Peroxisomal targeting, import, and assembly of alcohol oxidase in Pichia pastoris

Journal of Cell Biology

Volumn 139, Issue 6, 1997, Pages 1419-1431

  Waterham, Hans R ^a,b   Russell, Kimberly A ^a   De Vries, Yne ^a,c   Cregg, James M ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c INTERVET INTERNATIONAL BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL OXIDASE; BETA LACTAMASE; HEMAGGLUTININ;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENDOMYCETALES; NONHUMAN; OLIGOMERIZATION; PEROXISOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN TARGETING;

ALCOHOL OXIDOREDUCTASES; AMINO ACID SEQUENCE; BETA-LACTAMASES; CELL FRACTIONATION; CENTRIFUGATION, DENSITY GRADIENT; EPITOPES; ESCHERICHIA COLI; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HEMAGGLUTININS; MACROMOLECULAR SUBSTANCES; MICROBODIES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; ORGANELLES; PICHIA; RECOMBINANT FUSION PROTEINS;

PICHIA PASTORIS; SACCHAROMYCETALES;

EID: 0031439260     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.6.1419     Document Type: Article

References (55)

1. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1996. Analysis of proteins. In Current Protocols in Molecular Biology. Vol. 2. John Wiley and Sons, New York. pp. 10.1-10.20.
2. Bartel, P.L., C.-T. Chien, R. Sternglanz, and S. Fields. 1993. Elimination of false positives that arise in using the two-hybrid system. Biotechniques. 14:920-924.
3. Becker, D.M., and L. Guarente. 1991. High-efficiency transformation of yeast by electroporation. Methods Enzymol. 194:182-187.
4. Bellion, E., and J.M. Goodman. 1987. Proton ionophores prevent assembly of a peroxisomal protein. Cell. 48:165-173.
5. Cregg, J.M., K.J. Barringer, A.Y. Hessler, and K.R. Madden. 1985. Pichia pastoris as a host system for transformations. Mol. Cell Biol. 9:3376-3385.
6. Cregg, J.M., K.R. Madden, K.J. Barringer, G. Thill, and C.A. Stillman. 1989. Functional characterization of the two alcohol oxidase genes from the yeast Pichia pastoris. Mol. Cell Biol. 9:1316-1323.
7. 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.
8. Distel, B., M. Veenhuis, and H.F. Tabak. 1987. Import of alcohol oxidase into peroxisomes of Saccharomyces cerevisiae. EMBO (Eur. Mol. Biol. Organ.) J. 6:3111-3116.
9. 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.
10. Elgersma, Y., A. Vos, M. van den Berg, C.W. van Roermund, P. van der Swijs, B. Distel, and H.F. Tabak. 1996. Analysis of the carboxyl-terminal peroxisomal targeting signal 1 in a homologous context in Saccharomyces cerevisiae. J. Biol. Chem. 271:26375-26382.
11. Ellis, S.B., P.F. Brust, P.J. Koutz, A.F. Waters, M.M. Harphold, and T.R. Gingeras. 1985. Isolation of alcohol oxidase and two other methanol regulatable genes from the yeast Pichia pastoris. Mol. Cell Biol. 5:1111-1121.
12. Evers, M.E., V.I. Titorenko, I.J. van der Klei, W. Harder, and M. Veenhuis. 1994. Assembly of alcohol oxidase in peroxisomes of the yeast Hansenula polymorpha requires the cofactor flavin adenine dinucleotide. Mol. Biol. Cell. 5:829-837.
13. Evers, M.E., W. Harder, and M. Veenhuis. 1995. In vitro dissociation and reassembly of peroxisomal alcohol oxidases of Hansenula polymorpha and Fichia pastoris. FEBS (Fed. Eur. Biochem. Soc.) Lett. 368:293-296.
14. Evers, M.E., V. Titorenko, W. Harder, I.J. van der Klei, and M. Veenhuis. 1996. Flavin adenine dinucleotide binding is the crucial step in alcohol oxidase assembly in the yeast Hansenula polymorpha. Yeast. 12:917-923.
15. Faber, K.N., P. Haima, W. Harder, M. Veenhuis, and G. AB. 1994. Highly-efficient electrotransformation of the yeast Hansenula polymorpha. Curr. Genet. 25:305-310.
16. Glover, J.R., D.W. Andrews, and R.A. Rachubinski. 1994. Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc. Natl. Acad. Sci. USA. 91:10541-10545.
17. Goodman, J.M., C.W. Scott, P.N. Donahue, and J.P. Atherton. 1984. Alcohol oxidase assembles post-translationally into the peroxisome of Candida boidinii. J. Biol. Chem. 259:8485-8493.
18. 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.
19. Gould, S.J., G.-A. Keller, M. Scheider, S.H. Howell, L.J. Garrard, J.M. Goodman, B. Distel, H.F. Tabak, and S. Subramani. 1990. Peroxisomal protein import is conserved between yeast, plants, insects and mammals. EMBO (Eur. Mol. Biol. Organ.) J. 9:85-90.
20. 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. 6:613-628.
21. 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.
22. Koutz, P., G.R. Davis, C. Stillman, K. Barringer, J.M. Cregg. and G. Thill. 1989. Structural comparison of the Pichia pastoris alcohol oxidase genes. Yeast. 5: 167-177.
23. Kragler, F., A. Langeder, J. Raupachova, M. Binder, and A. Hartig. 1993. Two independent peroxisomal targeting signals in catalase A of Saccharomyces cerevisiae. J. Cell Biol. 120:665-673.
24. Lazarow, P.B., and H.W. Moser. 1994. Disorders in peroxisome biogenesis. In The Metabolic Basis of Inherited Disease. 7th ed. C.R. Scriver, A.L. Beaudet, W.S. Sly, and D. Valle, editors. McGraw Hill, New York. pp. 2287-2324.
25. Ledeboer, A.M., L. Edens, J. Maat, C. Visser, J.W. Bos, Z. Janowicz, M. Eckart, R. Roggenkamp, and C.P. Hollenberg. 1985. Molecular cloning and characterization of a gene coding for methanol oxidase in Hansenula polymorpha. Nucleic Acids Res. 13:3063-3082.
26. Leiper, J.M., P.B. Oatey, and C.J. Danpure. 1996. Inhibition of alanine:glyoxylate aminotransferase 1 dimerization is a prerequisite for its peroxisometo-mitochondrial mistargeting in primary hyperoxaluria type 1. J. Cell Biol. 135:939-951.
27. 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.
28. Liu, H., X. Tan, K.A. Russell, M. Veenhuis, and J.M. Cregg. 1995. PER3, a gene required for peroxisome biogenesis in Pichia pastoris, encodes a peroxisomal membrane protein involved in PTS1- and PTS2-protein import. J. Biol. Chem. 270:10940-10951.
29. McCollum, D., E. Monosov, and S. Subramani. 1993. The pas8 mutant of Pichia pastoris exhibits the peroxisomal 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
30. McNew, J.A., and J.M. Goodman. 1994. An oligomeric protein is imported into peroxisomes in vivo. J. Cell Biol. 127:1245-1257.
31. McNew, J.A., and J.M. Goodman. 1996. The targeting and assembly of peroxisomal proteins: some old rules do not apply. TIBS (Trends Biochem. Sci.) 21: 54-58.
32. 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 (Eur. Mol. Biol. Organ.) J. 15:2901-2913.
33. Roa, M., and G. Blobel. 1983. Biosynthesis of peroxisomal enzymes in the methylotrophic yeast Hansenula polymorpha. Proc. Natl. Acad. Sci. USA. 80:6872-6876.
34. Sakai, Y., and Y. Tani. 1992. Cloning and sequencing of the alcohol oxidase-encoding gene (AOD1) from the formaldehyde-producing asporogenous methylotrophic yeast, Candida boidinii S2. Gene. 114:67-73.
35. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Schram, A.W., A. Strijland, T. Hashimoto, R.J.A. Wanders, R.B.H. Schutgens, H. van den Bosch, and J.M. Tager. 1986. Biosynthesis and maturation of peroxisomal β-oxidation enzymes in fibroblasts in relation to the Zellweger syndrome and infantile Refsum disease. Proc. Natl. Acad. Sci. USA. 83:6156-6158.
37. Spong, A.P., and S. Subramani. 1993. Cloning and characterization of PAS5: a gene required for peroxisome biogenesis in the methylotrophic yeast Pichia pastoris. J. Cell Biol. 123:535-548.
38. Subramani, S. 1993. Protein import into peroxisomes and biogenesis of the organelle. Annu. Rev. Cell Biol. 9:445-478.
39. Sutcliffe, J.G. 1978. Nucleotide sequence of the ampicillin resistance gene of Escherichia coli plasmid pBR322. Proc. Natl. Acad. Sci. USA. 75:3737-3741.
40. Suzuki, Y., T. Orii, M. Mori, T. Tatibana, and T. Hashimoto. 1986. Deficient activities and proteins of peroxisomal beta oxidation enzymes in infants with Zellweger syndrome. Clin. Chim. Acta. 156:191-196.
41. 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 (Fed. Eur. Biochem. Soc.) Lett. 305:133-136.
42. Tan, X., V.I. Titorenko, I.J. van der Klei, G.J. Sulter, P. Haima, H.R. Waterham, M. Evers, W. Harder, M. Veenhuis, and J.M. Cregg. 1995a. Characterization of peroxisome-deficient mutants of Hansenula polymorpha. Curr. Genet. 28:248-257.
43. Tan, X., H.R. Waterham, M. Veenhuis, and J.M. Cregg. 1995b. The Hansenula polymorpha PER8 gene encodes a novel peroxisomal integral membrane protein involved in proliferation. J. Cell Biol. 128:307-319.
44. Terlecky, S.R., W.M. Nuttley, D. McCollum, E. Sock, and S. Subramani. 1995. The Pichia pastoris peroxisomal protein Pas8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. EMBO (Eur. Mol. Biol. Organ.) J. 14:3627-3634.
45. Tschopp, J.F., F.F. Brust, J.M. Cregg, C.A. Stillman, and T.R. Gingeras. 1987. Expression of the lacZ gene from two methanol-regulated promoters in Pichia pastoris. Nucleic Acids Res. 15:3859-3876.
46. van der Klei, I.J., W. Harder, and M. Veenhuis. 1991. Biosynthesis and assembly of alcohol oxidase, a peroxisomal matrix protein in methylotrophic yeasts: a review. Yeast. 7:195-209.
47. Veale, R.A., M.L.F. Guiseppin, H.M.J. van Eijk, P.E. Sudbery, and C.T. Verrips. 1992. Development of a strain of Hansenula polymorpha for the efficient expression of guar α-galactosidase. Yeast. 8:361-372.
48. Veenhuis, M., and W. Harder. 1991. Microbodies. In The Yeasts. 2nd ed., Vol. 4. A.H. Rose and J.S. Harrison, editors. Academic Press, London. pp. 601-653.
49. Walton, P.A., P.E. Hill, and S. Subramani. 1995. Import of stably folded proteins into peroxisomes. Mol. Biol. Cell. 6:675-683.
50. Waterham, H.R., and J.M. Cregg. 1997. Peroxisome biogenesis. Bioessays. 19: 57-66.
51. -) mutants of Hansenula polymorpha. Yeast. 8:961-972.
52. 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.
53. Waterham, H.R., Y. de Vries, K.A. Russell, W. Xie, M. Veenhuis, and J.M. Cregg. 1996. The Pichia pastoris PER6 gene product is a peroxisomal integral membrane protein essential for peroxisome biogenesis and has sequence similarity to the Zellweger Syndrome protein PAF-1. Mol. Cell. Biol. 16:2527-2536.
54. Waterham, H.R., M.E. Digan, P.J. Koutz, S.V. Lair, and J.M. Cregg. 1997. Isolation of the Pichia pastoris glyceraldehyde-3-phosphate dehydrogenase gene and use and regulation of its promoter. Gene. 186:37-14.
55. Wenzel, T.J., A. Migliazza, H.Y. Steensma, and J.A. van den Berg. 1992. Efficient selection of phleomycin-resistant Saccharomyces cerevisiae transformants. Yeast. 8:667-668.