Keeping mtDNA in Shape between Generations
Since the unexpected discovery that mitochondria contain their own distinct DNA molecules, studies of the mitochondrial DNA (mtDNA) have yielded many surprises. In animals, transmission of the mtDNA genome is explicitly non-Mendelian, with a very high number of genome copies being inherited from the mother after a drastic bottleneck. Recent work has begun to uncover the molecular details of this unusual mode of transmission. Many surprising variations in animal mitochondrial biology are known; however, a series of recent studies have identified a core of evolutionarily conserved mechanisms relating to mtDNA inheritance, e.g., mtDNA bottlenecks during germ cell development, selection against specific mtDNA mutation types during maternal transmission, and targeted destruction of sperm mitochondria. In this review, we outline recent literature on the transmission of mtDNA in animals and highlight the implications for human health and ageing.
Vyšlo v časopise:
Keeping mtDNA in Shape between Generations. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004670
Kategorie:
Review
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004670
Souhrn
Since the unexpected discovery that mitochondria contain their own distinct DNA molecules, studies of the mitochondrial DNA (mtDNA) have yielded many surprises. In animals, transmission of the mtDNA genome is explicitly non-Mendelian, with a very high number of genome copies being inherited from the mother after a drastic bottleneck. Recent work has begun to uncover the molecular details of this unusual mode of transmission. Many surprising variations in animal mitochondrial biology are known; however, a series of recent studies have identified a core of evolutionarily conserved mechanisms relating to mtDNA inheritance, e.g., mtDNA bottlenecks during germ cell development, selection against specific mtDNA mutation types during maternal transmission, and targeted destruction of sperm mitochondria. In this review, we outline recent literature on the transmission of mtDNA in animals and highlight the implications for human health and ageing.
Zdroje
1. RochetteNC, Brochier-ArmanetC, GouyM (2014) Phylogenomic Test of the Hypotheses for the Evolutionary Origin of Eukaryotes. Mol Biol Evol 4: 832–845.
2. MullerM, MentelM, van HellemondJJ, HenzeK, WoehleC, et al. (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76: 444–495.
3. KarlbergO, CanbackB, KurlandCG, AnderssonSG (2000) The dual origin of the yeast mitochondrial proteome. Yeast 17: 170–187.
4. PagliariniDJ, CalvoSE, ChangB, ShethSA, VafaiSB, et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134: 112–123.
5. MeisingerC, SickmannA, PfannerN (2008) The mitochondrial proteome: from inventory to function. Cell 134: 22–24.
6. BurgerG, GrayMW, Franz LangB (2003) Mitochondrial genomes: anything goes. Trends Genet 19: 709–716.
7. NassMM, NassS (1963) Intramitochondrial Fibers with DNA Characteristics. I. Fixation and Electron Staining Reactions. J Cell Biol 19: 593–611.
8. NassS, NassMM (1964) Intramitochondrial Fibers with Deoxyribonucleic Acid Characteristics: Observations of Ehrlich Ascites Tumor Cells. J Natl Cancer Inst 33: 777–798.
9. NassMM, NassS, AfzeliusBA (1965) The General Occurence of Mitochondrial DNA. Exp Cell Res 37: 516–539.
10. HikosakaK, KitaK, TanabeK (2013) Diversity of mitochondrial genome structure in the phylum Apicomplexa. Mol Biochem Parasitol 188: 26–33.
11. SlamovitsCH, SaldarriagaJF, LarocqueA, KeelingPJ (2007) The highly reduced and fragmented mitochondrial genome of the early-branching dinoflagellate Oxyrrhis marina shares characteristics with both apicomplexan and dinoflagellate mitochondrial genomes. J Mol Biol 372: 356–368.
12. LevinLA (2010) Anaerobic metazoans: no longer an oxymoron. BMC Biol 8: 31.
13. DanovaroR, Dell'AnnoA, PuscedduA, GambiC, HeinerI, et al. (2010) The first metazoa living in permanently anoxic conditions. BMC Biol 8: 30.
14. BerntM, BrabandA, SchierwaterB, StadlerPF (2013) Genetic aspects of mitochondrial genome evolution. Mol Phylogenet Evol 69: 328–338.
15. FalkenbergM, LarssonNG, GustafssonCM (2007) DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem 76: 679–699.
16. BooreJL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27: 1767–1780.
17. YangJS, YangWJ (2008) The complete mitochondrial genome sequence of the hydrothermal vent galatheid crab Shinkaia crosnieri (Crustacea: Decapoda: Anomura): a novel arrangement and incomplete tRNA suite. BMC Genomics 9: 257.
18. DornerM, AltmannM, PääboS, MorlM (2001) Evidence for import of a lysyl-tRNA into marsupial mitochondria. Mol Biol Cell 12: 2688–2698.
19. MercerTR, NephS, DingerME, CrawfordJ, SmithMA, et al. (2011) The human mitochondrial transcriptome. Cell 146: 645–658.
20. BeckenbachAT, JoyJB (2009) Evolution of the Mitochondrial Genomes of Gall Midges (Diptera: Cecidomyiidae): Rearrangement and Severe Truncation of tRNA Genes. Genome Biol Evol 1: 278–287.
21. MastaSE, BooreJL (2008) Parallel evolution of truncated transfer RNA genes in arachnid mitochondrial genomes. Mol Biol Evol 25: 949–959.
22. MastaSE, BooreJL (2004) The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Mol Biol Evol 21: 893–902.
23. SegoviaR, PettW, TrewickS, LavrovDV (2011) Extensive and evolutionarily persistent mitochondrial tRNA editing in Velvet Worms (phylum Onychophora). Mol Biol Evol 28: 2873–2881.
24. ShaoZ, GrafS, ChagaOY, LavrovDV (2006) Mitochondrial genome of the moon jelly Aurelia aurita (Cnidaria, Scyphozoa): A linear DNA molecule encoding a putative DNA-dependent DNA polymerase. Gene 381: 92–101.
25. WangX, LavrovDV (2008) Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae. PLoS ONE 3: e2723.
26. AmeurA, StewartJB, FreyerC, HagströmE, IngmanM, et al. (2011) Ultra-Deep Sequencing of Mouse Mitochondrial DNA: Mutational Patterns and Their Origins. PLoS Genet 7: e1002028.
27. SeidmanD, JohsnonD, GerbasiV, GoldenD, OrlandoR, et al. (2012) A Mitochondrial membrane complex that contains proteins necessary for tRNA import in Trypanosoma brucei. J Biol Chem 12: 8892–8903.
28. ChinneryPF, SamuelsDC (1999) Relaxed replication of mtDNA: A model with implications for the expression of disease. Am J Hum Genet 64: 1158–1165.
29. AshleyMV, LaipisPJ, HauswirthWW (1989) Rapid segregation of heteroplasmic bovine mitochondria. Nucleic Acids Res 17: 7325–7331.
30. OlivoPD, Van de WalleMJ, LaipisPJ, HauswirthWW (1983) Nucleotide sequence evidence for rapid genotypic shifts in the bovine mitochondrial DNA D-loop. Nature 306: 400–402.
31. HauswirthWW, LaipisPJ (1982) Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proc Natl Acad Sci U S A 79: 4686–4690.
32. JenuthJP, PetersonAC, FuK, ShoubridgeEA (1996) Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nat Genet 14: 146–151.
33. WolffJN, WhiteDJ, WoodhamsM, WhiteHE, GemmellNJ (2011) The strength and timing of the mitochondrial bottleneck in salmon suggests a conserved mechanism in vertebrates. PLoS ONE 6: e20522.
34. CreeLM, SamuelsDC, de Sousa LopesSC, RajasimhaHK, WonnapinijP, et al. (2008) A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat Genet 40: 249–254.
35. zPetitN, TourailleS, DebiseR, MorelF, RenouxM, et al. (1998) Developmental changes in heteroplasmy level and mitochondrial gene expression in a Drosophila subobscura mitochondrial deletion mutant. Curr Genet 33: 330–339.
36. MaH, XuH, O'FarrellPH (2014) Transmission of mitochondrial mutations and action of purifying selection in Drosophila melanogaster. Nat Genet 46: 393–397.
37. HillJH, ChenZ, XuH (2014) Selective propagation of functional mitochondrial DNA during oogenesis restricts the transmission of a deleterious mitochondrial variant. Nat Genet 46: 389–392.
38. ShitaraH, KanedaH, SatoA, InoueK, OguraA, et al. (2000) Selective and continuous elimination of mitochondria microinjected into mouse eggs from spermatids, but not from liver cells, occurs throughout embryogenesis. Genetics 156: 1277–1284.
39. DeLucaSZ, O'FarrellPH (2012) Barriers to male transmission of mitochondrial DNA in sperm development. Dev Cell 22: 660–668.
40. SatoM, SatoK (2011) Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 334: 1141–1144.
41. Al RawiS, Louvet-ValleeS, DjeddiA, SachseM, CulettoE, et al. (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334: 1144–1147.
42. StewartDT, SaavedraC, StanwoodRR, BallAO, ZourosE (1995) Male and female mitochondrial DNA lineages in the blue mussel (Mytilus edulis) species group. Mol Biol Evol 12: 735–747.
43. GyllenstenU, WhartonD, JosefssonA, WilsonAC (1991) Paternal inheritance of mitochondrial DNA in mice. Nature 352: 255–257.
44. GyllenstenU, WhartonD, WilsonAC (1985) Maternal inheritance of mitochondrial DNA during backcrossing of two species of mice. J Hered 76: 321–324.
45. UjvariB, DowtonM, MadsenT (2007) Mitochondrial DNA recombination in a free-ranging Australian lizard. Biol Lett 3: 189–192.
46. GuoX, LiuS, LiuY (2006) Evidence for recombination of mitochondrial DNA in triploid crucian carp. Genetics 172: 1745–1749.
47. LadoukakisED, TheologidisI, RodakisGC, ZourosE (2011) Homologous recombination between highly diverged mitochondrial sequences: examples from maternally and paternally transmitted genomes. Mol Biol Evol 28: 1847–1859.
48. SatoA, NakadaK, AkimotoM, IshikawaK, OnoT, et al. (2005) Rare creation of recombinant mtDNA haplotypes in mammalian tissues. Proc Natl Acad Sci U S A 102: 6057–6062.
49. HagstromE, FreyerC, BattersbyBJ, StewartJB, LarssonNG (2014) No recombination of mtDNA after heteroplasmy for 50 generations in the mouse maternal germline. Nucleic Acids Res 42: 1111–1116.
50. PesceM, ScholerHR (2001) Oct-4: gatekeeper in the beginnings of mammalian development. Stem Cells 19: 271–278.
51. PikoL, TaylorKD (1987) Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev Biol 123: 364–374.
52. WaiT, AoA, ZhangX, CyrD, DufortD, et al. (2010) The role of mitochondrial DNA copy number in mammalian fertility. Biol Reprod 83: 52–62.
53. CaoL, ShitaraH, HoriiT, NagaoY, ImaiH, et al. (2007) The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat Genet 39: 386–390.
54. WaiT, TeoliD, ShoubridgeEA (2008) The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat Genet 40: 1484–1488.
55. CaoL, ShitaraH, SugimotoM, HayashiJ, AbeK, et al. (2009) New evidence confirms that the mitochondrial bottleneck is generated without reduction of mitochondrial DNA content in early primordial germ cells of mice. PLoS Genet 5: e1000756.
56. WaiT, ShoubridgeEA (2010) Reply to “Reassessing evidence for a postnatal mitochondrial genetic bottleneck”. Nat Genet 42: 472–473.
57. SamuelsDC, WonnapinijP, CreeLM, ChinneryPF (2010) Reassessing evidence for a postnatal mitochondrial genetic bottleneck. Nat Genet 42: 471–472 author reply 472–473.
58. Haag-LiautardC, CoffeyN, HouleD, LynchM, CharlesworthB, et al. (2008) Direct Estimation of the Mitochondrial DNA Mutation Rate in Drosophila melanogaster. PLoS Biol 6: e204.
59. PikoL, HoughamAJ, BulpittKJ (1988) Studies of sequence heterogeneity of mitochondrial DNA from rat and mouse tissues: evidence for an increased frequency of deletions/additions with aging. Mech Ageing Dev 43: 279–293.
60. KatayamaM, TanakaM, YamamotoH, OhbayashiT, NimuraY, et al. (1991) Deleted mitochondrial DNA in the skeletal muscle of aged individuals. Biochem Int 25: 47–56.
61. WilliamsSL, HuangJ, EdwardsYJ, UlloaRH, DillonLM, et al. (2010) The mtDNA mutation spectrum of the progeroid Polg mutator mouse includes abundant control region multimers. Cell Metab 12: 675–682.
62. WilliamsSL, MashDC, ZuchnerS, MoraesCT (2013) Somatic mtDNA mutation spectra in the aging human putamen. PLoS Genet 9: e1003990.
63. TrifunovicA, WredenbergA, FalkenbergM, SpelbrinkJN, RovioAT, et al. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429: 417–423.
64. KornblumC, NichollsTJ, HaackTB, ScholerS, PeevaV, et al. (2013) Loss-of-function mutations in MGME1 impair mtDNA replication and cause multisystemic mitochondrial disease. Nat Genet 45: 214–219.
65. PayneBA, WilsonIJ, Yu-Wai-ManP, CoxheadJ, DeehanD, et al. (2013) Universal heteroplasmy of human mitochondrial DNA. Hum Mol Genet 22: 384–390.
66. LiM, SchonbergA, SchaeferM, SchroederR, NasidzeI, et al. (2010) Detecting heteroplasmy from high-throughput sequencing of complete human mitochondrial DNA genomes. Am J Hum Genet 87: 237–249.
67. HeY, WuJ, DressmanDC, Iacobuzio-DonahueC, MarkowitzSD, et al. (2010) Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature 464: 610–614.
68. LarssonNG (2010) Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem 79: 683–706.
69. HarmanD (1972) The biologic clock: the mitochondria? J Am Geriatr Soc 20: 145–147.
70. HarmanD (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11: 298–300.
71. ZhengW, KhrapkoK, CollerHA, ThillyWG, CopelandWC (2006) Origins of human mitochondrial point mutations as DNA polymerase gamma-mediated errors. Mutat Res 599: 11–20.
72. KhrapkoK, CollerHA, AndrePC, LiXC, HanekampJS, et al. (1997) Mitochondrial mutational spectra in human cells and tissues. Proc Natl Acad Sci U S A 94: 13798–13803.
73. ItsaraLS, KennedySR, FoxEJ, YuS, HewittJJ, et al. (2014) Oxidative stress is not a major contributor to somatic mitochondrial DNA mutations. PLoS Genet 10: e1003974.
74. KennedySR, SalkJJ, SchmittMW, LoebLA (2013) Ultra-sensitive sequencing reveals an age-related increase in somatic mitochondrial mutations that are inconsistent with oxidative damage. PLoS Genet 9: e1003794.
75. FayetG, JanssonM, SternbergD, MoslemiAR, BlondyP, et al. (2002) Ageing muscle: clonal expansions of mitochondrial DNA point mutations and deletions cause focal impairment of mitochondrial function. Neuromuscul Disord 12: 484–493.
76. CottrellDA, IncePG, WardellTM, TurnbullDM, JohnsonMA (2001) Accelerated ageing changes in the choroid plexus of a case with multiple mitochondrial DNA deletions. Neuropathol Appl Neurobiol 27: 206–214.
77. TaylorRW, BarronMJ, BorthwickGM, GospelA, ChinneryPF, et al. (2003) Mitochondrial DNA mutations in human colonic crypt stem cells. J Clin Invest 112: 1351–1360.
78. GreavesLC, ElsonJL, NooteboomM, GradyJP, TaylorGA, et al. (2012) Comparison of mitochondrial mutation spectra in ageing human colonic epithelium and disease: absence of evidence for purifying selection in somatic mitochondrial DNA point mutations. PLoS Genet 8: e1003082.
79. PereiraL, SoaresP, MaximoV, SamuelsDC (2012) Somatic mitochondrial DNA mutations in cancer escape purifying selection and high pathogenicity mutations lead to the oncocytic phenotype: pathogenicity analysis of reported somatic mtDNA mutations in tumors. BMC Cancer 12: 53.
80. TrifunovicA, HanssonA, WredenbergA, RovioAT, DufourE, et al. (2005) Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc Natl Acad Sci U S A 102: 17993–17998.
81. KujothGC, HionaA, PughTD, SomeyaS, PanzerK, et al. (2005) Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309: 481–484.
82. SamuelsDC, LiC, LiB, SongZ, TorstensonE, et al. (2013) Recurrent tissue-specific mtDNA mutations are common in humans. PLoS Genet 9: e1003929.
83. RandDM (2011) Population genetics of the cytoplasm and the units of selection on mitochondrial DNA in Drosophila melanogaster. Genetica 139: 685–697.
84. LiauWS, Gonzalez-SerricchioAS, DeshommesC, ChinK, LaMunyonCW (2007) A persistent mitochondrial deletion reduces fitness and sperm performance in heteroplasmic populations of C. elegans. BMC Genet 8: 8.
85. WanrooijS, Miralles FusteJ, StewartJB, WanrooijPH, SamuelssonT, et al. (2012) In vivo mutagenesis reveals that OriL is essential for mitochondrial DNA replication. EMBO Rep 13: 1130–1137.
86. RossJM, StewartJB, HagstromE, BreneS, MourierA, et al. (2013) Germline mitochondrial DNA mutations aggravate ageing and can impair brain development. Nature 501: 412–415.
87. LynchM (1996) Mutation accumulation in transfer RNAs: molecular evidence for Muller's ratchet in mitochondrial genomes. Mol Biol Evol 13: 209–220.
88. TaylorRW, TurnbullDM (2005) Mitochondrial DNA mutations in human disease. Nat Rev Genet 6: 389–402.
89. LarssonNG, TuliniusMH, HolmeE, OldforsA, AndersenO, et al. (1992) Segregation and manifestations of the mtDNA tRNA(Lys) A→G(8344) mutation of myoclonus epilepsy and ragged-red fibers (MERRF) syndrome. Am J Hum Genet 51: 1201–1212.
90. MullerHJ (1964) The Relation of Recombination to Mutational Advance. Mutat Res 1: 2–9.
91. FelsensteinJ (1974) The evolutionary advantage of recombination. Genetics 78: 737–756.
92. StewartJB, FreyerC, ElsonJL, WredenbergA, CansuZ, et al. (2008) Strong Purifying Selection in Transmission of Mammalian Mitochondrial DNA. PLoS Biol 6: e10.
93. FanW, WaymireKG, NarulaN, LiP, RocherC, et al. (2008) A Mouse Model of Mitochondrial Disease Reveals Germline Selection Against Severe mtDNA Mutations. Science 319: 958–962.
94. FreyerC, CreeLM, MourierA, StewartJB, KoolmeisterC, et al. (2012) Variation in germline mtDNA heteroplasmy is determined prenatally but modified during subsequent transmission. Nat Genet 44: 1282–1285.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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