Evidence for adaptive selection acting on the tRNA and rRNA genes of human mitochondrial DNA

Human Mutation

Volumn 27, Issue 11, 2006, Pages 1072-1081

  Ruiz Pesini, Eduardo ^a,b   Wallace, Douglas C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

Adaptive selection; Diseases; Evolutionary constraints; Evolutionary medicine; Mitochondrial DNA; Mitochondrial medicine; Polymorphisms; Purifying selection; rRNAs; tRNAs

Indexed keywords

MITOCHONDRIAL DNA; RIBOSOME RNA; TRANSFER RNA;

ARTICLE; BASE PAIRING; DNA POLYMORPHISM; DNA SEQUENCE; DNA STRUCTURE; GENE MUTATION; GENETIC SELECTION; HUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANIMALS; BASE SEQUENCE; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENES, RRNA; HUMANS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PRIMATES; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 16S; RNA, TRANSFER; SELECTION (GENETICS); VARIATION (GENETICS);

EID: 33750927660     PISSN: 10597794     EISSN: None     Source Type: Journal    
DOI: 10.1002/humu.20378     Document Type: Article

References (45)

1. Achilli A, Rengo C, Magri C, Battaglia V, Olivieri A, Scozzari R, Cruciani F, Zeviani M, Briem E, Carelli V, Moral P, Dugoujon JM, Roostalu U, Loogvali EL, Kivisild T, Bandelt HJ, Richards M, Villems R, Santachiara- Benerecetti AS, Semino O, Torroni A. 2004. The molecular dissection of mtDNA haplogroup H confirms that the Franco-Cantabrian glacial refuge was a major source for the European gene pool. Am J Hum Genet 75:910-918.
2. Burk A, Douzery EJP, Springer MS. 2002. The secondary structure of mammalian mitochondrial 16S rRNA molecules: refinements based on a comparative phylogenetic approach. J Mammal Evol 9:225-252.
3. Cann RL, Stoneking M, Wilson AC. 1987. Mitochondrial DNA and human evolution. Nature 325:31-36.
4. Coble MD, Just RS, O'Callaghan JE, Letmanyi IH, Peterson CT, Irwin JA, Parsons TJ. 2004. Single nucleotide polymorphisms over the entire mtDNA genome that increase the power of forensic testing in Caucasians. Int J Legal Med 118:137-146.
5. Crimi M, Del Bo R, Galbiati S, Sciacco M, Bordoni A, Bresolin N, Comi GP. 2003. Mitochondrial A12308G polymorphism affects clinical features in patients with single mtDNA macrodeletion. Eur J Hum Genet 11:896-898.
6. Finnila S, Autere J, Lehtovirta M, Hartikainen P, Mannermaa A, Soininen H, Majamaa K. 2001. Increased risk of sensorineural hearing loss and migraine in patients with a rare mitochondrial DNA variant 4336A>G in tRNAGln. J Med Genet 38: 400-405.
7. Fischel-Ghodsian N, Prezant TR, Bu X, Oztas S. 1993. Mitochondrial ribosomal RNA gene mutation in a patient with sporadic aminoglycoside ototoxicity. Am J Otolaryngol 14: 399-403.
8. Florentz C, Sissler M. 2001. Disease-related versus polymorphic mutations in human mitochondrial tRNAs. Where is the difference? EMBO Rep 2:481-486.
9. Hamasaki K, Rando RR. 1997. Specific binding of aminoglycosides to a human rRNA construct based on a DNA polymorphism which causes aminoglycoside-induced deafness. Biochemistry 36:12323-12328.
10. Hattori Y, Goto Y, Sakuta R, Nonaka I, Mizuno Y, Horai S. 1994. Point mutations in mitochondrial tRNA genes: sequence analysis of chronic progressive external ophthalmoplegia (CPEO). J Neurol Sci 125:50-55.
11. Helm M, Brule H, Friede D, Giege R, Putz D, Florentz C. 2000. Search for characteristic structural features of mammalian mitochondrial tRNAs. RNA 6:1356-1379.
12. Herrnstadt C, Elson JL, Fahy E, Preston G, Turnbull DM, Anderson C, Ghosh SS, Olefsky JM, Beal MF, Davis RE, Howell N. 2002. Reduced-median-network analysis of complete mitochondrial DNA coding-region sequences for the major African, Asian, and European haplogroups. Am J Hum Genet 70: 1152-1171.
13. Hutchin T, Haworth I, Higashi K, Fischel-Ghodsian N, Stoneking M, Saha N, Arnos C, Cortopassi G. 1993. A molecular basis for human hypersensitivity to aminoglycoside antibiotics. Nucleic Acids Res 21:4174-4179.
14. Hutchin T, Cortopassi G. 1995. A mitochondrial DNA clone is associated with increased risk for Alzheimer disease. Proc Natl Acad Sci USA 92:6892-6895.
15. Kern AD, Kondrashov FA. 2004. Mechanisms and convergence of compensatory evolution in mammalian mitochondrial tRNAs. Nat Genet 36:1207-1212.
16. Kivisild T, Shen P Wall DP, Do B, Sung R, Davis KK, Passarino G, Underhill PA, Scharfe C, Torroni A, Scozzari R, Modiano D, Coppa A, de Knijff P, Feldman M, Cavalli-Sforza LL, Oefher PJ. 2006. The role of selection in the evolution of human mitochondrial genomes. Genetics 172:373-387.
17. Kofoed CB, Vester B. 2002. Interaction of avilamycin with ribosomes and resistance caused by mutations in 23S rRNA. Antimicrob Agents Chemother 46:3339-3342.
18. Kondrashov FA. 2005. Prediction of pathogenic mutations in mitochondrially encoded human tRNAs. Hum Mol Genet 14: 2415-2419.
19. Kong QP, Yao YG, Sun C, Bandelt HJ, Zhu CL, Zhang YP. 2003. Phylogeny of East Asian mitochondrial DNA lineages inferred from complete sequences. [Erratum: Am J Hum Genet 75:157, 2004]. Am J Hum Genet 73:671-676.
20. Loogvali EL, Roostalu U, Malyarchuk BA, Derenko MV, Kivisild T, Metspalu E, Tambets K, Reidla M, Tolk HV, Parik J, Pennarun E, Laos S, Lunkina A, Golubenko M, Barac L, Pericic M, Balanovsky OP, Gusar V, Khusnutdinova EK, Stepanov V, Puzyrev V, Rudan P, Balanovska EV, Grechanina E, Richard C, Moisan JP, Chaventre A, Anagnou NP, Pappa KI, Michalodimitrakis EN, Claustres M, Golge M, Mikerezi J, Usanga E, Villems R. 2004- Disuniting uniformity: a pied cladistic canvas of mtDNA haplogroup H in Eurasia. Mol Biol Evol 21: 2012-2021.
21. Lynch M. 1996. Mutation accumulation in transfer RNAs: molecular evidence for Muller's ratchet in mitochondrial genomes. Mol Biol Evol 13:209-220.
22. McFarland R, Elson JL, Taylor RW, Howell N, Turnbull DM. 2004. Assigning pathogenicity to mitochondrial tRNA mutations: when "definitely maybe" is not good enough. Trends Genet 20:591-596.
23. Mishmar D, Ruiz-Pesini EE, Golik P, Macaulay V, Clark AG, Hosseini S, Brandon M, Easley K, Chen E, Brown MD, Sukernik RI, Olckers A, Wallace DC. 2003. Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci USA 100:171-176.
24. Montiel-Sosa F, Ruiz-Pesini E, Enríquez JA, Marcuello A, Díez-Sânchez C, Montoya J, Wallace DC, López-Pérez MJ. 2006. Differences of sperm motility in mitochondrial DNA haplogroup U sublineages. Gene 368:21-27.
25. Neckelmann N, Li K, Wade RP, Shuster R, Wallace DC. 1987. cDNA sequence of a human skeletal muscle ADP/ATP translocator: lack of a leader peptide, divergence from a fibroblast translocator cDNA, and coevolution with mitochondrial DNA genes. Proc Natl Acad Sci USA 84:7580-7584.
26. Neckelmann N, Warner CK, Chung A, Kudoh J, Minoshima S, Fukuyama R, Maekawa M, Shimizu Y, Shimizu N, Liu JD, Wallace DC. 1989. The human ATP synthase beta subunit gene: sequence analysis, chromosome assignment, and differential expression. Genomics 5:829-843.
27. Palanichamy MG, Sun C, Agrawal S, Bandelt HJ, Kong QP, Khan F, Wang CY, Chaudhuri TK, Palla V, Zhang YP. 2004. Phylogeny of mitochondrial DNA macrohaplogroup N in India, based on complete sequencing: implications for the peopling of South Asia. Am J Hum Genet 75:966-978.
28. Prezant TR, Agapian JV, Bohlman MC, Bu X, Oztas S, Qiu WQ, Arnos KS, Cortopassi GA, Jaber L, Rotter JI, Shohat M, Fischel-Ghodsin M. 1993. Mitochondrial ribosomal RNA mutation associated with both antibiotic-induced and non-syndromic deafness. Nat Genet 4:289-294.
29. Rose G, Passarino G, Carrieri G, Altomare K, Greco V, Bertolini S, Bonafe M, Franceschi C, De Benedictis G. 2001. Paradoxes in longevity: sequence analysis of mtDNA haplogroup J in centenarians. Eur J Hum Genet 9:701-707.
30. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC. 2004. Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303:223-226.
31. Santorelli FM, Schlessel JS, Slonim AE, DiMauro S. 1996. Novel mutation in the mitochondrial DNA tRNA glycine gene associated with sudden unexpected death. Pediatr Neurol 15: 145-149.
32. Lys mutation. Cell 61:931-937.
33. Shoffner JM, Brown MD, Torroni A, Lott MT, Cabell MR, Mirra SS, Beal MF, Yang C, Gearing M, Salvo R, Watts RL, Juncos JL, Hansen LA, Crain BJ, Fayad M, Reckford CL, Wallace DC. 1993. Mitochondrial DNA variants observed in Alzheimer disease and Parkinson disease patients. Genomics 17:171-184.
34. Sonneborn JS. 2005. The myth and reality of reversal of aging by hormesis. Ann NY Acad Sci 1057:165-176.
35. Springer MS, Douzery E. 1996. Secondary structure and patterns of evolution among mammalian mitochondrial 12S rRNA molecules. J Mol Evol 43:357-373.
36. Thyagarajan D, Bressman S, Bruno C, Przedborski S, Shanske S, Lynch T, Fahn S, DiMauro S. 2000. A novel mitochondrial 12SrRNA point mutation in parkinsonism, deafness, and neuropathy. Ann Neurol 48:730-736.
37. Tomari Y, Hino N, Nagaike T, Suzuki T, Ueda T. 2003. Decreased CCA-addition in human mitochondrial tRNAs bearing a pathogenic A4317G or A10044G mutation. J Biol Chem 278: 16828-16833.
38. Vilmi T, Moilanen JS, Finnila S, Majamaa K. 2005. Sequence variation in the tRNA genes of human mitochondrial DNA. J Mol Evol 60:587-597.
39. Wallace DC, Ye JH, Neckelmann SN, Singh G, Webster KA, Greenberg BD. 1987. Sequence analysis of cDNAs for the human and bovine ATP synthase β-subunit: mitochondrial DNA genes sustain seventeen times more mutations. Curr Genet 12:81-90.
40. Wallace DC, Zheng X, Lott MT, Shoffner JM, Hodge JA, Kelley RI, Epstein CM, Hopkins LC. 1988. Familial mitochondrial encephalomyopathy (MERRF): genetic, pathophysiological, and biochemical characterization of a mitochondrial DNA disease. Cell 55:601-610.
41. Wallace DC, Ruiz-Pesini E, Mishmar D. 2003. mtDNA variation, climatic adaptation, degenerative diseases, and longevity. Cold Spring Harb Symp Quant Biol 68:479-486.
42. Wallace DC. 2005. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359-407.
43. Wang Q, Li R, Zhao H, Peters JL, Liu Q, Yang L, Han D, Greinwald JH Jr, Young WY, Guan MX. 2005. Clinical and molecular characterization of a Chinese patient with auditory neuropathy associated with mitochondrial 12S rRNA T1095C mutation. Am J Med Genet 133A:27-30.
44. Zhao H, Li R, Wang Q, Yan Q, Deng JH, Han D, Bai Y, Young WY, Guan MX. 2004a. Maternally inherited aminoglycoside-induced and nonsyndromic deafness is associated with the novel C1494T mutation in the mitochondrial 12S rRNA gene in a large Chinese family. Am J Hum Genet 74:139-152.
45. Zhao L, Young WY, Li R, Wang Q, Qian Y, Guan MX. 2004b. Clinical evaluation and sequence analysis of the complete mitochondrial genome of three Chinese patients with hearing impairment associated with the 12S rRNA T1095C mutation. Biochem Biophys Res Commun 325:1503-1508.