Abstract
Extensive perexisome proliferation during growth on oleic acid, combined with the availability of excellent genetic tools, makes the dimorphic yeast, Yarrowia lipolytica, a powerful model system to study the molecular mechanisms involved in peroxisome biogenesis. A combined genetic, biochemical, and morphological approach has revealed that the endoplasmic reticulum (ER) plays an essential role in the assembly of functional peroxisomes in this yeast. The trafficking of some membrane proteins to the peroxisomes occurs via the ER, results in their glyco-sylation in the ER lumen, does not involve transit through the Golgi, and requires the products of the SEC238, SRP54, PEX1, and PEX6 genes. The authors' data suggest a model for protein import into peroxisomes via two subpopulations of ER-derived vesicles that are distinct from secretory vesicles. A kinetic analysis of the trafficking of peroxisomal proteins in vivo has demonstrated that membrane and matrix proteins are initially targeted to multiple vesicular precursors that represent intermediates in the assembly pathway of peroxisomes. The authors have also recently identified a novel cytosolic chaperone, Pex20p, that assists in the oligomerization of thiolase in the cytosol and promotes its targeting to the peroxisome. These data provide the first evidence that a chaperone-assisted folding and oligomerization of thiolase in the cytosol is required for the import of this protein into the peroxisomal matrix.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Lazarow, P. B. and Fujiki, Y. (1985) Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1, 489–530.
Subramani, S. (1993) Protein import into peroxisomes and biogenesis of the organelle. Annu. Rev. Cell Biol. 9, 445–478.
Van den Bosch, H., Schutgens, R. B. H., Wanders, R. J. A., and Tager, J. M. (1992) Biochemistry of peroxisomes. Annu. Rev. Biochem. 61, 157–197.
Subramani, S. 1998. Components involved in peroxisome import, biogenesis, proliferation, turnover, and movement. Pharmacol. Rev. 78, 171–188.
Novikoff, A. B. and Shin, W.-Y. (1964) The endoplasmic reticulum in the Golgi zone and its relations to microbodies, Golgi apparatus and autophagic vacuoles in rat liver cells. J. Microsc. 3, 187–206.
Higashi, T. and Peters, T., Jr. (1963) Studies on rat liver catalase. II. Incorporation of C14-leucine into catalase of liver cell fractions in vivo. J. Biol. Chem. 238, 3952–3954.
Titorenko, V. I., Ogrydziak, D. M., and Rachubinski, R. A. (1997) Four distinct secretory pathways serve protein secretion, ceil surface growth, and peroxisome biogenesis in the yeast Yarrowia lipolytica. Mol. Cell. Biol. 17, 5210–5226.
Titorenko, V. I. and Rachubinski, R. A. (1998a) Mutants of the yeast Yarrowia lipolytica defective in protein exit from the endoplasmic reticulum are also defective in peroxisome biogenesis. Mol. Cell. Biol. 18, 2789–2803.
Titorenko, V. I. and Rachubinski, R. A. (1998b) The endoplasmic reticulum plays an essential role in peroxisome biogenesis. Trends Biochem. Sci. 23, 231–233.
Fahimi, H. D., Baumgart, E., and Völkl, A. (1993) Ultrastructural aspects of biogenesis of peroxisomes in rat liver. Biochimie 75, 201–208.
Titorenko, V. I., Eitzen, G. A., and Rachubinski, R. A. (1996) Mutations in the PAY5 gene of the yeast Yarrowia lipolytica cause accumulation of multiple subpopulations of peroxisomes. J. Biol. Chem. 271, 20,307–20,314.
Passreiter, M., Anton, M., Lay, D., Frank, R., Harter, C., Wieland, F. T., Gorgas, K., and Just, W. W. (1998) Peroxisome biogenesis: involvement of ARF and coatomer. J. Cell Biol. 141, 373–383.
Titorenko, V. I., Smith, J. J., Szilard, R. K., and Rachubinski, R. A. (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.
McNew, J. A. and Goodman, J. M. (1996) The targeting and assembly of peroxisomal proteins: some old rules do not apply. Trends Biochem. Sci. 21, 54–58.
Schatz, G. and Dobberstein, B. (1996) Common principles of protein translocation across membranes. Science 271, 1519–1526.
Glover, J. R., Andrews, D. W., and Rachubinski, R. A. (1994) Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc. Natl. Acad. Sci. USA 91, 10,541–10,545.
McNew, J. A. and Goodman, J. M. (1994) An oligomeric protein is imported into peroxisomes in vivo. J. Cell Biol. 127, 1245–1257.
Walton, P. A., Hill, P. E., and Subramani, S. (1995) Import of stably folded proteins into peroxisomes. Mol. Biol. Cell 6, 675–683.
Elgersma, Y., Vos, A., van den Berg, M., van Roermund, C. W., van der Sluijs, P., Distel, B., and Tabak, H. F. (1996) Analysis of the carboxyl-terminal peroxisomal targeting signal 1 in a homologous context in Saccharomyces cerevisiae. J. Biol. Chem. 271, 26,375–26,382.
Häusler, T., Stierhof, Y., Wirtz, E., and Clayton, C. (1996) Import of DHFR hybrid protein into glycosomes in vivo is not inhibited by the folate-analogue aminopterin. J. Cell Biol. 132, 311–324.
Leiper, J. M., Oatey, P. B., and Danpure, C. J. (1996) Inhibition of alanine: glyoxylate amino-transferase 1 dimerization is a prerequisite for its peroxisome-to-mitochondrion mistargeting in primary hyperoxaluria type 1. J. Cell Biol. 135, 939–951.
Lee, M. S., Mullen, R. T., and Trelease, R. N. (1997) Oilseed isocitrate lyases lacking their essential type I peroxisomal targeting signal are piggybacked to glyoxysomes. Plant Cell 9, 185–197.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Titorenko, V.I., Smith, J.J., Szilard, R.K. et al. Peroxisome biogenesis in the yeast Yarrowia lipolytica . Cell Biochem Biophys 32, 21–26 (2000). https://doi.org/10.1385/CBB:32:1-3:21
Published:
Issue Date:
DOI: https://doi.org/10.1385/CBB:32:1-3:21