Pex5p stabilizes Pex14p: A study using a newly isolated pex5 CHO cell mutant, ZPEG101

Biochemical Journal

Volumn 449, Issue 1, 2013, Pages 195-207

  Natsuyama, Ryuichi ^a   Okumoto, Kanji ^a   Fujiki, Yukio ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Chinese hamster ovary cell mutant (CHO cell mutant); Matrix protein import; Peroxisome biogenesis; Peroxisome targeting signal type 1 (PTS1); Pex14p; PTS1 receptor (Pex5p)

Indexed keywords

CATALASE; PEROXISOME TARGETING SIGNAL TYPE 1 RECEPTOR; PEROXISOME TARGETING SIGNAL TYPE 2 RECEPTOR; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOGENESIS; CELL MEMBRANE; CELLULAR DISTRIBUTION; CHO CELL; CONTROLLED STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STABILITY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REPRESSOR PROTEINS;

CRICETULUS GRISEUS;

EID: 84870936161     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120911     Document Type: Article

References (50)

1. Wanders, R. J. A. and Waterham, H. R. (2006) Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75, 295-332 (Pubitemid 44118035)
2. Fujiki, Y., Okumoto, K., Kinoshita, N. and Ghaedi, K. (2006) Lessons from peroxisome-deficient Chinese hamster ovary (CHO) cell mutants. Biochim. Biophys. Acta 1763, 1374-1381 (Pubitemid 44883391)
3. Steinberg, S. J., Dodt, G., Raymond, G. V., Braverman, N. E., Moser, A. B. and Moser, H. W. (2006) Peroxisome biogenesis disorders. Biochim. Biophys. Acta 1763, 1733-1748 (Pubitemid 44880484)
4. Platta, H. W. and Erdmann, R. (2007) The peroxisomal protein import machinery. FEBS Lett. 581, 2811-2819 (Pubitemid 46874385)
5. Gould, S. J., Keller, G.-A., Hosken, N., Wilkinson, J. and Subramani, S. (1989) A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108, 1657-1664 (Pubitemid 19130498)
6. Miyazawa, S., Osumi, T., Hashimoto, T., Ohno, K., Miura, S. and Fujiki, Y. (1989) Peroxisome targeting signal of rat liver acyl-coenzyme A oxidase resides at the carboxy terminus. Mol. Cell. Biol. 9, 83-91 (Pubitemid 19024781)
7. Swinkels, B. W., Gould, S. J., Bodnar, A. G., Rachubinski, R. A. and Subramani, S. (1991) A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase. EMBO J. 10, 3255-3262 (Pubitemid 21905350)
8. Osumi, T., Tsukamoto, T., Hata, S., Yokota, S., Miura, S., Fujiki, Y., Hijikata, M., Miyazawa, S. and Hashimoto, T. (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
9. Dodt, G., Braverman, N., Wong, C. S., Moser, A., Moser, H. W., Watkins, P., Valle, D. and Gould, S. J. (1995) Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nat. Genet. 9, 115-125
10. Otera, H., Okumoto, K., Tateishi, K., Ikoma, Y., Matsuda, E., Nishimura, M., Tsukamoto, T., Osumi, T., Ohashi, K., Higuchi, O. and Fujiki, Y. (1998) Peroxisome targeting signal type 1 (PTS1) receptor is involved in import of both PTS1 and PTS2: studies with PEX5-defective CHO cell mutants. Mol. Cell. Biol. 18, 388-399 (Pubitemid 28021050)
11. Saidowsky, J., Dodt, G., Kirchberg, K., Wegner, A., Nastainczyk, W., Kunau, W.-H. and Schliebs, W. (2001) The di-aromatic pentapeptide repeats of the human peroxisome import receptor PEX5 are separate high affinity binding sites for the peroxisomal membrane protein PEX14. J. Biol. Chem. 276, 34524-34529
12. Otera, H., Setoguchi, K., Hamasaki, M., Kumashiro, T., Shimizu, N. and Fujiki, Y. (2002) Peroxisomal targeting signal receptor Pex5p interacts with cargoes and import machinery components in a spatiotemporally differentiated manner: conserved Pex5p WXXXF/Y motifs are critical for matrix protein import. Mol. Cell. Biol. 22, 1639-1655 (Pubitemid 34174982)
13. Otera, H., Harano, T., Honsho, M., Ghaedi, K., Mukai, S., Tanaka, A., Kawai, A., Shimizu, N. and Fujiki, Y. (2000) The mammalian peroxin Pex5pL, the longer isoform of the mobile PTS1-transporter, translocates Pex7p-PTS2 protein complex into peroxisomes via its initial docking site, Pex14p. J. Biol. Chem. 275, 21703-21714 (Pubitemid 30481879)
14. Matsumura, T., Otera, H. and Fujiki, Y. (2000) Disruption of interaction of the longer isoform of Pex5p, Pex5pL, with Pex7p abolishes the PTS2 protein import in mammals: study with a novel PEX5-impaired Chinese hamster ovary cell mutant. J. Biol. Chem. 275, 21715-21721 (Pubitemid 30481880)
15. Mukai, S. and Fujiki, Y. (2006) Molecular mechanisms of import of peroxisome-targeting signal type 2 (PTS2) proteins by PTS2 receptor Pex7p and PTS1 receptor Pex5pL. J. Biol. Chem. 281, 37311-37320 (Pubitemid 46042035)
16. Agne, B., Meindl, N. M., Niederhoff, K., Einwaechter, H., Rehling, P., Sickmann, A., Meyer, H. E., Girzalsky, W. and Kunau, W.-H. (2003) Pex8p: an intraperoxisomal organizer of the peroxisomal import machinery. Mol. Cell. 11, 635-646 (Pubitemid 36385119)
17. Platta, H. W., Grunau, S., Rosenkranz, K., Girzalsky, W. and Erdmann, R. (2005) Functional role of the AAA peroxins in dislocation of the cycling PTS1 receptor back to the cytosol. Nat. Cell Biol. 7, 817-822 (Pubitemid 41079054)
18. Miyata, N. and Fujiki, Y. (2005) Shuttling mechanism of peroxisome targeting signal type 1 receptor, Pex5: ATP-independent import and ATP-dependent export. Mol. Cell. Biol. 25, 10822-10832 (Pubitemid 41747127)
19. Tsukamoto, T., Yokota, S. and Fujiki, Y. (1990) Isolation and characterization of Chinese hamster ovary cell mutants defective in assembly of peroxisomes. J. Cell Biol. 110, 651-660
20. Toyama, R., Mukai, S., Itagaki, A., Tamura, S., Shimozawa, N., Suzuki, Y., Kondo, N., Wanders, R. J. A. and Fujiki, Y. (1999) Isolation, characterization, and mutation analysis of PEX13-defective Chinese hamster ovary cell mutants. Hum. Mol. Genet. 8, 1673-1681 (Pubitemid 29423876)
21. Shimizu, N., Itoh, R., Hirono, Y., Otera, H., Ghaedi, K., Tateishi, K., Tamura, S., Okumoto, K., Harano, T., Mukai, S. and Fujiki, Y. (1999) The peroxin Pex14p: cDNA cloning by functional complementation on a Chinese hamster ovary cell mutant, characterization, and functional analysis. J. Biol. Chem. 274, 12593-12604
22. Kawajiri, K., Harano, T. and Omura, T. (1977) Biogenesis of the mitochondrial matrix enzyme, glutamate dehydrogenase, in rat liver cells. I. Subcellular localization, biosynthesis, and intracellular translocation of glutamate dehydrogenase. J. Biochem. 82, 1403-1416 (Pubitemid 8221883)
23. Okumoto, K., Abe, I. and Fujiki, Y. (2000) Molecular anatomy of the peroxin Pex12p: RING finger domain is essential for Pex12p function and interacts with the peroxisome targeting signal type 1-receptor Pex5p and a RING peroxin, Pex10p. J. Biol. Chem. 275, 25700-25710
24. Tsukamoto, T., Bogaki, A., Okumoto, K., Tateishi, K., Fujiki, Y., Shimozawa, N., Suzuki, Y., Kondo, N. and Osumi, T. (1997) Isolation of a new peroxisome deficient CHO cell mutant defective in peroxisome targeting signal-1 receptor. Biochem. Biophys. Res. Commun. 230, 402-406 (Pubitemid 27212010)
25. Tamura, S., Okumoto, K., Toyama, R., Shimozawa, N., Tsukamoto, T., Suzuki, Y., Osumi, T., Kondo, N. and Fujiki, Y. (1998) 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. U.S.A. 95, 4350-4355 (Pubitemid 28207915)
26. Ghaedi, K. and Fujiki, Y. (2008) A new method for isolation of CHO cell mutants defective in peroxisome assembly, using ICR191 as a potent mutagenic agent. Cell. Biochem. Funct. 26, 684-691
27. Okumoto, K., Misono, S., Miyata, N., Matsumoto, Y., Mukai, S. and Fujiki, Y. (2011) Cysteine ubiquitination of PTS1-receptor Pex5p regulates Pex5p recycling. Traffic 12, 1067-1083
28. Vercesi, A. E., Bernardes, C. F., Hoffmann, M. E., Gadelha, F. R. and Docampo, R. (1991) Digitonin permeabilization does not affect mitochondrial function and allows the determination of the mitochondrial membrane potential of Trypanosoma cruzi in situ. J. Biol. Chem. 266, 14431-14434 (Pubitemid 21907520)
29. Morand, O. H., Allen, L.-A. H., Zoeller, R. A. and Raetz, C. R. H. (1990) A rapid selection for animal cell mutants with defective peroxisomes. Biochim. Biophys. Acta 1034, 132-141 (Pubitemid 20157817)
30. Fujiki, Y., Matsuzono, Y., Matsuzaki, T. and Fransen, M. (2006) Import of peroxisomal membrane proteins: the interplay of Pex3p- and Pex19p-mediated interactions. Biochim. Biophys. Acta 1763, 1639-1646 (Pubitemid 44880487)
31. Fujiki, Y., Yagita, Y. and Matsuzaki, T. (2012) Peroxisome biogenesis disorders: molecular basis for impaired peroxisomal membrane assembly in metabolic functions and biogenesis of peroxisomes in health and disease. Biochim. Biophys. Acta 1822, 1337-1342
32. Gouveia, A. M. M., Reguenga, C., Oliveira, M. E. M., Sá-Miranda, C. and Azevedo, J. E. (2000) Characterization of peroxisomal Pex5p from rat liver. Pex5p in the Pex5p-Pex14p membrane complex is a transmembrane protein. J. Biol. Chem. 275, 32444-32451
33. Reguenga, C., Oliveira, M. E. M., Gouveia, A. M. M., Sá-Miranda, C. and Azevedo, J. E. (2001) Characterization of the mammalian peroxisomal import machinery: Pex2p, Pex5p, Pex12p, and Pex14p are subunits of the same protein assembly. J. Biol. Chem. 276, 29935-29942
34. Su, J. R., Takeda, K., Tamura, S., Fujiki, Y. and Miki, K. (2009) Crystal structure of the conserved N-terminal domain of the peroxisomal matrix-protein-import receptor, Pex14p. Proc. Natl. Acad. Sci. U.S.A. 106, 417-421
35. Honsho, M., Hashiguchi, Y., Ghaedi, K. and Fujiki, Y. (2011) Interaction defect of the medium isoform of PTS1-receptor Pex5p with PTS2-receptor Pex7p abrogates the PTS2 protein import into peroxisomes in mammals. J. Biochem. 149, 203-210
36. Baes, M., Gressens, P., Baumgart, E., Carmeliet, P., Casteels, M., Fransen, M., Evrard, P., Fahimi, D., Declercq, P. E., Collen, D. et al. (1997) A mouse model for Zellweger syndrome. Nat. Genet. 17, 49-57 (Pubitemid 27377531)
37. Stanley, W. A. and Wilmanns, M. (2006) Dynamic architecture of the peroxisomal import receptor Pex5p. Biochim. Biophys. Acta 1763, 1592-1598
38. Girzalsky, W., Rehling, P., Stein, K., Kipper, J., Blank, L., Kunau, W.-H. and Erdmann, R. (1999) Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J. Cell Biol. 144, 1151-1162 (Pubitemid 29157295)
39. Kerssen, D., Hambruch, E., Klaas, W., Platta, H. W., de Kruijff, B., Erdmann, R., Kunau, W.-H. and Schliebs, W. (2006) Membrane association of the cycling peroxisome import receptor Pex5p. J. Biol. Chem. 281, 27003-27015 (Pubitemid 44401729)
40. Niederhoff, K., Meindl-Beinker, N. M., Kerssen, D., Perband, U., Schaefer, A., Schliebs, W. and Kunau, W.-H. (2005) Yeast Pex14p possesses two functionally distinct Pex5p and one Pex7p binding sites. J. Biol. Chem. 280, 35571-35578 (Pubitemid 41532749)
41. Williams, C., van den Berg, M. and Distel, B. (2005) Saccharomyces cerevisiae Pex14p contains two independent Pex5p binding sites, which are both essential for PTS1 protein import. FEBS Lett. 579, 3416-3420 (Pubitemid 40800291)
42. Freitas, M. O., Francisco, T., Rodrigues, T. A., Alencastre, I. S., Pinto, M. P., Grou, C. P., Carvalho, A. F., Fransen, M., Sá-Miranda, C. and Azevedo, J. E. (2011) PEX5 protein binds monomeric catalase blocking its tetramerization and releases it upon binding the N-terminal domain of PEX14. J. Biol. Chem. 286, 40509-40519
43. Itoh, R. and Fujiki, Y. (2006) Functional domains and dynamic assembly of the peroxin Pex14p, the entry site of matrix proteins. J. Biol. Chem. 281, 10196-10205 (Pubitemid 43864556)
44. Meinecke, M., Cizmowski, C., Schliebs, W., Krüger, V., Beck, S., Wagner, R. and Erdmann, R. (2010) The peroxisomal importomer constitutes a large and highly dynamic pore. Nat. Cell Biol. 12, 273-277
45. Schliebs, W., Saidowsky, J., Angianian, B., Dodt, G., Herberg, F. W. and Kunau, W.-H. (1999) Recombinant human peroxisomal targeting signal receptor PEX5. Structural basis for interaction of PEX5 with PEX14. J. Biol. Chem. 274, 5666-5673 (Pubitemid 29109219)
46. Miyata, N., Hosoi, K., Mukai, S. and Fujiki, Y. (2009) In vitro import of peroxisome-targeting signal 2 (PTS2) receptor Pex7p into peroxisomes. Biochim. Biophys. Acta 1793, 860-870
47. Bottger, G., Barnett, P., Klein, A. T. J., Kragt, A., Tabak, H. F. and Distel, B. (2000) Saccharomyces cerevisiae PTS1 receptor Pex5p interacts with the SH3 domain of the peroxisomal membrane protein Pex13p in an unconventional, non-PXXP-related manner. Mol. Biol. Cell 11, 3963-3976
48. Barnett, P., Bottger, G., Klein, A. T. J., Tabak, H. F. and Distel, B. (2000) The peroxisomal membrane protein Pex13p shows a novel mode of SH3 interaction. EMBO J. 19, 6382-6391
49. Gould, S. J., Kalish, J. E., Morrell, J. C., Bjorkman, J., Urquhart, A. J. and Crane, D. I. (1996) Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cytoplasmic PTS1 receptor. J. Cell Biol. 135, 85-95 (Pubitemid 26337739)
50. Wolf, J., Schliebs, W. and Erdmann, R. (2010) Peroxisomes as dynamic organelles: peroxisomal matrix protein import. FEBS J. 277, 3268-3278