Identification and characterization of the human peroxin PEX3

European Journal of Cell Biology

Volumn 78, Issue 6, 1999, Pages 357-374

  Soukupova, Monika ^a   Sprenger, Christiane ^a   Gorgas, Karin ^a   Kunau, Wolf H ^b   Dodt, Gabriele ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Membrane targeting signal; Peroxisome biogenesis; Peroxisome biogenesis disorders

Indexed keywords

AMINO ACID; COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN;

ARTICLE; BIOGENESIS; CELL MEMBRANE; CYTOPLASM; EXPRESSED SEQUENCE TAG; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MITOCHONDRION; MOLECULAR CLONING; MOLECULAR WEIGHT; PEROXISOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; YEAST;

MAMMALIA;

EID: 0032979799     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0171-9335(99)80078-8     Document Type: Article

References (76)

1. Allison, D. S., G. Schatz: Artificial mitochondrial presequences. Proc. Natl. Acad. Sci. USA 83, 9011-9015 (1986).
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, D. J. Lipman: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997).
3. Baerends, R. J., F. A. Salomons, K. N. Faber, J. A. Kiel, I. J. Van der Klei, M. Veenhuis: Deviant Pex3p levels affect normal peroxisome formation in Hansenula polymorpha: high steady-state levels of the protein fully abolish matrix protein import. Yeast 13, 1437-1448 (1997).
4. Baerends, R. J., F. A. Salomons, J. A. Kiel, I. J. van der Klei, M. Veenhuis: Deviant Pex3p levels affect normal peroxisome formation in Hansenula polymorpha: a sharp increase of the protein level induces the proliferation of numerous, small protein-import competent peroxisomes. Yeast 13, 1449-1463 (1997).
5. Baerends, R. J. S., S. W. Rasmussen, R. E. Hilbrands, M. van der Heide, K. N. Faber, P. T. W. Reuvekamp, J. A. K. W. Kiel, J. M. Cregg, I. J. van der Klei, M. Veenhuis: The Hansenula polymorpha PER9 gene encodes a peroxisomal membrane protein essential for peroxisome assembly and integrity. J. Biol. Chem. 271, 8887-8894 (1996).
6. Braun, A., S. Kammerer, W. Weissenhorn, E. H. Weis, H. Cleve: Sequence of a putative human housekeeping gene (HK33) localized on chromosome 1. Gene 146, 291-295 (1994).
7. Braverman, N., G. Steel, C. Obie, A. Moser, H. Moser, S. J. Gould, D. Valle: Human PEX7 encodes the peroxisomal PTS2 receptor and is responsible for rhizomelic chondrodysplasia punctata. Nature Genet. 15, 369-376 (1997).
8. Chang, C.-C., S. J. Gould: Phenotype-genotype relationships in complementation group 3 of the peroxisome-biogenesis disorders. Am. J. Hum. Genet. 63, 1294-1306 (1998).
9. Chang, C. C., W. H. Lee, H. Moser, D. Valle, S. J. Gould: Isolation of the human PEX12 gene, mutated in group 3 of the peroxisome biogenesis disorders. Nature Genet. 15, 385-388 (1997).
10. De Hoop, M. J., G. Ab: Import of proteins into peroxisomes and other microbodies. Biochem. J. 286, 657-669 (1992).
11. Diestelkötter, P., W. W. Just: In vitro insertion of the 22-kD peroxisomal membrane protein into isolated rat liver peroxisomes. J. Cell Biol. 123, 1717-1725 (1993).
12. Dodt, G., N. Braverman, D. Valle, S. J. Gould: From expressed sequence tags to peroxisome biogenesis disorder genes. Ann. N. Y. Acad. Sci. 804, 516-523 (1996).
13. Dodt, G., N. Braverman, C. Wong, A. Moser, H. W. Moser, P. Watkins, D. Valle, S. J. Gould: Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nature Genet. 9, 115-125 (1995).
14. Dodt, G., S. J. Gould: 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 (1996).
15. Dyer, J. M., J. A. McNew, J. M. Goodman: The sorting sequence of the peroxisomal integral membrane protein PMP47 is contained within a short hydrophilic loop. J. Cell Biol. 133, 269-280 (1996).
16. Elgersma, Y., L. Kwast, A. Klein, T. Voorn-Brouwer, M. van den Berg, B. Metzig, T. America, H. F. Tabak, B. Distel: 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 (1996).
17. Elgersma, Y., L. Kwast, M. van den Berg, W. B. Snyder, B. Distel, S. Subramani, H. F. Tabak: Overexpression of Pex15p, a phosphorylated peroxisomal integral membrane protein required for peroxisome assembly in S. cerevisiae, causes proliferation of the endoplasmic reticulum membrane. EMBO J. 16, 7326-7341 (1997).
18. Erdmann, R., G. Blobel: Identification of a peroxisomal membrane receptor for the C-terminal tripeptide signal recognition factor. J. Cell Biol. 135, 111-121 (1996).
19. Erdmann, R., M. Veenhuis, W-H. Kunau: Peroxisomes: organelles at the crossroads. Trends Cell Biol. 7, 400-407 (1997).
20. Evan, G. I., G. K. Lewis, G. Ramsay, J. M. Bishop: Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5, 3610-3616 (1985).
21. Faber, K. N., J. A. Heyman, S. Subramani: Two AAA family peroxins, PpPex1p and PpPex6p, interact with each other in an ATP-dependent manner and are associated with different subcellular membranous structures distinct from peroxisomes. Mol. Cell. Biol. 18, 936-943 (1998).
22. Fahimi, H. D., E. Baumgart, A. Völkl: Ultrastructural aspects of the biogenesis of peroxisomes in rat liver. Biochimie 75, 201-208 (1993).
23. Fransen, M., C. Brees, E. Baumgart, J. C. T. Vanhooren, M. Baes, G. Mannaerts, P. P. van Veldhoven: Identification and characterization of the putative human peroxisomal C-terminal targeting signal import receptor. J. Biol. Chem. 270, 7731-7736 (1995).
24. Fransen, M., S. R. Terlecky, S. Subramani: Identification of a human PTS1 receptor docking protein directly required for peroxisomal protein import. Proc. Natl. Acad. Sci. USA 95, 8087-8092 (1998).
25. Fukuda, S., N. Shimozawa, Y. Suzuki, Z. Zhang, S. Tomatsu, T. Tsukamoto, N. Hashiguchi, T. Osumi, M. Masuno, K. Imaizumi, Y. Kuroki, Y. Fujiki, T. Orii, N. Kondo: Human peroxisome assembly factor-2 (PAF-2): a gene responsible for group C peroxisome biogenesis disorder in humans. Am. J. Hum. Genet. 59, 1210-1220 (1996).
26. Gorgas, K.: Serial section analysis of mouse hepatic peroxisomes. Anat. Embryol. 172, 21-32 (1985).
27. Götte, K., W. Girzalsky, M. Linkert, E. Baumgart, S. Kammerer, W.-H. Kunau, R. Erdmann: Pex19p, a farnesylated protein essential for peroxisome biogenesis. Mol. Cell. Biol. 18, 616-628 (1998).
28. Gould, S. J., J. E. Kalish, J. E. Morrell, J. Bjorkman, A. J. Urquhart, D. I. Crane: An SH3 protein in the peroxisome membrane is a docking factor for the PTS1 receptor. J. Cell Biol. 135, 85-95 (1996).
29. Gould, S. J., G. A. Keller, N. Hosken, J. Wilkinson, S. Subramani: A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108, 1657-1664 (1989).
30. Höhfeld, J., M. Veenhuis, W.-H. Kunau: PAS3, a Saccharomyces cerevisiae gene encoding a peroxisomal integral membrane protein essential for peroxisome biogenesis. J. Cell Biol. 114, 1167-1178 (1991).
31. Imanaka, T., Y. Shiina, T. Takano, T. Hashimoto, T. Osumi: Insertion of the 70-kDa peroxisomal membrane protein into peroxisomal membranes in vivo and in vitro. J. Biol. Chem. 271, 3706-3713 (1996).
32. James, G. L., J. L. Goldstein, R. K. Pathak, R. G. W. Anderson, M. S. Brown: PxF, a prenylated protein of peroxisomes. J. Biol. Chem. 269, 14182-14190 (1994).
33. Just, W. W., P. Diestelkötter: Protein insertion into the peroxisomal membrane. Ann. NY Acad. Sci. 804, 60-75 (1996).
34. Kammerer, S., N. Arnold, W. Gutensohn, H. W. Mewes, W. H. Kunau, G. Hofler, A. A. Roscher, A. Braun: Genomic organization and molecular characterization of a gene encoding HsPXF, a human peroxisomal farnesylated protein. Genomics 45, 200-210 (1997).
35. Kammerer, S., A. Holzinger, U. Welsch, A. A. Roscher: Cloning and characterization of the gene encoding the human peroxisomal assembly protein Pex3p. FEBS Lett. 429, 53-60 (1998).
36. Krause, T.: Investigation on membrane proteins of Saccharomyces cerevisiae with the focus on Pas3p. PhD thesis, Bochum, Germany (1995).
37. Kunau, W.-H., R. Erdmann: Peroxisome biogenesis: Back to the endoplasmic reticulum? Curr. Biol. 8, R299-R302 (1998).
38. Kyte, J., R. F. Doolittle: A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132 (1982).
39. Lazarow, P. B., Y. Fujiki: Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1, 489-530 (1985).
40. Luo, Y., A. Batalao, H. Zhou, L. Zhu: Mammalian two-hybrid system: a complementary approach to the yeast two-hybrid system. Biotechniques 22, 350-352 (1997).
41. Moser, A. B., M. Rasmussen, S. Naidu, P. A. Watkins, M. McGuinness, A. K. Hajra, G. Chen, G. Raymond, A. Liu, D. Gordon, K. Garnaas, D. S. Walton, O. H. Okjeldal, M. A. Guggenheim, L. G. Jackson, E. R. Elias, H. W. Moser: Phenotype of patients with peroxisomal disorders subdivided into sixteen complementation groups. J. Pediatr. 127, 13-22 (1995).
42. Motley, A. M., E. H. Hettema, E. M. Hogenhout, P. Brites, A. L. ten Asbroek, F. A. Wijburg, F. Baas, H. S. Heijmans, H. F. Tabak, R. J. Wanders, B. Distel: Rhizomelic chondrodysplasia punctata is a peroxisomal protein targeting disease caused by a non-functional PTS2 receptor. Nature Genet. 15, 377-380 (1997).
43. Okumoto, K., Y. Fujiki: PEX12 encodes an integral membrane protein of peroxisomes. Nature Genet. 17, 265-266 (1997).
44. Okumoto, K., R. Itoh, N. Shimozawa, Y. Suzuki, S. Tamura, N. Kondo, Y. Fujiki: Mutations in PEX10 is the cause of Zellweger peroxisome deficiency syndrome of complementation group B. Hum. Mol. Genet. 7, 1399-1405 (1998).
45. Osumi, T., T. Tsukamoto, S. Hata, S. Yokota, S. Miura, Y. Fujiki, M. Hijikata, S. Miyazawa, T. Hashimoto: 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 (1991).
46. Passreiter, M., M. Anton, D. Lay, R. Frank, C. Harter, F. T. Wieland, K. Gorgas, W. W. Just: Peroxisome biogenesis: involvement of ARF and coatomer. J. Cell Biol. 141, 373-383 (1998).
47. Persson, B., P. Argos: Prediction of transmembrane segments in proteins utilizing multiple sequence alignments. J. Mol. Biol. 237, 182-192 (1994).
48. Portsteffen, H., A. Beyer, E. Becker, C. Epplen, A. Pawlak, W.-H. Kunau, G. Dodt: Human PEX1 is mutated in complementation group 1 of the peroxisome biogenesis disorders. Nature Genet. 17, 449-452 (1997).
49. Poulos, A., J. Christodoulou, C. W. Chow, J. Goldblatt, B. C. Paton, T. Orii, Y. Suzuki, N. Shimozawa: Peroxisomal assembly defects: clinical, pathologic, and biochemical findings in two patients in a newly identified complementation group. J. Pediatr. 127, 596-599 (1995).
50. Purdue, P. E., J. W. Zhang, M. Skoneczny, P. B. Lazarow: Rhizomelic chondrodysplasia punctata is caused by deficiency of human PEX7, a homologue of the yeast PTS2 receptor. Nature Genet. 15, 381-384 (1997).
51. Reuber, B. E., E. Germain-Lee, C. S. Collins, J. C. Morrell, R. Ameritunga, H. W. Moser, D. Valle, S. J. Gould: Mutations in PEX1 are the most common cause of peroxisome biogenesis disorders. Nature Genet. 17, 445-448 (1997).
52. Roise, D.: Interaction of a synthetic mitochondrial presequence with isolated yeast mitochondria: mechanism of binding and kinetics of import. Proc. Natl. Acad. Sci. USA 89, 608-612 (1992).
53. Roise, D., S. J. Horvath, J. M. Tomich, J. H. Richards, G. Schatz: A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO J. 5, 1327-1334 (1986).
54. Roise, D., F. Theiler, S. J. Horvath, J. M. Tomich, J. H. Richard, D. S. Allison, G. Schatz: Amphiphilicity is essential for mitochondrial presequence function. EMBO J. 7, 649-653 (1988).
55. Rost, B., R. Casadio, P. Fariselli, C. Sander: Prediction of helical transmembrane segments at 95% accuracy. Protein Sci. 4, 521-533 (1995).
56. Shani, N., G. Steel, M. Dean, D. Valle: Identification of a fourth half ABC transporter in the human peroxisomal membrane. Hum. Mol. Genet. 6, 1925-1931 (1997).
57. Shimozawa, N., Y. Suzuki, T. Orii, A. Moser, H. Moser, R. Wanders: Standardization of complementation grouping of peroxisome-deficient disorders and the second Zellweger patient with peroxisomal assembly factor-1 (PAF-1) defect. Am. J. Hum. Genet. 52, 843-844 (1993).
58. Shimozawa, N., Y. Suzuki, S. Tomatsu, H. Nakamura, T. Kono, H. Takada, T. Tsukamoto, Y. Fujiki, T. Orii, N. Kondo: A novel mutation, R125X in peroxisome assembly factor-1 responsible for Zellweger syndrome. Hum. Mutat. 1, 134-136 (1998).
59. Shimozawa, N., T. Tsukamoto, Y. Suzuki, T. Orii, Y. Shirayoshi, T. Mori, Y. Fujiki: A human gene responsible for Zellweger syndrome that affects peroxisome assembly. Science 255, 1132-1134 (1992).
60. Slawecki, M. L., G. Dodt, S. Steinberg, A. B. Moser, H. Moser, S. J. Gould: Identification of three distinct peroxisomal protein import defects in patients with peroxisome biogenesis disorders. J. Cell Sci. 108, 1817-1829 (1995).
61. Subramani, S.: Components involved in peroxisome import, biogenesis, proliferation, turnover, and movement. Physiol. Rev. 78, 171-188 (1998).
62. Swinkels, B. W., S. J. Gould, A. G. Bodnar, R. A. Rachubinski, S. Subramani: A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase. EMBO J. 10, 3255-3262 (1991).
63. Tamura, S., K. Okumoto, R. Toyama, N. Shimozawa, T. Tsukamoto, Y. Suzuki, T. Osumi, N. Kondo, Y. Fujiki: Human PEX1 cloned by functional complementation on a CHO cell mutant is responsible for peroxisome-deficient Zellweger syndrome of complementation group I. Proc. Natl. Acad. Sci. USA95, 4350-4355 (1998).
64. Tateishi, K., K. Okumoto, N. Shimozawa, T. Tsukamoto, T. Osumi, Y. Suzuki, N. Kondo, I. Okano, Y. Fujiki: Newly identified Chinese hamster ovary cell mutants defective in peroxisome biogenesis represent two novel complementation groups in mammals. Eur. J. Cell Biol. 73, 352-359 (1997).
65. Titorenko, V. I., D. M. Ogrydriak, R. A. Rachubinski: Four distinct secretory pathways serve protein secretion, cell surface growth, and peroxisome biogenesis in the yeast Yarrowia lipolytica. Mol. Cell. Biol. 17, 5210-5226 (1997).
66. Titorenko, V. I., R. A. Rachubinsky: Mutants of the yeast Yarrowia lipolytica defective in protein exit from the endoplasmatic reticulum are also defective in peroxisome biogenesis. Mol. Cell. Biol. 18, 2789-2803 (1998).
67. Van der Klei, I. J., M. Veenhuis: Peroxisome biogenesis in the yeast Hansenula polymorpha: a structural and functional analysis. Ann. N Y Acad. Sci. 804, 47-59 (1996).
68. Von Heijne, G.: Mitochondrial targeting sequences may form amphiphilic helices. EMBO J. 5, 1335-1342 (1986).
69. Warren, D. S., J. C. Morrell, H. W. Moser, D. Valle, S. J. Gould: Identification of PEX10, the gene defective in complementation group 7 of the peroxisome-biogenesis disorders. Am J. Hum. Genet. 63, 347-359 (1998).
70. Waterham, H. R., J. M. Cregg: Peroxisome biogenesis. Bioessays 19, 57-66 (1997).
71. Waterham, H. R., V. I. Titorenko, G. J. Swaving, W. Harder, M. Veenhuis: Peroxisomes in the methylotrophic yeast Hansenula polymorpha do not necessarily derive from pre-existing organelles. EMBO J. 12, 4785-4794 (1993).
72. Wiemer, E. A. C., G. H. Lüers, K. N. Faber, T. Wenzel, M. Veenhuis, S. Subramani: 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 (1996).
73. Wiemer, E. A. C., W. M. Nuttley, B. L. Bertolaet, X. Li, U. Francke, M. J. Wheelock, U. K. Anné, K. R. Johnson, S. Subramani: Human peroxisomal targeting signal-1 receptor restores peroxisomal protein import in cells from patients with fatal peroxisomal disorders. J. Cell Biol. 130, 51-65 (1995).
74. Will, G. K., M. Soukupova, X. Hong, K. S. Erdmann, J. A. K. W. Kiel, G. Dodt, W. H. Kunau, R. Erdmann: Identification and characterization of the human orthologue of yeast Pex14p. Mol. Cell. Biol. 19, 2265-2277 (1999).
75. Wright, R., M. Basson, L. D'Ari, J. Rine: Increased amounts of HMG-CoA reductase induce "karmellae": a proliferation of stacked membrane pairs surrounding the yeast nucleus. J. Cell Biol. 107, 101-114 (1988).
76. Yahraus, T., N. Braverman, G. Dodt, J. E. Kalish, J. C. Morell, H. W. Moser, D. Valle, S. J. Gould: The peroxisome biogenesis disorder group 4 gene, PXAAA1, encodes a cytoplasmic ATPase required for stability of the PTS1 receptor. EMBO J. 15, 2914-2923 (1996).