Preserving organelle vitality: Peroxisomal quality control mechanisms in yeast

FEMS Yeast Research

Volumn 9, Issue 6, 2009, Pages 808-820

  Aksam, Eda Bener ^a   De Vries, Bart ^a   Van Der Klei, Ida J ^a,b   Kiel, Jan A K W ^a,b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

Author keywords

Ageing; Pexophagy; Proteasome; Reactive oxygen species; Yeast

Indexed keywords

2 HYDROXYACID; ACYL COENZYME A OXIDASE; ALCOHOL OXIDASE; CATALASE; CELL PROTEIN; CELL RECEPTOR; CHAPERONE; DEXTRO AMINO ACID OXIDASE; MEMBRANE PROTEIN; OXIDOREDUCTASE; PEROXIN; PEROXIREDOXIN; PIPECOLIC ACID OXIDASE; POLYAMINE OXIDASE; PROTEASOME; PROTEIN PEX20; PROTEIN PEX5; PROTEINASE; REACTIVE OXYGEN METABOLITE; SARCOSINE OXIDASE; SULFITE OXIDASE; TRANSLOCON; UBIQUITIN; UNCLASSIFIED DRUG; URATE OXIDASE; XANTHINE OXIDASE;

AEROBIC METABOLISM; AUTOPHAGY; CELL FUNCTION; CELL MATURATION; CELL MEMBRANE; CELL METABOLISM; CYTOSOL; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; QUALITY CONTROL; SHORT SURVEY; YEAST;

DNA, FUNGAL; FUNGAL PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; ORGANELLES; SEQUENCE ANALYSIS, DNA; YEASTS;

EID: 68849107586     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2009.00534.x     Document Type: Short Survey

References (84)

1. Adames N, Blundell K, Ashby MN & Boone C (1995) Role of yeast insulin-degrading enzyme homologs in propheromone processing and bud site selection. Science 270: 464-467.
2. Aksam EB, Koek A, Kiel JAKW, Jourdan S, Veenhuis M & van der Klei IJ (2007) A peroxisomal lon protease and peroxisome degradation by autophagy play key roles in vitality of Hansenula polymorpha cells. Autophagy 3: 96-105.
3. Bener Aksam E, Jungwirth H, Kohlwein SD, Ring J, Madeo F, Veenhuis M & van der Klei IJ (2008) Absence of the peroxiredoxin Pmp20 causes peroxisomal protein leakage and necrotic cell death. Free Radical Bio Med 45: 1115-1124.
4. Anelli T & Sitia R (2008) Protein quality control in the early secretory pathway. EMBO J 27: 315-327.
5. Authier F, Bergeron JJ, Ou WJ, Rachubinski RA, Posner BI & Walton PA (1995) Degradation of the cleaved leader peptide of thiolase by a peroxisomal proteinase. P Natl Acad Sci USA 92: 3859-3863.
6. Bellu AR, Salomons FA, Kiel JAKW, Veenhuis M& van der Klei IJ (2002) Removal of Pex3p is an important initial stage in selective peroxisome degradation in Hansenula polymorpha. J Biol Chem 277: 42875-42880.
7. Bergamini E, Cavallini G, Donati A & Gori Z (2004) The role of macroautophagy in the ageing process, anti-ageing intervention and age-associated diseases. Int J Biochem Cell B 36: 2392-2404.
8. Bota DA & Davies KJ (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol 4: 674-680.
9. Boveris A, Oshino N & Chance B (1972) The cellular production of hydrogen peroxide. Biochem J 128: 617-630.
10. Brocard CB, Jedeszko C, Song HC, Terlecky SR &Walton PA (2003) Protein structure and import into the peroxisomal matrix. Traffic 4: 74-82.
11. Charette MF, Henderson GW & Markovitz A (1981) ATP hydrolysis-dependent protease activity of the lon (capR) protein of Escherichia coli K-12. P Natl Acad Sci USA 78: 4728-4732.
12. Ciechanover A (2005) Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Bio 6: 79-87.
13. Cu´ellar-Cruz M, Briones-Martin-del-Campo M, Ca&tild;nas-Villamar I, Montalvo-Arredondo J, Riego-Ruiz L, Casta&tild;no I & De Las Pe&tild;nas A (2008) High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot Cell 7: 814-825.
14. Dammai V & Subramani S (2001) The human peroxisomal targeting signal receptor, Pex5p, is translocated into the peroxisomal matrix and recycled to the cytosol. Cell 105: 187-196.
15. de Vries B, Todde V, Stevens P, Salomons F, van der Klei IJ & Veenhuis M (2006) Pex14p is not required for N-starvation induced microautophagy and in catalytic amounts for macropexophagy in Hansenula polymorpha. Autophagy 2: 183-188.
16. Distefano S, Palma JM, McCarthy II & del Rio LA (1999) Proteolytic cleavage of plant proteins by peroxisomal endoproteases from senescent pea leaves. Planta 209: 308-313.
17. Distel B, Erdmann R, Gould SJ et al. (1996) A unified nomenclature for peroxisome biogenesis factors. J Cell Biol 135: 1-3.
18. Dodt G & Gould SJ (2001) 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 135: 1763-1774.
19. Erdmann R & Schliebs W (2005) Peroxisomal matrix protein import: the transient pore model. Nat Rev Mol Cell Bio 6: 738-742.
20. Faber KN, van Dijk R, Keizer-Gunnink I, Koek A, van der Klei IJ & Veenhuis M (2002) Import of assembled PTS1 proteins into peroxisomes of the yeast Hansenula polymorpha: yes and no!. Biochim Biophys Acta 1591: 157-162.
21. Farcasanu IC, Hirata D, Tsuchiya E, Mizuta K & Miyakawa T (1999) Involvement of thioredoxin peroxidase type II (Ahp1p) of Saccharomyces cerevisiae in Mn21 homeostasis. Biosci Biotech Bioch 63: 1871-1881.
22. Farr´e JC & Subramani S (2004) Peroxisome turnover by micropexophagy: an autophagy-related process. Trends Cell Biol 14: 515-523.
23. Farr´e JC, Vidal J & Subramani S (2007) A cytoplasm to vacuole targeting pathway in P. pastoris. Autophagy 3: 230-234.
24. Friguet B, Bulteau AL & Petropoulos I (2008) Mitochondrial protein quality control: implications in ageing. Biotechnol J 3: 757-764.
25. Fujiki Y, Matsuzono Y, Matsuzaki T & Fransen M (2006) Import of peroxisomal membrane proteins: the interplay of Pex3pand Pex19p-mediated interactions. Biochim Biophys Acta 1763: 1639-1646.
26. Gilca M, Stoian I, Atanasiu V & Virgolici B (2007) The oxidative hypothesis of senescence. J Postgrad Med 53: 207-213.
27. G´oth L, Rass P & P´ay A (2004) Catalase enzyme mutations and their association with diseases. Mol Diagn 8: 141-149.
28. Grou CP, Carvalho AF, Pinto MP, Wiese S, Piechura H, Meyer HE, Warscheid B, S´a-Miranda C & Azevedo JE (2008) Members of the E2D (UbcH5) family mediate the ubiquitination of the conserved cysteine of Pex5p, the peroxisomal import receptor. J Biol Chem 283: 14190-14197.
29. Hansen H & Roggenkamp R (1989) Functional complementation of catalase-defective peroxisomes in a methylotrophic yeast by import of the catalase A from Saccharomyces cerevisiae. Eur J Biochem 184: 173-179.
30. Hettema EH, Ruigrok CC, Koerkamp MG, van den Berg M, Tabak HF, Distel B & Braakman I (1998) The cytosolic DnaJlike protein djp1p is involved specifically in peroxisomal protein import. J Cell Biol 142: 421-434.
31. Hettema EH, Girzalsky W, van Den Berg M, Erdmann R & Distel B (2000) Saccharomyces cerevisiae pex3p and pex19p are required for proper localization and stability of peroxisomal membrane proteins. EMBO J 19: 223-233.
32. Horiguchi H, Yurimoto H, Goh T, Nakagawa T, Kato N & Sakai Y (2001a) Peroxisomal catalase in the methylotrophic yeast Candida boidinii: transport efficiency and metabolic significance. J Bacteriol 183: 6372-6383.
33. Horiguchi H, Yurimoto H, Kato N & Sakai Y (2001b) Antioxidant system within yeast peroxisome. Biochemical and physiological characterization of CbPmp20 in the methylotrophic yeast Candida boidinii. J Biol Chem 276: 14279-14288.
34. Immenschuh S & Baumgart-Vogt E (2005) Peroxiredoxins, oxidative stress, and cell proliferation. Antioxid Redox Sign 7: 768-777.
35. Izawa S, Kuroki N & Inoue Y (2004) Nuclear thioredoxin peroxidase Dot5 in Saccharomyces cerevisiae: roles in oxidative stress response and disruption of telomeric silencing. Appl Microbiol Biot 64: 120-124.
36. Jungwirth H, Ring J, Mayer T, Schauer A, B̈uttner S, Eisenberg T, Carmona-Gutierrez D, Kuchler K & Madeo F (2008) Loss of peroxisome function triggers necrosis. FEBS Lett 582: 2882-2886.
37. Karnik SK & Trelease RN (2007) Arabidopsis peroxin 16 trafficks through the ER and an intermediate compartment to preexisting peroxisomes via overlapping molecular targeting signals. J Exp Bot 58: 1677-1693.
38. Kerssen D, Hambruch E, Klaas W, Platta HW, de Kruijff B, Erdmann R, Kunau WH & Schliebs W (2006) Membrane association of the cycling peroxisome import receptor Pex5p. J Biol Chem 281: 27003-27015.
39. Kiel JAKW, Komduur JA, van der Klei IJ & Veenhuis M (2003) Macropexophagy in Hansenula polymorpha: facts and views. FEBS Lett 549: 1-6.
40. Kiel JAKW, Emmrich K, Meyer HE & Kunau WH (2005a) Ubiquitination of the peroxisomal targeting signal type 1 receptor, Pex5p, suggests the presence of a quality control mechanism during peroxisomal matrix protein import. J Biol Chem 280: 1921-1930.
41. Kiel JAKW, Otzen M, Veenhuis M & van der Klei IJ (2005b) Obstruction of polyubiquitination affects PTS1 peroxisomal matrix protein import. Biochim Biophys Acta 1745: 176-186.
42. Kiel JAKW, Veenhuis M & van der Klei IJ (2006) PEX genes in fungal genomes: common, rare or redundant. Traffic 7: 1291-1303.
43. Kikuchi M, Hatano N, Yokota S, Shimozawa N, Imanaka T & Taniguchi H (2004) Proteomic analysis of rat liver peroxisome: presence of peroxisome-specific isozyme of Lon protease. J Biol Chem 279: 421-428.
44. Klionsky DJ, Cregg JM, Dunn WA Jr et al. (2003) A unified nomenclature for yeast autophagy-related genes. Dev Cell 5: 539-545.
45. Klionsky DJ, Cuervo AM, Dunn WA Jr, Levine B, van der Klei I & Seglen PO (2007) How shall I eat thee? Autophagy 3: 413-416.
46. Kurochkin IV, Mizuno Y, Konagaya A, Sakaki Y, Scḧonbach C & Okazaki Y (2007) Novel peroxisomal protease Tysnd1 processes PTS1- and PTS2-containing enzymes involved in beta-oxidation of fatty acids. EMBO J 26: 835-845.
47. 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.
48. L´eon S & Subramani S (2007) A conserved cysteine residue of Pichia pastoris Pex20p is essential for its recycling from the peroxisome to the cytosol. J Biol Chem 282: 7424-7430.
49. L´eon S, Zhang L, McDonald WH, Yates J III, Cregg JM & Subramani S (2006) Dynamics of the peroxisomal import cycle of PpPex20p: ubiquitin-dependent localization and regulation. J Cell Biol 172: 67-78.
50. Ma C, Haslbeck M, Babujee L, Jahn O & Reumann S (2006) Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiol 141: 47-60.
51. Malhotra JD & Kaufman RJ (2007) Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Sign 9: 2277-2293.
52. Martinez-Vicente M, Sovak G & Cuervo AM (2005) Protein degradation and aging. Exp Gerontol 40: 622-633.
53. Moldovan L & Moldovan NI (2004) Oxygen free radicals and redox biology of organelles. Histochem Cell Biol 122: 395-412.
54. Morita M, Kurochkin IV, Motojima K, Goto S, Takano T, Okamura S, Sato R, Yokota S & Imanaka T (2000) Insulindegrading enzyme exists inside of rat liver peroxisomes and degrades oxidized proteins. Cell Struct Funct 25: 309-315.
55. Munhoz DC & Netto LE (2004) Cytosolic thioredoxin peroxidase I and II are important defenses of yeast against organic hydroperoxide insult: catalases and peroxiredoxins cooperate in the decomposition of H2O2 by yeast. J Biol Chem 279: 35219-35227.
56. Nakatsukasa K & Brodsky JL (2008) The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic 9: 861-870.
57. Neutzner A, Youle RJ & Karbowski M (2007) Outer mitochondrial membrane protein degradation by the proteasome. Novart Fdn Symp 287: 4-14.
58. Ngo JK & Davies KJ (2007) Importance of the lon protease in mitochondrial maintenance and the significance of declining lon in aging. Ann NY Acad Sci 1119: 78-87.
59. Nguyen AT & Donaldson RP (2005) Metal catalyzed oxidation induces carbonylation of peroxisomal proteins and loss of enzymatic activities. Arch Biochem Biophys 439: 25-31.
60. Omi S, Nakata R, Okamura-Ikeda K, Konishi H & Taniguchi H (2008) Contribution of peroxisome-specific isoform of lon protease in sorting PTS1 proteins to peroxisomes. J Biochem 143: 649-660.
61. Ozimek P, van Dijk R, Latchev K, Gancedo C, Wang DY, van der Klei IJ & Veenhuis M (2003) Pyruvate carboxylase is an essential protein in the assembly of yeast peroxisomal oligomeric alcohol oxidase. Mol Biol Cell 14: 786-797.
62. Pedrajas JR, Miranda-Vizuete A, Javanmardy N, Gustafsson JA & Spyrou G (2000) Mitochondria of Saccharomyces cerevisiae contain one-conserved cysteine type peroxiredoxin with thioredoxin peroxidase activity. J Biol Chem 275: 16296-16301.
63. Petriv OI & Rachubinski RA (2004) Lack of peroxisomal catalase causes a progeric phenotype in Caenorhabditis elegans. J Biol Chem 279: 19996-20001.
64. Platta HW & Erdmann R (2007) The peroxisomal protein import machinery. FEBS Lett 581: 2811-2819.
65. Platta HW, Girzalsky W & Erdmann R (2004) Ubiquitination of the peroxisomal import receptor Pex5p. Biochem J 384: 37-45.
66. Platta HW, El Magraoui F, Schlee D, Grunau S, Girzalsky W & Erdmann R (2007) Ubiquitination of the peroxisomal import receptor Pex5p is required for its recycling. J Cell Biol 177: 197-204.
67. Sakai Y, Oku M, van der Klei IJ & Kiel JAKW (2006) Pexophagy: autophagic degradation of peroxisomes. Biochim Biophys Acta 1763: 1767-1775.
68. Schrader M & Fahimi HD (2006) Peroxisomes and oxidative stress. Biochim Biophys Acta 1763: 1755-1766.
69. Schrader M & Fahimi HD (2008) The peroxisome: still a mysterious organelle. Histochem Cell Biol 129: 421-440.
70. Scott SV, Hefner-Gravink A, Morano KA, Noda T, Ohsumi Y & Klionsky DJ (1996) Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. P Natl Acad Sci USA 93: 12304-12308.
71. Sheikh FG, Pahan K, Khan M, Barbosa E & Singh I (1998) Abnormality in catalase import into peroxisomes leads to severe neurological disorder. P Natl Acad Sci USA 95: 2961-2966.
72. Starkov AA (2008) The role of mitochondria in reactive oxygen species metabolism and signaling. Ann NY Acad Sci 1147: 37-52.
73. Stewart MQ, Esposito RD, Gowani J & Goodman JM (2001) Alcohol oxidase and dihydroxyacetone synthase, the abundant peroxisomal proteins of methylotrophic yeasts, assemble in different cellular compartments. J Cell Sci 114: 2863-2868.
74. Stewart MQ, van Dijk R, Veenhuis M & Goodman JM (2002) Monomeric alcohol oxidase is preferentially digested by a novel protease from Candida boidinii. Biochim Biophys Acta 1542: 160-172.
75. Terlecky SR, Koepke JI & Walton PA (2006) Peroxisomes and aging. Biochim Biophys Acta 1763: 1749-1754.
76. 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.
77. Titorenko VI, Nicaud JM, Wang H, Chan H & Rachubinski RA (2002) Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. J Cell Biol 156: 481-494.
78. van der Klei IJ & VeenhuisM(1996) Peroxisome biogenesis in the yeast Hansenula polymorpha: a structural and functional analysis. Ann NY Acad Sci 804: 47-59.
79. von Mikecz A (2006) The nuclear ubiquitin-proteasome system. J Cell Sci 119: 1977-1984.
80. Walton PA,Wendland M, Subramani S, Rachubinski RA &Welch WJ (1994) Involvement of 70 kD heat-shock proteins in peroxisomal import. J Cell Biol 125: 1037-1046.
81. Williams C, van den Berg M, Sprenger RR & Distel B (2007) A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p. J Biol Chem 282: 22534-22543.
82. Wimmer B, Lottspeich F, van der Klei I, Veenhuis M & Gietl C (1997) The glyoxysomal and plastid molecular chaperones (70-kDa heat shock protein) of watermelon cotyledons are encoded by a single gene. P Natl Acad Sci USA 94: 13624-13629.
83. Wood CS, Koepke JI, Teng H, Boucher KK, Katz S, Chang P, Terlecky LJ, Papanayotou I, Walton PA &Terlecky SR (2006) Hypocatalasemic fibroblasts accumulate hydrogen peroxide and display age-associated pathologies. Traffic 7: 97-107.
84. Yokota S, Haraguchi CM & Oda T (2008) Induction of peroxisomal Lon protease in rat liver after di-(2-ethylhexyl)phthalate treatment. Histochem Cell Biol 129: 73-83.