Peroxisomal catalase deficiency modulates yeast lifespan depending on growth conditions

Aging

Volumn 5, Issue 1, 2013, Pages 67-83

  Kawalek, Adam ^a,b   Lefevre, Sophie ^a,b   Veenhuis, Marten ^a,b   Van der Klei, Ida ^a,b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

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

Author keywords

Aging; Catalase; Chronological lifespan; Cytochrome c peroxidase; Hansenula polymorpha; Peroxisome

Indexed keywords

EID: 84874966979     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100519     Document Type: Article

References (56)

1. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956; 11:298-300.
2. Beckman KB and Ames BN. The free radical theory of aging matures. Physiol Rev. 1998; 78:547-581.
3. Antelmann H and Helmann JD. Thiol-based redox switches and gene regulation. Antioxid Redox Signal. 2011; 14:1049-1063.
4. Janssen-Heininger YMW, Mossman BT, Heintz NH, Forman HJ, Kalyanaraman B, Finkel T, Stamler JS, Rhee SG and van der Vliet A. Redox-based regulation of signal transduction: Principles, pitfalls, and promises. Free Radic Biol Med. 2008; 45:1-17.
5. Ray PD, Huang B-W and Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 2011; 24:981-990.
6. Sohal RS and Orr WC. The redox stress hypothesis of aging. Free Radic Biol Med. 2012; 52:539-555.
7. Balaban RS, Nemoto S and Finkel T. Mitochondria, oxidants, and aging. Cell. 2005; 120:483-495.
8. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet. 2005; 39:359-407.
9. Pan Y. Mitochondria, reactive oxygen species, and chronological aging: A message from yeast. Exp Geront. 2011; 46:847-852.
10. Antonenkov VD, Grunau S, Ohlmeier S and Hiltunen JK. Peroxisomes are oxidative organelles. Antioxid Redox Signal. 2010; 13:525-537.
11. Fransen M, Nordgren M, Wang B and Apanasets O. Role of peroxisomes in ROS/RNS-metabolism: Implications for human disease. Biochim Biophys Acta. 2011; 1822:1363-1373.
12. Giordano CR and Terlecky SR. Peroxisomes, cell senescence, and rates of aging. Biochim Biophys Acta. 2012; 1822:1358-1362.
13. Jungwirth H, Ring J, Mayer T, Schauer A, Büttner S, Eisenberg T, Carmona-Gutierrez D, Kuchler K and Madeo F. Loss of peroxisome function triggers necrosis. FEBS letters. 2008; 582:2882-2886.
14. Goldberg AA, Richard VR, Kyryakov P, Bourque SD, Beach A, Burstein MT, Glebov A, Koupaki O, Boukh-Viner T, Gregg C, Juneau M, English AM, Thomas DY, et al. Chemical genetic screen identifies lithocholic acid as an anti-aging compound that extends yeast chronological life span in a TOR-independent manner, by modulating housekeeping longevity assurance processes. Aging. 2010; 2:393-414.
15. Legakis JE, Koepke JI, Jedeszko C, Barlaskar F, Terlecky LJ, Edwards HJ, Walton PA and Terlecky SR. Peroxisome senescence in human fibroblasts. Mol Biol Cell. 2002; 13:4243-4255.
16. Koepke JI, Nakrieko KA, Wood CS, Boucher KK, Terlecky LJ, Walton PA and Terlecky SR. Restoration of peroxisomal catalase import in a model of human cellular aging. Traffic. 2007; 8:1590- 1600.
17. Koepke JI, Wood CS, Terlecky LJ, Walton PA and Terlecky SR. Progeric effects of catalase inactivation in human cells. Toxicol Appl Pharmacol. 2008; 232:99-108.
18. Ivashchenko O, Van Veldhoven PP, Brees C, Ho Y-S, Terlecky SR and Fransen M. Intraperoxisomal redox balance in mammalian cells: oxidative stress and interorganellar cross-talk. Mol Biol Cell. 2011; 22:1440-1451.
19. Kaeberlein M. Lessons on longevity from budding yeast. Nature. 2010; 464:513-519.
20. Cohen G, Rapatz W and Ruis H. Sequence of the Saccharomyces cerevisiae CATI gene and amino acid sequence of catalase A derived from it. Eur J Biochem. 1988; 176:159-163.
21. Lushchak VI and Gospodaryov DV. Catalases protect cellular proteins from oxidative modification in Saccharomyces cerevisiae. Cell Biol Int. 2005; 29:187-192.
22. Petriv OI and Rachubinski RA. Lack of peroxisomal catalase causes a progeric phenotype in Caenorhabditis elegans. J Biol Chem. 2004; 279:19996-20001.
23. Mesquita A, Weinberger M, Silva A, Sampaio-Marques B, Almeida B, Leào C, Costa V, Rodrigues F, Burhans WC and Ludovico P. Caloric restriction or catalase inactivation extends yeast chronological lifespan by inducing H2O2 and superoxide dismutase activity. PNAS. 2010; 107:15123-15128.
24. Dijken JP, Veenhuis M, Vermeulen CA and Harder W. Cytochemical localization of catalase activity in methanol-grown Hansenula polymorpha. Arch Microbiol. 1975; 105:261-267.
25. Keizer I, Roggenkamp R, Harder W and Veenhuis M. Location of catalase in crystalline peroxisomes of methanol-grown Hansenula polymorpha. FEMS Microbiol Lett. 1992; 72:7-11.
26. Aminova LR, Kyslikova E, Volfova O and Trotsenko YA. Characterization of catalase-negative mutants of methylotrophic yeast Hansenula polymorpha. Folia Microbiol (Praha). 1991; 36:158-163.
27. Kapahi P, Boulton ME and Kirkwood TB. Positive correlation between mammalian life span and cellular resistance to stress. Free Radic Biol Med. 1999; 26:495-500.
28. Larsen PL. Aging and resistance to oxidative damage in Caenorhabditis elegans. PNAS. 1993; 90:8905-8909.
29. Sharma P, Agrawal V and Roy N. Mitochondria-mediated hormetic response in life span extension of calorie-restricted Saccharomyces cerevisiae. AGE. 2011; 33:143-154.
30. Turton HE, Dawes IW and Grant CM. Saccharomyces cerevisiae exhibits a yAP-1-mediated adaptive response to malondialdehyde. J Bacteriol. 1997; 179:1096-1101.
31. Ouyang X, Tran QT, Goodwin S, Wible RS, Sutter CH and Sutter TR. Yap1 activation by H2O2 or thiol-reactive chemicals elicits distinct adaptive gene responses. Free Radic Biol Med. 2011; 50:1-13.
32. Yano T, Takigami E, Yurimoto H and Sakai Y. Yap1-regulated glutathione redox system curtails accumulation of formaldehyde and reactive oxygen species in methanol metabolism of Pichia pastoris. Eukaryot Cell. 2009; 8:540-549.
33. Toda T, Shimanuki M and Yanagida M. Fission yeast genes that confer resistance to staurosporine encode an AP-1-like transcription factor and a protein kinase related to the mammalian ERK1/MAP2 and budding yeast FUS3 and KSS1 kinases. Genes Dev. 1991; 5:60-73.
34. Fernandes L, Rodrigues-Pousada C and Struhl K. Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol Cell Biol. 1997; 17:6982-6993.
35. Nguyen Ba AN, Pogoutse A, Provart N and Moses AM. NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics. 2009; 10:202.
36. la Cour T, Kiemer L, Molgaard A, Gupta R, Skriver K and Brunak S. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel. 2004; 17:527-536.
37. Kumar S, Lefevre SD, Veenhuis M and van der Klei IJ. Extension of yeast chronological lifespan by methylamine. PloS ONE. 2012; 7:e48982.
38. Leontieva OV and Blagosklonny MV. Yeast-like chronological senescence in mammalian cells: phenomenon, mechanism and pharmacological suppression. Aging. 2011; 3:1078-1091.
39. Murakami C, Delaney JR, Chou A, Carr D, Schleit J, Sutphin GL, An EH, Castanza AS, Fletcher M, Goswami S, Higgins S, Holmberg M, Hui J, et al. pH neutralization protects against reduction in replicative lifespan following chronological aging in yeast. Cell Cycle. 2012; 11:3087-3096.
40. Komduur J, Leão A, Monastyrska I, Veenhuis M and Kiel J. Old yellow enzyme confers resistance of Hansenula polymorpha towards allyl alcohol. Curr Genet. 2002; 41:401-406.
41. Abdulrehman D, Monteiro PT, Teixeira MC, Mira NP, Lourenço AB, dos Santos SC, Cabrito TR, Francisco AP, Madeira SC, Aires RS, Oliveira AL, Sá-Correia I and Freitas AT. YEASTRACT: providing a programmatic access to curated transcriptional regulatory associations in Saccharomyces cerevisiae through a web services interface. Nucl Acids Res. 2011; 39:D136-D140.
42. Nguyen DT, Alarco AM and Raymond M. Multiple Yap1pbinding sites mediate induction of the yeast major facilitator FLR1 gene in response to drugs, oxidants, and alkylating agents. J Biol Chem. 2001; 276:1138-1145.
43. He XJ and Fassler JS. Identification of novel Yap1p and Skn7p binding sites involved in the oxidative stress response of Saccharomyces cerevisiae. Mol Microbiol. 2005; 58:1454-1467.
44. Dijken LP, Otto R and Harder W. Growth of Hansenula polymorpha in a methanol-limited chemostat. Arch Microbiol. 1976; 111:137-144.
45. Faber KN, Haima P, Harder W, Veenhuis M and Ab G. Highlyefficient electrotransformation of the yeast Hansenula polymorpha. Curr Genet. 1994; 25:305-310.
46. Waterham HR, Titorenko VI, Haima P, Cregg JM, Harder W and Veenhuis M. The Hansenula polymorpha PER1 gene is essential for peroxisome biogenesis and encodes a peroxisomal matrix protein with both carboxy- and amino-terminal targeting signals. J Cell Biol. 1994; 127:737-749.
47. Klei IJ, Harder W and Veenhuis M. Methanol metabolism in a peroxisome-deficient mutant of Hansenula polymorpha: a physiological study. Arch Microbiol. 1991; 156:15-23.
48. Lück H. (1963). Catalase. (New York: Academic Press).
49. Culotta VC, Klomp LWJ, Strain J, Casareno RLB, Krems B and Gitlin JD. The copper chaperone for superoxide dismutase. J Biol Chem. 1997; 272:23469-23472.
50. Flohe L and Otting F. Superoxide dismutase assays. Methods Enzymol. 1984; 105:93-104.
51. Verduyn C, Giuseppin MLF, Scheffers WA and van Dijken JP. Hydrogen peroxide metabolism in yeasts. Appl Environ Microbiol. 1988; 54 2086-2090.
52. Baerends RJ, Faber KN, Kram AM, Kiel JA, van der Klei IJ and Veenhuis M. A stretch of positively charged amino acids at the N terminus of Hansenula polymorpha Pex3p is involved in incorporation of the protein into the peroxisomal membrane. J Biol Chem. 2000; 275:9986-9995
53. Sudbery PE, Gleeson MA, Veale RA, Ledeboer AM and Zoetmulder MC Hansenula polymorpha as a novel yeast system for the expression of heterologous genes. Biochem Soc Trans. 1988; 16:1081-1083.
54. Nagotu S, Saraya R, Otzen M, Veenhuis M and van der Klei IJ. Peroxisome proliferation in Hansenula polymorpha requires Dnm1p which mediates fission but not de novo formation. Biochim Biophys Acta. 2008; 1783:760-769.
55. Nagotu S, Krikken AM, Otzen M, Kiel JAKW, Veenhuis M and Van Der Klei IJ. Peroxisome fission in Hansenula polymorpha requires Mdv1 and Fis1, two proteins also involved in mitochondrial fission. Traffic. 2008; 9:1471-1484.
56. Saraya R, Krikken AM, Veenhuis M and van der Klei IJ. Peroxisome reintroduction in Hansenula polymorpha requires Pex25 and Rho1. J Cell Biol. 2011; 193:885-900.