A single peroxisomal targeting signal mediates matrix protein import in diatoms

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Gonzalez, Nicola H ^a   Felsner, Gregor ^a   Schramm, Frederic D ^a   Klingl, Andreas ^b   Maier, Uwe G ^a,b   Bolte, Kathrin ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b Unit of Metabolism   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A ACYLTRANSFERASE; ACYL COENZYME A OXIDASE; CITRATE SYNTHASE; HYBRID PROTEIN; MALATE DEHYDROGENASE; MATRIX PROTEIN; PEROXIN; PEROXIN 10; PEROXIN 3; PEROXIN 7; UNCLASSIFIED DRUG; CELL RECEPTOR;

ARTICLE; CAENORHABDITIS ELEGANS; COMPUTER MODEL; CONSENSUS SEQUENCE; CONTROLLED STUDY; DIATOM; FLUORESCENCE MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOMAL TARGETING SIGNAL 1; PEROXISOMAL TARGETING SIGNAL 2; PEROXISOME; PHAEODACTYLUM TRICORNUTUM; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; TRANSMISSION ELECTRON MICROSCOPY; METABOLISM; SIGNAL TRANSDUCTION;

BACILLARIOPHYTA; CAENORHABDITIS ELEGANS; EUKARYOTA; PHAEODACTYLUM TRICORNUTUM;

DIATOMS; PEROXISOMES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION;

EID: 80053054984     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025316     Document Type: Article

References (60)

1. Schrader M, Fahimi HD, (2008) The peroxisome: still a mysterious organelle. Histochem Cell Biol 129: 421-440.
2. Agne B, Meindl NM, Niederhoff K, Einwachter H, Rehling P, et al. (2003) Pex8p: an intraperoxisomal organizer of the peroxisomal import machinery. Mol Cell 11: 635-646.
3. Gould SJ, Keller GA, Subramani S, (1987) Identification of a peroxisomal targeting signal at the carboxy terminus of firefly luciferase. J Cell Biol 105: 2923-2931.
4. 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.
5. Gould SJ, Keller GA, Subramani S, (1988) Identification of peroxisomal targeting signals located at the carboxy terminus of four peroxisomal proteins. J Cell Biol 107: 897-905.
6. Rucktäschel R, Girzalsky W, Erdmann R, (2010) Protein import machineries of peroxisomes. Biochim Biophys Acta 1808: 892-900.
7. 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.
8. Brocard C, Kragler F, Simon MM, Schuster T, Hartig A, (1994) The tetratricopeptide repeat-domain of the PAS10 protein of Saccharomyces cerevisiae is essential for binding the peroxisomal targeting signal-SKL. Biochem Biophys Res Commun 204: 1016-1022.
9. 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.
10. Lazarow PB, (2006) The import receptor Pex7p and the PTS2 targeting sequence. Biochim Biophys Acta 1763: 1599-1604.
11. Rachubinski RA, Subramani S, (1995) How proteins penetrate peroxisomes. Cell 83: 525-528.
12. Rehling P, Marzioch M, Niesen F, Wittke E, Veenhuis M, et al. (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.
13. Marzioch M, Erdmann R, Veenhuis M, Kunau WH, (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.
14. Zhang JW, Lazarow PB, (1995) PEB1 (PAS7) in Saccharomyces cerevisiae encodes a hydrophilic, intra-peroxisomal protein that is a member of the WD repeat family and is essential for the import of thiolase into peroxisomes. J Cell Biol 129: 65-80.
15. Brown LA, Baker A, (2008) Shuttles and cycles: transport of proteins into the peroxisome matrix (review). Mol Membr Biol 25: 363-375.
16. Erdmann R, Schliebs W, (2005) Peroxisomal matrix protein import: the transient pore model. Nat Rev Mol Cell Biol 6: 738-742.
17. Meinecke M, Cizmowski C, Schliebs W, Kruger V, Beck S, et al. (2010) The peroxisomal importomer constitutes a large and highly dynamic pore. Nat Cell Biol 12: 273-277.
18. Gabaldón T, Snel B, van Zimmeren F, Hemrika W, Tabak H, et al. (2006) Origin and evolution of the peroxisomal proteome. Biol Direct 1: 8.
19. Schliebs W, Girzalsky W, Erdmann R, (2010) Peroxisomal protein import and ERAD: variations on a common theme. Nat Rev Mol Cell Biol 11: 885-890.
20. Bolte K, Gruenheit N, Felsner G, Sommer MS, Maier UG, et al. (2011) Making new out of old: Recycling and modification of an ancient protein translocation system during eukaryotic evolution: Mechanistic comparison and phylogenetic analysis of ERAD, SELMA and the peroxisomal importomer. Bioessays 33: 368-376.
21. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, et al. (2005) The tree of eukaryotes. Trends Ecol Evol 20: 670-676.
22. Gabaldón T, (2010) Peroxisome diversity and evolution. Philos Trans R Soc Lond B Biol Sci 365: 765-773.
23. Gould SB, Waller RF, McFadden GI, (2008) Plastid evolution. Annu Rev Plant Biol 59: 491-517.
24. Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, et al. (2009) Protein targeting into secondary plastids. J Eukaryot Microbiol 56: 9-15.
25. Hempel F, Bozarth A, Sommer MS, Zauner S, Przyborski JM, et al. (2007) Transport of nuclear-encoded proteins into secondarily evolved plastids. Biol Chem 388: 899-906.
26. Keeling PJ, (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci 365: 729-748.
27. Philippi ML, Parish RW, Hohl HR, (1975) Histochemical and biochemical evidence for the presence of microbodies in phytophthora palmivora. Arch Microbiol 103: 127-132.
28. Muller M, (1973) Peroxisomes and hydrogenosomes in protozoa. J Histochem Cytochem 21: 955-957.
29. Stelly N, Balmefrezol M, Adoutte A, (1975) Diaminobenzidine reactivity of mitochondria and peroxisomes in Tetrahymena and in wild-type and cytochrome oxidase-deficient Paramecium. J Histochem Cytochem 23: 686-696.
30. Schluter A, Fourcade S, Ripp R, Mandel JL, Poch O, et al. (2006) The evolutionary origin of peroxisomes: an ER-peroxisome connection. Mol Biol Evol 23: 838-845.
31. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, et al. (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306: 79-86.
32. Winkler U, Stabenau H, (1995) Isolation and characterization of peroxisomes from diatoms. Planta 195: 403-407.
33. Soding J, (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951-960.
34. Platta HW, El Magraoui F, Schlee D, Grunau S, Girzalsky W, et al. (2007) Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. J Cell Biol 177: 197-204.
35. Elgersma Y, Kwast L, van den Berg M, Snyder WB, Distel B, et al. (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.
36. 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.
37. Fagarasanu A, Fagarasanu M, Rachubinski RA, (2007) Maintaining peroxisome populations: a story of division and inheritance. Annu Rev Cell Dev Biol 23: 321-344.
38. 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.
39. 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.
40. Mano S, Nakamori C, Hayashi M, Kato A, Kondo M, et al. (2002) Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: dynamic morphology and actin-dependent movement. Plant Cell Physiol 43: 331-341.
41. Peterhansel C, Maurino VG, (2011) Photorespiration redesigned. Plant Physiol 155: 49-55.
42. Kroth PG, Chiovitti A, Gruber A, Martin-Jezequel V, Mock T, et al. (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS One 3: e1426.
43. 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.
44. 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.
45. Otera H, Harano T, Honsho M, Ghaedi K, Mukai S, et al. (2000) The mammalian peroxin Pex5pL, the longer isoform of the mobile peroxisome targeting signal (PTS) type 1 transporter, translocates the Pex7p.PTS2 protein complex into peroxisomes via its initial docking site, Pex14p. J Biol Chem 275: 21703-21714.
46. Woodward AW, Bartel B, (2005) The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Mol Biol Cell 16: 573-583.
47. Carrie C, Murcha MW, Millar AH, Smith SM, Whelan J, (2007) Nine 3-ketoacyl-CoA thiolases (KATs) and acetoacetyl-CoA thiolases (ACATs) encoded by five genes in Arabidopsis thaliana are targeted either to peroxisomes or cytosol but not to mitochondria. Plant Mol Biol 63: 97-108.
48. Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, et al. (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19: 3170-3193.
49. Motley AM, Hettema EH, Ketting R, Plasterk R, Tabak HF, (2000) Caenorhabditis elegans has a single pathway to target matrix proteins to peroxisomes. EMBO Rep 1: 40-46.
50. Shinozaki A, Sato N, Hayashi Y, (2009) Peroxisomal targeting signals in green algae. Protoplasma 235: 57-66.
51. Kröger N, Poulsen N, (2008) Diatoms-from cell wall biogenesis to nanotechnology. Annu Rev Genet 42: 83-107.
52. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
53. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular Cloning. A laboratory manual Cold Spring Habor Labatory Press.
54. Zaslavskaia LA, Lippmeier JC, Kroth PG, Grossman AR, Apt KE, (2000) Transformation of the diatom Phaeodactylum tricornutum (bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol 36: 379-386.
55. Apt KE, Kroth-Pancic PG, Grossman AR, (1996) Stable nuclear transformation of the diatom Phaeodactylum tricornutum. Mol Gen Genet 252: 572-579.
56. Junglas B, Briegel A, Burghardt T, Walther P, Wirth R, et al. (2008) Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell-cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography. Arch Microbiol 190: 395-408.
57. Klingl A, Moissl-Eichinger C, Wanner G, Zweck J, Huber H, et al. (2011) Analysis of the surface proteins of Acidithiobacillus ferrooxidans strain SP5/1 and the new, pyrite-oxidizing Acidithiobacillus isolate HV2/2, and their possible involvement in pyrite oxidation. Arch Microbiol.
58. Rachel R, Meyer C, Klingl A, Gurster S, Heimerl T, et al. (2010) Analysis of the ultrastructure of archaea by electron microscopy. Methods Cell Biol 96: 47-69.
59. Walther P, Ziegler A, (2002) Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J Microsc 208: 3-10.
60. 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.