Titorenko, Vladimir I. ORCID: https://orcid.org/0000-0001-5819-7545, Nicaud, Jean-Marc, Wang, Huijie, Chan, Honey and Rachubinski, Richard A. (2002) Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. The Journal of Cell Biology, 156 (3). pp. 481-494. ISSN 00219525
Preview |
Text (application/pdf)
723kBTitorenko_JCB2002.pdf - Published Version |
Official URL: http://dx.doi.org/10.1083/jcb.200111075
Abstract
Five isoforms of acyl-CoA oxidase (Aox), designated Aox1p to Aox5p, constitute a 443-kD heteropentameric complex containing one polypeptide chain of each isoform within the peroxisomal matrix of the yeast Yarrowia lipolytica. Assembly of the Aox complex occurs in the cytosol and precedes its import into peroxisomes. Peroxisomal targeting of the Aox complex is abolished in a mutant lacking the peroxin Pex5p, a component of the matrix protein targeting machinery. Import of the Aox complex into peroxisomes does not involve the cytosolic chaperone Pex20p, which mediates the oligomerization and import of peroxisomal thiolase. Aox2p and Aox3p play a pivotal role in the formation of the Aox complex in the cytosol and can substitute for one another in promoting assembly of the complex. In vitro, these subunits retard disassembly of the Aox complex and increase the efficiency of its reassembly. Neither Aox2p nor Aox3p is required for acquisition of the cofactor FAD by other components of the complex. We provide evidence that the Aox2p- and Aox3p-assisted assembly of the Aox complex in the cytosol is mandatory for its import into peroxisomes and that no component of the complex can penetrate the peroxisomal matrix as a monomer.
Divisions: | Concordia University > Faculty of Arts and Science > Biology |
---|---|
Item Type: | Article |
Refereed: | Yes |
Authors: | Titorenko, Vladimir I. and Nicaud, Jean-Marc and Wang, Huijie and Chan, Honey and Rachubinski, Richard A. |
Journal or Publication: | The Journal of Cell Biology |
Date: | 28 January 2002 |
Digital Object Identifier (DOI): | 10.1083/jcb.200111075 |
ID Code: | 7566 |
Deposited By: | Danielle Dennie |
Deposited On: | 11 May 2011 16:54 |
Last Modified: | 28 May 2019 19:02 |
References:
Barth, G., and T. Scheuber. 1993. Cloning of the isocitrate lyase gene (ICL) from Yarrowia lipolytica and characterization of the deduced protein. Mol. Gen. Genet. 241:422–430.Dalbey, R.E., and C. Robinson. 1999. Protein translocation into and across the bacterial plasma membrane and the plant thylakoid membrane. Trends Biochem. Sci. 24:17–22.
Dansen, T.B., K.W.A. Wirtz, R.J.A. Wanders, and E.H.W. Pap. 2000. Peroxisomes in human fibroblasts have a basic pH. Nat. Cell Biol. 2:51–53.
Eitzen, G.A., R.K. Szilard, and R.A. Rachubinski. 1997. Enlarged peroxisomes are present in oleic acid-grown Yarrowia lipolytica overexpressing the PEX16 gene encoding an intraperoxisomal peripheral membrane peroxin. J. Cell Biol. 137:1265–1278.
Elgersma, Y., A. Vos, M. van den Berg, C.W. van Roermund, P. van der Sluijs, B. Distel, and H.F. Tabak. 1996. Analysis of the carboxyl-terminal peroxisomal targeting signal 1 in a homologous context in Saccharomyces cerevisiae. J. Biol. Chem. 271:26375–26382.
Glover, J.R., D.W. Andrews, and R.A. Rachubinski. 1994. Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc. Natl. Acad. Sci. USA. 91:10541–10545.
Häusler, T., Y. Stierhof, E. Wirtz, and C. Clayton. 1996. Import of DHFR hybrid protein into glycosomes in vivo is not inhibited by the folate-analogue aminopterin. J. Cell Biol. 132:311–324.
Kim, J., S.V. Scott, M.N. Oda, and D.J. Klionsky. 1997. Transport of a large oligomeric protein by the cytoplasm to vacuole targeting pathway. J. Cell Biol. 137:609–618.
Klionsky, D.J., and Y. Ohsumi. 1999. Vacuolar import of proteins and organelles from the cytoplasm. Annu. Rev. Cell Dev. Biol. 15:1–32.
Lee, M.S., R.T. Mullen, and R.N. Trelease. 1997. Oilseed isocitrate lyases lacking their essential type I peroxisomal targeting signal are piggybacked to glyoxysomes. Plant Cell. 9:185–197.
Leiper, J.M., P.B. Oatey, and C.J. Danpure. 1996. Inhibition of alanine:glyoxylate aminotransferase 1 dimerization is a prerequisite for its peroxisome-to-mitochondrion mistargeting in primary hyperoxaluria type 1. J. Cell Biol. 135:939–951.
Mannaerts, G.P., and P.P. van Veldhoven. 1996. Functions and organization of peroxisomal β-oxidation. Ann. NY Acad. Sci. 804:99–115.
McNew, J.A., and J.M. Goodman. 1994. An oligomeric protein is imported into peroxisomes in vivo. J. Cell Biol. 127:1245–1257.
McNew, J.A., and J.M. Goodman. 1996. The targeting and assembly of peroxisomal proteins: some old rules do not apply. Trends Biochem. Sci. 21:54–58.
Neuvéglise, C., J.M. Nicaud, P. Ross-Macdonald, and C. Gaillardin. 1998. A shuttle mutagenesis system for tagging genes in the yeast Yarrowia lipolytica. Gene. 213:37–46.
Rodrigue, A., A. Chanal, K. Beck, M. Müller, and L.-F. Wu. 1999. Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial Tat pathway. J. Biol. Chem. 274:13223–13228.
Santini, C.-L., B. Ize, A. Chanal, M. Müller, G. Giordano, and L.-F. Wu. 1998. A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17:101–112.
Schatz, G., and B. Dobberstein. 1996. Common principles of protein translocation across membranes. Science. 271:1519–1526.Abstract↵ Subramani, S. 1998. Components involved in peroxisome import, biogenesis, proliferation, turnover, and movement. Physiol. Rev. 78:171–188.
Stewart, M.Q., R.D. Esposito, J. Gowani, and J.M. Goodman. 2001. Alcohol oxidase and dihydroxyacetone synthase, the abundant peroxisomal proteins of methylotrophic yeasts, assemble in different cellular compartments. J. Cell Sci. 114:2863–2868.
Szilard, R.K., V.I. Titorenko, M. Veenhuis, and R.A. Rachubinski. 1995. Pay32p of the yeast Yarrowia lipolytica is an intraperoxisomal component of the matrix protein translocation machinery. J. Cell Biol. 131:1453–1469.
Teter, S.A., and D.J. Klionsky. 1999. How to get a folded protein across a membrane. Trends Cell Biol. 9:428–431.
Teter, S.A., and S.M. Theg. 1998. Energy-transducing thylakoid membranes remain highly impermeable to ions during protein translocation. Proc. Natl. Acad. Sci. USA. 95:1590–1594.
Titorenko, V.I., J.J. Smith, R.K. Szilard, and R.A. Rachubinski. 1998. Pex20p of the yeast Yarrowia lipolytica is required for the oligomerization of thiolase in the cytosol and for its targeting to the peroxisome. J. Cell Biol. 142:403–420.
Titorenko, V.I., H. Chan, and R.A. Rachubinski. 2000. Fusion of small peroxisomal vesicles in vitro reconstructs an early step in the in vivo multistep peroxisome assembly pathway of Yarrowia lipolytica. J. Cell Biol. 148:29–43.
Titorenko, V.I., and R.A. Rachubinski. 2001. The life cycle of the peroxisome. Nat. Rev. Mol. Cell Biol. 2:357–368.
van den Bosch, H., R.B.H. Schutgens, R.J.A. Wanders, and J.M. Tager. 1992. Biochemistry of peroxisomes. Annu. Rev. Biochem. 61:157–197.
Walton, P.A., P.E. Hill, and S. Subramani. 1995. Import of stably folded proteins into peroxisomes. Mol. Biol. Cell. 6:675–683.
Wang, H.J., M.-T. Le Dall, Y. Waché, C. Laroche, J.-M. Belin, C. Gaillardin, and J.-M. Nicaud. 1999a. Evaluation of acyl coenzyme A oxidase (Aox) isozyme function in the n-alkane-assimilating yeast Yarrowia lipolytica. J. Bacteriol. 181:5140–5148.
Wang, H.J., M.-T. Le Dall, Y. Waché, C. Laroche, J.-M. Belin, and J.-M. Nicaud. 1999b. Cloning, sequencing, and characterization of five genes coding for acyl-CoA oxidase isozymes of the yeast Yarrowia lipolytica. Cell Biochem. Biophys. 31:165–174.
Waterham, H.R., K.A. Russell, Y. de Vries, and J.M. Cregg. 1997. Peroxisomal targeting, import, and assembly of alcohol oxidase in Pichia pastoris. J. Cell Biol. 139:1419–1431.
Repository Staff Only: item control page