Very Low-Level Heteroplasmy mtDNA Variations Are Inherited in Humans

Journal of Genetics and Genomics

Volumn 40, Issue 12, 2013, Pages 607-615

  Guo, Yan ^a   Li, Chung I ^b   Sheng, Quanhu ^a   Winther, Jeanette F ^c   Cai, Qiuyin ^d   Boice, John D ^e   Shyr, Yu ^a  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b Chiayi University   (Taiwan)

^c INSTITUTE OF CANCER EPIDEMIOLOGY   (Denmark)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^e NATIONAL COUNCIL ON RADIATION PROTECTION AND MEASUREMENTS   (United States)

Author keywords

Bottleneck; Heteroplasmy; High depth sequencing; Maternal inheritance; MtDNA mutations; Next generation sequencing

Indexed keywords

MITOCHONDRIAL DNA;

ALLELE; ARTICLE; CLINICAL ARTICLE; FEMALE; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; HETEROPLASMY; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN TISSUE; INHERITANCE; MITOCHONDRIAL GENOME; MUTATION RATE; NUCLEOTIDE SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; DNA SEQUENCE; MUTATION; BOTTLENECK; CHEMISTRY; EXTRACHROMOSOMAL INHERITANCE; GENETICS; HIGH-DEPTH SEQUENCING; MOTHER; MTDNA MUTATIONS; NEXT-GENERATION SEQUENCING;

BOTTLENECK; HETEROPLASMY; HIGH-DEPTH SEQUENCING; MATERNAL INHERITANCE; MTDNA MUTATIONS; NEXT-GENERATION SEQUENCING;

DNA, MITOCHONDRIAL; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INHERITANCE PATTERNS; MOTHERS; MUTATION; SEQUENCE ANALYSIS, DNA;

EID: 84891044032     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2013.10.003     Document Type: Article

References (41)

1. Andrews R.M., Kubacka I., Chinnery P.F., Lightowlers R.N., Turnbull D.M., Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet. 1999, 23:147.
2. Chinnery P.F., Thorburn D.R., Samuels D.C., White S.L., Dahl H.H.M., Turnbull D.M., Lightowlers R.N., Howell N. The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or bothα. Trends Genet. 2000, 16:500-505.
3. Cock P.J., Fields C.J., Goto N., Heuer M.L., Rice P.M. The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants. Nucleic Acids Res. 2010, 38:1767-1771.
4. Cree L.M., Samuels D.C., Lopes S., Rajasimha H.K., Wonnapinij P., Mann J.R., Dahl H.H.M., Chinnery P.F. A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat. Genet. 2008, 40:249-254.
5. Curwen G.B., Cadwell K.K., Winther J.F., Tawn E.J., Rees G.S., Olsen J.H., Rechnitzer C., Schroeder H., Guldberg P., Cordell H.J., Boice J.D. The heritability of G2 chromosomal radiosensitivity and its association with cancer in Danish cancer survivors and their offspring. Int. J. Radiat. Biol. 2010, 86:986-995.
6. Curwen G.B., Winther J.F., Tawn E.J., Smart V., Whitehouse C.A., Rees G.S., Olsen J.H., Guldberg P., Rechnitzer C., Schroder H., Bryant P.E., Sheng X., Lee H.S., Chakraborty R., Boice J.D. G(2) chromosomal radiosensitivity in Danish survivors of childhood and adolescent cancer and their offspring. Br. J. Cancer 2005, 93:1038-1045.
7. Danecek P., Auton A., Abecasis G., Albers C.A., Banks E., DePristo M.A., Handsaker R.E., Lunter G., Marth G.T., Sherry S.T., McVean G., Durbin R. The variant call format and VCFtools. Bioinformatics 2011, 27:2156-2158.
8. Durbin R.M., Altshuler D.L., Abecasis G.R., Bentley D.R., Chakravarti A., Clark A.G., Collins F.S., De La Vega F.M., Donnelly P., Egholm M., Flicek P., Gabriel S.B., Gibbs R.A., Knoppers B.M., Lander E.S., Lehrach H., Mardis E.R., McVean G.A., Nickerson D., Peltonen L., Schafer A.J., Sherry S.T., Wang J., Wilson R.K., Gibbs R.A., Deiros D., Metzker M., Muzny D., Reid J., Wheeler D., Wang J., Li J.X., Jian M., Li G., Li R.Q., Liang H.Q., Tian G., Wang B., Wang J., Wang W., Yang H.M., Zhang X.Q., Zheng H.S., Lander E.S., Altshuler D.L., Ambrogio L., Bloom T., Cibulskis K., Fennell T.J., Gabriel S.B., Jaffe D.B., Shefler E., Sougnez C.L., Bentley D.R., Gormley N., Humphray S., Kingsbury Z., Koko-Gonzales P., Stone J., McKernan K.J., Costa G.L., Ichikawa J.K., Lee C.C., Sudbrak R., Lehrach H., Borodina T.A., Dahl A., Davydov A.N., Marquardt P., Mertes F., Nietfeld W., Rosenstiel P., Schreiber S., Soldatov A.V., Timmermann B., Tolzmann M., Egholm M., Affourtit J., Ashworth D., Attiya S., Bachorski M., Buglione E., Burke A., Caprio A., Celone C., Clark S., Conners D., Desany B., Gu L., Guccione L., Kao K., Kebbel A., Knowlton J., Labrecque M., McDade L., Mealmaker C., Minderman M., Nawrocki A., Niazi F., Pareja K., Ramenani R., Riches D., Song W., Turcotte C., Wang S., Mardis E.R., Dooling D., Fulton L., Fulton R., Weinstock G., Durbin R.M., Burton J., Carter D.M., Churcher C., Coffey A., Cox A., Palotie A., Quail M., Skelly T., Stalker J., Swerdlow H.P., Turner D., De Witte A., Giles S., Gibbs R.A., Wheeler D., Bainbridge M., Challis D., Sabo A., Yu F., Yu J., Wang J., Fang X.D., Guo X.S., Li R.Q., Li Y.R., Luo R.B., Tai S., Wu H.L., Zheng H.C., Zheng X.L., Zhou Y., Yang H.M., Marth G.T., Garrison E.P., Huang W., Indap A., Kural D., Lee W.P., Leong W.F., Huang W.C., Indap A., Kural D., Lee W.P., Leong W.F., Quinlan A.R., Stewart C., Stromberg M.P., Ward A.N., Wu J.T., Lee C., Mills R.E., Shi X.H., Daly M.J., DePristo M.A., Altshuler D.L., Ball A.D., Banks E., Bloom T., Browning B.L., Cibulskis K., Fennell T.J., Garimella K.V., Grossman S.R., Handsaker R.E., Hanna M., Hartl C., Jaffe D.B., Kernytsky A.M., Korn J.M., Li H., Maguire J.R., McCarroll S.A., McKenna A., Nemesh J.C., Philippakis A.A., Poplin R.E., Price A., Rivas M.A., Sabeti P.C., Schaffner S.F., Shefler E., Shlyakhter I.A., Cooper D.N., Ball E.V., Mort M., Phillips A.D., Stenson P.D., Sebat J., Makarov V., Ye K., Yoon S.C., Bustamante C.D., Clark A.G., Boyko A., Degenhardt J., Gravel S., Gutenkunst R.N., Kaganovich M., Keinan A., Lacroute P., Ma X., Reynolds A., Clarke L., Flicek P., Cunningham F., Herrero J., Keenen S., Kulesha E., Leinonen R., McLaren W., Radhakrishnan R., Smith R.E., Zalunin V., Zheng-Bradley X.Q., Korbel J.O., Stutz A.M., Humphray S., Bauer M., Cheetham R.K., Cox T., Eberle M., James T., Kahn S., Murray L., Ye K., De La Vega F.M., Fu Y.T., Hyland F.C.L., Manning J.M., McLaughlin S.F., Peckham H.E., Sakarya O., Sun Y.A., Tsung E.F., Batzer M.A., Konkel M.K., Walker J.A., Sudbrak R., Albrecht M.W., Amstislavskiy V.S., Herwig R., Parkhomchuk D.V., Sherry S.T., Agarwala R., Khouri H., Morgulis A.O., Paschall J.E., Phan L.D., Rotmistrovsky K.E., Sanders R.D., Shumway M.F., Xiao C.L., McVean G.A., Auton A., Iqbal Z., Lunter G., Marchini J.L., Moutsianas L., Myers S., Tumian A., Desany B., Knight J., Winer R., Craig D.W., Beckstrom-Sternberg S.M., Christoforides A., Kurdoglu A.A., Pearson J., Sinari S.A., Tembe W.D., Haussler D., Hinrichs A.S., Katzman S.J., Kern A., Kuhn R.M., Przeworski M., Hernandez R.D., Howie B., Kelley J.L., Melton S.C., Abecasis G.R., Li Y., Anderson P., Blackwell T., Chen W., Cookson W.O., Ding J., Kang H.M., Lathrop M., Liang L.M., Moffatt M.F., Scheet P., Sidore C., Snyder M., Zhan X.W., Zollner S., Awadalla P., Casals F., Idaghdour Y., Keebler J., Stone E.A., Zilversmit M., Jorde L., Xing J.C., Eichler E.E., Aksay G., Alkan C., Hajirasouliha I., Hormozdiari F., Kidd J.M., Sahinalp S.C., Sudmant P.H., Mardis E.R., Chen K., Chinwalla A., Ding L., Koboldt D.C., McLellan M.D., Dooling D., Weinstock G., Wallis J.W., Wendl M.C., Zhang Q.Y., Durbin R.M., Albers C.A., Ayub Q., Balasubramaniam S., Barrett J.C., Carter D.M. A map of human genome variation from population-scale sequencing. Nature 2010, 467:1061-1073.
9. Elson J.L., Samuels D.C., Turnbull D.M., Chinnery P.F. Random intracellular drift explains the clonal expansion of mitochondrial DNA mutations with age. Am. J. Hum. Genet. 2001, 68:802-806.
10. Goto H., Dickins B., Afgan E., Paul I.M., Taylor J., Makova K.D., Nekrutenko A. Dynamics of mitochondrial heteroplasmy in three families investigated via a repeatable re-sequencing study. Genome Biol. 2011, 12:R59.
11. Guo Y., Cai Q., Samuels D.C., Ye F., Long J., Li C.I., Winther J.F., Tawn E.J., Stovall M., Lahteenmaki P., Malila N., Levy S., Shaffer C., Shyr Y., Shu X.O., Boice J.D. The use of next generation sequencing technology to study the effect of radiation therapy on mitochondrial DNA mutation. Mutat. Res. 2012, 744:154-160.
12. Guo Y., Li J., Li C.I., Long J., Samuels D.C., Shyr Y. The effect of strand bias in Illumina short-read sequencing data. BMC Genomics 2012, 13:666.
13. Guo Y., Li J., Li C.I., Shyr Y., Samuels D.C. MitoSeek: extracting mitochondria information and performing high-throughput mitochondria sequencing analysis. Bioinformatics 2013, 29:1210-1211.
14. Holt I.J., Harding A.E., Petty R.K., Morgan-Hughes J.A. A new mitochondrial disease associated with mitochondrial DNA heteroplasmy. Am. J. Hum. Genet. 1990, 46:428-433.
15. Kann L.M., Rosenblum E.B., Rand D.M. Aging, mating, and the evolution of mtDNA heteroplasmy in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 1998, 95:2372-2377.
16. Koboldt D.C., Chen K., Wylie T., Larson D.E., McLellan M.D., Mardis E.R., Weinstock G.M., Wilson R.K., Ding L. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 2009, 25:2283-2285.
17. Lewis P.D., Baxter P., Paul Griffiths A., Parry J.M., Skibinski D.O. Detection of damage to the mitochondrial genome in the oncocytic cells of Warthin's tumour. J. Pathol. 2000, 191:274-281.
18. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
19. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
20. Li M., Schonberg A., Schaefer M., Schroeder R., Nasidze I., Stoneking M. Detecting heteroplasmy from high-throughput sequencing of complete human mitochondrial DNA genomes. Am. J. Hum. Genet. 2010, 87:237-249.
21. Li M., Stoneking M. A new approach for detecting low-level mutations in next-generation sequence data. Genome Biol. 2012, 13:R34.
22. Lombes A., Diaz C., Romero N.B., Ziegler F., Fardeau M. Analysis of the tissue distribution and inheritance of heteroplasmic mitochondrial DNA point mutation by denaturing gradient gel electrophoresis in MERRF syndrome. Neuromuscul. Disord. 1992, 2:323-330.
23. McKenna A., Hanna M., Banks E., Sivachenko A., Cibulskis K., Kernytsky A., Garimella K., Altshuler D., Gabriel S., Daly M., DePristo M.A. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010, 20:1297-1303.
24. Ng S.B., Buckingham K.J., Lee C., Bigham A.W., Tabor H.K., Dent K.M., Huff C.D., Shannon P.T., Jabs E.W., Nickerson D.A., Shendure J., Bamshad M.J. Exome sequencing identifies the cause of a Mendelian disorder. Nat. Genet. 2010, 42:30-35.
25. Park J.S., Sharma L.K., Li H., Xiang R., Holstein D., Wu J., Lechleiter J., Naylor S.L., Deng J.J., Lu J., Bai Y. A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Hum. Mol. Genet. 2009, 18:1578-1589.
26. Payne B.A., Wilson I.J., Yu-Wai-Man P., Coxhead J., Deehan D., Horvath R., Taylor R.W., Samuels D.C., Santibanez-Koref M., Chinnery P.F. Universal heteroplasmy of human mitochondrial DNA. Hum. Mol. Genet. 2013, 22:384-390.
27. Pereira L., Freitas F., Fernandes V., Pereira J.B., Costa M.D., Costa S., Maximo V., Macaulay V., Rocha R., Samuels D.C. The diversity present in 5140 human mitochondrial genomes. Am. J. Hum. Genet. 2009, 84:628-640.
28. Robin E.D., Wong R. Mitochondrial DNA molecules and virtual number of mitochondria per cell in mammalian cells. J. Cell. Physiol. 1988, 136:507-513.
29. Simon D.K., Friedman J., Breakefield X.O., Jankovic J., Brin M.F., Provias J., Bressman S.B., Charness M.E., Tarsy D., Johns D.R., Tarnopolsky M.A. A heteroplasmic mitochondrial complex I gene mutation in adult-onset dystonia. Neurogenetics 2003, 4:199-205.
30. Smigrodzki R.M., Khan S.M. Mitochondrial microheteroplasmy and a theory of aging and age-related disease. Rejuvenation Res. 2005, 8:172-198.
31. Sondheimer N., Glatz C.E., Tirone J.E., Deardorff M.A., Krieger A.M., Hakonarson H. Neutral mitochondrial heteroplasmy and the influence of aging. Hum. Mol. Genet. 2011, 20:1653-1659.
32. Stoneking M. Hypervariable sites in the mtDNA control region are mutational hotspots. Am. J. Hum. Genet. 2000, 67:1029-1032.
33. Tang S., Huang T. Characterization of mitochondrial DNA heteroplasmy using a parallel sequencing system. Biotechniques 2010, 48:287-296.
34. Tawn E.J., Rees G.S., Leith C., Winther J.F., Curwen G.B., Stovall M., Olsen J.H., Rechnitzer C., Schroeder H., Guldberg P., Boice J.D. Germline minisatellite mutations in survivors of childhood and young adult cancer treated with radiation. Int. J. Radiat. Biol. 2011, 87:330-340.
35. Tawn E.J., Whitehouse C.A., Winther J.F., Curwen G.B., Rees G.S., Stovall M., Olsen J.H., Guldberg P., Rechnitzer C., Schroder H., Boice J.D. Chromosome analysis in childhood cancer survivors and their offspring - no evidence for radiotherapy-induced persistent genomic instability. Mutat. Res. 2005, 583:198-206.
36. van Oven M., Kayser M. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum. Mutat. 2009, 30:E386-E394.
37. Wai T., Teoli D., Shoubridge E.A. The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat. Genet. 2008, 40:1484-1488.
38. Wong L.J., Wong H., Liu A. Intergenerational transmission of pathogenic heteroplasmic mitochondrial DNA. Genet. Med. 2002, 4:78-83.
39. Wonnapinij P., Chinnery P.F., Samuels D.C. The distribution of mitochondrial DNA heteroplasmy due to random genetic drift. Am. J. Hum. Genet. 2008, 83:582-593.
40. Wonnapinij P., Chinnery P.F., Samuels D.C. Previous estimates of mitochondrial DNA mutation level variance did not account for sampling error: comparing the mtDNA genetic bottleneck in mice and humans. Am. J. Hum. Genet. 2010, 86:540-550.
41. Yao Y.G., Kajigaya S., Feng X., Samsel L., McCoy J.P., Torelli G., Young N.S. Accumulation of mtDNA variations in human single CD34+ cells from maternally related individuals: effects of aging and family genetic background. Stem Cell Res. 2013, 10:361-370.