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Cited by 309Autophagy in Disease and TherapyParkinson's Disease Mechanisms and TreatmentsCalcium signaling and nucleotide metabolism

MiT/TFE transcription factors are activated during mitophagy downstream of Parkin and Atg5

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Nezich, Catherine L., Wang, Chunxin, Fogel, Adam I., Youle, Richard J.·2015·Journal of Cell Biology
DOI 10.1083/jcb.201501002PMC PMC4523611
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Abstract

The kinase PINK1 and ubiquitin ligase Parkin can regulate the selective elimination of damaged mitochondria through autophagy (mitophagy). Because of the demand on lysosomal function by mitophagy, we investigated a role for the transcription factor EB (TFEB), a master regulator of lysosomal biogenesis, in this process. We show that during mitophagy TFEB translocates to the nucleus and displays transcriptional activity in a PINK1- and Parkin-dependent manner. MITF and TFE3, homologues of TFEB belonging to the same microphthalmia/transcription factor E (MiT/TFE) family, are similarly regulated during mitophagy. Unlike TFEB translocation after starvation-induced mammalian target of rapamycin complex 1 inhibition, Parkin-mediated TFEB relocalization required Atg9A and Atg5 activity. However, constitutively active Rag guanosine triphosphatases prevented TFEB translocation during mitophagy, suggesting cross talk between these two MiT/TFE activation pathways. Analysis of clustered regularly interspaced short palindromic repeats–generated TFEB/MITF/TFE3/TFEC single, double, and triple knockout cell lines revealed that these proteins partly facilitate Parkin-mediated mitochondrial clearance. These results illuminate a pathway leading to MiT/TFE transcription factor activation, distinct from starvation-induced autophagy, which occurs during mitophagy.

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  • Recent studies demonstrated that mitophagy induction is sustained by concomitant activation of transcription factors such as TFEB and TFE3, which promote lysosomal and autophagic gene expressions.

    “Nonetheless, recent studies demonstrated that mitophagy induction is sustained by the concomitant activation of transcription factors, such as Transcription factor EB (TFEB) and TFE3 [36], that promote lysosomal and autophagic gene expressions.”

    From A gene toolbox for monitoring autophagy transcription (2021) · cites this paper as [36]

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  1. Aitken A. 2011 Post-translational modification of 14-3-3 isoforms and regulation of cellular function. Semin. Cell Dev. Biol. 22: 673– 680. 10.1016/j.semcdb.2011.08.003 21864699 · DOI
  2. Aksan I., and Goding C.R. 1998 Targeting the microphthalmia basic helix-loop-helix–leucine zipper transcription factor to a subset of E-box elements in vitro and in vivo. Mol. Cell. Biol. 18: 6930– 6938. 9819381 PMC109276
  3. Axe E.L., Walker S.A., Manifava M., Chandra P., Roderick H.L., Habermann A., Griffiths G., and Ktistakis N.T. 2008 Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182: 685– 701. 10.1083/jcb.200803137 18725538 PMC2518708 · DOI · Paper page
  4. Brown E.J., Beal P.A., Keith C.T., Chen J., Shin T.B., and Schreiber S.L. 1995 Control of p70 s6 kinase by kinase activity of FRAP in vivo. Nature. 377: 441– 446. 10.1038/377441a0 7566123 · DOI
  5. Brunet A., Kanai F., Stehn J., Xu J., Sarbassova D., Frangioni J.V., Dalal S.N., DeCaprio J.A., Greenberg M.E., and Yaffe M.B. 2002 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J. Cell Biol. 156: 817– 828. 10.1083/jcb.200112059 11864996 PMC2173313 · DOI
  6. Brunn G.J., Hudson C.C., Sekulić A., Williams J.M., Hosoi H., Houghton P.J., Lawrence J.C. Jr., and Abraham R.T. 1997 Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science. 277: 99– 101. 10.1126/science.277.5322.99 9204908 · DOI
  7. Burnett P.E., Barrow R.K., Cohen N.A., Snyder S.H., and Sabatini D.M. 1998 RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. USA. 95: 1432– 1437. 10.1073/pnas.95.4.1432 9465032 PMC19032 · DOI
  8. Chan N.C., Salazar A.M., Pham A.H., Sweredoski M.J., Kolawa N.J., Graham R.L.J., 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. 10.1093/hmg/ddr048 21296869 PMC3071670 · DOI · Paper page
  9. Clark I.E., Dodson M.W., Jiang C., Cao J.H., Huh J.R., Seol J.H., Yoo S.J., Hay B.A., and Guo M. 2006 Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature. 441: 1162– 1166. 10.1038/nature04779 16672981 · DOI · Paper page
  10. Decressac M., Mattsson B., Weikop P., Lundblad M., Jakobsson J., and Björklund A. 2013 TFEB-mediated autophagy rescues midbrain dopamine neurons from α-synuclein toxicity. Proc. Natl. Acad. Sci. USA. 110: E1817– E1826. 10.1073/pnas.1305623110 23610405 PMC3651458 · DOI · Paper page
  11. 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. 10.1038/sj.onc.1207072 14614460 · DOI
  12. Dennis P.B., Jaeschke A., Saitoh M., Fowler B., Kozma S.C., and Thomas G. 2001 Mammalian TOR: a homeostatic ATP sensor. Science. 294: 1102– 1105. 10.1126/science.1063518 11691993 · DOI · Paper page
  13. DiMauro S., and Schon E.A. 2008 Mitochondrial disorders in the nervous system. Annu. Rev. Neurosci. 31: 91– 123. 10.1146/annurev.neuro.30.051606.094302 18333761 · DOI
  14. Ferron M., Settembre C., Shimazu J., Lacombe J., Kato S., Rawlings D.J., Ballabio A., and Karsenty G. 2013 A RANKL–PKCβ–TFEB signaling cascade is necessary for lysosomal biogenesis in osteoclasts. Genes Dev. 27: 955– 969. 10.1101/gad.213827.113 23599343 PMC3650231 · DOI
  15. Fujita N., Itoh T., Omori H., Fukuda M., Noda T., and Yoshimori T. 2008 The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell. 19: 2092– 2100. 10.1091/mbc.E07-12-1257 18321988 PMC2366860 · DOI
  16. Guo B., Huang X., Zhang P., Qi L., Liang Q., Zhang X., Huang J., Fang B., Hou W., Han J., and Zhang H. 2014 Genome-wide screen identifies signaling pathways that regulate autophagy during Caenorhabditis elegans development. EMBO Rep. 15: 705– 713. 10.1002/embr.201338310 24764321 PMC4197881 · DOI
  17. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., Turk B.E., and Shaw R.J. 2008 AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell. 30: 214– 226. 10.1016/j.molcel.2008.03.003 18439900 PMC2674027 · DOI · Paper page
  18. Ha J., Daniel S., Broyles S.S., and Kim K.H. 1994 Critical phosphorylation sites for acetyl-CoA carboxylase activity. J. Biol. Chem. 269: 22162– 22168. 7915280
  19. Hara T., Takamura A., Kishi C., Iemura S., Natsume T., Guan J.L., and Mizushima N. 2008 FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J. Cell Biol. 181: 497– 510. 10.1083/jcb.200712064 18443221 PMC2364687 · DOI
  20. Hasson S.A., Fogel A.I., Wang C., MacArthur R., Guha R., Heman-Ackah S., Martin S., Youle R.J., and Inglese J. 2015 Chemogenomic profiling of endogenous PARK2 expression using a genome-edited coincidence reporter. ACS Chem. Biol. 10: 1188– 1197. 10.1021/cb5010417 25689131 PMC9927027 · DOI
  21. Hawley S.A., Davison M., Woods A., Davies S.P., Beri R.K., Carling D., and Hardie D.G. 1996 Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J. Biol. Chem. 271: 27879– 27887. 10.1074/jbc.271.44.27879 8910387 · DOI · Paper page
  22. Hawley S.A., Gadalla A.E., Olsen G.S., and Hardie D.G. 2002 The antidiabetic drug metformin activates the AMP-activated protein kinase cascade via an adenine nucleotide-independent mechanism. Diabetes. 51: 2420– 2425. 10.2337/diabetes.51.8.2420 12145153 · DOI · Paper page
  23. Hemesath T.J., Steingrímsson E., McGill G., Hansen M.J., Vaught J., Hodgkinson C.A., Arnheiter H., Copeland N.G., Jenkins N.A., and Fisher D.E. 1994 microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev. 8: 2770– 2780. 10.1101/gad.8.22.2770 7958932 · DOI · Paper page
  24. Holden P., and Horton W.A. 2009 Crude subcellular fractionation of cultured mammalian cell lines. BMC Res. Notes. 2: 243 10.1186/1756-0500-2-243 20003239 PMC2802353 · DOI
  25. Inoki K., Zhu T., and Guan K.-L. 2003 TSC2 mediates cellular energy response to control cell growth and survival. Cell. 115: 577– 590. 10.1016/S0092-8674(03)00929-2 14651849 · DOI · Paper page
  26. Itakura E., Kishi-Itakura C., Koyama-Honda I., and Mizushima N. 2012 Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J. Cell Sci. 125: 1488– 1499. 10.1242/jcs.094110 22275429 · DOI · Paper page
  27. 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. 10.1083/jcb.201008084 21115803 PMC2995166 · DOI · Paper page
  28. Katayama H., Kogure T., Mizushima N., Yoshimori T., and Miyawaki A. 2011 A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem. Biol. 18: 1042– 1052. 10.1016/j.chembiol.2011.05.013 21867919 · DOI · Paper page
  29. Kim J., Kundu M., Viollet B., and Guan K.-L. 2011 AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13: 132– 141. 10.1038/ncb2152 21258367 PMC3987946 · DOI · Paper page
  30. Kishi-Itakura C., Koyama-Honda I., Itakura E., and Mizushima N. 2014 Ultrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells. J. Cell Sci. 127: 4089– 4102. 10.1242/jcs.156034 25052093 · DOI
  31. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., and Shimizu N. 1998 Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 392: 605– 608. 10.1038/33416 9560156 · DOI · Paper page
  32. Klionsky D.J., and Schulman B.A. 2014 Dynamic regulation of macroautophagy by distinctive ubiquitin-like proteins. Nat. Struct. Mol. Biol. 21: 336– 345. 10.1038/nsmb.2787 24699082 PMC4036234 · DOI
  33. Kuiper R.P., Schepens M., Thijssen J., Schoenmakers E.F.P.M., and van Kessel A.G. 2004 Regulation of the MiTF/TFE bHLH-LZ transcription factors through restricted spatial expression and alternative splicing of functional domains. Nucleic Acids Res. 32: 2315– 2322. 10.1093/nar/gkh571 15118077 PMC419459 · DOI
  34. Lücking C.B., Dürr A., Bonifati V., Vaughan J., De Michele G., Gasser T., Harhangi B.S., Meco G., Denèfle P., Wood N.W., 2000 Association between early-onset Parkinson’s disease and mutations in the parkin gene. N. Engl. J. Med. 342: 1560– 1567. 10.1056/NEJM200005253422103 10824074 · DOI
  35. Mackintosh C. 2004 Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem. J. 381: 329– 342. 10.1042/BJ20031332 15167810 PMC1133837 · DOI
  36. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., and Church G.M. 2013 RNA-guided human genome engineering via Cas9. Science. 339: 823– 826. 10.1126/science.1232033 23287722 PMC3712628 · DOI · Paper page
  37. Marsin A.S., Bertrand L., Rider M.H., Deprez J., Beauloye C., Vincent M.F., Van den Berghe G., Carling D., and Hue L. 2000 Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 10: 1247– 1255. 10.1016/S0960-9822(00)00742-9 11069105 · DOI
  38. Martina J.A., and Puertollano R. 2013 Rag GTPases mediate amino acid–dependent recruitment of TFEB and MITF to lysosomes. J. Cell Biol. 200: 475– 491. 10.1083/jcb.201209135 23401004 PMC3575543 · DOI
  39. Martina J.A., Chen Y., Gucek M., and Puertollano R. 2012 MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy. 8: 903– 914. 10.4161/auto.19653 22576015 PMC3427256 · DOI
  40. Martina J.A., Diab H.I., Li H., and Puertollano R. 2014 a Novel roles for the MiTF/TFE family of transcription factors in organelle biogenesis, nutrient sensing, and energy homeostasis. Cell. Mol. Life Sci. 71: 2483– 2497. 10.1007/s00018-014-1565-8 24477476 PMC4057939 · DOI
  41. Martina J.A., Diab H.I., Lishu L., Jeong-A L., Patange S., Raben N., and Puertollano R. 2014 b The nutrient-responsive transcription factor TFE3 promotes autophagy, lysosomal biogenesis, and clearance of cellular debris. Sci. Signal. 7: ra9 10.1126/scisignal.2004754 24448649 PMC4696865 · DOI · Paper page
  42. Medina D.L., Fraldi A., Bouche V., Annunziata F., Mansueto G., Spampanato C., Puri C., Pignata A., Martina J.A., Sardiello M., 2011 Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev. Cell. 21: 421– 430. 10.1016/j.devcel.2011.07.016 21889421 PMC3173716 · DOI
  43. Medina D.L., Di Paola S., Peluso I., Armani A., De Stefani D., Venditti R., Montefusco S., Scotto-Rosato A., Prezioso C., Forrester A., 2015 Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat. Cell Biol. 17: 288– 299. 10.1038/ncb3114 25720963 PMC4801004 · DOI
  44. Meissner C., Lorenz H., Weihofen A., Selkoe D.J., and Lemberg M.K. 2011 The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J. Neurochem. 117: 856– 867. 10.1111/j.1471-4159.2011.07253.x 21426348 · DOI
  45. Mizushima N., Yamamoto A., Hatano M., Kobayashi Y., Kabeya Y., Suzuki K., Tokuhisa T., Ohsumi Y., and Yoshimori T. 2001 Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152: 657– 668. 10.1083/jcb.152.4.657 11266458 PMC2195787 · DOI · Paper page
  46. Obsilová V., Silhan J., Boura E., Teisinger J., and Obsil T. 2008 Physiol. Res. 57: S11– S21. 18481918
  47. Palmieri M., Impey S., Kang H., di Ronza A., Pelz C., Sardiello M., and Ballabio A. 2011 Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum. Mol. Genet. 20: 3852– 3866. 10.1093/hmg/ddr306 21752829 · DOI · Paper page
  48. Park J., Lee S.B., Lee S., Kim Y., Song S., Kim S., Bae E., Kim J., Shong M., Kim J.-M., and Chung J. 2006 Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature. 441: 1157– 1161. 10.1038/nature04788 16672980 · DOI · Paper page
  49. Pawlyk A.C., Giasson B.I., Sampathu D.M., Perez F.A., Lim K.L., Dawson V.L., Dawson T.M., Palmiter R.D., Trojanowski J.Q., and Lee V.M. 2003 Novel monoclonal antibodies demonstrate biochemical variation of brain parkin with age. J. Biol. Chem. 278: 48120– 48128. 10.1074/jbc.M306889200 12972409 · DOI
  50. Peña-Llopis S., Vega-Rubin-de-Celis S., Schwartz J.C., Wolff N.C., Tran T.A.T., Zou L., Xie X.-J., Corey D.R., and Brugarolas J. 2011 Regulation of TFEB and V-ATPases by mTORC1. EMBO J. 30: 3242– 3258. 10.1038/emboj.2011.257 21804531 PMC3160667 · DOI
  51. Polito V.A., Li H., Martini-Stoica H., Wang B., Yang L., Xu Y., Swartzlander D.B., Palmieri M., di Ronza A., Lee V.M., 2014 Selective clearance of aberrant tau proteins and rescue of neurotoxicity by transcription factor EB. EMBO Mol. Med. 6: 1142– 1160. 10.15252/emmm.201303671 25069841 PMC4197862 · DOI
  52. Roczniak-Ferguson A., Petit C.S., Froehlich F., Qian S., Ky J., Angarola B., Walther T.C., and Ferguson S.M. 2012 The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 5: ra42 10.1126/scisignal.2002790 22692423 PMC3437338 · DOI
  53. Sancak Y., Peterson T.R., Shaul Y.D., Lindquist R.A., Thoreen C.C., Bar-Peled L., and Sabatini D.M. 2008 The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science. 320: 1496– 1501. 10.1126/science.1157535 18497260 PMC2475333 · DOI · Paper page
  54. Sardiello M., Palmieri M., di Ronza A., Medina D.L., Valenza M., Gennarino V.A., Di Malta C., Donaudy F., Embrione V., Polishchuk R.S., et al. 2009 A gene network regulating lysosomal biogenesis and function. Science. 325: 473– 477. 19556463
  55. 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. 10.1038/nature12043 23503661 PMC3641819 · DOI
  56. Settembre C., Zoncu R., Medina D.L., Vetrini F., Erdin S., Erdin S., Huynh T., Ferron M., Karsenty G., Vellard M.C., 2012 A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 31: 1095– 1108. 10.1038/emboj.2012.32 22343943 PMC3298007 · DOI
  57. Sidransky E., Nalls M.A., Aasly J.O., Aharon-Peretz J., Annesi G., Barbosa E.R., Bar-Shira A., Berg D., Bras J., Brice A., 2009 Multicenter analysis of glucocerebrosidase mutations in Parkinson’s disease. N. Engl. J. Med. 361: 1651– 1661. 10.1056/NEJMoa0901281 19846850 PMC2856322 · DOI · Paper page
  58. Song W., Wang F., Savini M., Ake A., di Ronza A., Sardiello M., and Segatori L. 2013 TFEB regulates lysosomal proteostasis. Hum. Mol. Genet. 22: 1994– 2009. 10.1093/hmg/ddt052 23393155 · DOI · Paper page
  59. Spampanato C., Feeney E., Li L., Cardone M., Lim J.A., Annunziata F., Zare H., Polishchuk R., Puertollano R., Parenti G., 2013 Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease. EMBO Mol. Med. 5: 691– 706. 10.1002/emmm.201202176 23606558 PMC3662313 · DOI · Paper page
  60. Steingrimsson E., Tessarollo L., Pathak B., Hou L., Arnheiter H., Copeland N.G., and Jenkins N.A. 2002 Mitf and Tfe3, two members of the Mitf-Tfe family of bHLH-Zip transcription factors, have important but functionally redundant roles in osteoclast development. Proc. Natl. Acad. Sci. USA. 99: 4477– 4482. 10.1073/pnas.072071099 11930005 PMC123673 · DOI
  61. Tsunemi T., Ashe T.D., Morrison B.E., Soriano K.R., Au J., Roque R.A.V., Lazarowski E.R., Damian V.A., Masliah E., and La Spada A.R. 2012 PGC-1α rescues Huntington’s disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci. Transl. Med. 4: 142ra97 10.1126/scitranslmed.3003799 PMC4096245 22786682 · DOI
  62. Valente E.M., Salvi S., Ialongo T., Marongiu R., Elia A.E., Caputo V., Romito L., Albanese A., Dallapiccola B., and Bentivoglio A.R. 2004 PINK1 mutations are associated with sporadic early-onset parkinsonism. Ann. Neurol. 56: 336– 341. 10.1002/ana.20256 15349860 · DOI
  63. 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., 2010 PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc. Natl. Acad. Sci. USA. 107: 378– 383. 10.1073/pnas.0911187107 19966284 PMC2806779 · DOI · Paper page
  64. Witters L.A., Nordlund A.C., and Marshall L. 1991 Regulation of intracellular acetyl-CoA carboxylase by ATP depletors mimics the action of the 5′-AMP-activated protein kinase. Biochem. Biophys. Res. Commun. 181: 1486– 1492. 10.1016/0006-291X(91)92107-U 1684896 · DOI
  65. Yamano K., and Youle R.J. 2013 PINK1 is degraded through the N-end rule pathway. Autophagy. 9: 1758– 1769. 10.4161/auto.24633 24121706 PMC4028335 · DOI
  66. Yamano K., Fogel A.I., Wang C., van der Bliek A.M., and Youle R.J. 2014 Mitochondrial Rab GAPs govern autophagosome biogenesis during mitophagy. eLife. 3: e01612 10.7554/eLife.01612 24569479 PMC3930140 · DOI · Paper page
  67. Yang Y., Gehrke S., Imai Y., Huang Z., Ouyang Y., Wang J.-W., Yang L., Beal M.F., Vogel H., and Lu B. 2006 Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl. Acad. Sci. USA. 103: 10793– 10798. 10.1073/pnas.0602493103 16818890 PMC1502310 · DOI · Paper page
  68. 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. 10.1074/jbc.M110.209338 21454557 PMC3103342 · DOI · Paper page
  69. Zhou J., Tan S.H., Nicolas V., Bauvy C., Yang N.D., Zhang J., Xue Y., Codogno P., and Shen H.M. 2013 Activation of lysosomal function in the course of autophagy via mTORC1 suppression and autophagosome-lysosome fusion. Cell Res. 23: 508– 523. 10.1038/cr.2013.11 23337583 PMC3616426 · DOI

Cited by

Sorted by citations

Authors
Nezich, C. L., Wang, C., Fogel, A. I., & Youle, R. J.
Affiliations
National Institutes of Health (US)
Corresponding author
Youle, Richard J.
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2015-08-03
Volume
210
Issue
3
Pages
435-450
ISSN
  • 0021-9525 (ISSN-L)
  • 1540-8140
DOI
10.1083/jcb.201501002
PMC
PMC4523611
OpenAlex
W2137546031
Cited by
309
References
9
Citations by year
2026: 16 · 2025: 33 · 2024: 25 · 2023: 32 · 2022: 25 · 2021: 39 · 2020: 40 · 2019: 27 · 2018: 22 · 2017: 25 · 2016: 19 · 2015: 6
FWCI
18.83
Type
journal article
Language
en
Open access
Licence
cc-by-nc-sa
Locations
  • The Journal of Cell Biology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • Yale University
  • National Institutes of Health
  • National Institute of Neurological Disorders and Stroke
Topics
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
  • Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords
mitophagy, TFEB, MITF, TFE3, TFEC, Parkin, PINK1, ATG5, ATG9A, lysosomal biogenesis, Rag GTPases, mitochondrial clearance, transcriptional activation
MeSH terms
Autophagy-Related Proteins, Autophagy-Related Protein 5, Mechanistic Target of Rapamycin Complex 1, rab7 GTP-Binding Proteins, PTEN-Induced Putative Kinase, Autophagy, HeLa Cells, Humans, Lysosomes, Membrane Proteins, Microtubule-Associated Proteins, Mitochondria, Phagosomes, Protein Kinases, Homeodomain Proteins, rab GTP-Binding Proteins, Active Transport, Cell Nucleus, Mitochondrial Proteins, Vesicular Transport Proteins, RNA Interference, RNA, Small Interfering, Ubiquitin-Protein Ligases, Cell Line, Tumor, Multiprotein Complexes, 14-3-3 Proteins, Microphthalmia-Associated Transcription Factor, Basic Helix-Loop-Helix Leucine Zipper Transcription Factors, Gene Knockout Techniques, HEK293 Cells, TOR Serine-Threonine Kinases, Mitophagy

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