Evidence for balancing selection from nucleotide sequence analyses of human G6PD

American Journal of Human Genetics

Volumn 71, Issue 5, 2002, Pages 1112-1128

  Verrelli, Brian C ^a   McDonald, John H ^b   Argyropoulos, George ^c   Destro Bisol, Giovanni ^d   Froment, Alain ^e   Drousiotou, Anthi ^f   Lefranc, Gerard ^g   Helal, Ahmed N ^h   Loiselet, Jacques ⁱ   Tishkoff, Sarah A ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e IRD Centre d'Orleans   (France)

^f CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^g Inst Sci l'Evol Univ Sci T   (France)

^h UNIVERSITY OF MONASTIR   (Tunisia)

ⁱ SAINT JOSEPH UNIVERSITY   (Lebanon)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE 6 PHOSPHATE DEHYDROGENASE;

ALLELE; ARTICLE; ENZYME ACTIVITY; ENZYME DEFICIENCY; EVOLUTION; GENE LINKAGE DISEQUILIBRIUM; GENE MUTATION; GENE TARGETING; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HUMAN; HUMAN CELL; MALARIA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS;

PAN TROGLODYTES;

EID: 0036842917     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1086/344345     Document Type: Article

References (79)

1. Anderson TJ, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP (2000) Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 17:1467-1482
2. Aquadro CF, Bauer DuMont V, Reed FA (2001) Genome-wide variation in the human and fruitfly: A comparison. Curr Opin Genet Dev 11:627-634
3. Begun DJ, Aquadro CF (1993) African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365:548-550
4. Berry AJ, Kreitman M (1993) Molecular analysis of an allozyme cline: Alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. Genetics 134:869-893
5. Beutler E (1994) G6PD deficiency. Blood 84:3613-3636
6. Beutler E, Westwood B, Kuhl W, Hsia YE (1992) Glucose-6-phosphate dehydrogenase variants in Hawaii. Hum Hered 42:327-329
7. Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W (1995) The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140:783-796
8. Cavalli-Sforza LL, Menozzi P, Piazza A (1996) The History and Geography of Human Genes. Princeton University Press, Princeton, NJ
9. Chang J-G, Chiou S-S, Perng L-I, Chen T-C, Liu T-C, Lee L-S, Chen P-H, Tang T-K (1992) Molecular characterization of glucose-6-phosphate dehydrogenase (G6PD) deficiency by natural and amplification created restriction sites: Five mutations account for most G6PD deficiency cases in Taiwan. Blood 80:1079-1082
10. Clark AG, Weiss KM, Nickerson DA, Taylor SL, Buchanan A, Stengård J, Salomaa V, Vartiainen E, Perola M, Boerwinkle E, Sing CF (1998) Haplotype structure and population genetic inferences from nucleotide sequence variation in human lipoprotein lipase. Am J Hum Genet 63:595-612
11. Cooke GS, Hill AVS (2001) Genetics of susceptibility to human infectious disease. Nat Rev Genet 2:967-977
12. Deeb SS, Lindsey DT, Hibiya Y, Sanocki E, Winderickx J, Teller DY, Motulsky AG (1992) Genotype-phenotype relationships in human red/green color-vision defects: Molecular and psychophysical studies. Am J Hum Genet 51:687-700
13. Deinard AS, Kidd KK (2000) Identifying conservation units within captive chimpanzee populations. Am J Phys Anthropol 111:25-44
14. Donnelly MJ, Licht MC, Lehmann T (2001) Evidence for recent population expansion in the evolutionary history of the malaria vectors Anopheles arabiensis and Anopheles gambiae. Mol Biol Evol 18:1353-1364
15. Ebersberger I, Metzler D, Schwarz C, Pääbo S (2002) Genomewide comparison of DNA sequences between humans and chimpanzees. Am J Hum Genet 70:1490-1497
16. Fay JC, Wyckoff GJ, Wu C-I (2001) Positive and negative selection on the human genome. Genetics 158:1227-1234
17. Fullerton SM, Clark AG, Weiss KM, Nickerson DA, Taylor SL, Stengård JH, Salomaa V, Vartiainen E, Perola M, Boerwinkle E, Sing CF (2000) Apolipoprotein E variation at the sequence haplotype level: Implications for the origin and maintenance of a major human polymorphism. Am J Hum Genet 67:881-900
18. Ganczakowski M, Town M, Bowden DK, Vulliamy TJ, Kaneko A, Clegg JB, Weatherall DJ, Luzzatto L (1995) Multiple glucose-6-phosphate dehydrogenase-deficient variants correlate with malaria endemicity in the Vanuatu Archipelago (southwestern Pacific). Am J Hum Genet 56:294-301
19. Greenwood B, Mutabingwa T (2002) Malaria in 2002. Nature 415:670-672
20. Griffiths RC, Tavare S (1997) Computational methods for the coalescent. In: Donnelly P, Tavare S (eds) Progress in Population Genetics and Human Evolution. Springer-Verlag, New York, pp 165-182
21. Hamblin MT, Thompson EE, Di Rienzo A (2002) Complex signatures of natural selection at the Duffy blood group locus. Am J Hum Genet 70:369-383
22. Harding RM, Fullerton SM, Griffiths RC, Bond J, Cox MJ, Schneider JA, Moulin DS, Clegg JB (1997) Archaic African and Asian lineages in the genetic ancestry of modern humans. Am J Hum Genet 60:772-789
23. Harding RM, Healy E, Ray AJ, Ellis NS, Flanagan N, Todd C, Dixon C, Sajantila A, Jackson IJ, Birch-Machin MA, Rees JL (2000) Evidence for variable selective pressures at MC1R. Am J Hum Genet 66:1351-1361
24. Harris EE, Hey J (1999) X chromosome evidence for ancient human histories. Proc Natl Acad Sci USA 96:3320-3324
25. _ (2001) Human populations show reduced DNA sequence variation at the Factor IX locus. Curr Biol 11:774-778
26. Hey J (1997) Mitochondrial and nuclear genes present conflicting portraits of human origins. Mol Biol Evol 14:166-172
27. Hey J, Harris EE (1999) Population bottlenecks and patterns of human polymorphism. Mol Biol Evol 16:1423-1426
28. Hoffman SL, Subramanian GM, Collins FH, Venter JC (2002) Plasmodium, human and Anopheles genomics and malaria. Nature 415:702-709
29. Horai S, Satta Y, Hayasaka K, Kondo R, Inoue T, Ishida T, Hayashi S, Takahata N (1992) Man's place in Hominoidea revealed by mitochondrial DNA genealogy. J Mol Evol 35:32-43
30. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011-2014
31. Hudson RR, Bailey K, Skarecky D, Kwiatowski J, Ayala FJ (1994) Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics 136:1329-1340
32. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164
33. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159
34. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583-589
35. Jaruzelska J, Zietkiewicz E, Batzer M, Cole DEC, Moisan J-P, Scozzari R, Tavare S, Labuda D (1999) Spatial and temporal distribution of the neutral polymorphisms in the last ZFX intron: Analysis of the haplotype structure and genealogy. Genetics 152:1091-1101
36. Jorde LB, Rogers AR, Bamshad M, Watkins WS, Krakowiak P, Sung S, Kere J, Harpending HC (1997) Microsatellite diversity and the demographic history of modern humans. Proc Natl Acad Sci USA 94:3100-3103
37. Kaeda JS, Chhotray GP, Ranjit MR, Bautista JM, Reddy PH, Stevens D, Naidu JM, Britt RP, Vulliamy TJ, Luzzatto L, Mason PJ (1995) A new glucose-6-phosphate dehydrogenase variant, G6PD Orissa (44 Ala→Gly), is the major polymorphic variant in tribal populations in India. Am J Hum Genet 57:1335-1341
38. Kaessmann H, Wiebe V, Weiss G, Pääbo S (2001) Great ape DNA sequences reveal a reduced diversity and an expansion in humans. Nat Genet 27:155-156
39. Kay AC, Kuhl W, Prchal JT, Beutler E (1992) The origin of glucose-6-phosphate dehydrogenase (G6PD) polymorphisms in Afro-Americans. Am J Hum Genet 50:394-398
40. Kidd JR, Pakstis AJ, Zhao H, Lu R-B, Okonofua FE, Odunsi A, Grigorenko E, Batsheva B-T, Friedlaender J, Schulz LO, Parnas J, Kidd KK (2000) Haplotypes and linkage disequilibrium at the phenylalanine hydroxylase locus, PAH, in a global representation of populations. Am J Hum Genet 66:1882-1899
41. Koda Y, Tachida H, Pang H, Liu Y, Soejima M, Ghaderi AA, Takenaka O, Kimura H (2001) Contrasting patterns of polymorphisms at the ABO-secretor gene (FUT2) and plasma α(1,3)fucosyltransferase gene (FUT6) in human populations. Genetics 158:747-756
42. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis Software, Arizona State University, Tempe, AZ
43. Livingstone FB (1971) Malaria and human polymorphisms. Annu Rev Genet 5:33-64
44. Luzzatto L, Mehta A, Vulliamy TJ (2001) In: Scriver CR, Beaudet AL, Sly WS, Valle D (eds) The Metabolic and Molecular Bases of Inherited Disease. McGraw-Hill, New York, pp 4517-4553
45. Martin MP, Dean M, Smith MW, Winkler C, Gerrard B, Michael NL, Lee B, Doms RW, Margolick J, Buchbinder S, Goedert JJ, O'Brien TR, Hilgartner MW, Vlahov D, O'Brien SJ, Carrington M (1998) Genetic acceleration of AIDS progression by a promoter variant at CCR5. Science 282:1907-1911
46. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654
47. Miller LH (1994) Impact of malaria on genetic polymorphism and genetic diseases in Africans and African Americans. Proc Natl Acad Sci USA 91:2415-2419
48. Miller LH, Baruch DI, Marsh K, Doumbo OK (2002) The pathogenic basis of malaria. Nature 415:673-679
49. Mu J, Duan J, Makova KD, Joy DA, Huynh CQ, Branch OH, Li WH, Su XZ (2002) Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature 18:323-326
50. Nachman MW (2001) Single nucleotide polymorphisms and recombination rate in humans. Trends Genet 17:481-485
51. Nachman MW, Brown WM, Stoneking M, Aquadro CF (1996) Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 142:953-963
52. Nachman MW, Crowell SL (2000) Contrasting evolutionary histories of two introns of the Duchenne muscular dystrophy gene, Dmd, in humans. Genetics 155:1855-1864
53. Nathans J, Thomas D, Hogness DS (1986) Molecular genetics of human color vision: The genes encoding blue, green, and red pigments. Science 232:193-202
54. Nielsen R, Weinreich DM (1999) The age of nonsynonymous and synonymous mutations in animal mtDNA and implications for the mildly deleterious theory. Genetics 153:497-506
55. Ohta T (1992) The nearly neutral theory of molecular evolution. Ann Rev Ecol Syst 23:263-286
56. Ollomo B, Karch S, Bureau P, Elissa N, Georges AJ, Millet P (1997) Lack of malaria parasite transmission between apes and humans in Gabon. Am J Trop Med Hyg 56:440-445
57. Przeworski M, Hudson RR, Di Rienzo A (2000) Adjusting the focus on human variation. Trends Genet 16:296-302
58. Rozas J, Rozas R (1999) DnaSP version 3: An integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175
59. Ruwende C, Khoo SC, Snow RW, Yates SNR, Kwiatkowski D, Gupta S, Warn P, Allsopp CEM, Gilbert SC, Peschu N, Newbold CI, Greenwood BM, Marsh K, Hill AVS (1995) Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 376:246-249
60. Salamon H, Klitz W, Easteal S, Gao X, Erlich HA, Fernandez-Vina M, Trachtenburg EA, McWeeney SK, Nelson MP, Thomson G (1999) Evolution of HLA class II molecules: Allelic and amino acid site variability across populations. Genetics 152:393-400
61. Saunders MA, Hammer MF, Nachman MW. Nucleotide variability at G6PD and the signature of malarial selection in humans. Genetics (in press)
62. Simonsen KL, Churchill GA, Aquadro CF (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141:413-429
63. Slatkin M, Rannala B (1997) Estimating the age of alleles by use of intraallelic variability. Am J Hum Genet 60:447-458
64. Smirnova I, Hamblin MT, McBride C, Beutler B, Di Rienzo A (2001) Excess of rare amino acid polymorphisms in the Toll-like receptor 4 in humans. Genetics 158:1657-1664
65. Sokal RR, Rohlf FJ (1995) Biometry. W. H. Freeman, San Francisco
66. Stephens JC, Reich DE, Goldstein DB, Shin HD, Smith MW, Carrington M, Winkler C, et al (1998) Dating the origin of the CCR5-Δ32 AIDS-resistance allele by the coalescence of haplotypes. Am J Hum Genet 62:1507-1515
67. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595
68. Tishkoff SA, Dietzsch E, Speed W, Pakstis AJ, Kidd JR, Cheung K, Bonne-Tamir B, Santachiara-Benerecetti AS, Moral P, Krings M (1996) Global patterns of linkage disequilibrium at the CD4 locus and modern human origins. Science 271:1380-1387
69. Tishkoff SA, Goldman A, Calafell F, Speed WC, Deinard AS, Bonne-Tamir B, Kidd JR, Pakstis AJ, Jenkins T, Kidd KK (1998) A global haplotype analysis of the myotonic dystrophy locus: Implications for the evolution of modern humans and for the origin of myotonic dystrophy mutations. Am J Hum Genet 62:1389-1402
70. Tishkoff SA, Pakstis AJ, Stoneking M, Kidd JR, Destro-Bisol G, Sanjantila A, Lu RB, Deinard AS, Sirugo G, Jenkins T, Kidd KK, Clark AG (2000) Short tandem-repeat polymorphism/Alu haplotype variation at the PLAT locus: Implications for modern human origins. Am J Hum Genet 67:901-925
71. Tishkoff SA, Varkonyi R, Cahinhinan N, Abbes S, Argyropoulos G, Destro-Bisol G, Drousiotou A, Dangerfield B, Lefranc G, Loiselet J, Piro A, Stoneking M, Tagarelli A, Tagarelli G, Touma EH, Williams SM, Clark AG (2001) Haplotype diversity and linkage disequilibrium at human G6PD: Recent origin of alleles that confer malarial resistance. Science 293:455-462
72. Tishkoff SA, Williams SM (2002) Genetic analysis of African populations: Human evolution and complex disease. Nat Rev Genet 3:611-621
73. Toole JJ, Pittman DD, Orr EC, Murtha P, Wasley LC, Kaufman RJ (1986) A large region (approximately equal to 95 kDa) of human factor VIII is dispensable for in vitro procoagulant activity. Proc Natl Acad Sci USA 83:5939-5942
74. Town M, Bautista JM, Mason PJ, Luzzatto L (1992) Both mutations in G6PD A-Are necessary to produce the G6PD deficient phenotype. Hum Mol Genet 1:171-174
75. Verrelli BC, Eanes WF (2001) Clinal variation for amino acid polymorphisms at the Pgm locus in Drosophila melanogaster. Genetics 158:1649-1663
76. Vulliamy TJ, Mason P, Luzzatto L (1992) The molecular basis of glucose-6-phosphate dehydrogenase deficiency. Trends Genet 8:138-142
77. Wall JD, Przeworski M (2000) When did the human population size start increasing? Genetics 155:1865-1874
78. Watterson GA (1975) On the number of segregating sites in genetic models without recombination. Theor Popul Biol 7:256-276
79. Wuif C, Donnelly P (1999) Conditional genealogies and the age of a neutral mutant. Theor Popul Biol 56:183-201