Functional interplay between Parkin and Drp1 in mitochondrial fission and clearance

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 9, 2014, Pages 2012-2026

  Buhlman, Lori ^a,b,c,d   Damiano, Maria ^a,b,c   Bertolin, Giulia ^a,b,c   Ferrando Miguel, Rosa ^a,b,c   Lombès, Anne ^e,f   Brice, Alexis ^a,b,c   Corti, Olga ^a,b,c  

^a INSERM   (France)

^b CNRS   (France)

^c INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^d MIDWESTERN UNIVERSITY   (United States)

^e INSTITUT COCHIN   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Calcium calmodulin calcineurin signaling; Drp1; MiD51; Mitochondrial clearance; Mitochondrial dynamics; PINK1 Parkin pathway

Indexed keywords

CALCINEURIN; CALCIUM; CALMODULIN; DRP1 PROTEIN; GUANOSINE TRIPHOSPHATASE; PARKIN; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE PINK1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FRAGMENTATION REACTION; MITOCHONDRIAL DYNAMICS; MITOPHAGY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

CALCIUM/CALMODULIN/CALCINEURIN SIGNALING; DRP1; MID51; MITOCHONDRIAL CLEARANCE; MITOCHONDRIAL DYNAMICS; PINK1/PARKIN PATHWAY;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; DYNAMINS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MUTATION; PARKINSON DISEASE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASES; PROTEIN STRUCTURE, QUATERNARY; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES;

EID: 84902477543     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.05.012     Document Type: Article

References (68)

1. Corti O., Lesage S., Brice A. What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol. Rev. 2011, 91:1161-1218.
2. Park J., Lee S.B., Lee S., Kim Y., Song S., Kim S., Bae E., Kim J., Shong M., Kim J.M., Chung J. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 2006, 441:1157-1161.
3. Clark I.E., Dodson M.W., Jiang C., Cao J.H., Huh J.R., Seol J.H., Yoo S.J., Hay B.A., Guo M. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 2006, 441:1162-1166.
4. Yang Y., Gehrke S., Imai Y., Huang Z., Ouyang Y., Wang J.W., Yang L., Beal M.F., Vogel H., Lu B. Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10793-10798.
5. Poole A.C., Thomas R.E., Andrews L.A., McBride H.M., Whitworth A.J., Pallanck L.J. The PINK1/Parkin pathway regulates mitochondrial morphology. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1638-1643.
6. Deng H., Dodson M.W., Huang H., Guo M. The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14503-14508.
7. Yang Y., Ouyang Y., Yang L., Beal M.F., McQuibban A., Vogel H., Lu B. Pink1 regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7070-7075.
8. Burman J.L., Yu S., Poole A.C., Decal R.B., Pallanck L. Analysis of neural subtypes reveals selective mitochondrial dysfunction in dopaminergic neurons from parkin mutants. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:10438-10443.
9. Exner N., Treske B., Paquet D., Holmstrom K., Schiesling C., Gispert S., Carballo-Carbajal I., Berg D., Hoepken H.H., Gasser T., Kruger R., Winklhofer K.F., Vogel F., Reichert A.S., Auburger G., Kahle P.J., Schmid B., Haass C. Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J. Neurosci. 2007, 27:12413-12418.
10. Mortiboys H., Thomas K.J., Koopman W.J., Klaffke S., Abou-Sleiman P., Olpin S., Wood N.W., Willems P.H., Smeitink J.A., Cookson M.R., Bandmann O. Mitochondrial function and morphology are impaired in parkin-mutant fibroblasts. Ann. Neurol. 2008, 64:555-565.
11. Lutz A.K., Exner N., Fett M.E., Schlehe J.S., Kloos K., Lammermann K., Brunner B., Kurz-Drexler A., Vogel F., Reichert A.S., Bouman L., Vogt-Weisenhorn D., Wurst W., Tatzelt J., Haass C., Winklhofer K.F. Loss of Parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation. J. Biol. Chem. 2009, 284:22938-22951.
12. Dagda R.K., Cherra S.J., Kulich S.M., Tandon A., Park D., Chu C.T. Loss of pink1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem. 2009, 284:13843-13855.
13. Sandebring A., Thomas K.J., Beilina A., van der Brug M., Cleland M.M., Ahmad R., Miller D.W., Zambrano I., Cowburn R.F., Behbahani H., Cedazo-Minguez A., Cookson M.R. Mitochondrial alterations in PINK1 deficient cells are influenced by calcineurin-dependent dephosphorylation of dynamin-related protein 1. PLoS One 2009, 4:e5701.
14. Cui M., Tang X., Christian W.V., Yoon Y., Tieu K. Perturbations in mitochondrial dynamics induced by human mutant PINK1 can be rescued by the mitochondrial division inhibitor mdivi-1. J. Biol. Chem. 2010, 285:11740-11752.
15. Yu W., Sun Y., Guo S., Lu B. The PINK1/Parkin pathway regulates mitochondrial dynamics and function in mammalian hippocampal and dopaminergic neurons. Hum. Mol. Genet. 2011, 20:3227-3240.
16. Corti O., Brice A. Mitochondrial quality control turns out to be the principal suspect in parkin and PINK1-related autosomal recessive Parkinson's disease. Curr. Opin. Neurobiol. 2013, 23:100-108.
17. Sandebring A., Dehvari N., Perez-Manso M., Thomas K.J., Karpilovski E., Cookson M.R., Cowburn R.F., Cedazo-Minguez A. Parkin deficiency disrupts calcium homeostasis by modulating phospholipase C signalling. FEBS J. 2009, 276:5041-5052.
18. Shin J.H., Ko H.S., Kang H., Lee Y., Lee Y.I., Pletinkova O., Troconso J.C., Dawson V.L., Dawson T.M. PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell 2011, 144:689-702.
19. Kuroda Y., Mitsui T., Kunishige M., Shono M., Akaike M., Azuma H., Matsumoto T. Parkin enhances mitochondrial biogenesis in proliferating cells. Hum. Mol. Genet. 2006, 15:883-895.
20. Pacelli C., De Rasmo D., Signorile A., Grattagliano I., di Tullio G., D'Orazio A., Nico B., Comi G.P., Ronchi D., Ferranini E., Pirolo D., Seibel P., Schubert S., Gaballo A., Villani G., Cocco T. Mitochondrial defect and PGC-1alpha dysfunction in parkin-associated familial Parkinson's disease. Biochim. Biophys. Acta 2011, 1812:1041-1053.
21. Song L., Shan Y., Lloyd K.C., Cortopassi G.A. Mutant Twinkle increases dopaminergic neurodegeneration, mtDNA deletions and modulates Parkin expression. Hum. Mol. Genet. 2012, 21:5147-5158.
22. Wang X., Winter D., Ashrafi G., Schlehe J., Wong Y.L., Selkoe D., Rice S., Steen J., LaVoie M.J., Schwarz T.L. PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 2011, 147:893-906.
23. 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., Abramov A.Y. PINK1-associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol. Cell 2009, 33:627-638.
24. Weihofen A., Thomas K.J., Ostaszewski B.L., Cookson M.R., Selkoe D.J. Pink1 forms a multiprotein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking (dagger). Biochemistry 2009, 48:2045-2052.
25. Rothfuss O., Fischer H., Hasegawa T., Maisel M., Leitner P., Miesel F., Sharma M., Bornemann A., Berg D., Gasser T., Patenge N. Parkin protects mitochondrial genome integrity and supports mitochondrial DNA repair. Hum. Mol. Genet. 2009, 18:3832-3850.
26. Johnson B.N., Berger A.K., Cortese G.P., Lavoie M.J. The ubiquitin E3 ligase parkin regulates the proapoptotic function of Bax. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6283-6288.
27. Johnson B.N., Charan R.A., LaVoie M.J. Recognizing the cooperative and independent mitochondrial functions of Parkin and PINK1. Cell Cycle 2012, 11:2775-2776.
28. 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.
29. 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 actiavate Parkin. PLoS Biol 2010, 8:e1000298.
30. 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.
31. 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.
32. 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.
33. Tanaka A., Cleland M.M., Xu S., Narendra D.P., Suen D.F., Karbowski M., Youle R.J. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 2010, 191:1367-1380.
34. 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.
35. Chan N.C., Salazar A.M., Pham A.H., Sweredoski M.J., Kolawa N.J., Graham R.L., Hess S., Chan D.C. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum. Mol. Genet. 2011, 20:1726-1737.
36. Hampe C., Ardila-Osorio H., Fournier M., Brice A., Corti O. Biochemical analysis of Parkinson's disease-causing variants of Parkin, an E3 ubiquitin-protein ligase with monoubiquitylation capacity. Hum. Mol. Genet. 2006, 15:2059-2075.
37. Legros F., Lombes A., Frachon P., Rojo M. Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol. Biol. Cell 2002, 13:4343-4354.
38. Koopman W.J., Visch H.J., Verkaart S., van den Heuvel L.W., Smeitink J.A., Willems P.H. Mitochondrial network complexity and pathological decrease in complex I activity are tightly correlated in isolated human complex I deficiency. Am. J. Physiol. Cell Physiol. Oct 2005, 289(4):C881-C890.
39. Agier V., Oliviero P., Laine J., L'Hermitte-Stead C., Girard S., Fillaut S., Jardel C., Bouillaud F., Bulteau A.L., Lombes A. Defective mitochondrial fusion, altered respiratory function, and distorted cristae structure in skin fibroblasts with heterozygous OPA1 mutations. Biochim. Biophys. Acta 2012, 1822:1570-1580.
40. Snapp E.L., Hegde R.S. Rational design and evaluation of FRET experiments to measure protein proximities in cells. Curr. Protoc. Cell Biol. 2006, (Chapter 17, Unit 17 19). 10.1002/0471143030.cb1709s32.
41. Bertolin G., Ferrando-Miguel R., Jacoupy M., Traver S., Grenier K., Greene A.W., Dauphin A., Waharte F., Bayot A., Salamero J., Lombes A., Bulteau A.L., Fon E.A., Brice A., Corti O. The TOMM machinery is a molecular switch in PINK1 and PARK2/PARKIN-dependent mitochondrial clearance. Autophagy 2013, 9:1801-1817.
42. Cribbs J.T., Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 2007, 8:939-944.
43. Han X.J., Lu Y.F., Li S.A., Kaitsuka T., Sato Y., Tomizawa K., Nairn A.C., Takei K., Matsui H., Matsushita M. CaM kinase I alpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J. Cell Biol. 2008, 182:573-585.
44. Gomes L.C., Di Benedetto G., Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 2011, 13:589-598.
45. Rambold A.S., Kostelecky B., Elia N., Lippincott-Schwartz J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10190-10195.
46. Duvezin-Caubet S., Koppen M., Wagener J., Zick M., Israel L., Bernacchia A., Jagasia R., Rugarli E.I., Imhof A., Neupert W., Langer T., Reichert A.S. OPA1 processing reconstituted in yeast depends on the subunit composition of the m-AAA protease in mitochondria. Mol. Biol. Cell 2007, 18:3582-3590.
47. Griparic L., Kanazawa T., van der Bliek A.M. Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J. Cell Biol. 2007, 178:757-764.
48. Palmer C.S., Osellame L.D., Laine D., Koutsopoulos O.S., Frazier A.E., Ryan M.T. MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 2011, 12:565-573.
49. Zhao J., Liu T., Jin S., Wang X., Qu M., Uhlen P., Tomilin N., Shupliakov O., Lendahl U., Nister M. Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 2011, 30:2762-2778.
50. Koirala S., Guo Q., Kalia R., Bui H.T., Eckert D.M., Frost A., Shaw J.M. Interchangeable adaptors regulate mitochondrial dynamin assembly for membrane scission. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E1342-E1351.
51. Loson O.C., Song Z., Chen H., Chan D.C. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 2013, 24:659-667.
52. Palmer C.S., Elgass K.D., Parton R.G., Osellame L.D., Stojanovski D., Ryan M.T. 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, 288:27584-27593.
53. Vilain S., Esposito G., Haddad D., Schaap O., Dobreva M.P., Vos M., Van Meensel S., Morais V.A., De Strooper B., Verstreken P. The yeast complex I equivalent NADH dehydrogenase rescues pink1 mutants. PLoS Genet. 2012, 8:e1002456.
54. Muller-Rischart A.K., Pilsl A., Beaudette P., Patra M., Hadian K., Funke M., Peis R., Deinlein A., Schweimer C., Kuhn P.H., Lichtenthaler S.F., Motori E., Hrelia S., Wurst W., Trumbach D., Langer T., Krappmann D., Dittmar G., Tatzelt J., Winklhofer K.F. The E3 ligase parkin maintains mitochondrial integrity by increasing linear ubiquitination of NEMO. Mol. Cell 2013, 49:908-921.
55. Lazarou M., Jin S.M., Kane L.A., Youle R.J. Role of PINK1 binding to the TOM complex and alternate intracellular membranes in recruitment and activation of the E3 ligase Parkin. Dev. Cell 2011, 22:320-333.
56. Otera H., Ishihara N., Mihara K. New insights into the function and regulation of mitochondrial fission. Biochim. Biophys. Acta 2013, 1833:1256-1268.
57. Taguchi N., Ishihara N., Jofuku A., Oka T., Mihara K. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 2007, 282:11521-11529.
58. Chang C.R., Blackstone C. Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 2007, 282:21583-21587.
59. Cereghetti G.M., Costa V., Scorrano L. Inhibition of Drp1-dependent mitochondrial fragmentation and apoptosis by a polypeptide antagonist of calcineurin. Cell Death Differ. 2010, 17:1785-1794.
60. 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.
61. Gegg M.E., Cooper J.M., Chau K.Y., Rojo M., Schapira A.H., Taanman J.W. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum. Mol. Genet. 2010, 19:4861-4870.
62. Wang H., Song P., Du L., Tian W., Liu M., Li D., Wang B., Zhu Y., Cao C., Zhao J., Chen Q. Parkin ubiquitinates Drp1 for proteasome-dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson disease. J. Biol. Chem. 2011, 286:11649-11658.
63. Gispert S., Ricciardi F., Kurz A., Azizov M., Hoepken H.H., Becker D., Voos W., Leuner K., Muller W.E., Kudin A.P., Kunz W.S., Zimmermann A., Roeper J., Wenzel D., Jendrach M., Garcia-Arencibia M., Fernandez-Ruiz J., Huber L., Rohrer H., Barrera M., Reichert A.S., Rub U., Chen A., Nussbaum R.L., Auburger G. Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One 2009, 4:e5777.
64. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., Stiles L., Haigh S.E., Katz S., Las G., Alroy J., Wu M., Py B.F., Yuan J., Deeney J.T., Corkey B.E., Shirihai O.S. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008, 27:433-446.
65. 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 Cells 2010, 15:887-900.
66. 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.
67. 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.
68. Otera H., Wang C., Cleland M.M., Setoguchi K., Yokota S., Youle R.J., Mihara K. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 2010, 191:1141-1158.