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Fungal Peroxisomes Proteomics

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Proteomics of Peroxisomes

Part of the book series: Subcellular Biochemistry ((SCBI,volume 89))

Abstract

Peroxisomes in fungi are involved in a huge number of different metabolic processes. In addition, non-metabolic functions have also been identified. The proteins that are present in a particular peroxisome determine its metabolic function, whether they are the matrix localized enzymes of the different metabolic pathways or the membrane proteins involved in transport of metabolites across the peroxisomal membrane. Other peroxisomal proteins play a role in organelle biogenesis and dynamics, such as fission, transport and inheritance. Hence, obtaining a complete overview of which proteins are present in peroxisomes at a given time or under a given growth condition provides invaluable insights into peroxisome biology. Bottom up approaches are ideal to follow one or a few proteins at a time but they are not able to give a global view of the content of peroxisomes. To gain such information, top down approaches are required and one that has provided valuable insights into peroxisome function is mass spectrometry based organellar proteomics. Here, we discuss the findings of several such studies in yeast and filamentous fungi and outline new insights into peroxisomal function that were gained from these studies.

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Abbreviations

APEX:

Ascorbate peroxidase

DDA:

Data-dependent Acquisition

DIA:

Data-independent Acquisition

ESI:

Electro-spray Ionization

GFP:

Green fluorescent protein

GPF:

Gas Phase Fractionation

ICAT:

Isotope-coded affinity tags

MALDI:

Matrix Assisted Laser Desorption Ionization

MS:

Mass Spectrometry

MS/MS:

Tandem Mass Spectrometry

µLC:

Micro Liquid chromatography

nHPLC:

High performance liquid chromatography

nLC:

Nano Liquid chromatography

PMP:

Peroxisomal membrane protein

PNS:

Post nuclear supernatant

PTS:

Peroxisomal targeting signal

ROS:

Reactive oxygen species

SDS-PAGE:

Sodium dodecyl sulphate polyacrylamide gel electrophoresis

SGD:

Saccharomyces cerevisiae Genome Database

SILAC:

Stable Isotope Labelling by Amino acids in Cell culture

References

  • Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H (2008) A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 7:1389–1396

    Article  CAS  Google Scholar 

  • Alston TA, Mela L, Bright HJ (1977) 3-Nitropropionate, the toxic substance of Indigofera, is a suicide inactivator of succinate dehydrogenase. Proc Natl Acad Sci U S A 74:3767–3771

    Article  CAS  Google Scholar 

  • Bauer S, Morris MT (2017) Glycosome biogenesis in trypanosomes and the de novo dilemma. PLoS Negl Trop Dis 11:e0005333

    Article  Google Scholar 

  • Blobel F, Erdmann R (1996) Identification of a yeast peroxisomal member of the family of AMP-binding proteins. Eur J Biochem 240:468–476

    Article  CAS  Google Scholar 

  • David C, Koch J, Oeljeklaus S, Laernsack A, Melchior S, Wiese S, Schummer A, Erdmann R, Warscheid B, Brocard C (2013) A combined approach of quantitative interaction proteomics and live-cell imaging reveals a regulatory role for ER reticulon homology proteins in peroxisome biogenesis. Mol Cell Proteomics

    Google Scholar 

  • Davis MT, Spahr CS, McGinley MD, Robinson JH, Bures EJ, Beierle J, Mort J, Yu W, Luethy R, Patterson SD (2001) Towards defining the urinary proteome using liquid chromatography-tandem mass spectrometry. II. Limitations of complex mixture analyses. Proteomics 1:108–117

    Article  CAS  Google Scholar 

  • Effelsberg D, Cruz-Zaragoza LD, Schliebs W, Erdmann R (2016) Pex9p is a new yeast peroxisomal import receptor for PTS1-containing proteins. J Cell Sci 129:4057–4066

    CAS  PubMed  Google Scholar 

  • Elgersma Y, van Roermund CW, Wanders RJ, Tabak HF (1995) Peroxisomal and mitochondrial carnitine acetyltransferases of Saccharomyces cerevisiae are encoded by a single gene. EMBO J 14:3472–3479

    Article  CAS  Google Scholar 

  • Flavell RB, Woodward DO (1971) Metabolic role, regulation of synthesis, cellular localization, and genetic control of the glyoxylate cycle enzymes in Neurospora crassa. J Bacteriol 105:200–210

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiwara T, Tanaka K, Mino A, Kikyo M, Takahashi K, Shimizu K, Takai Y (1998) Rho1p-Bni1p-Spa2p interactions: implication in localization of Bni1p at the bud site and regulation of the actin cytoskeleton in Saccharomyces cerevisiae. Mol Biol Cell 9:1221–1233

    Article  CAS  Google Scholar 

  • Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 17:994–999

    Article  CAS  Google Scholar 

  • Hipkin CR, Salem MA, Simpson D, Wainwright SJ (1999) 3-nitropropionic acid oxidase from horseshoe vetch (Hippocrepis comosa): a novel plant enzyme. Biochem J 340(Pt 2):491–495

    Article  CAS  Google Scholar 

  • Hwang J, Espenshade PJ (2016) Proximity-dependent biotin labelling in yeast using the engineered ascorbate peroxidase APEX2. Biochem J 473:2463–2469

    Article  CAS  Google Scholar 

  • Islinger M, Manner A, Volkl A (2018) The craft of peroxisome purification—a technical survey through the decades. Proteomics of peroxisomes: an approach to identify novel functions and regulatory networks of these cellular organelles. Springer, Dordrecht

    Google Scholar 

  • Jedd G, Chua NH (2000) A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2:226–231

    Article  CAS  Google Scholar 

  • Jung S, Marelli M, Rachubinski RA, Goodlett DR, Aitchison JD (2010) Dynamic changes in the subcellular distribution of Gpd1p in response to cell stress. J Biol Chem 285:6739–6749

    Article  CAS  Google Scholar 

  • Kiel JA, van den Berg MA, Fusetti F, Poolman B, Bovenberg RA, Veenhuis M, van der Klei IJ (2009) Matching the proteome to the genome: the microbody of penicillin-producing Penicillium chrysogenum cells. Funct Integr Genomics 9:167–184

    Article  CAS  Google Scholar 

  • Kim DI, Roux KJ (2016) Filling the void: proximity-based labeling of proteins in living cells. Trends Cell Biol 26:804–817

    Article  CAS  Google Scholar 

  • Kindl H (1993) Fatty acid degradation in plant peroxisomes: function and biosynthesis of the enzymes involved. Biochimie 75:225–230

    Article  CAS  Google Scholar 

  • Kionka C, Kunau WH (1985) Inducible beta-oxidation pathway in Neurospora crassa. J Bacteriol 161:153–157

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knoops K, de Boer R, Kram A, van der Klei IJ (2015) Yeast pex1 cells contain peroxisomal ghosts that import matrix proteins upon reintroduction of Pex1. J Cell Biol 211:955–962

    Article  CAS  Google Scholar 

  • Knoops K, Manivannan S, Cepinska MN, Krikken AM, Kram AM, Veenhuis M, van der Klei IJ (2014) Preperoxisomal vesicles can form in the absence of Pex3. J Cell Biol 204:659–668

    Article  CAS  Google Scholar 

  • Kragt A, Voorn-Brouwer T, van den Berg M, Distel B (2005) The Saccharomyces cerevisiae peroxisomal import receptor Pex5p is monoubiquitinated in wild type cells. J Biol Chem 280:7867–7874

    Article  CAS  Google Scholar 

  • Kumar S, Singh R, Williams CP, van der Klei IJ (2016) Stress exposure results in increased peroxisomal levels of yeast Pnc1 and Gpd1, which are imported via a piggy-backing mechanism. Biochim Biophys Acta 1863:148–156

    Article  CAS  Google Scholar 

  • Kunau WH, Buhne S, de la Garza M, Kionka C, Mateblowski M, Schultz-Borchard U, Thieringer R (1988) Comparative enzymology of beta-oxidation. Biochem Soc Trans 16:418–420

    Article  CAS  Google Scholar 

  • Liu F, Ng SK, Lu Y, Low W, Lai J, Jedd G (2008) Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J Cell Biol 180:325–339

    Article  CAS  Google Scholar 

  • Managadze D, Wurtz C, Sichting M, Niehaus G, Veenhuis M, Rottensteiner H (2007) The peroxin PEX14 of Neurospora crassa is essential for the biogenesis of both glyoxysomes and Woronin bodies. Traffic 8:687–701

    Article  CAS  Google Scholar 

  • Managadze D, Wurtz 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

    Article  CAS  Google Scholar 

  • Mano S, Nishimura M (2005) Plant peroxisomes. Vitam Horm 72:111–154

    Article  CAS  Google Scholar 

  • Marelli M, Smith JJ, Jung S, Yi E, Nesvizhskii AI, Christmas RH, Saleem RA, Tam YY, 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. J Cell Biol 167:1099–1112

    Article  CAS  Google Scholar 

  • Martell JD, Deerinck TJ, Sancak Y, Poulos TL, Mootha VK, Sosinsky GE, Ellisman MH, Ting AY (2012) Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat Biotechnol 30:1143–1148

    Article  CAS  Google Scholar 

  • Motley AM, Galvin PC, Ekal L, Nuttall JM, Hettema EH (2015) Reevaluation of the role of Pex1 and dynamin-related proteins in peroxisome membrane biogenesis. J Cell Biol 211:1041–1056

    Article  CAS  Google Scholar 

  • Muller WH, Bovenberg RA, Groothuis MH, Kattevilder F, Smaal EB, Van der Voort LH, Verkleij AJ (1992) Involvement of microbodies in penicillin biosynthesis. Biochim Biophys Acta 1116:210–213

    Article  CAS  Google Scholar 

  • Muller WH, van der Krift TP, Krouwer AJ, Wosten HA, van der Voort LH, Smaal EB, Verkleij AJ (1991) Localization of the pathway of the penicillin biosynthesis in Penicillium chrysogenum. EMBO J 10:489–495

    Article  CAS  Google Scholar 

  • Neufeld C, Filipp FV, Simon B, Neuhaus A, Schuller N, David C, Kooshapur H, Madl T, Erdmann R, Schliebs W, Wilmanns M, Sattler M (2009) Structural basis for competitive interactions of Pex14 with the import receptors Pex5 and Pex19. EMBO J 28:745–754

    Article  CAS  Google Scholar 

  • Nonaka H, Tanaka K, Hirano H, Fujiwara T, Kohno H, Umikawa M, Mino A, Takai Y (1995) A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. EMBO J 14:5931–5938

    Article  CAS  Google Scholar 

  • Nuttall JM, Motley AM, Hettema EH (2014) Deficiency of the exportomer components Pex1, Pex6, and Pex15 causes enhanced pexophagy in Saccharomyces cerevisiae. Autophagy 10:835–845

    Article  CAS  Google Scholar 

  • Oeljeklaus S, Reinartz BS, Wolf J, Wiese S, Tonillo J, Podwojski K, Kuhlmann K, Stephan C, Meyer HE, Schliebs W, Brocard C, Erdmann R, Warscheid B (2012) Identification of core components and transient interactors of the peroxisomal importomer by dual-track stable isotope labeling with amino acids in cell culture analysis. J Proteome Res 11:2567–2580

    Article  CAS  Google Scholar 

  • Peikert CD, Mani J, Morgenstern M, Kaser S, Knapp B, Wenger C, Harsman A, Oeljeklaus S, Schneider A, Warscheid B (2017) Charting organellar importomes by quantitative mass spectrometry. Nat Commun 8:15272

    Article  CAS  Google Scholar 

  • Piechura H, Oeljeklaus S, Warscheid B (2012) SILAC for the study of mammalian cell lines and yeast protein complexes. Methods Mol Biol 893:201–221

    Article  CAS  Google Scholar 

  • Reguenga C, Oliveira ME, Gouveia AM, Sa-Miranda C, Azevedo JE (2001) Characterization of the mammalian peroxisomal import machinery: Pex2p, Pex5p, Pex12p, and Pex14p are subunits of the same protein assembly. J Biol Chem 276:29935–29942

    Article  CAS  Google Scholar 

  • Rhee HW, Zou P, Udeshi ND, Martell JD, Mootha VK, Carr SA, Ting AY (2013) Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 339:1328–1331

    Article  CAS  Google Scholar 

  • Rucktaschel R, Thoms S, Sidorovitch V, Halbach A, Pechlivanis M, Volkmer R, Alexandrov K, Kuhlmann J, Rottensteiner H, Erdmann R (2009) Farnesylation of pex19p is required for its structural integrity and function in peroxisome biogenesis. J Biol Chem 284:20885–20896

    Article  Google Scholar 

  • Saleem RA, Smith JJ, Aitchison JD (2006) Proteomics of the peroxisome. Biochim Biophys Acta 1763:1541–1551

    Article  CAS  Google Scholar 

  • Schäfer H, Nau K, Sickmann A, Erdmann R, Meyer HE (2001) Identification of peroxisomal membrane proteins of Saccharomyces cerevisiae by mass spectrometry. Electrophoresis 22:2955–2968

    Article  Google Scholar 

  • Schliebs W, Wurtz C, Kunau WH, Veenhuis M, Rottensteiner H (2006) A eukaryote without catalase-containing microbodies: neurospora crassa exhibits a unique cellular distribution of its four catalases. Eukaryot Cell 5:1490–1502

    Article  CAS  Google Scholar 

  • Smith JJ, Aitchison JD (2013) Peroxisomes take shape. Nat Rev Mol Cell Biol 14:803–817

    Article  CAS  Google Scholar 

  • Spahr CS, Davis MT, McGinley MD, Robinson JH, Bures EJ, Beierle J, Mort J, Courchesne PL, Chen K, Wahl RC, Yu W, Luethy R, Patterson SD (2001) Towards defining the urinary proteome using liquid chromatography-tandem mass spectrometry. I. Profiling an unfractionated tryptic digest. Proteomics 1:93–107

    Article  CAS  Google Scholar 

  • Steen H, Jebanathirajah JA, Rush J, Morrice N, Kirschner MW (2006) Phosphorylation analysis by mass spectrometry: myths, facts, and the consequences for qualitative and quantitative measurements. Mol Cell Proteomics 5:172–181

    Article  CAS  Google Scholar 

  • Valenciano S, De Lucas JR, Van der Klei I, Veenhuis M, Laborda F (1998) Characterization of Aspergillus nidulans peroxisomes by immunoelectron microscopy. Arch Microbiol 170:370–376

    Article  CAS  Google Scholar 

  • Van den Bosch H, Schutgens RB, Wanders RJ, Tager JM (1992) Biochemistry of peroxisomes. Annu Rev Biochem 61:157–197

    Article  Google Scholar 

  • Van Dijkan JP, Veenhuis M, Harder W (1982) Peroxisomes of methanol-grown yeasts. Ann NY Acad Sci 386:200–216

    Article  Google Scholar 

  • Veiga T, Gombert AK, Landes N, Verhoeven MD, Kiel JA, Krikken AM, Nijland JG, Touw H, Luttik MA, van der Toorn JC, Driessen AJ, Bovenberg RA, van den Berg MA, van der Klei IJ, Pronk JT, Daran JM (2012) Metabolic engineering of beta-oxidation in Penicillium chrysogenum for improved semi-synthetic cephalosporin biosynthesis. Metab Eng 14:437–448

    Article  CAS  Google Scholar 

  • Yamochi W, Tanaka K, Nonaka H, Maeda A, Musha T, Takai Y (1994) Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J Cell Biol 125:1077–1093

    Article  CAS  Google Scholar 

  • Yi EC, Marelli M, Lee H, Purvine SO, Aebersold R, Aitchison JD, Goodlett DR (2002) Approaching complete peroxisome characterization by gas-phase fractionation. Electrophoresis 23:3205–3216

    Article  CAS  Google Scholar 

  • Yifrach E, Chuartzman SG, Dahan N, Maskit S, Zada L, Weill U, Yofe I, Olender T, Schuldiner M, Zalckvar E (2016) Characterization of proteome dynamics during growth in oleate reveals a new peroxisome-targeting receptor. J Cell Sci 129:4067–4075

    CAS  Google Scholar 

  • Zipor G, Haim-Vilmovsky L, Gelin-Licht R, Gadir N, Brocard C, Gerst JE (2009) Localization of mRNAs coding for peroxisomal proteins in the yeast, Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 106:19848–19853

    Article  CAS  Google Scholar 

  • Zwart KB, Veenhuis M, Harder W (1983) Significance of yeast peroxisomes in the metabolism of choline and ethanolamine. Antonie Van Leeuwenhoek 49:369–385

    CAS  PubMed  Google Scholar 

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Acknowledgements

C.W. is supported by a VIDI Grant (723.013.004) from the Netherlands Organization for Scientific Research (NWO).

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Correspondence to Chris Williams .

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Chen, X., Williams, C. (2018). Fungal Peroxisomes Proteomics. In: del Río, L., Schrader, M. (eds) Proteomics of Peroxisomes. Subcellular Biochemistry, vol 89. Springer, Singapore. https://doi.org/10.1007/978-981-13-2233-4_3

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