Respiratory and TCA cycle activities affect S. cerevisiae lifespan, response to caloric restriction and mtDNA stability

  • Erich B. Tahara
  • Kizzy Cezário
  • Nadja C. Souza-Pinto
  • Mario H. Barros
  • Alicia J. Kowaltowski
Article

Abstract

We studied the importance of respiratory fitness in S. cerevisiae lifespan, response to caloric restriction (CR) and mtDNA stability. Mutants harboring mtDNA instability and electron transport defects do not respond to CR, while tricarboxylic acid cycle mutants presented extended lifespans due to CR. Interestingly, mtDNA is unstable in cells lacking dihydrolipoyl dehydrogenase under CR conditions, and cells lacking aconitase under standard conditions (both enzymes are components of the TCA and mitochondrial nucleoid). Altogether, our data indicate that respiratory integrity is required for lifespan extension by CR and that mtDNA stability is regulated by nucleoid proteins in a glucose-sensitive manner.

Keywords

Aging Calorie restriction Mitochondria Respiration Yeast Krebs cycle 

References

  1. Baker KP, Schatz G (1991) Nature 349:205–208CrossRefGoogle Scholar
  2. Barea F, Bonatto D (2009) Mech Ageing Dev 130:444–460CrossRefGoogle Scholar
  3. Barros MH, Bandy B, Tahara EB, Kowaltowski AJ (2004) J Biol Chem 279:49883–49888CrossRefGoogle Scholar
  4. Barros MH, da Cunha FM, Oliveira GA, Tahara EB, Kowaltowski AJ (2010) Mech Ageing Dev 131:494–502CrossRefGoogle Scholar
  5. Bitterman KJ, Medvedik O, Sinclair DA (2003) Microbiol Mol Biol Rev 67:376–399CrossRefGoogle Scholar
  6. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD (1998) Yeast 14:115–132CrossRefGoogle Scholar
  7. Brewer LR, Friddle R, Noy A, Baldwin E, Martin SS, Corzett M, Balhorn R, Baskin RJ (2003) Biophys J 85:2519–2524CrossRefGoogle Scholar
  8. Cerqueira FM, Laurindo FR, Kowaltowski AJ (2011) PLoS One 31:e18433CrossRefGoogle Scholar
  9. Chapman KB, Solomon SD, Boeke JD (1992) Gene 118:131–136CrossRefGoogle Scholar
  10. Chen XJ, Wang X, Kaufman BA, Butow RA (2005) Science 307:714–717CrossRefGoogle Scholar
  11. DeRisi JL, Iyer VR, Brown PO (1997) Science 278:680–686CrossRefGoogle Scholar
  12. Dickinson JR, Roy DJ, Dawes IW (1986) Mol Gen Genet 204:103–107CrossRefGoogle Scholar
  13. Diffley JF, Stillman B (1991) Proc Natl Acad Sci USA 88:7864–7868CrossRefGoogle Scholar
  14. Diffley JF, Stillman B (1992) J Biol Chem 267:3368–3374Google Scholar
  15. Fabrizio P, Longo VD (2003) Aging Cell 2:73–81CrossRefGoogle Scholar
  16. Fabrizio P, Li L, Longo VD (2005) Mech Ageing Dev 126:11–16CrossRefGoogle Scholar
  17. Falkenberg M, Larsson NG, Gustafsson CM (2007) Annu Rev Biochem 76:679–699CrossRefGoogle Scholar
  18. Ferguson LR, von Borstel RC (1992) Mutat Res 265:103–148Google Scholar
  19. Fernández E, Moreno F, Rodicio R (1992) Eur J Biochem 204:983–990CrossRefGoogle Scholar
  20. Fontana L, Partridge L, Longo VD (2010) Science 328:321–326CrossRefGoogle Scholar
  21. Foury F, Tzagoloff A (1976) Eur J Biochem 68:113–119CrossRefGoogle Scholar
  22. Foury F, Roganti T, Lecrenier N, Purnelle B (1998) FEBS Lett 440:325–331CrossRefGoogle Scholar
  23. Frick O, Wittmann C (2005) Microb Cell Fact 4:30CrossRefGoogle Scholar
  24. Gancedo JM (1998) Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62:334–361Google Scholar
  25. Gangloff SP, Marguet D, Lauquin GJ (1990) Mol Cell Biol 10:3551–3561Google Scholar
  26. 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 (2009) Exp Gerontol 44:555–571CrossRefGoogle Scholar
  27. Gombert AK, Moreira dos Santos M, Christensen B, Nielsen J (2001) J Bacteriol 183:1441–1451CrossRefGoogle Scholar
  28. Jazwinski SM (2002a) Exp Gerontol 37:1141–1146CrossRefGoogle Scholar
  29. Jazwinski SM (2002b) Annu Rev Microbiol 56:769–792CrossRefGoogle Scholar
  30. Jiang JC, Jaruga E, Repnevskaya MV, Jazwinski SM (2000) FASEB J 14:2135–2147Google Scholar
  31. Kaeberlein M, Hu D, Kerr EO, Tsuchiya M, Westman EA, Dang N, Fields S, Kennedy BK (2005) PloS Genet 1:e69CrossRefGoogle Scholar
  32. Kao LR, Megraw TL, Chae CB (1993) Proc Natl Acad Sci USA 90:5598–5602CrossRefGoogle Scholar
  33. Katic M, Kennedy AR, Leykin I, Norris A, McGettrick A, Gesta S, Russell SJ, Bluher M, Maratos-Flier E, Kahn CR (2007) Aging Cell 6:827–839CrossRefGoogle Scholar
  34. Kenyon C (2001) Cell 105:165–168CrossRefGoogle Scholar
  35. Klein CJ, Olsson L, Nielsen J (1998) Microbiology 144:13–24CrossRefGoogle Scholar
  36. Kucej M, Kucejova B, Subramanian R, Chen XJ, Butow RA (2008) J Cell Sci 121:1861–1868CrossRefGoogle Scholar
  37. Lin SJ, Guarente L (2006) PLoS Genet 2:e33CrossRefGoogle Scholar
  38. Lin SJ, Defossez PA, Guarente L (2000) Science 289:2126–2128CrossRefGoogle Scholar
  39. Linnane AW, Haslam JM, Lukins HB, Nagley P (1972) Annu Rev Microbiol 26:163–198CrossRefGoogle Scholar
  40. Linnane AW, Marzuki S, Ozawa T, Tanaka M (1989) Lancet 25:642–645CrossRefGoogle Scholar
  41. Lipinski KA, Kaniak-Golik A, Golik P (2010) Biochim Biophys Acta 1797:1086–1098CrossRefGoogle Scholar
  42. López-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R (2006) Proc Natl Acad Sci USA 103:1768–1773CrossRefGoogle Scholar
  43. MacLean M, Harris N, Piper PW (2001) Yeast 18:499–509CrossRefGoogle Scholar
  44. McAlister-Henn L, Thompson LM (1987) J Bacteriol 169:5157–5166Google Scholar
  45. Miyakawa I, Aoi H, Sando N, Kuroiwa T (1984) J Cell Sci 66:21–38Google Scholar
  46. Müller I, Zimmermann M, Becker D, Flömer M (1980) Mech Ageing Dev 12:47–52CrossRefGoogle Scholar
  47. Newman SM, Zelenaya-Troitskaya O, Perlman PS, Butow RA (1996) Nucleic Acids Res 24:386–393CrossRefGoogle Scholar
  48. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO (2005) Science 310:314–317CrossRefGoogle Scholar
  49. Oliveira GA, Tahara EB, Gombert AK, Barros MH, Kowaltowski AJ (2008) J Bioenerg Biomembr 40:381–388CrossRefGoogle Scholar
  50. Piper PW (2006) Yeast 23:215–226CrossRefGoogle Scholar
  51. Repetto B, Tzagoloff A (1989) Mol Cell Biol 9:2695–2705Google Scholar
  52. Reverter-Branchat G, Cabiscol E, Tamarit J, Ros J (2004) J Biol Chem 279:31983–31989CrossRefGoogle Scholar
  53. Rickwood D, Chambers JA, Barat M (1981) Exp Cell Res 133:1–13CrossRefGoogle Scholar
  54. Sadler I, Suda K, Schatz G, Kaudewitz F, Haid A (1984) EMBO J 3:2137–2143Google Scholar
  55. Saltzgaber-Muller J, Kunapuli SP, Douglas MG (1983) J Biol Chem 258:11465–11470Google Scholar
  56. Samokhvalov V, Ignatov V, Kondrashova M (2004) Biochimie 86:39–46CrossRefGoogle Scholar
  57. Schaffrath R, Breunig KD (2000) Fungal Genet Biol 30:173–190CrossRefGoogle Scholar
  58. Sidhu A, Beattie DS (1983) J Biol Chem 258:10649–10656Google Scholar
  59. Sinclair D, Mills K, Guarente L (1998) Annu Rev Microbiol 52:533–560CrossRefGoogle Scholar
  60. Slonimski PP, Tzagoloff A (1976) Eur J Biochem 61:27–41CrossRefGoogle Scholar
  61. Smith DL Jr, McClure JM, Matecic M, Smith JS (2007) Aging Cell 6:649–662CrossRefGoogle Scholar
  62. Stuart RA, Gruhler A, van der Klei I, Guiard B, Koll H, Neupert W (1994) Eur J Biochem 220:9–18CrossRefGoogle Scholar
  63. Tahara EB, Barros MH, Oliveira GA, Netto LE, Kowaltowski AJ (2007) FASEB J 21:274–283CrossRefGoogle Scholar
  64. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, Bohlooly-Y M, Gidlöf S, Oldfors A, Wibom R, Törnell J, Jacobs HT, Larsson NG (2004) Nature 429:417–423CrossRefGoogle Scholar
  65. Tzagoloff A, Dieckmann CL (1990) Microbiol Rev 54:211–225Google Scholar
  66. Tzagoloff A, Akai A, Needleman RB (1975) J Biol Chem 250:8236–8242Google Scholar
  67. Zelenaya-Troitskaya O, Perlman PS, Butow RA (1995) EMBO J 14:3268–3276Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Erich B. Tahara
    • 1
  • Kizzy Cezário
    • 2
  • Nadja C. Souza-Pinto
    • 1
  • Mario H. Barros
    • 2
  • Alicia J. Kowaltowski
    • 1
  1. 1.Departamento de Bioquímica, Instituto de QuímicaUniversidade de São PauloSão PauloBrazil
  2. 2.Departamento de Microbiologia, Instituto de Ciências BiomédicasUniversidade de São PauloSão PauloBrazil

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