Quality control of mitochondria: Protection against neurodegeneration and ageing

EMBO Journal

Volumn 27, Issue 2, 2008, Pages 306-314

  Tatsuta, Takashi ^a   Langer, Thomas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Mitochondria; Mitochondrial dynamics; Mitochondrial proteases; Mitophagy; Neurodegeneration

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; MITOCHONDRIAL PROTEIN; PROTEIN OPA1; UNCLASSIFIED DRUG;

AGING; APOPTOSIS; AUTOPHAGY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN LOCALIZATION; QUALITY CONTROL; REVIEW; RIBOSOME;

AGING; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; NERVE DEGENERATION;

EID: 38549101188     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601972     Document Type: Review

References (84)

1. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, Moore A, Rodriguez M, Kellner U, Leo-Kottler B, Auburger G, Bhattacharya SS, Wissinger B (2000) OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26: 211-215
2. Atorino L, Silvestri L, Koppen M, Cassina L, Ballabio A, Marconi R, Langer T, Casari G (2003) Loss of m-AAA protease in mitochondria causes complex I deficiency and increased sensitivity to oxidative stress in hereditary spastic paraplegia. J Cell Biol 163: 777-787
3. Baloh RH, Schmidt RE, Pestronk A, Milbrandt J (2007) Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations. J Neurosci 27: 422-430
4. Baricault L, Segui B, Guegand L, Olichon A, Valette A, Larminat F, Lenaers G (2007) OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. Exp Cell Res 313: 3800-3808
5. Barsoum MJ, Yuan H, Gerencser AA, Liot G, Kushnareva Y, Graber S, Kovacs I, Lee WD, Waggoner J, Cui J, White AD, Bossy B, Martinou JC, Youle RJ, Lipton SA, Ellisman MH, Perkins GA, Bossy-Wetzel E (2006) Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J 25: 3900-3911
6. Bateman JM, Iacovino M, Perlman PS, Butow RA (2002) Mitochondrial DNA instability mutants of the bifunctional protein Ilv5p have altered organization in mitochondria and are targeted for degradation by Hsp78 and the Pim1p protease. J Biol Chem 277: 47946-47953
7. Bota DA, Davies KJ (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol 4: 674-680
8. Bota DA, Ngo JK, Davies KJ (2005) Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radic Biol Med 38: 665-677
9. Bota DA, Van Remmen H, Davies KJ (2002) Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress. FEBS Lett 532: 103-106
10. Casari G, De-Fusco M, Ciarmatori S, Zeviani M, Mora M, Fernandez P, DeMichele G, Filla A, Cocozza S, Marconi R, Durr A, Fontaine B, Ballabio A (1998) Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell 93: 973-983
11. Cerveny KL, Tamura Y, Zhang Z, Jensen RE, Sesaki H (2007) Regulation of mitochondrial fusion and division. Trends Cell Biol 17: 563-569
12. Chen H, Chomyn A, Chan DC (2005) Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 280: 26185-26192
13. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160: 189-200
14. Chen H, McCaffery JM, Chan DC (2007) Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130: 548-562
15. Cheng X, Kanki T, Fukuoh A, Ohgaki K, Takeya R, Aoki Y, Hamasaki N, Kang D (2005) PDIP38 associates with proteins constituting the mitochondrial DNA nucleoid. J Biochem (Tokyo) 138: 673-678
16. Cipolat S, Rudka T, Hartmann D, Costa V, Serneels L, Craessaerts K, Metzger K, Frezza C, Annaert W, D'Adamio L, Derks C, Dejaegere T, Pellegrini L, D'Hooge R, Scorrano L, De Strooper B (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126: 163-175
17. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, Seol JH, Yoo SJ, Hay BA, Guo M (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441: 1162-1166
18. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, Astarie-Dequeker C, Lasquellec L, Arnaud B, Ducommun B, Kaplan J, Hamel CP (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26: 207-210
19. Delettre C, Lenaers G, Pelloquin L, Belenguer P, Hamel CP (2002) OPA1 (Kjer type) dominant optic atrophy: a novel mitochondrial disease. Mol Genet Metab 75: 97-107
20. Detmer SA, Chan DC (2007) Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol 8: 870-879
21. Dodson MW, Guo M (2007) Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson's disease. Curr Opin Neurobiol 17: 331-337
22. Duvezin-Caubet S, Jagasia R, Wagener J, Hofmann S, Trifunovic A, Hansson A, Chomyn A, Bauer MF, Attardi G, Larsson NG, Neupert W, Reichert AS (2006) Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J Biol Chem 281: 37972-37979
23. Duvezin-Caubet S, Koppen M, Wagener J, Zick M, Israel L, Bernacchia A, Jagasia R, Rugarli EI, Imhof A, Neupert W, Langer T, Reichert AS (2007) Processing of OPA1 reconstituted in yeast depends on the subunit composition of the m-AAA protease. Mol Biol Cell 18: 3582-3590
24. Escobar-Henriques M, Westermann B, Langer T (2006) Regulation of mitochondrial fusion by the F-box protein Mdm30 involves proteasome-independent turnover of Fzo1. J Cell Biol 173: 645-650
25. Esser K, Tursun B, Ingenhoven M, Michaelis G, Pratje E (2002) A novel two-step mechanism for removal of a mitochondrial signal sequence involves the m-AAA complex and the putative rhomboid protease Pcp1. J Mol Biol 323: 835-843
26. Exner N, Treske B, Paquet D, Holmstrom K, Schiesling C, Gispert S, Carballo-Carbajal I, Berg D, Hoepken HH, Gasser T, Kruger R, Winklhofer KF, Vogel F, Reichert AS, Auburger G, Kahle PJ, Schmid B, Haass C (2007) Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J Neurosci 27: 12413-12418
27. Ferreirinha F, Quattrini A, Priozzi M, Valsecchi V, Dina G, Broccoli V, Auricchio A, Piemonte F, Tozzi G, Gaeta L, Casari G, Ballabio A, Rugarli EI (2004) Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. J Clin Invest 113: 231-242
28. Griparic L, Kanazawa T, Van der Bliek AM (2007) Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J Cell Biol 178: 757-764
29. Habelhah H, Laine A, Erdjument-Bromage H, Tempst P, Gershwin ME, Bowtell DD, Ronai Z (2004) Regulation of 2-oxoglutarate (alpha-ketoglutarate) dehydrogenase stability by the RING finger ubiquitin ligase Siah. J Biol Chem 279: 53782-53788
30. Hansen JJ, Dürr A, Isabelle C-R, Georgopoulos C, Ang D, Nielson MN, Davoine CS, Brice A, Fontaine B, Gregersen N, Bross P (2002) Hereditary spastic paraplegia SPG13 is associated with a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am J Hum Genet 70: 1328-1332
31. Herlan M, Bornhovd C, Hell K, Neupert W, Reichert AS (2004) Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor. J Cell Biol 165: 167-173
32. Herlan M, Vogel F, Bornhövd C, Neupert W, Reichert AS (2003) Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J Biol Chem 278: 27781-27788
33. Hollenbeck PJ (1993) Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J Cell Biol 121: 305-315
34. Hoppins S, Lackner L, Nunnari J (2007) The machines that divide and fuse mitochondria. Annu Rev Biochem 76: 751-780
35. Ishihara N, Fujita Y, Oka T, Mihara K (2006) Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J 25: 2966-2977
36. Jones JM, Datta P, Srinivasula SM, Ji W, Gupta S, Zhang Z, Davies E, Hajnoczky G, Saunders TL, Van Keuren ML, Fernandes-Alnemri T, Meisler MH, Alnemri ES (2003) Loss of Omi mitochondrial protease activity causes the neuromuscular disorder of mnd2 mutant mice. Nature 425: 721-727
37. Karbowski M, Neutzner A, Youle RJ (2007) The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J Cell Biol 178: 71-84
38. Kim I, Rodriguez-Enriquez S, Lemasters JJ (2007) Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462: 245-253
39. Kissova I, Deffieu M, Manon S, Camougrand N (2004) Uth1p is involved in the autophagic degradation of mitochondria. J Biol Chem 279: 39068-39074
40. Koppen M, Langer T (2007) Protein degradation within mitochondria: versatile activities of AAA proteases and other peptidases. Crit Rev Biochem Mol Biol 42: 1-22
41. Koppen M, Metodiev MD, Casari G, Rugarli EI, Langer T (2007) Variable and tissue-specific subunit composition of mitochondrial m-AAA protease complexes linked to hereditary spastic paraplegia. Mol Cell Biol 27: 758-767
42. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87: 99-163
43. Leonhard K, Guiard B, Pellechia G, Tzagoloff A, Neupert W, Langer T (2000) Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol Cell 5: 629-638
44. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443: 787-795
45. Liu T, Lu B, Lee I, Ondrovicova G, Kutejova E, Suzuki CK (2004) DNA and RNA binding by the mitochondrial Lon protease is regulated by nucleotide and protein substrate. J Biol Chem 279: 13902-13910
46. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8: 741-752
47. Major T, von Janowsky B, Ruppert T, Mogk A, Voos W (2006) Proteomic analysis of mitochondrial protein turnover: identification of novel substrate proteins of the matrix protease Pim1. Mol Cell Biol 26: 762-776
48. Mandemakers W, Morais VA, De Strooper B (2007) A cell biological perspective on mitochondrial dysfunction in Parkinson disease and other neurodegenerative diseases. J Cell Sci 120: 1707-1716
49. Martins LM, Morrison A, Klupsch K, Fedele V, Moisoi N, Teismann P, Abuin A, Grau E, Geppert M, Livi GP, Creasy CL, Martin A, Hargreaves I, Heales SJ, Okada H, Brandner S, Schulz JB, Mak T, Downward J (2004) Neuroprotective role of the Reaper-related serine protease HtrA2/Omi revealed by targeted deletion in mice. Mol Cell Biol 24: 9848-9862
50. McBride HM, Neuspiel M, Wasiak S (2006) Mitochondria: more than just a powerhouse. Curr Biol 16: 551-560
51. McQuibban GA, Saurya S, Freeman M (2003) Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 423: 537-541
52. Meusser B, Hirsch C, Jarosch E, Sommer T (2005) ERAD: the long road to destruction. Nat Cell Biol 7: 766-772
53. Nakamura N, Kimura Y, Tokuda M, Honda S, Hirose S (2006) MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep 7: 1019-1022
54. Neutzner A, Youle RJ (2005) Instability of the mitofusin Fzo1 regulates mitochondrial morphology during the mating response of the yeast Saccharomyces cerevisiae. J Biol Chem 280: 18598-18603
55. Niemann A, Ruegg M, La Padula V, Schenone A, Suter U (2005) Ganglioside-induced differentiation associated protein 1 is a regulator of the mitochondrial network: new implications for Charcot-Marie-Tooth disease. J Cell Biol 170: 1067-1078
56. Nolden M, Ehses S, Koppen M, Bernacchia A, Rugarli EI, Langer T (2005) The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria. Cell 123: 277-289
57. Nowikovsky K, Reipert S, Devenish RJ, Schweyen RJ (2007) Mdm38 protein depletion causes loss of mitochondrial K(+)/H(+) exchange activity, osmotic swelling and mitophagy. Cell Death Differ 14: 1647-1656
58. Olichon A, Elachouri G, Baricault L, Delettre C, Belenguer P, Lenaers G (2007) OPA1 alternate splicing uncouples an evolutionary conserved function in mitochondrial fusion from a vertebrate restricted function in apoptosis. Cell Death Differ 14: 682-692
59. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, Bae E, Kim J, Shong M, Kim JM, Chung J (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441: 1157-1161
60. Pearce DA, Sherman F (1997) Differential ubiquitin-dependent degradation of the yeast apo-cytochrome c isozymes. J Biol Chem 272: 31829-31836
61. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, Roelofs J, Finley D, Gygi SP (2003) A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21: 921-926
62. Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6: 9-20
63. Plun-Favreau H, Klupsch K, Moisoi N, Gandhi S, Kjaer S, Frith D, Harvey K, Deas E, Harvey RJ, McDonald N, Wood NW, Martins LM, Downward J (2007) The mitochondrial protease HtrA2 is regulated by Parkinson's disease-associated kinase PINK1. Nat Cell Biol 9: 1243-1252
64. Pridgeon JW, Olzmann JA, Chin LS, Li L (2007) PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol 5: e172
65. Rainey RN, Glavin JD, Chen HW, French SW, Teitell MA, Koehler CM (2006) A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space. Mol Cell Biol 26: 8488-8497
66. Rodriguez-Enriquez S, Kim I, Currin RT, Lemasters JJ (2006) Tracker dyes to probe mitochondrial autophagy (mitophagy) in rat hepatocytes. Autophagy 2: 39-46
67. Röttgers K, Zufall N, Guiard B, Voos W (2002) The ClpB homolog Hsp78 is required for the efficient degradation of proteins in the mitochondrial matrix. J Biol Chem 277: 45829-45837
68. Rugarli EI, Langer T (2006) Translating m-AAA protease function in mitochondria to hereditary spastic paraplegia. Trends Mol Med 12: 262-269
69. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26: 1749-1760
70. Sesaki H, Southard SM, Hobbs AE, Jensen RE (2003) Cells lacking Pcp1p/Ugo2p, a rhomboid-like protease required for Mgm1p processing, lose mtDNA and mitochondrial structure in a Dnm1p-dependent manner, but remain competent for mitochondrial fusion. Biochem Biophys Res Commun 308: 276-283
71. Soderblom C, Blackstone C (2006) Traffic accidents: molecular genetic insights into the pathogenesis of the hereditary spastic paraplegias. Pharmacol Ther 109: 42-56
72. Song Z, Chen H, fiket M, Alexander C, Chan DC (2007) OPA1 processing control mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol 178: 749-755
73. Suzuki CK, Suda K, Wang N, Schatz G (1994) Requirement for the yeast gene LON in intramitochondrial proteolysis and maintenance of respiration. Science 264: 273-276
74. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahashi R (2001) A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 8: 613-621
75. Tal R, Winter G, Ecker N, Klionsky DJ, Abeliovich H (2007) Aup1p, a yeast mitochondrial protein phosphatase homolog, is required for efficient stationary phase mitophagy and cell survival. J Biol Chem 282: 5617-5624
76. Tatsuta T, Augustin S, Nolden M, Friedrichs B, Langer T (2007) m-AAA protease-driven membrane dislocation allows intramembrane cleavage by rhomboid in mitochondria. EMBO J 26: 325-335
77. Wagner I, Arlt H, van Dyck L, Langer T, Neupert W (1994) Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO J 13: 5135-5145
78. Xue L, Fletcher GC, Tolkovsky AM (2001) Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis. Curr Biol 11: 361-365
79. Yonashiro R, Ishido S, Kyo S, Fukuda T, Goto E, Matsuki Y, Ohmura-Hoshino M, Sada K, Hotta H, Yamamura H, Inatome R, Yanagi S (2006) A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J 25: 3618-3626
80. Yorimitsu T, Klionsky DJ (2005) Autophagy: molecular machinery for self-eating. Cell Death Differ 12: 1542-1552
81. Zahedi RP, Sickmann A, Boehm AM, Winkler C, Zufall N, Schonfisch B, Guiard B, Pfanner N, Meisinger C (2006) Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins. Mol Biol Cell 17: 1436-1450
82. Zhang Y, Qi H, Taylor R, Xu W, Liu LF, Jin S (2007) The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 3: 337-346
83. Züchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, Dadali EL, Zappia M, Nelis E, Patitucci A, Senderek J, Parman Y, Evgrafov O, Jonghe PD, Takahashi Y, Tsuji S, Pericak-Vance MA, Quattrone A, Battaloglu E, Polyakov AV, Timmerman V et al (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 36: 449-451
84. Züchner S, Vance JM (2005) Emerging pathways for hereditary axonopathies. J Mol Med 83: 935-943