Abstract
The essential role of the peroxisome in oxidizing fatty acids, maintaining reactive oxygen species homeostasis and replenishing tricarboxylic acid cycle intermediates is well known. Recent findings have broadened a spectrum of biomolecules that are synthesized and metabolized in peroxisomes. Emergent evidence supports the view that, by releasing various biomolecules known to modulate essential cellular processes, the peroxisome not only operates as an organizing platform for several developmental and differentiation programs but is also actively involved in defining the replicative and chronological age of a eukaryotic cell. The scope of this chapter is to summarize the evidence that the peroxisome defines yeast longevity by operating as a system controller that: (1) modulates levels of non-esterified fatty acids and diacylglycerol; (2) replenishes tricarboxylic acid cycle intermediates destined for mitochondria; and (3) contributes to the synthesis of polyamines. We critically evaluate molecular mechanisms underlying the essential role of peroxisomally produced and metabolized biomolecules in governing cellular aging in yeast.
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- ATG:
-
Autophagy-related genes
- CR:
-
Caloric restriction
- DAG:
-
Diacylglycerol
- ER:
-
Endoplasmic reticulum
- FA:
-
Fatty acids
- ODC:
-
Ornithine decarboxylase
- PTS1:
-
Peroxisomal targeting signal type 1
- PTS2:
-
Peroxisomal targeting signal type 2
- RNS:
-
Reactive nitrogen species
- ROS:
-
Reactive oxygen species
- RTG:
-
Retrograde signaling pathway
- TAG:
-
Triacylglycerols
References
Antonenkov VD, Grunau S, Ohlmeier S, Hiltunen JK (2010) Peroxisomes are oxidative organelles. Antioxid Redox Signal 13:525–537
Babujee L, Wurtz V, Ma C, Lueder F, Soni P, van Dorsselaer A, Reumann S (2010) The proteome map of spinach leaf peroxisomes indicates partial compartmentalization of phylloquinone (vitamin K1) biosynthesis in plant peroxisomes. J Exp Bot 61:1441–1453
Bartoszewska M, Kiel JA, Bovenberg RA, Veenhuis M, van der Klei IJ (2011) Autophagy deficiency promotes beta-lactam production in Penicillium chrysogenum. Appl Environ Microbiol 77:1413–1422
Beach A, Burstein MT, Richard VR, Leonov A, Levy S, Titorenko VI (2012) Integration of peroxisomes into an endomembrane system that governs cellular aging. Front Physiol 3:283
Binns D, Januszewski T, Chen Y, Hill J, Markin VS, Zhao Y, Gilpin C, Chapman KD, Anderson RG, Goodman JM (2006) An intimate collaboration between peroxisomes and lipid bodies. J Cell Biol 173:719–731
Borghouts C, Benguria A, Wawryn J, Jazwinski SM (2004) Rtg2 protein links metabolism and genome stability in yeast longevity. Genetics 166:765–777
Corpas FJ, de la Colina C, Sanchez-Rasero F, del Río LA (1997) A role for leaf peroxisomes in the catabolism of purines. J Plant Physiol 151:246–250
Corpas FJ, Palma JM, Sandalio LM, Valderrama R, Barroso JB, del Río LA (2008) Peroxisomal xanthine oxidoreductase: characterization of the enzyme from pea (Pisum sativum L.) leaves. J Plant Physiol 165:1319–1330
D’Autréaux B, Toledano MB (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8:813–824
del Río LA, Fernández VM, Rupérez FL, Sandalio LM, Palma JM (1989) NADH induces the generation of superoxide radicals in leaf peroxisomes. Plant Physiol 89:728–731
del Río LA, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jiménez A, López-Huertas E, Hernández JA (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiol 116:1195–1200
Dixit E, Boulant S, Zhang Y, Lee AS, Odendall C, Shum B, Hacohen N, Chen ZJ, Whelan SP, Fransen M, Nibert ML, Superti-Furga G, Kagan JC (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141:668–681
Eisenberg T, Knauer H, Schauer A, Büttner S, Ruckenstuhl C, Carmona-Gutierrez D, Ring J, Schroeder S, Magnes C, Antonacci L, Fussi H, Deszcz L, Hartl R, Schraml E, Criollo A, Megalou E, Weiskopf D, Laun P, Heeren G, Breitenbach M, Grubeck-Loebenstein B, Herker E, Fahrenkrog B, Fröhlich KU, Sinner F, Tavernarakis N, Minois N, Kroemer G, Madeo F (2009) Induction of autophagy by spermidine promotes longevity. Nat Cell Biol 11:1305–1314
Epstein CB, Waddle JA, Hale W, Davé V, Thornton J, Macatee TL, Garner HR, Butow RA (2001) Genome-wide responses to mitochondrial dysfunction. Mol Biol Cell 12:297–308
Fabrizio P, Gattazzo C, Battistella L, Wei M, Cheng C, McGrew K, Longo VD (2005) Sir2 blocks extreme life-span extension. Cell 123:655–667
Galluzzi L, Vicencio JM, Kepp O, Tasdemir E, Maiuri MC, Kroemer G (2008) To die or not to die: that is the autophagic question. Curr Mol Med 8:78–91
Goldberg AA, Bourque SD, Kyryakov P, Gregg C, Boukh-Viner T, Beach A, Burstein MT, Machkalyan G, Richard V, Rampersad S, Cyr D, Milijevic S, Titorenko VI (2009a) Effect of calorie restriction on the metabolic history of chronologically aging yeast. Exp Gerontol 44:555–571
Goldberg AA, Bourque SD, Kyryakov P, Boukh-Viner T, Gregg C, Beach A, Burstein MT, Machkalyan G, Richard V, Rampersad S, Titorenko VI (2009b) A novel function of lipid droplets in regulating longevity. Biochem Soc Trans 37:1050–1055
Goodman JM (2008) The gregarious lipid droplet. J Biol Chem 283:28005–28009
He C, Klionsky DJ (2009) Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43:67–93
Hiltunen JK, Mursula AM, Rottensteiner H, Wierenga RK, Kastaniotis AJ, Gurvitz A (2003) The biochemistry of peroxisomal β-oxidation in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 27:35–64
Imazaki A, Tanaka A, Harimoto Y, Yamamoto M, Akimitsu K, Park P, Tsuge T (2010) Contribution of peroxisomes to secondary metabolism and pathogenicity in the fungal plant pathogen Alternaria alternata. Eukaryot Cell 9:682–694
Islinger M, Grille S, Fahimi DH, Schrader M (2012) The peroxisome: an update on mysteries. Histochem Cell Biol 137:547–574
Ivashchenko O, Van Veldhoven PP, Brees C, Ho YS, Terlecky SR, Fransen M (2011) Intraperoxisomal redox balance in mammalian cells: oxidative stress and interorganellar cross-talk. Mol Biol Cell 22:1440–1451
Jazwinski SM (2005a) The retrograde response links metabolism with stress responses, chromatin-dependent gene activation, and genome stability in yeast aging. Gene 354:22–27
Jazwinski SM (2005b) Rtg2 protein: at the nexus of yeast longevity and aging. FEMS Yeast Res 5:1253–1259
Jazwinski SM (2012) The retrograde response and other pathways of interorganelle communication in yeast replicative aging. Subcell Biochem 57:79–100
Jazwinski SM, Kriete A (2012) The yeast retrograde response as a model of intracellular signaling of mitochondrial dysfunction. Front Physiol 3:139
Joo HJ, Kim KY, Yim YH, Jin YX, Kim H, Kim MY, Paik YK (2010) Contribution of the peroxisomal acox gene to the dynamic balance of daumone production in Caenorhabditis elegans. J Biol Chem 285:29319–29325
Kienow L, Schneider K, Bartsch M, Stuible HP, Weng H, Miersch O, Wasternack C, Kombrink E (2008) Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana. J Exp Bot 59:403–419
Kirchman PA, Kim S, Lai CY, Jazwinski SM (1999) Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae. Genetics 152:179–190
Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y, Sandoval IV, Sibirny A, Subramani S, Thumm M, Veenhuis M, Ohsumi Y (2003) A unified nomenclature for yeast autophagy‐related genes. Dev Cell 5:539–545
Kroemer G, Levine B (2008) Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 9:1004–1010
Kundu M, Thompson CB (2008) Autophagy: basic principles and relevance to disease. Annu Rev Pathol 3:427–455
Lai CY, Jaruga E, Borghouts C, Jazwinski SM (2002) A mutation in the ATP2 gene abrogates the age asymmetry between mother and daughter cells of the yeast Saccharomyces cerevisiae. Genetics 162:73–87
Legakis JE, Koepke JI, Jedeszko C, Barlaskar F, Terlecky LJ, Edwards HJ, Walton PA, Terlecky SR (2002) Peroxisome senescence in human fibroblasts. Mol Biol Cell 13:4243–4255
Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132:27–42
Liao XS, Small WC, Srere PA, Butow RA (1991) Intramitochondrial functions regulate nonmitochondrial citrate synthase (CIT2) expression in Saccharomyces cerevisiae. Mol Cell Biol 11:38–46
Lin SJ, Sinclair D (2008) Molecular mechanisms of aging: insights from budding yeast. In: Guarente LP, Partridge L, Wallace DC (eds) Molecular biology of aging. Spring Harbor Laboratory Press, Cold Spring Harbor
Liu Z, Butow RA (2006) Mitochondrial retrograde signaling. Annu Rev Genet 40:159–185
Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, Thompson CB (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120:237–248
Ma C, Agrawal G, Subramani S (2011) Peroxisome assembly: matrix and membrane protein biogenesis. J Cell Biol 193:7–16
Mair W, Dillin A (2008) Aging and survival: the genetics of life span extension by dietary restriction. Annu Rev Biochem 77:727–754
Mast FD, Li J, Virk MK, Hughes SC, Simmonds AJ, Rachubinski RA (2011) A Drosophila model for the Zellweger spectrum of peroxisome biogenesis disorders. Dis Model Mech 4:659–672
Mateos RM, León AM, Sandalio LM, Gómez M, del Río LA, Palma JM (2003) Peroxisomes from pepper fruits (Capsicum annuum L.): purification, characterisation and antioxidant activity. J Plant Physiol 160:1507–1516
Meijer WH, Gidijala L, Fekken S, Kiel JA, van den Berg MA, Lascaris R, Bovenberg RA, van der Klei IJ (2010) Peroxisomes are required for efficient penicillin biosynthesis in Penicillium chrysogenum. Appl Environ Microbiol 76:5702–5709
Minois N, Carmona-Gutierrez D, Madeo F (2011) Polyamines in aging and disease. Aging 3:716–732
Mitsuya S, Kuwahara J, Ozaki K, Saeki E, Fujiwara T, Takabe T (2011) Isolation and characterization of a novel peroxisomal choline monooxygenase in barley. Planta 234:1215–1226
Mizushima N, Klionsky DJ (2007) Protein turnover via autophagy: implications for metabolism. Annu Rev Nutr 27:19–40
Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self‐digestion. Nature 451:1069–1075
Morselli E, Galluzzi L, Kepp O, Criollo A, Maiuri MC, Tavernarakis N, Madeo F, Kroemer G (2009) Autophagy mediates pharmacological lifespan extension by spermidine and resveratrol. Aging 1:961–970
Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y (2009) Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10:458–467
Nishikawa M, Hagishita T, Yurimoto H, Kato N, Sakai Y, Hatanaka T (2000) Primary structure and expression of peroxisomal acetylspermidine oxidase in the methylotrophic yeast Candida boidinii. FEBS Lett 476:150–154
Olofsson SO, Boström P, Andersson L, Rutberg M, Perman J, Borén J (2009) Lipid droplets as dynamic organelles connecting storage and efflux of lipids. Biochim Biophys Acta 1791: 448–458
Ono Y, Kim DW, Watanabe K, Sasaki A, Niitsu M, Berberich T, Kusano T, Takahashi Y (2012) Constitutively and highly expressed Oryza sativa polyamine oxidases localize in peroxisomes and catalyze polyamine back conversion. Amino Acids 42:867–876
Parikh VS, Morgan MM, Scott R, Clements LS, Butow RA (1987) The mitochondrial genotype can influence nuclear gene expression in yeast. Science 235:576–580
Rucktäschel R, Girzalsky W, Erdmann R (2011) Protein import machineries of peroxisomes. Biochim Biophys Acta 1808:892–900
Sandalio LM, Fernández VM, Rupérez FL, del Río LA (1988) Superoxide free radicals are produced in glyoxysomes. Plant Physiol 87:1–4
Schlüter A, Real-Chicharro A, Gabaldón T, Sánchez-Jiménez F, Pujol A (2010) PeroxisomeDB 2.0: an integrative view of the global peroxisomal metabolome. Nucleic Acids Res 38: D800–D805
Seo JG, Lai CY, Miceli MV, Jazwinski SM (2007) A novel role of peroxin PEX6, suppression of aging defects in mitochondria. Aging Cell 6:405–413
Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458:1131–1135
Spiegel CN, Batista-Pereira LG, Bretas JA, Eiras AE, Hooper AM, Peixoto AA, Soares MJ (2011) Pheromone gland development and pheromone production in Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). J Med Entomol 48:489–495
Spröte P, Brakhage AA, Hynes MJ (2009) Contribution of peroxisomes to penicillin biosynthesis in Aspergillus nidulans. Eukaryot Cell 8:421–423
Tanabe Y, Maruyama J, Yamaoka S, Yahagi D, Matsuo I, Tsutsumi N, Kitamoto K (2011) Peroxisomes are involved in biotin biosynthesis in Aspergillus and Arabidopsis. J Biol Chem 286:30455–30461
Terlecky SR, Koepke JI, Walton PA (2006) Peroxisomes and aging. Biochim Biophys Acta 1763:1749–1754
Thabet I, Guirimand G, Courdavault V, Papon N, Godet S, Dutilleul C, Bouzid S, Giglioli-Guivarc’h N, Clastre M, Simkin AJ (2011) The subcellular localization of periwinkle farnesyl diphosphate synthase provides insight into the role of peroxisome in isoprenoid biosynthesis. J Plant Physiol 168:2110–2116
Thiele C, Spandl J (2008) Cell biology of lipid droplets. Curr Opin Cell Biol 20:378–385
Thoms S, Grønborg S, Gärtner J (2009) Organelle interplay in peroxisomal disorders. Trends Mol Med 15:293–302
Titorenko VI, Rachubinski RA (2004) The peroxisome: orchestrating important developmental decisions from inside the cell. J Cell Biol 164:641–645
Titorenko VI, Terlecky SR (2011) Peroxisome metabolism and cellular aging. Traffic 12:252–259
Traven A, Wong JM, Xu D, Sopta M, Ingles CJ (2001) Interorganellar communication. Altered nuclear gene expression profiles in a yeast mitochondrial DNA mutant. J Biol Chem 276: 4020–4027
van der Klei IJ, Yurimoto H, Sakai Y, Veenhuis M (2006) The significance of peroxisomes in methanol metabolism in methylotrophic yeast. Biochim Biophys Acta 1763:1453–1462
Vujcic S, Liang P, Diegelman P, Kramer DL, Porter CW (2003) Genomic identification and biochemical characterization of the mammalian polyamine oxidase involved in polyamine backconversion. Biochem J 370:19–28
Walther TC, Farese RV Jr (2009) The life of lipid droplets. Biochim Biophys Acta 1791:459–466
Wanders RJ, Waterham HR (2006) Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem 75:295–332
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Beach, A., Titorenko, V.I. (2013). Essential Roles of Peroxisomally Produced and Metabolized Biomolecules in Regulating Yeast Longevity. In: del Río, L. (eds) Peroxisomes and their Key Role in Cellular Signaling and Metabolism. Subcellular Biochemistry, vol 69. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6889-5_9
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