Protein degradation in mitochondria: Implications for oxidative stress, aging and disease:: A novel etiological classification of mitochondrial proteolytic disorders

Mitochondrion

Volumn 1, Issue 1, 2001, Pages 33-49

  Bota, Daniela A ^a   Davies, Kelvin J A ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Clp; Free radicals; Lon; Mitochondria; Oxidative stress; Protein turnover; Proteolysis

Indexed keywords

MAMMALIA;

EID: 0003097634     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1567-7249(01)00005-8     Document Type: Article

References (169)

1. Adamec J., Gakh O., Spizek J., Kalousek F. Complementation between mitochondrial processing peptidase (MPP) subunits from different species. Arch. Biochem. Biophys. 370:1999;77-85.
2. Amerik A.Y., Petukhova G.V., Grigorenko V.G., et al. Cloning and sequence analysis of cDNA for a human homolog of eubacterial ATP-dependent Lon proteases. FEBS Lett. 340:1994;25-28.
3. Arlt H., Tauer R., Feldmann H., Neupert W., Langer T. The YTA10-12 complex, an AAA-protease with chaperone-like activity in the inner membrane of the mitochondria. Cell. 85:1996;875-885.
4. Arlt H., Steglich G., Perryman R., Guiard B., Neupert W., Langer T. The formation of respiratory chain complexes in mitochondria is under the proteolytic control of the m-AAA protease. EMBO J. 17:1998;4837-4847.
5. Arribas J., Castano J.C. A comparative study of the chymotrypsin-like activity of the rat liver multicatalytic proteinase and the ClpP from Escherichia coli. J. Biol. Chem. 268:1993;21165-21171.
6. Babcock M., de Silva D., Oaks R., et al. Regulation of mitochondrial iron accumulation by Yfh1, a putative homolog of frataxin. Science. 276:1997;1709-1712.
7. Banfi S., Bassi M.T., Andolfi G., et al. Identification & characterization of AFG3L2, a novel paraplegin-related gene. Genomics. 59:1999;51-58.
8. Berger K.H., Yaffe M.P. Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:1998;4043-4052.
9. Bharadwaj D., Roy M.S., Bose D., Hati R.N. A new blood-coagulating protease in mitochondrial membranes of rat submaxillary glands. Purification and characterization of protease and its blood-coagulating activity. J. Biol. Chem. 269:1994;16229-16235.
10. Bharadwaj M., Bharadwaj D., Hati R.N. Characterization of a membrane protease from rat submaxillary-gland mitochondria that possesses thrombin-like activity. Biochem. J. 313:1996;193-199.
11. Bota D.A., Davies K.J.A. The Lon protease appears to be primarily responsible for degradation of oxidatively-denaturated aconitase in mitochondria. Free Radic. Biol. Med. 29:2000;S80.
12. Branda S.S., Cavadini P., Adamec J., Kalousek F., Taroni F., Isaya G. Yeast and human frataxin are processed to mature form in two sequential steps by the mitochondrial processing peptidase. J. Biol. Chem. 274:1999;22763-22769.
13. Brookes C., Wright A., Evans P.J., Mayer R.J. Aflatoxin B1: effect on the synthesis and degradation of mitochondrial proteins in hepatocyte monolayers. Carcinogenesis. 5:1984;759765.
14. Bross P., Andresen B.S., Knudsen L., Kruse T.A., Gregersen N. Human ClpP protease: cDNA sequence, tissue-specific expression and chromosomal assignment of the gene. FEBS Lett. 377:1995;249-252.
15. Brunner M., Neupert W. Purification and characterization of mitochondrial processing peptidase of Neurospora crassa. Methods Enzymol. 248:1995;717-728.
16. Cadenas E., Davies K.J.A. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29:2000;222-230.
17. Campuzano V., Montermini L., Molto M.D., et al. Friedreich ataxia; autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science. 271:1996;1423-1427.
18. Campuzano V., Montermini L., Lutz Y., et al. Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum. Mol. Genet. 6:1997;1771-1780.
19. Casari G., De Fusco M., Ciarmatori S., et al. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell. 93:1998;973-983.
20. Clenton-Jansen A.M., Moerland E.W., Kuipers-Dijkshoorn N.J., et al. At least two different regions are involved in allelic imbalance on chromosome arm 16q in breast cancer. Genes Chromosomes Cancer. 9:1994;101-107.
21. Coates P.J., Jamieson D.J., Prescott A.R., Hall P.A. The prohibitin family of mitochondrial proteins regulate replicative lifespan. Curr. Biol. 7:1997;R607-R610.
22. Coppola M., Pizzigoni A., Banfi S., Bassi M.T., Casari G., Incerti B. Identification and characterization of YME1L1, a novel paraplegin-related gene. Genomics. 66:2000;48-54.
23. Corydon T.J., Bross P., Holst H.U., et al. A human homologue of Escherichia coli ClpP caseinolytic protease: recombinant expression, intracellular processing and subcellular localization. Biochem. J. 331:1998;309-316.
24. Daum G., Gasser S., Schatz G. Import of proteins into mitochondria. Energy-dependent, two-step processing of the intermembrane space enzyme cytochrome b2 by isolated yeast mitochondria. J. Biol. Chem. 257:1982;13075-13080.
25. Davies K.J.A. Intracellular proteolytic systems may function as secondary antioxidant defenses: an hypothesis. J. Free Radic. Biol. Med. 2:1986;155173.
26. Davies K.J.A. The role of intracellular proteolytic systems in antioxidant defenses. Rotillio G. Superoxide and Superoxide Dismutase in Chemistry, Biology, and Medicine. 1986;443-450 Elsevier, Amsterdam.
27. Davies K.J.A. Proteolytic systems as secondary antioxidant defenses. Chow C.K. Cellular Antioxidant Defense Mechanisms. 1988;25-67 CRC Press, Boca Raton, FL.
28. Davies K.J.A. Oxidative Stress: the paradox of aerobic life. Biochem. Soc. Symp. 61:1995;1-31.
29. Davies K.J.A. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life. 2001;. in press.
30. Davies K.J.A., Doroshow J.H. Redox cycling of anthracyclines by cardiac mitochondria: I. Anthracycline radical formation by NADH dehydrogenase. J. Biol. Chem. 261:1986;3060-3067.
31. Davies K.J.A., Hochstein P. Ubisemiquinone radicals in liver: implications for a mitochondrial Q cycle in vivo. Biochem. Biophys. Res. Commun. 107:1982;1292-1299.
32. Davies K.J.A., Lin S.W. Degradation of oxidatively denatured proteins in Escherichia coli. Free Radic. Biol. Med. 5:1988;215-223.
33. Davies K.J.A., Lin S.W. Oxidatively denatured proteins are degraded by an ATP-independent pathway in Escherichia coli. Free Radic. Biol. Med. 5:1988;225-236.
34. Davies K.J.A., Quintanilha A.T., Brooks G.A., Packer L. Free radicals and tissue damage produced by exercise. Biochem. Biophys. Res. Commun. 107:1982;1198-1205.
35. De Michele G., De Fusco M., Cavalcanti F., et al. A new locus for autosomal recessive spastic paraplegia maps to chromosome 16q24.3. Am. J. Hum. Genet. 63:1998;135-139.
36. De Sagarra M.R., Mayo I., Marco S., et al. Mitochondrial localization and oligomeric structure of HclpP, the human homologue of E. coli ClpP. J. Mol. Biol. 292:1999;819-825.
37. Dean R.T., Pollak J.K. Endogenous free radical production may influence proteolysis in mitochondria. Biochem. Biophys Res. Commun. 126:1985;1082-1089.
38. Dell'Orco R.T., McClung J.K., Jupe E.R., Liu X.T. Prohibitin and the senescent phenotype. Exp. Gerontol. 31:1996;245-252.
39. Desautels M., Goldberg A.L. Liver mitochondria contain an ATP-dependent, vanadate-sensitive pathway for the degradation of proteins. Proc. Natl. Acad. Sci. USA. 79:1982;1869-1873.
40. Desautels M., Goldberg A.L. Demonstration of an ATP-sensitive endoprotease in the matrix of rat liver mitochondria. J. Biol. Chem. 257:1982;11673-11679.
41. Dice J.F., Goldberg A.L. Relationship between in vivo degradative rates and isoelectric points of proteins. Proc. Natl. Acad. Sci. USA. 72:1975;3893-3897.
42. Doroshow J.H., Davies K.J.A. Redox cycling of anthracyclines by cardiac mitochondria: II. Formation of superoxide anion, hydrogen peroxide, and hydroxyl radical. J. Biol. Chem. 261:1986;3068-3074.
43. Durbin H., Novelli M.R., Brodmer W.F. Genomic and cDNA sequence analysis of the cell matrix adhesion regulator gene. Proc. Natl. Acad. Sci. USA. 94:1997;14578-14583.
44. Positional cloning of the Fanconi anaemia group A gene. Nat. Genet. 14:1996;324-328.
45. Fu G.K., Markovitz D.M. The human Lon protease binds to mitochondrial promoters in a single-stranded, site-specific, strand-specific manner. Biochemistry. 37:1998;1905-1909.
46. Gasser S., Daum G., Schatz G. Import of proteins into mitochondria. Energy-dependent uptake of precursors by isolated mitochondria. J. Biol. Chem. 257:1982;13034-13041.
47. Gavel Y., von Heijne G. Cleavage-site motifs in mitochondrial targeting peptides. Protein Eng. 4:1990;33-37.
48. Geli V., Yang M., Suda K., Lustig A., Schatz G. The MAS-encoded processing protease of yeast mitochondria. Overproduction and characterization of its two nonidentical subunits. J. Biol. Chem. 265:1990;19216-19222.
49. Glick B., Schatz G. Import of proteins into mitochondria. Annu. Rev. Genet. 25:1991;21-44.
50. Gobel H.R. Neuronal ceroid-lipofuscinoses. The current status. Brain Dev. 14:1992;203-211.
51. Gottesman S., Clark W.P., Maurizi M.R. The ATP-dependent Clp protease of Escherichia coli. Sequence of clpA and identification of a Clp-specific substrate. J. Biol. Chem. 265:1990;7886-7893.
52. Gottesman S., Squires C., Pichersky E., et al. Conservation of the regulatory subunit for the Clp ATP-dependent protease in prokaryotes and eukaryotes. Proc. Natl. Acad. Sci. USA. 87:1990;3513-3517.
53. Gottesman S., Clark W.P., de Crecy-Lagard V., Maurizi M.R. ClpX, an alternative subunit for the ATP-dependent Clp protease of Escherichia coli. J. Biol. Chem. 268:1993;22618-22626.
54. Gottesman S., Maurizi M.R., Wickner S. Regulatory subunits of energy-dependent proteases. Cell. 91:1997;435-438.
55. Gottesman S., Wickner S., Maurizi M.R. Protein quality control: triage by chaperones and protease. Genes Dev. 12:1997;1338-13347.
56. Gottesman S., Roche E., Zhou Y., Sauer R.T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev. 12:1998;1338-1347.
57. Guelin E., Rep M., Grivell L.A. Afg3p, a mitochondrial ATP-dependent metalloprotease, is involved in degradation of mitochondrially-encoded Cox1, Cox3, Cob, Su6, Su8 and Su9 subunits of the inner membrane complexes III, IV and V. FEBS Lett. 381:1996;42-46.
58. Harding A.E. Friedreich's ataxia: a clinical and genetic study of 90 families with an analysis of early diagnosis criteria and intrafamilial clustering of clinical features. Brain. 104:1981;589-620.
59. Hawlitschek G., Schneider H., Schmidt B., Tropschug M., Hartl F.U., Neupert W. Mitochondrial protein import: identification of processing peptidase and of PEP, a processing enhancing protein. Cell. 53:1988;795-806.
60. Hendrick J.P., Hodges P.E., Rosenberg L.E. Survey of amino-terminal proteolytic cleavage sites in mitochondrial precursor proteins: leader peptides cleaved by two matrix proteases share a three-amino acid motif. Proc. Natl. Acad. Sci. USA. 86:1989;4056-4060.
61. Hwang B.J., Park W.J., Chung C.H., Goldberg A.L. Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La. Proc. Natl. Acad. Sci. USA. 84:1987;5550-5554.
62. Hwang B.J., Woo K.M., Goldberg A.L., Chung C.H. Protease Ti, a new ATP-dependent protease in Escherichia coli, contains protein-activated ATP-ase and proteolytic functions in distinct subunits. J. Biol. Chem. 263:1988;8727-8734.
63. Isaya G., Kalousek F. Mitochondrial intermediate peptidase. Methods Enzymol. 248:1995;556-567.
64. Isaya G., Kalousek F., Fenton W.A., Rosenberg L.E. Cleavage of precursors by the mitochondrial processing peptidase requires a compatible mature protein or an intermediate octapeptide. J. Cell Biol. 113:1991;65-76.
65. Isaya G., Kalousek F., Rosenberg L.E. Amino-terminal octapeptides function as recognition signals for the mitochondrial intermediate peptidase. J. Biol. Chem. 267:1992;7904-7910.
66. Isaya G., Kalousek F., Rosenberg L.E. Sequence analysis of rat mitochondrial intermediate peptidase: similarity to zinc metallopeptidases and to a putative yeast homologue. Proc. Natl. Acad. Sci. USA. 89:1992;8317-8321.
67. Ishii A., Watabe S., Hamada H. ATP-dependent protease in human placenta. Placenta. 13:1992;343-347.
68. Ito A. Mitochondrial processing peptidase: multiple-site recognition of precursor protein. Biochem. Biophys. Res. Commun. 265:1999;611-616.
69. Juhola M.K., Shah Z.H., Grivell L.A., Jacobs H.T. The mitochondrial inner membrane AAA metalloprotease family in metazoans. FEBS Lett. 481:2000;91-95.
70. Kalnov S.L., Novikova L.A., Zubatov A.S., Luzikov V.N. Proteolysis of the products of mitochondrial protein synthesis in yeast mitochondria and submitochondrial particles. Biochem. J. 182:1979;195-202.
71. Kalnov S.L., Novikova L.A., Zubatov A.S., Luzikov V.N. Participation of a mitochondrial proteinase in the breakdown of mitochondrial translation products in yeast. FEBS Lett. 101:1979;355-357.
72. Kalousek F., Hendrick J.P., Rosenberg L.E. Two mitochondrial matrix proteases act sequentially in the processing of mammalian matrix enzymes. Proc. Natl. Acad. Sci. USA. 85:1988;7536-7540.
73. Kalousek F., Isaya G., Rosenberg L.E. Rat liver mitochondrial intermediate peptidase (MIP): purification and initial characterization. EMBO J. 11:1992;2803-2809.
74. Kalousek F., Neupert W., Omura T., Schatz G., Schmitz U.K. Uniform nomenclature for the mitochondrial proteases cleaving precursors of mitochondrial proteins. Trends Biochem. Sci. 18:1993;249.
75. Katayama-Fujimura Y., Gottesman S., Maurizi M.R. A multiple-component. ATP-dependent protease from Escherichia coli. J. Biol. Chem. 262:1987;4477-4485.
76. Katayama-Fujimura Y., Gottesman S., Pumphrey J., Rudikoff S., Clark W.P., Maurizi M.R. The two-component. ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J. Biol. Chem. 263:1988;15226-15236.
77. Katz M.L., Gao C.L., Tompkins J.A., Bronson R.T., Chin D.T. Mitochondrial ATP synthase subunit c stored in hereditary ceroid-lipofuscinosis contains trimethyl-lysine. Biochem. J. 310:1995;887-892.
78. Kessel M., Maurizi M.R., Kim B., et al. Homology in structural organization between E. coli ClpAP protease and the eukaryotic 26 S proteasome. J. Mol. Biol. 250:1995;587-594.
79. Kleiber J., Kalousek F., Swaroop M., Rosenberg L.E. The general mitochondrial matrix processing protease from rat liver: structural characterization of the catalytic subunit. Proc. Natl. Acad. Sci. USA. 87:1990;7978-7982.
80. Kominami E.K., Ezaki J., Muno D., Ishido K., Ueno T., Wolfe L.S. Specific storage of subunit c of mitochondrial ATP synthase in lysosomes of neuronal ceroid lipofuscinosis (Batten Disease). J. Biochem. 111:1992;278-282.
81. Koutnikova H., Campuzano V., Koenig M. Maturation of wild-type and mutant frataxin by the mitochondrial processing peptidase. Hum. Mol. Genet. 7:1998;1485-1489.
82. Langer T. AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem. Sci. 25:2000;247-251.
83. Lee C.K., Klopp R.G., Weindruch R., Prolla T.A. Gene expression profile of aging and its retardation by caloric restriction. Science. 285:1999;1390-1393.
84. 0-ATPase subunit accumulation in an oxa1 deletion mutant of Saccharomyces cerevisiae. J. Biol. Chem. 275:2000;23471-23475.
85. 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. 15:1996;4218-4229.
86. Leonhard K., Stiegler A., Neupert W., Langer T. Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Nature. 398:1999;348-351.
87. Leonhard K., Guiard B., Pellechia G., Tzagoloff A., Neupert W., Langer T. Membrane protein degradation by AAA proteases in mitochondria: extraction of substrate from either membrane surface. Mol. Cell. 5:2000;629-638.
88. Leube B., Rudnicki D., Ratzlaff T., Kessler K.R., Benecke R., Auburger G. Idiopathic torsion dystonia: assignment of a gene to chromosome 18p in a German family with adult onset, autosomal dominant inheritance and purely focal distribution. Hum. Mol. Genet. 5:1996;1673-1677.
89. Levchenko I., Yamauchi M., Baker T.A. ClpX and MuB interact with overlapping regions of Mu transposase: implications for control of the transposition pathway. Genes Dev. 11:1997;1561-1572.
90. Lipsky N.G., Pedersen P.L. Protein turnover in animal cells: half-lives of mitochondria and mitochondrial subfractions of liver based on [14C]bicarbonate incorporation. J. Biol. Chem. 256:1981;8652-8657.
91. Luciakova K., Sokolikova B., Chloupkova M., Nelson B.D. Enhanced mitochondrial biogenesis is associated with increased expression of the mitochondrial ATP-dependent Lon protease. FEBS Lett. 444:1999;186-188.
92. Luciano P., Geoffroy S., Brandt A., Hernandez J.F., Geli V. Functional cooperation of the mitochondrial processing peptidase subunits. J. Mol. Biol. 272:1997;213-225.
93. Luciano P., Tokatlidis K., Chambre I., Germanique J.C., Geli V. The mitochondrial processing peptidase behaves as a Zn-metallopeptidase. J. Mol. Biol. 280:1998;193-199.
94. Marcillat O., Zhang Y., Lin S.W., Davies K.J.A. Mitochondria contain a proteolytic system which can recognize and degrade oxidatively-denatured proteins. Biochem. J. 254:1988;677-683.
95. Marcillat O., Zhang Y., Davies K.J.A. Oxidative and nonoxidative mechanisms in the inactivation of cardiac mitochondrial electron transport chain components by doxorubicin. Biochem. J. 259:1989;181-189.
96. Maurizi M.R., Clark W.P., Katayama Y., et al. Sequence and structure of ClpP, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J. Biol. Chem. 265:1990;12536-12545.
97. Maurizi M.R., Clark W.P., Kim S.H., Gottesman S. ClpP represents a unique family of serine proteases. J. Biol. Chem. 265:1990;12546-12552.
98. Meinhardt A., Wilhelm B., Seitz J. Expression of mitochondrial marker proteins during spermiogenesis. Hum. Reprod. Update. 5:1999;108-119.
99. Mountjoy K.G., Robbins L.S., Mortrud M.T., Cone R.D. The cloning of a family of genes that encode the melacortin receptors. Science. 257:1992;1248-1251.
100. Nakabayashi K., Ito M., Kiyosue T., Shinozaki K., Watanabe A. Identification of clp genes expressed in senescing Arabidopsis leaves. Plant Cell Physiol. 40:1999;504-514.
101. Nakai T., Mera Y., Yasuhara T., Ohashi A. Divalent metal ion-dependent mitochondrial degradation of unassembled subunits 2 and 3 of cytochrome c oxidase. J. Biochem. 116:1994;752-757.
102. Nakai T., Yasuhara T., Fujiki Y., Ohashi A. Multiple genes, including a member of the AAA family, are essential for degradation of unassembled subunit 2 of cytochrome c oxidase in yeast mitochondria. Mol. Cell. Biol. 15:1995;4441-4452.
103. Nakashima K., Kiyosue T., Yamaguchi-Shinozaki K., Shinozaki K. A nuclear gene. erd1, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence in Arabidopsis thaliana. Plant J. 1997:1997;851-861.
104. Nuell M.J., Stewart D.A., Walker L., et al. Prohibitin, an evolutionary conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Mol. Cell. Biol. 11:1991;1372-1381.
105. Omura T. Mitochondria-targeting sequence, a multi-role sorting sequence recognized at all steps of protein import into mitochondria. J. Biochem. 123:1998;1010-1016.
106. Ou W.J., Ito A., Okazaki H., Omura T. Purification and characterization of a processing peptidase from rat liver mitochondria. EMBO J. 8:1989;2605-2612.
107. Ou W.J., Kumamoto T., Mihara K., et al. Structural requirement for recognition of the precursor proteins by the mitochondrial processing peptidase. J. Biol. Chem. 1994:1994;24673-24678.
108. Ozelius L.J., Kramer P.L., Moskowitz C.B., et al. Human gene for torsion dystonia located on chromosome 9q32-q34. Neuron. 2:1989;1427-1434.
109. Ozelius L.J., Page C.E., Klein C., et al. The TOR1A (DYT1) gene family and its role in early onset torsion dystonia. Genomics. 62:1999;377-384.
110. Paces V., Rosenberg L.E., Fenton W.A., Kalousek F. The b subunit of the mitochondrial processing peptidase from rat liver: cloning and sequencing of a cDNA and comparison with a proposed family of metallopeptidases. Proc. Natl. Acad. Sci. USA. 90:1993;5355-5358.
111. Pajic A., Tauer R., Feldmann H., Neupert W., Langer T. Yta10p is required for the ATP-dependent degradation of polypeptides in the inner membrane of mitochondria. FEBS Lett. 353:1994;201-206.
112. Pak M., Hoskins J.R., Singh S.K., Maurizi M.R., Wickner S. Concurrent chaperone and protease activities of ClpAP and the requirement for the N-terminal ClpA ATP binding site for chaperone activity. J. Biol. Chem. 274:1999;19316-19322.
113. Palmer D.N., Fearnley I.M., Walker J.E., et al. Mitochondrial ATP synthase subunit c storage in the ceroid-lipofuscinosis (Batten Disease). Am. J. Med. Genet. 45:1992;561-567.
114. Pearce D.A. Hereditary spastic paraplegia: mitochondrial metalloproteases of yeast. Hum. Genet. 104:1999;443-448.
115. Pfanner N., Neupert W. The mitochondrial protein import apparatus. Annu. Rev. Biochem. 59:1990;331-353.
116. Pfeifer U. Inhibition by insulin of the formation of autophagic vacuoles in rat liver. A morphometric approach to the kinetics of intracellular protein degradation by autophagy. J. Cell Biol. 78:1987;152-167.
117. Pratje E., Mannhaupt G., Michaelis G., Beyreuther K. A nuclear mutation prevents processing of a mitochondrially encoded membrane protein in Saccharomyces cerevisiae. EMBO J. 2:1983;1049-1054.
118. Priller J., Scherzer C.R., Faber P.W., MacDonald M.E., Young A.B. Frataxin gene of Friedreich's ataxia is targeted to mitochondria. Ann. Neurol. 42:1997;265-269.
119. Rapoport S., Dubiel W., Muller M. Characteristics of an ATP-dependent proteolytic system of rat liver mitochondria. FEBS Lett. 147:1982;93-96.
120. Rider J.A., Dawson G., Siakatos A.N. Perspectives of biochemical research in the neuronal ceroid-lipofuscinosis. Am. J. Med. Genet. 42:1992;519-524.
121. Rosenberg L.E., Fenton W.A., Horwich A.L., Kalousek F., Kraus J.P. Targeting of nuclear-encoded proteins to the mitochondrial matrix: implication for human genetic defects. Ann. N.Y. Acad. Sci. 488:1986;99-108.
122. Russel S.M., Burgess R.L., Mayer R.J. Protein degradation in rat liver during post-natal development. Biochem. J. 192:1980;321-330.
123. Russel S.M., Burgess R.L., Mayer R.J. Protein degradation in rat liver. Evidence for populations of protein degradation rates in cellular organelles. Biochim. Biophys. Acta. 714:1982;34-45.
124. Saavedra-Alanis V.M., Rysavy P., Rosenberg L.E., Kalousek F. Rat liver mitochondrial processing peptidase. Both a and b subunits are required for activity. J. Biol. Chem. 269:1994;9284-9288.
125. Santagata S., Bhattacharyya D., Wang F.H., Singha N., Hodtsev A., Spanopoulou E. Molecular cloning and characterization of a mouse homolog of bacterial ClpX, a novel mammalian class II member of the Hsp100/Clp chaperone family. J. Biol. Chem. 274:1999;16311-16319.
126. Savel'ev A.S., Novikova L.A., Kovaleva I.E., Luzikov V.N., Neupert W., Langer T. ATP-dependent proteolysis in mitochondria. m-AAA protease and PIM1 protease exert overlapping substrate specificities and cooperate with the mtHsp70 system. J. Biol. Chem. 273:1998;20596-20602.
127. Schirmer E.C., Glover J.R., Singer M.A., Lindquist S. HSP 100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem. Sci. 21:1996;289-296.
128. Schneider H., Arretz M., Wachter E., Neupert W. Matrix processing peptidase of mitochondria. Structure-function relationship. J. Biol. Chem. 265:1990;9881-9887.
129. Schneider A., Behrens M., Scherer P., Pratje E., Michaelis G., Schatz G. Inner membrane protease I, an enzyme mediating intramitochondrial protein sorting in yeast. EMBO J. 10:1991;247-254.
130. S) by ClpXP protease. J. Bacteriol. 178:1996;470-476.
131. Settasatian C., Whitmore S.A., Crawford J., et al. Genomic structure and expression analysis of the spastic paraplegia gene, SPG7. Hum. Genet. 105:1999;139-144.
132. Sevarino K.A., Poyton R.O. Mitochondrial membrane biogenesis: identification of a precursor to yeast cytochrome c oxidase subunit II, an integral polypeptide. Proc. Natl. Acad. Sci. USA. 77:1980;142-146.
133. Shah Z.H., Migliosi V., Miller S.C.M., Wang A., Friedman T.B., Jacobs H.T. Chromosomal locations of three human nuclear genes (RPSM12, TUFM, and AFG3L1) specifying putative components of the mitochondrial gene expression apparatus. Genomics. 48:1998;384-388.
134. Shah Z.H., Hakkaart G.A.J., Arku B., et al. The human homologue of the yeast mitochondrial AAA metalloprotease Yme1p complements a yeast yme1 disruptant. FEBS Lett. 478:2000;267-270.
135. Sitte N., Drung I., Dubiel W. Identification of a novel ATP-dependent proteolytic activity in mitochondrial intermembrane space. Biochem. Mol. Biol. Int. 36:1995;871-881.
136. Sitte N., Drung I., Kloetzel P.M. Evidence for a novel ATP-dependent protease from the rat liver mitochondrial intermembrane space: purification and characterisation. J. Biochem. 123:1998;408-415.
137. Song M.C., Shimokata K., Kitada S., Ogishima T., Ito A. Role of basic amino acids in the cleavage of synthetic peptide substrates by mitochondrial processing peptidase. J. Biochem. 120:1996;1163-1166.
138. Steglich G., Neupert W., Langer T. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol. Cell. Biol. 19:1999;3435-3442.
139. Suzuki C.K., Suda K., Schatz G. Requirement for the yeast gene Lon in intramitochondrial proteolysis and maintenance of respiration. Science. 264:1994;273-276.
140. Suzuki H., Komiya A., Emi M., et al. Three distinct commonly deleted regions of chromosome arm 16q in human primary and metastatic prostate cancers. Genes Chromosom. Cancer. 17:1996;225-233.
141. Takeshige K., Baba M., Tsuboi S., Noda T., Ohsumi Y. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for induction. J. Cell Biol. 119:1992;301-311.
142. Tanner A.J., Dice J.F. Batten disease and mitochondrial pathways of proteolysis. Biochem. Mol. Med. 57:1996;1-9.
143. 0-ATP synthase subunit 9 and other proteolipids in normal and Batten disease fibroblasts. Biochim. Biophys. Acta. 1361:1997;251-262.
144. Teichmann U., Van Dick L., Guiard B., et al. Substitution of PIM1 protease in mitochondria by Escherichia coli Lon protease. J. Biol. Chem. 271:1996;10137-10142.
145. Thompson M.W., Maurizi M.R. Activity and specificity of Escherichia coli ClpAP protease in cleaving model peptide substrates. J. Biol. Chem. 269:1994;18201-18208.
146. Thompson M.W., Singh S.K., Maurizi M.R. Processive degradation of proteins by the ATP-dependent Clp protease from Escherichia coli. Requirement for the multiple array of active sites in ClpP but not ATP hydrolysis. J. Biol. Chem. 269:1994;18209-18215.
147. Tomoyasu T., Yuki T., Mori H., et al. The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATP-ases involved in membrane functions, cell cycle control, and gene expression. J. Bacteriol. 175:1993;1344-1355.
148. Tsuda H., Callen D.F., Fukutomi T., Nakamura Y., Harohashi S. Allelic loss on chromosome 16q24.2-qter occurs frequently in breast cancers irrespectively of differences in phenotype and extent of spread. Cancer Res. 54:1994;513-517.
149. Van Dyck L., Langer T. ATP-dependent proteases controlling mitochondrial function in the yeast Saccharomyces cerevisiae. Cell. Mol. Life Sci. 56:1999;825-842.
150. Van Dyck L., Pearce D.A., Sherman F. PIM1 encodes a mitochondrial ATP-dependent protease that is required for mitochondrial function in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 269:1994;238-242.
151. Van Dyck L., Neupert W., Langer T. The ATP-dependent PIM 1 protease is required for the expression of intron-containing genes in mitochondria. Genes Dev. 12:1998;1515-1524.
152. Van Dyck L., Dembowski M., Neupert W., Langer T. Mcx1p, a ClpX homologue in mitochondria of Saccharomyces cerevisiae. FEBS Lett. 438:1998;250-254.
153. Walker J.H., Burgess R.J., Mayer R.J. Relative rate of turnover of subunits of mitochondrial proteins. Biochem. J. 176:1978;927-932.
154. Wang N., Gottesman S., Willingham M.C., Gottesman M.M., Maurizi M.R. A human mitochondrial ATP-dependent protease that is highly homologous to bacterial Lon protease. Proc. Natl. Acad. Sci. USA. 1993;11247-11251.
155. Wang N., Maurizi M.R., Buck L.E., Gottesman M.M. Synthesis, processing and localization of human Lon protease. J. Biol. Chem. 269:1994;29308-29313.
156. Wang J., Hartling J.A., Flanagan J.M. The structure of ClpP at 2.3 A resolution suggests a model for ATP-dependent proteolysis. Cell. 91:1997;447-456.
157. Wang J., Hartling J.A., Flanagan J.M. Crystal structure determination of Escherichia coli ClpP starting from an EM-derived mask. J. Struct. Biol. 124:1998;151-163.
158. Watabe S., Kimura T. ATP-dependent protease in bovine adrenal cortex. Tissue specificity, subcellular localization and partial characterization. J. Biol. Chem. 260:1985;5511-5517.
159. Watabe S., Kimura T. Adrenal cortex mitochondrial enzyme with ATP-dependent protease and protein-dependent activities. J. Biol. Chem. 260:1985;14498-14504.
160. Watabe S., Hara T., Kohno H., Hiroi T., Yago N., Nakazawa T. In vitro degradation of mitochondrial proteins by ATP-dependent protease in bovine adrenal cortex. J. Biochem. 113:1993;672-676.
161. Watabe S., Kohno H., Kouyama H., Hiroi T., Yago N., Nakazawa T. Purification and characterization of a substrate protein for mitochondrial ATP-dependent protease in bovine adrenal cortex. J. Biochem. 115:1994;648-654.
162. Watabe S., Hasegawa H., Takimoto K., Yamamoto Y., Takahashi S.Y. Possible function of SP-22, a substrate of mitochondrial ATP-dependent protease, as radical scavenger. Biochem. Biophys. Res, Commun. 213:1995;1010-1016.
163. Weissman J.S., Sigler P.B., Horwich A.L. From the cradle to the grave: ring complexes in the life of a protein. Science. 268:1995;523-524.
164. Wickner S., Gottesman S., Skowyra D., Hoskins J., McKenney K., Maurizi M.R. A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc. Natl. Acad. Sci. USA. 91:1994;12218-12222.
165. Wojtkowiak D., Georgopoulos C., Zylicz M. Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli. J. Biol. Chem. 268:1993;22609-22617.
166. Yang M., Jensen R.E., Yaffe M.P., Schatz G. Import of proteins into yeast mitochondria: the purified matrix processing protease contains two subunits which are encoded by the nuclear MAS1 and MAS2 genes. EMBO J. 7:1988;3857-3862.
167. Yang M., Geli V., Oppliger W., Suda K., James P., Schatz G. The MAS-encoded processing protease of yeast mitochondria. Interaction of the purified enzyme with signal peptides and a purified precursor protein. J. Biol. Chem. 266:1991;6416-6423.
168. Yasuhara T., Mera Y., Nakai T., Ohashi A. ATP-dependent proteolysis in yeast mitochondria. J. Biochem. 115:1994;1166-1171.
169. Zhang Y., Marcillat O., Giulivi C., Ernster L., Davies K.J.A. The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 265:1990;16330-16336.