Formation of the peroxisome lumen is abolished by loss of Pichia pastoris Pas7p, a zinc-binding integral membrane protein of the peroxisome

Molecular and Cellular Biology

Volumn 15, Issue 11, 1995, Pages 6406-6419

  Kalish, Jennifer E ^a   Theda, Christiane ^a   Morrell, James C ^a   Berg, Jeremy M ^a   Gould, Stephen J ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; GENE PRODUCT; HYBRID PROTEIN; MEMBRANE PROTEIN; ZINC;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE TRANSPORT; ENDOMYCETALES; ESCHERICHIA COLI; FUNGAL GENETICS; FUNGUS MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN TRANSPORT; YEAST;

ESCHERICHIA COLI; FUNGI; MAMMALIA; PICHIA PASTORIS; SACCHAROMYCETALES;

EID: 0028801334     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.15.11.6406     Document Type: Article

References (88)

1. Aitchison, J. D., W. W. Murray, and R. Rachubinski. 1991. The carboxyterminal ala-lys-ile is essential for targeting Candida tropicalis trifunctional enzyme to yeast peroxisomes. J. Biol. Chem. 266:23197-23203.
2. 1H-nuclear magnetic resonance spectroscopy. J. Mol. Biol. 237:201-211.
3. Berg, J. M. 1990. Zinc fingers and other metal-binding domains. J. Biol. Chem. 265:6513-6516.
4. Blattner, J., B. Swinkels, H. Dorsam, T. Prospers, S. Subramani, and C. Clayton. 1992. Glycosome assembly in trypanosomes: variations in the acceptable degeneracy of a COOH-terminal microbody targeting signal. J. Cell Biol. 119:1129-1136.
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
6. Chatterjee, P. K., M. Bruner, S. J. Flint, and M. L. Harter. 1988. DNA-binding properties of an adenovirus 289 R E1A protein. EMBO J. 7:835-841.
7. Crane, D. I., and S. J. Gould. 1994. The Pichia pastoris HIS4 gene: nucleotide sequence, creation of a non-reverting his4 deletion mutant, and development of HIS4-based replicating and integrating plasmids. Curr. Genet. 26:443-450.
8. Crane, D. I., J. E. Kalish, and S. J. Gould. 1994. The Pichia pastoris PAS4 gene encodes a ubiquitin-conjugating enzyme required for peroxisome assembly. J. Biol. Chem. 269:21835-21844.
9. Cregg, J. Personal communication.
10. Cregg, J. M., I. J. Vankiel, G. J. Sulter, M. Veenhuis, and W. Harder. 1990. Peroxisome-deficient mutants of Hansenula polymorpha. Yeast 6:87-97.
11. Culp, J. S., L. C. Webster, D. J. Friedman, C. L. Smith, W.-J. Huang, F. Y.-H. Wu, M. Rosenberg, and R. P. Riccardi. 1988. The 289-amino acid E1A protein of adenovirus binds zinc in a region that is important for transactivation. Proc. Natl. Acad. Sci. USA 85:6450-6454.
12. Didion, T., and R. Roggenkamp. 1992. Targeting signal of the peroxisomal catalase in the methylotrophic yeast Hansenula polymorpha. FEBS Lett. 303:113-116.
13. 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.
14. Elgersma, Y., M. van den Berg, H. F. Tabak, and B. Distel. 1993. An efficient positive selection procedure for the isolation of peroxisome import and peroxisome assembly mutants of Saccharomyces cerevisiae. Genetics 135: 731-740.
15. Erdmann, R., D. Veenhuis, D. Mertens, and W. H. Kunau. 1989. Isolation of peroxisome-deficient mutants of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 86:5419-5423.
16. Erdmann, R., F. F. Wiebel, A. Flessau, J. Rytka, A. Beyer, K. U. Fröhlich, and W. H. Kunau. 1991. PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell 64:499-510.
17. 4 motif of an alpha herpes virus protein family. J. Mol. Biol. 234:1038-1047.
18. Freemont, P. S., I. M. Hanson, and J. Trowsdale. 1991. A novel cysteine-rich sequence motif. Cell 64:483-484.
19. Fujiki, Y., S. Fowler, H. Shio, A. L. Hubbard, and P. B. Lazarow. 1982. Polypeptide and phospholipid composition of the membrane of rat liver peroxisomes: comparison with endoplasmic reticulum and mitochondrial membranes. J. Cell Biol. 93:103-110.
20. Fujiki, Y., A. L. Hubbard, S. Fowler, and P. B. Lazarow. 1982. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93:97-102.
21. Giedroc, D. P., K. M. Keating, K. R. Williams, and J. E. Coleman. 1987. The function of zinc in gene 32 protein from T4. Biochemistry 26:5251-5259.
22. Giedroc, D. P., K. M. Keating, K. R. Williams, W. H. Konigsberg, and J. E. Coleman. 1986. Gene 32 protein, the single-stranded DNA binding protein from bacteriophage T4, is a zinc metalloprotein. Proc. Natl. Acad. Sci. USA 83:8452-8456.
23. Gietl, C., K. N. Faber, I. J. 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.
24. Ginsberg, A., M. E. Nelbach, V. P. Pigiet, J. C. Gerhart, and H. K. Schachman. 1972. A role for zinc in the quaternary structure of aspartate transcarbamoylase from Escherichia coli. Biochemistry 11:315-327.
25. Glover, J. R., D. A. Andrews, and R. A. Rachubinski. 1994. Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc. Natl. Acad. Sci. USA 91:10541-10545.
26. Glover, J. R., D. A. Andrews, S. Subramani, and R. A. Rachubinski. 1994. 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.
27. Gould, S. J. Unpublished data.
28. 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.
29. Gould, S. J., G.-A. Keller, M. Schneider, S. H. Howell, L. J. Garrard, J. M. Goodman, B. Distel, H. Tabak, and S. Subramani. 1990. Peroxisomal protein import is conserved between yeast, plants, insects and mammals. EMBO J. 9:85-90.
30. 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.
31. Gould, S. J., G.-A. Keller, and S. Subramani. 1988 Identification of peroxisomal targeting signals at the carboxy terminus of four peroxisomal proteins. J. Cell Biol. 107:897-905.
32. Gould, S. J., S. Krisans, G.-A. Keller, and S. Subramani. 1990. Antibodies directed against the peroxisomal targeting signal of firefly luciferase recognize multiple mammalian peroxisomal proteins. J. Cell Biol. 110:27-34.
33. 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.
34. Grant, S. G., J. Jessee, F. R. Bloom, and D. Hanahan. 1990. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc. Natl. Acad. Sci. USA 87:4645-4649.
35. Hansen, H., T. Didion, A. Thiemann, M. Veenhuis, and R. Roggenkamp. 1992. Targeting signals of the major peroxisomal proteins in the methylotrophic yeast Hansenula polymorpha. Mol. Gen. Genet. 235:269-278.
36. Heyman, J. A., E. Monosov, and S. Subramani. 1994. Role of the PAS1 gene of Pichia pastoris in peroxisome biogenesis. J. Cell Biol. 127:1259-1273.
37. Hoffman, C. S., and F. Winston. 1987. A ten minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of E. coli. Gene 57:267-272.
38. Höhfeld, J., M. Veenhuis, and W. H. Kunau. 1991. PAS3, a Saccharomyces cerevisiae gene encoding a peroxisomal integral membrane protein essential for peroxisome biogenesis. J. Cell Biol. 114:1167-1178.
39. Imanaka, T., G. M. Small, and P. B. Lazarow. 1987. Translocation of acyl-CoA oxidase into peroxisomes requires ATP hydrolysis but not a membrane potential. J. Cell Biol. 105:2915-2922.
40. Kalish, J. E., and S. J. Gould. Unpublished data.
41. Kalish, J. E., J. C. Morrell, and S. J. Gould. Pichia pastoris Pas10p, a 48-kDa zinc-binding protein of the peroxisome membrane, is essential for protein import into peroxisomes. Submitted for publication.
42. Keller, G.-A., S. Krisans, S. J. Gould, J. M. Sommer, W. Schleibs, W. H. Kunau, S. Brody, and S. Subramani. 1991. Evolutionary conservation of a microbody targeting signal that targets proteins to peroxisomes, glyoxysomes and glycosomes. J. Cell Biol. 114:893-904.
43. Kunau, W. H., A. Beyer, T. Franken, K. Gotte, M. Marzioch, J. Saidowsky, A. Skaletz-Rorowski, and F. F. Wiebel. 1993. Two complementary approaches to study peroxisome biogenesis in Saccharomyces cerevisiae: forward and reversed genetics. Biochimie 75:209-224.
44. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
45. Lazarow, P. B., and Y. Fujiki. 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1:489-530.
46. Lazarow, P. B., and H. W. Moser. 1994. Disorders of peroxisome biogenesis, p. 2287-2324. In C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle (ed.), The metabolic and molecular basis of inherited disease. McGraw Hill Book Co., New York.
47. Lillie, J. W., P. M. Loewenstein, M. R. Green, and M. Green. 1987. Functional domains of adenovirus type 5 Ela proteins. Cell 50:1091-1100.
48. Liu, H., X. Tan, M. Veenhuis, D. McCollum, and J. M. Cregg. 1992. An efficient screen for peroxisome-deficient mutants of Pichia pustoris. J. Bacteriol. 174:4943-4951.
49. Lovering, R., I. Hanson, K. L. B. Borden, S. Martin, N. O'Reilly, G. Evan, D. Rahman, D. J. C. Pappin, J. Trowsdale, and P. Freemont. 1993. Identification and preliminary characterization of a protein motif related to the zincfinger. Proc. Natl. Acad. Sci. USA 90:2112-2116.
50. Lüers, G., T. Hashimoto, H. D. Fahimi, and A. Völkl. 1993. Biogenesis of peroxisomes: isolation and characterization of two distinct peroxisomal populations from normal and regenerating rat liver. J. Cell Biol. 121:1271-1280.
51. 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.
52. McCammon, M. T., J. A. McNew, P. J. Willy, and J. M. Goodman. 1994. An internal region of the peroxisomal membrane protein PMP47 is essential for sorting to peroxisomes. J. Cell Biol. 124:915-925.
53. 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. 121:761-764.
54. McNew, J. A., and J. M. Goodman. 1994. An oligomeric protein is imported into peroxisomes in vivo. J. Cell Biol. 127:1245-1257.
55. Miura, S., I. Kasuya-Arai, H. Mori, S. Miyazawa, T. Osumi, T. Hashimoto, and Y. Fujiki. 1992. Carboxyl-terminal consensus Ser-Lys-Leu-relatcd tripeptide of peroxisomal proteins functions in vitro as a minimal peroxisomal-targeting signal. J. Biol. Chem. 267:14405-14411.
56. Motley, A., E. Hetterna, B. Distel, and H. Tabak. 1994. Differential protein import efficiencies in human peroxisome assembly disorders. J. Cell Biol. 125:755-767.
57. 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.
58. 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.
59. 1H NMR studies of T4 gene 32 protein: effects of zinc removal and reconstitution. Biochemistry 28:8828-8832.
60. Patarca, R., and M. A. Fletcher. 1992. Ring finger in the peroxisome assembly factor-1. FEBS Lett. 312:1-2.
61. Pennington, R. J. 1961. Biochemistry of dystrophic muscle: mitochondrial succinate-tetrazolium reductase and adenosine triphosphate. Biochem. J. 80:649-654.
62. Peters, T. J., M. Muller, and C. de Duve. 1972. Lysosomes of the arterial wall. I. Isolation and subcellular fractionation of cells from normal rat aorta. J. Exp. Med. 136:1179-1139.
63. Quest, A. F. G., J. Bloomenthal, E. S. G. Bardes, and R. M. Bell. 1992. The regulatory domain of protein kinase C coordinates four atoms of zinc. J. Biol. Chem. 267:10193-10197.
64. Rothstein, R. 1991. Targeting, disruption, replacement, and allele rescue: integrative transformation in yeast. Methods Enzymol. 194:281-301.
65. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
66. Sanger, F., S. Nicklin, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
67. Santos, M., T. Imanaka, H. Shio, G. M. Small, and P. B. Lazarow. 1988. Peroxisomal membrane ghosts in Zeliweger syndrome - aberrant organelle assembly. Science 239:1536-1538.
68. Shimozawa, N., T. Tsukamoto, Y. Suzuki, T. Orii, Y. Shirayoshi, T. Mori, and Y. Fujiki. 1992. A human gene responsible for Zellweger syndrome that affects peroxisome assembly. Science 255:1132-1134.
69. 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.
70. Spong, A. P., and S. Subramani. 1993. Cloning and characterization of PAS5: a gene required tor peroxisome biogenesis in the methylotrophic yeast Pichia pastoris. J. Cell Biol. 123:535-548.
71. Studier, F. W., A. H. Rosenberg, J. J. Dunn, and J. W. Dubendoff. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:60-89.
72. Subramani, S. 1993. Protein import into peroxisomes and biogenesis of the organelle. Annu. Rev. Cell Biol. 9:445-478.
73. 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.
74. Swinkels, B. W., S. J. Gould, and S. Subramani. 1992. Targeting efficiencies of various permutations of the consensus C-terminal tripeptide peroxisomal targeting signal. FEBS Lett. 305:133-136.
75. Tan, X., H. R. Waterham, M. Veenhuis, and J. M. Cregg. 1995. The Hansenula polymorpha PER8 gene encodes a novel peroxisomal integral membrane protein involved in proliferation. J. Cell Biol. 128:307-319.
76. Thieringer, R., and C. R. H. Raetz. 1993. Peroxisome-deficient chinese hamster ovary cells with point mutations in peroxisome assembly factor-1. J. Biol. Chem. 268:12631-12636.
77. Tolbert, N. E. 1981. Metabolic pathways in peroxisomes and glyoxysomes. Annu. Rev. Biochem. 50:133-157.
78. Tsukamoto, T., S. Miura, and Y. Fujiki. 1991. Restoration by a 35K membrane protein of peroxisome assembly in a peroxisome-deficient mammalian cell mutant. Nature (London) 350:77-81.
79. Tsukamoto, T., N. Shimozawa, and Y. Fujiki. 1994. Peroxisome assembly factor 1: nonsense mutation in a peroxisome-deficient Chinese hamster cell mutant and deletion analysis. Mol. Cell. Biol. 14:5458-5465.
80. Tuttle, D. L., A. S. Lewin, and W. A. Dunn. 1993. Selective autophagy of peroxisomes in methylotrophic yeasts. Eur. J. Cell Biol. 60:283-290.
81. 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.
82. Van der Leij, I., M. M. Franse, Y. Elgersman, 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.
83. Voorn-Brouer, T., I. van der Leij, W. Hemrika, B. Distel, and H. F. Tabak. 1993. Sequence of the PAS8 gene, the product of which is essential for biogenesis of peroxisomes in Saccharomyces cerevisiae. Biochem. Biophys. Acta 1216:325-328.
84. Waterham, H. R., V. I. Titorenko, P. Haima, J. M. Cregg, W. Harder, and M. Veenhuis. 1994. The Hansenula polymorpha PER1 gene is essential for peroxisome biogenesis and encodes a peroxisomal matrix protein with both carboxy- and amino-terminal targeting signals. J. Cell Biol. 127:737-749.
85. 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.
86. Wendland, M., and S. Subramani. 1993. Cytosol-dependent peroxisomal protein import in a permeabilized cell system. J. Cell Biol. 120:675-685.
87. Wiebel, F. F., and W.-F. Kunau. 1992. The Pas2 protein essential for peroxisome biogenesis is related to ubiquitin-conjugating enzymes. Nature (London) 359:73-76.
88. Wong, C., and S. J. Gould. Cloning and nucleotide sequence of the Pichia pastoris LEU2 gene. Gene, in press.