Saccharomyces cerevisiae Pex3p and Pex19p are required for proper localization and stability of peroxisomal membrane proteins

EMBO Journal

Volumn 19, Issue 2, 2000, Pages 223-233

  Hettema, Ewald H ^c   Girzalsky, Wolfgang ^a   Van Den Berg, Marlene ^c   Erdmann, Ralf ^b   Distel, Ben ^c  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Peroxisomal membrane protein; Pretein targeting; Protein degradation; Yeast

Indexed keywords

MATRIX PROTEIN; MEMBRANE PROTEIN;

ARTICLE; BIOGENESIS; ENDOPLASMIC RETICULUM; MEMBRANE STRUCTURE; MUTANT; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 0034677197     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.2.223     Document Type: Article

References (60)

1. Albertini, M., Rehling, P., Erdmann, R., Girzalsky, W., Kiel, J.A.K.W., Veenhuis, M. and Kunau, W.-H. (1997) Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell. 89, 1-20.
2. Baerends, R.J.S. et al. (1996) The Hansenula polymorpha PER9 gene encodes a peroxisomal membrane protein essential for peroxisome assembly and integrity. J. Biol. Chem., 271, 8887-8894.
3. Bodnar, A.G. and Rachubinski, R.A. (1991) Characterization of the integral membrane polypeptides of rat liver peroxisomes isolated from untreated and clofibrate-treated rats. Biochem. Cell Biol., 69, 499-508.
4. Bradford, M.M. (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
5. Brocard, C., Lametschwandtner, G., Koudelka, R. and Hartig, A. (1997) Pex14p is a member of the protein linkage map of Pex5p. EMBO J., 16, 5491-5500.
6. Diestelkötter, P. and Just, W.W. (1993) In vitro insertion of the 22 kD peroxisomal membrane protein into isolated rat liver peroxisomes. J. Cell Biol., 123, 1717-1725.
7. Distel, B., Gould, S., Voorn-Brouwer, T., Van den Berg, M., Tabak, H. F. and Subramani, S. (1992) The carboxyl-terminal tripeptide serine-lysine-leucine of firefly luciferase is necessary but not sufficient for peroxisomal import in yeast. New Biol., 4, 157-165.
8. Distel, B. et al. (1996) A unified nomenclature for peroxisome biogenesis. J. Cell Biol., 135, 1-3.
9. Dodt, G. and Gould, S.J. (1996) Multiple PEX genes are required for proper subcellular distribution and stability of Pex5p, the PTS1 receptor: evidence that PTS1 protein import is mediated by a cycling receptor. J. Cell Biol., 135, 1763-1774.
10. Dyer, J.M., McNew, J.A. and Goodman, J.M. (1996) The sorting sequence of the peroxisomal integral membrane protein PMP47 is contained within a short hydrophilic loop. J. Cell Biol., 133, 269-280.
11. Eitzen, G.A., Szilard, R.K. and Rachubinski, R.A. (1997) Enlarged peroxisomes are present in oleic acid-grown Yarrowia lipolytica overexpressing the PEX16 gene encoding an intraperoxisomal peripheral membrane protein. J. Cell Biol., 137, 1265-1278.
12. Elgersma, Y., Kwast, L., Klein, A., Voorn-Brouwer, T., Van den Berg, M., Metzig, B., America, T., Tabak, H.F. and Distel, B. (1996) The SH3 domain of the Succharomyces cerevisiae peroxisomal membrane protein Pex13p functions as a docking site for Pex5p, a mobile receptor for the import of PTS1 containing proteins. J. Cell Biol., 135, 97-109.
13. Elgersma, Y., Kwast, L., Van den Berg, M., Snyder, W.B., Distel, B., Subramani, S. and Tabak, H.F. (1997) Overexpression of Pex15p, a phosphorylated peroxisomal integral membrane protein required for peroxisome assembly in Saccharomyces cerevisiae, causes proliferation of the endoplasmic reticulum membrane. EMBO J., 16, 7326-7341.
14. Elgersma, Y., Elgersma, H.M., Wenzel, T., McCaffery, J.M., Farquhar, M.G. and Subramani, S. (1998) A mobile PTS2 receptor for peroxisomal protein import in Pichia pastoris. J. Cell Biol., 140, 807-820.
15. Erdmann, R. and Blobel, G. (1995) Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J. Cell Biol., 128, 509-523.
16. Erdmann, R. and Blobel, G. (1996) Identification of Pex13p, a peroxisomal membrane receptor for the PTS1 recognition factor. J. Cell Biol., 135, 111-121.
17. Erdmann, R. and Kunau, W.-H. (1994) Purification and immunolocalization of the peroxisomal 3-oxoacyl-CoA thiolase from Saccharomyces cerevisiae. Yeast, 10, 1173-1182.
18. Erdmann, R., Veenhuis, M. and Kunau, W.H. (1997) Peroxisomes: organelles at the crossroads. Trends Cell Biol., 7, 400-407.
19. Fransen, M., Terlecky, S.R. and Subramani, S. (1998) Identification of a human PTS1 receptor docking protein directly required for peroxisomal protein import. Proc. Natl Acad. Sci. USA, 95, 8087-8092.
20. Fujiki, Y., Rachubinski, R.A. and Lazarow, P.B. (1984) Synthesis of a major integral membrane polypeptide of rat liver peroxisomes on free polysomes. Proc. Natl Acad. Sci. USA, 81, 7127-7131.
21. Girzalsky, W., Rehling, P., Stein, K., Kipper, J., Blank, L., Kunau, W.-H. and Erdmann, R. (1999) Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J. Cell Biol., 144, 1151-1162.
22. 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, 10541-10545.
23. Gotte, K., Girzalsky, W., Linkert, M., Baumgart, E., Kammerer, S., Kunau, W.-H. and Erdmann, R. (1998) Pex19p, a farnesylated protein essential for peroxisome biogenesis. Mol. Cell. Biol., 18, 616-628.
24. Gould, S.J., Kalish, J.E., Monrell, J.C., Bjorkman, J., Urquhart, A.J. and Crane, D.I. (1996) An SH3 protein in the peroxisome membrane is a docking factor for the PTS1 receptor. J. Cell Biol., 135, 85-95.
25. Häusler, T., Stierhof, Y.-D., Wirtz, E. and Clayton, E. (1996) Import of a DHFR hybrid protein into glycosomes in vivo is not inhibited by the folate-analogue aminopterin. J. Cell Biol., 132, 311-324.
26. Hettema, E.H., Van Roermund, C.W.T., Distel, B., Van den Berg, M., Vilda, C., Rodrigues-Pousada, C., Wanders, R.J.A. and Tabak, H.F. (1996) The ABC transporter proteins Pat1 and Pat2 are required for import of long-chain fatty acids into peroxisomes of Saccharomyces cerevisiae. EMBO J., 15, 3813-3822.
27. Hettema, E.H., Ruigrok, C.C.M., Groot Koerkamp, M., Van den Berg, M., Tabak, H.F., Distel, B. and Braakman, I. (1998) The cytosolic DnaJ-like protein DJp1p is involved specifically in peroxisomal protein import. J. Cell Biol., 142, 421-434.
28. Hettema, E.H., Distel, B. and Tabak, H.F. (1999) Import of proteins into peroxisomes. Biochim. Biophys. Acta, 1451, 1-18.
29. Höhfeld, J., Veenhuis, M. and Kunau, W.H. (1991) PAS3, a Saccharomyces cerevisiae gene encoding a peroxisomal integral membrane protein essential for peroxisome biogenesis. J. Cell Biol., 114, 1167-1178.
30. Holthuis, J.C.M., Nichols, B. and Pelham, H.R.B. (1998) The syntaxin TIg1p mediates trafficking of chitin synthase III to polarized growth sites in yeast. Mol. Biol. Cell, 9, 3383-3397.
31. Honsho, M., Tamura, S., Shimozawa, N., Suzuki, Y., Kondo, N. and Fujiki, Y. (1999) Mutation in PEX16 is causal in the peroxisome-deficient Zellweger syndrome complementation group D. Am. J. Hum. Genet., 63, 1622-1630.
32. Huhse, B., Rehling, P., Albertini, M., Meller, K. and Kunau, W.-H. (1998) Pex17p of Saccharomyces cerevisiae is a novel peroxin and component of the peroxisomal translocation machinery. J. Cell Biol., 140, 49-60.
33. Imanaka, T., Shiina, Y., Takano, T., Hashimoto, T. and Osumi, T. (1996) Insertion of the 70-kDa peroxisomal membrane protein into peroxisomal membranes in vivo and in vitro. J. Biol. Chem., 271, 3706-3713.
34. Kammerer, S., Holzinger, S., Welsch, U. and Roscher, A.A. (1998) Cloning and characterization of the gene encoding the human peroxisomal assembly protein Pex3p. FEBS Lett., 429, 53-60.
35. Kinoshita, N. et al. (1998) Newly identified Chinese hamster ovary cell mutants are defective in biogenesis of peroxisomal membrane vesicles (peroxisomal ghosts), representing a novel complementation group in mammals. J. Biol. Chem., 273, 24122-24130.
36. Kutay, U., Ahnert, H.G., Hartmann, E., Wiedenmann, B. and Rapoport, T.A. (1995) Transport route for synaptobrevin via a novel pathway of insertion into the endoplasmic reticulum membrane. EMBO J., 14, 217-223.
37. Lazarow, P.B. and Fujiki, Y. (1985) Biogenesis of peroxisomes. Annu. Rev. Cell Biol., 1, 489-530.
38. Lin, Y., Sun, L., Nguyen, L.V., Rachubinski, R.A. and Goodman, H.M. (1999) The Pex16p homolog SSE1 and storage organelle formation in Arabidopsis seeds. Science, 284, 328-330.
39. Marshall, P.A., Krimkevich, Y.I., Lark, R.H., Dyer, J.M., Veenhuis, M. and Goodman, J.M. (1995) PMP27 promotes peroxisome proliferation. J. Cell Biol., 129, 345-355.
40. Marzioch, M., Erdmann, R., Veenhuis, M. and Kunau, W.-H. (1994) PAS7 encodes a novel yeast member of the WD-40 protein family essential for import of 3-oxoacyl-CoA thiolase, a PTS2-containing protein, into peroxisomes. EMBO J., 13, 4908-4917.
41. Matsuzono, Y. et al. (1999) Human PEX19: cDNA cloning by functional complementation, mutation analysis in a patient with Zellweger syndrome and potential role in peroxisomal membrane assembly. Proc. Natl Acad. Sci. USA, 96, 2116-2121.
42. McNew, J.A. and Goodman, J.M. (1994) An oligomeric protein is imported into peroxisomes in vivo. J. Cell Biol., 127, 1245-1257.
43. Motley, A., Hettema, E., Distel, B. and Tabak, H.F. (1994) Differential protein import deficiencies in human peroxisome assembly disorders. J. Cell Biol., 125, 755-767.
44. Pause, B., Diestelkötter, P., Heid, H. and Just, W.W. (1997) Cytosolic factors mediate protein insertion into the peroxisomal membrane. FEBS Lett., 414, 95-98.
45. Rehling, P., Marzioch, M., Niesen, E. Wittke, E., Veenhuis, M. and Kunau, W.-H. (1996) The import receptor for the peroxisomal targeting signal 2 (PTS2) in Saccharomyces cerevisiae is encoded by the PAS7 gene. EMBO J., 15, 2901-2913.
46. Rout, M.P. and Kilmartin, J.V. (1990) Components of the yeast spindle pole body. J. Cell Biol., 111, 1913-1927.
47. Santos, M.J., Imanaka, J., Shio, H., Small, G.M. and Lazarow, P.B. (1988) Peroxisomal membrane ghosts in Zellweger syndrome: aberrant organelle assembly. Science, 239, 1536-1538.
48. Schliebs, W., Saidowsky, J., Agianian, B., Dodt, G., Herberg, F.W. and Kunau, W.-H. (1999) Recombinant human peroxisomal targeting signal receptor PEX5. J. Biol. Chem., 274, 5666-5673.
49. Snyder, W.B., Faber, K.N., Wenzel, T., Koller, A., Lüers, G.H., Rangell, L., Keller, G.A. and Subramani, S. (1999) Pex19p interacts with Pex3p and Pex10p aṅd is essential for peroxisome biogenesis in Pichia postoris. Mol. Biol. Cell, 10, 1745-1761.
50. South, S.T. and Gould, S.J. (1999) Peroxisome synthesis in the absence of preexisting peroxisomes. J. Cell Biol., 144, 255-266.
51. Subramani, S. (1998) Components involved in peroxisome import, biogenesis, proliferation, turnover and movement. Physiol. Rev., 78, 171-188.
52. Suzuki, Y., Orii, T., Yakiguchi, M., Mori, M., Hijikata, M. and Hashimoto, T. (1987) Biosynthesis of membrane polypeptides of rat liver peroxisomes. J. Biochem., 101, 491-496.
53. Tabak, H.F., Braakman, I. and Distel, B. (1999) Peroxisomes: simple in function but complex in maintenance. Trends Cell Biol., 9, 447-453.
54. Titorenko, V.I. and Rachubinski, R.A. (1998) The endoplasmic reticulum plays an essential role in peroxisome biogenesis. Trends Biochem. Sci., 23, 231-233.
55. Van der Klei, I.J., Hilbrands, R.E., Kiel, J.A., Rasmussen, S.W., Cregg, J.M. and Veenhuis, M. (1998) The ubiquitin-conjugating enzyme Pex4p of Hansenula polymorpha is required for efficient functioning of the PTS1 import machinery. EMBO J., 17, 3608-3618.
56. Wach, A., Brachat, A., Pöhlmann, R. and Philippsen, P. (1994) New heterologous modules for classical or PCR-based disruptions in Saccharomyces cerevisiae. Yeast, 10, 1793-1808.
57. Walton, P.A., Hill, P.E. and Subramani, S. (1995) Import of stably folded proteins into peroxisomes. Mol. Biol. Cell, 6, 675-683.
58. Wiemer, E.A.C., Lüers, G.H., Faber, K.N., Wenzel, J., Veenhuis, M. and Subramani, S. (1996) Isolation and characterization of Pas2p, a peroxisomal membrane protein essential for peroxisome biogenesis in the methylotrophic yeast Pichia pastoris. J. Biol. Chem., 271, 18973-18980.
59. Yahraus, T., Braverman, N., Dodt, G., Kalish, J.E., Morrell, J.C., Moser, H.W., Valle, D. and Gould, S.J. (1996) The peroxisomal biogenesis disorder group 4 gene, PXAAA1, encodes a cytoplasmic ATPase required for the stability of the PTS1 receptor. EMBO J., 15, 2914-2923.
60. Zinser, E. and Daum, G. (1995) Isolation and biochemical characterization of organelles from the yeast, Saccharomyces cerevisiae. Yeast, 11, 493-536.