Abstract
A plant cysteine endopeptidase with a molecular mass of 35 kD was purified from microbodies of germinating castor bean (Ricinus communis) endosperm by virtue of its capacity to specifically process the glyoxysomal malate dehydrogenase precursor protein to the mature subunit in vitro. Processing of the glyoxysomal malate dehydrogenase precursor occurs sequentially in three steps, the first intermediate resulting from cleavage after arginine-13 within the presequence and the second from cleavage after arginine-33. The endopeptidase is unable to remove the presequences of prethiolases from rape (Brassica napus) glyoxysomes and rat peroxisomes at the expected cleavage site. Protein sequence analysis of N-terminal and internal peptides revealed high identity to the mature papain-type cysteine endopeptidases from cotyledons of germinating mung bean (Vigna mungo) and French bean (Phaseolus vulgaris) seeds. These endopeptidases are synthesized with an extended pre-/prosequence at the N terminus and have been considered to be processed in the endoplasmic reticulum and targeted to protein-storing vacuoles.
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- Akasofu H., Yamauchi D., Mitsuhashi W., Minamikawa T. Nucleotide sequence of cDNA for sulfhydryl-endopeptidase (SH-EP) from cotyledons of germinating Vigna mungo seeds. Nucleic Acids Res. 1989 Aug 25;17(16):6733–6733. doi: 10.1093/nar/17.16.6733. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BERNHARD W., ROUILLER C. Microbodies and the problem of mitochondrial regeneration in liver cells. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):355–360. doi: 10.1083/jcb.2.4.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bodnar A. G., Rachubinski R. A. Cloning and sequence determination of cDNA encoding a second rat liver peroxisomal 3-ketoacyl-CoA thiolase. Gene. 1990 Jul 16;91(2):193–199. doi: 10.1016/0378-1119(90)90088-9. [DOI] [PubMed] [Google Scholar]
- Cooper T. G., Beevers H. Mitochondria and glyoxysomes from castor bean endosperm. Enzyme constitutents and catalytic capacity. J Biol Chem. 1969 Jul 10;244(13):3507–3513. [PubMed] [Google Scholar]
- Faber K. N., Keizer-Gunnink I., Pluim D., Harder W., Ab G., Veenhuis M. The N-terminus of amine oxidase of Hansenula polymorpha contains a peroxisomal targeting signal. FEBS Lett. 1995 Jan 3;357(2):115–120. doi: 10.1016/0014-5793(94)01317-t. [DOI] [PubMed] [Google Scholar]
- Gietl C., Faber K. N., van der Klei I. J., Veenhuis M. Mutational analysis of the N-terminal topogenic signal of watermelon glyoxysomal malate dehydrogenase using the heterologous host Hansenula polymorpha. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3151–3155. doi: 10.1073/pnas.91.8.3151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gietl C. Glyoxysomal malate dehydrogenase from watermelon is synthesized with an amino-terminal transit peptide. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5773–5777. doi: 10.1073/pnas.87.15.5773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gietl C., Hock B. Organelle-bound malate dehydrogenase isoenzymes are synthesized as higher molecular weight precursors. Plant Physiol. 1982 Aug;70(2):483–487. doi: 10.1104/pp.70.2.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gietl C. Malate dehydrogenase isoenzymes: cellular locations and role in the flow of metabolites between the cytoplasm and cell organelles. Biochim Biophys Acta. 1992 Jun 19;1100(3):217–234. doi: 10.1016/0167-4838(92)90476-t. [DOI] [PubMed] [Google Scholar]
- Glover J. R., Andrews D. W., Subramani S., Rachubinski R. A. Mutagenesis of the amino targeting signal of Saccharomyces cerevisiae 3-ketoacyl-CoA thiolase reveals conserved amino acids required for import into peroxisomes in vivo. J Biol Chem. 1994 Mar 11;269(10):7558–7563. [PubMed] [Google Scholar]
- Guex N., Henry H., Flach J., Richter H., Widmer F. Glyoxysomal malate dehydrogenase and malate synthase from soybean cotyledons (Glycine max L.): enzyme association, antibody production and cDNA cloning. Planta. 1995;197(2):369–375. doi: 10.1007/BF00202659. [DOI] [PubMed] [Google Scholar]
- Hijikata M., Ishii N., Kagamiyama H., Osumi T., Hashimoto T. Structural analysis of cDNA for rat peroxisomal 3-ketoacyl-CoA thiolase. J Biol Chem. 1987 Jun 15;262(17):8151–8158. [PubMed] [Google Scholar]
- 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. 1991 Apr;113(1):65–76. doi: 10.1083/jcb.113.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mitsuhashi W., Minamikawa T. Synthesis and Posttranslational Activation of Sulfhydryl-Endopeptidase in Cotyledons of Germinating Vigna mungo Seeds. Plant Physiol. 1989 Jan;89(1):274–279. doi: 10.1104/pp.89.1.274. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Okamoto T., Nakayama H., Seta K., Isobe T., Minamikawa T. Posttranslational processing of a carboxy-terminal propeptide containing a KDEL sequence of plant vacuolar cysteine endopeptidase (SH-EP) FEBS Lett. 1994 Aug 29;351(1):31–34. doi: 10.1016/0014-5793(94)00809-4. [DOI] [PubMed] [Google Scholar]
- Osumi T., Tsukamoto T., Hata S., Yokota S., Miura S., Fujiki Y., Hijikata M., Miyazawa S., Hashimoto T. Amino-terminal presequence of the precursor of peroxisomal 3-ketoacyl-CoA thiolase is a cleavable signal peptide for peroxisomal targeting. Biochem Biophys Res Commun. 1991 Dec 31;181(3):947–954. doi: 10.1016/0006-291x(91)92028-i. [DOI] [PubMed] [Google Scholar]
- Preisig-Müller R., Kindl H. Thiolase mRNA translated in vitro yields a peptide with a putative N-terminal presequence. Plant Mol Biol. 1993 Apr;22(1):59–66. doi: 10.1007/BF00038995. [DOI] [PubMed] [Google Scholar]
- Sautter C., Hock B. Fluorescence immunohistochemical localization of malate dehydrogenase isoenzymes in watermelon cotyledons : a developmental study of glyoxysomes and mitochondria. Plant Physiol. 1982 Oct;70(4):1162–1168. doi: 10.1104/pp.70.4.1162. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh K. K., Small G. M., Lewin A. S. Alternative topogenic signals in peroxisomal citrate synthase of Saccharomyces cerevisiae. Mol Cell Biol. 1992 Dec;12(12):5593–5599. doi: 10.1128/mcb.12.12.5593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steffan J. S., McAlister-Henn L. Isolation and characterization of the yeast gene encoding the MDH3 isozyme of malate dehydrogenase. J Biol Chem. 1992 Dec 5;267(34):24708–24715. [PubMed] [Google Scholar]
- Subramani S. Protein import into peroxisomes and biogenesis of the organelle. Annu Rev Cell Biol. 1993;9:445–478. doi: 10.1146/annurev.cb.09.110193.002305. [DOI] [PubMed] [Google Scholar]
- Swinkels B. W., Gould S. J., Bodnar A. G., Rachubinski R. A., Subramani S. A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase. EMBO J. 1991 Nov;10(11):3255–3262. doi: 10.1002/j.1460-2075.1991.tb04889.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tanaka T., Yamauchi D., Minamikawa T. Nucleotide sequence of cDNA for an endopeptidase (EP-C1) from pods of maturing Phaseolus vulgaris fruits. Plant Mol Biol. 1991 Jun;16(6):1083–1084. doi: 10.1007/BF00016081. [DOI] [PubMed] [Google Scholar]
- Trelease R. N., Choe S. M., Jacobs B. L. Conservative amino acid substitutions of the C-terminal tripeptide (Ala-Arg-Met) on cottonseed isocitrate lyase preserve import in vivo into mammalian cell peroxisomes. Eur J Cell Biol. 1994 Dec;65(2):269–279. [PubMed] [Google Scholar]
- Tsukamoto T., Hata S., Yokota S., Miura S., Fujiki Y., Hijikata M., Miyazawa S., Hashimoto T., Osumi T. Characterization of the signal peptide at the amino terminus of the rat peroxisomal 3-ketoacyl-CoA thiolase precursor. J Biol Chem. 1994 Feb 25;269(8):6001–6010. [PubMed] [Google Scholar]
- Valpuesta V., Lange N. E., Guerrero C., Reid M. S. Up-regulation of a cysteine protease accompanies the ethylene-insensitive senescence of daylily (Hemerocallis) flowers. Plant Mol Biol. 1995 Jun;28(3):575–582. doi: 10.1007/BF00020403. [DOI] [PubMed] [Google Scholar]
- Zhang J. W., Lazarow P. B. PEB1 (PAS7) in Saccharomyces cerevisiae encodes a hydrophilic, intra-peroxisomal protein that is a member of the WD repeat family and is essential for the import of thiolase into peroxisomes. J Cell Biol. 1995 Apr;129(1):65–80. doi: 10.1083/jcb.129.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Hoop M. J., Ab G. Import of proteins into peroxisomes and other microbodies. Biochem J. 1992 Sep 15;286(Pt 3):657–669. doi: 10.1042/bj2860657. [DOI] [PMC free article] [PubMed] [Google Scholar]