A mobile PTS2 receptor for peroxisomal protein import in Pichia pastoris

Journal of Cell Biology

Volumn 140, Issue 4, 1998, Pages 807-820

  Elgersma, Ype ^a,b   Elgersma Hooisma, Minetta ^a,b   Wenzel, Thibaut ^a,c   McCaffery, J Michael ^a   Farquhar, Marilyn G ^a   Subramani, Suresh ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c DSM FOOD SPECIALTIES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CELL RECEPTOR; MUTANT PROTEIN;

ARTICLE; CELLULAR DISTRIBUTION; CHONDRODYSPLASIA PUNCTATA; CLINICAL ARTICLE; GENE MUTATION; HUMAN; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN TRANSPORT; YEAST;

ACETYL-COA C-ACYLTRANSFERASE; AMINO ACID SEQUENCE; ANTIBODIES; BIOLOGICAL TRANSPORT; CLONING, MOLECULAR; CYTOSOL; FUNGAL PROTEINS; GENE EXPRESSION; GENES, FUNGAL; GENETIC COMPLEMENTATION TEST; HUMANS; MICROBODIES; MOLECULAR SEQUENCE DATA; MUTATION; OLIGOPEPTIDES; PICHIA; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUBCELLULAR FRACTIONS;

PICHIA PASTORIS; SACCHAROMYCES CEREVISIAE;

EID: 0032559639     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.140.4.807     Document Type: Article

References (55)

1. Albertini, M., P. Rehling, R. Erdmann, W. Girzalsky, J.A.K.W. Kiel, M. Veenhuis, and W.H. Kunau. 1997. Pex14p, a peroxisomal membrane protein binding both receplors of the two PTS-dependent import pathways. Cell. 89:83-92.
2. Bartel, P., C.T. Chien, R. Sternglanz, and S. Fields. 1993. Using the two-hybrid system to detect protein-protein interactions. In Cellular Interactions in Development: A Practical Approach. D.A. Hartley, editor. IRL Press, Oxford. 153-179.
3. Braverman, N., G. Steel, C. Obie, A. Moser, H. Moser, S.J. Gould, and D. Valle. 1997. Human PEX7 encodes the peroxisomal PTS2 receptor and is responsible for rhizomelic chondrodysplasia punctata. Nat. Genet. 15:369-376.
4. Cregg, J.M., I.J. Van der Klei, G.J. Sulter, M. Veenhuis, and W. Harder. 1990. Peroxisome-deficient mutants of Hansenula polymorpha. Yeast. 6:87-97.
5. Dodt, G., and S.J. Gould. 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.
6. Dodt, G., N. Braverman, C. Wong, A. Moser, H.W. Moser, P. Watkins, D. Valle, and S.J. Gould. 1995. Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nat. Genet. 9:115-125.
7. Elgersma, Y., and H.F. Tabak. 1996. Proteins involved in peroxisome biogenesis and functioning. Biochim. Biophys. Acta. 1286:269-283.
8. Elgersma, Y., M. Van den Berg, H.F. Tabak, and B. Distel. 1993. An efficient positive selection procedure for the isolation of peroxisomal import and peroxisome assembly mutants of Saccharomyces cerevisiae. Genetics. 135:731-740.
9. Elgersma, Y., L. Kwast, A. Klein, T. Voorn-Brouwer, M. Van den Berg, B. Metzig, T. America, H.F. Tabak, and B. Distel. 1996a. The SH3 domain of the Saccharomyces 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.
10. Elgersma, Y., A. Vos, M. Van den Berg, C.W.T. Van Roermund, P. Van der Sluijs, B. Distel, and H.F. Tabak. 1996b. Analysis of the carboxyl-terminal peroxisomal targeting signal 1 in a homologous context in Saccharomyces cerevisiae. J. Biol. Chem. 271:26375-26382.
11. Erdmann, R., and G. Blobel. 1996. Identification of Pex13p, a peroxisomal membrane receptor for the PTS1 recognition factor. J. Cell Biol. 135:111-121.
12. Faber, K.N., P. Haima, C. Gietl, W. Harder, G. Ab, and M. Veenhuis. 1994. The methylotrophic yeast Hansenula polymorpha contains an inducible import Pathway for peroxisomal matrix proteins with an N-terminal targeting signal (PTS2 proteins). Proc. Natl. Acad. Sci. USA. 91:12985-12989.
13. Fields, S., and O. Song. 1989. A novel genetic system to detect protein-protein interactions. Nature. 340:245-246.
14. Fransen, M., C. Brees, E. Baumgart, J.C.T. Vanhooren, M. Baes, G.P. Mannaerts, and P.P. Van Veldhoven. 1995. Identification and characterization of the putative human peroxisomal C-terminal targeting signal import receptor. J. Biol. Chem. 270:7731-7736.
15. Gartner, J., C. Obie, P. Watkins, and D. Valle. 1994. Restoration of peroxisome biogenesis in a peroxisome-deficient mammalian cell line by expression of either the 35 kDa or the 70 kDa peroxisomal membrane proteins. J. Inherited. Metab. Dis. 17:327-329.
16. Gietl, C., K.N. Faber, I.J. van der Klei, and M. Veenhuis. 1994. Mutational analysis of the N-terminal topogenic signal of watermelon glyoxysomal malate dehydrogenase using the heterologous host Hansenula polymorpha. Proc. Natl. Acad. Sci. USA. 91:3151-3155.
17. Glover, J.R., D.W. Andrews, and R.A. Rachubinski. 1994a. Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc. Natl. Acad. Sci. USA. 91:10541-10545.
18. Glover, J.R., D.W. Andrews, S. Subramani, and R.A. Rachubinski. 1994b. Mutagenesis of the amino targeting signal of Saccharomyces cerevisiae 3-ketoacyl-CoA thiolase reveals conserved amino acids required for import into peroxisomes in vivo. J. Biol. Chem. 269:7558-7563.
19. Goebl, M., and M. Yanagida. 1991. The TPR snap helix: a novel protein repeat motif from mitosis to transcription. Trends Biol. Sci. 16:173-177.
20. Görlich, D., and I.W. Mattaj. 1996. Nucleocytoplasmic transport. Science. 271: 1513-1518.
21. Gould, S.J., G.A. Keller, and S. Subramani. 1987. Identification of a peroxisomal targeting signal at the carboxy terminus of firefly luciferase. J. Cell Biol. 105:2923-2931.
22. Gould, S.J., G.A. Keller, N. Hosken, J. Wilkinson, and S. Subramani. 1989. A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108:1657-1664.
23. Gould, S.J., D. McCollum, A.P. Spong, J.A. Heyman, and S. Subramani. 1992. Development of the yeast Pichia pastoris as a model organism for a genetic and molecular analysis of peroxisome assembly. Yeast. 8:613-628.
24. Gould, S.J., J.E. Kalish, J.C. Morrell, J. Bjorkman, A.J. Urquhart, and D.I. Crane. 1996. Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cvtoplasmic PTS1 receptor. J. Cell Biol. 135:85-95.
25. Hettema, E.H., C.W.T. Van Roermund, B. Distel, M. Van den Berg, C. Vilela, C. Rodrigues-Pousada, R.J.A. Wanders, and H.F. Tabak. 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.
26. Hollenberg, S.M., R. Sternglanz, P.F. Cheng, and H. Weintraub. 1995. Identification of a new family of tissue specific basic helix-loop-helix proteins with a two-hybrid system. Mol. Cell. Biol. 15:3813-3822.
27. Komachi, K., M.J. Redd, and A.D. Johnson. 1994. The WD repeats of Tup1 interact with the homeo domain protein a2. Genes Der. 8:2857-2867.
28. Lazarow, P.B., and Y. Fujiki. 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1:489-530.
29. Liu, H., X. Tan, M. Veenhuis, D. McCollum, and J.M. Cregg. 1992. An efficient screen for peroxisome-deficient mutants of Pichia pastoris. J. Bacteriol. 174: 4943-4951.
30. Marzioch, M., R. Erdmann, M. Veenhuis, and W.H. Kunau. 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. 13:4908-4918.
31. McCollum, D., E. Monosov, and S. Subramani. 1993. The pas8 mutant of Pichia pastoris exhibits the peroxisomal protein import deficiencies of Zellweger syndrome cells. The PAS8 protein binds to the COOH-terminal tripeptide peroxisomal targeting signal and is a member of the TPR protein family. J. Cell Biol. 121:761-774.
32. Monosov, E.Z., T.J. Wenzel, G.H. Luers, J.A. Heyman, and S. Subramani. 1996. Labeling of peroxisomes with green fluorescent protein in living P. pastoris cells. J. Histochem. Cytochem. 44:581-589.
33. Motley, A., E. Hettema, B. Distel, and H. Tabak. 1994. Differential protein import deficiencies in human peroxisome assembly disorders. J. Cell Biol. 125: 755-767.
34. Motley, A.M., E.H. Hettema, E.M. Hogenhout, P. Brites, A.L.M.A. Ten Asbroek, F.A. Wijburg, F. Baas, H.S. Heijmans, H.F. Tabak, R.J.A. Wanders, et al. 1997. Rhizomelic chondrodysplasia punctata is a peroxisomal protein targeting disease caused by a non-functional PTS receptor. Nat. Genet. 15: 377-380.
35. Neer, E.J., C.J. Schmidt, R. Nambudripad, and T.F. Smith. 1994. The ancient regulatory-protein family of WD-repeat proteins. Nature. 371:297-300.
36. Nuttley, W.M., R.K. Szilard, J.J. Smith, M. Veenhuis, and R.A. Rachubinski. 1995. The PAH2 gene is required for peroxisome assembly in the methylotrophic yeast Hansenula polymorpha and encodes a member of the tetratricopeptide repeat family of proteins. Gene (Amst.). 160:33-39.
37. Osumi, T., T. Tsukamoto, S. Hata, S. Yokota, S. Miura, Y. Fujiki, M. Hijikata, S. Miyazawa, and T. Hashimoto. 1991. Amino-terminal presequence of the precursor of peroxisomal 3-ketoacyl-CoA thiolase is a cleavable signal peptide for peroxisomal targeting. Biochem. Biophys. Res. Commun. 181:947-954.
38. Purdue, P.E., J.W. Zhang, M. Skoneczny, and P.B. Lazarow. 1997. Rhizomelic chondrodysplasia punctata is caused by deficiency of human PEX7, a homologue of the yeast PTS2 receptor. Nat. Genet. 15:381-384.
39. Rehling, P., M. Marzioch, F. Niesen, E. Wittke, M. Veenhuis, and W.H. Kunau. 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.
40. Ruigrok, C.C.M. H.F. Tabak, and I. Braakman. 1996. Import and oligomerization of peroxisomal proteins. Mol. Biol. Cell. 7:495.
41. Schatz, G., and B. Dobberstein. 1996. Common principles of protein translocation across membranes. Science. 271:1519-1526.
42. Schnell, D.J. 1995. Shedding light on the chloroplast protein import machinery. Cell. 83:521-524.
43. Slawecki, M.L., G. Dodt, S. Steinberg, A.B. Moser, H.W. Moser, and S.J. Gould. 1995. Identification of three distinct peroxisomal protein import defects in patients with peroxisome biogenesis disorders. J. Cell Sci. 108:1817-1829.
44. Subramani, S. 1997. PEX genes on the rise. Nat. Genet. 15:331-333.
45. Swinkels, B.W., S.J. Gould, A.G. Bodnar, R.A. Rachubinski, and S. Subramani. 1991. A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase. EMBO J. 10:3255-3262.
46. 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.
47. Tsukamoto, T., S. Hata, S. Yokota, S. Miura, Y. Fujiki, M. Hijikata, T. Hashimoto, and T. Osumi. 1994. Characterization of the signal peptide at the amino terminus of the rat peroxisomal 3-ketoacyl-CoA thiolase precursor. J. Biol. Chem. 269:6001-6010.
48. Van der Klei, I., R.E. Hilbrands, G.J. Swaving, H.R. Waterham, E.g., Vrieling, V.I. Titorenko, J.M. Cregg, W. Harder, and M. Veenhuis. 1995. The Hansenula polymorpha PER3 gene is essential for the import of PTS1 proteins into the peroxisomal matrix. J. Biol. Chem. 270:17229-17236.
49. Van der Leij, I., M. Van den Berg, R. Boot, M. Franse, B. Distel, and H.F. Tabak. 1992. Isolation of peroxisome assembly mutants from Saccharomyces cerevisiae with different morphologies using a novel positive selection procedure. J. Cell Biol. 119:153-162.
50. Van der Leij, I., M.M. Franse, Y. Elgersma, B. Distel, and H.F. Tabak. 1993. PAS10 is a tetratricopeptide-repeat protein that is essential for the import of most matrix proteins into peroxisomes of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 90:11782-11786.
51. Van der Voorn, L., and H.L. Ploegh. 1992. The WD-40 repeat. FEBS Lett. 307: 131-134.
52. Wiemer, E., W.M. Nuttley, B.L. Bertolaet, X. Li, U. Francke, M.J. Wheelock, U.K. Anné, K.R. Johnson, and S. Subramani. 1995. The human PTS1 receptor restores peroxisomal protein import deficiency in cells from patients with fatal peroxisomal disorders. J. Cell Biol. 130:51-65.
53. Wiemer, E.A.C., G.H. Lüers, K.N. Faber, T. Wenzel, M. Veenhuis, and S. Subramani. 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.
54. Zhang, J.W., and P.B. Lazarow. 1995. PEB1 (PAS7) in Saccharomyces cerevisiae encodes a hydrophilic, intra-peroxisomal protein that is a member of the WD repeat family and is essential for the import of thiolase into peroxisomes. J. Cell Biol. 129:65-80.
55. 2-terminal peptide. J. Cell Biol. 132:325-334.