Mitochondria, maternal inheritance, and asymmetric fitness: Why males die younger

BioEssays

Volumn 35, Issue 2, 2013, Pages 93-99

  Wolff, Jonci N ^a   Gemmell, Neil J ^b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Asymmetry; Drosophila; Evolution; Mitochondria; MtDNA; Oxphos; Selection

Indexed keywords

MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

AGING; ARTICLE; ASYMMETRIC FITNESS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DROSOPHILA; EPIGENETICS; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; EXTRACHROMOSOMAL INHERITANCE; FERTILITY; FITNESS; GENE DISRUPTION; GENE EXPRESSION; GENETIC RISK; GENETIC SELECTION; GENOME; GEOGRAPHICAL VARIATION (SPECIES); HAPLOTYPE; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRION; MOLECULAR GENETICS; NONHUMAN; SEX DIFFERENCE;

AGING; ANIMALS; DNA, MITOCHONDRIAL; DROSOPHILA MELANOGASTER; EPIGENESIS, GENETIC; FEMALE; GENOME, MITOCHONDRIAL; HAPLOTYPES; HUMANS; INHERITANCE PATTERNS; LONGEVITY; MALE; MITOCHONDRIA; MUTATION; REACTIVE OXYGEN SPECIES; SEX CHARACTERISTICS; SEX FACTORS;

EID: 84872395711     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201200141     Document Type: Article

References (93)

1. Gregersen N, Hansen J, Palmfeldt J. 2012. Mitochondrial proteomics - a tool for the study of metabolic disorders. J Inherit Metab Dis 35: 715-26.
2. Sickmann A, Reinders J, Jr., Wagner Y, Joppich C, et al. 2003. The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci USA 100: 13207-12.
3. Mootha VK, Bunkenborg J, Olsen JV, Hjerrild M, et al. 2003. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115: 629-40.
4. Woodson JD, Chory J. 2008. Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9: 383-95.
5. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, et al. 2009. Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-44.
6. Kujoth GC, Bradshaw PC, Haroon S, Prolla TA. 2007. The role of mitochondrial DNA mutations in mammalian aging. PLoS Genet 3: e24.
7. Pichaud N, Ballard JWO, Tanguay RM, Blier PU. 2012. Naturally occurring mitochondrial DNA haplotypes exhibit metabolic differences: insight into functional properties of mitochondria. Evolution 66: 3189-97.
8. Correa CC, Aw WC, Melvin RG, Pichaud N, et al. 2012. Mitochondrial DNA variants influence mitochondrial bioenergetics in Drosophila melanogaster. Mitochondrion 12: 459-64.
9. Lane N. 2011. Mitonuclear match: optimizing fitness and fertility over generations drives ageing within generations. BioEssays 33: 860-9.
10. Wallace DC. 2010. Mitochondrial DNA mutations in disease and aging. Environ Mol Mutagen 51: 440-50.
11. Ellison CK, Burton RS. 2008. Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62: 631-8.
12. Burton RS, Ellison CK, Harrison JS. 2006. The sorry state of F2 hybrids: consequences of rapid mitochondrial DNA evolution in allopatric populations. Am Nat 168: S14-24.
13. Duchen MR. 2000. Mitochondria and calcium: from cell signalling to cell death. J Physiol 529: 57-68.
14. Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, Vercesi AE. 2009. Mitochondria and reactive oxygen species. Free Radic Biol Med 47: 333-43.
15. D'Autreaux B, Toledano MB. 2007. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8: 813-24.
16. Coskun P, Wyrembak J, Schriner SE, Chen HW, et al. 2012. A mitochondrial etiology of Alzheimer and Parkinson disease. Biochim Biophys Acta 1820: 553-64.
17. Chen PL, Chen CF, Chen Y, Guo XE, et al. 2012. Mitochondrial genome instability resulting from SUV3 haploinsufficiency leads to tumorigenesis and shortened lifespan. Oncogene, in press. DOI: 10.1038/onc.2012.120.
18. St John JC, Facucho-Oliveira J, Jiang Y, Kelly R, et al. 2010. Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Hum Reprod Update 16: 488-509.
19. Dey R, Barrientos A, Moraes CT. 2000. Functional constraints of nuclear-mitochondrial DNA interactions in xenomitochondrial rodent cell lines. J Biol Chem 275: 31520-7.
20. Osada N, Akashi H. 2012. Mitochondrial-nuclear interactions and accelerated compensatory evolution: evidence from the primate cytochrome c oxidase complex. Mol Biol Evol 29: 337-46.
21. Ruiz-Pesini E, Lapena AC, Diez-Sanchez C, Perez-Martos A, et al. 2000. Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am J Hum Genet 67: 682-96.
22. Holyoake AJ, McHugh P, Wu M, O'Carroll S, et al. 2001. High incidence of single nucleotide substitutions in the mitochondrial genome is associated with poor semen parameters in men. Int J Androl 24: 175-82.
23. Mitomap. 2011. A Human Mitochondrial Genome Database.
24. Wallace D, Singh G, Lott M, Hodge J, et al. 1988. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science 242: 1427-30.
25. Nakamura M, Yabe I, Sudo A, Hosoki K, et al. 2010. MERRF/MELAS overlap syndrome: a double pathogenic mutation in mitochondrial tRNA genes. J Med Genet 47: 659-64.
26. Wallace DC. 1992. Diseases of the mitochondrial DNA. Annu Rev Biochem 61: 1175-212.
27. Bayat V, Thiffault I, Jaiswal M, Tetreault M, et al. 2012. Mutations in the mitochondrial methionyl-tRNA synthetase cause a neurodegenerative phenotype in flies and a recessive ataxia (ARSAL) in humans. PLoS Biology 10: e1001288.
28. Khusnutdinova E, Gilyazova I, Ruiz-Pesini E, Derbeneva O, et al. 2008. A mitochondrial etiology of neurodegenerative diseases: evidence from Parkinson's disease. Ann N Y Acad Sci 1147: 1-20.
29. Park CB, Larsson NG. 2011. Mitochondrial DNA mutations in disease and aging. J Cell Biol 193: 809-18.
30. Edgar D, Trifunovic A. 2009. The mtDNA mutator mouse: dissecting mitochondrial involvement in aging. Aging 1: 1028-32.
31. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, et al. 2004. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429: 417-23.
32. White DJ, Wolff JN, Pierson M, Gemmell NJ. 2008. Revealing the hidden complexities of mtDNA inheritance. Mol Ecol 17: 4925-42.
33. Wolff JN, Nafisinia M, Sutovsky P, Ballard JWO. 2012. Paternal transmission of mitochondrial DNA as an integral part of mitochondrial inheritance in metapopulations of Drosophila simulans. Heredity, in press. DOI: 10.1038/hdy.2012.60.
34. Gemmell NJ, Metcalf VJ, Allendorf FW. 2004. Mother's curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol Evol 19: 238-44.
35. Frank SA, Hurst LD. 1996. Mitochondria and male disease. Nature 383: 224.
36. Zeh JA, Zeh DW. 2005. Maternal inheritance, sexual conflict and the maladapted male. Trends Genet 21: 281-6.
37. Nielsen R. 2001. Mutations as missing data: inferences on the ages and distributions of nonsynonymous and synonymous mutations. Genetics 159: 401-11.
38. Nielsen R, Weinreich DM. 1999. The age of nonsynonymous and synonymous mutations in animal mtDNA and implications for the mildly deleterious theory. Genetics 153: 497-506.
39. Pereira L, Soares P, Radivojac P, Li B, et al. 2011. Comparing phylogeny and the predicted pathogenicity of protein variations reveals equal purifying selection across the global human mtDNA diversity. Am J Hum Genet 88: 433-9.
40. Stewart JB, Freyer C, Elson JL, Wredenberg A, et al. 2008. Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol 6: e10.
41. Fan W, Waymire KG, Narula N, Li P, et al. 2008. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 319: 958-62.
42. Poulton J, Chiaratti MR, Meirelles FV, Kennedy S, et al. 2010. Transmission of mitochondrial DNA diseases and ways to prevent them. PLoS Genet 6: e1001066.
43. Gemmell NJ, Sin FYT. 2002. Mitochondrial mutations may drive Y chromosome evolution. BioEssays 24: 275-9.
44. Innocenti P, Morrow EH, Dowling DK. 2011. Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science 332: 845-8.
45. Clancy DJ. 2008. Variation in mitochondrial genotype has substantial lifespan effects which may be modulated by nuclear background. Aging Cell 7: 795-804.
46. Innocenti P, Morrow EH. 2010. The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol 8: e1000335.
47. St John JC, Jokhi RP, Barratt CL. 2001. Men with oligoasthenoteratozoospermia harbour higher numbers of multiple mitochondrial DNA deletions in their spermatozoa, but individual deletions are not indicative of overall aetiology. Mol Hum Reprod 7: 103-11.
48. Ieremiadou F, Rodakis GC. 2009. Correlation of the 4977bp mitochondrial DNA deletion with human sperm dysfunction. BMC Res Notes 2: 18.
49. Nakada K, Sato A, Yoshida K, Morita T, et al. 2006. Mitochondria-related male infertility. Proc Natl Acad Sci USA 103: 15148-53.
50. Clancy DJ, Hime GR, Shirras AD. 2011. Cytoplasmic male sterility in Drosophila melanogaster associated with a mitochondrial CYTB variant. Heredity 107: 374-6.
51. Camus MF, Clancy DJ, Dowling DK. 2012. Mitochondria, maternal inheritance, and male aging. Curr Biol 22: 1-5.
52. Wade MJ, Brandvain Y. 2009. Reversing mother's curse: selection on male mitochondrial fitness effects. Evolution 63: 1084-9.
53. Hedrick PW. 2012. Reversing mother's curse revisited. Evolution 66: 612-6.
54. Unckless RL, Herren JK. 2009. Population genetics of sexually antagonistic mitochondrial mutants under inbreeding. J Theor Biol 260: 132-6.
55. Schnable PS, Wise RP. 1998. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3: 175-80.
56. Gemmell NJ, Braisher TL. 2001. Organelle genome evolution. Trends Ecol Evol 16: 489-90.
57. Dowling DK, Nowostawski AL, Arnqvist G. 2007. Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory? J Evol Biol 20: 358-68.
58. Wolstenholme DR. 1992. Mitochondrial genomes. In Wolstenholme DR, Jeon KW, eds. International Review of Cytology. Maryland Heights: Elsevier. p. 173-216.
59. Doonan R, McElwee JJ, Matthijssens F, Walker GA, et al. 2008. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev 22: 3236-41.
60. Back P, Matthijssens F, Vlaeminck C, Braeckman BP, et al. 2010. Effects of sod gene overexpression and deletion mutation on the expression profiles of reporter genes of major detoxification pathways in Caenorhabditis elegans. Exp Gerontol 45: 603.
61. Neretti N, Wang PY, Brodsky AS, Nyguyen HH, et al. 2009. Long-lived Indy induces reduced mitochondrial reactive oxygen species production and oxidative damage. Proc Natl Acad Sci USA 106: 2277-82.
62. Kirkwood TBL, Kowald A. 2012. The free-radical theory of ageing - older, wiser and still alive. BioEssays 34: 692-700.
63. Harmann D. 1956. Aging: a theory based on free radical and radiation chemistry. J Gerontol 11: 298-300.
64. Murphy MP. 2009. How mitochondria produce reactive oxygen species. Biochem J 417: 1-13.
65. 2 generation in isolated mitochondria. J Bioenerg Biomembr 34: 227-33.
66. 2 in living Drosophila. Nat Protoc 7: 946-58.
67. Ballard JW, Melvin RG. 2011. Early life benefits and later life costs of a two amino acid deletion in Drosophila simulans. Evolution 65: 1400-12.
68. Pichaud N, Ballard JW, Tanguay RM, Blier PU. 2011. Thermal sensitivity of mitochondrial functions in permeabilized muscle fibers from two populations of Drosophila simulans with divergent mitotypes. Am J Physiol Regul Integr Comp Physiol 301: R48-59.
69. Wallace DC, Fan W. 2010. Energetics, epigenetics, mitochondrial genetics. Mitochondrion 10: 12-31.
70. Saxonov S, Berg P, Brutlag DL. 2006. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci USA 103: 1412-7.
71. Smiraglia DJ, Kulawiec M, Bistulfi GL, Gupta SG, et al. 2008. A novel role for mitochondria in regulating epigenetic modification in the nucleus. Cancer Biol Ther 7: 1182-90.
72. Bellizzi D, D'Aquila P, Giordano M, Montesanto A, et al. 2012. Global DNA methylation levels are modulated by mitochondrial DNA variants. Epigenomics 4: 17-27.
73. Xie CH, Naito A, Mizumachi T, Evans TT, et al. 2007. Mitochondrial regulation of cancer associated nuclear DNA methylation. Biochem Biophys Res Commun 364: 656-61.
74. Shock LS, Thakkar PV, Peterson EJ, Moran RG, et al. 2011. DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proc Natl Acad Sci USA 108: 3630-5.
75. Chinnery PF, Elliott HR, Hudson G, Samuels DC, et al. 2012. Epigenetics, epidemiology and mitochondrial DNA diseases. Int J Epidemiol 41: 177-87.
76. O'Hagan HM, Wang W, Sen S, Destefano Shields C, et al. 2011. Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell 20: 606-19.
77. Lim LP, Lau NC, Garrett-Engele P, Grimson A, et al. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-73.
78. Carthew RW, Sontheimer EJ. 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136: 642-55.
79. Somel M, Guo S, Fu N, Yan Z, et al. 2010. MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. Genome Res 20: 1207-18.
80. Kloosterman WP, Plasterk RH. 2006. The diverse functions of microRNAs in animal development and disease. Dev Cell 11: 441-50.
81. Liu N, Landreh M, Cao K, Abe M, et al. 2012. The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 482: 519-23.
82. Mercer TR, Neph S, Dinger ME, Crawford J, et al. 2011. The human mitochondrial transcriptome. Cell 146: 645-58.
83. Haussecker D, Huang Y, Lau A, Parameswaran P, et al. 2010. Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 16: 673-95.
84. Lee YS, Shibata Y, Malhotra A, Dutta A. 2009. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 23: 2639-49.
85. Tajima H, Niikura T, Hashimoto Y, Ito Y, et al. 2002. Evidence for in vivo production of humanin peptide, a neuroprotective factor against Alzheimer's disease-related insults. Neurosci Lett 324: 227-31.
86. Hashimoto Y, Niikura T, Tajima H, Yasukawa T, et al. 2001. A rescue factor abolishing neuronal cell death by a wide spectrum of familial Alzheimer's disease genes and Abeta. Proc Natl Acad Sci USA 98: 6336-41.
87. Durieux J, Wolff S, Dillin A. 2011. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144: 79-91.
88. Hoang PT, Park P, Cobb LJ, Paharkova-Vatchkova V, et al. 2010. The neurosurvival factor humanin inhibits beta-cell apoptosis via signal transducer and activator of transcription 3 activation and delays and ameliorates diabetes in nonobese diabetic mice. Metabolism 59: 343-9.
89. Colon E, Strand ML, Carlsson-Skwirut C, Wahlgren A, et al. 2006. Anti-apoptotic factor humanin is expressed in the testis and prevents cell-death in leydig cells during the first wave of spermatogenesis. J Cell Physiol 208: 373-85.
90. Zhang W, Li Z, Hao J, Zhang Z, et al. 2012. S14G-humanin improves cognitive deficits and reduces amyloid pathology in the middle-aged APPswe/PS1dE9 mice. Pharmacol Biochem Behav 100: 361-9.
91. Andersen AA, Panning B. 2003. Epigenetic gene regulation by noncoding RNAs. Curr Opin Cell Biol 15: 281-9.
92. Kunert N, Marhold J, Stanke J, Stach D, et al. 2003. A Dnmt2-like protein mediates DNA methylation in Drosophila. Development 130: 5083-90.
93. Yang X, Schadt EE, Wang S, Wang H, et al. 2006. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16: 995-1004.