Proteolytic control of mitochondrial function and morphogenesis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 1, 2013, Pages 195-204

  Anand, Ruchika ^a   Langer, Thomas ^a,b   Baker, Michael James ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

AAA protease; Lon protease; Mitochondria; Mitochondrial dynamics; Mitophagy; Quality control

Indexed keywords

DRP1 PROTEIN; ENDOPEPTIDASE LA; F BOX PROTEIN; KINESIN; M AAA PROTEASE; MGM1 PROTEIN; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOFUSIN 1; MITOFUSIN 2; OPA1 PROTEIN; PARAPLEGIN; PARKIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PINK1 PROTEIN; PROTEINASE; TAFAZZIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

APOPTOSIS; AUTOPHAGY; CALCIUM CELL LEVEL; CELL FUNCTION; CELLULAR STRESS RESPONSE; CYTOSOL; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; IN VITRO STUDY; MITOCHONDRION; MITOPHAGY; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; STEROIDOGENESIS; THERMOGENESIS; UBIQUITINATION;

ANIMALS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MORPHOGENESIS; PROTEIN STABILITY; PROTEOLYSIS;

EID: 84871821553     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.06.025     Document Type: Review

References (151)

1. Glancy B., Balaban R.S. Role of mitochondrial Ca(2+) in the regulation of cellular energetics. Biochemistry 2012, 51:2959-2973.
2. Estaquier J., Vallette F., Vayssiere J.L., Mignotte B. The mitochondrial pathways of apoptosis. Adv. Exp. Med. Biol. 2012, 942:157-183.
3. Osman C., Voelker D.R., Langer T. Making heads or tails of phospholipids in mitochondria. J. Cell Biol. 2011, 192:7-16.
4. Braschi E., McBride H.M. Mitochondria and the culture of the Borg: understanding the integration of mitochondrial function within the reticulum, the cell, and the organism. Bioessays 2010, 32:958-966.
5. Nunnari J., Suomalainen A. Mitochondria: in sickness and in health. Cell 2012, 148:1145-1159.
6. Koopman W.J., Willems P.H., Smeitink J.A. Monogenic mitochondrial disorders. N. Engl. J. Med. 2012, 366:1132-1141.
7. Jiang Y., Wang X. Comparative mitochondrial proteomics: perspective in human disease. J. Hematol. Oncol. 2012, 5:11.
8. Chen X., Li J., Hou J., Xie Z., Yang F. Mammalian mitochondrial proteomics: insights into mitochondrial functions and mitochondria-related diseases. Expert Rev. Proteomics 2010, 7:333-345.
9. Wang C., Youle R.J. The role of mitochondria in apoptosis*. Annu. Rev. Genet. 2009, 43:95-118.
10. Martinou J.C., Youle R.J. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev. Cell 2011, 21:92-101.
11. Baker M.J., Tatsuta T., Langer T. Quality control of mitochondrial proteostasis. Cold Spring Harb. Perspect. Biol. 2011, 3.
12. Baker B.M., Haynes C.M. Mitochondrial protein quality control during biogenesis and aging. Trends Biochem. Sci. 2011, 36:254-261.
13. Weber T.A., Reichert A.S. Impaired quality control of mitochondria: aging from a new perspective. Exp. Gerontol. 2010, 45:503-511.
14. Luce K., Weil A.C., Osiewacz H.D. Mitochondrial protein quality control systems in aging and disease. Adv. Exp. Med. Biol. 2010, 694:108-125.
15. Tatsuta T., Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J. 2008, 27:306-314.
16. Rugarli E.I., Langer T. Mitochondrial quality control: a matter of life and death for neurons. EMBO J. 2012, 31:1336-1349.
17. Gerdes F., Tatsuta T., Langer T. Mitochondrial AAA proteases - towards a molecular understanding of membrane-bound proteolytic machines. Biochim. Biophys. Acta 2012, 1823:49-55.
18. Käser M., Kambacheld M., Kisters-Woike B., Langer T. Oma1, a novel membrane-bound metallopeptidase in mitochondria with activities overlapping with the m-AAA protease. J. Biol. Chem. 2003, 278:46414-46423.
19. Khalimonchuk O., Jeong M.Y., Watts T., Ferris E., Winge D.R. Selective Oma1 protease-mediated proteolysis of Cox1 subunit of cytochrome oxidase in assembly mutants. J. Biol. Chem. 2012, 287:7289-7300.
20. Bender T., Lewrenz I., Franken S., Baitzel C., Voos W. Mitochondrial enzymes are protected from stress-induced aggregation by mitochondrial chaperones and the Pim1/LON protease. Mol. Biol. Cell 2011, 22:541-554.
21. Bota D.A., Davies K.J. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol. 2002, 4:674-680.
22. Wagner I., Arlt H., van Dyck L., Langer T., Neupert W. Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO J. 1994, 13:5135-5145.
23. Pellegrino M.W., Nargund A.M., Haynes C.M. Signaling the mitochondrial unfolded protein response. Biochim. Biophys. Acta 2012, 10.1016/j.bbamcr.2012.02.019.
24. Haynes C.M., Ron D. The mitochondrial UPR - protecting organelle protein homeostasis. J. Cell Sci. 2010, 123:3849-3855.
25. Haynes C.M., Petrova K., Benedetti C., Yang Y., Ron D. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 2007, 13:467-480.
26. Livnat-Levanon N., Glickman M.H. Ubiquitin-proteasome system and mitochondria-reciprocity. Biochim. Biophys. Acta 2011, 1809:80-87.
27. Radke S., Chander H., Schafer P., Meiss G., Kruger R., Schulz J.B., Germain D. Mitochondrial protein quality control by the proteasome involves ubiquitination and the protease Omi. J. Biol. Chem. 2008, 283:12681-12685.
28. Karbowski M., Youle R.J. Regulating mitochondrial outer membrane proteins by ubiquitination and proteasomal degradation. Curr. Opin. Cell Biol. 2011, 23:476-482.
29. Palmer C.S., Osellame L.D., Stojanovski D., Ryan M.T. The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery. Cell. Signal. 2011, 23:1534-1545.
30. Westermann B. Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 2010, 11:872-884.
31. Chen H., McCaffery J.M., Chan D.C. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 2007, 130:548-562.
32. Chen H., Vermulst M., Wang Y.E., Chomyn A., Prolla T.A., McCaffery J.M., Chan D.C. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010, 141:280-289.
33. Ono T., Isobe K., Nakada K., Hayashi J.I. Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria. Nat. Genet. 2001, 28:272-275.
34. Tondera D., Grandemange S., Jourdain A., Karbowski M., Mattenberger Y., Herzig S., Da Cruz S., Clerc P., Raschke I., Merkwirth C., Ehses S., Krause F., Chan D.C., Alexander C., Bauer C., Youle R., Langer T., Martinou J.C. SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J. 2009, 28:1589-1600.
35. 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.
36. 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.
37. 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.
38. Kim I., Rodriguez-Enriquez S., Lemasters J.J. Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 2007, 462:245-253.
39. Landes T., Martinou J.C. Mitochondrial outer membrane permeabilization during apoptosis: the role of mitochondrial fission. Biochim. Biophys. Acta 2011, 1813:540-545.
40. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 2001, 1:515-525.
41. Soubannier V., McLelland G.L., Zunino R., Braschi E., Rippstein P., Fon E.A., McBride H.M. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr. Biol. 2012, 22:135-141.
42. Neuspiel M., Schauss A.C., Braschi E., Zunino R., Rippstein P., Rachubinski R.A., Andrade-Navarro M.A., McBride H.M. Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 2008, 18:102-108.
43. Andrade-Navarro M.A., Sanchez-Pulido L., McBride H.M. Mitochondrial vesicles: an ancient process providing new links to peroxisomes. Curr. Opin. Cell Biol. 2009, 21:560-567.
44. Matsushima Y., Kaguni L.S. Matrix proteases in mitochondrial DNA function. Biochim. Biophys. Acta 2011, 10.1016/j.bbagrm.2011.11.008.
45. Venkatesh S., Lee J., Singh K., Lee I., Suzuki C.K. Multitasking in the mitochondrion by the ATP-dependent Lon protease. Biochim. Biophys. Acta 2012, 1823:56-66.
46. van Dyck L., Neupert W., Langer T. The ATP-dependent PIM1 protease is required for the expression of intron-containing genes in mitochondria. Genes Dev. 1998, 12:1515-1524.
47. Matsushima Y., Goto Y., Kaguni L.S. Mitochondrial Lon protease regulates mitochondrial DNA copy number and transcription by selective degradation of mitochondrial transcription factor A (TFAM). Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18410-18415.
48. Charette M.F., Henderson G.W., Doane L.L., Markovitz A. DNA-stimulated ATPase activity on the lon (CapR) protein. J. Bacteriol. 1984, 158:195-201.
49. Fu G.K., Markovitz D.M. The human LON protease binds to mitochondrial promoters in a single-stranded, site-specific, strand-specific manner. Biochemistry 1998, 37:1905-1909.
50. Pierson T.M., Adams D., Bonn F., Martinelli P., Cherukuri P.F., Teer J.K., Hansen N.F., Cruz P., Mullikin J.C., For The Nisc Comparative Sequencing Program, Blakesley R.W., Golas G., Kwan J., Sandler A., Fuentes Fajardo K., Markello T., Tifft C., Blackstone C., Rugarli E.I., Langer T., Gahl W.A., Toro C. Whole-exome sequencing identifies homozygous AFG3L2 mutations in a spastic ataxia-neuropathy syndrome linked to mitochondrial m-AAA proteases. PLoS Genet. 2011, 7:e1002325.
51. Di Bella D., Lazzaro F., Brusco A., Plumari M., Battaglia G., Pastore A., Finardi A., Cagnoli C., Tempia F., Frontali M., Veneziano L., Sacco T., Boda E., Brussino A., Bonn F., Castellotti B., Baratta S., Mariotti C., Gellera C., Fracasso V., Magri S., Langer T., Plevani P., Di Donato S., Muzi-Falconi M., Taroni F. Mutations in the mitochondrial protease gene AFG3L2 cause dominant hereditary ataxia SCA28. Nat. Genet. 2010, 42:313-321.
52. Casari G., De Fusco M., Ciarmatori S., Zeviani M., Mora M., Fernandez P., De Michele G., Filla A., Cocozza S., Marconi R., Durr A., Fontaine B., Ballabio A. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell 1998, 93:973-983.
53. Bonn F., Tatsuta T., Petrungaro C., Riemer J., Langer T. Presequence-dependent folding ensures MrpL32 processing by the m-AAA protease in mitochondria. EMBO J. 2011, 30:2545-2556.
54. Nolden M., Ehses S., Koppen M., Bernacchia A., Rugarli E.I., Langer T. The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria. Cell 2005, 123:277-289.
55. Rugarli E.I., Langer T. Translating m-AAA protease function in mitochondria to hereditary spastic paraplegia. Trends Mol. Med. 2006, 12:262-269.
56. Gebert N., Joshi A.S., Kutik S., Becker T., McKenzie M., Guan X.L., Mooga V.P., Stroud D.A., Kulkarni G., Wenk M.R., Rehling P., Meisinger C., Ryan M.T., Wiedemann N., Greenberg M.L., Pfanner N. Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome. Curr. Biol. 2009, 19:2133-2139.
57. Choi S.Y., Gonzalvez F., Jenkins G.M., Slomianny C., Chretien D., Arnoult D., Petit P.X., Frohman M.A. Cardiolipin deficiency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis. Cell Death Differ. 2007, 14:597-606.
58. Zhong Q., Gohil V.M., Ma L., Greenberg M.L. Absence of cardiolipin results in temperature sensitivity, respiratory defects, and mitochondrial DNA instability independent of pet56. J. Biol. Chem. 2004, 279:32294-32300.
59. Bione S., D'Adamo P., Maestrini E., Gedeon A.K., Bolhuis P.A., Toniolo D. A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat. Genet. 1996, 12:385-389.
60. Schlame M., Ren M. Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett. 2006, 580:5450-5455.
61. Houtkooper R.H., Turkenburg M., Poll-The B.T., Karall D., Perez-Cerda C., Morrone A., Malvagia S., Wanders R.J., Kulik W., Vaz F.M. The enigmatic role of tafazzin in cardiolipin metabolism. Biochim. Biophys. Acta 2009, 1788:2003-2014.
62. Potting C., Wilmes C., Engmann T., Osman C., Langer T. Regulation of mitochondrial phospholipids by Ups1/PRELI-like proteins depends on proteolysis and Mdm35. EMBO J. 2010, 29:2888-2898.
63. Dee C.T., Moffat K.G. A novel family of mitochondrial proteins is represented by the Drosophila genes slmo, preli-like and real-time. Dev. Genes Evol. 2005, 215:248-254.
64. Fox E.J., Stubbs S.A., Kyaw Tun J., Leek J.P., Markham A.F., Wright S.C. PRELI (protein of relevant evolutionary and lymphoid interest) is located within an evolutionarily conserved gene cluster on chromosome 5q34-q35 and encodes a novel mitochondrial protein. Biochem. J. 2004, 378:817-825.
65. Tamura Y., Endo T., Iijima M., Sesaki H. Ups1p and Ups2p antagonistically regulate cardiolipin metabolism in mitochondria. J. Cell Biol. 2009, 185:1029-1045.
66. Osman C., Haag M., Potting C., Rodenfels J., Dip P.V., Wieland F.T., Brugger B., Westermann B., Langer T. The genetic interactome of prohibitins: coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria. J. Cell Biol. 2009, 184:583-596.
67. Leonhard K., Herrmann J.M., Stuart R.A., Mannhaupt G., Neupert W., Langer T. AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J. 1996, 15:4218-4229.
68. Nebauer R., Schuiki I., Kulterer B., Trajanoski Z., Daum G. The phosphatidylethanolamine level of yeast mitochondria is affected by the mitochondrial components Oxa1p and Yme1p. FEBS J. 2007, 274:6180-6190.
69. Granot Z., Kobiler O., Melamed-Book N., Eimerl S., Bahat A., Lu B., Braun S., Maurizi M.R., Suzuki C.K., Oppenheim A.B., Orly J. Turnover of mitochondrial steroidogenic acute regulatory (StAR) protein by Lon protease: the unexpected effect of proteasome inhibitors. Mol. Endocrinol. 2007, 21:2164-2177.
70. Granot Z., Melamed-Book N., Bahat A., Orly J. Turnover of StAR protein: roles for the proteasome and mitochondrial proteases. Mol. Cell. Endocrinol. 2007, 265-266:51-58.
71. Lin D., Sugawara T., Strauss J.F., Clark B.J., Stocco D.M., Saenger P., Rogol A., Miller W.L. Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 1995, 267:1828-1831.
72. Granot Z., Geiss-Friedlander R., Melamed-Book N., Eimerl S., Timberg R., Weiss A.M., Hales K.H., Hales D.B., Stocco D.M., Orly J. Proteolysis of normal and mutated steroidogenic acute regulatory proteins in the mitochondria: the fate of unwanted proteins. Mol. Endocrinol. 2003, 17:2461-2476.
73. Ondrovicova G., Liu T., Singh K., Tian B., Li H., Gakh O., Perecko D., Janata J., Granot Z., Orly J., Kutejova E., Suzuki C.K. Cleavage site selection within a folded substrate by the ATP-dependent Lon protease. J. Biol. Chem. 2005, 280:25103-25110.
74. Bolender N., Sickmann A., Wagner R., Meisinger C., Pfanner N. Multiple pathways for sorting mitochondrial precursor proteins. EMBO Rep. 2008, 9:42-49.
75. Abe Y., Shodai T., Muto T., Mihara K., Torii H., Nishikawa S., Endo T., Kohda D. Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 2000, 100:551-560.
76. Neupert W., Herrmann J.M. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 2007, 76:723-749.
77. Gakh O., Cavadini P., Isaya G. Mitochondrial processing peptidases. Biochim. Biophys. Acta 2002, 1592:63-77.
78. Vogtle F.N., Wortelkamp S., Zahedi R.P., Becker D., Leidhold C., Gevaert K., Kellermann J., Voos W., Sickmann A., Pfanner N., Meisinger C. Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 2009, 139:428-439.
79. Vogtle F.N., Prinz C., Kellermann J., Lottspeich F., Pfanner N., Meisinger C. Mitochondrial protein turnover: role of the precursor intermediate peptidase Oct1 in protein stabilization. Mol. Biol. Cell 2011, 22:2135-2143.
80. Mossmann D., Meisinger C., Vogtle F.N. Processing of mitochondrial presequences. Biochim. Biophys. Acta 2011, 10.1016/j.bbagrm.2011.11.007.
81. Varshavsky A. The N-end rule pathway and regulation by proteolysis. Protein Sci. 2011, 20:1298-1345.
82. Sriram S.M., Kim B.Y., Kwon Y.T. The N-end rule pathway: emerging functions and molecular principles of substrate recognition. Nat. Rev. Mol. Cell Biol. 2011, 12:735-747.
83. Anton F., Fres J.M., Schauss A., Pinson B., Praefcke G.J., Langer T., Escobar-Henriques M. Ugo1 and Mdm30 act sequentially during Fzo1-mediated mitochondrial outer membrane fusion. J. Cell Sci. 2011, 124:1126-1135.
84. Cohen M.M., Amiott E.A., Day A.R., Leboucher G.P., Pryce E.N., Glickman M.H., McCaffery J.M., Shaw J.M., Weissman A.M. Sequential requirements for the GTPase domain of the mitofusin Fzo1 and the ubiquitin ligase SCFMdm30 in mitochondrial outer membrane fusion. J. Cell Sci. 2011, 124:1403-1410.
85. Cohen M.M., Leboucher G.P., Livnat-Levanon N., Glickman M.H., Weissman A.M. Ubiquitin-proteasome-dependent degradation of a mitofusin, a critical regulator of mitochondrial fusion. Mol. Biol. Cell 2008, 19:2457-2464.
86. Escobar-Henriques M., Westermann B., Langer T. Regulation of mitochondrial fusion by the F-box protein Mdm30 involves proteasome-independent turnover of Fzo1. J. Cell Biol. 2006, 173:645-650.
87. Fritz S., Weinbach N., Westermann B. Mdm30 is an F-box protein required for maintenance of fusion-competent mitochondria in yeast. Mol. Biol. Cell 2003, 14:2303-2313.
88. Karbowski M., Neutzner A., Youle R.J. The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 2007, 178:71-84.
89. Nakamura N., Kimura Y., Tokuda M., Honda S., Hirose S. MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 2006, 7:1019-1022.
90. Park Y.Y., Lee S., Karbowski M., Neutzner A., Youle R.J., Cho H. Loss of MARCH5 mitochondrial E3 ubiquitin ligase induces cellular senescence through dynamin-related protein 1 and mitofusin 1. J. Cell Sci. 2010, 123:619-626.
91. 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. A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. EMBO J. 2006, 25:3618-3626.
92. Karbowski M., Lee Y.J., Gaume B., Jeong S.Y., Frank S., Nechushtan A., Santel A., Fuller M., Smith C.L., Youle R.J. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 2002, 159:931-938.
93. Smirnova E., Griparic L., Shurland D.L., van der Bliek A.M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 2001, 12:2245-2256.
94. Ingerman E., Perkins E.M., Marino M., Mears J.A., McCaffery J.M., Hinshaw J.E., Nunnari J. Dnm1 forms spirals that are structurally tailored to fit mitochondria. J. Cell Biol. 2005, 170:1021-1027.
95. Chang C.R., Blackstone C. Dynamic regulation of mitochondrial fission through modification of the dynamin-related protein Drp1. Ann. N. Y. Acad. Sci. 2010, 1201:34-39.
96. Braschi E., Zunino R., McBride H.M. MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep. 2009, 10:748-754.
97. Harder Z., Zunino R., McBride H. Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol. 2004, 14:340-345.
98. Zunino R., Braschi E., Xu L., McBride H.M. Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J. Biol. Chem. 2009, 284:17783-17795.
99. Wong E.D., Wagner J.A., Scott S.V., Okreglak V., Holewinske T.J., Cassidy-Stone A., Nunnari J. The intramitochondrial dynamin-related GTPase, Mgm1p, is a component of a protein complex that mediates mitochondrial fusion. J. Cell Biol. 2003, 160:303-311.
100. Frezza C., Cipolat S., Martins de Brito O., Micaroni M., Beznoussenko G.V., Rudka T., Bartoli D., Polishuck R.S., Danial N.N., De Strooper B., Scorrano L. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 2006, 126:177-189.
101. Ishihara N., Fujita Y., Oka T., Mihara K. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 2006, 25:2966-2977.
102. Meeusen S., DeVay R., Block J., Cassidy-Stone A., Wayson S., McCaffery J.M., Nunnari J. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell 2006, 127:383-395.
103. DeVay R.M., Dominguez-Ramirez L., Lackner L.L., Hoppins S., Stahlberg H., Nunnari J. Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J. Cell Biol. 2009, 186:793-803.
104. Herlan M., Vogel F., Bornhovd C., Neupert W., Reichert A.S. Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J. Biol. Chem. 2003, 278:27781-27788.
105. Song Z., Chen H., Fiket M., Alexander C., Chan D.C. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J. Cell Biol. 2007, 178:749-755.
106. Zick M., Duvezin-Caubet S., Schafer A., Vogel F., Neupert W., Reichert A.S. Distinct roles of the two isoforms of the dynamin-like GTPase Mgm1 in mitochondrial fusion. FEBS Lett. 2009, 583:2237-2243.
107. McQuibban G.A., Saurya S., Freeman M. Mitochondrial membrane remodelling regulated by a conserved rhomboid protease. Nature 2003, 423:537-541.
108. Herlan M., Bornhovd C., Hell K., Neupert W., Reichert A.S. Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor. J. Cell Biol. 2004, 165:167-173.
109. Baricault L., Segui B., Guegand L., Olichon A., Valette A., Larminat F., Lenaers G. OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. Exp. Cell Res. 2007, 313:3800-3808.
110. Duvezin-Caubet S., Jagasia R., Wagener J., Hofmann S., Trifunovic A., Hansson A., Chomyn A., Bauer M.F., Attardi G., Larsson N.G., Neupert W., Reichert A.S. Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J. Biol. Chem. 2006, 281:37972-37979.
111. Guillery O., Malka F., Landes T., Guillou E., Blackstone C., Lombes A., Belenguer P., Arnoult D., Rojo M. Metalloprotease-mediated OPA1 processing is modulated by the mitochondrial membrane potential. Biol. Cell 2008, 100:315-325.
112. 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. Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 2006, 126:163-175.
113. 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.
114. 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.
115. Ehses S., Raschke I., Mancuso G., Bernacchia A., Geimer S., Tondera D., Martinou J.C., Westermann B., Rugarli E.I., Langer T. Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 2009, 187:1023-1036.
116. Head B., Griparic L., Amiri M., Gandre-Babbe S., van der Bliek A.M. Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J. Cell Biol. 2009, 187:959-966.
117. Quiros P.M., Ramsay A.J., Sala D., Fernandez-Vizarra E., Rodriguez F., Peinado J.R., Fernandez-Garcia M.S., Vega J.A., Enriquez J.A., Zorzano A., Lopez-Otin C. Loss of mitochondrial protease OMA1 alters processing of the GTPase OPA1 and causes obesity and defective thermogenesis in mice. EMBO J. 2012, 31:2117-2133.
118. Youle R.J., Narendra D.P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 2011, 12:9-14.
119. Kanki T., Wang K., Cao Y., Baba M., Klionsky D.J. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 2009, 17:98-109.
120. Okamoto K., Kondo-Okamoto N., Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 2009, 17:87-97.
121. Novak I., Kirkin V., McEwan D.G., Zhang J., Wild P., Rozenknop A., Rogov V., Lohr F., Popovic D., Occhipinti A., Reichert A.S., Terzic J., Dotsch V., Ney P.A., Dikic I. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010, 11:45-51.
122. 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 activate Parkin. PLoS Biol. 2010, 8:e1000298.
123. 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.
124. Narendra D., Tanaka A., Suen D.F., Youle R.J. Parkin-induced mitophagy in the pathogenesis of Parkinson disease. Autophagy 2009, 5:706-708.
125. 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.
126. Kawajiri S., Saiki S., Sato S., Sato F., Hatano T., Eguchi H., Hattori N. PINK1 is recruited to mitochondria with parkin and associates with LC3 in mitophagy. FEBS Lett. 2010, 584:1073-1079.
127. 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.
128. Deas E., Plun-Favreau H., Gandhi S., Desmond H., Kjaer S., Loh S.H., Renton A.E., Harvey R.J., Whitworth A.J., Martins L.M., Abramov A.Y., Wood N.W. PINK1 cleavage at position A103 by the mitochondrial protease PARL. Hum. Mol. Genet. 2011, 20:867-879.
129. Greene A.W., Grenier K., Aguileta M.A., Muise S., Farazifard R., Haque M.E., McBride H.M., Park D.S., Fon E.A. Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep. 2012, 13:378-385.
130. Jin S.M., Lazarou M., Wang C., Kane L.A., Narendra D.P., Youle R.J. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 2010, 191:933-942.
131. Meissner C., Lorenz H., Weihofen A., Selkoe D.J., Lemberg M.K. The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J. Neurochem. 2011, 117:856-867.
132. Shi G., Lee J.R., Grimes D.A., Racacho L., Ye D., Yang H., Ross O.A., Farrer M., McQuibban G.A., Bulman D.E. Functional alteration of PARL contributes to mitochondrial dysregulation in Parkinson's disease. Hum. Mol. Genet. 2011, 20:1966-1974.
133. 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 2012, 22:320-333.
134. Becker D., Richter J., Tocilescu M.A., Przedborski S., Voos W. Pink1 and its {Delta}psi-dependent cleavage product both localize to the outer mitochondrial membrane by a unique targeting mode. J. Biol. Chem. 2012, 287:22969-22987.
135. 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.
136. 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.
137. Lee J.Y., Nagano Y., Taylor J.P., Lim K.L., Yao T.P. Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J. Cell Biol. 2010, 189:671-679.
138. 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.
139. 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.
140. Glauser L., Sonnay S., Stafa K., Moore D.J. Parkin promotes the ubiquitination and degradation of the mitochondrial fusion factor mitofusin 1. J. Neurochem. 2011, 118:636-645.
141. Poole A.C., Thomas R.E., Yu S., Vincow E.S., Pallanck L. The mitochondrial fusion-promoting factor mitofusin is a substrate of the PINK1/parkin pathway. PLoS One 2010, 5:e10054.
142. 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.
143. 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.
144. 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.
145. 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.
146. Sandoval H., Thiagarajan P., Dasgupta S.K., Schumacher A., Prchal J.T., Chen M., Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008, 454:232-235.
147. Mortensen M., Ferguson D.J., Simon A.K. Mitochondrial clearance by autophagy in developing erythrocytes: clearly important, but just how much so?. Cell Cycle 2010, 9:1901-1906.
148. Schweers R.L., Zhang J., Randall M.S., Loyd M.R., Li W., Dorsey F.C., Kundu M., Opferman J.T., Cleveland J.L., Miller J.L., Ney P.A. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19500-19505.
149. Xu S., Peng G., Wang Y., Fang S., Karbowski M. The AAA-ATPase p97 is essential for outer mitochondrial membrane protein turnover. Mol. Biol. Cell 2011, 22:291-300.
150. Heo J.M., Livnat-Levanon N., Taylor E.B., Jones K.T., Dephoure N., Ring J., Xie J., Brodsky J.L., Madeo F., Gygi S.P., Ashrafi K., Glickman M.H., Rutter J. A stress-responsive system for mitochondrial protein degradation. Mol. Cell 2010, 40:465-480.
151. Shcherbik N., Haines D.S. Cdc48p(Npl4p/Ufd1p) binds and segregates membrane-anchored/tethered complexes via a polyubiquitin signal present on the anchors. Mol. Cell 2007, 25:385-397.