Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin

Journal of Cell Biology

Volumn 191, Issue 7, 2010, Pages 1367-1380

  Tanaka, Atsushi ^a   Cleland, Megan M ^a   Xu, Shan ^b   Narendra, Derek P ^a   Suen, Der Fen ^a   Karbowski, Mariusz ^b   Youle, Richard J ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE; MITOFUSIN 1; MITOFUSIN 2; PARKIN; PROTEASOME; PROTEIN P97;

ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL FUSION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; UBIQUITINATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; AUTOPHAGY; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; CELL LINE, TUMOR; FIBROBLASTS; GTP PHOSPHOHYDROLASES; HCT116 CELLS; HELA CELLS; HUMANS; LEUPEPTINS; MEMBRANE FUSION; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN KINASES; RNA, SMALL INTERFERING; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 78650729600     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201007013     Document Type: Article

References (57)

1. Amiott, E.A., M.M. Cohen, Y. Saint-Georges, A.M. Weissman, and J.M. Shaw. 2009. A mutation associated with CMT2A neuropathy causes defects in Fzol GTP hydrolysis, ubiquitylation, and protein turnover. Mol. Biol. Cell. 20:5026-5035. doi:10.1091/mbc.E09-07-0622
2. Betarbet, R., T.B. Sherer, G. MacKenzie, M. Garcia-Osuna, A.V. Panov, and J.T. Greenamyre. 2000. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3:1301-1306. doi:10.1038/81834
3. Brooks, A.I., C.A. Chadwick, H.A. Gelbard, D.A. Cory-Slechta, and H.J. Federoff. 1999. Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res. 823:1-10. doi:10.1016/S0006-8993(98)01192-5 (Pubitemid 29225488)
4. Btieler, H. 2009. Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson's disease. Exp. Neurol. 218:235-246. doi:10.1016/j.expneurol.2009.03.006
5. Chen, H., A. Chomyn, and D.C. Chan. 2005. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280:26185-26192. doi:10.1074/jbc.M503062200 (Pubitemid 41022214)
6. Cipolat, S., O. Martins de Brito, B. Dal Zilio, and L. Scorrano. 2004. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl. Acad. Sci. USA. 101:15927-15932. doi:10.1073/pnas.0407043101 (Pubitemid 39507904)
7. Clark, I.E., M.W. Dodson, C. Jiang, J.H. Cao, J.R. Huh, J.H. Seol, S.J. Yoo, B.A. Hay, and M. Guo. 2006. Drosophila pinkl is required for mitochondrial function and interacts genetically with parkin. Nature. 441:1162-1166. doi: 10.1038/nature04779 (Pubitemid 43990738)
8. Cocheme, H.M., and M.P Murphy. 2008. Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem. 283:1786-1798. doi:10.1074/jbc.M708597200
9. Cohen, M.M., G.P Leboucher, N. Livnat-Levanon, M.H. Glickman, and A.M. Weissman. 2008. Ubiquitin-proteasome-dependent degradation of a mitofusin, a critical regulator of mitochondrial fusion. Mol. Biol. Cell. 19:2457-2464. doi:10.1091/mbc.E08-02-0227
10. Dagda, R.K., S.J. Cherra III, S.M. Kulich, A. Tandon, D. Park, and C.T. Chu. 2009. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem. 284:13843-13855. doi:10.1074/jbc.M808515200
11. Deng, H., M.W. Dodson, H. Huang, and M. Guo. 2008. The Parkinson's disease genes pinkl and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl. Acad. Sci. USA. 105:14503-14508. doi:10.1073/pnas.0803998105
12. Denison, S.R., F. Wang, N.A. Becker, B. Schtile, N. Kock, L.A. Phillips, C. Klein, and D.I. Smith. 2003. Alterations in the common fragile site gene Parkin in ovarian and other cancers. Oncogene. 22:8370-8378. doi: 10.1038/sj.onc. 1207072
13. Dtirr, M., M. Escobar-Henriques, S. Merz, S. Geimer, T. Langer, and B. Westermann. 2006. Nonredundant roles of mitochondria-associated F-box proteins Mfbl and Mdm30 in maintenance of mitochondrial morphology in yeast. Mol. Biol. Cell. 17:3745-3755. doi:10.1091/mbc.E06-01-0053 (Pubitemid 44330862)
14. Escobar-Henriques, M., B. Westermann, and T. Langer. 2006. Regulation of mitochondrial fusion by the F-box protein Mdm30 involves protea-some-independent turnover of Fzol. J. Cell Biol. 173:645-650. doi:10,1083/jcb.200512079
15. Exner, N., B. Treske, D. Paquet, K. Holmstrom, C. Schiesling, S. Gispert, I. Carballo-Carbajal, D. Berg, H.H. Hoepken, T. Gasser, et al. 2007. Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J. Neurosci. 27:12413-12418. doi: 10.1523/JNEUROSCI. 0719-07.2007
16. Fallon, L., CM. Belanger, A.T. Corera, M. Kontogiannea, E. Regan-Klapisz, F Moreau, J. Voortman, M. Haber, G. Rouleau, T. Thorarinsdottir, et al. 2006. A regulated interaction with the UIM protein Epsl5 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat. Cell Biol. 8:834-842. doi:10.1038/ncbl441
17. Geisler, S., K.M. Holmstrom, D. Skujat, EC. Fiesel, O.C. Rothfuss, P.J. Kahle, and W Springer. 2010. PINK 1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTMl. Nat Cell Biol. 12:119-131. doi:10.1038/ncb2012
18. Greene, J.C., A.J. Whitworth, I. Kuo, L.A. Andrews, M.B. Feany, and L.J. Pallanck. 2003. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl. Acad. Sci. USA. 100:4078-4083. doi:10.1073/pnas.0737556100 (Pubitemid 36418160)
19. Griparic, L., T. Kanazawa, and A.M. van der Bliek. 2007. Regulation of the mitochondrial dynamin-like protein Opal by proteolytic cleavage. J. Cell Biol. 178:757-764. doi:10.1083/jcb.200704112 (Pubitemid 47347361)
20. Ishihara, N., Y. Fujita, T. Oka, and K. Mihara. 2006. Regulation of mitochondrial morphology through proteolytic cleavage of OPAL EMBO J. 25:2966-2977. doi:10.1038/sj.emboj.7601184 (Pubitemid 44106750)
21. Ishihara, N., M. Nomura, A. Jofuku, H. Kato, S.O. Suzuki, K. Masuda, H. Otera, Y Nakanishi, I. Nonaka, Y Goto, et al. 2009. Mitochondrial fission factor Drpl is essential for embryonic development and synapse formation in mice. Ato. Cell Biol. 11:958-966. doi:10.1038/ncbl907
22. Kanki, T., K. Wang, M. Baba, C.R. Bartholomew, M.A. Lynch-Day, Z. Du, J. Geng, K. Mao, Z. Yang, W.L. Yen, and D.J. Klionsky. 2009. A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol. Biol. Cell. 20:4730-4738. doi:10.1091/mbc.E09-03-0225
23. Karbowski, M., K.L. Norris, M.M. Cleland, S.Y Jeong, and R.J. Youle. 2006. Role of Bax and Bak in mitochondrial morphogenesis. Nature. 443:658-662. doi:10.1038/nature05111 (Pubitemid 44564703)
24. Karbowski, M., A. Neutzner, and R.J. Youle. 2007. The mitochondrial E3 ubiq-uitin ligase MARCH5 is required for Drp 1 dependent mitochondrial division. J. Cell Biol. 178:71-84. doi:10.1083/jcb.200611064 (Pubitemid 47026403)
25. Kim, I., S. Rodriguez-Enriquez, and J.J. Lemasters. 2007. Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 462:245-253. doi:10.1016/j.abb.2007.03.034 (Pubitemid 46876640)
26. Kitada, T, S. Asakawa, N. Hattori, H. Matsumine, Y Yamamura, S. Minoshima, M. Yokochi, Y Mizuno, and N. Shimizu. 1998. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 392:605-608. doi:10.1038/33416 (Pubitemid 28207717)
27. Krick, R., S. Bremer, E. Welter, P. Schlotterhose, Y Muehe, E.L. Eskelinen, and M. Thumm. 2010. Cdc48/p97 and Shpl/p47 regulate autophagosome biogenesis in concert with ubiquitin-like Atg8. J. Cell Biol 190:965-973. doi:10.1083/jcb.201002075
28. Lee, J.Y., Y. Nagano, J.P. Taylor, K.L. Lim, and T.P. Yao. 2010. Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J. Cell Biol. 189:671-679. doi:10.1083/jcb.201001039
29. Li, H., and M. Guo. 2009. Protein degradation in Parkinson disease revisited: it's complex. J. Clin. Invest. 119:442-445. doi:10.1172/JCI38619
30. Lutz, A.K., N. Exner, M.E. Fett, J.S. Schlehe, K. Kloos, K. Lammermann, B. Brunner, A. Kurz-Drexler, F. Vogel, A.S. Reichert, et al. 2009. Loss of parkin or PINK1 function increases Drpl-dependent mitochondrial fragmentation. J. Biol. Chem. 284:22938-22951. doi:10.1074/jbc.M109.035774
31. Matsuda, N., and K. Tanaka. 2010. Does impairment of the ubiquitin-protea-some system or the autophagy-lysosome pathway predispose individuals to neurodegenerative disorders such as Parkinson's disease? J. Alzheimers Dis. 19:1-9.
32. Matsuda, N., T. Kitami, T. Suzuki, Y Mizuno, N. Hattori, and K. Tanaka. 2006. Diverse effects of pathogenic mutations of Parkin that catalyze multiple monoubiquitylation in vitro. J. Biol. Chem. 281:3204-3209. doi:10.1074/jbc. M510393200 (Pubitemid 43845931)
33. Matsuda, N., S. Sato, K. Shiba, K. Okatsu, K. Saisho, C.A. Gautier, YS. Sou, S. Saiki, S. Kawajiri, F Sato, et al. 2010. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J. Cell Biol. 189:211-221. doi:10.1083/jcb.200910140
34. Narendra, D., A. Tanaka, D.F Suen, and R.J. Youle. 2008. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol 183:795-803. doi:10.1083/jcb.200809125
35. Narendra, D.P, S.M. Jin, A. Tanaka, D.F. Suen, C.A. Gautier, J. Shen, M.R. Cookson, and R.J. Youle. 2010. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8:el000298. doi:10.1371/journal. pbio. 1000298
36. Neutzner, A., and R.J. Youle. 2005. Instability of the mitofusin Fzol regulates mitochondrial morphology during the mating response of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 280:18598-18603. doi:10.1074/jbc. M500807200 (Pubitemid 41379558)
37. Neutzner, A., R.J. Youle, and M. Karbowski. 2007. Outer mitochondrial membrane protein degradation by the proteasome. Novartis Found. Symp. 287:4-14, discussion:14-20. doi:10.1002/9780470725207.ch2
38. Nowikovsky, K., S. Reipert, R.J. Devenish, and R.J. Schweyen. 2007. Mdm38 protein depletion causes loss of mitochondrial K+/H+ exchange activity, osmotic swelling and mitophagy. Cell Death Differ. 14:1647-1656. doi:10.1038/sj.cdd. 4402167 (Pubitemid 47278850)
39. Park, J., S.B. Lee, S. Lee, Y Kim, S. Song, S. Kim, E. Bae, J. Kim, M. Shong, J.M. Kim, and J. Chung. 2006. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature. 441:1157-1161. doi:10.1038/nature04788 (Pubitemid 43990737)
40. Park, J., G. Lee, and J. Chung. 2009. The PINKl-Parkin pathway is involved in the regulation of mitochondrial remodeling process. Biochem. Biophys. Res. Commun. 378:518-523. doi:10.1016/j.bbrc.2008.11.086
41. Pawlyk, A.C., B.I. Giasson, D.M. Sampathu, FA. Perez, K.L. Lim, V.L. Dawson, T.M. Dawson, R.D. Palmiter, J.Q. Trojanowski, and V.M. Lee. 2003. Novel monoclonal antibodies demonstrate biochemical variation of brain parkin with age. J. Biol. Chem. 278:48120-48128. doi:10.1074/jbc.M306889200 (Pubitemid 37523264)
42. Phair, R.D., and T Misteli. 2000. High mobility of proteins in the mammalian cell nucleus. Nature. 404:604-609. doi: 10.1038/35007077 (Pubitemid 30205058)
43. Poole, A.C., R.E. Thomas, L.A. Andrews, H.M. McBride, A.J. Whitworth, and L.J. Pallanck. 2008. The PINKl/Parkin pathway regulates mitochondrial morphology. Proc. Natl. Acad. Sci. USA. 105:1638-1643. doi:10.1073/pnas. 0709336105 (Pubitemid 351346567)
44. Poole, A.C., R.E. Thomas, S. Yu, E.S. Vincow, and L. Pallanck. 2010. The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINKl/parkin pathway. PLoS One. 5:el0054. doi:10.1371/journal.pone.0010054
45. Rabinovich, E., A. Kerem, K.U. Frohlich, N. Diamant, and S. Bar-Nun. 2002. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell. Biol. 22: 626-634. doi: 10.1128/MCB.22.2.626-634.2002 (Pubitemid 34027506)
46. Rizzuto, R., P. Pinton, W. Carrington, FS. Fay, K.E. Fogarty, L.M. Lifshitz, R.A. Tuft, and T Pozzan. 1998. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 280:1763-1766. doi: 10.1126/science.280.5370.1763 (Pubitemid 28283502)
47. Sandebring, A., K.J. Thomas, A. Beilina, M. van der Brug, M.M. Cleland, R. Ahmad, D.W. Miller, I. Zambrano, R.F Cowburn, H. Behbahani, et al. 2009. Mitochondrial alterations in PINK1 deficient cells are influenced by calcineurin-dependent dephosphorylation of dynamin-related protein 1. PLoS One. 4:e5701. doi:10.1371/journal.pone.0005701
48. Staropoli, J.F, C. McDermott, C. Martinat, B. Schulman, E. Demireva, and A. Abeliovich. 2003. Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron. 37:735-749. doi:10.1016/S0896-6273(03)00084-9 (Pubitemid 36288547)
49. Tresse, E., FA. Salomons, J. Vesa, L.C. Bott, V. Kimonis, T.P. Yao, N.P Dantuma, and J.P. Taylor. 2010. VCP/p97 is essential for maturation of ubiquitin-containing autophagosomes and this function is impaired by mutations that cause IBMPFD. Autophagy. 6:217-227. doi:10.4161/auto.6.2.11014
50. Twig, G., A. Elorza, A.J. Molina, H. Mohamed, J.D. Wikstrom, G. Walzer, L. Stiles, S.E. Haigh, S. Katz, G. Las, et al. 2008. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBOJ. 27:433-146. doi:10.1038/sj.emboj.7601963 (Pubitemid 351161653)
51. Valente, E.M., P.M. Abou-Sleiman, V. Caputo, M.M. Muqit, K. Harvey, S. Gispert, Z. Ali, D. Del Turco, A.R. Bentivoglio, D.G. Healy, et al. 2004. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science. 304:1158-1160. doi: 10.1126/science. 1096284
52. Vives-Bauza, C, C. Zhou, Y Huang, M. Cui, R.L. de Vries, J. Kim, J. May, M.A. Tocilescu, W. Liu, H.S. Ko, et al. 2010. PINK 1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc. Natl. Acad. Sci. USA. 107:378-383. doi:10.1073/pnas.0911187107
53. Yang, Y, S. Gehrke, Y Imai, Z. Huang, Y Ouyang, J.W. Wang, L. Yang, M.F Beal, H. Vogel, and B. Lu. 2006. Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pinkl is rescued by Parkin. Proc. Natl. Acad. Sci. USA. 103:10793-10798. doi: 10.1073/pnas.0602493103 (Pubitemid 44078055)
54. Yang, Y, Y Ouyang, L. Yang, M.F. Beal, A. McQuibban, H. Vogel, and B. Lu. 2008. Pinkl regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc. Natl. Acad. Sci. USA. 105:7070-7075. doi: 10.1073/pnas.0711845105 (Pubitemid 351754531)
55. Ye, Y, H.H. Meyer, and T.A. Rapoport. 2001. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature. 414:652-656. doi:10.1038/414652a (Pubitemid 33151262)
56. Ye, Y, H.H. Meyer, and T.A. Rapoport. 2003. Function of the p97-Ufdl-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol 162:71-84. doi:10.1083/jcb.200302169 (Pubitemid 36859536)
57. Ziviani, E., R.N. Tao, and A.J. Whitworth. 2010. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. USA. 107:5018-5023. doi: 10.1073/pnas.0913485107