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. 1995 Nov;15(11):6406–6419. doi: 10.1128/mcb.15.11.6406

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

J E Kalish 1, C Theda 1, J C Morrell 1, J M Berg 1, S J Gould 1
PMCID: PMC230892  PMID: 7565793

Abstract

We have cloned and sequenced PAS7, a gene required for peroxisome assembly in the yeast Pichia pastoris. The product of this gene, Pas7p, is a member of the C3HC4 superfamily of zinc-binding proteins. Point mutations that alter conserved residues of the C3HC4 motif abolish PAS7 activity and reduce zinc binding, suggesting that Pas7p binds zinc in vivo and that zinc binding is essential for PAS7 function. As with most pas mutants, pas7 cells exhibit a pronounced deficiency in import of peroxisomal matrix proteins that contain either the type 1 peroxisomal targeting signal (PTS1) or the type 2 PTS (PTS2). However, while other yeast and mammalian pas mutants accumulate ovoid, vesicular peroxisomal intermediates, loss of Pas7p leads to accumulation of membrane sheets and vesicles which lack a recognizable lumen. Thus, Pas7p appears to be essential for protein translocation into peroxisomes as well as formation of the lumen of the organelle. Consistent with these data, we find that Pas7p is an integral peroxisomal membrane protein which is entirely resistant to exogenous protease and thus appears to reside completely within the peroxisome. Our observations suggest that the function of Pas7p defines a previously unrecognized step in peroxisome assembly: formation of the peroxisome lumen. Furthermore, because the peroxisomal intermediates in the pas7 delta mutant proliferate in response to peroxisome-inducing environmental conditions, we conclude that Pas7p is not required for peroxisome proliferation.

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Selected References

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  1. Aitchison J. D., Murray W. W., Rachubinski R. A. The carboxyl-terminal tripeptide Ala-Lys-Ile is essential for targeting Candida tropicalis trifunctional enzyme to yeast peroxisomes. J Biol Chem. 1991 Dec 5;266(34):23197–23203. [PubMed] [Google Scholar]
  2. Barlow P. N., Luisi B., Milner A., Elliott M., Everett R. Structure of the C3HC4 domain by 1H-nuclear magnetic resonance spectroscopy. A new structural class of zinc-finger. J Mol Biol. 1994 Mar 25;237(2):201–211. doi: 10.1006/jmbi.1994.1222. [DOI] [PubMed] [Google Scholar]
  3. Berg J. M. Zinc fingers and other metal-binding domains. Elements for interactions between macromolecules. J Biol Chem. 1990 Apr 25;265(12):6513–6516. [PubMed] [Google Scholar]
  4. Blattner J., Swinkels B., Dörsam H., Prospero T., Subramani S., Clayton C. Glycosome assembly in trypanosomes: variations in the acceptable degeneracy of a COOH-terminal microbody targeting signal. J Cell Biol. 1992 Dec;119(5):1129–1136. doi: 10.1083/jcb.119.5.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  6. Chatterjee P. K., Bruner M., Flint S. J., Harter M. L. DNA-binding properties of an adenovirus 289R E1A protein. EMBO J. 1988 Mar;7(3):835–841. doi: 10.1002/j.1460-2075.1988.tb02882.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crane D. I., Gould S. J. 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. 1994 Nov-Dec;26(5-6):443–450. doi: 10.1007/BF00309932. [DOI] [PubMed] [Google Scholar]
  8. Crane D. I., Kalish J. E., Gould S. J. The Pichia pastoris PAS4 gene encodes a ubiquitin-conjugating enzyme required for peroxisome assembly. J Biol Chem. 1994 Aug 26;269(34):21835–21844. [PubMed] [Google Scholar]
  9. Culp J. S., Webster L. C., Friedman D. J., Smith C. L., Huang W. J., Wu F. Y., Rosenberg M., Ricciardi R. P. The 289-amino acid E1A protein of adenovirus binds zinc in a region that is important for trans-activation. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6450–6454. doi: 10.1073/pnas.85.17.6450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Didion T., Roggenkamp R. Targeting signal of the peroxisomal catalase in the methylotrophic yeast Hansenula polymorpha. FEBS Lett. 1992 Jun 1;303(2-3):113–116. doi: 10.1016/0014-5793(92)80500-g. [DOI] [PubMed] [Google Scholar]
  11. Dodt G., Braverman N., Wong C., Moser A., Moser H. W., Watkins P., Valle D., Gould S. J. Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nat Genet. 1995 Feb;9(2):115–125. doi: 10.1038/ng0295-115. [DOI] [PubMed] [Google Scholar]
  12. Elgersma Y., van den Berg M., Tabak H. F., Distel B. An efficient positive selection procedure for the isolation of peroxisomal import and peroxisome assembly mutants of Saccharomyces cerevisiae. Genetics. 1993 Nov;135(3):731–740. doi: 10.1093/genetics/135.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Erdmann R., Veenhuis M., Mertens D., Kunau W. H. Isolation of peroxisome-deficient mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5419–5423. doi: 10.1073/pnas.86.14.5419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Erdmann R., Wiebel F. F., Flessau A., Rytka J., Beyer A., Fröhlich K. U., Kunau W. H. PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell. 1991 Feb 8;64(3):499–510. doi: 10.1016/0092-8674(91)90234-p. [DOI] [PubMed] [Google Scholar]
  15. Everett R. D., Barlow P., Milner A., Luisi B., Orr A., Hope G., Lyon D. A novel arrangement of zinc-binding residues and secondary structure in the C3HC4 motif of an alpha herpes virus protein family. J Mol Biol. 1993 Dec 20;234(4):1038–1047. doi: 10.1006/jmbi.1993.1657. [DOI] [PubMed] [Google Scholar]
  16. Freemont P. S., Hanson I. M., Trowsdale J. A novel cysteine-rich sequence motif. Cell. 1991 Feb 8;64(3):483–484. doi: 10.1016/0092-8674(91)90229-r. [DOI] [PubMed] [Google Scholar]
  17. Fujiki Y., Fowler S., Shio H., Hubbard A. L., Lazarow P. B. Polypeptide and phospholipid composition of the membrane of rat liver peroxisomes: comparison with endoplasmic reticulum and mitochondrial membranes. J Cell Biol. 1982 Apr;93(1):103–110. doi: 10.1083/jcb.93.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fujiki Y., Hubbard A. L., Fowler S., Lazarow P. B. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol. 1982 Apr;93(1):97–102. doi: 10.1083/jcb.93.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Giedroc D. P., Keating K. M., Williams K. R., Coleman J. E. The function of zinc in gene 32 protein from T4. Biochemistry. 1987 Aug 25;26(17):5251–5259. doi: 10.1021/bi00391a007. [DOI] [PubMed] [Google Scholar]
  20. Giedroc D. P., Keating K. M., Williams K. R., Konigsberg W. H., Coleman J. E. Gene 32 protein, the single-stranded DNA binding protein from bacteriophage T4, is a zinc metalloprotein. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8452–8456. doi: 10.1073/pnas.83.22.8452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gietl C., Faber K. N., van der Klei I. J., Veenhuis M. Mutational analysis of the N-terminal topogenic signal of watermelon glyoxysomal malate dehydrogenase using the heterologous host Hansenula polymorpha. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3151–3155. doi: 10.1073/pnas.91.8.3151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Glover J. R., Andrews D. W., Rachubinski R. A. Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10541–10545. doi: 10.1073/pnas.91.22.10541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Glover J. R., Andrews D. W., Subramani S., Rachubinski R. A. 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. 1994 Mar 11;269(10):7558–7563. [PubMed] [Google Scholar]
  24. Gould S. G., Keller G. A., Subramani S. Identification of a peroxisomal targeting signal at the carboxy terminus of firefly luciferase. J Cell Biol. 1987 Dec;105(6 Pt 2):2923–2931. doi: 10.1083/jcb.105.6.2923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gould S. J., Keller G. A., Hosken N., Wilkinson J., Subramani S. A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol. 1989 May;108(5):1657–1664. doi: 10.1083/jcb.108.5.1657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gould S. J., Keller G. A., Schneider M., Howell S. H., Garrard L. J., Goodman J. M., Distel B., Tabak H., Subramani S. Peroxisomal protein import is conserved between yeast, plants, insects and mammals. EMBO J. 1990 Jan;9(1):85–90. doi: 10.1002/j.1460-2075.1990.tb08083.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Gould S. J., Keller G. A., Subramani S. Identification of peroxisomal targeting signals located at the carboxy terminus of four peroxisomal proteins. J Cell Biol. 1988 Sep;107(3):897–905. doi: 10.1083/jcb.107.3.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gould S. J., Krisans S., Keller G. A., Subramani S. Antibodies directed against the peroxisomal targeting signal of firefly luciferase recognize multiple mammalian peroxisomal proteins. J Cell Biol. 1990 Jan;110(1):27–34. doi: 10.1083/jcb.110.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gould S. J., McCollum D., Spong A. P., Heyman J. A., Subramani S. Development of the yeast Pichia pastoris as a model organism for a genetic and molecular analysis of peroxisome assembly. Yeast. 1992 Aug;8(8):613–628. doi: 10.1002/yea.320080805. [DOI] [PubMed] [Google Scholar]
  30. Grant S. G., Jessee J., Bloom F. R., Hanahan D. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4645–4649. doi: 10.1073/pnas.87.12.4645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hansen H., Didion T., Thiemann A., Veenhuis M., Roggenkamp R. Targeting sequences of the two major peroxisomal proteins in the methylotrophic yeast Hansenula polymorpha. Mol Gen Genet. 1992 Nov;235(2-3):269–278. doi: 10.1007/BF00279370. [DOI] [PubMed] [Google Scholar]
  32. Heyman J. A., Monosov E., Subramani S. Role of the PAS1 gene of Pichia pastoris in peroxisome biogenesis. J Cell Biol. 1994 Dec;127(5):1259–1273. doi: 10.1083/jcb.127.5.1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hoffman C. S., Winston F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene. 1987;57(2-3):267–272. doi: 10.1016/0378-1119(87)90131-4. [DOI] [PubMed] [Google Scholar]
  34. Höhfeld J., Veenhuis M., Kunau W. H. PAS3, a Saccharomyces cerevisiae gene encoding a peroxisomal integral membrane protein essential for peroxisome biogenesis. J Cell Biol. 1991 Sep;114(6):1167–1178. doi: 10.1083/jcb.114.6.1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Imanaka T., Small G. M., Lazarow P. B. Translocation of acyl-CoA oxidase into peroxisomes requires ATP hydrolysis but not a membrane potential. J Cell Biol. 1987 Dec;105(6 Pt 2):2915–2922. doi: 10.1083/jcb.105.6.2915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Keller G. A., Krisans S., Gould S. J., Sommer J. M., Wang C. C., Schliebs W., Kunau W., Brody S., Subramani S. Evolutionary conservation of a microbody targeting signal that targets proteins to peroxisomes, glyoxysomes, and glycosomes. J Cell Biol. 1991 Sep;114(5):893–904. doi: 10.1083/jcb.114.5.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kunau W. H., Beyer A., Franken T., Götte K., Marzioch M., Saidowsky J., Skaletz-Rorowski A., Wiebel F. F. Two complementary approaches to study peroxisome biogenesis in Saccharomyces cerevisiae: forward and reversed genetics. Biochimie. 1993;75(3-4):209–224. doi: 10.1016/0300-9084(93)90079-8. [DOI] [PubMed] [Google Scholar]
  38. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  39. Lazarow P. B., Fujiki Y. Biogenesis of peroxisomes. Annu Rev Cell Biol. 1985;1:489–530. doi: 10.1146/annurev.cb.01.110185.002421. [DOI] [PubMed] [Google Scholar]
  40. Lillie J. W., Loewenstein P. M., Green M. R., Green M. Functional domains of adenovirus type 5 E1a proteins. Cell. 1987 Sep 25;50(7):1091–1100. doi: 10.1016/0092-8674(87)90175-9. [DOI] [PubMed] [Google Scholar]
  41. Liu H., Tan X., Veenhuis M., McCollum D., Cregg J. M. An efficient screen for peroxisome-deficient mutants of Pichia pastoris. J Bacteriol. 1992 Aug;174(15):4943–4951. doi: 10.1128/jb.174.15.4943-4951.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lovering R., Hanson I. M., Borden K. L., Martin S., O'Reilly N. J., Evan G. I., Rahman D., Pappin D. J., Trowsdale J., Freemont P. S. Identification and preliminary characterization of a protein motif related to the zinc finger. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2112–2116. doi: 10.1073/pnas.90.6.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lüers G., Hashimoto T., Fahimi H. D., Völkl A. Biogenesis of peroxisomes: isolation and characterization of two distinct peroxisomal populations from normal and regenerating rat liver. J Cell Biol. 1993 Jun;121(6):1271–1280. doi: 10.1083/jcb.121.6.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Marzioch M., Erdmann R., Veenhuis M., Kunau W. H. 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. 1994 Oct 17;13(20):4908–4918. doi: 10.1002/j.1460-2075.1994.tb06818.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. McCammon M. T., McNew J. A., Willy P. J., Goodman J. M. An internal region of the peroxisomal membrane protein PMP47 is essential for sorting to peroxisomes. J Cell Biol. 1994 Mar;124(6):915–925. doi: 10.1083/jcb.124.6.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. McCollum D., Monosov E., Subramani S. 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. 1993 May;121(4):761–774. doi: 10.1083/jcb.121.4.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. McNew J. A., Goodman J. M. An oligomeric protein is imported into peroxisomes in vivo. J Cell Biol. 1994 Dec;127(5):1245–1257. doi: 10.1083/jcb.127.5.1245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Miura S., Kasuya-Arai I., Mori H., Miyazawa S., Osumi T., Hashimoto T., Fujiki Y. Carboxyl-terminal consensus Ser-Lys-Leu-related tripeptide of peroxisomal proteins functions in vitro as a minimal peroxisome-targeting signal. J Biol Chem. 1992 Jul 15;267(20):14405–14411. [PubMed] [Google Scholar]
  49. Motley A., Hettema E., Distel B., Tabak H. Differential protein import deficiencies in human peroxisome assembly disorders. J Cell Biol. 1994 May;125(4):755–767. doi: 10.1083/jcb.125.4.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Nelbach M. E., Pigiet V. P., Jr, Gerhart J. C., Schachman H. K. A role for zinc in the quaternary structure of aspartate transcarbamylase from Escherichia coli. Biochemistry. 1972 Feb 1;11(3):315–327. doi: 10.1021/bi00753a002. [DOI] [PubMed] [Google Scholar]
  51. Nuttley W. M., Brade A. M., Eitzen G. A., Veenhuis M., Aitchison J. D., Szilard R. K., Glover J. R., Rachubinski R. A. 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. 1994 Jan 7;269(1):556–566. [PubMed] [Google Scholar]
  52. Osumi T., Tsukamoto T., Hata S., Yokota S., Miura S., Fujiki Y., Hijikata M., Miyazawa S., Hashimoto T. Amino-terminal presequence of the precursor of peroxisomal 3-ketoacyl-CoA thiolase is a cleavable signal peptide for peroxisomal targeting. Biochem Biophys Res Commun. 1991 Dec 31;181(3):947–954. doi: 10.1016/0006-291x(91)92028-i. [DOI] [PubMed] [Google Scholar]
  53. PENNINGTON R. J. Biochemistry of dystrophic muscle. Mitochondrial succinate-tetrazolium reductase and adenosine triphosphatase. Biochem J. 1961 Sep;80:649–654. doi: 10.1042/bj0800649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Pan T., Giedroc D. P., Coleman J. E. 1H NMR studies of T4 gene 32 protein: effects of zinc removal and reconstitution. Biochemistry. 1989 Oct 31;28(22):8828–8832. doi: 10.1021/bi00448a022. [DOI] [PubMed] [Google Scholar]
  55. Patarca R., Fletcher M. A. Ring finger in the peroxisome assembly factor-1. FEBS Lett. 1992 Nov 2;312(1):1–2. doi: 10.1016/0014-5793(92)81397-5. [DOI] [PubMed] [Google Scholar]
  56. Peters T. J., Müller M., De Duve C. Lysosomes of the arterial wall. I. Isolation and subcellular fractionation of cells from normal rabbit aorta. J Exp Med. 1972 Nov 1;136(5):1117–1139. doi: 10.1084/jem.136.5.1117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Quest A. F., Bloomenthal J., Bardes E. S., Bell R. M. The regulatory domain of protein kinase C coordinates four atoms of zinc. J Biol Chem. 1992 May 15;267(14):10193–10197. [PubMed] [Google Scholar]
  58. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  59. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Santos M. J., Imanaka T., Shio H., Small G. M., Lazarow P. B. Peroxisomal membrane ghosts in Zellweger syndrome--aberrant organelle assembly. Science. 1988 Mar 25;239(4847):1536–1538. doi: 10.1126/science.3281254. [DOI] [PubMed] [Google Scholar]
  61. Shimozawa N., Tsukamoto T., Suzuki Y., Orii T., Shirayoshi Y., Mori T., Fujiki Y. A human gene responsible for Zellweger syndrome that affects peroxisome assembly. Science. 1992 Feb 28;255(5048):1132–1134. doi: 10.1126/science.1546315. [DOI] [PubMed] [Google Scholar]
  62. Slawecki M. L., Dodt G., Steinberg S., Moser A. B., Moser H. W., Gould S. J. Identification of three distinct peroxisomal protein import defects in patients with peroxisome biogenesis disorders. J Cell Sci. 1995 May;108(Pt 5):1817–1829. doi: 10.1242/jcs.108.5.1817. [DOI] [PubMed] [Google Scholar]
  63. Spong A. P., Subramani S. Cloning and characterization of PAS5: a gene required for peroxisome biogenesis in the methylotrophic yeast Pichia pastoris. J Cell Biol. 1993 Nov;123(3):535–548. doi: 10.1083/jcb.123.3.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. doi: 10.1016/0076-6879(90)85008-c. [DOI] [PubMed] [Google Scholar]
  65. Subramani S. Protein import into peroxisomes and biogenesis of the organelle. Annu Rev Cell Biol. 1993;9:445–478. doi: 10.1146/annurev.cb.09.110193.002305. [DOI] [PubMed] [Google Scholar]
  66. Swinkels B. W., Gould S. J., Bodnar A. G., Rachubinski R. A., Subramani S. A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase. EMBO J. 1991 Nov;10(11):3255–3262. doi: 10.1002/j.1460-2075.1991.tb04889.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Swinkels B. W., Gould S. J., Subramani S. Targeting efficiencies of various permutations of the consensus C-terminal tripeptide peroxisomal targeting signal. FEBS Lett. 1992 Jun 29;305(2):133–136. doi: 10.1016/0014-5793(92)80880-p. [DOI] [PubMed] [Google Scholar]
  68. Tan X., Waterham H. R., Veenhuis M., Cregg J. M. The Hansenula polymorpha PER8 gene encodes a novel peroxisomal integral membrane protein involved in proliferation. J Cell Biol. 1995 Feb;128(3):307–319. doi: 10.1083/jcb.128.3.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Thieringer R., Raetz C. R. Peroxisome-deficient Chinese hamster ovary cells with point mutations in peroxisome assembly factor-1. J Biol Chem. 1993 Jun 15;268(17):12631–12636. [PubMed] [Google Scholar]
  70. Tolbert N. E. Metabolic pathways in peroxisomes and glyoxysomes. Annu Rev Biochem. 1981;50:133–157. doi: 10.1146/annurev.bi.50.070181.001025. [DOI] [PubMed] [Google Scholar]
  71. Tsukamoto T., Miura S., Fujiki Y. Restoration by a 35K membrane protein of peroxisome assembly in a peroxisome-deficient mammalian cell mutant. Nature. 1991 Mar 7;350(6313):77–81. doi: 10.1038/350077a0. [DOI] [PubMed] [Google Scholar]
  72. Tsukamoto T., Shimozawa N., Fujiki Y. Peroxisome assembly factor 1: nonsense mutation in a peroxisome-deficient Chinese hamster ovary cell mutant and deletion analysis. Mol Cell Biol. 1994 Aug;14(8):5458–5465. doi: 10.1128/mcb.14.8.5458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Tuttle D. L., Lewin A. S., Dunn W. A., Jr Selective autophagy of peroxisomes in methylotrophic yeasts. Eur J Cell Biol. 1993 Apr;60(2):283–290. [PubMed] [Google Scholar]
  74. Van der Leij I., Franse M. M., Elgersma Y., Distel B., Tabak H. F. 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 U S A. 1993 Dec 15;90(24):11782–11786. doi: 10.1073/pnas.90.24.11782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Voorn-Brouwer T., van der Leij I., Hemrika W., Distel B., Tabak H. F. Sequence of the PAS8 gene, the product of which is essential for biogenesis of peroxisomes in Saccharomyces cerevisiae. Biochim Biophys Acta. 1993 Nov 16;1216(2):325–328. doi: 10.1016/0167-4781(93)90166-b. [DOI] [PubMed] [Google Scholar]
  76. Waterham H. R., Titorenko V. I., Haima P., Cregg J. M., Harder W., Veenhuis M. 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. 1994 Nov;127(3):737–749. doi: 10.1083/jcb.127.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Waterham H. R., Titorenko V. I., Swaving G. J., Harder W., Veenhuis M. Peroxisomes in the methylotrophic yeast Hansenula polymorpha do not necessarily derive from pre-existing organelles. EMBO J. 1993 Dec;12(12):4785–4794. doi: 10.1002/j.1460-2075.1993.tb06167.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Wendland M., Subramani S. Cytosol-dependent peroxisomal protein import in a permeabilized cell system. J Cell Biol. 1993 Feb;120(3):675–685. doi: 10.1083/jcb.120.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Wiebel F. F., Kunau W. H. The Pas2 protein essential for peroxisome biogenesis is related to ubiquitin-conjugating enzymes. Nature. 1992 Sep 3;359(6390):73–76. doi: 10.1038/359073a0. [DOI] [PubMed] [Google Scholar]
  80. van den Bosch H., Schutgens R. B., Wanders R. J., Tager J. M. Biochemistry of peroxisomes. Annu Rev Biochem. 1992;61:157–197. doi: 10.1146/annurev.bi.61.070192.001105. [DOI] [PubMed] [Google Scholar]

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