A cargo-centered perspective on the PEX5 receptor-mediated peroxisomal protein import pathway

Journal of Biological Chemistry

Volumn 288, Issue 40, 2013, Pages 29151-29159

  Francisco, Tânia ^a,b   Rodrigues, Tony A ^a,b   Freitas, Marta O ^a,b   Grou, Cláudia P ^a   Carvalho, Andreia F ^a   Sá Miranda, Clara ^a   Pinto, Manuel P ^a   Azevedo, Jorge E ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

PEROXISOMAL MEMBRANES; PROTEIN IMPORT PATHWAYS; SOLUBLE RECEPTOR;

MACHINERY;

CYTOLOGY;

MATRIX PROTEIN; MEMBRANE PROTEIN; PROTEIN PEX5; RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL ORGANELLE; CENTRIFUGATION; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; LIVER; MOUSE; NONHUMAN; PEROXISOME; PLASMID; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SUCROSE GRADIENT;

IN VITRO IMPORT ASSAYS; PEROXISOMES; PEX5; PROTEIN SORTING; PROTEIN TRANSLOCATION; PTS1 PROTEIN; SUBCELLULAR ORGANELLES; UBIQUITINATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CARRIER PROTEINS; CYTOSOL; HUMANS; MICE; MODELS, BIOLOGICAL; PEROXISOMES; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; TEMPERATURE;

EID: 84885091904     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.487140     Document Type: Article

References (62)

1. Lazarow, P. B., and Fujiki, Y. (1985) Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1, 489-530
2. Brocard, C., and Hartig, A. (2006) Peroxisome targeting signal 1: is it really a simple tripeptide? Biochim. Biophys. Acta 1763, 1565-1573
3. 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
4. Kunze, M., Neuberger, G., Maurer-Stroh, S., Ma, J., Eck, T., Braverman, N., Schmid, J. A., Eisenhaber, F., and Berger, J. (2011) Structural requirements for interaction of peroxisomal targeting signal 2 and its receptor PEX7. J. Biol. Chem. 286, 45048-45062
5. Lazarow, P. B. (2006) The import receptor Pex7p and the PTS2 targeting sequence. Biochim. Biophys. Acta 1763, 1599-1604
6. 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
7. Carvalho, A. F., Costa-Rodrigues, J., Correia, I., Costa Pessoa, J., Faria, T. Q., Martins, C. L., Fransen, M., Sá-Miranda, C., and Azevedo, J. E. (2006) The N-terminal half of the peroxisomal cycling receptor Pex5p is a natively unfolded domain. J. Mol. Biol. 356, 864-875
8. Costa-Rodrigues, J., Carvalho, A. F., Fransen, M., Hambruch, E., Schliebs, W., Sá-Miranda, C., and Azevedo, J. E. (2005) Pex5p, the peroxisomal cycling receptor, is a monomeric non-globular protein. J. Biol. Chem. 280, 24404-24411
9. Shiozawa, K., Konarev, P. V., Neufeld, C., Wilmanns, M., and Svergun, D. I. (2009) Solution structure of human Pex5Pex14PTS1 protein complexes obtained by small angle X-ray scattering. J. Biol. Chem. 284, 25334-25342
10. Dodt, G., and Gould, S. J. (1996) 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
11. 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
12. Gatto, G. J., Jr., Geisbrecht, B. V., Gould, S. J., and Berg, J. M. (2000) A proposed model for the PEX5-peroxisomal targeting signal-1 recognition complex. Proteins 38, 241-246
13. Gunkel, K., van Dijk, R., Veenhuis, M., and van der Klei, I. J. (2004) Routing of Hansenula polymorpha alcohol oxidase: an alternative peroxisomal protein-sorting machinery. Mol. Biol. Cell 15, 1347-1355
14. Klein, A. T., van den Berg, M., Bottger, G., Tabak, H. F., and Distel, B. (2002) Saccharomyces cerevisiae acyl-CoA oxidase follows a novel, non-PTS1, import pathway into peroxisomes that is dependent on Pex5p. J. Biol. Chem. 277, 25011-25019
15. Oshima, Y., Kamigaki, A., Nakamori, C., Mano, S., Hayashi, M., Nishimura, M., and Esaka, M. (2008) Plant catalase is imported into per-oxisomes by Pex5p but is distinct from typical PTS1 import. Plant Cell Physiol. 49, 671-677
16. Titorenko, V. I., Nicaud, J. M., Wang, H., Chan, H., and Rachubinski, R. A. (2002) Acyl-CoA oxidase is imported as a heteropentameric, cofactorcontaining complex into peroxisomes of Yarrowia lipolytica. J. Cell Biol. 156, 481-494
17. Braverman, N., Dodt, G., Gould, S. J., and Valle, D. (1998) An isoform of pex5p, the human PTS1 receptor, is required for the import of PTS2 proteins into peroxisomes. Hum. Mol. Genet. 7, 1195-1205
18. Galland, N., Demeure, F., Hannaert, V., Verplaetse, E., Vertommen, D., Van der Smissen, P., Courtoy, P. J., and Michels, P. A. (2007) Characterization of the role of the receptors PEX5 and PEX7 in the import of proteins into glycosomes of Trypanosoma brucei. Biochim. Biophys. Acta 1773, 521-535
19. 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
20. Woodward, A. W., and Bartel, B. (2005) The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Mol. Biol. Cell 16, 573-583
21. Dodt, G., Warren, D., Becker, E., Rehling, P., and Gould, S. J. (2001) Domain mapping of human PEX5 reveals functional and structural similarities to Saccharomyces cerevisiae Pex18p and Pex21p. J. Biol. Chem. 276, 41769-41781
22. Schliebs, W., and Kunau, W. H. (2006) PTS2 co-receptors: diverse proteins with common features. Biochim. Biophys. Acta 1763, 1605-1612
23. Grou, C. P., Carvalho, A. F., Pinto, M. P., Alencastre, I. S., Rodrigues, T. A., Freitas, M. O., Francisco, T., Sá-Miranda, C., and Azevedo, J. E. (2009) The peroxisomal protein import machinery-a case report of transient ubiquitination with a new flavor. Cell. Mol. Life Sci. 66, 254-262
24. Hu, J., Baker, A., Bartel, B., Linka, N., Mullen, R. T., Reumann, S., and Zolman, B. K. (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24, 2279-2303
25. Liu, X., Ma, C., and Subramani, S. (2012) Recent advances in peroxisomal matrix protein import. Curr. Opin Cell Biol. 24, 484-489
26. Platta, H. W., Hagen, S., and Erdmann, R. (2013) The exportomer: the peroxisomal receptor export machinery. Cell. Mol. Life Sci. 70, 1393-1411
27. Agne, B., Meindl, N. M., Niederhoff, K., Einwächter, 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
28. Oeljeklaus, S., Reinartz, B. S., Wolf, J., Wiese, S., Tonillo, J., Podwojski, K., Kuhlmann, K., Stephan, C., Meyer, H. E., Schliebs, W., Brocard, C., Erdmann, R., and Warscheid, B. (2012) Identification of core components and transient interactors of the peroxisomal importomer by dual-track stable isotope labeling with amino acids in cell culture analysis. J. Proteome Res. 11, 2567-2580
29. Reguenga, C., Oliveira, M. E., Gouveia, A. 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
30. Gouveia, A. M., Guimarães, C. P., Oliveira, M. E., Sá-Miranda, C., and Azevedo, J. E. (2003) Insertion of Pex5p into the peroxisomal membrane is cargo protein-dependent. J. Biol. Chem. 278, 4389-4392
31. Gouveia, A. M., Reguenga, C., Oliveira, M. E., Sa-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
32. Carvalho, A. F., Pinto, M. P., Grou, C. P., Alencastre, I. S., Fransen, M., Sá-Miranda, C., and Azevedo, J. E. (2007) Ubiquitination of mammalian Pex5p, the peroxisomal import receptor. J. Biol. Chem. 282, 31267-31272
33. Williams, C., van den Berg, M., Sprenger, R. R., and Distel, B. (2007) A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p. J. Biol. Chem. 282, 22534-22543
34. Platta, H. W., El Magraoui, F., Schlee, D., Grunau, S., Girzalsky, W., and Erdmann, R. (2007) Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. J. Cell Biol. 177, 197-204
35. 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
36. 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
37. Debelyy, M. O., Platta, H. W., Saffian, D., Hensel, A., Thoms, S., Meyer, H. E., Warscheid, B., Girzalsky, W., and Erdmann, R. (2011) Ubp15p, a ubiquitin hydrolase associated with the peroxisomal export machinery. J. Biol. Chem. 286, 28223-28234
38. Grou, C. P., Carvalho, A. F., Pinto, M. P., Huybrechts, S. J., Sá-Miranda, C., Fransen, M., and Azevedo, J. E. (2009) Properties of the ubiquitin-pex5p thiol ester conjugate. J. Biol. Chem. 284, 10504-10513
39. Grou, C. P., Francisco, T., Rodrigues, T. A., Freitas, M. O., Pinto, M. P., Carvalho, A. F., Domingues, P., Wood, S. A., Rodríguez-Borges, J. E., Sá-Miranda, C., Fransen, M., and Azevedo, J. E. (2012) Identification of ubiquitin-specific protease 9X (USP9X) as a deubiquitinase acting on ubiquitin-peroxin 5 (PEX5) thioester conjugate. J. Biol. Chem. 287, 12815-12827
40. Alencastre, I. S., Rodrigues, T. A., Grou, C. P., Fransen, M., Sá-Miranda, C., and Azevedo, J. E. (2009) Mapping the cargo protein membrane translocation step into the PEX5 cycling pathway. J. Biol. Chem. 284, 27243-27251
41. Seedorf, U., Raabe, M., and Assmann, G. (1993) Cloning, expression and sequences of mouse sterol-carrier protein-x-encoding cDNAs and a related pseudogene. Gene 123, 165-172
42. Gallegos, A. M., Atshaves, B. P., Storey, S. M., Starodub, O., Petrescu, A. D., Huang, H., McIntosh, A. L., Martin, G. G., Chao, H., Kier, A. B., and Schroeder, F. (2001) Gene structure, intracellular localization, and functional roles of sterol carrier protein-2. Prog. Lipid Res. 40, 498-563
43. Fransen, M., Terlecky, S. R., and Subramani, S. (1998) Identification of a human PTS1 receptor docking protein directly required for peroxisomal protein import. Proc. Natl. Acad. Sci. U.S.A. 95, 8087-8092
44. Carvalho, A. F., Grou, C. P., Pinto, M. P., Alencastre, I. S., Costa-Rodrigues, J., Fransen, M., Sá-Miranda, C., and Azevedo, J. E. (2007) Functional characterization of two missense mutations in Pex5p-C11S and N526K. Biochim. Biophys. Acta 1773, 1141-1148
45. Dodt, G., Braverman, N., Wong, C., 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
46. Gatto, G. J., Jr., Geisbrecht, B. V., Gould, S. J., and Berg, J. M. (2000) Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat. Struct. Biol. 7, 1091-1095
47. Pinto, M. P., Grou, C. P., Alencastre, I. S., Oliveira, M. E., Sá-Miranda, C., Fransen, M., and Azevedo, J. E. (2006) The import competence of a peroxisomal membrane protein is determined by Pex19p before the docking step. J. Biol. Chem. 281, 34492-34502
48. De Nys, K., Meyhi, E., Mannaerts, G. P., Fransen, M., and Van Veldhoven, P. P. (2001) Characterisation of human peroxisomal 2,4-dienoyl-CoA reductase. Biochim. Biophys. Acta 1533, 66-72
49. Gouveia, A. M., Guimaraes, C. P., Oliveira, M. E., Reguenga, C., Sa-Miranda, C., and Azevedo, J. E. (2003) Characterization of the peroxisomal cycling receptor, Pex5p, using a cell-free in vitro import system. J. Biol. Chem. 278, 226-232
50. Oliveira, M. E., Gouveia, A. M., Pinto, R. A., Sá-Miranda, C., and Azevedo, J. E. (2003) The energetics of Pex5p-mediated peroxisomal protein import. J. Biol. Chem. 278, 39483-39488
51. Szilard, R. K., and Rachubinski, R. A. (2000) Tetratricopeptide repeat domain of Yarrowia lipolytica Pex5p is essential for recognition of the type 1 peroxisomal targeting signal but does not confer full biological activity on Pex5p. Biochem. J. 346, 177-184
52. Schliebs, W., Saidowsky, J., Agianian, 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
53. 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
54. Hartl, F. U., Just, W. W., Köster, A., and Schimassek, H. (1985) Improved isolation and purification of rat liver peroxisomes by combined rate zonal and equilibrium density centrifugation. Arch Biochem. Biophys. 237, 124-134
55. Haas, A. L., Warms, J. V., and Rose, I. A. (1983) Ubiquitin adenylate: structure and role in ubiquitin activation. Biochemistry 22, 4388-4394
56. Hwang, S. T., and Schatz, G. (1989) Translocation of proteins across the mitochondrial inner membrane, but not into the outer membrane, requires nucleoside triphosphates in the matrix. Proc. Natl. Acad. Sci. U.S.A. 86, 8432-8436
57. Seedorf, U., Brysch, P., Engel, T., Schrage, K., and Assmann, G. (1994) Sterol carrier protein X is peroxisomal 3-oxoacyl coenzyme A thiolase with intrinsic sterol carrier and lipid transfer activity. J. Biol. Chem. 269, 21277-21283
58. Costa-Rodrigues, J., Carvalho, A. F., Gouveia, A. M., Fransen, M., Sá-Miranda, C., and Azevedo, J. E. (2004) 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, 46573-46579
59. Fujiki, Y., Matsuzono, Y., Matsuzaki, T., and Fransen, M. (2006) Import of peroxisomal membrane proteins: the interplay of Pex3p-and Pex19pmediated interactions. Biochim Biophys Acta 1763, 1639-1646
60. Azevedo, J. E., Costa-Rodrigues, J., Guimarães, C. P., Oliveira, M. E., and Sã-Miranda, C. (2004) Protein translocation across the peroxisomal membrane. Cell Biochem. Biophys. 41, 451-468
61. Nair, D. M., Purdue, P. E., and Lazarow, P. B. (2004) Pex7p translocates in and out of peroxisomes in Saccharomyces cerevisiae. J. Cell Biol. 167, 599-604
62. Oliveira, M. E., Reguenga, C., Gouveia, A. M., Guimarães, C. P., Schliebs, W., Kunau, W. H., Silva, M. T., Sá-Miranda, C., and Azevedo, J. E. (2002) Mammalian Pex14p: membrane topology and characterisation of the Pex14p-Pex14p interaction. Biochim. Biophys. Acta 1567, 13-22