Publikationsserver der Universitätsbibliothek Marburg

Titel:Neue Enzyme für ein altes Organell: Kryptische peroxisomale Lokalisationssignale
Autor:Freitag, Johannes
Weitere Beteiligte: Bölker, Michael (Prof. Dr.)
Veröffentlicht:2013
URI:https://archiv.ub.uni-marburg.de/diss/z2013/0477
URN: urn:nbn:de:hebis:04-z2013-04775
DOI: https://doi.org/10.17192/z2013.0477
DDC: Biowissenschaften, Biologie
Titel (trans.):Cryptic peroxisomal targeting of glycoloytic enzymes
Publikationsdatum:2014-04-10
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Ustilago zeae, Peroxisom, Duale Lokalisierung, glycolysis, Glykolyse, alternative splicing, dual localization, peroxisome, Spleißen, Translational readthrough, Stopcodon, Proteintransport

Zusammenfassung:
Peroxisomen sind nahezu ubiquitäre, eukaryotische Zellorganellen, die am Abbau von Fettsäuren und an der Entgiftung des dabei entstehenden Wasserstoffperoxids beteiligt sind. Neben dieser generellen Funktion beherbergen die Peroxisomen weitere Stoffwechselwege. Dazu zählen Teile des Glyoxylatwegs in Pflanzen und Pilzen und Stoffwechselwege für die Bildung von Sekundärmetaboliten. Eine Sonderform der Peroxisomen sind die Glycosomen, die in Trypanosomen identifiziert werden konnten und einen Großteil der glykolytischen Enzyme enthalten. Peroxisomale Matrixproteine enthalten entweder carboxyterminale oder aminoterminale PTS („peroxisomal targeting signal“)-Motive (C-terminal: PTS1; N-terminal: PTS2). Diese werden von zytoplasmatischen Rezeptoren erkannt, die gefaltete und sogar im Komplex vorliegende Proteine in die Peroxisomen überführen. In dem pflanzenpathogenen Basidiomyceten Ustilago maydis konnten im Verlauf dieser Arbeit kryptische PTS1-Motive in einer Reihe von Enzymen aus der Glykolyse bzw. Gluconeogenese identifiziert werden. Peroxisomale Isoformen dieser Enzyme entstehen durch alternatives Spleißen oder durch Überlesen von Stopcodons während der Translation. Eine bioinformatische Analyse ergab, dass in einer Vielzahl von Pilzen Isoformen glykolytischer Enzyme mit PTS1-Motiv gebildet werden, wobei die Mechanismen zur Herstellung dieser Isoformen in unterschiedlichen Spezies variieren. Zudem wurden in einigen glykolytischen Enzymen ungewöhnliche PTS1-Motive gefunden, die vom bisher gültigen Konsensus für PTS1-Motive abweichen und ebenfalls eine duale Lokalisierung der Enzyme in Peroxisomen und dem Zytoplasma hervorrufen können. Bei der genaueren Charakterisierung der Peroxisomen in U. maydis fiel auf, dass diese Organellen nicht nur für die β-Oxidation von Fettsäuren benötigt werden, sondern auch eine Funktion beim Zuckerstoffwechsel und der biotrophen Interaktion mit der Wirtspflanze Mais haben. Außerdem konnte gezeigt werden, dass Peroxisomen in U. maydis an der Synthese eines extrazellulären Glykolipids beteiligt sind. Die Ergebnisse dieser Arbeit legen nahe, dass die Peroxisomen in Pilzen durch eine größere metabolische Vielfalt charakterisiert sind, als bisher angenommen wurde. Die Identifizierung kryptischer PTS1-Motive in Enzymen aus der Glykolyse lässt die Vermutung zu, dass Peroxisomen auch in anderen Organismen noch weitere unerwartete Proteine beinhalten.

Bibliographie / References

  1. Stalder L & Mühlemann O (2008) The meaning of nonsense. Trends in Cell Biology 18: 315–321
  2. Liu H, Tan X, Veenhuis M, McCollum D & Cregg JM (1992) An efficient screen for peroxisome-deficient mutants of Pichia pastoris. Journal of Bacteriology 174: 4943–4951
  3. McNew JA & Goodman JM (1994) An oligomeric protein is imported into peroxisomes in vivo. The Journal of Cell Biology 127: 1245–1257
  4. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, Bruno D, Vamathevan J, Miranda M, Anderson IJ, Fraser JA & others (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307: 1321–1324
  5. Maggio-Hall LA, Wilson RA & Keller NP (2005) Fundamental contribution of β-oxidation to polyketide mycotoxin production in planta. Molecular Plant-Microbe Interactions 18: 783–793
  6. Yogev O & Pines O (2011) Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochimica et Biophysica Acta 1808: 1012–1020
  7. Tabak HF, Hoepfner D, V.d. Zand A, Geuze HJ, Braakman I & Huynen MA (2006) Formation of peroxisomes: Present and past. Biochimica et Biophysica Acta 1763: 1647–1654
  8. Van der Zand A, Braakman I & Tabak HF (2010) Peroxisomal membrane proteins insert into the endoplasmic reticulum. Molecular Biology of the Cell 21: 2057–2065
  9. Van der Zand A, Gent J, Braakman I & Tabak H (2012) Biochemically Distinct Vesicles from the Endoplasmic Reticulum Fuse to Form Peroxisomes. Cell 149: 397–409
  10. Martinez-Espinoza AD, Garcia-Pedrajas MD & Gold SE (2002) The Ustilaginales as plant pests and model systems. Fungal Genetics and Biology 35: 1–20
  11. Morita T, Fukuoka T, Imura T & Kitamoto D (2013a) Production of mannosylerythritol lipids and their application in cosmetics. Applied Microbiology and Biotechnology: 1–10
  12. Shen YQ & Burger G (2009) Plasticity of a key metabolic pathway in fungi. Functional & Integrative Genomics 9: 145–151
  13. Skarznski T, Moody PCE & Wonacott AJ (1987) Structure of holo-glyceraldehyde-3-phosphate dehydrogenase from Bacillus stearothermophilus at 1.8 Å resolution. Journal of Molecular Biology 193: 171–187
  14. Voorn-Brouwer T, Van der Leij I, Hemrika W, Distel B & Tabak HF (1993) Sequence of the PAS8 gene, the product of which is essential for biogenesis of peroxisomes in Saccharomyces cerevisiae. Biochimica et Biophysica Acta 1216: 325–328
  15. Muirhead H & Watson H (1992) Glycolytic enzymes: from hexose to pyruvate. Current Opinion in Structural Biology 2: 870–876
  16. Visser WF, Van Roermund CWT, Ijlst L, Hellingwerf KJ, Waterham HR & Wanders RJA (2006) First identification of a 2-ketoglutarate/isocitrate transport system in mammalian peroxisomes and its characterization. Biochemical and Biophysical Research Communications 348: 1224–1231
  17. Steinberg G & Perez-Martin J (2008) Ustilago maydis, a new fungal model system for cell biology. Trends in Cell Biology 18: 61–67
  18. Visser WF, Van Roermund CWT, Waterham HR & Wanders RJA (2002) Identification of human PMP34 as a peroxisomal ATP transporter. Biochemical and Biophysical Research Communications 299: 494–497
  19. Maeting I, Schmidt G, Sahm H, Revuelta JL, Stierhof Y-D, Stahmann K & others (1999) Isocitrate lyase of Ashbya gossypii--transcriptional regulation and peroxisomal localization. FEBS Letters 444: 15–21
  20. Zheng L, Roeder RG & Luo Y (2003) S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114: 255–266
  21. Wilson RA & Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nature Reviews Microbiology 7: 185–195
  22. Yan M, Rachubinski DA, Joshi S, Rachubinski RA & Subramani S (2008) Dysferlin domain-containing proteins, Pex30p and Pex31p, localized to two compartments, control the number and size of oleate- induced peroxisomes in Pichia pastoris. Molecular Biology of the Cell 19: 885–898
  23. Schluter A, Ripp R, Fourcade S, Mandel JL, Poch O & Pujol A (2006) The Evolutionary Origin of Peroxisomes: An ER-Peroxisome Connection. Mol Biol Evol 23(4): 838-845
  24. Steneberg P, Englund C, Kronhamn J, Weaver TA & Samakovlis C (1998) Translational readthrough in the hdc mRNA generates a novel branching inhibitor in theDrosophila trachea. Genes & Development 12: 956– 967
  25. Mendoza-Mendoza A, Berndt P, Djamei A, Weise C, Linne U, Marahiel M, Vraneš M, Kämper J & Kahmann R (2009) Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Molecular Microbiology 71: 895–911
  26. Strijbis K, Den Burg J, F Visser W, Den Berg M & Distel B (2012) Alternative splicing directs dual localization of Candida albicans 6-phosphogluconate dehydrogenase to cytosol and peroxisomes. FEMS Yeast Research 12 (1): 61-8
  27. Mielnichuk N, Sgarlata C & Pérez-Martín J (2009) A role for the DNA-damage checkpoint kinase Chk1 in the virulence program of the fungus Ustilago maydis. Journal of Cell Science 122: 4130–4140
  28. Schirmer T & Evans PR (1990) Structural basis of the allosteric behaviour of phosphofructokinase. Nature 343: 140–145
  29. Wang D, Visser N V, Veenhuis M & Der Klei IJ (2003) Physical interactions of the peroxisomal targeting signal 1 receptor pex5p, studied by fluorescence correlation spectroscopy. Journal of Biological Chemistry 278: 43340–43345
  30. Schuetz R, Zamboni N, Zampieri M, Heinemann M & Sauer U (2012) Multidimensional Optimality of Microbial Metabolism. Science 336: 601–604
  31. Visser WF, Van Roermund CWT, Ijlst L, Waterham HR & Wanders RJA (2007) Metabolite transport across the peroxisomal membrane. Biochemical Journal 401: 365
  32. Strijbis K & Distel B (2010) Intracellular acetyl unit transport in fungal carbon metabolism. Eukaryotic Cell 9: 1809–1815
  33. Wanders RJA & Waterham HR (2006) Biochemistry of mammalian peroxisomes revisited. Annual Review Biochemistry 75: 295–332
  34. Michels PAM, Bringaud F, Herman M & Hannaert V (2006) Metabolic functions of glycosomes in trypanosomatids. Biochimica et Biophysica Acta 1763: 1463–1477
  35. Matlin AJ, Clark F & Smith CWJ (2005) Understanding alternative splicing: towards a cellular code. Nature Reviews Molecular Cell Biology 6: 386–398
  36. Mayer BJ (2001) SH3 domains: complexity in moderation. Journal of Cell Science 114: 1253–1263
  37. Sullivan DT, MacIntyre R, Fuda N, Fiori J, Barrilla J & Ramizel L (2003) Analysis of glycolytic enzyme co- localization in Drosophila flight muscle. Journal of Experimental Biology 206: 2031–2038
  38. Masters C (1997) Gluconeogenesis and the peroxisome. Molecular and Cellular Biochemistry 166: 159–168
  39. Mano S, Hayashi M & Nishimura M (2000) A leaf-peroxisomal protein, hydroxypyruvate reductase, is produced by light-regulated alternative splicing. Cell Biochemistry and Biophysics 32: 147–154
  40. Szewczyk E, Andrianopoulos A, Davis MA & Hynes MJ (2001a) A Single Gene Produces Mitochondrial, Cytoplasmic, and Peroxisomal NADP-dependent Isocitrate Dehydrogenase in Aspergillus nidulans. Journal of Biological Chemistry 276: 37722–37729
  41. McKee T & McKee JR (2009) Biochemistry: The Molecular Basis of Life Oxford University Press
  42. Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. Journal of Molecular Biology 98: 503–517
  43. McAlister L & Holland MJ (1985) Differential expression of the three yeast glyceraldehyde-3-phosphate dehydrogenase genes. Journal of Biological Chemistry 260: 15019–15027
  44. Winterberg B, Uhlmann S, Linne U, Lessing F, Marahiel MA, Eichhorn H, Kahmann R & Schirawski J (2010) Elucidation of the complete ferrichrome A biosynthetic pathway in Ustilago maydis. Molecular Microbiology 75: 1260–1271
  45. Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA & Arnheim N (1985) Enzymatic amplification of b-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230: 1350–1354
  46. McAlister-Henn L, Steffan JS, Minard KI & Anderson SL (1995) Expression and function of a mislocalized form of peroxisomal malate dehydrogenase (MDH3) in yeast. Journal of Biological Chemistry 270: 21220–21225
  47. Spellig T, Bottin A & Kahmann R (1996) Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungusUstilago maydis. Molecular and General Genetics 252: 503–509
  48. Shaner NC, Campbell RE, Steinbach PA, Giepmans BNG, Palmer AE & Tsien RY (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nature Biotechnology 22: 1567–1572
  49. Müller WH, Bovenberg RAL, Groothuis MH, Kattevilder F, Smaal EB, Der Voort LHM & Verkleij AJ (1992) Involvement of microbodies in penicillin biosynthesis. Biochimica et Biophysica Acta 1116: 210–213
  50. Maggio-Hall LA & Keller NP (2004) Mitochondrial β-oxidation in Aspergillus nidulans. Molecular Microbiology 54: 1173–1185
  51. Wolfe KH, Shields DC & others (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708–712
  52. of machine learning methods and in vivo subcellular targeting analyses. The Plant Cell 23: 1556–1572
  53. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB & Erlich HA (1988) Primer- directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491
  54. Wickner W & Schekman R (2005) Protein translocation across biological membranes. Science 310: 1452–1456
  55. Singh R, Green MR & others (1993) Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase. Science 259: 365
  56. Mullis KB, Faloona FA, Scharf SJ, Saiki RK, Horn GT, Erlich H & others (1986) Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. In Cold Spring Harb Symp Quant Biol pp 263–273.
  57. Zarnack K, Maurer S, Kaffarnik F, Ladendorf O, Brachmann A, Kämper J & Feldbrügge M (2006) Tetracycline- regulated gene expression in the pathogen Ustilago maydis. Fungal Genetics and Biology 43: 727–738
  58. Zala D, Hinckelmann M V, Yu H, Da Cunha MM, Liot G, Cordelières FP, Marco S & Saudou F (2013) Vesicular Glycolysis Provides On-Board Energy for Fast Axonal Transport. Cell 152: 479–491
  59. Mendgen K & Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends in Plant Science 7: 352–356
  60. Meyer T, Hölscher C, Schwöppe C & Von Schaewen A (2011) Alternative targeting of Arabidopsis plastidic glucose-6-phosphate dehydrogenase G6PD1 involves cysteine-dependent interaction with G6PD4 in the cytosol. The Plant Journal 66: 745–758
  61. Schirawski J, Mannhaupt G, Münch K, Brefort T, Schipper K, Doehlemann G, Di Stasio M, Rössel N, Mendoza- Mendoza A, Pester D & others (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330: 1546–1548
  62. Snetselaar KM & Mims CW (1994) Light and electron microscopy of Ustilago maydis hyphae in maize. Mycological Research 98: 347–355
  63. Snetselaar KM (1993) Microscopic Observation of Ustilago maydis Mating Interactions. Experimental Mycology 17: 345–355
  64. Snetselaar KM & Mims CW (1993) Infection of maize stigmas by Ustilago maydis: light and electron microscopy. Phytopathology 83: 843
  65. Snetselaar KM & Mims CW (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia: 193–203
  66. 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
  67. Steneberg P & Samakovlis C (2001) A novel stop codon readthrough mechanism produces functional Headcase protein in Drosophila trachea. EMBO Reports 2: 593–7
  68. Sriram G, Martinez JA, McCabe ERB, Liao JC & Dipple KM (2005) Single-gene disorders: what role could moonlighting enzymes play? The American Journal of Human Genetics 76: 911–924
  69. Mortimer RK & Johnston JR (1986) Genealogy of principal strains of the yeast genetic stock center. Genetics 113: 35–43
  70. Sambrook J, Fritsch EF & Maniatis T (1989) Molecular Cloning: A Laboratory Manual Argentine J (ed) Cold Spring Harbor Laboratory Press
  71. 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. Molecular Biology of the Cell 14: 810–821
  72. Scherer M, Heimel K, Starke V & Kämper J (2006) The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. The Plant Cell 18: 2388–2401
  73. Sauer U (2006) Metabolic networks in motion: 13C-based flux analysis. Molecular Systems Biology 2: 62
  74. Williams C, Van den Berg M, Geers E & Distel B (2008) Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. Biochemical and Biophysical Research Communications 374: 620–624
  75. Marelli M, Smith JJ, Jung S, Yi E, Nesvizhskii AI, Christmas RH, Saleem RA, Tam YYC, Fagarasanu A, Goodlett DR, Aebersold R, Rachubinski RA & Aitchison JD (2004) Quantitative mass spectrometry reveals a role for the GTPase Rho1p in actin organization on the peroxisome membrane. The Journal of Cell Biology 167: 1099–1112
  76. Marshall PA, Krimkevich YI, Lark RH, Dyer JM, Veenhuis M & Goodman JM (1995) Pmp27 promotes peroxisomal proliferation. The Journal of Cell Biology 129: 345–355
  77. Stark A, Lin MF, Kheradpour P, Pedersen JS, Parts L, Carlson JW, Crosby MA, Rasmussen MD, Roy S, Deoras AN & others (2007) Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450: 219–232
  78. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP & Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470–476
  79. Spröte P, Brakhage AA & Hynes MJ (2009) Contribution of peroxisomes to penicillin biosynthesis in Aspergillus nidulans. Eukaryotic Cell 8: 421–423
  80. Menand B, Marechal-Drouard L, Sakamoto W, Dietrich A & Wintz H (1998) A single gene of chloroplast origin codes for mitochondrial and chloroplastic methionyl--tRNA synthetase in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 95: 11014–11019
  81. Yogev O, Singer E, Shaulian E, Goldberg M, Fox TD & Pines O (2010) Fumarase: a mitochondrial metabolic enzyme and a cytosolic/nuclear component of the DNA damage response. PLoS Biology 8: e1000328
  82. Walton PA, Hill PE & Subramani S (1995) Import of stably folded proteins into peroxisomes. Molecular Biology of the Cell 6: 1253–1263
  83. Wojtas K, Slepecky N, Von Kalm L & Sullivan D (1997) Flight muscle function in Drosophila requires colocalization of glycolytic enzymes. Molecular Biology of the Cell 8: 1665
  84. Magliano P, Flipphi M, Arpat BA, Delessert S & Poirier Y (2011) Contributions of the Peroxisome and β- Oxidation Cycle to Biotin Synthesis in Fungi. Journal of Biological Chemistry 286: 42133–42140
  85. Miura N, Kirino A, Endo S, Morisaka H, Kuroda K, Takagi M & Ueda M (2012) Tracing Putative Trafficking of the Glycolytic Enzyme Enolase via SNARE-Driven Unconventional Secretion. Eukaryotic Cell 11: 1075– 1082
  86. Singh I, Moser AE, Goldfischer S & Moser HW (1984) Lignoceric acid is oxidized in the peroxisome: implications for the Zellweger cerebro-hepato-renal syndrome and adrenoleukodystrophy. Proceedings of the National Academy of Sciences 81: 4203–4207
  87. Stein I, Peleg Y, Even-Ram S & Pines O (1994) The single translation product of the FUM1 gene (fumarase) is processed in mitochondria before being distributed between the cytosol and mitochondria in Saccharomyces cerevisiae. Molecular and Cellular Biology 14: 4770–4778
  88. Minard KI & McAlister-Henn L (1991) Isolation, nucleotide sequence analysis, and disruption of the MDH2 gene from Saccharomyces cerevisiae: evidence for three isozymes of yeast malate dehydrogenase. Molecular and Cellular Biology 11: 370–380
  89. Marshall AN, Montealegre MC, Jiménez-López C, Lorenz MC & Van Hoof A (2013) Alternative Splicing and Subfunctionalization Generates Functional Diversity in Fungal Proteomes. PLoS Genetics 9: e1003376
  90. Moore PA, Sagliocco FA, Wood RM & Brown AJ (1991) Yeast glycolytic mRNAs are differentially regulated. Molecular and Cellular Biology 11: 5330–5337
  91. Morita T, Koike H, Koyama Y, Hagiwara H, Ito E, Fukuoka T, Imura T, Machida M & Kitamoto D (2013b) Genome sequence of the basidiomycetous yeast Pseudozyma antarctica T-34, a producer of the glycolipid biosurfactants mannosylerythritol lipids. Genome Announcements
  92. Spellig T, Bölker M, Lottspeich F, Frank RW & Kahmann R (1994) Pheromones trigger filamentous growth in Ustilago maydis. The EMBO Journal 13: 1620
  93. Müller WH, Van Der Krift TP, Krouwer AJ, Wösten HA, Van Der Voort LH, Smaal EB & Verkleij AJ (1991) Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum. The EMBO Journal 10: 489–495
  94. Vellieux FM, Hajdu J, Verlinde CL, Groendijk H, Read RJ, Greenhough TJ, Campbell JW, Kalk KH, Littlechild JA & Watson HC (1993) Structure of glycosomal glyceraldehyde-3-phosphate dehydrogenase from Trypanosoma brucei determined from Laue data. Proceedings of the National Academy of Sciences 90: 2355–2359
  95. Soundararajan S, Jedd G, Li X, Ramos-Pamploña M, Chua NH & Naqvi NI (2004) Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. The Plant Cell 16: 1564–1574
  96. Voet D, Beck-Sickinger A, Voet JG & Pratt CW (2010) Lehrbuch der Biochemie Wiley VCH Vongsamphanh R, Fortier PK & Ramotar D (2001) Pir1p mediates translocation of the yeast Apn1p endonuclease into the mitochondria to maintain genomic stability. Molecular and Cellular Biology 21: 1647–1655
  97. Sanger F, Nicklen S & Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences 74: 5463–5467
  98. Schulz B, Banuett F, Dahl M, Schlesinger R, Schäfer W, Martin T, Herskowitz I & Kahmann R (1990) The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60: 295–306
  99. McClelland GB, Khanna S, González GF, Eric Butz C & Brooks GA (2003) Peroxisomal membrane monocarboxylate transporters: evidence for a redox shuttle system? Biochemical and Biophysical Research Communications 304: 130–135
  100. Steinberg G & Schuster M (2011) The dynamic fungal cell. Fungal Biology Reviews 25: 14–37
  101. Managadze D, Würtz C, Wiese S, Meyer HE, Niehaus G, Erdmann R, Warscheid B & Rottensteiner H (2010) A proteomic approach towards the identification of the matrix protein content of the two types of microbodies in Neurospora crassa. Proteomics 10: 3222–3234
  102. Meinecke M, Cizmowski C, Schliebs W, Krüger V, Beck S, Wagner R & Erdmann R (2010) The peroxisomal importomer constitutes a large and highly dynamic pore. Nature Cell Biology 12: 273–277
  103. Rucktäschel R, Girzalsky W & Erdmann R (2011) Protein import machineries of peroxisomes. Biochimica et Biophysica Acta 1808: 892–900
  104. Zhang H, Wang L, Deroles S, Bennett R & Davies K (2006) New insight into the structures and formation of anthocyanic vacuolar inclusions in flower petals. BMC Plant Biology 6: 29


* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten