This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Titorenko, V. I.
Right arrow Articles by Rachubinski, R. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Titorenko, V. I.
Right arrow Articles by Rachubinski, R. A.

 Previous Article  |  Next Article 

Mol Cell Biol, May 1998, p. 2789-2803, Vol. 18, No. 5
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Mutants of the Yeast Yarrowia lipolytica Defective in Protein Exit from the Endoplasmic Reticulum Are Also Defective in Peroxisome Biogenesis

Vladimir I. Titorenko and Richard A. Rachubinski*

Department of Cell Biology and Anatomy, University of Alberta, Edmonton, Alberta T6G 2H7, Canada

Received 23 September 1997/Returned for modification 21 November 1997/Accepted 26 February 1998

Mutations in the SEC238 and SRP54 genes of the yeast Yarrowia lipolytica not only cause temperature-sensitive defects in the exit of the precursor form of alkaline extracellular protease and of other secretory proteins from the endoplasmic reticulum and in protein secretion but also lead to temperature-sensitive growth in oleic acid-containing medium, the metabolism of which requires the assembly of functionally intact peroxisomes. The sec238A and srp54KO mutations at the restrictive temperature significantly reduce the size and number of peroxisomes, affect the import of peroxisomal matrix and membrane proteins into the organelle, and significantly delay, but do not prevent, the exit of two peroxisomal membrane proteins, Pex2p and Pex16p, from the endoplasmic reticulum en route to the peroxisomal membrane. Mutations in the PEX1 and PEX6 genes, which encode members of the AAA family of N-ethylmaleimide-sensitive fusion protein-like ATPases, not only affect the exit of precursor forms of secretory proteins from the endoplasmic reticulum but also prevent the exit of the peroxisomal membrane proteins Pex2p and Pex16p from the endoplasmic reticulum and cause the accumulation of an extensive network of endoplasmic reticulum membranes. None of the peroxisomal matrix proteins tested associated with the endoplasmic reticulum in sec238A, srp54KO, pex1-1, and pex6KO mutant cells. Our data provide evidence that the endoplasmic reticulum is required for peroxisome biogenesis and suggest that in Y. lipolytica, the trafficking of some membrane proteins, but not matrix proteins, to the peroxisome occurs via the endoplasmic reticulum, results in their glycosylation within the lumen of the endoplasmic reticulum, does not involve transport through the Golgi, and requires the products encoded by the SEC238, SRP54, PEX1, and PEX6 genes.

* Corresponding author. Mailing address: Department of Cell Biology and Anatomy, University of Alberta, Medical Sciences Building 5-14, Edmonton, Alberta T6G 2H7, Canada. Phone: (403) 492-9868. Fax: (403) 492-9278. E-mail: rrachubi{at}anat.med.ualberta.ca.

Mol Cell Biol, May 1998, p. 2789-2803, Vol. 18, No. 5
0270-7306/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Chang, J., Mast, F. D., Fagarasanu, A., Rachubinski, D. A., Eitzen, G. A., Dacks, J. B., Rachubinski, R. A. (2009). Pex3 peroxisome biogenesis proteins function in peroxisome inheritance as class V myosin receptors. JCB 187: 233-246 [Abstract] [Full Text]  
  • Perry, R. J., Mast, F. D., Rachubinski, R. A. (2009). Endoplasmic Reticulum-Associated Secretory Proteins Sec20p, Sec39p, and Dsl1p Are Involved in Peroxisome Biogenesis. Eukaryot Cell 8: 830-843 [Abstract] [Full Text]  
  • Matsuzaki, T., Fujiki, Y. (2008). The peroxisomal membrane protein import receptor Pex3p is directly transported to peroxisomes by a novel Pex19p- and Pex16p-dependent pathway. JCB 183: 1275-1286 [Abstract] [Full Text]  
  • Yan, M., Rachubinski, D. A., Joshi, S., Rachubinski, R. A., Subramani, S. (2008). Dysferlin Domain-containing Proteins, Pex30p and Pex31p, Localized to Two Compartments, Control the Number and Size of Oleate-induced Peroxisomes in Pichia pastoris. Mol. Biol. Cell 19: 885-898 [Abstract] [Full Text]  
  • Karnik, S. K., Trelease, R. N. (2007). Arabidopsis peroxin 16 trafficks through the ER and an intermediate compartment to pre-existing peroxisomes via overlapping molecular targeting signals. J Exp Bot 58: 1677-1693 [Abstract] [Full Text]  
  • Pinto, M. P., Grou, C. P., Alencastre, I. S., Oliveira, M. E., Sa-Miranda, C., Fransen, M., Azevedo, J. E. (2006). The Import Competence of a Peroxisomal Membrane Protein Is Determined by Pex19p before the Docking Step. J. Biol. Chem. 281: 34492-34502 [Abstract] [Full Text]  
  • Titorenko, V. I., Mullen, R. T. (2006). Peroxisome biogenesis: the peroxisomal endomembrane system and the role of the ER. JCB 174: 11-17 [Abstract] [Full Text]  
  • Vizeacoumar, F. J., Vreden, W. N., Aitchison, J. D., Rachubinski, R. A. (2006). Pex19p Binds Pex30p and Pex32p at Regions Required for Their Peroxisomal Localization but Separate from Their Peroxisomal Targeting Signals. J. Biol. Chem. 281: 14805-14812 [Abstract] [Full Text]  
  • Navarro, B., Russo, M., Pantaleo, V., Rubino, L. (2006). Cytological analysis of Saccharomyces cerevisiae cells supporting cymbidium ringspot virus defective interfering RNA replication.. J. Gen. Virol. 87: 705-714 [Abstract] [Full Text]  
  • Kragt, A., Voorn-Brouwer, T., van den Berg, M., Distel, B. (2005). Endoplasmic Reticulum-directed Pex3p Routes to Peroxisomes and Restores Peroxisome Formation in a Saccharomyces cerevisiae pex3{Delta} Strain. J. Biol. Chem. 280: 34350-34357 [Abstract] [Full Text]  
  • Sparkes, I. A., Hawes, C., Baker, A. (2005). AtPEX2 and AtPEX10 Are Targeted to Peroxisomes Independently of Known Endoplasmic Reticulum Trafficking Routes. Plant Physiol. 139: 690-700 [Abstract] [Full Text]  
  • Karnik, S. K., Trelease, R. N. (2005). Arabidopsis Peroxin 16 Coexists at Steady State in Peroxisomes and Endoplasmic Reticulum. Plant Physiol. 138: 1967-1981 [Abstract] [Full Text]  
  • Wang, X., McMahon, M. A., Shelton, S. N., Nampaisansuk, M., Ballard, J. L., Goodman, J. M. (2004). Multiple Targeting Modules on Peroxisomal Proteins Are Not Redundant: Discrete Functions of Targeting Signals within Pmp47 and Pex8p. Mol. Biol. Cell 15: 1702-1710 [Abstract] [Full Text]  
  • Titorenko, V. I., Rachubinski, R. A. (2004). The peroxisome: orchestrating important developmental decisions from inside the cell. JCB 164: 641-645 [Abstract] [Full Text]  
  • Zolman, B. K., Bartel, B. (2004). An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. Proc. Natl. Acad. Sci. USA 101: 1786-1791 [Abstract] [Full Text]  
  • Murphy, M. A., Phillipson, B. A., Baker, A., Mullen, R. T. (2003). Characterization of the Targeting Signal of the Arabidopsis 22-kD Integral Peroxisomal Membrane Protein. Plant Physiol. 133: 813-828 [Abstract] [Full Text]  
  • Schumann, U., Wanner, G., Veenhuis, M., Schmid, M., Gietl, C. (2003). AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proc. Natl. Acad. Sci. USA 100: 9626-9631 [Abstract] [Full Text]  
  • Bascom, R. A., Chan, H., Rachubinski, R. A. (2003). Peroxisome Biogenesis Occurs in an Unsynchronized Manner in Close Association with the Endoplasmic Reticulum in Temperature-sensitive Yarrowia lipolytica Pex3p Mutants. Mol. Biol. Cell 14: 939-957 [Abstract] [Full Text]  
  • Petriv, O. I., Pilgrim, D. B., Rachubinski, R. A., Titorenko, V. I. (2002). RNA interference of peroxisome-related genes in C. elegans: a new model for human peroxisomal disorders. Physiol. Genomics 10: 79-91 [Abstract] [Full Text]  
  • Kimura, A., Takano, Y., Furusawa, I., Okuno, T. (2001). Peroxisomal Metabolic Function Is Required for Appressorium-Mediated Plant Infection by Colletotrichum lagenarium. Plant Cell 13: 1945-1957 [Abstract] [Full Text]  
  • Voorn-Brouwer, T., Kragt, A., Tabak, H. F., Distel, B. (2001). Peroxisomal membrane proteins are properly targeted to peroxisomes in the absence of COPI- and COPII-mediated vesicular transport. J. Cell Sci. 114: 2199-2204 [Abstract] [Full Text]  
  • Titorenko, V. I., Rachubinski, R. A. (2000). Peroxisomal Membrane Fusion Requires Two Aaa Family Atpases, Pex1p and Pex6p. JCB 150: 881-886 [Abstract] [Full Text]  
  • South, S. T., Sacksteder, K. A., Li, X., Liu, Y., Gould, S. J. (2000). Inhibitors of Copi and Copii Do Not Block PEX3-Mediated Peroxisome Synthesis. JCB 149: 1345-1360 [Abstract] [Full Text]  
  • Titorenko, V. I., Chan, H., Rachubinski, R. A. (2000). Fusion of Small Peroxisomal Vesicles in Vitro Reconstructs an Early Step in the in Vivo Multistep Peroxisome Assembly Pathway of Yarrowia lipolytica. JCB 148: 29-44 [Abstract] [Full Text]  
  • Brown, T. W., Titorenko, V. I., Rachubinski, R. A. (2000). Mutants of the Yarrowia lipolytica PEX23 Gene Encoding an Integral Peroxisomal Membrane Peroxin Mislocalize Matrix Proteins and Accumulate Vesicles Containing Peroxisomal Matrix and Membrane Proteins. Mol. Biol. Cell 11: 141-152 [Abstract] [Full Text]  
  • Chang, C.-C., Warren, D. S., Sacksteder, K. A., Gould, S. J. (1999). Pex12 Interacts with Pex5 and Pex10 and Acts Downstream of Receptor Docking in Peroxisomal Matrix Protein Import. JCB 147: 761-774 [Abstract] [Full Text]  
  • Mullen, R. T., Lisenbee, C. S., Miernyk, J. A., Trelease, R. N. (1999). Peroxisomal Membrane Ascorbate Peroxidase Is Sorted to a Membranous Network That Resembles a Subdomain of the Endoplasmic Reticulum. Plant Cell 11: 2167-2186 [Abstract] [Full Text]  
  • Lin, Y., Sun, L., Nguyen, L. V., Rachubinski, R. A., Goodman, H. M. (1999). The Pex16p Homolog SSE1 and Storage Organelle Formation in Arabidopsis Seeds. Science 284: 328-330 [Abstract] [Full Text]  
  • South, S. T., Gould, S. J. (1999). Peroxisome Synthesis in the Absence of Preexisting Peroxisomes. JCB 144: 255-266 [Abstract] [Full Text]  
  • Chang, C., South, S, Warren, D, Jones, J, Moser, A., Moser, H., Gould, S. (1999). Metabolic control of peroxisome abundance. J. Cell Sci. 112: 1579-1590 [Abstract]  
  • Hettema, E. H., Ruigrok, C. C.M., Koerkamp, M. G., van den Berg, M., Tabak, H. F., Distel, B., Braakman, I. (1998). The Cytosolic DnaJ-like Protein Djp1p Is Involved Specifically in Peroxisomal Protein Import. JCB 142: 421-434 [Abstract] [Full Text]  
  • Titorenko, V. I., Smith, J. J., Szilard, R. K., 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. JCB 142: 403-420 [Abstract] [Full Text]  
  • Mullen, R. T., Trelease, R. N. (2000). The Sorting Signals for Peroxisomal Membrane-bound Ascorbate Peroxidase Are within Its C-terminal Tail. J. Biol. Chem. 275: 16337-16344 [Abstract] [Full Text]  
  • Honsho, M., Fujiki, Y. (2001). Topogenesis of Peroxisomal Membrane Protein Requires a Short, Positively Charged Intervening-loop Sequence and Flanking Hydrophobic Segments. STUDY USING HUMAN MEMBRANE PROTEIN PMP34. J. Biol. Chem. 276: 9375-9382 [Abstract] [Full Text]  
  • Fujiwara, C., Imamura, A., Hashiguchi, N., Shimozawa, N., Suzuki, Y., Kondo, N., Imanaka, T., Tsukamoto, T., Osumi, T. (2000). Catalase-less Peroxisomes. IMPLICATION IN THE MILDER FORMS OF PEROXISOME BIOGENESIS DISORDER. J. Biol. Chem. 275: 37271-37277 [Abstract] [Full Text]  
  • Wang, X., Unruh, M. J., Goodman, J. M. (2001). Discrete Targeting Signals Direct Pmp47 to Oleate-induced Peroxisomes in Saccharomyces cerevisiae. J. Biol. Chem. 276: 10897-10905 [Abstract] [Full Text]  
  • Faber, K. N., Kram, A. M., Ehrmann, M., Veenhuis, M. (2001). A Novel Method to Determine the Topology of Peroxisomal Membrane Proteins in Vivo Using the Tobacco Etch Virus Protease. J. Biol. Chem. 276: 36501-36507 [Abstract] [Full Text]  
  • Hashiguchi, N., Kojidani, T., Imanaka, T., Haraguchi, T., Hiraoka, Y., Baumgart, E., Yokota, S., Tsukamoto, T., Osumi, T. (2002). Peroxisomes Are Formed from Complex Membrane Structures in PEX6-deficient CHO Cells upon Genetic Complementation. Mol. Biol. Cell 13: 711-722 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»