Structural and functional analysis of the interaction of the AAA-peroxins Pex1p and Pex6p

FEBS Journal

Volumn 272, Issue 1, 2005, Pages 47-58

  Birschmann, Ingvíld ^a,b   Rosenkranz, Katja ^a   Erdmann, Ralf ^a   Kunau, Wolf H ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

AAA proteins; Peroxin; Peroxisomal biogenesis; Pex1p; Pex6p

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; PEROXIN; PEX1P PROTEIN; PEX6P PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BIOGENESIS; GENETIC CONSERVATION; HYDROLYSIS; PEROXISOME; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BASE SEQUENCE; DNA PRIMERS; FUNGAL PROTEINS; MEMBRANE PROTEINS; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 11444254468     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04393.x     Document Type: Article

References (55)

1. van den Bosch H, Schutgens RB, Wanders RJ & Tager JM (1992) Biochemistry of peroxisomes. Annu Rev Biochem 61, 157-197.
2. Eckert JH & Erdmann R (2003) Peroxisome biogenesis. Rev Physiol Biochem Pharmacol 147, 75-121.
3. Matsumoto N, Tamura S & Fujiki Y (2003) The pathogenic peroxin Pex26p recruits the Pex1p-Pex6p AAA ATPase complexes to peroxisomes. Nat Cell Biol 5, 454-460.
4. Rottensteiner H, Stein K, Sonnenhol E & Erdmann R (2003) Conserved function of pex11p and the novel pex25p and pex27p in peroxisome biogenesis. Mol Biol Cell 14, 4316-4328.
5. Vizeacoumar FJ, Torres-Guzman JC, Tam YY, Aitchison JD & Rachubinski RA (2003) YHR150w and YDR479c encode peroxisomal integral membrane proteins involved in the regulation of peroxisome number, size, and distribution in Saccharomyces cerevisiae. J Cell Biol 161, 321-332.
6. Vizeacoumar FJ, Torres-Guzman JC, Bouard D, Aitchison JD & Rachubinski RA (2004) Pex30p, Pex31p, and Pex32p form a family of peroxisomal integral membrane proteins regulating peroxisome size and number in Saccharomyces cerevisiae. Mol Biol Cell 15, 665-677.
7. Lazarow PB & Fujiki Y (1985) Biogenesis of peroxisomes. Ann Rev Cell Biol 1, 489-530.
8. Titorenko VI & Rachubinski RA (2001) Dynamics of peroxisome assembly and function. Trends Cell Biol 11, 22-29.
9. Subramani S (2002) Hitchhiking fads en route to peroxisomes. J Cell Biol 156, 415-417.
10. 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.
11. Gould SJ & Valle D (2000) Peroxisome biogenesis disorders: genetics and cell biology. Trends Genet 16, 340-345.
12. Lazarow PB (2003) Peroxisome biogenesis: advances and conundrums. Curr Opin Cell Biol 15, 489-497.
13. 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.
14. Agne B, Meindl NM, Niederhoff K, Einwachter H, Rehling P, Sickmann A, Meyer HE, Girzalsky W & Kunau WH (2003) Pex8p: an intraperoxisomal organizer of the peroxisomal import machinery. Mol Cell 11, 635-646.
15. Dalal S & Hanson PI (2001) Membrane traffic: what drives the AAA motor? Cell 104, 5-8.
16. Ogura T & Wilkinson AJ (2001) AAA+ superfamily ATPases: common structure - diverse function. Genes Cells 6, 575-597.
17. Lupas AN & Martin J (2002) AAA proteins. Curr Opin Struct Biol 12, 746-753.
18. Dougan DA, Mogk A, Zeth K, Turgay K & Bukau B (2002) AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett 529, 6-10.
19. Whiteheart SW, Rossnagel K, Buhrow SA, Brunner M, Jaenicke R. & Rothman JE (1994) N-ethymaleimide-sensitive fusion protein: a trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J Cell Biol 126, 945-954.
20. Beyer A (1997) Sequence analysis of the AAA protein family. Protein Sci 6, 2043-2058.
21. Faber KN, Heyman JA & Subramani S (1998) Two AAA family peroxins, PpPex1p and PpPex6p, interact with each other in an ATP-dependent manner and are associated with different subcellular membranous structures distinct from peroxisomes. Mol Cell Biol 18, 936-943.
22. Tamura S, Shimozawa N, Suzuki Y, Tsukamoto T, Osumi T & Fujiki Y (1998) A cytoplasmic AAA family peroxin, Pex1p, interacts with Pex6p. Biochem Biophys Res Commun 245, 883-886.
23. Geisbrecht BV, Collins CS, Reuber BE & Gould SJ (1998) Disruption of a PEX1-PEX6 interaction is the most common cause of the neurologic disorders Zellweger syndrome, neonatal adrenoleukodystrophy, and infantile Refsum disease. Proc Natl Acad Sci USA 95, 8630-8635.
24. Kiel JA, Hilbrands RE, van der Klei IJ, Rasmussen SW, Salomons FA, van der Heide M, Faber KN, Cregg JM & Veenhuis M (1999) Hansenula polymorpha Pex1p and Pex6p are peroxisome-associated AAA proteins that functionally and physically interact. Yeast 15, 1059-1078.
25. Whiteheart SW & Kubalek EW (1995) SNAPs and NSF: general members of the fusion apparatus. Trends Cell Biol 5, 64-68.
26. May AP, Whiteheart SW & Weis WI (2001) Unraveling the mechanism of the vesicle transport ATPase NSF, the N-ethylmaleimide-sensitive factor. J Biol Chem 276, 21991-21994.
27. Birschmann I, Stroobants AK, van den Berg M, Schafer A, Rosenkranz K, Kunau WH & Tabak HF (2003) Pex15p of Saccharomyces cerevisiae provides a molecular basis for recruitment of the AAA peroxin Pex6p to peroxisomal membranes. Mol Biol Cell 14, 2226-2236.
28. Erdmann R., Wiebel FF, Flessau A, Rytka J, Beyer A, Fröhlich KU & Kunau W-H (1991) PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell 64, 499-510.
29. Hettema EH, Distel B & Tabak HF (1999) Import of proteins into peroxisomes. Biochim Biophys Acta 1451, 17-34.
30. Hashiguchi N, Kojidani T, Imanaka T, Haraguchi T, Hiraoka Y, Baumgart E, Yokota S, Tsukamoto T & Osumi T (2002) Peroxisomes are formed from complex membrane structures in PEX6-deficient CHO cells upon genetic complementation. Mol Biol Cell 13, 711-722.
31. Komori M, Rasmussen SW, Kiel JAKW, Baerends RJS, Cregg JM, van der Klei IJ & Veenhuis M (1997) The Hansenula polymorpha PEX14 gene encodes a novel peroxisomal membrane protein essential for peroxisome biogenesis. EMBO J 16, 44-53.
32. Bottger G, Barnett P, Klein AT, Kragt A, Tabak HF & Distel B (2000) Saccharomyces cerevisiae PTS1 Receptor Pex5p Interacts with the SH3 domain of the peroxisomal membrane protein Pex13p in an unconventional, non-PXXP-related manner. Mol Biol Cell 11, 3963-3976.
33. Albertini M, Girzalsky W, Veenhuis M & Kunau WH (2001) Pex12p of Saccharomyces cerevisiae is a component of a multi-protein complex essential for peroxisomal matrix protein import. Eur J Cell Biol 80, 257-270.
34. Walker JE, Saraste M, Runswick MJ & Gay NJ (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1, 945-951.
35. Krause T, Kunau W-H & Erdmann R. (1994) Effect of site-directed mutagenesis of conserved lysin residues upon Pas1-protein funtion in peroxisome biogenesis. Yeast 10, 1613-1620.
36. Matveeva EA, He P & Whiteheart SW (1997) N-ethylmaleimide-sensitive fusion protein contains high and low affinity ATP-binding sites that are functionally distinct. J Biol Chem 272, 26413-26418.
37. Linder P, Lasko PF, Ashburner M, Leroy P, Nielsen PJ, Nishi K, Schnier J & Slonimski PP (1989) Birth of the D-E-A-D box. Nature 337, 121-122.
38. Hettema EH, Girzalsky W, van Den Berg M, 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.
39. Tamura S, Matsumoto N, Imamura A, Shimozawa N, Suzuki Y, Kondo N & Fujiki Y (2001) Phenotype-genotype relationships in peroxisome biogenesis disorders of PEX1-defective complementation group 1 are defined by Pex1p-Pex6p interaction. Biochem J 357, 417-426.
40. Nagiec EE, Bernstein A & Whiteheart SW (1995) Each domain of the N-ethylmaleimide-sensitive fusion protein contributes to its transport activity. J Biol Chem 270, 29182-29188.
41. Hay JC & Scheller RH (1997) SNAREs and NSF in targeted membrane fusion. Curr Opin Cell Biol 9, 505-512.
42. Hanson PI, Roth R., Morisaki H, Jahn R. & Heuser JE (1997) Structure and conformational chages in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch eletron mycroscopy. Cell 90, 523-553.
43. Steel GJ & Morgan A (1998) Selective stimulation of the Dl ATPase domain of N-ethylmaleimide-sensitive fusion protein (NSF) by soluble NSF attachment proteins. FEBS Lett 423, 113-116.
44. Poll-The BT, Gootjes J, Duran M, De Klerk JB, Wenniger-Prick LJ, Admiraal RJ, Waterham HR, Wanders RJ & Barth PG (2004) Peroxisome biogenesis disorders with prolonged survival: phenotypic expression in a cohort of 31 patients. Am J Med Genet 126A, 333-338.
45. Chevray PM & Nathans D (1992) Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun. Proc Natl Acad Sci USA 89, 5789-5793.
46. Güldener U, Heck S, Fiedler T, Beinhauer J & Hegemann JH (1996) A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 24, 2519-2524.
47. Erdmann R., Veenhuis M, Mertens D & Kunau W-H (1989) Isolation of peroxisome-deficient mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 86, 5419-5423.
48. Knop M, Siegers K, Pereira G, Zachariae W, Winsor B, Nasmyth K & Schiebel E (1999) Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15, 963-972.
49. Maniatis T, Fritsch EF & Sambrook J (1982) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
50. Ausubel FJ, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA & Struhl K (1992) Current Protocols in Molecular Biology. Greene Publishing Associates, New York.
51. Harlow E & Lane D (1988) Antibodies - A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
52. Fields S & Song OK (1989) A novel genetic system to detect protein-protein interactions. Nature 340, 245-246.
53. Gietz RD & Woods RA (1994) High efficiency transformation in yeast. In Molecular Genetics of Yeast: Practical Approaches (Johnston JA, ed), 121-134. Oxford University Press, Oxford.
54. Rehling P, Marzioch M, Niesen 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.
55. Lamb JR, Michaud WA, Sikorski RS & Hieter PA (1994) Cdc16p, Cdc23p and Cdc27p form a complex essential for mitosis. EMBO J 13, 4321-4328.