6,879
Views
26
CrossRef citations to date
0
Altmetric
Research Paper

Loss of MIEF1/MiD51 confers susceptibility to BAX-mediated cell death and PINK1-PRKN-dependent mitophagy

& ORCID Icon
Pages 2107-2125 | Received 19 Aug 2018, Accepted 01 Mar 2019, Published online: 28 Mar 2019

References

  • Chan DC. Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet. 2012;46:265–287.
  • Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337(6098):1062–1065.
  • Shutt TE, McBride HM. Staying cool in difficult times: mitochondrial dynamics, quality control and the stress response. Biochim Biophys Acta. 2013;1833(2):417–424.
  • Liu X, Kim CN, Yang J, et al. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 1996;86(1):147–157.
  • Sorrentino G, Mioni M, Giorgi C, et al. The prolyl-isomerase Pin1 activates the mitochondrial death program of p53. Cell Death Differ. 2013;20(2):198–208.
  • Ellis HM, Horvitz HR. Genetic control of programmed cell death in the nematode C. elegans. Cell. 1986;44(6):817–829.
  • Hengartner MO, Horvitz HR. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell. 1994;76(4):665–676.
  • Yuan J, Shaham S, Ledoux S, et al. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell. 1993;75(4):641–652.
  • Brown JM, Attardi LD. The role of apoptosis in cancer development and treatment response. Nat Rev Cancer. 2005;5(3):231–237.
  • Honig LS, Rosenberg RN. Apoptosis and neurologic disease. Am J Med. 2000;108(4):317–330.
  • Hockenbery D, Nuñez G, Milliman C, et al. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature. 1990;348(6299):334–336.
  • Brunelle JK, Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J Cell Sci. 2009;122(Pt 4):437–441.
  • Gross A, Jockel J, Wei MC, et al. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. Embo J. 1998;17(14):3878–3885.
  • Wei MC, Zong WX, Cheng EH, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 2001;292(5517):727–730.
  • Zou H, Henzel WJ, Liu X, et al. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 1997;90(3):405–413.
  • Li P, Nijhawan D, Budihardjo I, et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91(4):479–489.
  • Santel A, Fuller MT. Control of mitochondrial morphology by a human mitofusin. J Cell Sci. 2001;114(Pt 5):867–874.
  • Hermann GJ, Thatcher JW, Mills JP, et al. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J Cell Biol. 1998;143(2):359–373.
  • Mozdy AD, McCaffery JM, Shaw JM. Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J Cell Biol. 2000;151(2):367–380.
  • Wasiak S, Zunino R, McBride HM. Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J Cell Biol. 2007;177(3):439–450.
  • Neuspiel M, Zunino R, Gangaraju S, et al. Activated mitofusin 2 signals mitochondrial fusion, interferes with Bax activation, and reduces susceptibility to radical induced depolarization. J Biol Chem. 2005;280(26):25060–25070.
  • Frank S, Gaume B, Bergmann-Leitner ES, et al. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell. 2001;1(4):515–525.
  • Karbowski M, Lee Y-J, Gaume B, et al. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J Cell Biol. 2002;159(6):931–938.
  • Cassidy-Stone A, Chipuk JE, Ingerman E, et al. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev Cell. 2008;14(2):193–204.
  • Germain M, Mathai JP, McBride HM, et al. Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. Embo J. 2005;24(8):1546–1556.
  • Lee YJ, Jeong S-Y, Karbowski M, et al. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell. 2004;15(11):5001–5011.
  • Parone PA, James DI, Da Cruz S, et al. Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol Cell Biol. 2006;26(20):7397–7408.
  • Estaquier J, Arnoult D. Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ. 2007;14(6):1086–1094.
  • Wakabayashi J, Zhang Z, Wakabayashi N, et al. The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J Cell Biol. 2009;186(6):805–816.
  • Ishihara N, Nomura M, Jofuku A, et al. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol. 2009;11(8):958–966.
  • Chen Q, Vazquez EJ, Moghaddas S, et al. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem. 2003;278(38):36027–36031.
  • Kissova I, Deffieu M, Manon S, et al. Uth1p is involved in the autophagic degradation of mitochondria. J Biol Chem. 2004;279(37):39068–39074.
  • Lemasters JJ. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 2005;8(1):3–5.
  • Anding AL, Baehrecke EH. Autophagy in cell life and cell death. Curr Top Dev Biol. 2015;114:67–91.
  • Narendra D, Tanaka A, Suen D-F, et al. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008;183(5):795–803.
  • Narendra, DP, Jin SM, Tanaka A, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010;8(1):e1000298.
  • Vives-Bauza C, Zhou C, Huang Y, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci USA. 2010;107(1):378–383.
  • Pickrell AM, Youle RJ. The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson’s disease. Neuron. 2015;85(2):257–273.
  • Okatsu K, Koyano F, Kimura M, et al. Phosphorylated ubiquitin chain is the genuine Parkin receptor. J Cell Biol. 2015;209(1):111–128.
  • Tanaka A, Cleland MM, Xu S, et al. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol. 2010;191(7):1367–1380.
  • Chen Y, Dorn GW 2nd. PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science. 2013;340(6131):471–475.
  • Narendra D, Kane LA, Hauser DN, et al. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy. 2010;6(8):1090–1106.
  • Geisler S, Holmström KM, Skujat D, et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol. 2010;12(2):119–131.
  • Yamano K, Fogel AI, Wang C, et al. Mitochondrial Rab GAPs govern autophagosome biogenesis during mitophagy. Elife. 2014;3:e01612.
  • Nezich CL, Wang C, Fogel AI, et al. MiT/TFE transcription factors are activated during mitophagy downstream of Parkin and Atg5. J Cell Biol. 2015;210(3):435–450.
  • Lazarou M, Sliter DA, Kane LA, et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015;524(7565):309–314.
  • Schapira AH. Mitochondrial complex I deficiency in Parkinson’s disease. Adv Neurol. 1993;60:288–291.
  • Exner N, Lutz AK, Haass C, et al. Mitochondrial dysfunction in Parkinson’s disease: molecular mechanisms and pathophysiological consequences. Embo J. 2012;31(14):3038–3062.
  • Palmer CS, Osellame LD, Laine D, et al. MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 2011;12(6):565–573.
  • Zhao J, Liu T, Jin S, et al. Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. Embo J. 2011;30(14):2762–2778.
  • Loson OC, Song Z, Chen H, et al. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol Biol Cell. 2013;24(5):659–667.
  • Palmer CS, Elgass KD, Parton RG, et al. Adaptor proteins MiD49 and MiD51 can act independently of Mff and Fis1 in Drp1 recruitment and are specific for mitochondrial fission. J Biol Chem. 2013;288(38):27584–27593.
  • Otera H, Miyata N, Kuge O, et al. Drp1-dependent mitochondrial fission via MiD49/51 is essential for apoptotic cristae remodeling. J Cell Biol. 2016;212(5):531–544.
  • Norbury CJ, Hickson ID. Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol. 2001;41:367–401.
  • Hirsch T, Marchetti P, Susin SA, et al. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene. 1997;15(13):1573–1581.
  • Lindsten T, Ross AJ, King A, et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell. 2000;6(6):1389–1399.
  • De Chiara G, Marcocci ME, Torcia M, et al. Bcl-2 Phosphorylation by p38 MAPK: identification of target sites and biologic consequences. J Biol Chem. 2006;281(30):21353–21361.
  • Sarraf SA, Raman M, Guarani-Pereira V, et al. Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature. 2013;496(7445):372–376.
  • McLelland, GL, Goiran T, Yi W, et al. Mfn2 ubiquitination by PINK1/parkin gates the p97-dependent release of ER from mitochondria to drive mitophagy. Elife. 2018;7:e32866.
  • Xiao B, Goh J-Y, Xiao L, et al. Reactive oxygen species trigger Parkin/PINK1 pathway-dependent mitophagy by inducing mitochondrial recruitment of Parkin. J Biol Chem. 2017;292(40):16697–16708.
  • Xiao, B, Deng X, Lim GG, et al. Superoxide drives progression of Parkin/PINK1-dependent mitophagy following translocation of Parkin to mitochondria. Cell Death Dis. 2017;8(10):e3097.
  • Dingley S, Chapman KA, Falk MJ. Fluorescence-activated cell sorting analysis of mitochondrial content, membrane potential, and matrix oxidant burden in human lymphoblastoid cell lines. Methods Mol Biol. 2012;837:231–239.
  • Woo CC, Hsu A, Kumar AP, et al. Thymoquinone inhibits tumor growth and induces apoptosis in a breast cancer xenograft mouse model: the role of p38 MAPK and ROS. PLoS One. 2013;8(10):e75356.
  • Buhlman L, Damiano M, Bertolin G, et al. Functional interplay between Parkin and Drp1 in mitochondrial fission and clearance. Biochim Biophys Acta. 2014;1843(9):2012–2026.
  • Rojansky R, Cha MY, Chan DC. Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1. Elife. 2016;5.
  • Nowikovsky K, Reipert S, Devenish RJ, et al. Mdm38 protein depletion causes loss of mitochondrial K+/H+ exchange activity, osmotic swelling and mitophagy. Cell Death Differ. 2007;14(9):1647–1656.
  • Twig G, Elorza A, Molina AJA, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. Embo J. 2008;27(2):433–446.
  • Xiao L, Xian H, Lee KY, et al. Death-associated protein 3 regulates mitochondrial-encoded protein synthesis and mitochondrial dynamics. J Biol Chem. 2015;290(41):24961–24974.
  • Yamano, K, Wang C, Sarraf SA, et al. Endosomal Rab cycles regulate Parkin-mediated mitophagy. Elife. 2018;7:e31326

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.