Structural basis for docking of peroxisomal membrane protein carrier Pex19p onto its receptor Pex3p

EMBO Journal

Volumn 29, Issue 24, 2010, Pages 4083-4093

  Sato, Yasuhiko ^a   Shibata, Hiroyuki ^b   Nakatsu, Toru ^a,d   Nakano, Hiroaki ^a   Kashiwayama, Yoshinori ^c   Imanaka, Tsuneo ^c   Kato, Hiroaki ^a,d  

^a KYOTO UNIVERSITY   (Japan)

^b NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^c UNIVERSITY OF TOYAMA   (Japan)

^d RIKEN SPring 8 Center ^*  (Japan)

Author keywords

crystal structure; peroxin; peroxisomal membrane protein; protein protein interactions

Indexed keywords

CARRIER PROTEIN; DOCKING PROTEIN; LEUCINE; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; PEROXIN 13; PEROXIN 13 RECEPTOR; PEROXIN 19; PEROXISOMAL MEMBRANE PROTEIN; PHENYLALANINE; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BIOGENESIS; CONTROLLED STUDY; CYTOSOL; HUMAN; HUMAN CELL; MOLECULAR DOCKING; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; BINDING SITES; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; LIPOPROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, QUATERNARY; SEQUENCE ALIGNMENT;

EID: 78650269198     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.293     Document Type: Article

References (41)

1. Abe Y, Shodai T, Muto T, Mihara K, Torii H, Nishikawa S, Endo T, Kohda D (2000) Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100: 551-560
2. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221
3. Chen YH, Yang JT, Martinez HM (1972) Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion. Biochemistry 11 : 4120-4131
4. Distel B, Erdmann R, Gould SJ, Blobel G, Crane DI, Cregg JM, Dodt G, Fujiki Y, Goodman JM, Just WW, Kiel JA, Kunau WH, Lazarow PB, Mannaerts GP, Moser HW, Osumi T, Rachubinski RA, Roscher A, Subramani S, Tabak HF, Tsukamoto T, Valle D, van der Klei I, van Veldhoven PP, Veenhuis M (1996) A unified nomenclature for peroxisome biogenesis factors. J Cell Biol 135: 1-3
5. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208
6. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132
7. Fang Y, Morrell JC, Jones JM, Gould SJ (2004) PEX3 functions as a PEX19 docking factor in the import of class I peroxisomal membrane proteins. J Cell Biol 164: 863-875
8. 0s domain structure by pentapeptide scanning mutagenesis. J Mol Biol 346: 1275-1286
9. Fujiki Y, Matsuzono Y, Matsuzaki T, Fransen M (2006) Import of peroxisomal membrane proteins: the interplay of Pex3p- and Pex19p-mediated interactions. Biochim Biophys Acta 1763: 1639-1646
10. Geuze HJ, Murk JL, Stroobants AK, Griffith JM, Kleijmeer MJ, Koster AJ, Verkleij AJ, Distel B, Tabak HF (2003) Involvement of the endoplasmic reticulum in peroxisome formation. Mol Biol Cell 14: 2900-2907
11. Ghaedi K, Kawai A, Okumoto K, Tamura S, Shimozawa N, Suzuki Y, Kondo N, Fujiki Y (1999) Isolation and characterization of novel peroxisome biogenesis-defective Chinese hamster ovary cell mutants using green fluorescent protein. Exp Cell Res 248: 489-497
12. Ghaedi K, Tamura S, Okumoto K, Matsuzono Y, Fujiki Y (2000) The peroxin pex3p initiates membrane assembly in peroxisome biogenesis. Mol Biol Cell 11 : 2085-2102
13. Hendrickson WA, Horton JR, LeMaster DM (1990) Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J 9: 1665-1672
14. Hoepfner D, Schildknegt D, Braakman I, Philippsen P, Tabak HF (2005) Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122: 85-95
15. Imanaka T, Shiina Y, Takano T, Hashimoto T, Osumi T (1996) Insertion of the 70-kDa peroxisomal membrane protein into peroxisomal membranes in vivo and in vitro. J Biol Chem 271: 3706-3713 (Pubitemid 26065689)
16. Jones JM, Morrell JC, Gould SJ (2004) PEX19 is a predominantly cytosolic chaperone and import receptor for class 1 peroxisomal membrane proteins. J Cell Biol 164: 57-67
17. Kammerer S, Holzinger A, Welsch U, Roscher AA (1998) Cloning and characterization of the gene encoding the human peroxiso-mal assembly protein Pex3p. FEBS Lett 429: 53-60
18. Kashiwayama Y, Asahina K, Shibata H, Morita M, Muntau AC, Roscher AA, Wanders RJ, Shimozawa N, Sakaguchi M, Kato H, Imanaka T (2005) Role of Pex19p in the targeting of PMP70 to peroxisome. Biochim Biophys Acta 1746: 116-128
19. Kim PK, Mullen RT, Schumann U, Lippincott-Schwartz J (2006) The origin and maintenance of mammalian peroxisomes involves a de novo PEX16-dependent pathway from the ER. J Cell Biol 173: 521-532
20. Kinoshita N, Ghaedi K, Shimozawa N, Wanders RJ, Matsuzono Y, Imanaka T, Okumoto K, Suzuki Y, Kondo N, Fujiki Y (1998) Newly identified Chinese hamster ovary cell mutants are defective in biogenesis of peroxisomal membrane vesicles (Peroxisomal ghosts), representing a novel complementation group in mammals. J Biol Chem 273: 24122-24130
21. Lazarow PB, Fujiki Y (1985) Biogenesis of peroxisomes. Annu Rev Cell Biol 1: 489-530
22. Matsuzono Y, Kinoshita N, Tamura S, Shimozawa N, Hamasaki M, Ghaedi K, Wanders RJ, Suzuki Y, Kondo N, Fujiki Y (1999) Human PEX19: cDNA cloning by functional complementation, mutation analysis in a patient with Zellweger syndrome, and potential role in peroxisomal membrane assembly. Proc Natl Acad Sci USA 96: 2116-2121
23. Matsuzono Y, Matsuzaki T, Fujiki Y (2006) Functional domain mapping of peroxin Pex19p: interaction with Pex3p is essential for function and translocation. J Cell Sci 119: 3539-3550
24. Muntau AC, Mayerhofer PU, Paton BC, Kammerer S, Roscher AA (2000) Defective peroxisome membrane synthesis due to mutations in human PEX3 causes Zellweger syndrome, complementation group G. Am J Hum Genet 67: 967-975
25. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macro-molecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255
26. Osumi T, Tsukamoto T, Hata S, Yokota S, Miura S, Fujiki Y, Hijikata M, Miyazawa S, Hashimoto T (1991) Amino-terminal prese-quence of the precursor of peroxisomal 3-ketoacyl-CoA thiolase is a cleavable signal peptide for peroxisomal targeting. Biochem Biophys Res Commun 181: 947-954
27. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. In Methods in Enzymology, CW Carter J, Sweet RM (eds), Vol. 276, pp 307-326.
28. New York: Academic Press Pinto MP, Grou CP, Fransen M, Sa-Miranda C, Azevedo JE (2009) The cytosolic domain of PEX3, a protein involved in the biogenesis of peroxisomes, binds membrane lipids. Biochim Biophys Acta 1793: 1669-1675
29. Platta HW, Erdmann R (2007) Peroxisomal dynamics. Trends Cell Biol 17: 474-484
30. Saitoh T, Igura M, Obita T, Ose T, Kojima R, Maenaka K, Endo T, Kohda D (2007) Tom20 recognizes mitochondrial presequences through dynamic equilibrium among multiple bound states. EMBO J 26: 4777-4787
31. Sato Y, Shibata H, Nakano H, Matsuzono Y, Kashiwayama Y, Kobayashi Y, Fujiki Y, Imanaka T, Kato H (2008) Characterization of the interaction between recombinant human peroxin Pex3p and Pex19p: identification of TRP-104 IN Pex3p as a critical residue for the interaction. J Biol Chem 283: 6136-6144
32. Schmidt F, Treiber N, Zocher G, Bjelic S, Steinmetz MO, Kalbacher H, Stehle T, Dodt G (2010) Insights into peroxisome function from the structure of PEX3 in complex with a soluble fragment of PEX19. J Biol Chem 285: 25410-25417
33. Schueller N, Holton SJ, Fodor K, Milewski M, Konarev P, Stanley WA, Wolf J, Erdmann R, Schliebs W, Song YH, Wilmanns M (2010) The peroxisomal receptor Pex19p forms a helical mPTS recognition domain. EMBO J 29: 2491-2500
34. Shibata H, Kashiwayama Y, Imanaka T, Kato H (2004) Domain architecture and activity of human Pex19p, a chaperone-like protein for intracellular trafficking of peroxisomal membrane proteins. J Biol Chem 279: 38486-38494
35. Shimozawa N, Suzuki Y, Zhang Z, Imamura A, Ghaedi K, Fujiki Y, Kondo N (2000) Identification of PEX3 as the gene mutated in a Zellweger syndrome patient lacking peroxisomal remnant structures. Hum Mol Genet 9: 1995-1999
36. Soukupova M, Sprenger C, Gorgas K, Kunau WH, Dodt G (1999) Identification and characterization of the human peroxin PEX3. Eur J Cell Biol 78: 357-374 (Pubitemid 29317372)
37. van der Zand A, Braakman I, Tabak H (2010) Peroxisomal membrane proteins insert into the endoplasmic reticulum. Mol Biol Cell 21 : 2057-2065
38. Visser WF, van Roermund CW, Ijlst L, Waterham HR, Wanders RJ (2007) Metabolite transport across the peroxisomal membrane. Biochem J 401: 365-375
39. Wickner W, Schekman R (2005) Protein translocation across biological membranes. Science 310 : 1452-1456
40. Wiedemann N, van der Laan M, Pfanner N (2009) SnapShot: import and sorting of mitochondrial proteins. Cell 138: 808-808.e1
41. Young JC, Hoogenraad NJ, Hartl FU (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112: 41-50