Lysine 27 ubiquitination of the mitochondrial transport protein miro is dependent on serine 65 of the parkin ubiquitin ligase

Journal of Biological Chemistry

Volumn 289, Issue 21, 2014, Pages 14569-14582

  Birsa, Nicol ^a   Norkett, Rosalind ^a   Wauer, Tobias ^b   Mevissen, Tycho E T ^b   Wu, Hsiu Chuan ^a   Foltynie, Thomas ^a   Bhatia, Kailash ^a   Hirst, Warren D ^c   Komander, David ^b   Plun Favreau, Helene ^a   Kittler, Josef T ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL CULTURE; CELL MEMBRANES; DISEASES; GENE ENCODING; MACHINERY; PHOSPHORYLATION; PROTEINS;

BUFFERING REQUIREMENTS; ENERGY PRODUCTIONS; MITOCHONDRIAL DAMAGE; NEUROBLASTOMA CELLS; OUTER MITOCHONDRIAL MEMBRANES; PATHOGENIC MUTATION; PROTEASOMAL DEGRADATION; TRANSPORT PROTEINS;

MITOCHONDRIA;

CARRIER PROTEIN; LYSINE; PARKIN; PROTEASOME; PROTEIN MIRO; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; COMPLEX FORMATION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYO; FEMALE; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MALE; MITOCHONDRION; NEUROBLASTOMA CELL; NEUROPATHOLOGY; NONHUMAN; PARK2 GENE; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; RAT; UBIQUITINATION;

MITOCHONDRIAL TRANSPORT; MITOPHAGY; PARKIN; PARKINSON DISEASE; PINK1; UBIQUITINATION;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; FIBROBLASTS; HEK293 CELLS; HELA CELLS; HUMANS; LYSINE; MALE; MICROSCOPY, CONFOCAL; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MUTATION; PARKINSON DISEASE; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN KINASES; RATS, SPRAGUE-DAWLEY; RHO GTP-BINDING PROTEINS; RNA INTERFERENCE; SERINE; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84901407276     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.563031     Document Type: Article

References (49)

1. Macaskill, A. F., Rinholm, J. E., Twelvetrees, A. E., Arancibia-Carcamo, I. L., Muir, J., Fransson, A., Aspenstrom, P., Attwell, D., and Kittler, J. T. (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61, 541-555
2. 2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 136, 163-174
3. Russo, G. J., Louie, K., Wellington, A., Macleod, G. T., Hu, F., Panchumarthi, S., and Zinsmaier, K. E. (2009) Drosophila Miro is required for both anterograde and retrograde axonal mitochondrial transport. J. Neurosci. 29, 5443-5455
4. 2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc. Natl. Acad. Sci. U.S.A. 105, 20728-20733
5. Fransson, A., Ruusala, A., and Aspenström, P. (2003) Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J. Biol. Chem. 278, 6495-6502 (Pubitemid 36800910)
6. Thomas, B., and Beal, M. F. (2007) Parkinson's disease. Hum. Mol. Genet. 16, R183-R194
7. Deas, E., Plun-Favreau, H., Gandhi, S., Desmond, H., Kjaer, S., Loh, S. H., Renton, A. E., Harvey, R. J., Whitworth, A. J., Martins, L. M., Abramov, A. Y., and Wood, N. W. (2011) PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum. Mol. Genet. 20, 867-879
8. Jin, S. M., Lazarou, M., Wang, C., Kane, L. A., Narendra, D. P., and Youle, R. J. (2010) Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 191, 933-942
9. Vives-Bauza, C., Zhou, C., Huang, Y., Cui, M., de Vries, R. L., Kim, J., May, J., Tocilescu, M. A., Liu, W., Ko, H. S., Magrané, J., Moore, D. J., Dawson, V. L., Grailhe, R., Dawson, T. M., Li, C., Tieu, K., and Przedborski, S. (2010) PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc. Natl. Acad. Sci. U.S.A. 107, 378-383
10. Sarraf, S. A., Raman, M., Guarani-Pereira, V., Sowa, M. E., Huttlin, E. L., Gygi, S. P., and Harper, J. W. (2013) Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 496, 372-376
11. Cai, Q., Zakaria, H. M., Simone, A., and Sheng, Z. H. (2012) Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr. Biol. 22, 545-552
12. Exner, N., Lutz, A. K., Haass, C., and Winklhofer, K. F. (2012) Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J. 31, 3038-3062
13. Geisler, S., Holmström, K. M., Skujat, D., Fiesel, F. C., Rothfuss, O. C., Kahle, P. J., and Springer, W. (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131
14. Wang, H., Song, P., Du, L., Tian, W., Yue, W., Liu, M., Li, D., Wang, B., Zhu, Y., Cao, C., Zhou, J., and Chen, Q. (2011) Parkin ubiquitinates Drp1 for proteasome- dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson disease. J. Biol. Chem. 286, 11649-11658
15. Ziviani, E., Tao, R. N., and Whitworth, A. J. (2010) Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. U.S.A. 107, 5018-5023
16. Yoshii, S. R., Kishi, C., Ishihara, N., and Mizushima, N. (2011) Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J. Biol. Chem. 286, 19630-19640
17. Poole, A. C., Thomas, R. E., Yu, S., Vincow, E. S., and Pallanck, L. (2010) The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINK1/parkin pathway. PLoS One 5, e10054
18. Wang, X., Winter, D., Ashrafi, G., Schlehe, J., Wong, Y. L., Selkoe, D., Rice, S., Steen, J., LaVoie, M. J., and Schwarz, T. L. (2011) PINK1 and Parkin target miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147, 893-906
19. Liu, S., Sawada, T., Lee, S., Yu, W., Silverio, G., Alapatt, P., Millan, I., Shen, A., Saxton, W., Kanao, T., Takahashi, R., Hattori, N., Imai, Y., and Lu, B. (2012) Parkinson's disease-associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet. 8, e1002537
20. Chan, N. C., Salazar, A. M., Pham, A. H., Sweredoski, M. J., Kolawa, N. J., Graham, R. L., Hess, S., and Chan, D. C. (2011) Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum. Mol. Genet. 20, 1726-1737
21. Tanaka, A., Cleland, M. M., Xu, S., Narendra, D. P., Suen, D. F., Karbowski, M., and Youle, R. J. (2010) Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 191, 1367-1380
22. Kondapalli, C., Kazlauskaite, A., Zhang, N., Woodroof, H. I., Campbell, D. G., Gourlay, R., Burchell, L., Walden, H., Macartney, T. J., Deak, M., Knebel, A., Alessi, D. R., and Muqit, M. M. (2012) PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine
23. Fransson, S., Ruusala, A., and Aspenström, P. (2006) The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem. Biophys. Res. Commun. 344, 500-510
24. Piatkevich, K. D., Hulit, J., Subach, O. M., Wu, B., Abdulla, A., Segall, J. E., and Verkhusha, V. V. (2010) Monomeric red fluorescent proteins with a large Stokes shift. Proc. Natl. Acad. Sci. U.S.A. 107, 5369-5374
25. Zhang, Y., Gao, J., Chung, K. K., Huang, H., Dawson, V. L., and Dawson, T. M. (2000) Parkin functions as an E2-dependent ubiquitin-protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc. Natl. Acad. Sci. U.S.A. 97, 13354-13359
26. Narendra, D., Tanaka, A., Suen, D. F., and Youle, R. J. (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803
27. Lim, K. L., Chew, K. C., Tan, J. M., Wang, C., Chung, K. K., Zhang, Y., Tanaka, Y., Smith, W., Engelender, S., Ross, C. A., Dawson, V. L., and Dawson, T. M. (2005) Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J. Neurosci. 25, 2002-2009 (Pubitemid 40289405)
28. Livingston, C. M., Ifrim, M. F., Cowan, A. E., and Weller, S. K. (2009) Virus-induced chaperone-enriched (VICE) domains function as nuclear protein quality control centers during HSV-1 infection. PLoS Pathog. 5, e1000619
29. Ardley, H. C., Scott, G. B., Rose, S. A., Tan, N. G., Markham, A. F., and Robinson, P. A. (2003) Inhibition of proteasomal activity causes inclusion formation in neuronal and non-neuronal cells overexpressing Parkin. Mol. Biol. Cell 14, 4541-4556 (Pubitemid 37444654)
30. Wood-Kaczmar, A., Gandhi, S., Yao, Z., Abramov, A. Y., Abramov, A. S., Miljan, E. A., Keen, G., Stanyer, L., Hargreaves, I., Klupsch, K., Deas, E., Downward, J., Mansfield, L., Jat, P., Taylor, J., Heales, S., Duchen, M. R., Latchman, D., Tabrizi, S. J., and Wood, N. W. (2008) PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons. PLoS One 3, e2455
31. Gandhi, S., Wood-Kaczmar, A., Yao, Z., Plun-Favreau, H., Deas, E., Klupsch, K., Downward, J., Latchman, D. S., Tabrizi, S. J., Wood, N. W., Duchen, M. R., and Abramov, A. Y. (2009) PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol. Cell 33, 627-638
32. Twelvetrees, A. E., Yuen, E. Y., Arancibia-Carcamo, I. L., MacAskill, A. F., Rostaing, P., Lumb, M. J., Humbert, S., Triller, A., Saudou, F., Yan, Z., and Kittler, J. T. (2010) Delivery of GABAARs to synapses is mediated by HAP1-KIF5 and disrupted by mutant huntingtin. Neuron 65, 53-65
33. Kittler, J. T., Thomas, P., Tretter, V., Bogdanov, Y. D., Haucke, V., Smart, T. G., and Moss, S. J. (2004) Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating γ-aminobutyric acid type A receptor membrane trafficking. Proc. Natl. Acad. Sci. U.S.A. 101, 12736-12741 (Pubitemid 39122092)
34. Licchesi, J. D., Mieszczanek, J., Mevissen, T. E., Rutherford, T. J., Akutsu, M., Virdee, S., El Oualid, F., Chin, J. W., Ovaa, H., Bienz, M., and Komander, D. (2012) An ankyrin-repeat ubiquitin-binding domain determines TRABID's specificity for atypical ubiquitin chains. Nat. Struct. Mol. Biol. 19, 62-71
35. Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D. F., Gautier, C. A., Shen, J., Cookson, M. R., and Youle, R. J. (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298
36. Brickley, K., Smith, M. J., Beck, M., and Stephenson, F. A. (2005) 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, 14723-14732 (Pubitemid 40562820)
37. MacAskill, A. F., Brickley, K., Stephenson, F. A., and Kittler, J. T. (2009) GTPase dependent recruitment of Grif-1 by Miro1 regulates mitochondrial trafficking in hippocampal neurons. Mol. Cell. Neurosci. 40, 301-312
38. Misko, A., Jiang, S., Wegorzewska, I., Milbrandt, J., and Baloh, R. H. (2010) Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J. Neurosci. 30, 4232-4240
39. Gegg, M. E., Cooper, J. M., Chau, K. Y., Rojo, M., Schapira, A. H., and Taanman, J. W. (2010) Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum. Mol. Genet. 19, 4861-4870
40. Weihofen, A., Thomas, K. J., Ostaszewski, B. L., Cookson, M. R., and Selkoe, D. J. (2009) Pink1 forms a multiprotein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking. Biochemistry 48, 2045-2052
41. Komander, D., and Rape, M. (2012) The ubiquitin code. Annu. Rev. Biochem. 81, 203-229
42. Mevissen, T. E., Hospenthal, M. K., Geurink, P. P., Elliott, P. R., Akutsu, M., Arnaudo, N., Ekkebus, R., Kulathu, Y., Wauer, T., El Oualid, F., Freund, S. M., Ovaa, H., and Komander, D. (2013) OTU deubiquitinases reveal mechanisms of linkage specificity and enable ubiquitin chain restriction analysis. Cell 154, 169-184
43. Ye, Y., Akutsu, M., Reyes-Turcu, F., Enchev, R. I., Wilkinson, K. D., and Komander, D. (2011) Polyubiquitin binding and cross-reactivity in the USP domain deubiquitinase USP21. EMBO Rep. 12, 350-357
44. Keusekotten, K., Elliott, P. R., Glockner, L., Fiil, B. K., Damgaard, R. B., Kulathu, Y., Wauer, T., Hospenthal, M. K., Gyrd-Hansen, M., Krappmann, D., Hofmann, K., and Komander, D. (2013) OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 153, 1312-1326
45. Denison, S. R., Wang, F., Becker, N. A., Schüle, B., Kock, N., Phillips, L. A., Klein, C., and Smith, D. I. (2003) Alterations in the common fragile site gene Parkin in ovarian and other cancers. Oncogene 22, 8370-8378 (Pubitemid 37485529)
46. Chaugule, V. K., Burchell, L., Barber, K. R., Sidhu, A., Leslie, S. J., Shaw, G. S., and Walden, H. (2011) Autoregulation of Parkin activity through its ubiquitin-like domain. EMBO J. 30, 2853-2867
47. Shiba-Fukushima, K., Imai, Y., Yoshida, S., Ishihama, Y., Kanao, T., Sato, S., and Hattori, N. (2012) PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci. Rep. 2, 1002
48. Kim, W., Bennett, E. J., Huttlin, E. L., Guo, A., Li, J., Possemato, A., Sowa, M. E., Rad, R., Rush, J., Comb, M. J., Harper, J. W., and Gygi, S. P. (2011) Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44, 325-340
49. Chen, Y., and Dorn, G. W., 2nd (2013) PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science 340, 471-475