Uniqueness of the mechanism of protein import into the peroxisome matrix: Transport of folded, co-factor-bound and oligomeric proteins by shuttling receptors

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1763, Issue 12, 2006, Pages 1552-1564

  Léon, Sébastien ^a   Goodman, Joel M ^b   Subramani, Suresh ^a  

^a SECTION OF MOLECULAR BIOLOGY   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Extended shuttle; Import of folded and oligomeric protein; Peroxisomal matrix protein import; Peroxisomal RADAR; Quality control; Shuttling receptor

Indexed keywords

MATRIX PROTEIN; MEMBRANE PROTEIN; OLIGOMER; PROTEIN PEX18P; PROTEIN PEX20P; PROTEIN PEX5P; PROTEIN PEX7P; RECEPTOR PROTEIN;

CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL MEMBRANE; CELL ORGANELLE; COMPARATIVE STUDY; EXTRACELLULAR MATRIX; GENE TRANSLOCATION; MOLECULAR DYNAMICS; NUCLEAR IMPORT; PEROXISOME; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECRETION; PROTEIN TRANSPORT; QUALITY CONTROL; REVIEW; SHUTTLE VECTOR; SIGNAL TRANSDUCTION;

CYTOPLASM; HUMANS; INTRACELLULAR MEMBRANES; MODELS, BIOLOGICAL; PEROXISOMES; PLANT PROTEINS; PROTEIN FOLDING; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 33845318489     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2006.08.037     Document Type: Review

References (122)

1. Collinson I. The structure of the bacterial protein translocation complex SecYEG. Biochem. Soc. Trans. 33 (2005) 1225-1230
2. Eilers M., Hwang S., and Schatz G. Unfolding and refolding of a purified precursor protein during import into isolated mitochondria. EMBO J. 7 (1988) 1139-1145
3. Ottado J., and Ceccarelli E.A. A fully active FAD-containing precursor remains folded up to its translocation across the chloroplast membranes. Eur. J. Biochem. 253 (1998) 132-138
4. Lazarow P.B. Peroxisome biogenesis advances and conundrums. Curr. Opin. Cell Biol. 15 (2003) 489-497
5. Gutensohn M., Fan E., Frielingsdorf S., Hanner P., Hou B., Hust B., Klosgen R.B., Toc, Tic, Tat, et al. structure and function of protein transport machineries in chloroplasts. J. Plant Physiol. 163 (2006) 333-347
6. Russel M. Macromolecular assembly and secretion across the bacterial cell envelope: type II protein secretion systems. J. Mol. Biol. 279 (1998) 485-499
7. Gorlich D. Nuclear protein import. Curr. Opin. Cell Biol. 9 (1997) 412-419
8. Taylor R.D., and Pfanner N. The protein import and assembly machinery of the mitochondrial outer membrane. Biochim. Biophys. Acta 1658 (2004) 37-43
9. Muller M., and Klosgen R.B. The Tat pathway in bacteria and chloroplasts (review). Mol. Membr. Biol. 22 (2005) 113-121
10. Pool M.R. Signal recognition particles in chloroplasts, bacteria, yeast and mammals (review). Mol. Membr. Biol. 22 (2005) 3-15
11. Karamyshev A.L., and Johnson A.E. Selective SecA association with signal sequences in ribosome-bound nascent chains: a potential role for SecA in ribosome targeting to the bacterial membrane. J. Biol. Chem. 280 (2005) 37930-37940
12. Ivanova Y., Smith M.D., Chen K., and Schnell D.J. Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol. Biol. Cell 15 (2004) 3379-3392
13. Dammai V., and Subramani S. The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisomal matrix and recycled to the cytosol. Cell 105 (2001) 187-196
14. Nair D.M., Purdue P.E., and Lazarow P.B. Pex7p translocates in and out of peroxisomes in Saccharomyces cerevisiae. J. Cell Biol. 167 (2004) 599-604
15. Miyata N., and Fujiki Y. Shuttling mechanism of peroxisome targeting signal type 1 receptor Pex5: ATP-independent import and ATP-dependent export. Mol. Cell. Biol. 25 (2005) 10822-10832
16. Leon S., Zhang L., McDonald W.H., Yates III J., Cregg J.M., and Subramani S. Dynamics of the peroxisomal import cycle of PpPex20p: ubiquitin-dependent localization and regulation. J. Cell Biol. 172 (2006) 67-78
17. Platta H.W., Girzalsky W., and Erdmann R. Ubiquitination of the peroxisomal import receptor Pex5p. Biochem. J. 384 (2004) 37-45
18. Kiel J.A., Emmrich K., Meyer H.E., and Kunau W.H. 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. 280 (2005) 1921-1930
19. Kiel J.A., Otzen M., Veenhuis M., and van der Klei I.J. Obstruction of polyubiquitination affects PTS1 peroxisomal matrix protein import. Biochim. Biophys. Acta 1745 (2005) 176-186
20. Kragt A., Voorn-Brouwer T., van den Berg M., and Distel B. The Saccharomyces cerevisiae peroxisomal import receptor Pex5p is monoubiquitinated in wild type cells. J. Biol. Chem. 280 (2005) 7867-7874
21. McCollum D., Monosov E., and 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. 121 (1993) 761-774
22. Terlecky S.R., Nuttley W.M., McCollum D., Sock E., and Subramani S. The Pichia pastoris peroxisomal protein PAS8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. EMBO J. 14 (1995) 3627-3634
23. Rehling P., Marzioch M., Niesen F., Wittke E., Veenhuis M., and Kunau W.H. The import receptor for the peroxisomal targeting signal 2 (PTS2) in Saccharomyces cerevisiae is encoded by the PAS7 gene. EMBO J. 15 (1996) 2901-2913
24. Zhang J.W., Cai X., and Lazarow P.B. Peb1p (Pas7p) is an intra-peroxisomal receptor for the N-terminal, type 2, peroxisomal targeting signal of thiolase. Ann. N. Y. Acad. Sci. 804 (1996) 654-655
25. Stein K., Schell-Steven A., Erdmann R., and 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. 22 (2002) 6056-6069
26. Titorenko V.I., Smith J.J., Szilard R.K., and Rachubinski R.A. Pex20p of the yeast Yarrowia lipolytica is required for the oligomerization of thiolase in the cytosol and for its targeting to the peroxisome. J. Cell Biol. 142 (1998) 403-420
27. Jones J.M., Morrell J.C., and Gould S.J. PEX19 is a predominantly cytosolic chaperone and import receptor for class 1 peroxisomal membrane proteins. J. Cell Biol. 164 (2004) 57-67
28. Agne B., Meindl N.M., Niederhoff K., Einwachter H., Rehling P., Sickmann A., Meyer H.E., Girzalsky W., and Kunau W.H. Pex8p: an intraperoxisomal organizer of the peroxisomal import machinery. Mol. Cell 11 (2003) 635-646
29. Hazra P.P., Suriapranata I., Snyder W.B., and Subramani S. Peroxisome remnants in pex3Δ cells and the requirement of Pex3p for interactions between the peroxisomal docking and translocation subcomplexes. Traffic 3 (2002) 560-574
30. Fang Y., Morrell J.C., Jones J.M., and Gould S.J. PEX3 functions as a PEX19 docking factor in the import of class I peroxisomal membrane proteins. J. Cell Biol. 164 (2004) 863-875
31. Heiland I., and Erdmann R. Biogenesis of peroxisomes. Topogenesis of the peroxisomal membrane and matrix proteins. FEBS J. 272 (2005) 2362-2372
32. Platta H.W., Grunau S., Rosenkranz K., Girzalsky W., and Erdmann R. Functional role of the AAA peroxins in dislocation of the cycling PTS1 receptor back to the cytosol. Nat. Cell Biol. 7 (2005) 817-822
33. Zhang L., Leon S., and Subramani S. Two independent pathways traffic the intraperoxisomal peroxin PpPex8p into peroxisomes: mechanism and evolutionary implications. Mol. Biol. Cell 17 (2006) 690-699
34. Dodt G., and Gould S.J. 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 (1996) 1763-1774
35. Chang C.C., Warren D.S., Sacksteder K.A., and Gould S.J. PEX12 interacts with PEX5 and PEX10 and acts downstream of receptor docking in peroxisomal matrix protein import. J. Cell Biol. 147 (1999) 761-774
36. Koller A., Snyder W.B., Faber K.N., Wenzel T.J., Rangell L., Keller G.A., and 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. 146 (1999) 99-112
37. Collins C.S., Kalish J.E., Morrell J.C., McCaffery J.M., and Gould S.J. The peroxisome biogenesis factors Pex4p, Pex22p, Pex1p, and Pex6p act in the terminal steps of peroxisomal matrix protein import. Mol. Cell Biol. 20 (2000) 7516-7526
38. Hettema E.H., Girzalsky W., van Den Berg M., Erdmann R., and Distel B. Saccharomyces cerevisiae Pex3p and Pex19p are required for proper localization and stability of peroxisomal membrane proteins. EMBO J. 19 (2000) 223-233
39. Hoepfner D., Schildknegt D., Braakman I., Philippsen P., and Tabak H.F. Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122 (2005) 85-95
40. Otzen M., Perband U., Wang D., Baerends R.J., Kunau W.H., Veenhuis M., and Van der Klei I.J. Hansenula polymorpha Pex19p is essential for the formation of functional peroxisomal membranes. J. Biol. Chem. 279 (2004) 19181-19190
41. Sacksteder K.A., Jones J.M., South S.T., Li X., Liu Y., and Gould S.J. PEX19 binds multiple peroxisomal membrane proteins, is predominantly cytoplasmic, and is required for peroxisome membrane synthesis. J. Cell Biol. 148 (2000) 931-944
42. Banerjee S.K., Kessler P.S., Saveria T., and Parsons M. Identification of trypanosomatid PEX19: functional characterization reveals impact on cell growth and glycosome size and number. Mol. Biochem. Parasitol. 142 (2005) 47-55
43. Lambkin G.R., and Rachubinski R.A. Yarrowia lipolytica cells mutant for the peroxisomal peroxin Pex19p contain structures resembling wild-type peroxisomes. Mol. Biol. Cell 12 (2001) 3353-3364
44. Lazarow P.B., and de Duve C. The synthesis and turnover of rat liver peroxisomes. V. Intracellular pathway of catalase synthesis. J. Cell Biol. 59 (1973) 507-524
45. Lazarow P.B., and de Duve C. The synthesis and turnover of rat liver of rat liver peroxisomes. IV. Biochemical pathway of catalase synthesis. J. Cell Biol. 59 (1973) 491-506
46. Kruse C., and Kindl H. Oligomerization of malate synthase during glyoxysome biosynthesis. Arch. Biochem. Biophys. 223 (1983) 629-638
47. Goodman J.M., Scott C.W., Donahue P.N., and Atherton J.P. Alcohol oxidase assembles post-translationally into the peroxisome of Candida boidinii. J. Biol. Chem. 259 (1984) 8485-8493
48. Brul S., Westerveld A., Strijland A., Wanders R.J., Schram A.W., Heymans H.S., Schutgens R.B., van den Bosch H., and Tager J.M. Genetic heterogeneity in the cerebrohepatorenal (Zellweger) syndrome and other inherited disorders with a generalized impairment of peroxisomal functions. A study using complementation analysis. J. Clin. Invest. 81 (1988) 1710-1715
49. Brul S., Wiemer E.A., Westerveld A., Strijland A., Wanders R.J., Schram A.W., Heymans H.S., Schutgens R.B., Van den Bosch H., and Tager J.M. Kinetics of the assembly of peroxisomes after fusion of complementary cell lines from patients with the cerebro-hepato-renal (Zellweger) syndrome and related disorders. Biochem. Biophys. Res. Commun. 152 (1988) 1083-1089
50. Middelkoop E., Strijland A., and Tager J.M. Does aminotriazole inhibit import of catalase into peroxisomes by retarding unfolding?. FEBS Lett. 279 (1991) 79-82
51. Walton P.A., Hill P.E., and Subramani S. Import of stably folded proteins into peroxisomes. Mol. Biol. Cell 6 (1995) 675-683
52. Keller G.A., Gould S., Deluca M., and Subramani S. Firefly luciferase is targeted to peroxisomes in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 3264-3268
53. Walton P.A., Gould S.J., Rachubinski R.A., Subramani S., and Feramisco J.R. Transport of microinjected alcohol oxidase from Pichia pastoris into vesicles in mammalian cells: involvement of the peroxisomal targeting signal. J. Cell Biol. 118 (1992) 499-508
54. Glover J.R., Andrews D.W., and Rachubinski R.A. Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 10541-10545
55. McNew J.A., and Goodman J.M. An oligomeric protein is imported into peroxisomes in vivo. J. Cell Biol. 127 (1994) 1245-1257
56. Elgersma Y., Vos A., van den Berg M., van Roermund C.W., van der Sluijs P., Distel B., and Tabak H.F. Analysis of the carboxyl-terminal peroxisomal targeting signal 1 in a homologous context in Saccharomyces cerevisiae. J. Biol. Chem. 271 (1996) 26375-26382
57. Lee M.S., Mullen R.T., and Trelease R.N. Oilseed isocitrate lyases lacking their essential type 1 peroxisomal targeting signal are piggybacked to glyoxysomes. Plant Cell 9 (1997) 185-197
58. Wendland M., and Subramani S. Cytosol-dependent peroxisomal protein import in a permeabilized cell system. J. Cell Biol. 120 (1993) 675-685
59. Hausler T., Stierhof Y.D., Wirtz E., and Clayton C. Import of a DHFR hybrid protein into glycosomes in vivo is not inhibited by the folate-analogue aminopterin. J. Cell Biol. 132 (1996) 311-324
60. Purdue P.E., Allsop J., Isaya G., Rosenberg L.E., and Danpure C.J. Mistargeting of peroxisomal l-alanine:glyoxylate aminotransferase to mitochondria in primary hyperoxaluria patients depends upon activation of a cryptic mitochondrial targeting sequence by a point mutation. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 10900-10904
61. Zhang X., Roe S.M., Hou Y., Bartlam M., Rao Z., Pearl L.H., and Danpure C.J. Crystal structure of alanine: glyoxylate aminotransferase and the relationship between genotype and enzymatic phenotype in primary hyperoxaluria type 1. J. Mol. Biol. 331 (2003) 643-652
62. Yang X., Purdue P.E., and Lazarow P.B. Eci1p uses a PTS1 to enter peroxisomes: either its own or that of a partner, Dci1p. Eur. J. Cell Biol. 80 (2001) 126-138
63. Geisbrecht B.V., Schulz K., Nau K., Geraghty M.T., Schulz H., Erdmann R., and Gould S.J. Preliminary characterization of Yor180Cp: identification of a novel peroxisomal protein of Saccharomyces cerevisiae involved in fatty acid metabolism. Biochem. Biophys. Res. Commun. 260 (1999) 28-34
64. Stewart M.Q., Esposito R.D., Gowani J., and Goodman J.M. Alcohol oxidase and dihydroxyacetone synthase, the abundant peroxisomal proteins of methylotrophic yeasts, assemble in different cellular compartments. J. Cell Sci. 114 (2001) 2863-2868
65. Evers M.E., Titorenko V., Harder W., ven der Klei I., and Veenhuis M. Flavin adenine dinucleotide binding is the crucial step in alcohol oxidase assembly in the yeast Hansenula polymorpha. Yeast 12 (1996) 917-923
66. Faber K.N., van Dijk R., Keizer-Gunnink I., Koek A., van der Klei I.J., and Veenhuis M. Import of assembled PTS1 proteins into peroxisomes of the yeast Hansenula polymorpha: yes and no!. Biochim. Biophys. Acta 1591 (2002) 157-162
67. Wimmer B., Lottspeich F., van der Klei I., Veenhuis M., and Gietl C. The glyoxysomal and plastid molecular chaperones (70-kDa heat shock protein) of watermelon cotyledons are encoded by a single gene. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 13624-13629
68. Stewart M.Q., van Dijk R., Veenhuis M., and Goodman J.M. Monomeric alcohol oxidase is preferentially digested by a novel protease from Candida boidinii. Biochim. Biophys. Acta 1542 (2002) 160-172
69. Titorenko V.I., Nicaud J.M., Wang H., Chan H., and Rachubinski R.A. Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. J. Cell Biol. 156 (2002) 481-494
70. Brocard C.B., Jedeszko C., Song H.C., Terlecky S.R., and Walton P.A. Protein structure and import into the peroxisomal matrix. Traffic 4 (2003) 74-82
71. Crookes W.J., and Olsen L.J. The effects of chaperones and the influence of protein assembly on peroxisomal protein import. J. Biol. Chem. 273 (1998) 17236-17242
72. Harper C.C., Berg J.M., and Gould S.J. PEX5 binds the PTS1 independently of Hsp70 and the peroxin PEX12. J. Biol. Chem. 278 (2003) 7897-7901
73. Legakis J.E., and Terlecky S.R. PTS2 protein import into mammalian peroxisomes. Traffic 2 (2001) 252-260
74. Walton P.A., Wendland M., Subramani S., Rachubinski R.A., and Welch W.J. Involvement of 70-kD heat-shock proteins in peroxisomal import. J. Cell Biol. 125 (1994) 1037-1046
75. Diefenbach J., and Kindl H. The membrane-bound DnaJ protein located at the cytosolic site of glyoxysomes specifically binds the cytosolic isoform 1 of Hsp70 but not other Hsp70 species. Eur. J. Biochem. 267 (2000) 746-754
76. Ma C., Haslbeck M., Babujee L., Jahn O., and Reumann S. Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiol. 141 (2006) 47-60
77. Titorenko V.I., Smith J.J., Szilard R.K., and Rachubinski R.A. Pex20p of the yeast Yarrowia lipolytica is required for the oligomerization of thiolase in the cytosol and for its targeting to the peroxisome. J. Cell Biol. 142 (1998) 403-420
78. Dodt G., Braverman N., Wong C., Moser A., Moser H.W., Watkins P., Valle D., and Gould S.J. Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nat. Genet. 9 (1995) 115-125
79. Wiemer E.A., Nuttley W.M., Bertolaet B.L., Li X., Francke U., Wheelock M.J., Anne U.K., Johnson K.R., and Subramani S. Human peroxisomal targeting signal-1 receptor restores peroxisomal protein import in cells from patients with fatal peroxisomal disorders. J. Cell Biol. 130 (1995) 51-65
80. Rachubinski R.A., and Subramani S. How proteins penetrate peroxisomes. Cell 83 (1995) 525-528
81. Walter P., and Blobel G. Translocation of proteins across the endoplasmic reticulum. II. Signal recognition protein (SRP) mediates the selective binding to microsomal membranes of in-vitro-assembled polysomes synthesizing secretory protein. J. Cell Biol. 91 (1981) 551-556
82. Marzioch M., Erdmann R., Veenhuis M., and 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. 13 (1994) 4908-4918
83. Kunau W.H. Peroxisomes: the extended shuttle to the peroxisome matrix. Curr. Biol. 11 (2001) R659-R662
84. Erdmann R., and Schliebs W. Peroxisomal matrix protein import: the transient pore model. Nat. Rev., Mol. Cell Biol. 6 (2005) 738-742
85. Gouveia A.M., Guimaraes C.P., Oliveira M.E., Sa-Miranda C., and Azevedo J.E. Insertion of Pex5p into the peroxisomal membrane is cargo protein-dependent. J. Biol. Chem. 278 (2003) 4389-4392
86. Gouveia A.M., Reguenga C., Oliveira M.E., Sa-Miranda C., and Azevedo J.E. Characterization of peroxisomal Pex5p from rat liver. Pex5p in the Pex5p-Pex14p membrane complex is a transmembrane protein. J. Biol. Chem. 275 (2000) 32444-32451
87. Azevedo J.E., Costa-Rodrigues J., Guimaraes C.P., Oliveira M.E., and Sa-Miranda C. Protein translocation across the peroxisomal membrane. Cell Biochem. Biophys. 41 (2004) 451-468
88. Kerssen D., Hambruch E., Klaas W., Platta H.W., de Kruijff B., Erdmann R., Kunau W.H., and Schliebs W. Membrane association of the cycling peroximase import receptor Pex5p. J. Biol. Chem. 281 (2006) 27003-27015
89. Gouveia A.M., Guimaraes C.P., Oliveira M.E., Reguenga C., Sa-Miranda C., and Azevedo J.E. Characterization of the peroxisomal cycling receptor, Pex5p, using a cell-free in vitro import system. J. Biol. Chem. 278 (2003) 226-230
90. Zhang J.W., and Lazarow P.B. 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. 129 (1995) 65-80
91. Zhang J.W., and Lazarow P.B. Peb1p (Pas7p) is an intraperoxisomal receptor for the NH2-terminal, type 2, peroxisomal targeting sequence of thiolase: Peb1p itself is targeted to peroxisomes by an NH2-terminal peptide. J. Cell Biol. 132 (1996) 325-334
92. Elgersma Y., Elgersma-Hooisma M., Wenzel T., McCaffery J.M., Farquhar M.G., and Subramani S. A mobile PTS2 receptor for peroxisomal protein import in Pichia pastoris. J. Cell Biol. 140 (1998) 807-820
93. Braverman N., Steel G., Obie C., Moser A., Moser H., Gould S.J., and Valle D. Human PEX7 encodes the peroxisomal PTS2 receptor and is responsible for rhizomelic chondrodysplasia punctata. Nat. Genet. 15 (1997) 369-376
94. Mukai S., Ghaedi K., and Fujiki Y. Intracellular localization, function, and dysfunction of the peroxisome-targeting signal type 2 receptor, Pex7p, in mammalian cells. J. Biol. Chem. 277 (2002) 9548-9561
95. Purdue P.E., Yang X., and Lazarow P.B. Pex18p and Pex21p, a novel pair of related peroxins essential for peroxisomal targeting by the PTS2 pathway. J. Cell Biol. 143 (1998) 1859-1869
96. Otzen M., Wang D., Lunenborg M.G., and van der Klei I.J. Hansenula polymorpha Pex20p is an oligomer that binds the peroxisomal targeting signal 2 (PTS2). J. Cell Sci. 118 (2005) 3409-3418
97. Matsumura T., Otera H., and Fujiki Y. Disruption of the interaction of the longer isoform of Pex5p, Pex5pL, with Pex7p abolishes peroxisome targeting signal type 2 protein import in mammals. Study with a novel Pex5-impaired Chinese hamster ovary cell mutant. J. Biol. Chem. 275 (2000) 21715-21721
98. Otera H., Harano T., Honsho M., Ghaedi K., Mukai S., Tanaka A., Kawai A., Shimizu N., and 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. 275 (2000) 21703-21714
99. Dodt G., Warren D., Becker E., Rehling P., and Gould S.J. Domain mapping of human PEX5 reveals functional and structural similarities to Saccharomyces cerevisiae Pex18p and Pex21p. J. Biol. Chem. 276 (2001) 41769-41781
100. Einwächter H., Sowinski S., Kunau W.H., and Schliebs W. Yarrowia lipolytica Pex20p, Saccharomyces cerevisiae Pex18p/Pex21p and mammalian Pex5pL fulfill a common function in the early steps of the peroxisomal PTS2 import pathway. EMBO Rep. 2 (2001) 1035-1039
101. Purdue P.E., and Lazarow P.B. Pex18p is constitutively degraded during peroxisome biogenesis. J. Biol. Chem. 276 (2001) 47684-47689
102. Schäfer A., Kerssen D., Veenhuis M., Kunau W.H., and Schliebs W. Functional similarity between the peroxisomal PTS2 receptor binding protein Pex18p and the N-terminal half of the PTS1 receptor Pex5p. Mol. Cell Biol. 24 (2004) 8895-8906
103. Smith J.J., and Rachubinski R.A. A role for the peroxin Pex8p in Pex20p-dependent thiolase import into peroxisomes of the yeast Yarrowia lipolytica. J. Biol. Chem. 276 (2001) 1618-1625
104. Bottger G., Barnett P., Klein A.T., Kragt A., Tabak H.F., and Distel B. 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 (2000) 3963-3976
105. Albertini M., Rehling P., Erdmann R., Girzalsky W., Kiel J.A., Veenhuis M., and Kunau W.H. Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell 89 (1997) 83-92
106. Niederhoff K., Meindl-Beinker N.M., Kerssen D., Perband U., Schafer A., Schliebs W., and Kunau W.H. Yeast Pex14p possesses two functionally distinct Pex5p and one Pex7p binding sites. J. Biol. Chem. 280 (2005) 35571-35578
107. Girzalsky W., Rehling P., Stein K., Kipper J., Blank L., Kunau W.H., and Erdmann R. Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J. Cell Biol. 144 (1999) 1151-1162
108. Wang D., Visser N.V., Veenhuis M., and van der Klei I.J. Physical interactions of the peroxisomal targeting signal 1 receptor Pex5p, studied by fluorescence correlation spectroscopy. J. Biol. Chem. 278 (2003) 43340-43345
109. Waterham H.R., Titorenko V.I., Haima P., Cregg J.M., Harder W., and 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. 127 (1994) 737-749
110. Oliveira M.E., Gouveia A.M., Pinto R.A., Sa-Miranda C., and Azevedo J.E. The energetics of Pex5p-mediated peroxisomal protein import. J. Biol. Chem. 278 (2003) 39483-39488
111. Costa-Rodrigues J., Carvalho A.F., Gouveia A.M., Fransen M., Sa-Miranda C., and Azevedo J.E. The N terminus of the peroxisomal cycling receptor, Pex5p, is required for redirecting the peroxisome-associated peroxin back to the cytosol. J. Biol. Chem. 279 (2004) 46573-46579
112. Ghys K., Fransen M., Mannaerts G.P., and Van Veldhoven P.P. Functional studies on human Pex7p: subcellular localisation and interaction with proteins containing a peroxisome targeting signal type 2 and other peroxins. Biochem. J. 365 (2002) 41-50
113. van der Klei I.J., Hilbrands R.E., Kiel J.A., Rasmussen S.W., Cregg J.M., and Veenhuis M. The ubiquitin-conjugating enzyme Pex4p of Hansenula polymorpha is required for efficient functioning of the PTS1 import machinery. EMBO J. 17 (1998) 3608-3618
114. Faber K.N., Heyman J.A., and Subramani S. 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 (1998) 936-943
115. Romisch K. Endoplasmic reticulum-associated degradation. Annu. Rev. Cell Dev. Biol. 21 (2005) 435-456
116. Zolman B.K., Monroe-Augustus M., Silva I.D., and Bartel B. Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22. Plant Cell 17 (2005) 3422-3435
117. Eckert J.H., and Johnsson N. Pex10p links the ubiquitin conjugating enzyme Pex4p to the protein import machinery of the peroxisome. J. Cell Sci. 116 (2003) 3623-3634
118. Shiozawa K., Maita N., Tomii K., Seto A., Goda N., Akiyama Y., Shimizu T., Shirakawa M., and Hiroaki H. Structure of the N-terminal domain of PEX1 AAA-ATPase. Characterization of a putative adaptor-binding domain. J. Biol. Chem. 279 (2004) 50060-50068
119. Yahraus T., Braverman N., Dodt G., Kalish J.E., Morrell J.C., Moser H.W., Valle D., and Gould S.J. The peroxisome biogenesis disorder group 4 gene, PXAAA1, encodes a cytoplasmic ATPase required for stability of the PTS1 receptor. EMBO J. 15 (1996) 2914-2923
120. Zolman B.K., and Bartel B. An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 1786-1791
121. Urquhart A.J., Kennedy D., Gould S.J., and Crane D.I. Interaction of Pex5p, the type 1 peroxisome targeting signal receptor, with the peroxisomal membrane proteins Pex14p and Pex13p. J. Biol. Chem. 275 (2000) 4127-4136
122. Farre J.C., and Subramani S. Peroxisome turnover by micropexophagy: an autophagy-related process. Trends Cell Biol. 14 (2004) 515-523