PEX14 binding to Arabidopsis PEX5 has differential effects on PTS1 and PTS2 cargo occupancy of the receptor

FEBS Letters

Volumn 588, Issue 14, 2014, Pages 2223-2229

  Lanyon Hogg, Thomas ^a   Hooper, Jacob ^a   Gunn, Sarah ^a   Warriner, Stuart L ^a   Baker, Alison ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Arabidopsis thaliana; Cargo unloading; Peroxisome; PEX14; PEX5; PEX7; PTS1; PTS2

Indexed keywords

ACETYL COENZYME A ACETYLTRANSFERASE; MATRIX PROTEIN; PEROXISOMAL MATRIX PROTEIN 14; PEROXISOMAL MATRIX PROTEIN 5; PEROXISOMAL TARGETING SIGNAL PROTEIN 1; PEROXISOMAL TARGETING SIGNAL PROTEIN 2; TRIPEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANISOTROPY; ARABIDOPSIS THALIANA; ARTICLE; BINDING AFFINITY; CHEMOLUMINESCENCE; COMPLEX FORMATION; CONTROLLED STUDY; COVALENT BOND; CYTOSOL; FLUORESCENCE; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RECEPTOR BINDING;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS THALIANA; CARGO UNLOADING; PEROXISOME; PEX14; PEX5; PEX7; PTS1; PTS2;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; KINETICS; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REPRESSOR PROTEINS;

EID: 84902689128     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.05.038     Document Type: Article

References (48)

1. T. Lanyon-Hogg, S.L. Warriner, and A. Baker Getting a camel through the eye of a needle: the import of folded proteins by peroxisomes Biol. Cell 102 2010 245 263
2. R. Rucktaschel, W. Girzalsky, and R. Erdmann Protein import machineries of peroxisomes Biochim. Biophys. Acta 1808 2011 892 900
3. G. Lametschwandtner, C. Brocard, M. Fransen, P. Van Veldhoven, J. Berger, and A. Hartig 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. 273 1998 33635 33643
4. S. Reumann, S. Quan, K. Aung, P.F. Yang, K. Manandhar-Shrestha, D. Holbrook, N. Linka, R. Switzenberg, C.G. Wilkerson, A.P.M. Weber, L.J. Olsen, and J.P. Hu In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes Plant Physiol. 150 2009 125 143
5. R.A. Rachubinski, and S. Subramani How proteins penetrate peroxisomes Cell 83 1995 525 528
6. L.A. Brown, and A. Baker Shuttles and cycles: transport of proteins into the peroxisome matrix Mol. Membr. Biol. 25 2008 363 375
7. D.Q. Pan, T. Nakatsu, and H. Kato Crystal structure of peroxisomal targeting signal-2 bound to its receptor complex Pex7p-Pex21p Nat. Struct. Mol. Biol. 20 2013 987 993
8. M. Hayashi, M. Yagi, K. Nito, T. Kamada, and M. Nishimura Differential contribution of two peroxisomal protein receptors to the maintenance of peroxisomal functions in Arabidopsis J. Biol. Chem. 280 2005 14829 14835
9. A.W. Woodward, and B. Bartel The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5 Mol. Biol. Cell 16 2005 573 583
10. H. Otera, T. Harano, M. Honsho, K. Ghaedi, S. Mukai, A. Tanaka, A. Kawai, N. Shimizu, and Y. Fujiki 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
11. B. Agne, N.M. Meindl, K. Niederhoff, H. Einwachter, P. Rehling, A. Sickmann, H.E. Meyer, W. Girzalsky, and W.H. Kunau Pex8p: an intraperoxisomal organizer of the peroxisomal import machinery Mol. Cell 11 2003 635 646
12. J. Saidowsky, G. Dodt, K. Kirchberg, A. Wegner, W. Nastainczyk, W.H. Kunau, and W. Schliebs 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 2001 34524 34529
13. A. Neuhaus, H. Kooshapur, J. Wolf, N.H. Meyer, T. Madl, J. Saidowsky, E. Hambrunch, A. Lazam, M. Jung, M. Settler, W. Schliebs, and R. Erdman A novel PEX14 protein-interacting site of human PEX5 is critical for matrix protein import into peroxisomes J. Biol. Chem. 289 2014 437 448
14. D. Kerssen, E. Hambruch, W. Klaas, H.W. Platta, B. de Kruijff, R. Erdmann, W.H. Kunau, and W. Schliebs Membrane association of the cycling peroxisome import receptor Pex5p J. Biol. Chem. 281 2006 27003 27015
15. M. Meinecke, C. Cizmowski, W. Schliebs, V. Kruger, S. Beck, R. Wagner, and R. Erdmann The peroxisomal importomer constitutes a large and highly dynamic pore Nat. Cell Biol. 12 2010 273-U68
16. M.E. Oliveira, A.M. Gouveia, R.A. Pinto, C. Sa-Miranda, and J.E. Azevedo The energetics of Pex5p-mediated peroxisomal protein import J. Biol. Chem. 278 2003 39483 39488
17. N. Miyata, and Y. Fujiki Shuttling mechanism of peroxisome targeting signal type 1 receptor Pex5: ATP-independent import and ATP-dependent export Mol. Cell. Biol. 25 2005 10822 10832
18. C. Williams, M. van den Berg, E. Geers, and B. Distel Pex10p functions as an E3 ligase for the Ubc4p-dependent ubiquitination of Pex5p Biochem. Biophys. Res. Commun. 374 2008 620 624
19. J. Kiel, K. Emmrich, H.E. Meyer, and W.H. Kunau 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
20. C.C. Harper, J.M. Berg, and S.J. Gould PEX5 binds the PTS1 independently of Hsp70 and the peroxin PEX12 J. Biol. Chem. 278 2003 7897 7901
21. C.P. Grou, A.F. Carvalho, M.P. Pinto, S.J. Huybrechts, C. Sa-Miranda, M. Fransen, and J.E. Azevedo Properties of the ubiquitin-Pex5p thiol ester conjugate J. Biol. Chem. 284 2009 10504 10513
22. I.S. Alencastre, T.A. Rodrigues, C.P. Grou, M. Fransen, C. Sá-Miranda, and J.E. Azevedo Mapping the cargo protein membrane translocation step into the PEX5 cycling pathway J. Biol. Chem. 284 2009 27243 27251
23. C. Ma, D. Hagstrom, S.G. Polley, and S. Subramani Redox-regulated cargo binding and release by the peroxisomal targeting signal receptor, Pex5 J. Biol. Chem. 288 2013 27220 27231
24. M.O. Freitas, T. Francisco, T.A. Rodrigues, I.S. Alencastre, M.P. Pinto, C.P. Grou, A.F. Carvalho, M. Fransen, C. Sa-Miranda, and J.E. Azevedo PEX5 protein binds monomeric catalase blocking its tetramerization and releases it upon binding the N-terminal domain of PEX14 J. Biol. Chem. 286 2011 40509 40519
25. C. Williams, E. Bener Aksam, K. Gunkel, M. Veenhuis, and I.J. van der Klei The relevance of the non-canonical PTS1 of peroxisomal catalase Biochim. Biophys. Acta 1823 2012 1133 1141
26. P.E. Purdue, and P.B. Lazarow Targeting of human catalase to peroxisomes is dependent upon a novel COOH-terminal peroxisomal targeting sequence J. Cell Biol. 134 1996 849 862
27. Y. Oshima, A. Kamigaki, C. Nakamori, S. Mano, M. Hayashi, M. Nishimura, and M. Esaka Plant catalase is imported into peroxisomes by pex5p but is distinct from typical PTS1 import Plant Cell Physiol. 49 2008 671 677
28. K.P. Madrid, G. De Crescenzo, S.W. Wang, and A. Jardim Modulation of the Leishmania donovani peroxin 5 quaternary structure by peroxisomal targeting signal 1 ligands Mol. Cell. Biol. 24 2004 7331 7344
29. K. Nito, M. Hayashi, and M. Nishimura Direct interaction and determination of binding domains among peroxisomal import factors in Arabidopsis thaliana Plant Cell Physiol. 43 2002 355 366
30. S. Mitsuya, M. El-Shami, I.A. Sparkes, W.L. Charlton, M. Lousa Cde, B. Johnson, and A. Baker Salt stress causes peroxisome proliferation, but inducing peroxisome proliferation does not improve NaCl tolerance in Arabidopsis thaliana PloS One 5 2010 e9408
31. L.A. Brown, C. O'Leary-Steele, P. Brookes, L. Armitage, S. Kepinski, S.L. Warriner, and A. Baker A small molecule with differential effects on the PTS1 and PTS2 peroxisome matrix import pathways Plant J. 65 2011 980 990
32. V. Germain, E.L. Rylott, T.R. Larson, S.M. Sherson, N. Bechtold, J.P. Carde, J.H. Bryce, I.A. Graham, and S.M. Smith Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid beta-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings Plant J. 28 2001 1 12
33. G.J. Gatto, B.V. Geisbrecht, S.J. Gould, and J.M. Berg Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5 Nat. Struct. Biol. 7 2000 1091 1095
34. J. Costa-Rodrigues, A.F. Carvalho, M. Fransen, E. Hambruch, W. Schliebs, C. Sa-Miranda, and J.E. Azevedo Pex5p, the peroxisomal cycling receptor, is a monomeric non-globular protein J. Biol. Chem. 280 2005 24404 24411
35. A.F. Carvalho, J. Costa-Rodrigues, I. Correia, J.C. Pessoa, T.Q. Faria, C.L. Martins, M. Fransen, C. Sa-Miranda, and J.E. Azevedo The N-terminal half of the peroxisomal cycling receptor Pex5p is a natively unfolded domain J. Mol. Biol. 356 2006 864 875
36. K.B. Moscicka, S.H. Klompmaker, D.Y. Wang, I.J. van der Klei, and E.J. Boekema The Hansenula polymorpha peroxisomal targeting signal 1 receptor, Pex5p, functions as a tetramer FEBS Lett. 581 2007 1758 1762
37. S. Goepfert, C. Vidoudez, E. Rezzonico, J.K. Hiltunen, and Y. Poirier Molecular identification and characterization of the Arabidopsis Delta(3,5), Delta (2,4)-dienoyl-coenzyme A isomerase, a peroxisomal enzyme participating in the beta-oxidation cycle of unsaturated fatty acids Plant Physiol. 138 2005 1947 1956
38. I. Pracharoenwattana, J.E. Cornah, and S.M. Smith Arabidopsis peroxisomal malate dehydrogenase functions in beta-oxidation but not in the glyoxylate cycle Plant J. 50 2007 381 390
39. A.M. Gouveia, C.P. Guimaraes, M.E. Oliveira, C. Sa-Miranda, and J.E. Azevedo Insertion of Pex5p into the peroxisomal membrane is cargo protein-dependent J. Biol. Chem. 278 2003 4389 4392
40. T. Harano, S. Nose, R. Uezu, N. Shimizu, and Y. Fujiki Hsp70 regulates the interaction between the peroxisome targeting signal type 1 (PTS1)-receptor Pex5p and PTS1 Biochem. J. 357 2001 157 165
41. A.J. Urquhart, D. Kennedy, S.J. Gould, and D.I. Crane 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
42. K. Shiozawa, P.V. Konarev, C. Neufeld, M. Wilmanns, and D.I. Svergun Solution structure of human Pex5.Pex14.PTS1 protein complexes obtained by small angle X-ray scattering J. Biol. Chem. 284 2009 25334 25342
43. D. Ghosh, and J.M. Berg A proteome-wide perspective on peroxisome targeting signal 1(PTS1)-Pex5p affinities J. Am. Chem. Soc. 132 2010 3973 3979
44. W.A. Stanley, and M. Wilmanns Dynamic architecture of the peroxisomal import receptor Pex5p Biochim. Biophys. Acta 1763 2006 1592 1598
45. P. Bharti, W. Schliebs, T. Schievelbusch, A. Neuhaus, C. David, K. Kock, C. Herrmann, H.E. Meyer, S. Wiese, B. Warscheid, C. Theiss, and R. Erdmann PEX14 is required for microtubule-based peroxisome motility in human cells J. Cell Sci. 124 2011 1759 1768
46. S. Mukai, and Y. Fujiki Molecular mechanisms of import of peroxisome-targeting signal type 2 (PTS2) proteins by PTS2 receptor pex7p and PTS1 receptor Pex5pL J. Biol. Chem. 281 2006 37311 37320
47. J.R. Pires, X.J. Hong, C. Brockmann, R. Volkmer-Engert, J. Schneider-Mergener, H. Oschkinat, and R. Erdmann The ScPex13p SH3 domain exposes two distinct binding sites for Pex5p and Pex14p J. Mol. Biol. 326 2003 1427 1435
48. A. Schell-Steven, K. Stein, M. Amoros, C. Landgraf, R. Volkmer-Engert, H. Rottensteiner, and R. Erdmann Identification of a novel, intraperoxisomal Pex14-binding site in Pex13: association of Pex13 with the docking complex is essential for peroxisomal matrix protein import Mol. Cell. Biol. 25 2005 3007 3018