Mitochondrial protein quality control during biogenesis and aging

Trends in Biochemical Sciences

Volumn 36, Issue 5, 2011, Pages 254-261

  Baker, Brooke M ^a   Haynes, Cole M ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 70; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; PARKIN; PDZ PROTEIN; PRESENILIN; PROTEASOME; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SERINE PROTEINASE OMI;

AGING; BIOGENESIS; CAENORHABDITIS ELEGANS; CELL DAMAGE; CELL ORGANELLE; CELL STRESS; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA REPLICATION; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; EXTRACELLULAR MATRIX; MITOCHONDRION; NEOPLASM; NONHUMAN; OUTER MEMBRANE; OXIDATIVE PHOSPHORYLATION; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN QUALITY; PROTEIN TRANSPORT; QUALITY CONTROL; REVIEW; TRANSCRIPTION REGULATION; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE;

AGING; ANIMALS; GENOME, MITOCHONDRIAL; HOMEOSTASIS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MUTATION; REACTIVE OXYGEN SPECIES;

EID: 79955664111     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2011.01.004     Document Type: Review

References (80)

1. Balaban R.S., et al. Mitochondria, oxidants, and aging. Cell 2005, 120:483-495.
2. Larsson N.G. Somatic mitochondrial DNA mutations in mammalian aging. Annu. Rev. Biochem. 2010, 79:683-706.
3. Tatsuta T., Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J. 2008, 27:306-314.
4. Pagliarini D.J., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
5. Wallace D.C. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 2005, 39:359-407.
6. Chen H., Chan D.C. Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 2009, 18:R169-176.
7. Youle R.J., Narendra D.P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 2011, 12:9-14.
8. Haynes C.M., et al. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 2007, 13:467-480.
9. Zhao Q., et al. A mitochondrial specific stress response in mammalian cells. EMBO J. 2002, 21:4411-4419.
10. Kirkwood T.B., et al. Stability of the cellular translation process. Int. Rev. Cytol. 1984, 92:93-132.
11. Qian S.B., et al. Characterization of rapidly degraded polypeptides in mammalian cells reveals a novel layer of nascent protein quality control. J. Biol. Chem. 2006, 281:392-400.
12. Schubert U., et al. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000, 404:770-774.
13. de Moura M.B., et al. Mitochondrial dysfunction in neurodegenerative diseases and cancer. Environ. Mol. Mutagen. 2010, 51:391-405.
14. Fernandez-Vizarra E., et al. Assembly of the oxidative phosphorylation system in humans: what we have learned by studying its defects. Biochim. Biophys. Acta 2009, 1793:200-211.
15. Keeney P.M., et al. Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J. Neurosci. 2006, 26:5256-5264.
16. Bonora E., et al. Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III. Cancer Res. 2006, 66:6087-6096.
17. Hao H.X., et al. SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 2009, 325:1139-1142.
18. Young J.C., et al. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 2003, 112:41-50.
19. Peng J., et al. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 2003, 21:921-926.
20. Jeon H.B., et al. A proteomics approach to identify the ubiquitinated proteins in mouse heart. Biochem. Biophys. Res. Commun. 2007, 357:731-736.
21. Fan A.C., et al. Hsp90 functions in the targeting and outer membrane translocation steps of Tom70-mediated mitochondrial import. J. Biol. Chem. 2006, 281:33313-33324.
22. Margineantu D.H., et al. Hsp90 inhibition decreases mitochondrial protein turnover. PLoS ONE 2007, 2:e1066.
23. Neutzner A., et al. Role of the ubiquitin conjugation system in the maintenance of mitochondrial homeostasis. Ann. N. Y. Acad. Sci. 2008, 1147:242-253.
24. Yonashiro R., et al. Mitochondrial ubiquitin ligase MITOL ubiquitinates mutant SOD1 and attenuates mutant SOD1-induced reactive oxygen species generation. Mol. Biol. Cell 2009, 20:4524-4530.
25. Jarosch E., et al. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat. Cell Biol. 2002, 4:134-139.
26. Xu S., et al. The AAA-ATPase p97 is essential for outer mitochondrial membrane protein turnover. Mol. Biol. Cell 2010, 10.1091/mbc.E10-09-0748.
27. Gegg M.E., et al. Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/Parkin-dependent manner upon induction of mitophagy. Hum. Mol. Genet. 2010, 19:4861-4870.
28. Tanaka A., et al. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 2010, 191:1367-1380.
29. Heo J.M., et al. A stress-responsive system for mitochondrial protein degradation. Mol. Cell 2010, 40:465-480.
30. Koehler C.M. The small Tim proteins and the twin Cx3C motif. Trends Biochem. Sci. 2004, 29:1-4.
31. Johnson F., Kaplitt M.G. Novel mitochondrial substrates of omi indicate a new regulatory role in neurodegenerative disorders. PLoS ONE 2009, 4:e7100.
32. Zhang Y., et al. Structural and functional analysis of the ligand specificity of the HtrA2/Omi PDZ domain. Protein Sci. 2007, 16:1738-1750.
33. Sohn J., et al. Allosteric activation of DegS, a stress sensor PDZ protease. Cell 2007, 131:572-583.
34. Kieper N., et al. Modulation of mitochondrial function and morphology by interaction of Omi/HtrA2 with the mitochondrial fusion factor OPA1. Exp. Cell Res. 2010, 316:1213-1224.
35. Martins L.M., et al. Neuroprotective role of the Reaper-related serine protease HtrA2/Omi revealed by targeted deletion in mice. Mol. Cell. Biol. 2004, 24:9848-9862.
36. McKenzie M., Ryan M.T. Assembly factors of human mitochondrial complex I and their defects in disease. IUBMB Life 2010, 62:497-502.
37. Leonhard K., et al. Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol. Cell 2000, 5:629-638.
38. Korbel D., et al. Membrane protein turnover by the m-AAA protease in mitochondria depends on the transmembrane domains of its subunits. EMBO Rep. 2004, 5:698-703.
39. Pajic A., et al. Yta10p is required for the ATP-dependent degradation of polypeptides in the inner membrane of mitochondria. FEBS Lett. 1994, 353:201-206.
40. Thorsness P.E., et al. Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol. Cell. Biol. 1993, 13:5418-5426.
41. Di Bella D., et al. Mutations in the mitochondrial protease gene AFG3L2 cause dominant hereditary ataxia SCA28. Nat. Genet. 2010, 42:313-321.
42. Nolden M., et al. The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria. Cell 2005, 123:277-289.
43. Tatsuta T., et al. m-AAA protease-driven membrane dislocation allows intramembrane cleavage by rhomboid in mitochondria. EMBO J. 2007, 26:325-335.
44. Jin S.M., et al. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 2010, 191:933-942.
45. Bukau B., et al. Molecular chaperones and protein quality control. Cell 2006, 125:443-451.
46. Kang S.G., et al. Human mitochondrial ClpP is a stable heptamer that assembles into a tetradecamer in the presence of ClpX. J. Biol. Chem. 2005, 280:35424-35432.
47. Yu A.Y., Houry W.A. ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett. 2007, 581:3749-3757.
48. Haynes C.M., et al. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol. Cell 2010, 37:529-540.
49. 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.
50. Bayot A., et al. Identification of novel oxidized protein substrates and physiological partners of the mitochondrial ATP-dependent Lon-like protease Pim1. J. Biol. Chem. 2010, 285:11445-11457.
51. Bender T., et al. The role of protein quality control in mitochondrial protein homeostasis under oxidative stress. Proteomics 2011, 10:1426-1443.
52. Suzuki C.K., et al. Requirement for the yeast gene LON in intramitochondrial proteolysis and maintenance of respiration. Science 1994, 264:273-276.
53. Bota D.A., et al. Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radic. Biol. Med. 2005, 38:665-677.
54. Vögtle F.N., et al. Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 2009, 139:428-439.
55. Aldridge J.E., et al. Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS ONE 2007, 2:e874.
56. Wang X., et al. Reduced cytosolic protein synthesis suppresses mitochondrial degeneration. Nat. Cell Biol. 2008, 10:1090-1097.
57. Harman D. The biologic clock: the mitochondria?. J. Am. Geriatr. Soc. 1972, 20:145-147.
58. Vermulst M., et al. DNA deletions and clonal mutations drive premature aging in mitochondrial mutator mice. Nat. Genet. 2008, 40:392-394.
59. Kujoth G.C., et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005, 309:481-484.
60. Trifunovic A., et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 2004, 429:417-423.
61. Chen Y.F., et al. Cisd2 deficiency drives premature aging and causes mitochondria-mediated defects in mice. Genes Dev. 2009, 23:1183-1194.
62. Bakala H., et al. Changes in rat liver mitochondria with aging. Lon protease-like reactivity and N(epsilon)-carboxymethyllysine accumulation in the matrix. Eur. J. Biochem. 2003, 270:2295-2302.
63. Hansen J., et al. Decreased expression of the mitochondrial matrix proteases Lon and ClpP in cells from a patient with hereditary spastic paraplegia (SPG13). Neuroscience 2008, 153:474-482.
64. Luce K., Osiewacz H.D. Increasing organismal healthspan by enhancing mitochondrial protein quality control. Nat. Cell Biol. 2009, 11:852-858.
65. Ben-Zvi A., et al. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14914-14919.
66. David D.C., et al. Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol. 2010, 8:e1000450.
67. Durieux J., et al. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 2011, 144:79-91.
68. Balch W.E., et al. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
69. Kirstein J., et al. The antibiotic ADEP reprogrammes ClpP, switching it from a regulated to an uncontrolled protease. EMBO Mol. Med. 2009, 1:37-49.
70. Fukuda R., et al. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 2007, 129:111-122.
71. Greenamyre J.T., et al. Complex I and Parkinson's disease. IUBMB Life 2001, 52:135-141.
72. Narendra D.P., et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010, 8:e1000298.
73. Clark I.E., et al. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 2006, 441:1162-1166.
74. Park J., et al. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 2006, 441:1157-1161.
75. Strauss K.M., et al. Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease. Hum. Mol. Genet. 2005, 14:2099-2111.
76. Gogvadze V., et al. Mitochondria in cancer cells: what is so special about them?. Trends Cell Biol. 2008, 18:165-173.
77. Kang B.H., et al. Regulation of tumor cell mitochondrial homeostasis by an organelle-specific Hsp90 chaperone network. Cell 2007, 131:257-270.
78. Tsai Y.P., et al. Direct regulation of HSP60 expression by c-MYC induces transformation. FEBS Lett. 2008, 582:4083-4088.
79. Dewhirst M.W., et al. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat. Rev. Cancer 2008, 8:425-437.
80. Baysal B.E., et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000, 287:848-851.