Running on empty: Does mitochondrial DNA mutation limit replicative lifespan in yeast?: Mutations that increase the division rate of cells lacking mitochondrial DNA also extend replicative lifespan in Saccharomyces cerevisiae

BioEssays

Volumn 33, Issue 10, 2011, Pages 742-748

  Dunn, Cory D ^a  

^a KOÇ UNIVERSITY   (Turkey)

Author keywords

Longevity; MtDNA; Petite; Ribosome; Yeast

Indexed keywords

CYCLOHEXIMIDE; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

BIOGENESIS; DELETION MUTANT; DNA REPLICATION; GENE DELETION; LIFESPAN; LONGEVITY; MITOCHONDRIAL GENOME; MUTATION; NONHUMAN; REVIEW; RIBOSOME; SACCHAROMYCES CEREVISIAE; SENESCENCE; YEAST; YEAST CELL;

CELL DIVISION; CELL PROLIFERATION; DNA DAMAGE; DNA, MITOCHONDRIAL; GENOME, FUNGAL; GENOMIC INSTABILITY; MITOCHONDRIA; MUTATION; PHENOTYPE; REACTIVE OXYGEN SPECIES; RIBOSOMAL PROTEINS; RIBOSOMES; SACCHAROMYCES CEREVISIAE; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; SIRTUIN 2;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 80052841754     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201100050     Document Type: Review

References (89)

1. Mair W, Dillin A. 2008. Aging and survival: the genetics of life span extension by dietary restriction. Annu Rev Biochem 77: 727-54.
2. Colman RJ, Anderson RM, Johnson SC, Kastman EK, et al. 2009. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325: 201-4.
3. Kukat A, Trifunovic A. 2009. Somatic mtDNA mutations and aging-facts and fancies. Exp Gerontol 44: 101-5.
4. Kujoth GC, Hiona A, Pugh TD, Someya S, et al. 2005. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309: 481-4.
5. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, et al. 2004. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429: 417-23.
6. Edgar D, Shabalina I, Camara Y, Wredenberg A, et al. 2009. Random point mutations with major effects on protein-coding genes are the driving force behind premature aging in mtDNA mutator mice. Cell Metab 10: 131-8.
7. Edgar D, Trifunovic A. 2009. The mtDNA mutator mouse: dissecting mitochondrial involvement in aging. Aging (Albany NY) 1: 1028-32.
8. Vermulst M, Bielas JH, Kujoth GC, Ladiges WC, et al. 2007. Mitochondrial point mutations do not limit the natural lifespan of mice. Nat Genet 39: 540-3.
9. Vermulst M, Wanagat J, Kujoth GC, Bielas JH, et al. 2008. DNA deletions and clonal mutations drive premature aging in mitochondrial mutator mice. Nat Genet 40: 392-4.
10. Greaves LC, Beadle NE, Taylor GA, Commane D, et al. 2009. Quantification of mitochondrial DNA mutation load. Aging Cell 8: 566-72.
11. Kraytsberg Y, Simon DK, Turnbull DM, Khrapko K. 2009. Do mtDNA deletions drive premature aging in mtDNA mutator mice? Aging Cell 8: 502-6.
12. Khrapko K, Kraytsberg Y, de Grey AD, Vijg J, et al. 2006. Does premature aging of the mtDNA mutator mouse prove that mtDNA mutations are involved in natural aging? Aging Cell 5: 279-82.
13. Steinkraus KA, Kaeberlein M, Kennedy BK. 2008. Replicative aging in yeast: the means to the end. Annu Rev Cell Dev Biol 24: 29-54.
14. Chen XJ, Clark-Walker GD. 2000. The petite mutation in yeasts: 50 years on. Int Rev Cytol 194: 197-238.
15. Mounolou JC, Lacroute F. 2005. Mitochondrial DNA: an advance in eukaryotic cell biology in the 1960s. Biol Cell 97: 743-8.
16. Veatch JR, McMurray MA, Nelson ZW, Gottschling DE. 2009. Mitochondrial dysfunction leads to nuclear genome instability via an iron-sulfur cluster defect. Cell 137: 1247-58.
17. Schatz G, Haslbrunner E, Tuppy H. 1964. Deoxyribonucleic acid associated with yeast mitochondria. Biochem Biophys Res Commun 15: 127-32.
18. Corneo G, Moore C, Sanadi DR, Grossman LI, et al. 1966. Mitochondrial DNA in yeast and some mammalian species. Science 151: 687-9.
19. Moustacchi E, Williamson DH. 1966. Physiological variations in satellite components of yeast DNA detected by density gradient centrifugation. Biochem Biophys Res Commun 23: 56-61.
20. Mounolou JC, Jakob H, Slonimski PP. 1966. Mitochondrial DNA from yeast "petite" mutants: specific changes in buoyant density corresponding to different cytoplasmic mutations. Biochem Biophys Res Commun 24: 218-24.
21. Tewari KK, Votsch W, Mahler HR, Mackler B. 1966. Biochemical correlates of respiratory deficiency. VI. Mitochondrial DNA. J Mol Biol 20: 453-81.
22. Rabinowitz M, Swift H. 1970. Mitochondrial nucleic acids and their relation to the biogenesis of mitochondria. Physiol Rev 50: 376-427.
23. Mortimer RK, Johnston JR. 1959. Life span of individual yeast cells. Nature 183: 1751-2.
24. McMurray MA, Gottschling DE. 2003. An age-induced switch to a hyper-recombinational state. Science 301: 1908-11.
25. Kispal G, Sipos K, Lange H, Fekete Z, et al. 2005. Biogenesis of cytosolic ribosomes requires the essential iron-sulphur protein Rli1p and mitochondria. EMBO J 24: 589-98.
26. Schleyer M, Schmidt B, Neupert W. 1982. Requirement of a membrane potential for the posttranslational transfer of proteins into mitochondria. Eur J Biochem 125: 109-16.
27. Giraud MF, Velours J. 1997. The absence of the mitochondrial ATP synthase delta subunit promotes a slow growth phenotype of rho- yeast cells by a lack of assembly of the catalytic sector F1. Eur J Biochem 245: 813-8.
28. Buchet K, Godinot C. 1998. Functional F1-ATPase essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted rho degrees cells. J Biol Chem 273: 22983-9.
29. Schnaufer A, Clark-Walker GD, Steinberg AG, Stuart K. 2005. The F1-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. EMBO J 24: 4029-40.
30. Francis BR, White KH, Thorsness PE. 2007. Mutations in the Atp1p and Atp3p subunits of yeast ATP synthase differentially affect respiration and fermentation in Saccharomyces cerevisiae . J Bioenerg Biomembr 39: 127-44.
31. Dunn CD, Jensen RE. 2003. Suppression of a defect in mitochondrial protein import identifies cytosolic proteins required for viability of yeast cells lacking mitochondrial DNA. Genetics 165: 35-45.
32. Kerscher O, Sepuri NB, Jensen RE. 2000. Tim18p is a new component of the Tim54p-Tim22p translocon in the mitochondrial inner membrane. Mol Biol Cell 11: 103-16.
33. Senapin S, Chen XJ, Clark-Walker GD. 2003. Transcription of TIM9, a new factor required for the petite-positive phenotype of Saccharomyces cerevisiae, is defective in spt7 mutants. Curr Genet 44: 202-10.
34. Dunn CD, Lee MS, Spencer FA, Jensen RE. 2006. A genomewide screen for petite-negative yeast strains yields a new subunit of the i-AAA protease complex. Mol Biol Cell 17: 213-26.
35. Dunn CD, Tamura Y, Sesaki H, Jensen RE. 2008. Mgr3p and Mgr1p are adaptors for the mitochondrial i-AAA protease complex. Mol Biol Cell 19: 5387-97.
36. Thorsness PE, White KH, Fox TD. 1993. Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae . Mol Cell Biol 13: 5418-26.
37. Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, et al. 2000. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J 19: 2444-51.
38. Kennedy BK, Steffen KK, Kaeberlein M. 2007. Ruminations on dietary restriction and aging. Cell Mol Life Sci 64: 1323-8.
39. Wang X, Zuo X, Kucejova B, Chen X. 2008. Reduced cytosolic protein synthesis suppresses mitochondrial degeneration. Nature 10: 1090-7.
40. Fabrizio P, Pletcher SD, Minois N, Vaupel JW, et al. 2004. Chronological aging-independent replicative life span regulation by Msn2/Msn4 and Sod2 in Saccharomyces cerevisiae . FEBS Lett 557: 136-42.
41. Kaeberlein M, Powers RW, third, Steffen KK, Westman EA, et al. 2005. Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310: 1193-6.
42. Lin SJ, Defossez PA, Guarente L. 2000. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae . Science 289: 2126-8.
43. Steffen KK, MacKay VL, Kerr EO, Tsuchiya M, et al. 2008. Yeast life span extension by depletion of 60s ribosomal subunits is mediated by Gcn4. Cell 133: 292-302.
44. Curran SP, Ruvkun G. 2007. Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet 3: e56.
45. Hansen M, Taubert S, Crawford D, Libina N, et al. 2007. Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans . Aging Cell 6: 95-110.
46. Harrison DE, Strong R, Sharp ZD, Nelson JF, et al. 2009. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460: 392-5.
47. Kapahi P, Zid BM, Harper T, Koslover D, et al. 2004. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol 14: 885-90.
48. Pan KZ, Palter JE, Rogers AN, Olsen A, et al. 2007. Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans . Aging Cell 6: 111-9.
49. Vellai T, Takacs-Vellai K, Zhang Y, Kovacs AL, et al. 2003. Genetics: influence of TOR kinase on lifespan in C. elegans . Nature 426: 620.
50. Maleszka R, Clark-Walker GD. 1989. A petite positive strain of Kluyveromyces lactis has a 300kb deletion in the rDNA cluster. Curr Genet 16: 429-32.
51. Zhang X, Moye-Rowley WS. 2001. Saccharomyces cerevisiae multidrug resistance gene expression inversely correlates with the status of the F(0) component of the mitochondrial ATPase. J Biol Chem 276: 47844-52.
52. Zinzalla V, Stracka D, Oppliger W, Hall MN. 2011. Activation of mTORC2 by association with the ribosome. Cell 144: 757-68.
53. Valenzuela L, Aranda C, Gonzalez A. 2001. TOR modulates GCN4-dependent expression of genes turned on by nitrogen limitation. J Bacteriol 183: 2331-4.
54. Cherkasova VA, Hinnebusch AG. 2003. Translational control by TOR and TAP42 through dephosphorylation of eIF2alpha kinase GCN2. Genes Dev 17: 859-72.
55. Natarajan K, Meyer MR, Jackson BM, Slade D, et al. 2001. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol Cell Biol 21: 4347-68.
56. Kaeberlein M, Hu D, Kerr EO, Tsuchiya M, et al. 2005. Increased life span due to calorie restriction in respiratory-deficient yeast. PLoS Genet 1: e69.
57. Kirchman PA, Kim S, Lai CY, Jazwinski SM. 1999. Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae . Genetics 152: 179-90.
58. Kaeberlein M, Kirkland KT, Fields S, Kennedy BK. 2005. Genes determining yeast replicative life span in a long-lived genetic background. Mech Ageing Dev 126: 491-504.
59. Kaeberlein M, Steffen KK, Hu D, Dang N, et al. 2006. Comment on "HST2 mediates SIR2-independent life-span extension by calorie restriction". Science 312: 1312; author reply.
60. Brachmann CB, Davies A, Cost GJ, Caputo E, et al. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-32.
61. Copeland JM, Cho J, Lo T, Jr., Hur JH, et al. 2009. Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain. Curr Biol 19: 1591-8.
62. Dillin A, Hsu AL, Arantes-Oliveira N, Lehrer-Graiwer J, et al. 2002. Rates of behavior and aging specified by mitochondrial function during development. Science 298: 2398-401.
63. Lee SS, Lee RY, Fraser AG, Kamath RS, et al. 2003. A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat Genet 33: 40-8.
64. Feng J, Bussiere F, Hekimi S. 2001. Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans . Dev Cell 1: 633-44.
65. Liu X, Jiang N, Hughes B, Bigras E, et al. 2005. Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice. Genes Dev 19: 2424-34.
66. Rea SL, Ventura N, Johnson TE. 2007. Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans . PLoS Biol 5: e259.
67. Durieux J, Wolff S, Dillin A. 2011. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144: 79-91.
68. Luce K, Osiewacz HD. 2009. Increasing organismal healthspan by enhancing mitochondrial protein quality control. Nat Cell Biol 11: 852-8.
69. Lee SJ, Hwang AB, Kenyon C. 2010. Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity. Curr Biol 20: 2131-6.
70. Laun P, Pichova A, Madeo F, Fuchs J, et al. 2001. Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol Microbiol 39: 1166-73.
71. Aguilaniu H, Gustafsson L, Rigoulet M, Nystrom T. 2003. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299: 1751-3.
72. Chen XJ, Butow RA. 2005. The organization and inheritance of the mitochondrial genome. Nat Rev Genet 6: 815-25.
73. Chen XJ, Wang X, Kaufman BA, Butow RA. 2005. Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 307: 714-7.
74. Chen XJ, Wang X, Butow RA. 2007. Yeast aconitase binds and provides metabolically coupled protection to mitochondrial DNA. Proc Natl Acad Sci USA 104: 13738-43.
75. Cabiscol E, Piulats E, Echave P, Herrero E, et al. 2000. Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae . J Biol Chem 275: 27393-8.
76. Gardner PR, Raineri I, Epstein LB, White CW. 1995. Superoxide radical and iron modulate aconitase activity in mammalian cells. J Biol Chem 270: 13399-405.
77. Klinger H, Rinnerthaler M, Lam YT, Laun P, et al. 2010. Quantitation of (a)symmetric inheritance of functional and of oxidatively damaged mitochondrial aconitase in the cell division of old yeast mother cells. Exp Gerontol 45: 533-42.
78. Perez VI, Bokov A, Van Remmen H, Mele J, et al. 2009. Is the oxidative stress theory of aging dead? Biochim Biophys Acta 1790: 1005-14.
79. Dimitrov LN, Brem RB, Kruglyak L, Gottschling DE. 2009. Polymorphisms in multiple genes contribute to the spontaneous mitochondrial genome instability of Saccharomyces cerevisiae S288C strains. Genetics 183: 365-83.
80. Van Goethem G, Dermaut B, Lofgren A, Martin JJ, et al. 2001. Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat Genet 28: 211-2.
81. Naviaux RK, Nguyen KV. 2004. POLG mutations associated with Alpers' syndrome and mitochondrial DNA depletion. Ann Neurol 55: 706-12.
82. Chen XJ. 2002. Induction of an unregulated channel by mutations in adenine nucleotide translocase suggests an explanation for human ophthalmoplegia. Hum Mol Genet 11: 1835-43.
83. Lindstrom DL, Leverich CK, Henderson KA, Gottschling DE. 2011. Replicative age induces mitotic recombination in the ribosomal RNA gene cluster of Saccharomyces cerevisiae . PLoS Genet 7: e1002015.
84. Hess DC, Myers CL, Huttenhower C, Hibbs MA, et al. 2009. Computationally driven, quantitative experiments discover genes required for mitochondrial biogenesis. PLoS Genet 5: e1000407.
85. Scheckhuber CQ, Erjavec N, Tinazli A, Hamann A, et al. 2007. Reducing mitochondrial fission results in increased life span and fitness of two fungal ageing models. Nat Cell Biol 9: 99-105.
86. Bleazard W, McCaffery JM, King EJ, Bale S, et al. 1999. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1: 298-304.
87. Sesaki H, Jensen RE. 1999. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J Cell Biol 147: 699-706.
88. Chen H, Vermulst M, Wang YE, Chomyn A, et al. 2010. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141: 280-9.
89. Paddison PJ, Silva JM, Conklin DS, Schlabach M, et al. 2004. A resource for large-scale RNA-interference-based screens in mammals. Nature 428: 427-31.