PINK1 and Parkin target miro for phosphorylation and degradation to arrest mitochondrial motility

Cell

Volumn 147, Issue 4, 2011, Pages 893-906

  Wang, Xinnan ^a,b   Winter, Dominic ^a   Ashrafi, Ghazaleh ^a,c   Schlehe, Julia ^d   Wong, Yao Liang ^e   Selkoe, Dennis ^d   Rice, Sarah ^e   Steen, Judith ^a   Lavoie, Matthew J ^d   Schwarz, Thomas L ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD UNIVERSITY   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; KINESIN; MIRO PROTEIN; PARKIN; PINK1 PROTEIN; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MOTILITY; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; MITOCHONDRION; MOUSE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RAT; REGULATORY MECHANISM;

EID: 81055140895     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.10.018     Document Type: Article

References (48)

1. A.K. Berger, G.P. Cortese, K.D. Amodeo, A. Weihofen, A. Letai, and M.J. LaVoie Parkin selectively alters the intrinsic threshold for mitochondrial cytochrome c release Hum. Mol. Genet. 18 2009 4317 4328
2. K. Brickley, M.J. Smith, M. Beck, and F.A. Stephenson GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin J. Biol. Chem. 280 2005 14723 14732
3. K. Brickley, K. Pozo, and F.A. Stephenson N-acetylglucosamine transferase is an integral component of a kinesin-directed mitochondrial trafficking complex Biochim. Biophys. Acta 1813 2011 269 281
4. N.C. Chan, A.M. Salazar, A.H. Pham, M.J. Sweredoski, N.J. Kolawa, R.L. Graham, S. Hess, and D.C. Chan Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy Hum. Mol. Genet. 20 2011 1726 1737
5. I.E. Clark, M.W. Dodson, C. Jiang, J.H. Cao, J.R. Huh, J.H. Seol, S.J. Yoo, B.A. Hay, and M. Guo Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin Nature 441 2006 1162 1166
6. E. Deas, H. Plun-Favreau, S. Gandhi, H. Desmond, S. Kjaer, S.H. Loh, A.E. Renton, R.J. Harvey, A.J. Whitworth, and L. Martins PINK1 cleavage at position A103 by the mitochondrial protease PARL Hum. Mol. Genet. 20 2011 867 879
7. H. Deng, M.W. Dodson, H. Huang, and M. Guo The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila Proc. Natl. Acad. Sci. USA 105 2008 14503 14508
8. N. Exner, B. Treske, D. Paquet, K. Holmström, C. Schiesling, S. Gispert, I. Carballo-Carbajal, D. Berg, H.H. Hoepken, and T. Gasser Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin J. Neurosci. 27 2007 12413 12418
9. S. Fransson, A. Ruusala, and P. Aspenström The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking Biochem. Biophys. Res. Commun. 344 2006 500 510
10. R.L. Frederick, and J.M. Shaw Moving mitochondria: establishing distribution of an essential organelle Traffic 8 2007 1668 1675
11. S. Gandhi, A. Wood-Kaczmar, Z. Yao, H. Plun-Favreau, E. Deas, K. Klupsch, J. Downward, D.S. Latchman, S.J. Tabrizi, and N.W. Wood PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death Mol. Cell 33 2009 627 638
12. C.A. Gautier, T. Kitada, and J. Shen Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress Proc. Natl. Acad. Sci. USA 105 2008 11364 11369
13. S. Geisler, K.M. Holmström, D. Skujat, F.C. Fiesel, O.C. Rothfuss, P.J. Kahle, and W. Springer PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1 Nat. Cell Biol. 12 2010 119 131
14. E.E. Glater, L.J. Megeath, R.S. Stowers, and T.L. Schwarz Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent J. Cell Biol. 173 2006 545 557
15. M.S. Goldberg, S.M. Fleming, J.J. Palacino, C. Cepeda, H.A. Lam, A. Bhatnagar, E.G. Meloni, N. Wu, L.C. Ackerson, and G.J. Klapstein Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons J. Biol. Chem. 278 2003 43628 43635
16. S.M. Jin, M. Lazarou, C. Wang, L.A. Kane, D.P. Narendra, and R.J. Youle Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL J. Cell Biol. 191 2010 933 942
17. M. Karbowski, and R.J. Youle Regulating mitochondrial outer membrane proteins by ubiquitination and proteasomal degradation Curr. Opin. Cell Biol. 23 2011 476 482
18. T. Kitada, S. Asakawa, N. Hattori, H. Matsumine, Y. Yamamura, S. Minoshima, M. Yokochi, Y. Mizuno, and N. Shimizu Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism Nature 392 1998 605 608
19. A.F. Macaskill, J.E. Rinholm, A.E. Twelvetrees, I.L. Arancibia-Carcamo, J. Muir, A. Fransson, P. Aspenstrom, D. Attwell, and J.T. Kittler Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses Neuron 61 2009 541 555
20. A. Misko, S. Jiang, I. Wegorzewska, J. Milbrandt, and R.H. Baloh Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex J. Neurosci. 30 2010 4232 4240
21. D.P. Narendra, A. Tanaka, D.F. Suen, and R.J. Youle Parkin is recruited selectively to impaired mitochondria and promotes their autophagy J. Cell Biol. 183 2008 795 803
22. D.P. Narendra, S.M. Jin, A. Tanaka, D.F. Suen, C.A. Gautier, J. Shen, M.R. Cookson, and R.J. Youle PINK1 is selectively stabilized on impaired mitochondria to activate Parkin PLoS Biol. 8 2010 e1000298
23. J.J. Palacino, D. Sagi, M.S. Goldberg, S. Krauss, C. Motz, M. Wacker, J. Klose, and J. Shen Mitochondrial dysfunction and oxidative damage in parkin-deficient mice J. Biol. Chem. 279 2004 18614 18622
24. J.H. Park, A.J. Schroeder, C. Helfrich-Förster, F.R. Jackson, and J. Ewer Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior Development 130 2003 2645 2656
25. J. Park, S.B. Lee, S. Lee, Y. Kim, S. Song, S. Kim, E. Bae, J. Kim, M. Shong, J.M. Kim, and J. Chung Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin Nature 441 2006 1157 1161
26. A.D. Pilling, D. Horiuchi, C.M. Lively, and W.M. Saxton Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons Mol. Biol. Cell 17 2006 2057 2068
27. A.C. Poole, R.E. Thomas, L.A. Andrews, H.M. McBride, A.J. Whitworth, and L.J. Pallanck The PINK1/Parkin pathway regulates mitochondrial morphology Proc. Natl. Acad. Sci. USA 105 2008 1638 1643
28. A.C. Poole, R.E. Thomas, S. Yu, E.S. Vincow, and L.J. Pallanck The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINK1/parkin pathway PLoS ONE 5 2010 e10054
29. M. Saotome, D. Safiulina, G. Szabadkai, S. Das, A. Fransson, P. Aspenstrom, R. Rizzuto, and G. Hajnóczky Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase Proc. Natl. Acad. Sci. USA 105 2008 20728 20733
30. E.A. Schon, and S. Przedborski Mitochondria: the next (neurode)generation Neuron 70 2011 1033 1053
31. J.H. Shin, H.S. Ko, H. Kang, Y. Lee, Y.I. Lee, O. Pletinkova, J.C. Troconso, V.L. Dawson, and T.M. Dawson PARIS (ZNF746) repression of PGC-1α contributes to neurodegeneration in Parkinson's disease Cell 144 2011 689 702
32. S.R. Sriram, X. Li, H.S. Ko, K.K. Chung, E. Wong, K.L. Lim, V.L. Dawson, and T.M. Dawson Familial-associated mutations differentially disrupt the solubility, localization, binding and ubiquitination properties of parkin Hum. Mol. Genet. 14 2005 2571 2586
33. R.S. Stowers, L.J. Megeath, J. Górska-Andrzejak, I.A. Meinertzhagen, and T.L. Schwarz Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein Neuron 36 2002 1063 1077
34. D.J. Surmeier, J.N. Guzman, J. Sanchez-Padilla, and J.A. Goldberg What causes the death of dopaminergic neurons in Parkinson's disease? Prog. Brain Res. 183 2010 59 77
35. G. Twig, X. Liu, M. Liesa, J.D. Wikstrom, A.J. Molina, G. Las, G. Yaniv, G. Hajnóczky, and O.S. Shirihai Biophysical properties of mitochondrial fusion events in pancreatic beta-cells and cardiac cells unravel potential control mechanisms of its selectivity Am. J. Physiol. Cell Physiol. 299 2010 C477 C487
36. E.M. Valente, P.M. Abou-Sleiman, V. Caputo, M.M. Muqit, K. Harvey, S. Gispert, Z. Ali, D. Del Turco, A.R. Bentivoglio, and D.G. Healy Hereditary early-onset Parkinson's disease caused by mutations in PINK1 Science 304 2004 1158 1160
37. V.S. Van Laar, B. Arnold, S.J. Cassady, C.T. Chu, E.A. Burton, and S.B. Berman Bioenergetics of neurons inhibit the translocation response of Parkin following rapid mitochondrial depolarization Hum. Mol. Genet. 20 2011 927 940
38. K. Venderova, G. Kabbach, E. Abdel-Messih, Y. Zhang, R.J. Parks, Y. Imai, S. Gehrke, J. Ngsee, M.J. Lavoie, and R.S. Slack Leucine-Rich Repeat Kinase 2 interacts with Parkin, DJ-1 and PINK-1 in a Drosophila melanogaster model of Parkinson's disease Hum. Mol. Genet. 18 2009 4390 4404
39. C. Vives-Bauza, and S. Przedborski Mitophagy: the latest problem for Parkinson's disease Trends Mol. Med. 17 2011 158 165
40. X. Wang, and T.L. Schwarz The mechanism of Ca2+ -dependent regulation of kinesin-mediated mitochondrial motility Cell 136 2009 163 174
41. X. Wang, and T.L. Schwarz Imaging axonal transport of mitochondria Methods Enzymol. 457 2009 319 333
42. A. Weihofen, K.J. Thomas, B.L. Ostaszewski, M.R. Cookson, and D.J. Selkoe Pink1 forms a multiprotein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking Biochemistry 48 2009 2045 2052
43. A.J. Whitworth, and L.J. Pallanck The PINK1/Parkin pathway: a mitochondrial quality control system? J. Bioenerg. Biomembr. 41 2009 499 503
44. Y. Yang, S. Gehrke, Y. Imai, Z. Huang, Y. Ouyang, J.W. Wang, L. Yang, M.F. Beal, H. Vogel, and B. Lu Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin Proc. Natl. Acad. Sci. USA 103 2006 10793 10798
45. R.J. Youle, and D.P. Narendra Mechanisms of mitophagy Nat. Rev. Mol. Cell Biol. 12 2011 9 14
46. E. Ziviani, R.N. Tao, and A.J. Whitworth Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin Proc. Natl. Acad. Sci. USA 107 2010 5018 5023
47. C. Zhou, Y. Huang, Y. Shao, J. May, D. Prou, C. Perier, W. Dauer, E.A. Schon, and S. Przedborski The kinase domain of mitochondrial PINK1 faces the cytoplasm Proc. Natl. Acad. Sci. USA 105 2008 12022 12027
48. Winter, D.; Seidler, J.; Ziv, Y.; Shiloh, Y.; and Lehmann, W.D. (2009). Citrate boosts the performance of phosphopeptide analysis by UPLC-ESI-MS/MS. J. Proteome Res. 8, 418-424.