Autophagy machinery in the context of mammalian mitophagy

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 10, 2015, Pages 2797-2801

  Yoshii, Saori R ^a,b   Mizushima, Noboru ^b  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Mitophagy; Parkin; Selective autophagy; Two step model

Indexed keywords

ATG PROTEIN; PARKIN; PINK1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; MITOCHONDRIAL PROTEIN; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; UBIQUITIN PROTEIN LIGASE;

AUTOPHAGOSOME; AUTOPHAGY; CANONICAL ANALYSIS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; MAMMAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MITOPHAGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; AUTOPHAGY; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; PROTEIN KINASES; UBIQUITIN-PROTEIN LIGASES;

EID: 84940718245     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.01.013     Document Type: Review

References (69)

1. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998, 392:605-608.
2. Valente E.M., Abou-Sleiman P.M., Caputo V., Muqit M.M., Harvey K., Gispert S., Ali Z., Del Turco D., Bentivoglio A.R., Healy D.G., Albanese A., Nussbaum R., Gonzalez-Maldonado R., Deller T., Salvi S., Cortelli P., Gilks W.P., Latchman D.S., Harvey R.J., Dallapiccola B., Auburger G., Wood N.W. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004, 304:1158-1160.
3. Narendra D., Tanaka A., Suen D.F., Youle R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 2008, 183:795-803.
4. Jin S.M., Lazarou M., Wang C., Kane L.A., Narendra D.P., Youle R.J. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 2010, 191:933-942.
5. Kane L.A., Lazarou M., Fogel A.I., Li Y., Yamano K., Sarraf S.A., Banerjee S., Youle R.J. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 2014, 205:143-153.
6. Koyano F., Okatsu K., Kosako H., Tamura Y., Go E., Kimura M., Kimura Y., Tsuchiya H., Yoshihara H., Hirokawa T., Endo T., Fon E.A., Trempe J.F., Saeki Y., Tanaka K., Matsuda N. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 2014, 510:162-166.
7. Matsuda N., Sato S., Shiba K., Okatsu K., Saisho K., Gautier C.A., Sou Y.S., Saiki S., Kawajiri S., Sato F., Kimura M., Komatsu M., Hattori N., Tanaka K. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J. Cell Biol. 2010, 189:211-221.
8. Narendra D.P., Jin S.M., Tanaka A., Suen D.F., Gautier C.A., Shen J., Cookson M.R., Youle R.J. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010, 8:e1000298.
9. Shiba-Fukushima K., Imai Y., Yoshida S., Ishihama Y., Kanao T., Sato S., Hattori N. PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci. Rep. 2012, 2:1002.
10. 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., Magrane J., Moore D.J., Dawson V.L., Grailhe R., Dawson T.M., Li C., Tieu K., Przedborski S. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:378-383.
11. Ziviani E., Tao R.N., Whitworth A.J. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5018-5023.
12. Itakura E., Kishi-Itakura C., Koyama-Honda I., Mizushima N. Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J. Cell Sci. 2012, 125:1488-1499.
13. Itakura E., Mizushima N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 2010, 6:764-776.
14. Ganley I.G., Lam du H., Wang J., Ding X., Chen S., Jiang X. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J. Biol. Chem. 2009, 284:12297-12305.
15. Hosokawa N., Hara T., Kaizuka T., Kishi C., Takamura A., Miura Y., Iemura S., Natsume T., Takehana K., Yamada N., Guan J.L., Oshiro N., Mizushima N. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 2009, 20:1981-1991.
16. Jung C.H., Jun C.B., Ro S.H., Kim Y.M., Otto N.M., Cao J., Kundu M., Kim D.H. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 2009, 20:1992-2003.
17. Mercer C.A., Kaliappan A., Dennis P.B. A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 2009, 5:649-662.
18. Karanasios E., Stapleton E., Manifava M., Kaizuka T., Mizushima N., Walker S.A., Ktistakis N.T. Dynamic association of the ULK1 complex with omegasomes during autophagy induction. J. Cell Sci. 2013, 126:5224-5238.
19. Hayashi-Nishino M., Fujita N., Noda T., Yamaguchi A., Yoshimori T., Yamamoto A. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 2009, 11:1433-1437.
20. Uemura T., Yamamoto M., Kametaka A., Sou Y.S., Yabashi A., Yamada A., Annoh H., Kametaka S., Komatsu M., Waguri S. A cluster of thin tubular structures mediates transformation of the endoplasmic reticulum to autophagic isolation membrane. Mol. Cell. Biol. 2014, 34:1695-1706.
21. Yla-Anttila P., Vihinen H., Jokitalo E., Eskelinen E.L. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009, 5:1180-1185.
22. Young A.R., Chan E.Y., Hu X.W., Kochl R., Crawshaw S.G., High S., Hailey D.W., Lippincott-Schwartz J., Tooze S.A. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 2006, 119:3888-3900.
23. Axe E.L., Walker S.A., Manifava M., Chandra P., Roderick H.L., Habermann A., Griffiths G., Ktistakis N.T. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 2008, 182:685-701.
24. Kishi-Itakura C., Koyama-Honda I., Itakura E., Mizushima N. Ultrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells. J. Cell Sci. 2014, 127:4089-4102.
25. Mizushima N., Yoshimori T., Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 2011, 27:107-132.
26. Mizushima N., Yamamoto A., Hatano M., Kobayashi Y., Kabeya Y., Suzuki K., Tokuhisa T., Ohsumi Y., Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 2001, 152:657-668.
27. Sou Y.S., Waguri S., Iwata J., Ueno T., Fujimura T., Hara T., Sawada N., Yamada A., Mizushima N., Uchiyama Y., Kominami E., Tanaka K., Komatsu M. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice. Mol. Biol. Cell 2008, 19:4762-4775.
28. Itakura E., Kishi-Itakura C., Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 2012, 151:1256-1269.
29. Jiang P., Nishimura T., Sakamaki Y., Itakura E., Hatta T., Natsume T., Mizushima N. The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol. Biol. Cell 2014, 25:1327-1337.
30. Takats S., Nagy P., Varga A., Pircs K., Karpati M., Varga K., Kovacs A.L., Hegedus K., Juhasz G. Autophagosomal Syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila. J. Cell Biol. 2013, 201:531-539.
31. Takats S., Pircs K., Nagy P., Varga A., Karpati M., Hegedus K., Kramer H., Kovacs A.L., Sass M., Juhasz G. Interaction of the HOPS complex with Syntaxin 17 mediates autophagosome clearance in Drosophila. Mol. Biol. Cell 2014, 25:1338-1354.
32. Yoshii S.R., Kishi C., Ishihara N., Mizushima N. Parkin mediates proteasome-dependent protein degradation and rupture of the outer mitochondrial membrane. J. Biol. Chem. 2011, 286:19630-19640.
33. Rogov V., Dotsch V., Johansen T., Kirkin V. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol. Cell 2014, 53:167-178.
34. Stolz A., Ernst A., Dikic I. Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 2014, 16:495-501.
35. Joo J.H., Dorsey F.C., Joshi A., Hennessy-Walters K.M., Rose K.L., McCastlain K., Zhang J., Iyengar R., Jung C.H., Suen D.F., Steeves M.A., Yang C.Y., Prater S.M., Kim D.H., Thompson C.B., Youle R.J., Ney P.A., Cleveland J.L., Kundu M. Hsp90-Cdc37 chaperone complex regulates Ulk1- and Atg13-mediated mitophagy. Mol. Cell 2011, 43:572-585.
36. Johansen T., Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011, 7:279-296.
37. Ding W.X., Ni H.M., Li M., Liao Y., Chen X., Stolz D.B., Dorn G.W., Yin X.M. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62-mediated mitochondrial priming. J. Biol. Chem. 2010, 285:27879-27890.
38. Geisler S., Holmstrom K.M., Skujat D., Fiesel F.C., Rothfuss O.C., Kahle P.J., Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 2010, 12:119-131.
39. Lee J.Y., Nagano Y., Taylor J.P., Lim K.L., Yao T.P. Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J. Cell Biol. 2010, 189:671-679.
40. Huang C., Andres A.M., Ratliff E.P., Hernandez G., Lee P., Gottlieb R.A. Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS ONE 2011, 6:e20975.
41. Narendra D., Kane L.A., Hauser D.N., Fearnley I.M., Youle R.J. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 2010, 6:1090-1106.
42. Okatsu K., Saisho K., Shimanuki M., Nakada K., Shitara H., Sou Y.S., Kimura M., Sato S., Hattori N., Komatsu M., Tanaka K., Matsuda N. p62/SQSTM1 cooperates with Parkin for perinuclear clustering of depolarized mitochondria. Genes to cells 2010, 15:887-900.
43. Wong Y.C., Holzbaur E.L. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:E4439-E4448.
44. Shen Q., Yamano K., Head B.P., Kawajiri S., Cheung J.T., Wang C., Cho J.H., Hattori N., Youle R.J., van der Bliek A.M. Mutations in Fis1 disrupt orderly disposal of defective mitochondria. Mol. Biol. Cell 2014, 25:145-159.
45. Yamano K., Fogel A.I., Wang C., van der Bliek A.M., Youle R.J. Mitochondrial Rab GAPs govern autophagosome biogenesis during mitophagy. ELife 2014, 3:e01612.
46. Hamacher-Brady A., Brady N.R., Logue S.E., Sayen M.R., Jinno M., Kirshenbaum L.A., Gottlieb R.A., Gustafsson A.B. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ. 2007, 14:146-157.
47. Hanna R.A., Quinsay M.N., Orogo A.M., Giang K., Rikka S., Gustafsson A.B. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J. Biol. Chem. 2012, 287:19094-19104.
48. Melser S., Chatelain E.H., Lavie J., Mahfouf W., Jose C., Obre E., Goorden S., Priault M., Elgersma Y., Rezvani H.R., Rossignol R., Benard G. Rheb regulates mitophagy induced by mitochondrial energetic status. Cell Metab. 2013, 17:719-730.
49. Rikka S., Quinsay M.N., Thomas R.L., Kubli D.A., Zhang X., Murphy A.N., Gustafsson A.B. Bnip3 impairs mitochondrial bioenergetics and stimulates mitochondrial turnover. Cell Death Differ. 2011, 18:721-731.
50. Sandoval H., Thiagarajan P., Dasgupta S.K., Schumacher A., Prchal J.T., Chen M., Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008, 454:232-235.
51. Schweers R.L., Zhang J., Randall M.S., Loyd M.R., Li W., Dorsey F.C., Kundu M., Opferman J.T., Cleveland J.L., Miller J.L., Ney P.A. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19500-19505.
52. Zhu Y., Massen S., Terenzio M., Lang V., Chen-Lindner S., Eils R., Novak I., Dikic I., Hamacher-Brady A., Brady N.R. Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J. Biol. Chem. 2013, 288:1099-1113.
53. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., Rogov V., Lohr F., Popovic D., Occhipinti A., Reichert A.S., Terzic J., Dotsch V., Ney P.A., Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11:45-51.
54. Li W., Zhang X., Zhuang H., Chen H.G., Chen Y., Tian W., Wu W., Li Y., Wang S., Zhang L., Li L., Zhao B., Sui S., Hu Z., Feng D. MicroRNA-137 is a novel hypoxia-responsive microRNA that inhibits mitophagy via regulation of two mitophagy receptors FUNDC1 and NIX. J. Biol. Chem. 2014, 289:10691-10701.
55. Liu L., Feng D., Chen G., Chen M., Zheng Q., Song P., Ma Q., Zhu C., Wang R., Qi W., Huang L., Xue P., Li B., Wang X., Jin H., Wang J., Yang F., Liu P., Zhu Y., Sui S., Chen Q. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 2012, 14:177-185.
56. Wu W., Tian W., Hu Z., Chen G., Huang L., Li W., Zhang X., Xue P., Zhou C., Liu L., Zhu Y., Zhang X., Li L., Zhang L., Sui S., Zhao B., Feng D. ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. EMBO Rep. 2014, 15:566-575.
57. Iwata A., Riley B.E., Johnston J.A., Kopito R.R. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J. Biol. Chem. 2005, 280:40282-40292.
58. Pandey U.B., Nie Z., Batlevi Y., McCray B.A., Ritson G.P., Nedelsky N.B., Schwartz S.L., DiProspero N.A., Knight M.A., Schuldiner O., Padmanabhan R., Hild M., Berry D.L., Garza D., Hubbert C.C., Yao T.P., Baehrecke E.H., Taylor J.P. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007, 447:859-863.
59. Newman A.C., Scholefield C.L., Kemp A.J., Newman M., McIver E.G., Kamal A., Wilkinson S. TBK1 kinase addiction in lung cancer cells is mediated via autophagy of Tax1bp1/Ndp52 and non-canonical NF-kappaB signalling. PLoS ONE 2012, 7:e50672.
60. Thurston T.L., Ryzhakov G., Bloor S., von Muhlinen N., Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 2009, 10:1215-1221.
61. Orvedahl A., Sumpter R., Xiao G., Ng A., Zou Z., Tang Y., Narimatsu M., Gilpin C., Sun Q., Roth M., Forst C.V., Wrana J.L., Zhang Y.E., Luby-Phelps K., Xavier R.J., Xie Y., Levine B. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 2011, 480:113-117.
62. Liu L., Sakakibara K., Chen Q., Okamoto K. Receptor-mediated mitophagy in yeast and mammalian systems. Cell Res. 2014, 24:787-795.
63. Itakura E., Mizushima N. p62 targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding. J. Cell Biol. 2011, 192:17-27.
64. Ichimura Y., Kumanomidou T., Sou Y.S., Mizushima T., Ezaki J., Ueno T., Kominami E., Yamane T., Tanaka K., Komatsu M. Structural basis for sorting mechanism of p62 in selective autophagy. J. Biol. Chem. 2008, 283:22847-22857.
65. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.A., Outzen H., Overvatn A., Bjorkoy G., Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282:24131-24145.
66. Kageyama S., Omori H., Saitoh T., Sone T., Guan J.L., Akira S., Imamoto F., Noda T., Yoshimori T. The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol. Biol. Cell 2011, 22:2290-2300.
67. Fujita N., Morita E., Itoh T., Tanaka A., Nakaoka M., Osada Y., Umemoto T., Saitoh T., Nakatogawa H., Kobayashi S., Haraguchi T., Guan J.L., Iwai K., Tokunaga F., Saito K., Ishibashi K., Akira S., Fukuda M., Noda T., Yoshimori T. Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J. Cell Biol. 2013, 203:115-128.
68. Mancias J.D., Wang X., Gygi S.P., Harper J.W., Kimmelman A.C. Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 2014, 509:105-109.
69. Maejima I., Takahashi A., Omori H., Kimura T., Takabatake Y., Saitoh T., Yamamoto A., Hamasaki M., Noda T., Isaka Y., Yoshimori T. Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. EMBO J. 2013, 32:2336-2347.