Abstract
Cytochrome c reductase from potato is a bifunctional protein complex located in the inner mitochondrial membrane, which is involved in respiratory electron transport and processing of mitochondrial precursor proteins. The three largest subunits of the complex share the highest degree of sequence identity with the α- and β-subunits of the soluble processing peptidase (MPP) from fungi and mammals. Evidence is provided that another substoichiometric polypeptide of the cytochrome c reductase complex resembles the α-subunit of MPP. A cDNA clone corresponding to the second α-MPP protein (α-II MPP) encodes a polypeptide of 504 amino acids which is 84% identical to α-I MPP. The two different a-MPP polypeptides have similar sizes on SDS-polyacrylamide gels but can be distinguished with an antibody raised against a decapeptide that is specific for a-II MPP. The presequences of both α-subunits of MPP are proteolytically removed by the integrated processing enzyme complex indicating that it acts on the targeting signals of its own precursor proteins. Gene-specific oligonucleotides reveal that the genes encoding a-subunit I and α-subunit II of MPP are differentially expressed in all tissues analysed but the transcript levels do not vary between tissues.
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References
Amasino RM (1986) Acceleration of nucleic acid hybridization rate by polyethylene glycol. Anal Biochem 152:304–307
Bathgate B, Baker A, Leaver CJ (1989) Two genes encode the adenine nucleotide translocator of maize mitochondria. Eur J Biochem 183:303–310
Berry EA, Huang L, DeRose VJ (1991) Ubiquinol-cytochrome c oxidoreductase of higher plants. J Biol Chem 266:9064–9077
Braun HP, Schmitz UK (1992) Affinity purification of cytochrome c reductase from potato mitochondria. Eur J Biochem 208:761–767
Braun HP, Emmermann M, Kruft V, Schmitz UK (1992a) The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. EMBO J 11:3219–3227
Braun HP, Emmermann M, Kruft V, Schmitz UK (1992b) Cytochrome cl from potato: a protein with a presequence for targeting to the mitochondrial intermembrane space. Mol Gen Genet 231:217–225
Braun HP, Emmermann M, Mentzel H, Schmitz UK (1994) Primary structure and expression of a gene encoding the cytosolic ribosomal protein S4 from potato. Biochim Biophys Acta 1218:435–438
Chua NH, Schmidt GW (1979) Transport of proteins into mitochondria and chloroplasts. J Cell Biol 81:461–483
Dale RMK, McClure BA, Houchins JP (1985) A rapid singlestranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application for sequencing the corn mitochondrial 18S rDNA. Plasmid 13:31–40
Doolittle RF (1981) Similar amino acid sequences: chance or common ancestry? Science 214:149–159
Emmermann M, Schmitz UK (1993) The cytochrome c reductase integrated processing peptidase from potato mitochondria belongs to a new class of metalloendoproteases. Plant Physiol 103:615–620
Emmermann M, Braun HP, Schmitz UK (1991) The ADP/ATP translocator from potato has a long amino terminal extension. Curr Genet 20:405–410
Emmermann M, Braun HP, Schmitz UK (1993a) The two high molecular weight subunits of cytochrome c reductase from potato are immunologically related to the mitochondrial processing enhancing protein. Biochim Biophys Acta 1142:306–310
Emmermann M, Braun HP, Arretz M, Schmitz UK (1993b) Characterization of the bifunctional cytochrome c reductase/processing peptidase complex from potato mitochondria. J Biol Chem 268:18936–18942
Eriksson AC, Glaser E (1992) Mitochondrial processing peptidase: a general processing peptidase of spinach leaf mitochondria is a membrane-bound enzyme. Biochim Biophys Acta 1140:208–214
Eriksson A, Sjöling S, Glaser E (1993) A general processing proteinase of spinach leaf mitochondria is associated with the bc 1 complex of the respiratory chain. In: Brennicke A, Kück U (eds) Plant mitochondria. VCH Weinheim, New York, pp 299–306
Hawlitschek G, Schneider H, Schmidt B, Tropschug M, Hartl F-U, Neupert W (1988) Mitochondrial protein import: identification of processing peptidase and of PEP, a processing enhancing protein. Cell 53:795–806
Hurt EC, van Loon APGM (1986) How proteins find mitochondria and mitochondrial compartments. Trends Biochim Sci 11:204–207
Jensen RE, Yaffe MP (1988) Import of proteins into yeast mitochondria: the nuclear MAS2 gene encodes a component of the processing protease that is homologous to the MAS1-encoded subunit. EMBO J 7:3863–3871
Jones JDG, Dunsmuir P, Bedbrook J (1985) High level expression of introduced chimaeric genes in regenerated transformed plants. EMBO J 4:2411–2418
Kalousek F, Neupert W, Omura T, Schatz G, Schmitz UK (1993) Uniform nomenclature for the mitochondrial proteases cleaving precursors of mitochondrial proteins. Trends Biochem Sci 18:249
Kleiber J, Kalousek F, Swaroop M, Rosenberg LE (1990) The general mitochondrial rtlatrix processing protease from rat liver: structural characterization of the catalytic subunit. Proc Natl Acad Sci USA 87:7978–7982
Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Laz TM, Pietras DF, Sherman F (1984) Differential regulation of the duplicated isocytochrome c genes in yeast. Proc Natl Acad Sci USA 81:4475–4479
Lunardi J, Attardi G (1991) Differential regulation of expression of the multiple ADP/ATP translocase genes in human cells. J Biol Chem 266:16534–16540
Ou W-J, Ito A, Okazaki H, Omura T (1989) Purification and characterization of a processing protease from rat liver mitochondria. EMBO J 8:2605–2612
Proudfoot NJ, Brownlee GG (1976) 3′non-coding region sequences in eukaryotic messenger RNA. Nature 263:211–214
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74:5463–5470
Schneider H, Arretz M, Wachter E, Neupert W (1990) Matrix processing peptidase of mitochondria. J Biol Chem 265:9881–9887
Trueblood CE, Poyton RO (1987) Differential effectiveness of yeast cytochrome c oxidase subunit V genes results from differences in expression not function. Mol Cell Biol 7:3520–3526
Witte C, Jensen RE, Yaffe MP, Schatz G (1988) MAS1, a gene essential for yeast mitochondrial assembly, encodes a subunit of the mitochondrial processing protease. EMBO J 7:1439–1447
Yaffe MP, Schatz G (1984) Two nuclear mutations that block mitochondrial protein import in yeast. Proc Natl Acad Sci USA 81:4819–4823
Yang M, Jensen RE, Yaffe MP, Oppliger W, Schatz G (1988) 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 7:3857–3862
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Communicated by D. Lonsdale
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Emmermann, M., Braun, H.P. & Schmitz, U.K. The mitochondrial processing peptidase from potato: a self-processing enzyme encoded by two differentially expressed genes. Molec. Gen. Genet. 245, 237–245 (1994). https://doi.org/10.1007/BF00283272
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DOI: https://doi.org/10.1007/BF00283272