Molecular instability in the COII-tRNALys intergenic region of the human mitochondrial genome: Multiple origins of the 9-bp deletion and heteroplasmy for expanded repeats

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 353, Issue 1371, 1998, Pages 955-965

  Thomas, Mark G ^a,b   Cook, Charles E ^a,c   Miller, Kevin W P ^a,d   Waring, Michael J ^a   Hagelberg, Erika ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY MUSEUM OF ZOOLOGY   (United Kingdom)

^d North Louisiana Criminalistics Laboratory   (United States)

Author keywords

9 bp deletion; DNA binding drugs; Heteroplasmy; Human; mtDNA; Slipped strand mispairing

Indexed keywords

CRYSTAL VIOLET; CYTOCHROME OXIDASE II; DNA REPLICATION; EXPANDED REPEAT; GENE DELETION; GENETIC STABILITY; HETEROPLASMY; INTERGENIC REGION; LYSINE; MITOCHONDRIAL DNA; POLYMERASE CHAIN REACTION; TRANSFER RNA; UNITED KINGDOM;

VIOLA (ANGIOSPERM);

EID: 0032578022     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1998.0260     Document Type: Article

References (67)

1. Anderson, S. (and 13 others) 1981 Sequence and organization of the human mitochondrial genome. Nature 290, 457-465.
2. Ashley, M. V., Laipis, P. J. & Hauswirth, W. W. 1989 Rapid segregation of heteroplasmic bovine mitochondria. Nucl. Acids Res. 17, 7325-7331.
3. Bailliet, G., Rothhammer, F., Carnese, F. R., Bravi, C. M. & Bianchi, N. O. 1994 Founder mitochondrial haplotypes in Amerindian population. Am. J. Hum. Genet. 55, 27-33.
4. Ballinger, S.W., Schurr, T. G., Torroni, A., Gan, Y.Y., Hodge,J. A., Hassan, K., Chen, K. H. & Wallace, D. C. 1992 Southeast-Asian mitochondrial-DNA analysis reveals genetic continuity of ancient mongoloid migrations. Genetics 130, 139-152.
5. Behnkrappa, A. & Doerfler, W. 1994 Enzymatic amplification of synthetic oligodeoxyribonucleotides - implications for triplet repeat expansions in the human genome. Hum. Mutat. 3, 19-24.
6. Bendall, K. E. & Sykes, B. C. 1995 Length heteroplasmy in the first hypervariable segment of the human mtDNA control region. Am. J. Hum. Genet. 57, 248-256.
7. Bendall, K. E., Macaulay, V. A., Baker, J. R. & Sykes, B. C. 1996 Heteroplasmic point mutations in the human mtDNA control region. Am. J. Hum. Genet. 59, 1276-1287.
8. Cacerescortes,J. & Wang, A. H. J. 1996 Binding of the antitumor drug nogalamycin to bulged DNA structures. Biochemistry 35, 616-625.
9. Cann, R. L. 1994 MtDNA and native-Americans - a southern perspective. Am. J. Hum. Genet. 55, 7-11.
10. Casane, D., Dennebouy, N., de Rochambeau, H., Mounolou, J. C. & Monnerot, M. 1994 Genetic analysis of systematic mitochondrial heteroplasmy in rabbits. Genetics 138, 471-480.
11. Demarini, D. M., Abushakra, A., Gupta, R., Hendee, L. J. & Levine, J. G. 1992 Molecular analysis of mutations induced by the intercalating agent ellipticine at the hisd3052 allele of Salmonella-Typhimurium ta98. Environ. Molec. Mutag. 20, 12-18.
12. Felsenstein, J. 1975 Confidence limits on phytogenies: an approach using the bootstrap. Evolution 39, 783-791.
13. Felsenstein, J. 1995 PHYLIP: Phylogenetic Inference Package, version 3.57c. Distributed by author. Department of Genetics, University of Washington, Seattle, WA, USA.
14. Fumagalli, L., Taberlet, P. & Favre, L. H. J. 1996 Origin and evolution of homologous repeated sequences in the mitochondrial DNA control region of shrews. Molec. Biol. Evol. 13, 31-46.
15. Gale, E. F., Cundliffe, E., Reynolds, P. E., Richmond, M. H. & Waring, M. J. 1981 The molecular basis of antibiotic action, 2nd edn. London: Wiley.
16. Genetics Computer Group 1994 Program manual for the Wisconsin Package. Madison, WI: Genetics Computer Group.
17. Grcenblatt, M. S., Grollman, A. P. & Harris, C. C. 1996 Deletions and insertions in the p53 tumor-suppressor gene in human cancers-confirmation of the DNA-polymerase slippage misalignment model. Cancer Res. 56, 2130-2136.
18. Hagelberg, E. & Clegg, J. B. 1993 Genetic polymorphisms in prehistoric Pacific Islanders determined by analysis of ancient bone DNA. Proc. R. Soc. Lond. B 252, 163-170.
19. Hagelberg, E., Quevedo, S., Turbon, D. & Clegg, J. B. 1994 DNA from ancient Easter-islanders. Nature 369, 25-26.
20. Harihara, S., Hirai, M., Suutou, Y., Shimizu, K. & Omoto, K. 1992 Frequency of a 9-bp deletion in the mitochondrial DNA among Asian populations. Hum. Biol. 64, 161-166.
21. Harrison, R. G., Rand, D. M. & Wheeler, W. C. 1985 Mitochondrial DNA size variation within individual crickets. Science 228, 1446-1448.
22. Hertzberg, M., Mickleson, K. N. P., Serjeantson, S. W., Prior, J. F. & Trent, R. J. 1989 An Asian-specific 9-bp deletion of mitochondrial DNA is frequently found in Polynesians. Am. J. Hum. Genet. 44, 504-510.
23. Hoelzel, A. R., Hancock, J. M. & Dover, G. A. 1991 Evolution of the cetacean mitochondrial D-loop region. Molec. Biol. Evol. 8, 475-493.
24. Hoelzel, A. R., Lopez, J.V., Dover, G. A. & O'Brien, S. J. 1994 Rapid evolution of a heteroplasmic repetitive sequence in the mitochondrial-DNA control region of carnivores. J. Molec. Evol. 39, 191-199.
25. Horai, S., Kondo, R., Nakagawahattori, Y., Hayashi, S., Sonoda, S. & Tajima, K. 1993 Peopling of the America, founded by 4 major lineages of mitochondrial-DNA. Molec. Biol. Evol. 10, 23-47.
26. Horai, S., Hayasaka, K., Kondo, R.,Tsugane, K. & Takahata, N. 1995 Recent African origin of modern humans revealed by complete sequences of hominoid mitochondrial DNAs. Proc. Natn. Acad. Sci. USA 92, 532-536.
27. Imada, M., Inouye, M., Eda, M. & Tsugita, A. 1970 Frameshift mutation in the lysozyme gene of bacteriophage T4: demonstration of the insertion of four bases and the preferential occurrence of base addition in acridine mutagenesis. J. Molec. Biol. 54, 199-217.
28. Ivanov, P. L., Wadhams, M. J., Roby, R. K., Holland, M. M., Weedn, V. W. & Parsons, T. J. 1996 Mitochondrial DNA sequence heteroplasmy in the Grand Duke of Russia Georgij Romanov establishes the authenticity of the remains of Tsar Nicholas II. Nat. Genet. 12, 417-420.
29. Jenuth, J. P., Peterson, A. C., Fu, K. & Shoubridge, E. A. 1996 Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nat. Genet. 14, 146-151.
30. Kimura, M. 1980 A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequence. J. Molec. Evol. 16, 111-120.
31. Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S.V., Pääbo, S., Villabianca, F. X. & Wilson, A. C. 1989 Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natn. Acad. Sci. USA 86, 6196-6200.
32. Levinson, G. & Gutman, G. A. 1987 Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Molec. Biol. Evol. 4, 203-221.
33. Lum, K. J., Rickards, O., Ching, C. & Cann, R. L. 1994 Polynesian mitochondrial DNAs reveal three deep maternal lineage clusters. Hum. Biol. 66, 567-590.
34. Marchington, D. R., Hartshorne, G. M., 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, 408-416.
35. Melton, T., Peterson, R., Redd, A. J., Saha, N., Sofro, A. S. M., Martinson, J. & Stoneking, M. 1995 Polynesian genetic affinities with Southeast Asian populations as identified by mtDNA analysis. Am. J. Hum. Genet. 57, 403-414.
36. Merriwether, D. A., Rothhammer, F. & Ferrell, R. E. 1994 Genetic-variation in the new-world - ancient teeth, bone, and tissue as sources of DNA. Experientia 50, 592-601.
37. Monsalve, M. V., Derestrepo, H. G., Espinel, A., Correal, G. & Devine, D. V. 1994 Evidence of mitochondrial-DNA diversity in South-American aboriginals. Ann. Hum. Genet. 58, 265-273.
38. Nei, M. & Li, W.-H. 1979 Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natn. Acad. Sci. USA 76, 5269-5273.
39. Passarino, G., Semino, O., Modiano, G. & Santachiarabenerecetti, A. S. 1993 COII transfer RNA(lys) intergenic 9-bp deletion and other mtDNA markers clearly reveal that the Tharus (southern Nepal) have oriental affinities. Am. J. Hum. Genet. 53, 609-618.
40. Piercy, R., Sullivan, K. M., Benson, N. & Gill, P. 1993 The application of mitochondrial DNA typing to the study of white Caucasian genetic identification. Int. J. Legal Med. 106, 85-90.
41. Piko, L. & Matsumoto, L. 1976 Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev. Biol. 49, 1-10.
42. Redd, A. J., Takezaki, N., Sherry, S.T., Megarvey, S.T., Sofro, A. & Stoneking, M. 1995 Evolutionary history of the COII-tRNA(lys) intergenic 9-base-pair deletion in human mitochondrial DNAs from the Pacific. Molec. Biol. Evol. 12, 604-615.
43. Rentzeperis, D., Medero, M. & Marky, L. A. 1995 Thermodynamic investigation of the association of ethidium, propidium and bis-ethidium to DNA hairpins. Bioorg. Med. Chem. 3, 751-759.
44. Richards, R. I. & Sutherland, G. R. 1994 Simple repeat DNA is not replicated simply. Nat. Genet. 6, 14-16.
45. Rosche, W. A., Trinh, T. Q. & Sinden, R. R. 1995 Differential DNA secondary structure-mediated deletion mutation in the leading and lagging strands. J. Bacteriol. 177, 4385-4391.
46. Schurr, T. G., Ballinger, S. W., Gan, Y. Y., Hodge, J. A., Merriwether, D. A., Lawrence, D. N., Knowler, W. C., Weiss, K. M. & Wallace, D. C. 1990 Amerindian mitochondrial DNAs have rare Asian mutations at high-frequencies, suggesting they derived from 4 primary maternal lineages. Am. J. Hum. Genet. 46, 613-623.
47. Shields, G. F., Hecker, K., Voevoda, M. I. & Reed, J. K. 1992 Absence of the Asian-specific region-V mitochondrial marker in native Beringians. Am. J. Hum. Genet. 50, 758-765.
48. Soodyall, H., Jenkins, T. & Stoneking, M. 1995 Polynesian mtDNA in the Malagasy. Nat. Genet. 10, 377-378.
49. Soodyall, H., Vigilant, L., Hill, A. V., Stoneking, M. & Jenkins, T. 1996 MtDNA control-region sequence variation suggests multiple independent origins of an Asian-specific 9-bp deletion in sub-Saharan Africans. Am. J. Hum. Genet. 58, 595-608.
50. Stoneking, M., Sherry, S.T., Redd, A. J. & Vigilant, L. 1992 New approaches to dating suggest a recent age for the human mtDNA ancestor. Phil. Trans. R. Soc. Lond. B 337, 167-175.
51. Streisinger, G., Okada, Y., Emrich, J., Newton, J., Tsugita, J., Terzaghi, E. & Inouye, M. 1966 Frameshift mutations and the genetic code. Cold Spring Harb. Symp. Quant. Biol. 31, 77-84.
52. Sykes, B., Leiboff, A., Lowbeer, J., Tetzner, S. & Richards, M. 1995 The origins of the Polynesians - an interpretation from mitochondrial lineage analysis. Am. J. Hum. Genet. 57, 1463-1475.
53. Thomas, M. G., Miller, K., Cook, C. E. & Hagelberg, E. 1994 A method for avoiding mis-priming when sequencing with dynabeads. Nucl. Acids Res. 22, 3243-3244.
54. Thomas, M. G., Hesse, S. A., Foss.Y. J. & Farzaneh, F. 1996 The use of PCR for differential screening of cDNA libraries. In Preparative PCR: protocols for molecular cloning and genetic engineering (ed. B. White), ch. 39 pp. 405-418. Totowa, NJ: Humana.
55. Torroni, A. (and 10 others) 1992 Native-American mitochondrial-DNA analysis indicates that the Amerind and the Nadene populations were founded by two independent migrations. Genetics 130, 153-162.
56. Torroni, A., Schurr, T. G., Cabell, M. F., Brown, M. D., Neel, J.V., Larsen, M., Smith, D. G., Vullo, C. M. & Wallace, D. C. 1993a Asian affinities and continental radiation of the 4 founding Native-American mtDNAs. Am. J. Hum. Genet. 53, 563-590.
57. Tbrroni, A., Sukernik, R. I., Schurr, T. G., Starikovskaya, Y. B., Cabell, M. F., Crawford, M. H., Comuzzie, A. G. & Wallace, D. C. 1993b MtDNA variation of aboriginal Siberians reveals distinct genetic affinities with native-Americans. Am. J. Hum. Genet. 53, 591-608.
58. Torroni, A., Petrozzi, M., Santolamazza, P., Sellitto, D., Cruciani, F. & Scozzari, R. 1995 About the 'Asian'-specific 9-bp deletion of mtDNA. Am. J. Hum. Genet. 57, 507-508.
59. Tran, H. T., Degtyareva, N. P., Koloteva, N. N., Sugino, A., Masumoto, H., Gordenin, D. A. & Resnick, M. A. 1995 Replication slippage between distant short repeats in Saccharomyces-cerevisiae depends on the direction of replication and the rad50 and rad52 genes. Molec. Cell Biol. 15, 5607-5617.
60. Tuite, E. & Norden, B. 1995 Intercalative interactions of ethidium dyes with triplex structures. Bioorg. Med. Chem. 3, 701-711.
61. Vigilant, L. 1990 Control region sequences from African populations and the evolution of human mitochondrial DNA. PhD thesis, University of California, Berkeley, CA, USA.
62. Wakelin, L. P. G., Adams, A., Hunter, C. & Waring, M. J. 1981 Interaction of crystal violet with nucleic acids. Biochemistry 20, 5779-5787.
63. Wallace, D. C. & Torroni, A. 1992 American-Indian prehistory as written in the mitochondrial-DNA - a review. Hum. Biol. 64, 403-416.
64. Wilkinson, G. S. & Chapman, A. M. 1991 Length and sequence variation in evening bat D-loop mtDNA. Genetics 128, 607-617.
65. Wrischnik, L. A., Higuchi, R. G., Stoneking, M., Erlich, H., Arnheim, N. & Wilson, A. C. 1987 Length mutations in human mitochondrial DNA: direct sequencing of enzymatically amplified DNA. Nucl. Acids Res. 15, 529-542.
66. Zharkikh, A. & Li, W. H. 1992 Statistical properties of bootstrap estimation of phylogenetic variability from nucleotide-sequences. 1. 4 taxa with a molecular clock. Molec. Biol. Evol. 9, 1119-1147.
67. Zhou, B.W., Puga, E., Sun, J. S., Garestier, T. & Helene, C. 1995 Stable triple helices formed by acridine-containing oligonucleotides with oligopurine tracts of DNA interrupted by one or 2 pyrimidines. J. Am. Chem. Soc. 117, 10 425-10 428.