New insights into dynamic and functional assembly of the AAA peroxins, Pex1p and Pex6p, and their membrane receptor Pex26p in shuttling of PTS1-receptor Pex5p during peroxisome biogenesis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 1, 2012, Pages 145-149

  Fujiki, Yukio ^a,b   Nashiro, Chika ^a   Miyata, Non ^a   Tamura, Shigehiko ^a   Okumoto, Kanji ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

AAA peroxin; CHO cell mutant; Peroxisome biogenesis; Peroxisome biogenesis disorder; PTS1 receptor shuttling; Ubiquitination

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ALANINE; CYSTEINE; CYTOSOL RECEPTOR; MATRIX PROTEIN; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; PEROXIN; PROTEIN PEX 1P; PROTEIN PEX 26P; PROTEIN PEX 5P; PROTEIN PEX 6P; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CYTOSOL; GENE; HUMAN; HYDROLYSIS; NONHUMAN; PEROXISOME; PEX1 GENE; PEX6 GENE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; UBIQUITINATION; ZELLWEGER SYNDROME;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; HUMANS; MEMBRANE PROTEINS; PEROXISOMES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EUKARYOTA;

EID: 84855195598     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.10.012     Document Type: Review

References (68)

1. Fujiki Y. Peroxisome biogenesis disorders. Encyclopedia of Life Sciences May 2011, 1-9. vol., John Wiley & Sons, Chichester, UK.
2. Weller S., Gould S.J., Valle D. Peroxisome biogenesis disorders. Annu. Rev. Genomics Hum. Genet. 2003, 4:165-211.
3. Matsumoto N., Tamura S., Fujiki Y. The pathogenic peroxin Pex26p recruits the Pex1p-Pex6p AAA ATPase complexes to peroxisomes. Nat. Cell Biol. 2003, 5:454-460.
4. Shimozawa N., Tsukamoto T., Nagase T., Takemoto Y., Koyama N., Suzuki Y., Komori M., Osumi T., Jeannette G., Wanders R.J.A., Kondo N. Identification of a new complementation group of the peroxisome biogenesis disorders and PEX14 as the mutated gene. Hum. Mutat. 2004, 23:552-558.
5. Tamura S., Okumoto K., Toyama R., Shimozawa N., Tsukamoto T., Suzuki Y., Osumi T., Kondo N., Fujiki Y. 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. 1998, 95:4350-4355.
6. Tsukamoto T., Miura S., Nakai T., Yokota S., Shimozawa N., Suzuki Y., Orii T., Fujiki Y., Sakai F., Bogaki A., Yasumo H., Osumi T. Peroxisome assembly factor-2, a putative ATPase cloned by functional complementation on a peroxisome-deficient mammalian cell mutant. Nat. Genet. 1995, 11:395-401.
7. Fukuda S., Shimozawa N., Suzuki Y., Zhang Z., Tomatsu S., Tsukamoto T., Hashiguchi N., Osumi T., Masuno M., Imaizumi K., Kuroki Y., Fujiki Y., Orii T., Kondo N. Human peroxisome assembly factor-2 (PAF-2): a gene responsible for group C peroxisome biogenesis disorder in humans. Am. J. Hum. Genet. 1996, 59:1210-1220.
8. Reuber B.E., Germain-Lee E., Collins C.S., Morrell J.C., Ameritunga R., Moser H.W., Valle D., Gould S.J. Mutations in PEX1 are the most common cause of peroxisome biogenesis disorders. Nat. Genet. 1997, 17:445-448.
9. Portsteffen H., Beyer A., Becker E., Epplen C., Pawlak A., Kunau W.-H., Dodt G. Human PEX1 is mutated in complementation group 1 of the peroxisome biogenesis disorders. Nat. Genet. 1997, 17:449-452.
10. Yahraus T., Braverman N., Dodt G., Kalish J.E., Morrell J.C., Moser H.W., Valle D., Gould S.J. 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.
11. Matsumoto N., Tamura S., Furuki S., Miyata N., Moser A., Shimozawa N., Moser H.W., Suzuki Y., Kondo N., Fujiki Y. Mutations in novel peroxin gene PEX26 that cause peroxisome biogenesis disorders of complementation group 8 provide a genotype-phenotype correlation. Am. J. Hum. Genet. 2003, 73:233-246.
12. Birschmann I., Rosenkranz K., Erdmann R., Kunau W.-H. Structural and functional analysis of the interaction of the AAA-peroxins Pex1p and Pex6p. FEBS J. 2005, 272:47-58.
13. Lazarow P.B., Fujiki Y. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1985, 1:489-530.
14. Sacksteder K.A., Gould S.J. The genetics of peroxisome biogenesis. Annu. Rev. Genet. 2000, 34:623-652.
15. Subramani S., Koller A., Snyder W.B. Import of peroxisomal matrix and membrane proteins. Annu. Rev. Biochem. 2000, 69:399-418.
16. 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 WXXXF/Y motifs are critical for matrix protein import. Mol. Cell. Biol. 2002, 22:1639-1655.
17. 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.
18. Platta H.W., 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.
19. Miyata N., Hosoi K., Mukai S., Fujiki Y. In vitro import of peroxisome-targeting signal 2 (PTS2) receptor Pex7p into peroxisomes. Biochim. Biophys. Acta, Mol. Cell Res. 2009, 1793:860-870.
20. Vale R.D. AAA proteins: lords of the ring. J. Cell Biol. 2000, 150:F13-F19.
21. Ogura T., Wilkinson A.J. AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 2001, 6:575-597.
22. Lupas A.N., Martin J. AAA proteins. Curr. Opin. Struct. Biol. 2002, 12:746-753.
23. Beyer A. Sequence analysis of the AAA protein family. Protein Sci. 1997, 6:2043-2058.
24. Hanson P.I., Whiteheart S.W. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 2005, 6:519-529.
25. Furuki S., Tamura S., Matsumoto N., Miyata N., Moser A., Moser H.W., Fujiki Y. Mutations in the peroxin Pex26p responsible for peroxisome biogenesis disorders of complementation group 8 impair its stability, peroxisomal localization, and interaction with the Pex1p-Pex6p complex. J. Biol. Chem. 2006, 281:1317-1323.
26. Okumoto K., Misono S., Miyata N., Matsumoto Y., Mukai S., Fujiki Y. Cysteine ubiquitination of PTS1-receptor Pex5p regulates Pex5p recycling. Traffic 2011, 12:1067-1083.
27. Platta H.W., Magraoui F.E., 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.
28. Grou C.P., Carvalho A.F., Pinto M.P., Huybrechts S.J., Sá-Miranda C., Fransen M., Azevedo J.E. Properties of the ubiquitin-Pex5p thiol ester conjugate. J. Biol. Chem. 2009, 284:10504-10513.
29. Schliebs W., Girzalsky W., Erdmann R. Peroxisomal protein import and ERAD: variations on a common theme. Nat. Rev. Mol. Cell Biol. 2010, 11:885-890.
30. Tamura S., Yasutake S., Matsumoto N., Fujiki Y. Dynamic and functional assembly of the AAA peroxins, Pex1p and Pex6p, and their membrane receptor Pex26p. J. Biol. Chem. 2006, 281:27693-27704.
31. Weller S., Cajigas I., Morrell J., Obie C., Steel G., Gould S.J., Valle D. Alternative splicing suggests extended function of PEX26 in peroxisome biogenesis. Am. J. Hum. Genet. 2005, 76:987-1007.
32. Shiozawa K., Maita N., Tomii K., Seto A., Goda N., Akiyama Y., Shimizu T., Shirakawa M., Hiroaki H. Structure of the N-terminal domain of PEX1 AAA-ATPase: characterization of a putative adaptor-binding domain. J. Biol. Chem. 2004, 279:50060-50068.
33. Shiozawa K., Goda N., Shimizu T., Mizoguchi K., Kondo N., Shimozawa N., Shirakawa M., Hiroaki H. The common phospholipid-binding activity of the N-terminal domains of PEX1 and VCP/p97. FEBS J. 2006, 273:4959-4971.
34. Zhang X., Shaw A., Bates P.A., Newman R.H., Gowen B., Orlova E., Gorman M.A., Kondo H., Dokurno P., Lally J., Leonard G., Meyer H., van Heel M., Freemont P.S. Structure of the AAA ATPase p97. Mol. Cell 2000, 6:1473-1484.
35. Wang Q., Song C., Yang X., Li C.-C.H. D1 ring is stable and nucleotide-independent, whereas D2 ring undergoes major conformational changes during the ATPase cycle of p97-VCP. J. Biol. Chem. 2003, 278:32784-32793.
36. Titorenko V.I., Rachubinski R.A. Peroxisomal membrane fusion requires two AAA family ATPases, Pex1p and Pex6p. J. Cell Biol. 2000, 150:881-886.
37. Fujiki Y., Miyata N., Matsumoto N., Tamura S. Dynamic and functional assembly of the AAA peroxins, Pex1p and Pex6p, and their membrane receptor Pex26p involved in shuttling of the PTS1 receptor Pex5p in peroxisome biogenesis. Biochem. Soc. Trans. 2008, 36:109-113.
38. Platta H.W., Erdmann R. Peroxisomal dynamics. Trends Cell Biol. 2007, 17:474-484.
39. Birschmann I., Stroobants A.K., van den Berg M., Schafer A., Rosenkranz K., Kunau W.-H., Tabak H.F. 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.
40. Rosenkranz K., Birschmann I., Grunau S., Girzalsky W., Kunau W.-H., Erdmann R. Functional association of the AAA complex and the peroxisomal importomer. FEBS J. 2006, 273:3804-3815.
41. Clary D.O., Griff I.C., Rothman J.E. SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell 1990, 61:709-721.
42. Rothman J.E. Mechanisms of intracellular protein transport. Nature 1994, 372:55-63.
43. Rabinovich E., Kerem A., Fröhlich K.-U., Diamant N., Bar-Nun S. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell. Biol. 2002, 22:626-634.
44. Whiteheart S.W., Kubalek E.W. SNAPs and NSF: general members of the fusion apparatus. Trends Cell Biol. 1995, 5:64-68.
45. Hay J.C., Scheller R.H. SNAREs and NSF in targeted membrane fusion. Curr. Opin. Cell Biol. 1997, 9:505-512.
46. Ye Y., Shibata Y., Kikkert M., van Voorden S., Wiertz E., Rapoport T.A. Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:14132-14138.
47. Nashiro C., Kashiwagi A., Matsuzaki T., Tamura S., Fujiki Y. Recruiting mechanism of the AAA peroxins, Pex1p and Pex6p, to Pex26p on peroxisome membrane. Traffic 2011, 12:774-788.
48. Albertini M., Rehling P., Erdmann R., Girzalsky W., Kiel J.A.K.W., Veenhuis M., Kunau W.-H. Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell 1997, 89:83-92.
49. Fransen M., Terlecky S.R., Subramani S. Identification of a human PTS1 receptor docking protein directly required for peroxisomal protein import. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:8087-8092.
50. 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 PTS1-transporter, translocates Pex7p-PTS2 protein complex into peroxisomes via its initial docking site, Pex14p. J. Biol. Chem. 2000, 275:21703-21714.
51. Itoh R., Fujiki Y. Functional domains and dynamic assembly of the peroxin Pex14p, the entry site of matrix proteins. J. Biol. Chem. 2006, 281:10196-10205.
52. 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.
53. Agne B., Meindl N.M., Niederhoff K., Einwaechter H., Rehling P., Sickmann A., Meyer H.E., Girzalsky W., Kunau W.-H. Pex8p: an intraperoxisomal organizer of the peroxisomal import machinery. Mol. Cell 2003, 11:635-646.
54. Neupert W. Protein import into mitochondria. Annu. Rev. Biochem. 1997, 66:863-917.
55. Rapoport T.A., Jungnickel B., Kutay U. Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu. Rev. Biochem. 1996, 65:271-303.
56. Oliveira M.E., Gouveia A.M., Pinto R.A., Sa-Miranda C., Azevedo J.E. The energetics of Pex5p-mediated peroxisomal protein import. J. Biol. Chem. 2003, 278:39483-39488.
57. Ye Y., Meyer H.H., Rapoport T.A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 2001, 414:652-656.
58. Leonhard K., Guiard B., Pellecchia G., Tzagoloff A., Neupert W., Langer T. Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol. Cell 2000, 5:629-638.
59. Kihara A., Akiyama Y., Ito K. Dislocation of membrane proteins in FtsH-mediated proteolysis. EMBO J. 1999, 18:2970-2981.
60. Platta H.W., Erdmann R. The peroxisomal protein import machinery. FEBS Lett. 2007, 581:2811-2819.
61. Carvalho A.F., Pinto M.P., Grou C.P., Alencastre I.S., Fransen M., Sá-Miranda C., Azevedo J.E. Ubiquitination of mammalian Pex5p, the peroxisomal import receptor. J. Biol. Chem. 2007, 282:31267-31272.
62. Platta H.W., Magraoui F.E., Bäumer B.E., Schlee D., Girzalsky W., Erdmann R. Pex2 and Pex12 function as protein-ubiquitin ligases in peroxisomal protein import. Mol. Cell. Biol. 2009, 29:5505-5516.
63. Williams C., van den Berg M., Sprenger R.R., Distel B. A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p. J. Biol. Chem. 2007, 282:22534-22543.
64. Léon S., Subramani S. A conserved cysteine residue of Pichia pastoris Pex20p is essential for its recycling from the peroxisome to the cytosol. J. Biol. Chem. 2007, 282:7424-7430.
65. Grou C.P., Carvalho A.F., Pinto M.P., Wiese S., Piechura H., Meyer H.E., Warscheid B., Sá-Miranda C., Azevedo J.E. Members of the E2D (UbcH5) family mediate the ubiquitination of the conserved cysteine of Pex5p, the peroxisomal import receptor. J. Biol. Chem. 2008, 283:14190-14197.
66. Miyata N., Okumoto K., Mukai S., Noguchi M., Fujiki Y. AWP1/ZFAND6 functions in Pex5 export by interacting with Cys-monoubiquitinated Pex5 and Pex6 AAA ATPase. Traffic 2012, 13:168-183.
67. Debelyy M.O., Platta H.W., Saffian D., Hensel A., Thoms S., Meyer H.E., Warscheid B., Girzalsky W., Erdmann R. Ubp15p, a ubiquitin hydrolase associated with the peroxisomal export machinery. J. Biol. Chem. 2011, 286:28223-28234.
68. Goto S., Mano S., Nakamori C., Nishimura M. Arabidopsis ABERRANT PEROXISOME MORPHOLOGY9 is a peroxin that recruits the PEX1-PEX6 complex to peroxisomes. Plant Cell 2011, 23:1573-1587.