Identification of PEX33, a novel component of the peroxisomal docking complex in the filamentous fungus Neurospora crassa

European Journal of Cell Biology

Volumn 89, Issue 12, 2010, Pages 955-964

  Managadze, David ^a   Würtz, Christian ^a   Wiese, Sebastian ^b,c   Schneider, Michael ^a   Girzalsky, Wolfgang ^a   Meyer, Helmut E ^b   Erdmann, Ralf ^a   Warscheid, Bettina ^b,c   Rottensteiner, Hanspeter ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Glyoxysomes; Neurospora crassa; Peroxins; PEX33

Indexed keywords

FUNGAL PROTEIN; MEMBRANE PROTEIN; PEROXIN; PEX33 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOGENESIS; FUNGAL STRAIN; GENE DELETION; MICROBODY; NEUROSPORA CRASSA; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; TWO HYBRID SYSTEM;

CHROMATOGRAPHY, LIQUID; FUNGAL PROTEINS; NEUROSPORA CRASSA; PEROXISOMES; TANDEM MASS SPECTROMETRY;

FUNGI; NEUROSPORA CRASSA;

EID: 78149407181     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2010.07.003     Document Type: Article

References (63)

1. Agne B., Meindl N.M., Niederhoff K., Einwächter H., Rehling P., Sickmann A., Meyer H.E., Girzalsky W., Kunau W.H. Pex8p. An intraperoxisomal organizer of the peroxisomal import machinery. Mol. Cell 2003, 11:635-646.
2. Albertini M., Rehling P., Erdmann R., Girzalsky W., Kiel J.A.K.W., Veenhuis M., Kunau W.-H. Pex14p, a peroxisomal membrane protein binding both receptors of the two PTS-dependent import pathways. Cell 1997, 89:83-92.
3. Birschmann I., Stroobants A.K., Van Den Berg M., Schäfer A., Rosenkranz K., Kunau W.H., Tabak H.F. Pex15p of Saccharomyces cerevisiae provides a molecular basis for recruitment of the AAA Peroxin Pex6p to peroxisomal membranes. Mol. Biol. Cell 2003, 14:2226-2236.
4. Brocard C., Kragler F., Simon M.M., Schuster T., Hartig A. The tetratricopeptide repeat-domain of the Pas10 protein of Saccharomyces cerevisiae is essential for binding the peroxisomal targeting signal-SKL. Biochem. Biophys. Res. Commun. 1994, 204:1016-1022.
5. Brown L.A., Baker A. Shuttles and cycles: transport of proteins into the peroxisome matrix. Mol. Membr. Biol. 2008, 25:363-375.
6. Carvalho A.F., Pinto M.P., Grou C.P., Alencastre I.S., Fransen M., Sá-Miranda C., Azevedo J.E. Ubiquitination of mammalian Pex5p, the peroxisomal import receptor. J. Biol. Chem. 2007, 282:31267-31272.
7. Colot H.V., Park G., Turner G.E., Ringelberg C., Crew C.M., Litvinkova L., Weiss R.L., Borkovich K.A., Dunlap J.C. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10352-10357.
8. Davies R. Genetic, Biochemical, and Molecular Techniques. Neurospora: Contributions of a Model Organism 2000, Oxford University Press, Oxford, UK, pp. 283-302.
9. Dodt G., Gould S.J. 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. 1996, 135:1763-1774.
10. Dodt G., Warren D., Becker E., Rehling P., Gould S.J. Domain mapping of human PEX5 reveals functional and structural similarities to S. cerevisiae Pex18p and Pex21p. J. Biol. Chem. 2001, 276:41769-41781.
11. Erdmann R., Wiebel F.F., Flessau A., Rytka J., Beyer A., Fröhlich K.U., Kunau W.-H. PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell 1991, 64:499-510.
12. Fagarasanu A., Fagarasanu M., Eitzen G.A., Aitchison J.D., Rachubinski R.A. The peroxisomal membrane protein Inp2p Is the peroxisome-specific receptor for the myosin V motor Myo2p of Saccharomyces cerevisiae. Dev. Cell 2006, 10:587-600.
13. Garceau N.Y., Liu Y., Loros J.J., Dunlap J.C. Alternative initiation of translation and time-specific phosphorylation yield multiple forms of the essential clock protein FREQUENCY. Cell 1997, 89:469-476.
14. Gould S.J., Keller G.A., Hosken N., Wilkinson J., Subramani S. A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 1989, 108:1657-1664.
15. Grou C.P., Carvalho A.F., Pinto M.P., Wiese S., Piechura H., Meyer H.E., Warscheid B., Sa-Miranda C., Azevedo J.E. Members of the E2D (UbcH5) family mediate the ubiquitination of the conserved cysteine of Pex5p, the peroxisomal import receptor. J. Biol. Chem. 2008, 283:14190-14197.
16. Grunau S., Schliebs W., Linnepe R., Neufeld C., Cizmowski C., Reinartz B., Meyer H.E., Warscheid B., Girzalsky W., Erdmann R. Peroxisomal targeting of PTS2-pre-import complexes in the yeast Saccharomyces cerevisiae. Traffic 2009, 10:451-460.
17. Hayashi M., Toriyama K., Kondo M., Kato A., Mano S., De Bellis L., Hayashi-Ishimaru Y., Yamaguchi K., Hayashi H., Nishimura M. Functional transformation of plant peroxisomes. Cell. Biochem. Biophys. 2000, 32:295-304. Spring.
18. Hoepfner D., van den Berg M., Philippsen P., Tabak H.F., Hettema E.H. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 2001, 155:979-990.
19. Huhse B., Rehling P., Albertini M., Blank L., Meller K., Kunau W.-H. Pex17p of Saccharomyces cerevisiae is a novel peroxin and component of the peroxisomal protein translocation machinery. J. Cell Biol. 1998, 140:49-60.
20. James P., Halladay J., Craig E.A. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 1996, 144:1425-1436.
21. Jedd G., Chua N.H. A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat. Cell Biol. 2000, 2:226-231.
22. Kiel J.A., Veenhuis M., van der Klei I.J. PEX genes in fungal genomes: common, rare or redundant. Traffic 2006, 7:1291-1303.
23. Lanyon-Hogg T., Warriner S.L., Baker A. Getting a camel through the eye of a needle: the import of folded proteins by peroxisomes. Biol. Cell 2010, 102:245-263.
24. Lazarow P.B., Fujiki Y. Biogenesis of peroxisomes. Ann. Rev. Cell. Biol. 1985, 1:489-530.
25. Lazarow P.B. The import receptor Pex7p and the PTS2 targeting sequence. Biochim. Biophys. Acta 2006, 1763:1599-1604.
26. Ma C., Schumann U., Rayapuram N., Subramani S. The peroxisomal matrix import of Pex8p requires only PTS receptors and Pex14p. Mol. Biol. Cell 2009, 20:3680-3689.
27. Maeting I., Schmidt G., Sahm H., Revuelta J.L., Stierhof Y.D., Stahmann K.P. Isocitrate lyase of Ashbya gossypii-transcriptional regulation and peroxisomal localization. FEBS Lett. 1999, 444:15-21.
28. Managadze D., Würtz C., Sichting M., Niehaus G., Veenhuis M., Rottensteiner H. The peroxin PEX14 of Neurospora crassa is essential for the biogenesis of both glyoxysomes and Woronin bodies. Traffic 2007, 8:687-701.
29. Marzioch M., Erdmann R., Veenhuis M., Kunau W.-H. 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. 1994, 13:4908-4918.
30. Matsumoto N., Tamura S., Fujiki Y. The pathogenic peroxin Pex26p recruits the Pex1p-Pex6p AAA ATPase complexes to peroxisomes. Nat. Cell. Biol. 2003, 5:454-460.
31. Matsumura T., Otera H., Fujiki Y. 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-impaired Chinese hamster ovary cell mutant. J. Biol. Chem. 2000, 275:21715-21721.
32. Meinecke M., Cizmowski C., Schliebs W., Kruger V., Beck S., Wagner R., Erdmann R. The peroxisomal importomer constitutes a large and highly dynamic pore. Nat. Cell Biol. 2010, 12:273-277.
33. Miyata N., Fujiki Y. Shuttling mechanism of peroxisome targeting signal type 1 receptor Pex5: ATP-independent import and ATP-dependent export. Mol. Cell. Biol. 2005, 25:10822-10832.
34. Mokranjac D., Paschen S.A., Kozany C., Prokisch H., Hoppins S.C., Nargang F.E., Neupert W., Hell K. Tim50, a novel component of the TIM23 preprotein translocase of mitochondria. EMBO J. 2003, 22:816-825.
35. Neuhoff V., Stamm R., Eibl H. Highly sensitive colloidal staining in phosphatatic acid. Electrophoresis 1985, 6:427-448.
36. Oliveira M.E., Gouveia A.M., Pinto R.A., Sa-Miranda C., Azevedo J.E. The energetics of Pex5p-mediated peroxisomal protein import. J. Biol. Chem. 2003, 278:39483-39488.
37. Perkins D.N., Pappin D.J., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
38. Platta H.W., Grunau S., Rosenkranz K., Girzalsky W., Erdmann R. Functional role of the AAA peroxins in dislocation of the cycling PTS1 receptor back to the cytosol. Nat. Cell Biol. 2005, 7:817-822.
39. Platta H.W., El Magraoui F., Schlee D., Grunau S., Girzalsky W., Erdmann R. Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. J. Cell Biol. 2007, 177:197-204.
40. Platta H.W., Debelyy M.O., El Magraoui F., Erdmann R. The AAA peroxins Pex1p and Pex6p function as dislocases for the ubiquitinated peroxisomal import receptor Pex5p. Biochem. Soc. Trans. 2008, 36:99-104.
41. Poirier Y., Antonenkov V.D., Glumoff T., Hiltunen J.K. Peroxisomal beta-oxidation-a metabolic pathway with multiple functions. Biochim. Biophys. Acta 2006, 1763:1413-1426.
42. Rachubinski R.A., Subramani S. How proteins penetrate peroxisomes. Cell 1995, 83:525-528.
43. Rehling P., Marzioch M., Niesen F., Wittke E., Veenhuis M., Kunau W.-H. The import receptor for the peroxisomal targeting signal 2 (PTS2) in Saccharomyces cerevisiae is encoded by the PAS7 gene. EMBO J. 1996, 15:2901-2913.
44. Reichle R.E., Alexander J.V. Multiperforate septations, Woronin bodies, and septal plugs in Fusarium. J. Cell Biol. 1965, 24:489-496.
45. Rottensteiner H., Kramer A., Lorenzen S., Stein K., Landgraf C., Volkmer-Engert R., Erdmann R. Peroxisomal membrane proteins contain common Pex19p-binding sites that are an integral part of their targeting signals (mPTS). Mol. Biol. Cell 2004, 7:3406-3417.
46. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Schiestl R.H., Gietz R.D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 1989, 16:339-346.
48. Schliebs W., Kunau W.H. PTS2 co-receptors: diverse proteins with common features. Biochim. Biophys. Acta 2006, 1763:1605-1612.
49. Schliebs W., Würtz C., Kunau W.H., Veenhuis M., Rottensteiner H. A eukaryote without catalase-containing microbodies: Neurospora crassa exhibits a unique cellular distribution of its four catalases. Eukaryot. Cell 2006, 5:1490-1502.
50. Schrader M., Fahimi H.D. Growth and division of peroxisomes. Int. Rev. Cytol. 2007, 255:237-290.
51. Sichting M., Schell-Steven A., Prokisch H., Erdmann R., Rottensteiner H. Pex7p and Pex20p of Neurospora crassa function together in PTS2-dependent protein import into peroxisomes. Mol. Biol. Cell 2003, 14:810-821.
52. Soundararajan S., Jedd G., Li X., Ramos-Pamplona M., Chua N.H., Naqvi N.I. Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell 2004, 16:1564-1574.
53. Stein K., Schell-Steven A., Erdmann R., Rottensteiner H. Interactions of Pex7p and Pex18p/Pex21p with the peroxisomal docking machinery: implications for the first steps in PTS2 protein import. Mol. Cell. Biol. 2002, 22:6059-6069.
54. Stephan C., Reidegeld K.A., Hamacher M., van Hall A., Marcus K., Taylor C., Jones P., Muller M., Apweiler R., Martens L., Korting G., Chamrad D.C., Thiele H., Bluggel M., Parkinson D., Binz P.A., Lyall A., Meyer H.E. Automated reprocessing pipeline for searching heterogeneous mass spectrometric data of the HUPO Brain Proteome Project pilot phase. Proteomics 2006, 6:5015-5029.
55. Terlecky S.R., Nuttley W.M., McCollum D., Sock E., Subramani S. The Pichia pastoris peroxisomal protein Pas8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. EMBO J. 1995, 14:3627-3634.
56. Thieringer R., Kunau W.-H. Beta-oxidation system of the filamentous fungus Neurospora crassa. Structural characterization of the trifunctional protein. J. Biol. Chem. 1991, 266:13118-13123.
57. Voorn-Brouwer T., van der Leij I., Hemrika W., Distel B., Tabak H.F. Sequence of the PAS8 gene, the product of which is essential for biogenesis of peroxisomes in Saccharomyces cerevisiae. Biochem. Biophys. Acta 1993, 1216:325-328.
58. Wanders R.J., Waterham H.R. Peroxisomal disorders: the single peroxisomal enzyme deficiencies. Biochim. Biophys. Acta 2006, 1763:1707-1720.
59. Wanner G., Theimer R.R. Two types of microbodies in Neurospora crassa. Ann. N Y Acad. Sci. 1982, 386:269-284.
60. Wergin W.P. Development of Woronin bodies from microbodies in Fusarium oxysporum f.sp. lycopersici. Protoplasma 1973, 76:249-260.
61. Wiese S., Gronemeyer T., Ofman R., Kunze M., Grou C.P., Almeida J.A., Eisenacher M., Stephan C., Hayen H., Schollenberger L., Korosec T., Waterham H.R., Schliebs W., Erdmann R., Berger J., Meyer H.E., Just W., Azevedo J.E., Wanders R.J., Warscheid B. Proteomics characterization of mouse kidney peroxisomes by tandem mass spectrometry and protein correlation profiling. Mol. Cell. Proteom. 2007, 6:2045-2057.
62. Würtz C., Schliebs W., Erdmann R., Rottensteiner H. The Woronin body as a peroxisome with a function in the maintenance of cellular integrity. Res. Singpost 2009, 37(661):43-59.
63. Yaffe M.P., Schatz G. Two nuclear mutations that block mitochondrial protein import in yeast. Proc. Natl. Acad. Sci. U.S.A. 1984, 81:4819-4823.