BECN1 is involved in the initiation of mitophagy: It facilitates PARK2 translocation to mitochondria

Autophagy

Volumn 10, Issue 6, 2014, Pages 1105-1119

  Choubey, Vinay ^a   Cagalinec, Michal ^a   Liiv, Joanna ^a   Safiulina, Dzhamilja ^a   Hickey, Miriam A ^a   Kuum, Malle ^a   Liiv, Mailis ^a   Anwar, Tahira ^b   Eskelinen, Eeva Liisa ^b   Kaasik, Allen ^a  

^a Faculty of Medicine   (Estonia)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

BECN1; MFN2; Mitochondrial dynamics; Mitophagy; PARK2 translocation

Indexed keywords

BECLIN 1; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; MEMBRANE PROTEIN; MITOFUSIN 2; PARK2 PROTEIN; PROTEIN KINASE; PTEN INDUCED PUTATIVE KINASE 1; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, RAT; MITOCHONDRIAL PROTEIN; MITOFUSIN 2 PROTEIN, RAT; MUTANT PROTEIN; PARKIN; PTEN-INDUCED PUTATIVE KINASE; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE;

ARTICLE; AUTOPHAGOSOME; CONTROLLED STUDY; CYTOSOL; HUMAN; HUMAN CELL; MITOCHONDRION; MITOPHAGY; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; ACTIVE TRANSPORT; ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; CELL CULTURE; GENE SILENCING; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; PC12 CELL LINE; PHYSIOLOGY; RAT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BIOLOGICAL TRANSPORT, ACTIVE; CELLS, CULTURED; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL PROTEINS; MUTANT PROTEINS; PC12 CELLS; PROTEIN KINASES; RATS; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84903635313     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.28615     Document Type: Article

References (45)

1. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18:571-80; PMID:21311563; http://dx.doi.org/10.1038/cdd.2010.191
2. Itakura E, Kishi C, Inoue K, Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008; 19:5360-72; PMID:18843052; http://dx.doi.org/10.1091/mbc.E08-01-0080
3. Zhong Y, Wang QJ, Li X, Yan Y, Backer JM, Chait BT, Heintz N, Yue Z. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol 2009; 11:468-76; PMID:19270693; http://dx.doi.org/10.1038/ncb1854
4. Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C, et al. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 2008; 10:776-87; PMID:18552835; http://dx.doi.org/10.1038/ncb1740 (Pubitemid 351927707)
5. Takahashi Y, Meyerkord CL, Wang HG. Bif-1/endophilin B1: a candidate for crescent driving force in autophagy. Cell Death Differ 2009; 16:947-55; PMID:19265852; http://dx.doi.org/10.1038/cdd.2009.19
6. Matsunaga K, Saitoh T, Tabata K, Omori H, Satoh T, Kurotori N, Maejima I, Shirahama-Noda K, Ichimura T, Isobe T, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 2009; 11:385-96; PMID:19270696; http://dx.doi.org/10.1038/ncb1846
7. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, Herman B, Levine B. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 1998; 72:8586-96; PMID:9765397 (Pubitemid 28471796)
8. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122:927-39; PMID:16179260; http://dx.doi.org/10.1016/j. cell.2005.07.002 (Pubitemid 41345209)
9. Luo S, Garcia-Arencibia M, Zhao R, Puri C, Toh PP, Sadiq O, Rubinsztein DC. Bim inhibits autophagy by recruiting Beclin 1 to microtubules. Mol Cell 2012; 47:359-70; PMID:22742832; http://dx.doi.org/10.1016/j.molcel.2012.05.040
10. Di Bartolomeo S, Corazzari M, Nazio F, Oliverio S, Lisi G, Antonioli M, Pagliarini V, Matteoni S, Fuoco C, Giunta L, et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 2010; 191:155-68; PMID:20921139; http://dx.doi.org/10.1083/jcb.201002100
11. Michiorri S, Gelmetti V, Giarda E, Lombardi F, Romano F, Marongiu R, Nerini-Molteni S, Sale P, Vago R, Arena G, et al. The Parkinson-associated protein PINK1 interacts with Beclin1 and promotes autophagy. Cell Death Differ 2010; 17:962-74; PMID:20057503; http://dx.doi.org/10.1038/cdd.2009.200
12. Lin W, Kang UJ. Characterization of PINK1 processing, stability, and subcellular localization. J Neurochem 2008; 106:464-74; PMID:18397367; http://dx.doi.org/10.1111/j.1471-4159.2008.05398.x (Pubitemid 351840220)
13. 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; 191:933-42; PMID:21115803; http://dx.doi.org/10.1083/ jcb.201008084
14. Deas E, Plun-Favreau H, Gandhi S, Desmond H, Kjaer S, Loh SH, Renton AE, Harvey RJ, Whitworth AJ, Martins LM, et al. PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum Mol Genet 2011; 20:867-79; PMID:21138942; http://dx.doi.org/10.1093/hmg/ddq526
15. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, Sou YS, Saiki S, Kawajiri S, Sato F, et al. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol 2010; 189:211-21; PMID:20404107; http://dx.doi.org/10. 1083/jcb.200910140
16. Geisler S, Holmström KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12:119-31; PMID:20098416; http://dx.doi.org/10. 1038/ncb2012
17. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8:e1000298; PMID:20126261; http://dx.doi.org/10.1371/ journal. pbio.1000298
18. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, May J, Tocilescu MA, Liu W, Ko HS, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A 2010; 107:378-83; PMID:19966284; http://dx.doi.org/10.1073/pnas.0911187107
19. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 2008; 183:795-803; PMID:19029340; http://dx.doi.org/10.1083/jcb.200809125
20. Narendra D, Kane LA, Hauser DN, Fearnley IM, Youle RJ. p62/SQSTM1 is required for Parkininduced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 2010; 6:1090-106; PMID:20890124; http://dx.doi.org/10.4161/auto.6.8.13426
21. Tanaka A, Cleland MM, Xu S, Narendra DP, Suen DF, Karbowski M, Youle RJ. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol 2010; 191:1367-80; PMID:21173115; http://dx.doi.org/10.1083/ jcb.201007013
22. Van Humbeeck C, Cornelissen T, Hofkens H, Mandemakers W, Gevaert K, De Strooper B, Vandenberghe W. Parkin interacts with Ambra1 to induce mitophagy. J Neurosci 2011; 31:10249-61; PMID:21753002; http://dx.doi.org/10.1523/JNEUROSCI. 1917-11.2011
23. Lazarou M, Narendra DP, Jin SM, Tekle E, Banerjee S, Youle RJ. PINK1 drives Parkin self-association and HECT-like E3 activity upstream of mitochondrial binding. J Cell Biol 2013; 200:163-72; PMID:23319602; http://dx.doi.org/10.1083/jcb.201210111
24. Kondapalli C, Kazlauskaite A, Zhang N, Woodroof HI, Campbell DG, Gourlay R, Burchell L, Walden H, Macartney TJ, Deak M, et al. PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol 2012; 2:120080; PMID:22724072; http://dx.doi.org/10.1098/rsob.120080
25. 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; 22:320-33; PMID:22280891; http://dx.doi.org/10.1016/j. devcel.2011.12.014
26. 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; PMID:23256036; http://dx.doi.org/10.1038/srep01002
27. Poole AC, Thomas RE, Yu S, Vincow ES, Pallanck L. The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINK1/parkin pathway. PLoS One 2010; 5:e10054; PMID:20383334; http://dx.doi.org/10.1371/journal.pone. 0010054
28. Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum Mol Genet 2010; 19:4861-70; PMID:20871098; http://dx.doi.org/10.1093/hmg/ddq419
29. Ziviani E, Tao RN, Whitworth AJ. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc Natl Acad Sci U S A 2010; 107:5018-23; PMID:20194754; http://dx.doi.org/10.1073/pnas.0913485107
30. Cagalinec M, Safiulina D, Liiv M, Liiv J, Choubey V, Wareski P, Veksler V, Kaasik A. Principles of the mitochondrial fusion and fission cycle in neurons. J Cell Sci 2013; 126:2187-97; PMID:23525002; http://dx.doi.org/10.1242/ jcs.118844
31. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003; 112:1809-20; PMID:14638851; http://dx.doi.org/10.1172/JCI20039 (Pubitemid 38063704)
32. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, et al. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 2008; 118:2190-9; PMID:18497889 (Pubitemid 351872337)
33. Shibata M, Lu T, Furuya T, Degterev A, Mizushima N, Yoshimori T, MacDonald M, Yankner B, Yuan J. Regulation of intracellular accumulation of mutant Huntingtin by Beclin 1. J Biol Chem 2006; 281:14474-85; PMID:16522639; http://dx.doi.org/10.1074/jbc.M600364200 (Pubitemid 43848378)
34. Nascimento-Ferreira I, Santos-Ferreira T, Sousa-Ferreira L, Auregan G, Onofre I, Alves S, Dufour N, Colomer Gould VF, Koeppen A, Déglon N, et al. Overexpression of the autophagic beclin-1 protein clears mutant ataxin-3 and alleviates Machado-Joseph disease. Brain 2011; 134:1400-15; PMID:21478185; http://dx.doi.org/10.1093/brain/awr047
35. Rohn TT, Wirawan E, Brown RJ, Harris JR, Masliah E, Vandenabeele P. Depletion of Beclin-1 due to proteolytic cleavage by caspases in the Alzheimer's disease brain. Neurobiol Dis 2011; 43:68-78; PMID:21081164; http://dx.doi.org/10.1016/j. nbd.2010.11.003
36. Spencer B, Potkar R, Trejo M, Rockenstein E, Patrick C, Gindi R, Adame A, Wyss-Coray T, Masliah E. Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in alpha-synuclein models of Parkinson's and Lewy body diseases. J Neurosci 2009; 29:13578-88; PMID:19864570; http://dx.doi.org/10.1523/JNEUROSCI.4390-09.2009
37. Lonskaya I, Hebron ML, Desforges NM, Franjie A, Moussa CE. Tyrosine kinase inhibition increases functional parkin-Beclin-1 interaction and enhances amyloid clearance and cognitive performance. EMBO Mol Med 2013; 5:1247-62; PMID:23737459; http://dx.doi.org/10.1002/emmm.201302771
38. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, et al. Ambra1 regulates autophagy and development of the nervous system. Nature 2007; 447:1121-5; PMID:17589504 (Pubitemid 47014434)
39. Chen D, Gao F, Li B, Wang H, Xu Y, Zhu C, Wang G. Parkin mono-ubiquitinates Bcl-2 and regulates autophagy. J Biol Chem 2010; 285:38214-23; PMID:20889974; http://dx.doi.org/10.1074/jbc. M110.101469
40. Shiba K, Arai T, Sato S, Kubo S, Ohba Y, Mizuno Y, Hattori N. Parkin stabilizes PINK1 through direct interaction. Biochem Biophys Res Commun 2009; 383:331-5; PMID:19358826; http://dx.doi.org/10.1016/j.bbrc.2009.04.006
41. Honda S, Hirose S. Stage-specific enhanced expression of mitochondrial fusion and fission factors during spermatogenesis in rat testis. Biochem Biophys Res Commun 2003; 311:424-32; PMID:14592431; http://dx.doi.org/10.1016/j.bbrc. 2003.10.008 (Pubitemid 37340094)
42. Xu J. Preparation, culture, and immortalization of mouse embryonic fibroblasts. Curr Protoc Mol Biol 2005; Chapter 28:Unit 28 1.
43. Söderberg O, Gullberg M, Jarvius M, Ridderstråle K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 2006; 3:995-1000; PMID:17072308; http://dx.doi.org/10. 1038/nmeth947 (Pubitemid 44782698)
44. Katayama H, Kogure T, Mizushima N, Yoshimori T, Miyawaki A. A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem Biol 2011; 18:1042-52; PMID:21867919; http://dx.doi.org/10.1016/ j. chembiol.2011.05.013
45. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496