINK1). J Neurochem. 2008;105(1):18-33.
42. Muqit MM, Abou-Sleiman PM, Saurin AT, Harvey K, Gandhi S, Deas E, et al. Altered cleavage and localization of PINK1 to aggresomes in the presence of proteasomal stress. J Neurochem. 2006;98(1):156-69.
43. Silvestri L, Caputo V, Bellacchio E, Atorino L, Dallapiccola B, Valente EM, et al. Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism. Hum Mol Genet. 2005;14(22):3477-92.
44. Fallaize D, Chin LS, Li L. Differential submitochondrial localization of PINK1 as a molecular switch for mediating distinct mitochondrial signaling pathways. Cell Signal. 2015;27(12):2543-54.
45. Beinlich FR, Drees C, Piehler J, Busch KB. Shuttling of PINK1 between Mitochondrial Microcompartments Resolved by Triple-Color Superresolution Microscopy. ACS Chem Biol. 2015;10(9):1970-6.
46. Hertz NT, Berthet A, Sos ML, Thorn KS, Burlingame AL, Nakamura K, et al. A neo-substrate that amplifies catalytic activity of parkinson's-disease-related kinase PINK1. Cell. 2013;154(4):737-47.
47. Morais VA, Haddad D, Craessaerts K, De Bock PJ, Swerts J, Vilain S, et al. PINK1 loss-of-function mutations affect mitochondrial complex I activity via NdufA10 ubiquinone uncoupling. Science. 2014;344(6180):203-7.
48. Plun-Favreau H, Klupsch K, Moisoi N, Gandhi S, Kjaer S, Frith D, et al. The mitochondrial protease HtrA2 is regulated by Parkinson's disease-associated kinase PINK1. Nat Cell Biol. 2007;Sep 30; [Epub ahead of print]
49. Jin SM, Youle RJ. The accumulation of misfolded proteins in the mitochondrial matrix is sensed by PINK1 to induce PARK2/Parkin-mediated mitophagy of polarized mitochondria. Autophagy. 2013;9(11):1750-7.
50. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, et al. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol. 2010;189(2):211-21.
51. Okatsu K, Uno M, Koyano F, Go E, Kimura M, Oka T, et al. A dimeric PINK1-containing complex on depolarized mitochondria stimulates Parkin recruitment. J Biol Chem. 2013;288(51):36372-84.
52. Okatsu K, Oka T, Iguchi M, Imamura K, Kosako H, Tani N, et al. PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat Commun. 2012;3:1016.
53. Aerts L, Craessaerts K, De Strooper B, Morais VA. PINK1 kinase catalytic activity is regulated by phosphorylation on serines 228 and 402. J Biol Chem. 2015;290(5):2798-811.
54. Kane LA, Lazarou M, Fogel AI, Li Y, Yamano K, Sarraf SA, et al. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol. 2014;205(2):143-53.
55. Kazlauskaite A, Kondapalli C, Gourlay R, Campbell DG, Ritorto MS, Hofmann K, et al. Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem J. 2014;460(1):127-39.
56. Koyano F, Okatsu K, Kosako H, Tamura Y, Go E, Kimura M, et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature. 2014;510(7503):162-6.
57. Ordureau A, Sarraf SA, Duda DM, Heo JM, Jedrychowski MP, Sviderskiy VO, et al. Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol Cell. 2014;56(3):360-75.
58. Okatsu K, Koyano F, Kimura M, Kosako H, Saeki Y, Tanaka K, et al. Phosphorylated ubiquitin chain is the genuine Parkin receptor. J Cell Biol. 2015;209(1):111-28.
59. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, et al. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol. 2003;21(8):921-6.
60. Wauer T, Swatek KN, Wagstaff JL, Gladkova C, Pruneda JN, Michel MA, et al. Ubiquitin Ser65 phosphorylation affects ubiquitin structure, chain assembly and hydrolysis. EMBO J. 2015;34(3):307-25.
61. Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, et al. S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science. 2004;304(5675):1328-31.
62. Yao D, Gu Z, Nakamura T, Shi ZQ, Ma Y, Gaston B, et al. Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci U S A. 2004;101(29):10810-4.
63. Lavoie MJ, Ostaszewski BL, Weihofen A, Schlossmacher MG, Selkoe DJ. Dopamine covalently modifies and functionally inactivates parkin. Nat Med. 2005;11(11):1214-21.
64. Trempe JF, Sauve V, Grenier K, Seirafi M, Tang MY, Menade M, et al. Structure of parkin reveals mechanisms for ubiquitin ligase activation. Science. 2013;340(6139):1451-5.
65. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, Seol JH, et al. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature. 2006;441(7097):1162-6.
66. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, et al. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature. 2006;441(7097):1157-61.
67. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008;183(5):795-803.
68. Geisler S, Holmstrom KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol. 2010;12(2):119-31.
69. Sha D, Chin LS, Li L. Phosphorylation of parkin by Parkinson disease-linked kinase PINK1 activates parkin E3 ligase function and NF-kappaB signaling. Hum Mol Genet. 2010;19(2):352-63.
70. Shiba-Fukushima K, Imai Y, Yoshida S, Ishihama Y, Kanao T, Sato S, et al. PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep. 2012;2:1002.
71. Kondapalli C, Kazlauskaite A, Zhang N, Woodroof HI, Campbell DG, Gourlay R, et al. PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol. 2012;2(5):120080.
72. Wauer T, Simicek M, Schubert A, Komander D. Mechanism of phospho-ubiquitin-induced PARKIN activation. Nature. 2015;524(7565):370-4.
73. Kazlauskaite A, Martinez-Torres RJ, Wilkie S, Kumar A, Peltier J, Gonzalez A, et al. Binding to serine 65-phosphorylated ubiquitin primes Parkin for optimal PINK1-dependent phosphorylation and activation. EMBO Rep. 2015;16(8):939-54.
74. Sauve V, Lilov A, Seirafi M, Vranas M, Rasool S, Kozlov G, et al. A Ubl/ubiquitin switch in the activation of Parkin. EMBO J. 2015;34(20):2492-505.
75. Kumar A, Aguirre JD, Condos TE, Martinez-Torres RJ, Chaugule VK, Toth R, et al. Disruption of the autoinhibited state primes the E3 ligase parkin for activation and catalysis. EMBO J. 2015;34(20):2506-21.
76. Wauer T, Komander D. Structure of the human Parkin ligase domain in an autoinhibited state. EMBO J. 2013;32(15):2099-112.
77. Chan NC, Salazar AM, Pham AH, Sweredoski MJ, Kolawa NJ, Graham RL, et al. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet. 2011;20(9):1726-37.
78. Sarraf SA, Raman M, Guarani-Pereira V, Sowa ME, Huttlin EL, Gygi SP, et al. Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature. 2013;496(7445):372-6.
79. Ordureau A, Heo JM, Duda DM, Paulo JA, Olszewski JL, Yanishevski D, et al. Defining roles of PARKIN and ubiquitin phosphorylation by PINK1 in mitochondrial quality control using a ubiquitin replacement strategy. Proc Natl Acad Sci U S A. 2015;112(21):6637-42.
80. Lazarou M, Sliter DA, Kane LA, Sarraf SA, Wang C, Burman JL, et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015;524(7565):309-14.
81. Narendra DP, Wang C, Youle RJ, Walker JE. PINK1 rendered temperature sensitive by disease-associated and engineered mutations. Hum Mol Genet. 2013;22(13):2572-89.
82. Geisler S, Holmstrom KM, Treis A, Skujat D, Weber SS, Fiesel FC, et al. The PINK1/Parkin-mediated mitophagy is compromised by PD-associated mutations. Autophagy. 2010;6(7):871-8.
83. Fiesel FC, Ando M, Hudec R, Hill AR, Castanedes-Casey M, Caulfield TR, et al. (Patho-)physiological relevance of PINK1-dependent ubiquitin phosphorylation. EMBO Rep. 2015;16(9):1114-30.
84. Pickrell AM, Huang CH, Kennedy SR, Ordureau A, Sideris DP, Hoekstra JG, et al. Endogenous Parkin Preserves Dopaminergic Substantia Nigral Neurons following Mitochondrial DNA Mutagenic Stress. Neuron. 2015;87(2):371-81.
85. Kazlauskaite A, Kelly V, Johnson C, Baillie C, Hastie CJ, Peggie M, et al. Phosphorylation of Parkin at Serine65 is essential for activation: elaboration of a Miro1 substrate-based assay of Parkin E3 ligase activity. Open Bol. 2014;4:130213.
86. Durcan TM, Tang MY, Perusse JR, Dashti EA, Aguileta MA, McLelland GL, et al. USP8 regulates mitophagy by removing K6-linked ubiquitin conjugates from parkin. EMBO J. 2014;33(21):2473-91.
87. Cornelissen T, Haddad D, Wauters F, Van Humbeeck C, Mandemakers W, Koentjoro B, et al. The deubiquitinase USP15 antagonizes Parkin-mediated mitochondrial ubiquitination and mitophagy. Hum Mol Genet. 2014;23(19):5227-42.
88. Bingol B, Tea JS, Phu L, Reichelt M, Bakalarski CE, Song Q, et al. The mitochondrial deubiquitinase USP30 opposes parkin-mediated mitophagy. Nature. 2014;510(7505):370-5.
89. Mortiboys H, Aasly J, Bandmann O. Ursocholanic acid rescues mitochondrial function in common forms of familial Parkinson's disease. Brain. 2013;136(Pt 10):3038-50.
90. Vos M, Esposito G, Edirisinghe JN, Vilain S, Haddad DM, Slabbaert JR, et al. Vitamin K2 is a mitochondrial electron carrier that rescues pink1 deficiency. Science. 2012;336(6086):1306-10.