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Chaperone proteins and peroxisomal protein import

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Chaperones

Part of the book series: Topics in Current Genetics ((TCG,volume 16))

Abstract

Peroxisomes are ubiquitous organelles present in most eukaryotic cells. Their role in cellular metabolism is diverse among species. An array of genes involved in the formation and maintenance of peroxisomes has been discovered, and can be categorised into genes important for protein import into the peroxisome and genes involved in the maintenance of the organelles’ size and abundance. Thorough cell biological and biochemical studies revealed great detail about the process of peroxisomal protein import. Although involvement of several classes of molecular chaperone proteins in peroxisomal protein import has been demonstrated, details regarding the mechanistic aspects of chaperone involvement in this process are not known yet. This review aims to discuss peroxisomal maintenance, with the emphasis on protein import. A general overview of chaperone proteins and their role in protein import processes will be used as context to discuss the – possible – roles of chaperone proteins in peroxisomal protein import.

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References

  • 1. Agarraberes FA, Dice JF (2001) A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J Cell Sci 114:2491-2499

    PubMed  CAS  Google Scholar 

  • 2. Agarraberes FA, Terlecky SR, Dice JF (1997) An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J Cell Biol 137:825-834

    PubMed  CAS  Google Scholar 

  • 3. Agne B, Meindl NM, Niederhoff K, Einwachter H, Rehling P, Sickmann A, Meyer HE, Girzalsky W, Kunau W-H (2003) Pex8p: An intraperoxisomal organizer of the peroxisomal import machinery. Mol Cell 11:635-646

    PubMed  CAS  Google Scholar 

  • 4. Albertini M, Rehling P, Erdmann R, Girzalsky W, Kiel JAKW, Veenhuis M, Kunau W-H (1997) Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell 89:83-92

    PubMed  CAS  Google Scholar 

  • 5. Angeletti PC, Walker D, Panganiban AT, Wu Y, Hu Z, Thompson LJ, Yin LY, Patterson C (2002) Small glutamine-rich protein/viral protein U-binding protein is a novel cochaperone that affects heat shock protein 70 activity. Cell Stress Chaperones 7:258-268

    PubMed  CAS  Google Scholar 

  • 6. Artigues A, Iriarte A, Martinez-Carrion M (2002) Binding to chaperones allows import of a purified mitochondrial precursor into mitochondria. J Biol Chem 277:25047-25055

    PubMed  CAS  Google Scholar 

  • 7. Asai T, Takahashi T, Esaki M, Nishikawa S, Ohtsuka K, Nakai M, Endo T (2004) Reinvestigation of the requirement of cytosolic ATP for mitochondrial protein import. J Biol Chem 279:19464-19470. Epub 12004 Mar 19464

    PubMed  CAS  Google Scholar 

  • 8. Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin LY, Patterson C (1999) Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 19:4535-4545

    PubMed  CAS  Google Scholar 

  • 9. Becker J, Walter W, Yan W, Craig EA (1996) Functional interaction of cytosolic hsp70 and a DnaJ-related protein, Ydj1p, in protein translocation in vivo. Mol Cell Biol 16:4378-4386

    PubMed  CAS  Google Scholar 

  • 10. Behari R, Baker A (1993) The carboxyl terminus of isocitrate lyase is not essential for import into glyoxysomes in an in vitro system. J Biol Chem 268:7315-7322

    PubMed  CAS  Google Scholar 

  • 11. Bellion E, Goodman JM (1987) Proton ionophores prevent assembly of a peroxisomal protein. Cell 48:165-173

    PubMed  CAS  Google Scholar 

  • 12. Blond-Elguindi S, Cwirla SE, Dower WJ, Lipshutz RJ, Sprang SR, Sambrook JF, Gething MJ (1993) Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75:717-728

    PubMed  CAS  Google Scholar 

  • 13. Braverman N, Dodt G, Gould SJ, 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

    PubMed  CAS  Google Scholar 

  • 14. Brown CR, McCann JA, Chiang HL (2000) The heat shock protein Ssa2p is required for import of fructose-1, 6-bisphosphatase into Vid vesicles. J Cell Biol 150:65-76

    PubMed  CAS  Google Scholar 

  • 15. Buchberger A, Theyssen H, Schroder H, McCarty JS, Virgallita G, Milkereit P, Reinstein J, Bukau B (1995) Nucleotide-induced conformational changes in the ATPase and substrate binding domains of the DnaK chaperone provide evidence for interdomain communication. J Biol Chem 270:16903-16910

    PubMed  CAS  Google Scholar 

  • 16. Chen S, Smith DF (1998) Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery. J Biol Chem 273:35194-35200

    PubMed  CAS  Google Scholar 

  • 17. Chiang HL, Terlecky SR, Plant CP, Dice JF (1989) A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246:382-385

    PubMed  CAS  Google Scholar 

  • 18. Chung KT, Shen Y, Hendershot LM, Siegers K, Moarefi I, Wente SR, Hartl FU, Young JC (2002) BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J Biol Chem 277:47557-47563

    PubMed  CAS  Google Scholar 

  • 19. Collins CS, Kalish JE, Morrell JC, McCaffery JM, Gould SJ (2000) The peroxisome biogenesis factors pex4p, pex22p, pex1p, and pex6p act in the terminal steps of peroxisomal matrix protein import. Mol Cell Biol 20:7516-7526

    PubMed  CAS  Google Scholar 

  • 20. Corpas F, Trelease RN (1997) The plant 73 kDa peroxisomal membrane protein (PMP73) is immunorelated to molecular chaperones. Eur J Cell Biol 73:49-57

    PubMed  CAS  Google Scholar 

  • 21. Crookes W, Olsen LJ (1998) The effects of chaperones and the influence of protein assembly on peroxisomal protein import. J Biol Chem 273:17236-17242

    PubMed  CAS  Google Scholar 

  • 22. Cyr DM, Langer T, Douglas MG (1994) DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends Biochem Sci 19:176-181

    PubMed  CAS  Google Scholar 

  • 23. Dammai V, Subramani S (2001) The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisomal matrix and recycled to the cytosol. Cell 105:187-196

    PubMed  CAS  Google Scholar 

  • 24. Dansen TB, Wirtz KW, Wanders RJ, Pap EH, Behari R, Baker A (2000) Peroxisomes in human fibroblasts have a basic pH. Nat Cell Biol 2:51-53

    PubMed  CAS  Google Scholar 

  • 25. Davies TH, Ning YM, Sanchez ER (2002) A new first step in activation of steroid receptors: hormone-induced switching of FKBP51 and FKBP52 immunophilins. J Biol Chem 277:4597-4600

    PubMed  CAS  Google Scholar 

  • 26. Deshaies RJ, Koch BD, Werner-Washburne M, Craig EA, Schekman R (1988) A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332:800-805

    PubMed  CAS  Google Scholar 

  • 27. Diefenbach J, H K (2000) 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 267:746-754

    PubMed  CAS  Google Scholar 

  • 28. Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, Mohr C, Pohlmann R, Luedi P, Choi S, Wing RA, Flavier A, Gaffney TD, Philippsen P (2004) The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304:304-307. Epub 2004 Mar 2004

    PubMed  CAS  Google Scholar 

  • 29. Distel B, Erdmann R, Gould SJ, Blobel G, Crane DI, Cregg JM, Dodt G, Fujiki Y, Goodman JM, Just WW, Kiel JAKW, Kunau W-H, 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

    PubMed  CAS  Google Scholar 

  • 30. Dodt G, Braverman N, Wong C, Moser A, Moser HW, Watkins P, Valle D, Gould SJ (1995) Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nat Genet 9:115-125

    PubMed  CAS  Google Scholar 

  • 31. Dodt G, Gould SJ (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

    PubMed  CAS  Google Scholar 

  • 32. Dodt G, Warren D, Becker E, Rehling P, Gould SJ (2001) Domain mapping of human PEX5 reveals functional and structural similarities to Saccharomyces cerevisiae Pex18p and Pex21p. J Biol Chem 276:41769-41781

    PubMed  CAS  Google Scholar 

  • 33. Dyer JM, McNew JA, Goodman JM (1996) The sorting sequence of the peroxisomal integral membrane protein PMP47 is contained within a short hydrophilic loop. J Cell Biol 133:269-280

    PubMed  CAS  Google Scholar 

  • 34. Economou A, Wickner W (1994) SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78:835-843

    PubMed  CAS  Google Scholar 

  • 35. Einwachter H, Sowinski S, Kunau WH, Schliebs W (2001) Yarrowia lipolytica Pex20p, Saccharomyces cerevisiae Pex18p/Pex21p and mammalian Pex5pL fulfil a common function in the early steps of the peroxisomal PTS2 import pathway. EMBO Rep 2:1035-1039. Epub 2001 Oct 1017

    PubMed  CAS  Google Scholar 

  • 36. Elgersma Y, Elgersma-Hooisma M, Wenzel T, McCaffery JM, Farquhar MG, Subramani S (1998) A mobile PTS2 receptor for peroxisomal protein import in Pichia pastoris. J Cell Biol 140:807-820

    PubMed  CAS  Google Scholar 

  • 37. Elgersma Y, Kwast L, van den Berg M, Snyder WB, Distel B, Subramani S, Tabak HF (1997) Overexpression of Pex15p, a phosphorylated peroxisomal integral membrane protein required for peroxisome assembly in S. cerevisiae, causes proliferation of the endoplasmic reticulum membrane. EMBO J 16:7326-7341

    PubMed  CAS  Google Scholar 

  • 38. Elgersma Y, Kwast L, Klein A, Voorn-Brouwer T, van den Berg M, Metzig B, America T, Tabak HF, Distel B (1996a) The SH3 domain of the Saccharomyces cerevisiae peroxisomal membrane protein Pex13p functions as a docking site for Pex5p, a mobile receptor for the import of PTS1-containing proteins. J Cell Biol 135:97-109

    PubMed  CAS  Google Scholar 

  • 39. Elgersma Y, Vos A, van den Berg M, Van Roermund CW, van der Sluijs P, Distel B, Tabak HF (1996b) Analysis of the carboxyl-terminal peroxisomal targeting signal 1 in a homologous context in Saccharomyces cerevisiae. J Biol Chem 271:26375-26382

    PubMed  CAS  Google Scholar 

  • 40. Erdmann R, Blobel G (1996) Identification of Pex13p, a peroxisomal membrane receptor for the PTS1 recognition factor. J Cell Biol 135:111-121

    PubMed  CAS  Google Scholar 

  • 41. 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. Epub 2004 Mar 2008

    PubMed  CAS  Google Scholar 

  • 42. Fransen M, Brees C, Baumgart E, Vanhooren JC, Baes M, Mannaerts GP, van Veldhoven PP (1995) Identification and characterization of the putative human peroxisomal C-terminal targeting signal import receptor. J Biol Chem 270:7731-7736

    PubMed  CAS  Google Scholar 

  • 43. Freeman BC, Morimoto RI (1996) The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J 15:2969-2979

    PubMed  CAS  Google Scholar 

  • 44. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603-647

    PubMed  CAS  Google Scholar 

  • 45. Frydman J, Nimmesgern E, Oktsuka K, Hartl FU (1994) Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370:111-117

    PubMed  CAS  Google Scholar 

  • 46. Galigniana MD, Harrell JM, Murphy PJ, Chinkers M, Radanyi C, Renoir JM, Zhang M, Pratt WB (2002) Binding of hsp90-associated immunophilins to cytoplasmic dynein: direct binding and in vivo evidence that the peptidylprolyl isomerase domain is a dynein interaction domain. Biochemistry 41:13602-13610

    PubMed  CAS  Google Scholar 

  • 47. Gatto GJ Jr, Geisbrecht BV, Gould SJ, Berg JM (2000) Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5. Nat Struct Biol 7:1091-1095

    PubMed  CAS  Google Scholar 

  • 48. Gautschi M, Mun A, Ross S, Rospert S, Wu Y, Hu Z, Thompson LJ, Yin LY, Patterson C (2002) A functional chaperone triad on the yeast ribosome. Proc Natl Acad Sci USA 99:4209-4214

    PubMed  CAS  Google Scholar 

  • 49. 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. Epub 2003 Apr 2904

    PubMed  CAS  Google Scholar 

  • 50. Gietl C, Faber KN, van der Klei IJ, Veenhuis M (1994) Mutational analysis of the N-terminal topogenic signal of watermelon glyoxysomal malate dehydrogenase using the heterologous host Hansenula polymorpha. Proc Natl Acad Sci USA 91:3151-3155

    PubMed  CAS  Google Scholar 

  • 51. Girzalsky W, Rehling P, Stein K, Kipper J, Blank L, Kunau W-H, Erdmann R (1999) Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J Cell Biol 144:1151-1162

    PubMed  CAS  Google Scholar 

  • 52. Glover JR, Andrews DW, Rachubinski RA (1994) Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc Natl Acad Sci USA 91:10541-10545

    PubMed  CAS  Google Scholar 

  • 53. Gould SJ, Collins CS, Wirtz E, Clayton C (2002) Opinion: peroxisomal-protein import: is it really that complex? Nat Rev Mol Cell Biol 3:382-389

    PubMed  CAS  Google Scholar 

  • 54. Gould SJ, Kalish JE, Morrell JC, Bjorkman J, Urquhart AJ, Crane DI (1996) Pex13p is an SH3 protein of the peroxisome membrane and a docking factor for the predominantly cytoplasmic PTS1 receptor. J Cell Biol 135:85-95

    PubMed  CAS  Google Scholar 

  • 55. Gould SJ, Keller GA, Hosken N, Wilkinson J, Subramani S (1989) A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol 108:1657-1664

    PubMed  CAS  Google Scholar 

  • 56. Gould SJ, Keller GA, Schneider M, Howell SH, Garrard LJ, Goodman JM, Distel B, Tabak H, Subramani S (1990) Peroxisomal protein import is conserved between yeast, plants, insects and mammals. EMBO J 9:85-90

    PubMed  CAS  Google Scholar 

  • 57. Gouveia AM, Guimaraes CP, Oliveira ME, Reguenga C, Sa-Miranda C, Azevedo JE (2003) Characterization of the peroxisomal cycling receptor, Pex5p, using a cell-free in vitro import system. J Biol Chem 278:226-232

    PubMed  CAS  Google Scholar 

  • 58. Gouveia AM, Reguenga C, Oliveira ME, Sa-Miranda C, Azevedo JE (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

    PubMed  CAS  Google Scholar 

  • 59. Harano T, Nose S, Uezu R, Shimizu N, Fujiki Y (2001) Hsp70 regulates the interaction between the peroxisome targeting signal type 1 (PTS1)-receptor Pex5p and PTS1. Biochem J 357:157-165

    PubMed  CAS  Google Scholar 

  • 60. Hardonk MJ, Harms G, Koudstaal J (1985) Zonal heterogeneity of rat hepatocytes in the in vivo uptake of 17 nm colloidal gold granules. Histochemistry 83:473-477

    PubMed  CAS  Google Scholar 

  • 61. Harper CC, Berg JM, Gould SJ, Harano T, Nose S, Uezu R, Shimizu N, Fujiki Y (2002) PEX5 binds the PTS1 independently of Hsp70 and the peroxin PEX12. J Biol Chem 26:26

    Google Scholar 

  • 62. Harrison CJ, Hayer-Hartl M, Di Liberto M, Hartl F, Kuriyan J (1997) Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276:431-435

    PubMed  CAS  Google Scholar 

  • 63. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858

    PubMed  CAS  Google Scholar 

  • 64. Hausler T, Stierhof YD, Wirtz E, Clayton C (1996) Import of a DHFR hybrid protein into glycosomes in vivo is not inhibited by the folate-analogue aminopterin. J Cell Biol 132:311-324

    PubMed  CAS  Google Scholar 

  • 65. Hazra PP, Suriapranata I, Snyder WB, Subramani S (2002) Peroxisome remnants in pex3delta cells and the requirement of Pex3p for interactions between the peroxisomal docking and translocation subcomplexes. Traffic 3:560-574

    PubMed  CAS  Google Scholar 

  • 66. Hettema EH (1998), Import of proteins and fatty acids into peroxisomes. PhD thesis University of Amsterdam

    Google Scholar 

  • 67. Hettema EH, Girzalsky W, Berg Mvd, Erdmann R, Distel B (2000) Saccharomyces cerevisiae Pex3p and Pex19p are required for proper localization and stability of peroxisomal membrane proteins. EMBO J 19:223-233

    PubMed  CAS  Google Scholar 

  • 68. Hines V, Brandt A, Griffiths G, Horstmann H, Brutsch H, Schatz G (1990) Protein import into yeast mitochondria is accelerated by the outer membrane protein MAS70. EMBO J 9:3191-3200

    PubMed  CAS  Google Scholar 

  • 69. Hoepfner D, van den Berg M, Philippsen P, Tabak HF, Hettema EH (2001) A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J Cell Biol 155:979-990. Epub 2001 Dec 2003

    PubMed  CAS  Google Scholar 

  • 70. Hohfeld J, Minami Y, Hartl FU (1995) Hip, a novel cochaperone involved in the eukaryotic Hsc70/Hsp40 reaction cycle. Cell 83:589-598

    PubMed  CAS  Google Scholar 

  • 71. Huang S, Ratliff KS, Matouschek A (2002) Protein unfolding by the mitochondrial membrane potential. Nat Struct Biol 9:301-307

    PubMed  CAS  Google Scholar 

  • 72. Hundley H, Eisenman H, Walter W, Evans T, Hotokezaka Y, Wiedmann M, Craig E (2002) The in vivo function of the ribosome-associated Hsp70, Ssz1, does not require its putative peptide-binding domain. Proc Natl Acad Sci USA 99:4203-4208

    PubMed  CAS  Google Scholar 

  • 73. Hutchison KA, Dittmar KD, Pratt WB (1994) All of the factors required for assembly of the glucocorticoid receptor into a functional heterocomplex with heat shock protein 90 are preassociated in a self-sufficient protein folding structure, a ”foldosome”. J Biol Chem 269:27894-27899

    PubMed  CAS  Google Scholar 

  • 74. Itoh T, Matsuda H, Mori H (1999) Phylogenetic analysis of the third hsp70 homolog in Escherichia coli; a novel member of the Hsc66 subfamily and its possible co-chaperone. DNA Res 6:299-305

    PubMed  CAS  Google Scholar 

  • 75. James P, Pfund C, Craig EA (1997) Functional specificity among Hsp70 molecular chaperones. Science 275:387-389

    PubMed  CAS  Google Scholar 

  • 76. Jankowski A, Kim JH, Collins RF, Daneman R, Walton P, Grinstein S (2001) In situ measurements of the pH of mammalian peroxisomes using the fluorescent protein pHluorin. J Biol Chem 276:48748-48753

    PubMed  CAS  Google Scholar 

  • 77. Johnson MA, Snyder WB, Cereghino JL, Veenhuis M, Subramani S, Cregg JM (2001) Pichia pastoris Pex14p, a phosphorylated peroxisomal membrane protein, is part of a PTS-receptor docking complex and interacts with many peroxins. Yeast 18:621-641

    PubMed  CAS  Google Scholar 

  • 78. Jones JM, Morrell JC, Gould SJ (2001) Multiple distinct targeting signals in integral peroxisomal membrane proteins. J Cell Biol 153:1141-1150

    PubMed  CAS  Google Scholar 

  • 79. 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

    PubMed  CAS  Google Scholar 

  • 80. Kabani M, Beckerich JM, Brodsky JL (2002a) Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol Cell Biol 22:4677-4689

    PubMed  CAS  Google Scholar 

  • 81. Kabani M, Beckerich JM, Gaillardin C (2000) Sls1p stimulates Sec63p-mediated activation of Kar2p in a conformation-dependent manner in the yeast endoplasmic reticulum. Mol Cell Biol 20:6923-6934

    PubMed  CAS  Google Scholar 

  • 82. Kabani M, McLellan C, Raynes DA, Guerriero V, Brodsky JL (2002b) HspBP1, a homologue of the yeast Fes1 and Sls1 proteins, is an Hsc70 nucleotide exchange factor. FEBS Lett 531:339-342

    PubMed  CAS  Google Scholar 

  • 83. Kawula TH, Lelivelt MJ (1994) Mutations in a gene encoding a new Hsp70 suppress rapid DNA inversion and bgl activation, but not proU derepression, in hns-1 mutant Escherichia coli. J Bacteriol 176:610-619

    PubMed  CAS  Google Scholar 

  • 84. Kazlauskas A, Poellinger L, Pongratz I (2002) Two distinct regions of the immunophilin-like protein XAP2 regulate dioxin receptor function and interaction with hsp90. J Biol Chem 277:11795-11801

    PubMed  CAS  Google Scholar 

  • 85. Kikuchi M, Hatano N, Yokota S, Shimozawa N, Imanaka T, Taniguchi H (2004) Proteomic analysis of rat liver peroxisome: presence of peroxisome-specific isozyme of Lon protease. J Biol Chem 279:421-428. Epub 2003 Oct 2015

    PubMed  CAS  Google Scholar 

  • 86. Kim S, Schilke B, Craig EA, Horwich AL (1998) Folding in vivo of a newly translated yeast cytosolic enzyme is mediated by the SSA class of cytosolic yeast Hsp70 proteins. Proc Natl Acad Sci USA 95:12860-12865

    PubMed  CAS  Google Scholar 

  • 87. Klein AT, Barnett P, Bottger G, Konings D, Tabak HF, Distel B (2001) Recognition of peroxisomal targeting signal type 1 by the import receptor Pex5p. J Biol Chem 276:15034-15041

    PubMed  CAS  Google Scholar 

  • 88. Klein AT, van den Berg M, Bottger G, Tabak HF, 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

    PubMed  CAS  Google Scholar 

  • 89. Koch A, Thiemann M, Grabenbauer M, Yoon Y, McNiven MA, Schrader M (2003) Dynamin-like protein 1 is involved in peroxisomal fission. J Biol Chem 278:8597-8605. Epub 2002 Dec 8523

    PubMed  CAS  Google Scholar 

  • 90. Komori M, Kiel JA, Veenhuis M (1999) The peroxisomal membrane protein Pex14p of Hansenula polymorpha is phosphorylated in vivo. FEBS lett 457:397-399

    PubMed  CAS  Google Scholar 

  • 91. Lametschwandtner G, Brocard C, Fransen M, van Veldhoven P, Berger J, Hartig A (1998) 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 toiIt. J Biol Chem 273:33635-33643

    PubMed  CAS  Google Scholar 

  • 92. Lazarow PB, Fujiki Y (1985) Biogenesis of peroxisomes. Annu Rev Cell Biol 1:489-530

    PubMed  CAS  Google Scholar 

  • 93. Legakis J, Terlecky S (2001) PTS2 protein import into mammalian peroxisomes. Traffic 2:252-260

    PubMed  CAS  Google Scholar 

  • 94. Leiper JM, Oatey PB, Danpure CJ (1996) Inhibition of alanine:glyoxylate aminotransferase 1 dimerization is a prerequisite for its peroxisome-to-mitochondrion mistargeting in Primary Hyperoxaluria Type 1. J Cell Biol 135:939-951

    PubMed  CAS  Google Scholar 

  • 95. Li X, Gould SJ (2003) The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J Biol Chem 278:17012-17020 Epub 12003 Mar 17014

    PubMed  CAS  Google Scholar 

  • 96. Liberek K, Marszalek J, Ang D, Georgopoulos C, Zylicz M (1991) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA 88:2874-2878

    PubMed  CAS  Google Scholar 

  • 97. Louvion JF, Abbas-Terki T, Picard D (1998) Hsp90 is required for pheromone signaling in yeast. Mol Biol Cell 9:3071-3083

    PubMed  CAS  Google Scholar 

  • 98. Marzioch M, Erdmann R, Veenhuis M, Kunau W-H (1994) 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 13:4908-4918

    PubMed  CAS  Google Scholar 

  • 99. Matouschek A, Pfanner N, Voos W, Strobel G, Zollner A, Angermayr M, Bandlow W (2000) Protein unfolding by mitochondria. The Hsp70 import motor. EMBO Rep 1:404-410

    PubMed  CAS  Google Scholar 

  • 100. Matsumura T, Otera H, Fujiki Y (2000) 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-impared Chinese hamster ovary cell mutant. J Biol Chem 275:21715-21721

    PubMed  CAS  Google Scholar 

  • 101. Mayer MP, Schroder H, Rudiger S, Paal K, Laufen T, Bukau B (2000) Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nat Struct Biol 7:586-593

    PubMed  CAS  Google Scholar 

  • 102. McNew JA, Goodman JM (1996) The targeting and assembly of peroxisomal proteins: some old rules do not apply. Trends Biochem Sci 21:54-58

    PubMed  CAS  Google Scholar 

  • 103. Misselwitz B, Staeck O, Rapoport TA (1998) J proteins catalytically activate Hsp70 molecules to trap a wide range of peptide sequences. Mol Cell 2:593-603

    PubMed  CAS  Google Scholar 

  • 104. Motley A, Lumb MJ, Patel PB, Jennings PR, Zoysa PD, Wanders RJA, Tabak HF, Danpure CJ (1995) Identification of the peroxisomal targeting sequence of mammalian alanine: glyoxylate aminotransferase 1. Increased degeneracy and contaxt specificity of the mammalian PTS1 motif and implications for the peroxisome-to-mitochondrion mistargeting of AGT in primary hyperoxaluria type 1. J Cell Biol 131:95-109

    PubMed  CAS  Google Scholar 

  • 105. Motley AM, Hettema EH, Ketting R, Plasterk R, Tabak HF (2000) Caenorhabditis elegans has a single pathway to target matrix proteins to peroxisomes. EMBO reports 1:40-46

    PubMed  CAS  Google Scholar 

  • 106. Nelson R, T Z, C N, M W-W, EA C (1992) The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 71:97-105

    PubMed  CAS  Google Scholar 

  • 107. Neuberger G, Maurer-Stroh S, Eisenhaber B, Hartig A, Eisenhaber F (2003) Motif refinement of the peroxisomal targeting signal 1 and evaluation of taxon-specific differences. J Mol Biol 328:567-579

    PubMed  CAS  Google Scholar 

  • 108. Ngosuwan J, Wang NM, Fung KL, Chirico WJ (2002) Roles of cytosolic Hsp70 and Hsp40 molecular chaperones in post-translational translocation of presecretory proteins into the endoplasmic reticulum. J Biol Chem 19:19

    Google Scholar 

  • 109. Nicola A, W C, A H (1999) Co-translational folding of an alphavirus capsid protein in the cytosol of living cells. Nat Cell Biol 1:341-345

    PubMed  CAS  Google Scholar 

  • 110. Nicolet CM, Craig EA (1989) Isolation and characterization of STI1, a stress-inducible gene from Saccharomyces cerevisiae. Mol Cell Biol 9:3638-3646

    PubMed  CAS  Google Scholar 

  • 111. Novikoff PM, Novikoff AB (1972) Peroxisomes in absorptive cells of mammalian small intestine. J Cell Biol 53:532-560

    PubMed  CAS  Google Scholar 

  • 112. Pfund C, Lopez-Hoyo N, Ziegelhoffer T, Schilke BA, Lopez-Buesa P, Walter WA, Craig EA (1998) The molecular chaperone Ssb from Saccharomyces cerevisiae is a component of the ribosome-nascent chain complex. EMBO J 17:3981-3989

    PubMed  CAS  Google Scholar 

  • 113. Picard D, Khursheed B, Garabedian MJ, Fortin MG, Lindquist S, Yamamoto KR (1990) Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348:166-168

    PubMed  CAS  Google Scholar 

  • 114. Pishvaee B, Costaguta G, Yeung BG, Ryazantsev S, Greener T, Greene LE, Eisenberg E, McCaffery JM, Payne GS (2000) A yeast DNA J protein required for uncoating of clathrin-coated vesicles in vivo. Nat Cell Biol 2:958-963

    PubMed  CAS  Google Scholar 

  • 115. Pratt WB, Krishna P, Olsen LJ (2001) Hsp90-binding immunophilins in plants: the protein movers. Trends Plant Sci 6:54-58

    PubMed  CAS  Google Scholar 

  • 116. Purdue PE, Yang X, Lazarow PB (1998) Pex18p and Pex21p, a novel pair of related peroxins essential for peroxisomal targeting by the PTS2 pathway. J Cell Biol 143:1859-1869

    PubMed  CAS  Google Scholar 

  • 117. Raynes DA, Guerriero V Jr (1998) Inhibition of Hsp70 ATPase activity and protein renaturation by a novel Hsp70-binding protein. J Biol Chem 273:32883-32888

    PubMed  CAS  Google Scholar 

  • 118. Reguenga C, Oliveira ME, Gouveia AM, Sa-Miranda C, Azevedo JE (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

    PubMed  CAS  Google Scholar 

  • 119. Rehling P, Marzioch M, Niessen F, Wittke E, Veenhuis M, Kunau W-H (1996) The import receptor for the peroxisomal targeting signal 2 (PTS2) in Saccharomyces cerevisiae is encoded by the PAS7 gene. EMBO J 15:2901-2913

    PubMed  CAS  Google Scholar 

  • 120. Rottensteiner H, Kramer A, Lorenzen S, Stein K, Landgraf C, Volkmer-Engert R, Erdmann R (2004) Peroxisomal membrane proteins contain common Pex19p-binding sites that are an integral part of their targeting signals. Mol Biol Cell 15:3406-3417. Epub 2004 May 3407

    PubMed  CAS  Google Scholar 

  • 121. Rudiger S, Germeroth L, Schneider-Mergener J, Bukau B (1997) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J 16:1501-1507

    PubMed  CAS  Google Scholar 

  • 122. Ruigrok CCM, de Jonge W, Tabak HF, Braakman LJ (manuscript in preparation) Efficiency of peroxisomal protein import is determined by competition between translocation and a change into import-incompetence

    Google Scholar 

  • 123. Sacksteder KA, Jones JM, South ST, Li X, Liu Y, Gould SJ (2000) PEX19 binds multiple peroxisomal membrane proteins, is predominantly cytoplasmic, and is required for peroxisome membrane synthesis. J Cell Biol 148:931-944

    PubMed  CAS  Google Scholar 

  • 124. Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:199-210

    PubMed  CAS  Google Scholar 

  • 125. Schmid D, Baici A, Gehring H, Christen P, Reinstein J, Bukau B (1994) Kinetics of molecular chaperone action. Science 263:971-973

    PubMed  CAS  Google Scholar 

  • 126. Schulte TW, Blagosklonny MV, Ingui C, Neckers L (1995) Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J Biol Chem 270:24585-24588

    PubMed  CAS  Google Scholar 

  • 127. Sichting M, Schell-Steven A, Prokisch H, Erdmann R, Rottensteiner H (2003) Pex7p and Pex20p of Neurospora crassa function together in PTS2-dependent protein import into peroxisomes. Mol Biol Cell 14:810-821

    PubMed  CAS  Google Scholar 

  • 128. Silver PA, Way JC, James P, Pfund C, Craig EA (1993) Eukaryotic DnaJ homologs and the specificity of Hsp70 activity. Cell 74:5-6

    PubMed  CAS  Google Scholar 

  • 129. Silverstein AM, Galigniana MD, Kanelakis KC, Radanyi C, Renoir JM, Pratt WB (1999) Different regions of the immunophilin FKBP52 determine its association with the glucocorticoid receptor, hsp90, and cytoplasmic dynein. J Biol Chem 274:36980-36986

    PubMed  CAS  Google Scholar 

  • 130. Sondermann H, Ho AK, Listenberger LL, Siegers K, Moarefi I, Wente SR, Hartl FU, Young JC (2002) Prediction of novel Bag-1 homologs based on structure/function analysis identifies Snl1p as an Hsp70 co-chaperone in Saccharomyces cerevisiae. J Biol Chem 277:33220-33227

    PubMed  CAS  Google Scholar 

  • 131. Soto U, Pepperkok R, Ansorge W, Just WW (1993) Import of firefly luciferase into mammalian peroxisomes in vivo requires nucleoside triphosphates. Exp Cell Res 205:66-75

    PubMed  CAS  Google Scholar 

  • 132. South ST, Baumgart E, Gould SJ (2001) Inactivation of the endoplasmic reticulum protein translocation factor, Sec61p, or its homolog, Ssh1p, does not affect peroxisome biogenesis. Proc Natl Acad Sci USA 98:12027-12031. Epub 12001 Oct 12022

    PubMed  CAS  Google Scholar 

  • 133. South ST, Sacksteder KA, Li X, Liu Y, Gould SJ (2000) Inhibitors of COPI and COPII do not block PEX3-mediated peroxisome synthesis. J Cell Biol 149:1345-1359

    PubMed  CAS  Google Scholar 

  • 134. Strobel G, Zollner A, Angermayr M, Bandlow W (2002) Competition of spontaneous protein folding and mitochondrial import causes dual subcellular location of major adenylate kinase. Mol Biol Cell 13:1439-1448

    PubMed  CAS  Google Scholar 

  • 135. Subramani S (1996) Protein translocation into peroxisomes. J Biol Chem 271:32483-32486

    PubMed  CAS  Google Scholar 

  • 136. Swinkels BW, Gould SJ, Bodnar AG, Rachubinski RA, 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

    PubMed  CAS  Google Scholar 

  • 137. Szilard RK, Titorenko VI, Veenhuis M, Rachubinski RA (1995) Pay 32p of the yeast Yarrowia lipolytica is an intraperoxisomal component of the matrix protein translocation machinery. J Cell Biol 131:1453-1469

    PubMed  CAS  Google Scholar 

  • 138. Tabak HF, Murk JL, Braakman I, Geuze HJ (2003) Peroxisomes start their life in the endoplasmic reticulum. Traffic 4:512-518

    PubMed  CAS  Google Scholar 

  • 139. Takayama S, Bimston DN, Matsuzawa S, Freeman BC, Aime-Sempe C, Xie Z, Morimoto RI, Reed JC (1997) BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO J 16:4887-4896

    PubMed  CAS  Google Scholar 

  • 140. Terlecky SR, Dice JF (1993) Polypeptide import and degradation by isolated lysosomes. J Biol Chem 268:23490-23495

    PubMed  CAS  Google Scholar 

  • 141. Terlecky SR, Nuttley WM, McCollum D, Sock E, Subramani S (1995) The Pichia pastoris peroxisomal protein PAS8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. EMBO J 14:3627-3634

    PubMed  CAS  Google Scholar 

  • 142. Titorenko VI, Nicaud JM, Wang H, Chan H, Rachubinski RA (2002) Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. J Cell Biol 156:481-494

    PubMed  CAS  Google Scholar 

  • 143. Titorenko VI, Smith JJ, Szilard RK, Rachubinski RA (1998) 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 142:403-420

    PubMed  CAS  Google Scholar 

  • 144. Tsukamoto T, Hata S, Yokota S, Miura S, Fujiki Y, Hijikata M, Miyazawa S, Hashimoto T, Osumi T (1994) Characterization of the signal peptide at the amino terminus of the rat peroxisomal 3-ketoacyl-CoA thiolase precursor. J Biol Chem 269:6001-6010

    PubMed  CAS  Google Scholar 

  • 145. Ungewickell E, Ungewickell H, Holstein SE, Lindner R, Prasad K, Barouch W, Martin B, Greene LE, Eisenberg E (1995) Role of auxillin in uncoating clathrin-coated vesicles. Nature 378:632-635

    PubMed  CAS  Google Scholar 

  • 146. Urquhart AJ, Kennedy D, Gould SJ, Crane DI (2000) Interaction of Pex5p, the type 1 peroxisome targeting signal receptor, with the peroxisomal membrane proteins Pex14p and Pex13p. J Biol Chem 275:4127-4136

    PubMed  CAS  Google Scholar 

  • 147. van der Klei IJ, Hilbrands RE, Swaving GJ, Waterham HR, Vrieling EG, Titorenko VI, Cregg JM, Harder W, Veenhuis M (1995) The Hansenula polymorpha PER3 gene is essential for the import of PTS1 proteins into the peroxisomal matrix. J Biol Chem 270:17229-17236

    Google Scholar 

  • 148. Van der Leij I, Franse MM, Elgersma Y, Distel B, Tabak HF (1993) PAS10 is a tetratricopeptide-repeat protein that is essential for the import of most matrix proteins into peroxisomes of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 90:11782-11786

    Google Scholar 

  • 149. van der Lende TR, Breeuwer P, Abee T, Konings WN, Driessen AJ (2002) Assessment of the microbody luminal pH in the filamentous fungus Penicillium chrysogenum. Biochim Biophys Acta 1589:104-111

    Google Scholar 

  • 150. Van Roermund CW, De Jong M, L IJ, Van Marle J, Dansen TB, Wanders RJ, Waterham HR (2004) The peroxisomal lumen in Saccharomyces cerevisiae is alkaline. J Cell Sci 117:4231-4237

    Google Scholar 

  • 151. Verner K, Schatz G (1987) Import of an incompletely folded precursor protein into isolated mitochondria requires an energized inner membrane, but no added ATP. EMBO J 6:2449-2456

    PubMed  CAS  Google Scholar 

  • 152. Voorn-Brouwer T, Kragt A, Tabak HF, Distel B (2001) Peroxisomal membrane proteins are properly targeted to peroxisomes in the absence of COPI- and COPII-mediated vesicular transport. J Cell Sci 114:2199-2204

    PubMed  CAS  Google Scholar 

  • 153. Walton PA, Wendland M, Subramani S, Rachubinski RA, Welch WJ (1994) Involvement of 70-kD heat-shock proteins in peroxisomal import. J Cell Biol 125:1037-1046

    PubMed  CAS  Google Scholar 

  • 154. Wendland M, Subramani S (1993) Cytosol-dependent peroxisomal protein import in a permeabilized cell system. J Cell Biol 120:675-685

    PubMed  CAS  Google Scholar 

  • 155. Werner-Washburne M, Stone DE, Craig EA (1987) Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Mol Cell Biol 7:2568-2577

    PubMed  CAS  Google Scholar 

  • 156. Wiemer E, Nuttley WM, Bertolaet BL, Li X, Francke U, Wheelock MJ, Anne UK, Johnson KR, Subramani S (1995a) The human PTS1 receptor restores peroxisomal protein import deficiency in cells from patients with fatal peroxisomal disorders. J Cell Biol 130:51-65

    PubMed  CAS  Google Scholar 

  • 157. Wiemer EA, Terlecky SR, Nuttley WM, Subramani S, van der Klei IJ, Hilbrands RE, Swaving GJ, Waterham HR, Vrieling EG, Titorenko VI, Cregg JM, Harder W, Veenhuis M (1995b) Characterization of the yeast and human receptors for the carboxy-terminal tripeptide peroxisomal targeting signal. Cold Spring Harb Symp Quant Biol 60:637-648. Biotechnology Institute, University of Groningen, Haren, The Netherlands

    PubMed  CAS  Google Scholar 

  • 158. Wimmer B, Lottspeich F, van der Klei I, Veenhuis M, Gietl C (1997) The glyoxysomal and plastid molecular chaperones (70-kDa heat shock protein) of watermelon cotyledons are encoded by a single gene. Proc Natl Acad Sci USA 94:13624-13629

    PubMed  CAS  Google Scholar 

  • 159. Xu Y, Lindquist S (1993) Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc Natl Acad Sci USA 90:7074-7078

    PubMed  CAS  Google Scholar 

  • 160. Yang X, Purdue P, Lazarow P (2001) Eci1p uses a PTS1 to enter peroxisomes: either its own or that of a partner, Dci1p. Eur J Cell Biol 80:126-138

    PubMed  CAS  Google Scholar 

  • 161. Young JC, Hoogenraad NJ, Hartl FU, Obermann WM (2003) Molecular chaperones hsp90 and hsp70 deliver preproteins to the mitochondrial import receptor tom70. Cell 112:41-50

    PubMed  CAS  Google Scholar 

  • 162. Young JC, Obermann WM, Hartl FU (1998) Specific binding of tetratricopeptide repeat proteins to the C-terminal 12-kDa domain of hsp90. J Biol Chem 273:18007-18010

    PubMed  CAS  Google Scholar 

  • 163. Zhang JW, Lazarow PB (1994) PEB1 (PAS7) in Saccharomyces cerevisiae encodes a hydrophilic, intraperoxisomal protein which is a member of the WD repeat family and is essential for the import of thiolase into peroxisomes. J Cell Biol 129:65-80

    Google Scholar 

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  1. Department of Cellular Protein Chemistry, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands. Current adress: Institute of Information and Computing Sciences, Utrecht University, Padualaan 14, 3584CH Utrecht, The Netherlands

    Wim de Jonge

  2. Department of Cellular Protein Chemistry, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands, and Laboratory of Cell Biology, University Medical Center Utrecht and Center for Biomedical Genetics, 3584 CX Utrecht, The Netherlands

    Henk F. Tabak

  3. Department of Cellular Protein Chemistry, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Ineke Braakman

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de Jonge, W., Tabak, H.F., Braakman, I. Chaperone proteins and peroxisomal protein import. In: Braakman, I. (eds) Chaperones. Topics in Current Genetics, vol 16. Springer, Berlin, Heidelberg. https://doi.org/10.1007/b136669

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