Maternal age effect and severe germ-line bottleneck in the inheritance of human mitochondrial DNA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 43, 2014, Pages 15474-15479

  Rebolledo Jaramillo, Boris ^a   Su, Marcia Shu Wei ^a   Stoler, Nicholas ^a   McElhoe, Jennifer A ^a   Dickins, Benjamin ^a   Blankenberg, Daniel ^a   Korneliussen, Thorfinn S ^b,c   Chiaromonte, Francesca ^d   Nielsen, Rasmus ^b   Holland, Mitchell M ^a   Paul, Ian M ^a   Nekrutenko, Anton ^a   Makova, Kateryna D ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Heteroplasmy; Mitochondria

Indexed keywords

CELL NUCLEUS DNA; MITOCHONDRIAL DNA;

ARTICLE; DISEASE ASSOCIATION; FEMALE; FERTILIZATION; GENE FREQUENCY; GERM LINE; GERMLINE MUTATION; HETEROPLASMY; HUMAN; HUMAN CELL; HUMAN TISSUE; INHERITANCE; MATERNAL AGE; MITOCHONDRIAL GENOME; MUTATION RATE; OOCYTE; POLYMERASE CHAIN REACTION SYSTEM; POPULATION GENETICS; AGE; CHILD; DISEASES; DNA SEQUENCE; GENETICS; GERM CELL; INDEL MUTATION; METABOLISM; REPRODUCIBILITY;

AGE FACTORS; CHILD; DISEASE; DNA, MITOCHONDRIAL; FEMALE; GENE FREQUENCY; GERM CELLS; HUMANS; INDEL MUTATION; INHERITANCE PATTERNS; MATERNAL AGE; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, DNA;

EID: 84908292423     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1409328111     Document Type: Article

References (58)

1. Wallace DC, Chalkia D (2013) Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold Spring Harb Perspect Biol 5(11):a021220.
2. Galtier N, Nabholz B, Glémin S, Hurst GD (2009) Mitochondrial DNA as a marker of molecular diversity: A reappraisal. Mol Ecol 18(22):4541-4550.
3. Pesole G, et al. (2012) The neglected genome. EMBO Rep 13(6):473-474.
4. Payne BA, et al. (2013) Universal heteroplasmy of human mitochondrial DNA. Hum Mol Genet 22:384-90.
5. Li M, et al. (2010) Detecting heteroplasmy from high-throughput sequencing of complete human mitochondrial DNA genomes. Am J Hum Genet 87(2):237-249.
6. Cree LM, et al. (2008) A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat Genet 40(2):249-254.
7. Wai T, Teoli D, Shoubridge EA (2008) The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat Genet 40(12):1484-1488.
8. Cao L, 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(12):e1000756.
9. Jenuth JP, Peterson AC, Fu K, Shoubridge EA (1996) Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nat Genet 14(2):146-151.
10. Marchington DR, Hartshorne GM, Barlow D, Poulton J (1997) Homopolymeric tract heteroplasmy in mtDNA from tissues and single oocytes: Support for a genetic bottleneck. Am J Hum Genet 60(2):408-416.
11. Guo Y, et al. (2013) Very low-level heteroplasmy mtDNA variations are inherited in humans. J Genet Genomics 40(12):607-615.
12. Poulton J, et al. (2010) Transmission of mitochondrial DNA diseases and ways to prevent them. PLoS Genet 6(8):6.
13. Parsons TJ, et al. (1997) A high observed substitution rate in the human mitochondrial DNA control region. Nat Genet 15(4):363-368.
14. Henn BM, Gignoux CR, Feldman MW, Mountain JL (2009) Characterizing the time dependency of human mitochondrial DNAmutation rate estimates. Mol Biol Evol 26(1):217-230.
15. Simone D, Calabrese FM, Lang M, Gasparre G, Attimonelli M (2011) The reference human nuclear mitochondrial sequences compilation validated and implemented on the UCSC genome browser. BMC Genomics 12:517.
16. Dickins B, et al. (2014) Controlling for contamination in re-sequencing studies with a reproducible web-based phylogenetic approach. Biotechniques 56(3):134-136, 138-141.
17. Li M, Stoneking M (2012) A new approach for detecting low-level mutations in nextgeneration sequence data. Genome Biol 13(5):R34.
18. Hindson BJ, et al. (2011) High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal Chem 83(22):8604-8610.
19. Ye K, Lu J, Ma F, Keinan A, Gu Z (2014) Extensive pathogenicity of mitochondrial heteroplasmy in healthy human individuals. Proc Natl Acad Sci USA 111(29):10654-10659.
20. Rollins B, et al. (2009) Mitochondrial variants in schizophrenia, bipolar disorder, and major depressive disorder. PLoS ONE 4(3):e4913.
21. Prasad GN, et al. (2006) Novel mitochondrial DNA mutations in a rare variety of hypertrophic cardiomyopathy. Int J Cardiol 109(3):432-433.
22. Tang S, et al. (2010) Left ventricular noncompaction is associated with mutations in the mitochondrial genomes. Mitochondrion 10(4):350-357.
23. Abu-Amero KK, Alzahrani AS, Zou M, Shi Y (2005) High frequency of somatic mitochondrial DNA mutations in human thyroid carcinomas and complex I respiratory defect in thyroid cancer cell lines. Oncogene 24(8):1455-1460.
24. del Castillo FJ, et al. (2003) Heteroplasmy for the 1555A>G mutation in the mitochondrial 12S rRNA gene in six Spanish families with non-syndromic hearing loss. J Med Genet 40(8):632-636.
25. Wortmann SB, et al. (2012) Mitochondrial DNA m.3242G > A mutation, an under diagnosed cause of hypertrophic cardiomyopathy and renal tubular dysfunction? Eur J Med Genet 55(10):552-556.
26. Du W-D, et al. (2011) A simple oligonucleotide biochip capable of rapidly detecting known mitochondrial DNA mutations in Chinese patients with Leber's hereditary optic neuropathy (LHON). Dis Markers 30(4):181-190.
27. Ma Y, et al. (2009) The study of mitochondrial A3243G mutation in different samples. Mitochondrion 9(2):139-143.
28. Chinnery PF, et al. (2000) The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both? Trends Genet 16(11):500-505.
29. Hill JH, Chen Z, Xu H (2014) Selective propagation of functional mitochondrial DNA during oogenesis restricts the transmission of a deleterious mitochondrial variant. Nat Genet 46(4):389-392.
30. Millar CD, et al. (2008) Mutation and evolutionary rates in adélie penguins from the antarctic. PLoS Genet 4(10):e1000209.
31. Hendy MD, Woodhams MD, Dodd A (2009)Modelling mitochondrial site polymorphisms to infer the number of segregating units and mutation rate. Biol Lett 5(3):397-400.
32. Goto H, et al. (2011) Dynamics of mitochondrial heteroplasmy in three families investigated via a repeatable re-sequencing study. Genome Biol 12(6):R59.
33. Samuels DC, et al. (2013) Recurrent tissue-specific mtDNA mutations are common in humans. PLoS Genet 9(11):e1003929.
34. Avital G, et al. (2012)Mitochondrial DNA heteroplasmy in diabetes and normal adults: Role of acquired and inherited mutational patterns in twins. Hum Mol Genet 21(19):4214-4224.
35. Kennedy SR, Salk JJ, Schmitt MW, Loeb LA (2013) Ultra-sensitive sequencing reveals an age-related increase in somatic mitochondrial mutations that are inconsistent with oxidative damage. PLoS Genet 9(9):e1003794.
36. Larsson N-G (2010) Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem 79:683-706.
37. Itsara LS, et al. (2014) Oxidative stress is not a major contributor to somatic mitochondrial DNA mutations. PLoS Genet 10(2):e1003974.
38. Seifer DB, DeJesus V, Hubbard K (2002) Mitochondrial deletions in luteinized granulosa cells as a function of age in women undergoing in vitro fertilization. Fertil Steril 78(5):1046-1048.
39. Barritt JA, Cohen J, Brenner CA (2000) Mitochondrial DNA point mutation in human oocytes is associated with maternal age. Reprod Biomed Online 1(3):96-100.
40. Eichenlaub-Ritter U (2012) Oocyte ageing and its cellular basis. Int J Dev Biol 56(10-12):841-852.
41. Barritt JA, Brenner CA, Cohen J, Matt DW (1999) Mitochondrial DNA rearrangements in human oocytes and embryos. Mol Hum Reprod 5(10):927-933.
42. Bartmann AK, Romão GS, Ramos EdaS, Ferriani RA (2004) Why do older women have poor implantation rates? A possible role of the mitochondria. J Assist Reprod Genet 21(3):79-83.
43. Olivo PD, Van de Walle MJ, Laipis PJ, Hauswirth WW (1983) Nucleotide sequence evidence for rapid genotypic shifts in the bovine mitochondrial DNA D-loop. Nature 306(5941):400-402.
44. Ashley MV, Laipis PJ, Hauswirth WW (1989) Rapid segregation of heteroplasmic bovine mitochondria. Nucleic Acids Res 17(18):7325-7331.
45. Howell N, et al. (1992) Mitochondrial gene segregation in mammals: Is the bottleneck always narrow? Hum Genet 90(1-2):117-120.
46. Lutz S, Weisser HJ, Heizmann J, Pollak S (2000) Mitochondrial heteroplasmy among maternally related individuals. Int J Legal Med 113(3):155-161.
47. Monnot S, et al. (2011) Segregation of mtDNA throughout human embryofetal development: m.3243A>G as a model system. Hum Mutat 32(1):116-125.
48. Kong A, et al. (2012) Rate of de novo mutations and the importance of father's age to disease risk. Nature 488(7412):471-475.
49. Howell N, et al. (2003) The pedigree rate of sequence divergence in the human mitochondrial genome: There is a difference between phylogenetic and pedigree rates. Am J Hum Genet 72(3):659-670.
50. Santos C, et al. (2005) Understanding differences between phylogenetic and pedigree-derived mtDNA mutation rate: A model using families from the Azores Islands (Portugal). Mol Biol Evol 22(6):1490-1505.
51. Sigurʇardóttir S, Helgason A, Gulcher JR, Stefansson K, Donnelly P (2000) The mutation rate in the human mtDNA control region. Am J Hum Genet 66(5):1599-1609.
52. Denver DR, Moris K, Lynch M, Vassilieva LL, Thomas WK (2000) High direct estimate of the mutation rate in the mitochondrial genome of Caenorhabditis elegans. Science 289:2342-2344.
53. Haag-Liautard C, et al. (2008) Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. PLoS Biol 6(8):e204.
54. Lynch M (2010) Evolution of the mutation rate. Trends Genet 26(8):345-352.
55. Sung W, Ackerman MS, Miller SF, Doak TG, Lynch M (2012) Drift-barrier hypothesis and mutation-rate evolution. Proc Natl Acad Sci USA 109(45):18488-18492.
56. Kenney MC, et al. (2014) Molecular and bioenergetic differences between cells with African versus European inherited mitochondrial DNA haplogroups: Implications for population susceptibility to diseases. Biochim Biophys Acta 1842(2):208-219.
57. McElhoe JA, et al. (2014) Development and assessment of an optimized next-generation DNA sequencing approach for the mtgenome using the Illumina MiSeq. Forensic Sci Int Genet 13C:20-29.
58. Guo Y, et al. (2012) The effect of strand bias in Illumina short-read sequencing data. BMC Genomics 13:666.