Shuttles and cycles: transport of proteins into the peroxisome matrix (Review)

References

• Cavalier-Smith T. The simultaneous symbiotic origin of mitochondria, chloroplasts and microbodies. Ann NY Acad Sci 1987; 503: 55–71
   PubMed Web of Science ®Google Scholar
• Wanders RJA. Metabolic and molecular basis of peroxisomal disorders: A review. Am J Med Genetics Part A 2004; 126A: 355–375
   Google Scholar
• Baker A, Sparkes IA. Peroxisome protein import: some answers, more questions. Curr Opin Plant Biol 2005; 8: 640–647
   PubMed Web of Science ®Google Scholar
• Hayashi M, Nishimura M. Arabidopsis thaliana – a model organism to study plant peroxisomes. Biochimica et Biophysica Acta-Molec Cell Res 2006; 1763: 1382–1391
   Google Scholar
• Veenhuis M. Peroxisome biogenesis and function in Hansenula polymorpha. Cell Biochem Funct 1992; 10: 175–184
   PubMedGoogle Scholar
• Debellis L, Tsugeki R, Nishimura M. Glyoxylate cycle enzymes in peroxisomes isolated from petals of pumpkin (Cucurbita Sp.) during senescence. Plant Cell Physiol 1991; 32: 1227–1235
   Google Scholar
• Debellis L, Nishimura M. Development of enzymes of the glyoxylate cycle during senescence of pumpkin cotyledons. Plant Cell Physiol 1991; 32: 555–561
   Google Scholar
• Titus DE, Becker WM. Investigation of the glyoxysome peroxisome transition in germinating cucumber cotyledons using double-label immunoelectron microscopy. J Cell Biol 1985; 101: 1288–1299
   PubMedGoogle Scholar
• Nishimura M, Yamaguchi J, Mori H, Akazawa T, Yokota S. Analytical studies on microbody transition. 5. Immunocytochemical analysis shows that glyoxysomes are directly transformed to leaf peroxisomes during greening of pumpkin cotyledons. Plant Physiol 1986; 81: 313–316
   PubMedGoogle Scholar
• Nishimura M, Takeuchi Y, Debellis L, Haranishimura I. Leaf peroxisomes are directly transformed to glyoxysomes during senescence of pumpkin cotyledons. Protoplasma 1993; 175: 131–137
   Google Scholar
• Erdmann R, Wiebel FF, Flessau A, Rytka J, Beyer A, Frohlich KU, Kunau WH. Pas1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell 1991; 64: 499–510
   PubMed Web of Science ®Google Scholar
• Lazarow PB. Genetic approaches to studying peroxisome biogenesis. Trends Cell Biol 1993; 3: 89–93
   Google Scholar
• Nuttley WM, Brade AM, Gaillardin C, Eitzen GA, Glover JR, Aitchison JD, Rachubinski RA. Rapid identification and characterization of peroxisomal assembly mutants in Yarrowia lipolytica. Yeast 1993; 9: 507–517
   Google Scholar
• Fujiki Y. Peroxisome biogenesis and peroxisome biogenesis disorders. FEBS Lett 2000; 476: 42–46
   PubMedGoogle Scholar
• Zolman BK, Yoder A, Bartel B. Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes. Genetics 2000; 156: 1323–1337
   PubMed Web of Science ®Google Scholar
• Hayashi M, Toriyama K, Kondo M, Nishimura M. 2,4-dichlorophenoxybutyric acid-resistant mutants of Arabidopsis have defects in glyoxysomal fatty acid beta-oxidation. Plant Cell 1998; 10: 183–195
   PubMed Web of Science ®Google Scholar
• Emanuelsson O, Elofsson A, von Heijne G, Cristobal S. In silico prediction of the peroxisomal proteome in fungi, plants and animals. J Mol Biol 2003; 330: 443–456
   Google Scholar
• Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F. Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J Mol Biol 2003; 328: 567–579
   PubMed Web of Science ®Google Scholar
• Reumann S, Ma CL, Lemke S, Babujee L. AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiol 2004; 136: 2587–2608
   PubMed Web of Science ®Google Scholar
• Kiel J, Veenhuis M, van der Klei IJ. PEX genes in fungal genomes: common, rare or redundant. Traffic 2006; 7: 1291–1303
   PubMed Web of Science ®Google Scholar
• Fujiki Y, Matsuzono Y, Matsuzaki T, Fransen M. Import of peroxisomal membrane proteins: The interplay of Pex3p- and Pex19p-mediated interactions. Biochimica et Biophysica Acta-Molec Cell Res 2006; 1763: 1639–1646
   PubMed Web of Science ®Google Scholar
• Van Ael E, Fransen M. Targeting signals in peroxisomal membrane proteins. Biochimica et Biophysica Acta-Molecular Cell Research 2006; 1763: 1629–1638
   Google Scholar
• Fagarasanu A, Fagarasanu M, Rachubinski RA. Maintaining peroxisome populations: a story of division and inheritance. Annu Rev Cell Dev Biol 2007; 23: 321–344
   PubMed Web of Science ®Google Scholar
• Lazarow PB, Fujiki Y. Biogenesis of peroxisomes. Annu Rev Cell Biol 1985; 1: 489–530
   PubMedGoogle Scholar
• Lametschwandtner G, Brocard C, Fransen M, Van Veldhoven P, Berger J, Hartig A. The difference in recognition of terminal tripeptides as peroxisomal targeting signal 1 between yeast and human is due to different affinities of their receptor Pex5p to the cognate signal and to residues adjacent to it. J Biol Chem 1998; 273: 33635–33643
   PubMedGoogle Scholar
• Gatto GJ, Geisbrecht BV, Gould SJ, Berg JM. Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat Struct Biol 2000; 7: 1091–1095
   PubMedGoogle Scholar
• Stanley WA, Filipp FV, Kursula P, Schuller N, Erdmann R, Schliebs W, Sattler M, Wilmanns M. Recognition of a functional peroxisome type 1 target by the dynamic import receptor Pex5p. Mol Cell 2006; 24: 653–663
   Google Scholar
• Klein ATJ, Barnett P, Bottger G, Konings D, Tabak HF, Distel B. Recognition of peroxisomal targeting signal type 1 by the import receptor Pex5p. J Biol Chem 2001; 276: 15034–15041
   Google Scholar
• Otera H, Setoguchi K, Hamasaki M, Kumashiro T, Shimizu N, Fujiki Y. Peroxisomal targeting signal receptor Pex5p interacts with cargoes and import machinery components in a spatiotemporally differentiated manner: Conserved Pex5p WXXYF/Y motifs are critical for matrix protein import. Mol Cell Biol 2002; 22: 1639–1655
   PubMedGoogle Scholar
• Saidowsky J, Dodt G, Kirchberg K, Wegner A, Nastainczyk W, Kunau WH, Schliebs W. 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 2001; 276: 34524–34529
   PubMedGoogle Scholar
• Carvalho AF, Grou CP, Pinto MP, Alencastre IS, Costa-Rodrigues J, Fransen M, Sa-Miranda C, Azevedo JE. Functional characterization of two missense mutations in Pex5p-C11S and N526K. Biochimica et Biophysica Acta-Molec Cell Res 2007; 1773: 1141–1148
   PubMedGoogle Scholar
• Schliebs W, Saidowsky J, Agianian B, Dodt G, Herberg FW, Kunau WH. Recombinant human peroxisomal targeting signal receptor PEX5 – structural basis for interaction of PEX5 with PEX14. J Biol Chem 1999; 274: 5666–5673
   PubMed Web of Science ®Google Scholar
• Moscicka KB, Klompmaker SH, Wang DY, van der Klei IJ, Boekema EJ. The Hansenula polymorpha peroxisomal targeting signal 1 receptor, Pex5p, functions as a tetramer. FEBS Lett 2007; 581: 1758–1762
   Google Scholar
• Costa-Rodrigues J, Carvalho AF, Fransen M, Hambruch E, Schliebs W, Sa-Miranda C, Azevedo JE. Pex5p, the peroxisomal cycling receptor, is a monomeric non-globular protein. J Biol Chem 2005; 280: 24404–24411
   PubMedGoogle Scholar
• Lazarow PB. The import receptor Pex7p and the PTS2 targeting sequence. Biochimica et Biophysica Acta-Molec Cell Res 2006; 1763: 1599–1604
   PubMedGoogle Scholar
• Motley AM, Hettema EH, Ketting R, Plasterk R, Tabak HF. Caenorhabditis elegans has a single pathway to target matrix proteins to peroxisomes. EMBO Rep 2000; 1: 40–46
   PubMedGoogle Scholar
• Zhang JW, Lazarow PB. Peb1 (Pas7) in Saccharomyces cerevisiae encodes a hydrophilic, intra-peroxisomal protein that is a member of the WD repeat family and is essential for the import of thiolase into peroxisomes. J Cell Biol 1995; 129: 65–80
   PubMedGoogle Scholar
• Marzioch M, Erdmann R, Veenhuis M, Kunau WH. 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; 13: 4908–4918
   PubMed Web of Science ®Google Scholar
• Nair DM, Purdue PE, Lazarow PB. Pex7p translocates in and out of peroxisomes in Saccharomyces cerevisiae. J Cell Biol 2004; 167: 599–604
   PubMed Web of Science ®Google Scholar
• Stein K, Schell-Steven A, Erdmann R, Rottensteiner H. Interactions of Pex7p and Pex18p/Pex21p with the peroxisomal docking machinery: implications for the first steps in PTS2 protein import. Mol Cell Biol 2002; 22: 6056–6069
   PubMedGoogle Scholar
• Purdue PE, Yang XD, Lazarow PB. Pex18p and Pex21p, a novel pair of related peroxins essential for peroxisomal targeting by the PTS2 pathway. J Cell Biol 1998; 143: 1859–1869
   PubMed Web of Science ®Google Scholar
• Einwachter H, Sowinski S, Kunau WH, Schliebs W. Yarrowia lipolytica Pex20p, Saccharomyces cerevisiae Pex18p/Pex21p and mammalian Pex5pL fulfil a common function in the early steps of the peroxisomal PTS2 import pathway. EMBO Rep 2001; 2: 1035–1039
   PubMedGoogle Scholar
• Leon S, Zhang L, McDonald WH, Yates J, Cregg JM, Subramani S. Dynamics of the peroxisomal import cycle of PpPex20p: ubiquitin-dependent localization and regulation. J Cell Biol 2006; 172: 67–78
   PubMed Web of Science ®Google Scholar
• Sichting M, Schell-Steven A, Prokisch H, Erdmann R, Rottensteiner H. Pex7p and Pex20p of Neurospora crassa function together in PTS2-dependent protein import into peroxisomes. Mol Biol Cell 2003; 14: 810–821
   PubMedGoogle Scholar
• Otzen M, Wang DY, Lunenborg MGJ, van der Kiel IJ. Hansenula polymorpha Pex20p is an oligomer that binds the peroxisomal targeting signal 2 (PTS2). J Cell Sci 2005; 118: 3409–3418
   PubMedGoogle Scholar
• Otera H, Harano T, Honsho M, Ghaedi K, Mukai S, Tanaka A, Kawai A, Shimizu N, Fujiki Y. The mammalian peroxin Pex5pL, the longer isoform of the mobile peroxisome targeting signal (PTS) type 1 transporter, translocates the Pex7p-PTS2 protein complex into peroxisomes via its initial docking site, Pex14p. J Biol Chem 2000; 275: 21703–21714
   PubMedGoogle Scholar
• Matsumura T, Otera H, Fujiki Y. Disruption of the interaction of the longer isoform of Pex5p, Pex5pL, with Pex7p abolishes peroxisome targeting signal type 2 – study with a novel PEX5-impaired Chinese hamster ovary cell mutant. J Biol Chem 2000; 275: 21715–21721
   PubMedGoogle Scholar
• Nito K, Hayashi M, Nishimura M. Direct interaction and determination of binding domains among peroxisomal import factors in Arabidopsis thaliana. Plant Cell Physiol 2002; 43: 355–366
   PubMedGoogle Scholar
• Woodward AW, Bartel B. The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Mol Biol Cell 2005; 16: 573–583
   PubMed Web of Science ®Google Scholar
• Hayashi M, Yagi M, Nito K, Kamada T, Nishimura M. Differential contribution of two peroxisomal protein receptors to the maintenance of peroxisomal functions in Arabidopsis. J Biol Chem 2005; 280: 14829–14835
   Google Scholar
• Dodt G, Warren D, Becker E, Rehling P, Gould SJ. Domain mapping of human PEX5 reveals functional and structural similarities to Saccharomyces cerevisiae Pex18p and Pex21p. J Biol Chem 2001; 276: 41769–41781
   PubMedGoogle Scholar
• Klein ATJ, van den Berg M, Bottger G, Tabak H, Distel B. Saccharomyces cerevisiae acyl-CoA oxidase follows a novel, non-PTS1, import pathway into peroxisomes that is dependent on Pex5p. J Biol Chem 2002; 277: 25011–25019
   PubMed Web of Science ®Google Scholar
• McNew JA, Goodman HM. An oligomeric protein is imported into peroxisomes in vivo. J Cell Biol 1994; 127: 1245–1257
   PubMed Web of Science ®Google Scholar
• Glover JR, Andrews DW, Rachubinski RA. Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc Natl Acad Sci USA 1994; 91: 10541–10545
   PubMed Web of Science ®Google Scholar
• Agne B, Meindl NM, Niederhoff K, Einwachter H, Rehling P, Sickmann A, Meyer HE, Girzalsky W, Kunau WH. Pex8p: An intraperioxisomal organizer of the peroxisomal import machinery. Mol Cell 2003; 11: 635–646
   PubMedGoogle Scholar
• Mano S, Nakamori C, Nito K, Kondo M, Nishimura M. The Arabidopsis pex12 and pex13 mutants are defective in both PTS1- and PTS2-dependent protein transport to peroxisomes. Plant J 2006; 47: 604–618
   PubMed Web of Science ®Google Scholar
• Pires JR, Hong XJ, Brockmann C, Volkmer-Engert R, Schneider-Mergener J, Oschkinat H, Erdmann R. The ScPex13p SH3 domain exposes two distinct binding sites for Pex5p and Pex14p. J Mol Biol 2003; 326: 1427–1435
   PubMedGoogle Scholar
• Urquhart AJ, Kennedy D, Gould SJ, Crane DI. Interaction of Pex5p, the type 1 peroxisome targeting signal receptor, with the peroxisomal membrane proteins Pex14p and Pex13p. J Biol Chem 2000; 275: 4127–4136
   PubMed Web of Science ®Google Scholar
• Hayashi M, Nito K, Toriyama-Kato K, Kondo M, Yamaya T, Nishimura M. AtPex14p maintains peroxisomal functions by determining protein targeting to three kinds of plant peroxisomes. EMBO J 2000; 19: 5701–5710
   Google Scholar
• Kunau WH. Peroxisomes: the extended shuttle to the peroxisome matrix. Curr Biol 2001; 11: R659–R662
   Google Scholar
• Rachubinski RA, Subramani S. How proteins penetrate peroxisomes. Cell 1995; 83: 525–528
   PubMedGoogle Scholar
• Smith MD, Schnell DJ. Peroxisomal protein import: the paradigm shifts. Cell 2001; 105: 293–296
   Google Scholar
• Gouveia AM, Guimaraes CP, Oliveira ME, Reguenga C, Sa-Miranda C, Azevedo JE. in Peroxisomal Disorders and Regulation of Genes 2003; 544: 219–220
   Google Scholar
• Dammai V, Subramani S. The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisomal matrix and recycled to the cytosol. Cell 2001; 105: 187–196
   PubMed Web of Science ®Google Scholar
• Rehling P, Skaletz-Rorowski A, Girzalsky W, Voorn-Brouwer T, Franse MM, Distel B, Veenhuis M, Kunau WH, Erdmann R. Pex8p, an intraperoxisomal peroxin of Saccharomyces cerevisiae required for protein transport into peroxisomes binds the PTS1 receptor Pex5p. J Biol Chem 2000; 275: 3593–3602
   PubMedGoogle Scholar
• Miura S, Miyazawa S, Osumi T, Hashimoto T, Fujiki Y. Post-translational import of 3-ketoacyl-CoA thiolase into rat-liver peroxisomes in vitro. J Biochem (Tokyo) 1994; 115: 1064–1068
   PubMedGoogle Scholar
• Kurochkin IV, Mizuno Y, Konagaya A, Sakaki Y, Schonbach C, Okazaki Y. Novel peroxisomal protease Tysnd1 processes PTS1- and PTS2-containing enzymes involved in beta-oxidation of fatty acids. EMBO J 2007; 26: 835–845
   PubMedGoogle Scholar
• Helm M, Luck C, Prestele J, Hierl G, Huesgen PF, Froehlich T, Arnold GJ, Adamska I, Gorg A, Lottspeich F, et al. Dual specificities of the glyoxysomal/peroxisomal processing protease Deg15 in higher plants. Proc Natl Acad Sci USA 2007; 104: 11501–11506
   PubMedGoogle Scholar
• Gouveia AMM, Reguenga C, Oliveira MEM, Sa-Miranda C, Azevedo JE. Characterization of peroxisomal Pex5p from rat liver – Pex5p in the Pex5p-Pex14p membrane complex is a transmembrane protein. J Biol Chem 2000; 275: 32444–32451
   PubMedGoogle Scholar
• Kerssen D, Hambruch E, Klaas W, Platta HW, de Kruijff B, Erdmann R, Kunau WH, Schliebs W. Membrane association of the cycling peroxisome import receptor Pex5p. J Biol Chem 2006; 281: 27003–27015
   PubMed Web of Science ®Google Scholar
• Erdmann R, Schliebs W. Peroxisomal matrix protein import: The transient pore model. Nature Rev Molec Cell Biol 2005; 6: 738–742
   PubMedGoogle Scholar
• Wang DY, Visser NV, Veenhuis M, van der Klei IJ. Physical interactions of the peroxisomal targeting signal 1 receptor Pex5p, studied by fluorescence correlation spectroscopy. J Biol Chem 2003; 278: 43340–43345
   PubMedGoogle Scholar
• Waterham HR, Titorenko VI, Haima P, Cregg JM, Harder W, Veenhuis M. The Hansenula polymorpha Per1 gene is essential for peroxisome biogenesis and encodes a peroxisomal matrix protein with both carboxy-terminal and amino-terminal targeting signals. J Cell Biol 1994; 127: 737–749
   PubMedGoogle Scholar
• Zhang L, Leon S, Subramani S. Two independent pathways traffic the interperoxisomal peroxin PpPex8p into peroxisomes: mechanism and evolutionary implications. Mol Biol Cell 2006; 17: 690–699
   PubMed Web of Science ®Google Scholar
• Chang CC, Warren DS, Sacksteder KA, Gould SJ. PEX12 interacts with PEX5 and PEX10 and acts downstream of receptor docking in peroxisomal matrix protein import. J Cell Biol 1999; 147: 761–773
   PubMedGoogle Scholar
• Dodt G, Gould SJ. 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 1996; 135: 1763–1774
   PubMed Web of Science ®Google Scholar
• Hu JP, Aguirre M, Peto C, Alonso J, Ecker J, Chory J. A role for peroxisomes in photomorphogenesis and development of Arabidopsis. Science 2002; 297: 405–409
   PubMed Web of Science ®Google Scholar
• Schumann U, Wanner G, Veenhuis M, Schmid M, Gietl C. AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proc Natl Acad Sci USA 2003; 100: 9626–9631
   PubMedGoogle Scholar
• Sparkes IA, Brandizzi F, Slocombe SP, El-Shami M, Hawes C, Baker A. An Arabidopsis pex10 null mutant is embryo lethal, implicating peroxisomes in an essential role during plant embryogenesis. Plant Physiol 2003; 133: 1809–1819
   PubMed Web of Science ®Google Scholar
• Fan JL, Quan S, Orth T, Awai C, Chory J, Hu JP. The Arabidopsis PEX12 gene is required for peroxisome biogenesis and is essential for development. Plant Physiol 2005; 139: 231–239
   PubMed Web of Science ®Google Scholar
• Nito K, Kamigaki A, Kondo M, Hayashi M, Nishimura M. Functional classification of Arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants. Plant Cell Physiol 2007; 48: 763–774
   PubMed Web of Science ®Google Scholar
• Platta HW, Grunau S, Rosenkranz K, Girzalsky W, Erdmann R. Functional role of the AAA peroxins in dislocation of the cycling PTS1 receptor back to the cytosol. Nat Cell Biol 2005; 7: 817–822
   PubMed Web of Science ®Google Scholar
• Miyata N, Fujiki Y. Shuttling mechanism of peroxisome targeting signal type 1 receptor Pex5: ATP-independent import and ATP-dependent export. Mol Cell Biol 2005; 25: 10822–10832
   PubMedGoogle Scholar
• Koller A, Snyder WB, Faber KN, Wenzel TJ, Rangell L, Keller GA, Subramani S. Pex22p of Pichia pastoris, essential for peroxisomal matrix protein import, anchors the ubiquitin-conjugating enzyme, Pex4p, on the peroxisomal membrane. J Cell Biol 1999; 146: 99–112
   PubMedGoogle Scholar
• Collins CS, Kalish JE, Morrell JC, McCaffery JM, Gould SJ. The peroxisome biogenesis factors Pex4p, Pex22p, Pex1p, and Pex6p act in the terminal steps of peroxisomal matrix protein import. Mol Cell Biol 2000; 20: 7516–7526
   PubMedGoogle Scholar
• Zolman BK, Monroe-Augustus M, Silva ID, Bartel B. Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22. Plant Cell 2005; 17: 3422–3435
   Google Scholar
• Zolman BK, Bartel B. An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. Proc Natl Acad Sci USA 2004; 101: 1786–1791
   PubMed Web of Science ®Google Scholar
• Wiebel FF, Kunau WH. The Pas2 protein essential for peroxisome biogenesis is related to ubiquitin-conjugating enzymes. Nature 1992; 359: 73–76
   PubMedGoogle Scholar
• Kiel J, Emmrich K, Meyer HE, Kunau WH. Ubiquitination of the peroxisomal targeting signal type 1 receptor, Pex5p, suggests the presence of a quality control mechanism during peroxisomal matrix protein import. J Biol Chem 2005; 280: 1921–1930
   PubMed Web of Science ®Google Scholar
• Kragt A, Brouwer TV, van den Berg M, Distel B. The Saccharomyces cerevisiae peroxisomal import receptor Pex5p is monoubiquitinated in wild type cells. J Biol Chem 2005; 280: 7867–7874
   PubMedGoogle Scholar
• Platta H, Girzalsky W, Erdmann R. Ubiquitination of the peroxisomal import receptor Pex5p. Biochem J 2004; 384: 37–45
   PubMedGoogle Scholar
• Purdue PE, Lazarow PB. Pex18p is constitutively degraded during peroxisome biogenesis. J Biol Chem 2001; 276: 47684–47689
   PubMedGoogle Scholar
• Platta HW, El Magraoui F, Schlee D, Grunau S, Girzalsky W, Erdmann R. Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. J Cell Biol 2007; 177: 197–204
   PubMed Web of Science ®Google Scholar
• Williams C, van den Berg M, Sprenger RR, Distel B. A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p. J Biol Chem 2007; 282: 22534–22543
   PubMed Web of Science ®Google Scholar
• Kiel J, Otzen M, Veenhuis M, van der Klei IJ. Obstruction of polyubiquitination affects PTS1 peroxisomal matrix protein import. Biochimica et Biophysica Acta-Molec Cell Res 2005; 1745: 176–186
   Google Scholar
• Yahraus T, Braverman N, Dodt G, Kalish JE, Morrell JC, Moser HW, Valle D, Gould SJ. The peroxisome biogenesis disorder group 4 gene, PXAAA1, encodes a cytoplasmic ATPase required for stability of the PTS1 receptor. EMBO J 1996; 15: 2914–2923
   PubMed Web of Science ®Google Scholar
• van der Klei IJ, Hilbrands RE, Kiel J, Rasmussen SW, Cregg JM, Veenhuis M. The ubiquitin-conjugating enzyme Pex4p of Hansenula polymorpha is required for efficient functioning of the PTS1 import machinery. EMBO J 1998; 17: 3608–3618
   PubMedGoogle Scholar
• Kiel J, Hilbrands RE, Van der Klei IJ, Rasmussen SW, Salomons FA, Van der Heide M, Faber KN, Cregg JM, Veenhuis M. Hansenula polymorpha Pex1p and Pex6p are peroxisome-associated AAA proteins that functionally and physically interact. Yeast 1999; 15: 1059–1078
   PubMedGoogle Scholar
• Pickart CM. Mechanisms underlying ubiquitination. Annu Rev Biochem 2001; 70: 503–533
   PubMed Web of Science ®Google Scholar
• Carvalho AF, Pinto MP, Grou UP, Alencastre IS, Fransen M, Sa-Miranda C, Azevedo JE. Ubiquitination of mammalian pex5p, the peroxisomal import receptor. J Biol Chem 2007; 282: 31267–31272
   PubMedGoogle Scholar
• Freemont PS, Hanson IM, Trowsdale J. A novel cysteine-rich sequence motif. Cell 1991; 64: 483–484
   PubMed Web of Science ®Google Scholar
• Barlow PN, Luisi B, Milner A, Elliott M, Everett R. Structure of the C3hc4 domain by H-1-nuclear magnetic-resonance spectroscopy – a new structural class of zinc-finger. J Mol Biol 1994; 237: 201–211
   PubMed Web of Science ®Google Scholar
• Borden KLB. RING domains: master builders of molecular scaffolds?. J Mol Biol 2000; 295: 1103–1112
   PubMedGoogle Scholar
• Borden KLB, Boddy MN, Lally J, O'Reilly NJ, Martin S, Howe K, Solomon E, Freemont PS. The solution structure of the RING finger domain from the acute promyelocytic leukemia proto-oncoprotein Pml. EMBO J 1995; 14: 1532–1541
   PubMed Web of Science ®Google Scholar
• Lovering R, Hanson IM, Borden KLB, Martin S, Oreilly NJ, Evan GI, Rahman D, Pappin DJC, Trowsdale J, Freemont PS. Identification and preliminary characterization of a protein motif related to the zinc finger. Proc Natl Acad Sci USA 1993; 90: 2112–2116
   PubMed Web of Science ®Google Scholar
• Lorick KL, Jensen JP, Fang SY, Ong AM, Hatakeyama S, Weissman AM. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci USA 1999; 96: 11364–11369
   PubMed Web of Science ®Google Scholar
• Okumoto K, Abe I, Fujiki Y. 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 2000; 275: 25700–25710
   PubMedGoogle Scholar
• Hazra PP, Suriapranata I, Snyder WB, Subramani S. Peroxisome remnants in pex3-delta cells and the requirement of Pex3p for interactions between the peroxisomal docking and translocation subcomplexes. Traffic 2002; 3: 560–574
   PubMedGoogle Scholar
• Eckert JH, Johnsson N. Pex10p links the ubiquitin conjugating enzyme Pex4p to the protein import machinery of the peroxisome. J Cell Sci 2003; 116: 3623–3634
   Google Scholar
• Birschmann I, Stroobants AK, van den Berg M, Schafer A, Rosenkranz K, Kunau WH, Tabak HF. Pex15p of Saccharomyces cerevisiae provides a molecular basis for recruitment of the AAA peroxin Pex6p to peroxisomal membranes. Mol Biol Cell 2003; 14: 2226–2236
   PubMedGoogle Scholar
• Rosenkranz K, Birschmann I, Grunau S, Girzalsky W, Kunau WH, Erdmann R. Functional association of the AAA complex and the peroxisomal importomer. FEBS J 2006; 273: 3804–3815
   PubMedGoogle Scholar
• Gould SJ, Keller GA, Subramani S. Identification of a peroxisomal targeting signal at the carboxy-terminus of firefly luciferase. J Cell Biol 1987; 105: 2923–2931
   PubMedGoogle Scholar
• Gould SJ, Collins CS. Peroxisomal-protein import: is it really that complex?. Nature Reviews Molecular Cell Biology 2002; 3: 382–389
   PubMedGoogle Scholar
• Aksam EB, Koek A, Kiel J, Jourdan S, Veenhuis M, van der Klei IJ. A peroxisomal lon protease and peroxisome degradation by autophagy play key roles in vitality of Hansenula polymorpha cells. Autophagy 2007; 3: 96–105
   PubMed Web of Science ®Google Scholar
• Walton PA, Wendland M, Subramani S, Rachubinski RA, Welch WJ. Involvement of 70-Kd heat shock proteins in peroxisomal import. J Cell Biol 1994; 125: 1037–1046
   PubMedGoogle Scholar
• Harano T, Nose S, Uezu R, Shimizu N, Fujiki Y. Hsp70 regulates the interaction between the peroxisome targeting signal type 1 (PTS1)-receptor Pex5p and PTS1. Biochem J 2001; 357: 157–165
   PubMedGoogle Scholar
• Hettema EH, Ruigrok CCM, Koerkamp MG, van den Berg M, Tabak HF, Distel B, Braakman I. The cytosolic DnaJ-like protein Djp1p is involved specifically in peroxisomal protein import. J Cell Biol 1998; 142: 421–434
   PubMedGoogle Scholar