PEX3 functions as a PEX19 docking factor in the import of class I peroxisomal membrane proteins

Journal of Cell Biology

Volumn 164, Issue 6, 2004, Pages 863-875

  Fang, Yi ^a   Morrell, James C ^a   Jones, Jacob M ^a   Gould, Stephen J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Organelle biogenesis; PMP import; Protein import; Temperature sensitive mutants; Zellweger syndrome

Indexed keywords

CHAPERONE; COMPLEMENTARY DNA; MEMBRANE PROTEIN; PEROXISOMAL MEMBRANE PROTEIN; PEX19 DOCKING FACTOR; PEX19 PROTEIN; PEX3 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; FIBROBLAST; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; TEMPERATURE SENSITIVE MUTANT; YEAST;

AMINO ACID MOTIFS; CELL LINE; FIBROBLASTS; HUMANS; LIPOPROTEINS; MEMBRANE PROTEINS; PEROXISOMES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

INSERTION SEQUENCES; RUMEX;

EID: 1642394134     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200311131     Document Type: Article

References (55)

1. Albertini, M., P. Rehling, R. Erdmann, W. Girzalsky, J.A.K.W. Kiel, M. Veenhuis, and W.-H. Kunau. 1997. Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell. 89:83-92.
2. Baker-Brachmann, C., A. Davies, G.J. Cost, E. Caputo, J. Li, P. Hieter, and J.D. Boeke. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast. 14:115-132.
3. Brosius, U., T. Dehmel, and J. Gartner. 2002. Two different targeting signals direct human peroxisomal membrane protein 22 to peroxisomes. J. Biol. Chem. 277:774-784.
4. Chang, C.C., W.H. Lee, H.W. Moser, D. Valle, and S.J. Gould. 1997. Isolation of the human PEX12 gene, mutated in group 3 of the peroxisome biogenesis disorders. Nat. Genet. 15:385-388.
5. Chang, C.C., S. South, D. Warren, J. Jones, A.B. Moser, H.W. Moser, and S.J. Gould. 1999a. Metabolic control of peroxisome abundance. J. Cell Sci. 112: 1579-1590.
6. Chang, C.C., D.S. Warren, K.A. Sacksteder, and S.J. Gould. 1999b. PEX12 binds PEX5 and PEX10 and acts downstream of receptor docking in peroxisomal matrix protein import. J. Cell Biol. 147:761-773.
7. Chen, S., M.C. Liang, J.N. Chia, J.K. Ngsee, and A.E. Ting. 2001. Rab8b and its interacting partner TRIP8b are involved in regulated secretion in AtT20 cells. J. Biol. Chem. 276:13209-13216.
8. Diestelkotter, P., and W.W. Just. 1993. In vitro insertion of the 22 kD peroxisomal membrane protein into isolated rat liver peroxisomes. J. Cell Biol. 123: 1717-1725.
9. Distel, B., R. Erdmann, S.J. Gould, G. Blobel, D.I. Crane, J.M. Cregg, G. Dodt, Y. Fujiki, J.M. Goodman, W.W. Just, et al. 1996. A unified nomenclature for peroxisome biogenesis. J. Cell Biol. 135:1-3.
10. Dodt, G., N. Braverman, C. Wong, A. Moser, H.W. Moser, P. Watkins, D. Valle, and S.J. Gould. 1995. Mutations in the PTS1 receptor gene, PXR1, define complementation group 2 of the peroxisome biogenesis disorders. Nat. Genet. 9:115-124.
11. Dyer, J.M., J.A. McNew, and J.M. Goodman. 1996. The sorting sequence of the peroxisomal integral membrane protein PMP47 is contained within a short hydrophilic loop. J. Cell Biol. 133:269-280.
12. Eitzen, G.A., R.K. Szilard, and R.A. Rachubinski. 1997. Enlarged peroxisomes are present in oleic acid-grown Yarrowia lipolytica overexpressing the PEX16 gene encoding an intraperoxisomal peripheral membrane protein. J. Cell Biol. 137:1265-1278.
13. Elgersma, Y., L. Kwast, A. Klein, T. Voorn-Brouwer, M. van den Berg, B. Metzig, T. America, H.F. Tabak, and B. Distel. 1996. 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.
14. Elgersma, Y., L. Kwast, M. van den Berg, W.B. Snyder, B. Distel, S. Subramani, and H.F. Tabak. 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.
15. Erdmann, R., and G. Blobel. 1996. Identification Pex13p, a peroxisomal membrane receptor for the PTS1 recognition factor. J. Cell Biol. 135:111-121.
16. Faber, K.N., G.J. Haan, R.J. Baerends, A.M. Kram, and M. Veenhuis. 2002. Normal peroxisome development from vesicles induced by truncated Hansenula polymorpha Pex3p. J. Biol. Chem. 277:11026-11033.
17. Fransen, M., T. Wylin, C. Brees, G.P. Mannaerts, and P.P. Van Veldhoven. 2001. Human pex19p binds peroxisomal integral membrane proteins at regions distinct from their sorting sequences. Mol. Cell. Biol. 21:4413-4424.
18. Fujiki, Y., R.A. Rachubinski, and P.B. Lazarow. 1984. Synthesis of a major integral membrane polypeptide of rat liver peroxisomes on free polysomes. Proc. Natl. Acad. Sci. USA. 81:7127-7131.
19. Girzalsky, W., P. Rehling, K. Stein, J. Kipper, L. Blank, W.H. Kunau, and R. Erdmann. 1999. Involvement of Pex13p in Pex14p localization and peroxisomal targeting signal 2-dependent protein import into peroxisomes. J. Cell Biol. 144:1151-1162.
20. Gloeckner, C.J., P.U. Mayerhofer, P. Landgraf, A.C. Muntau, A. Holzinger, J.K. Gerber, S. Kammerer, J. Adamski, and A.A. Roscher. 2000. Human adrenoleukodystrophy protein and related peroxisomal ABC transporters interact with the peroxisomal assembly protein PEX19p. Biochem. Biophys. Res. Commun. 271:144-150.
21. Gould, S.J., and C.S. Collins. 2002. Opinion: peroxisomal-protein import: is it really that complex? Nat. Rev. Mol. Cell Biol. 3:382-389.
22. Gould, S.J., and D. Valle. 2000. The genetics and cell biology of the peroxisome biogenesis disorders. Trends Genet. 16:340-344.
23. Gould, S.J., G.A. Keller, N. Hosken, J. Wilkinson, and S. Subramani. 1989. A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108:1657-1664.
24. Gould, S.J., J.E. Kalish, J.C. Morrell, J. Bjorkman, A.J. Urquhart, and D.I. Crane. 1996. PEX13p is an SH3 protein in the peroxisome membrane and a docking factor for the PTS1 receptor. J. Cell Biol. 135:85-95.
25. Haan, G.J., K.N. Faber, R.J. Baerends, A. Koek, A. Krikken, J.A. Kiel, I.J. van der Klei, and M. Veenhuis. 2002. Hansenula polymorpha Pex3p is a peripheral component of the peroxisomal membrane. J. Biol. Chem. 277:26609-26617.
26. Hazra, P.P., I. Suriapranata, W.B. Snyder, and S. Subramani. 2002. Peroxisome remnants in pex3delta cells and the requirement of Pex3p for interactions between the peroxisomal docking and translocation subcomplexes. Traffic. 3:560-574.
27. Hettema, E.H., W. Girzalsky, M. van Den Berg, R. Erdmann, and B. Distel. 2000. Saccharomyces cerevisiae pex3p and pex19p are required for proper localization and stability of peroxisomal membrane proteins. EMBO J. 19:223-233.
28. Honsho, M., S. Tamura, N. Shimozawa, Y. Suzuki, N. Kondo, Y. Fujiki. 1998. Mutation in PEX16 is causal in the peroxisome-deficient Zellweger syndrome of complementation group D. Am. J. Hum. Genet. 63:1622-1630.
29. Imanaka, T., Y. Shiina, T. Hashimoto, and T. Osumi. 1996. Insertion of the 70-kDa peroxisomal membrane protein into peroxisomal membranes in vivo and in vitro. J. Biol. Chem. 271:3706-3713.
30. Jones, J.M., K. Nau, M.T. Geraghty, R. Erdmann, and S.J. Gould. 1999. Identification of peroxisomal acyl-CoA thioesterases in yeast and humans. J. Biol. Chem. 274:9216-9223.
31. Jones, J.M., J.C. Morrell, and S.J. Gould. 2001. Multiple distinct targeting signals in integral peroxisomal membrane proteins. J. Cell Biol. 153:1141-1150.
32. Jones, J.M., J.C. Morrell, and S.J. Gould. 2004. PEX19 is a predominantly cytosolic chaperone and import receptor for class 1 peroxisomal membrane proteins. J. Cell Biol. 164:57-67.
33. Kalish, J.E., C. Theda, J.C. Morrell, J.M. Berg, and S.J. Gould. 1995. Formation of the peroxisome lumen is abolished by loss of Pichia pastoris Pas7p, a zinc-binding integral membrane protein of the peroxisome. Mol. Cell. Biol. 15: 6406-6419.
34. Kalish, J.E., G.A. Keller, J.C. Morrell, S.J. Mihalik, B. Smith, J.M. Cregg, and S.J. Gould. 1996. Characterization of a novel component of the peroxisomal protein import apparatus using fluorescent peroxisomal proteins. EMBO J. 15:3275-3285.
35. Lazarow, P.B., and Y. Fujiki. 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1:489-530.
36. Marzioch, M., R. Erdmann, M. Veenhuis, and W.-H. Kunau. 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.
37. Matsuzono, Y., N. Kinoshita, S. Tamura, N. Shimozawa, M. Hamasaki, K. Ghaedi, R.J. Wanders, Y. Suzuki, N. Kondo, and Y. Fujiki. 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.
38. McCollum, D., E. Monosov, and S. Subramani. 1993. 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. 121:761-774.
39. Mullen, R.T., C.R. Flynn, and R.N. Trelease. 2001. How are peroxisomes formed? The role of the endoplasmic reticulum and peroxins. Trends Plant Sci. 6:256-261.
40. Muntau, A.C., A.A. Roscher, W.H. Kunau, and G. Dodt. 2003. The interaction between human PEX3 and PEX19 characterized by fluorescence resonance energy transfer (FRET) analysis. Eur. J. Cell Biol. 82:333-342.
41. Palmieri, L., H. Rottensteiner, W. Girzalsky, P. Scarcia, F. Palmieri, and R. Erdmann. 2001. Identification and functional reconstitution of the yeast peroxisomal adenine nucleotide transporter. EMBO J. 20:5049-5059.
42. Pause, B., P. Diestelkotter, H. Heid, and W.W. Just. 1997. Cytosolic factors mediate protein insertion into the peroxisomal membrane. FEBS Lett. 414:95-98.
43. Sacksteder, K.A., and S.J. Gould. 2000. The genetics of peroxisome biogenesis. Annu. Rev. Genet. 34:623-652.
44. Sacksteder, K.A., J.M. Jones, S.T. South, X. Li, Y. Liu, and S.J. Gould. 2000. PEX19 binds multiple peroxisomal membrane proteins, is predominantly cytoplasmic, and is required for peroxisome membrane synthesis. J. Cell Biol. 148:931-944.
45. Schrader, M., B.E. Reuber, J.C. Morrell, G. Jimenez-Sanchez, C. Obie, T. Stroh, D. Valle, T.A. Schroer, and S.J. Gould. 1998. Expression of PEX11b mediates peroxisome proliferation in the absence of extracellular stimuli. J. Biol. Chem. 273:29607-29614.
46. Snyder, W.B., A. Koller, A.J. Choy, and S. Subramani. 2000. The peroxin Pex19p interacts with multiple, integral membrane proteins at the peroxisomal membrane. J. Cell Biol. 149:1-7.
47. South, S.T., and S.J. Gould. 1999. Peroxisome synthesis in the absence of preexisting peroxisomes. J. Cell Biol. 144:255-266.
48. South, S.T., K.A. Sacksteder, X. Li, Y. Liu, and S.J. Gould. 2000. Inhibitors of COPI and COPII do not block PEX3-mediated peroxisome synthesis. J. Cell Biol. 149:1345-1360.
49. South, S.T., E. Baumgart, and S.J. Gould. 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.
50. Stein, K., A. Schell-Steven, R. Erdmann, and H. Rottensteiner. 2002. Interactions of Pex7p and Pex18p/Pex21p with the peroxisomal docking machinery: implications for the first steps in PTS2 protein import. Mol. Cell. Biol. 22: 6056-6069.
51. Swinkels, B.W., S.J. Gould, A.G. Bodnar, R.A. Rachubinski, and S. Subramani. 1991. A novel, cleavable peroxisomal targeting signal at the amino-terminus of the rat 3-ketoacyl-CoA thiolase. EMBO J. 10:3255-3262.
52. Tabak, H.F., J.L. Murk, I. Braakman, and H.J. Geuze. 2003. Peroxisomes start their life in the endoplasmic reticulum. Traffic 4:512-518.
53. Titorenko, V.I., and R.A. Rachubinski. 2001a. Dynamics of peroxisome assembly and function. Trends Cell Biol. 11:22-29.
54. Titorenko, V.I., and R.A. Rachubinski. 2001b. The life cycle of the peroxisome. Nat. Rev. Mol. Cell Biol. 2:357-368.
55. Wiemer, E.A.C., W.M. Nuttley, B.L. Bertolaet, X. Li, U. Franke, M.J. Wheelock, W.K. Anne, K.R. Johnson, and S. Subramani. 1995. Human peroxisomal targeting signal-1 receptor restores peroxisomal protein import in cells from patients with fatal peroxisomal disorders. J. Cell Biol. 130:51-65.