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

REFERENCES

• Abeijon, C., P. Orlean, P. W. Robins, and C. B. Hirschberg 1989. Topography of glycosylation in yeast: characterization of GDP-mannose transport and lumenal guanosine diphosphatase activities in Golgi-like vesicles. Proc. Natl. Acad. Sci. USA 86: 6935–6939.
   PubMed Web of Science ®Google Scholar
• Baerends, R. J. S., S. W. Rasmussen, R. E. Hilbrands, M. van der Heide, K. N. Faber, P. T. W. Reuvekamp, J. A. K. W. Kiel, J. M. Cregg, I. J. van der Klei, and M. Veenhuis 1996. The Hansenula polymorpha PER9 gene encodes a peroxisomal membrane protein essential for peroxisome assembly and integrity. J. Biol. Chem. 271: 8887–8894.
   PubMedGoogle Scholar
• Berteaux-Lecellier, V., M. Picard, C. Thompson-Coffe, D. Zickler, A. Panvier-Adoutte, and J.-M. Simonet 1995. A nonmammalian homolog of the PAF1 gene (Zellweger syndrome) discovered as a gene involved in caryogamy in the fungus Podospora anserina. Cell 81: 1043–1051.
   PubMed Web of Science ®Google Scholar
• Bodnar, A. G., and R. A. Rachubinski 1991. Characterization of the integral membrane polypeptides of rat liver peroxisomes isolated from untreated and clofibrate-treated rats. Biochem. Cell Biol. 69: 499–508.
   PubMedGoogle Scholar
• Boisramé, A., J.-M. Beckerich, and C. Gaillardin 1996. Sls1p, an endoplasmic reticulum component, is involved in the protein translocation process in the yeast Yarrowia lipolytica. J. Biol. Chem. 271: 11668–11675.
   PubMedGoogle Scholar
• Chelstowska, A., and R. A. Butow 1995. RTG genes in yeast that function in communication between mitochondria and the nucleus are also required for expression of genes encoding peroxisomal proteins. J. Biol. Chem. 270: 18141–18146.
   PubMed Web of Science ®Google Scholar
• Coligan, J. E., B. M. Dunn, H. L. Ploegh, D. W. Speicher, and P. T. Wingfield 1995. Current protocols in protein science. Wiley Interscience, New York, N.Y.
   Google Scholar
• Distel, B., R. Erdmann, S. J. Gould, G. Blobel, D. I. Crane, J. M. Cregg, G. Dodt, Y. Fujiki, J. M. Goodman, W. W. Just, J. A. K. W. Kiel, W.-H. Kunau, P. B. Lazarow, G. P. Mannaerts, H. Moser, T. Osumi, R. A. Rachubinski, A. Roscher, S. Subramani, H. F. Tabak, D. Valle, I. van der Klei, P. P. van Veldhoven, and M. Veenhuis 1996. A unified nomenclature for peroxisome biogenesis. J. Cell Biol. 135: 1–3.
   PubMedGoogle Scholar
• Dyer, J. M., J. A. McNew, and J. M. Goodman 1996. The sorting sequence of the peroxisomal integral membrane protein PMP47 is contained within a short hydrophilic loop. J. Cell Biol. 133: 269–280.
   PubMedGoogle Scholar
• Eitzen, G. A., J. D. Aitchison, R. K. Szilard, M. Veenhuis, W. M. Nuttley, and R. A. Rachubinski 1995. The Yarrowia lipolytica gene PAY2 encodes a 42-kDa peroxisomal integral membrane protein essential for matrix protein import and peroxisome enlargement but not for peroxisome membrane proliferation. J. Biol. Chem. 270: 1429–1436.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Eitzen, G. A., V. I. Titorenko, J. J. Smith, M. Veenhuis, R. K. Szilard, and R. A. Rachubinski 1996. The Yarrowia lipolytica gene PAY5 encodes a peroxisomal integral membrane protein homologous to the mammalian peroxisome assembly factor PAF-1. J. Biol. Chem. 271: 20300–20306.
   PubMedGoogle Scholar
• Elgersma, Y. 1995. Transport of proteins and metabolites across the peroxisomal membrane in Saccharomyces cerevisiae. Ph.D. thesis. University of Amsterdam, Amsterdam, The Netherlands.
   Google Scholar
• Fabre, E., C. Tharaud, and C. Gaillardin 1992. Intracellular transit of a yeast protease is rescued by trans-complementation with its prodomain. J. Biol. Chem. 267: 15049–15055.
   PubMedGoogle Scholar
• Fahimi, H. D., E. Baumgart, and A. Völkl 1993. Ultrastructural aspects of the biogenesis of peroxisomes in rat liver. Biochimie 75: 201–208.
   PubMedGoogle Scholar
• Goodman, J. M., S. B. Trapp, H. Hwang, and M. Veenhuis 1990. Peroxisomes induced in Candida boidinii by methanol, oleic acid and d-alanine vary in metabolic function but share common integral membrane proteins. J. Cell Sci. 97: 193–204.
   PubMedGoogle Scholar
• He, F., D. Yaver, J.-M. Beckerich, D. Ogrydziak, and C. Gaillardin 1990. The yeast Yarrowia lipolytica has two, functional, signal recognition particle 7S RNA genes. Curr. Genet. 17: 289–292.
   PubMedGoogle Scholar
• Kaiser, C. A., and R. Schekman 1990. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell 61: 723–733.
   PubMed Web of Science ®Google Scholar
• Kyhse-Andersen, J. 1984. Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods 10: 203–209.
   PubMedGoogle Scholar
• Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227: 680–685.
   PubMed Web of Science ®Google Scholar
• Lanzetta, P. A., L. J. Alvarez, P. S. Reinach, and O. A. Candia 1979. An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100: 95–97.
   PubMed Web of Science ®Google Scholar
• Lazarow, P. B., and Y. Fujiki 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1: 489–530.
   PubMedGoogle Scholar
• Lazarow, P. B., and H. W. Moser 1994. Disorders of peroxisome biogenesis The metabolic basis of inherited disease7th ed.Scriver, C. R., A. L. Beaudet, W. S. Sly, and A. D. Valle2287–2324McGraw-Hill, New York, N.Y.
   Google Scholar
• Lee, I. H., and D. M. Ogrydziak 1997. Yarrowia lipolytica SRP54 homolog and translocation of Kar2p. Yeast 13: 499–513.
   PubMedGoogle Scholar
• Lopez, M. C., J.-M. Nicaud, H. B. Skinner, C. Vergnolle, J. C. Kader, V. A. Bankaitis, and C. Gaillardin 1994. A phosphatidylinositol/phosphatidylcholine transfer protein is required for differentiation of the dimorphic yeast Yarrowia lipolytica from the yeast to the mycelial form. J. Cell Biol. 125: 113–127.
   PubMedGoogle Scholar
• Matoba, S., J. Fukayama, R. A. Wing, and D. M. Ogrydziak 1988. Intracellular precursors and secretion of alkaline extracellular protease of Yarrowia lipolytica. Mol. Cell. Biol. 8: 4904–4916.
   PubMedGoogle Scholar
• Mellman, I., and K. Simons 1992. The Golgi complex: in vitro veritas? Cell 68: 829–840.
   PubMed Web of Science ®Google Scholar
• Novick, P., S. Ferro, and R. Schekman 1981. Order of events in the yeast secretory pathway. Cell 25: 461–469.
   PubMedGoogle Scholar
• Novick, P., C. Field, and R. Schekman 1980. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21: 205–215.
   PubMed Web of Science ®Google Scholar
• Novick, P., and R. Schekman 1979. Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 76: 1858–1862.
   PubMed Web of Science ®Google Scholar
• Novick, P., and R. Schekman 1983. Export of major cell surface proteins is blocked in yeast secretory mutants. J. Cell Biol. 96: 541–547.
   PubMed Web of Science ®Google Scholar
• Nunnari, J., and P. Walter 1996. Regulation of organelle biogenesis. Cell 84: 389–394.
   PubMed Web of Science ®Google Scholar
• Nuttley, W. M., A. M. Brade, C. Gaillardin, G. A. Eitzen, J. R. Glover, J. D. Aitchison, and R. A. Rachubinski 1993. Rapid identification and characterization of peroxisomal assembly mutants in Yarrowia lipolytica. Yeast 9: 507–517.
   Google Scholar
• Nuttley, W. M., A. M. Brade, G. A. Eitzen, M. Veenhuis, J. D. Aitchison, R. K. Szilard, J. R. Glover, and R. A. Rachubinski 1994. PAY4, a gene required for peroxisome assembly in the yeast Yarrowia lipolytica, encodes a novel member of a family of putative ATPases. J. Biol. Chem. 269: 556–566.
   PubMedGoogle Scholar
• Ogrydziak, D. M., S.-C. Cheng, and S. J. Scharf 1982. Characterization of Saccharomycopsis lipolytica mutants producing lowered levels of alkaline extracellular protease. J. Gen. Microbiol. 128: 2271–2280.
   Google Scholar
• Palade, G. 1975. Intracellular aspects of the process of protein synthesis. Science 189: 347–358.
   PubMed Web of Science ®Google Scholar
• Pidoux, A. L., and J. Armstrong 1992. Analysis of the BiP gene and identification of an ER retention signal in Schizosaccharomyces pombe. EMBO J. 11: 1583–1591.
   PubMedGoogle Scholar
• Pryer, N. K., L. J. Wuestehube, and R. Schekman 1992. Vesicle-mediated protein sorting. Annu. Rev. Biochem. 61: 471–516.
   PubMed Web of Science ®Google Scholar
• Roberts, C. J., C. K. Raymond, C. T. Yamashiro, and T. H. Stevens 1991. Methods for studying the yeast vacuole. Methods Enzymol. 194: 644–661.
   PubMedGoogle Scholar
• Rose, M. D., L. M. Misra, and J. P. Vogel 1989. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57: 1211–1221.
   PubMed Web of Science ®Google Scholar
• Rothman, J. E., and L. Orci 1992. Molecular dissection of the secretory pathway. Nature (London) 355: 409–415.
   PubMed Web of Science ®Google Scholar
• Subramani, S. 1993. Protein import into peroxisomes and biogenesis of the organelle. Annu. Rev. Cell Biol. 9: 445–478.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Thieringer, R., H. Shio, Y. S. Han, G. Cohen, and P. B. Lazarow 1991. Peroxisomes in Saccharomyces cerevisiae: immunofluorescence analysis and import of catalase A into isolated peroxisomes. Mol. Cell. Biol. 11: 510–522.
   PubMedGoogle Scholar
• Titorenko, V. I., G. A. Eitzen, and R. A. Rachubinski 1996. Mutations in the PAY5 gene of the yeast Yarrowia lipolytica cause the accumulation of multiple subpopulations of peroxisomes. J. Biol. Chem. 271: 20307–20314.
   PubMedGoogle Scholar
• Titorenko, V. I., D. M. Ogrydziak, and R. A. Rachubinski 1997. Four distinct secretory pathways serve protein secretion, cell surface growth, and peroxisome biogenesis in the yeast Yarrowia lipolytica. Mol. Cell. Biol. 17: 5210–5226.
   PubMedGoogle Scholar
• Titorenko, V. I., and R. A. Rachubinski. Unpublished data.
   Google Scholar
• Titorenko, V. I., and R. A. Rachubinski. Unpublished data.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Walton, P. A., S. J. Gould, R. A. Rachubinski, S. Subramani, and J. R. Feramisco 1992. Transport of microinjected alcohol oxidase from Pichia pastoris into vesicles in mammalian cells: involvement of the peroxisomal targeting signal. J. Cell Biol. 118: 499–508.
   PubMedGoogle Scholar
• Waterham, H. R., V. I. Titorenko, G. J. Swaving, W. Harder, and M. Veenhuis 1993. Peroxisomes in the methylotrophic yeast Hansenula polymorpha do not necessarily derive from pre-existing organelles. EMBO J. 12: 4785–4794.
   PubMedGoogle Scholar
• Wuestehube, L. J., R. Duden, A. Eun, S. Hamamoto, P. Korn, R. Ram, and R. Schekman 1996. New mutants of Saccharomyces cerevisiae affected in the transport of proteins from the endoplasmic reticulum to the Golgi complex. Genetics 142: 393–406.
   PubMedGoogle Scholar