Genetic adaptation to levels of dietary selenium in recent human history

Molecular Biology and Evolution

Volumn 32, Issue 6, 2015, Pages 1507-1518

  White, Louise ^a   Romagné, Frédéric ^a   Müller, Elias ^a   Erlebach, Eva ^a   Weihmann, Antje ^a   Parra, Genís ^a   Andrés, Aida M ^a   Castellano, Sergi ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

local adaptation; micronutrients; polygenic adaptation

Indexed keywords

15 KDA SELENOPROTEIN; GENOMIC DNA; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 5; GLUTATHIONE PEROXIDASE 7; GLUTATHIONE PEROXIDASE 8; IODIDE PEROXIDASE; IODOTHYRONINE; METHIONINE SULFOXIDE REDUCTASE B; SELENIUM; SELENOPROTEIN; SELENOPROTEIN H; SELENOPROTEIN I; SELENOPROTEIN K; SELENOPROTEIN M; SELENOPROTEIN N; SELENOPROTEIN O; SELENOPROTEIN P; SELENOPROTEIN R 2; SELENOPROTEIN R 3; SELENOPROTEIN S; SELENOPROTEIN T; SELENOPROTEIN V; SELENOPROTEIN W; SELENOPROTEIN W 1; THIOREDOXIN REDUCTASE 1; THIOREDOXIN REDUCTASE 2; THIOREDOXIN REDUCTASE 3; TRIIODOTHYRONINE DERIVATIVE; UNCLASSIFIED DRUG; UNINDEXED DRUG; MESSENGER RNA; SELENOCYSTEINE;

ARTICLE; ASIA; CHINA; CONTROLLED STUDY; DIET; DIETARY INTAKE; EVOLUTIONARY ADAPTATION; FEMALE; GENE CONTROL; GENE FREQUENCY; GENETIC EPIGENESIS; GENETIC VARIABILITY; HISTORY; HUMAN; MAJOR CLINICAL STUDY; MALE; MIGRATION; SELENIUM BLOOD LEVEL; SELENIUM DEFICIENCY; SINGLE NUCLEOTIDE POLYMORPHISM; ADAPTATION; DEFICIENCY; GENETIC SELECTION; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS;

ADAPTATION, PHYSIOLOGICAL; CHINA; DIET; EVOLUTION, MOLECULAR; GENE FREQUENCY; HUMANS; MOLECULAR SEQUENCE ANNOTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA, MESSENGER; SELECTION, GENETIC; SELENIUM; SELENOCYSTEINE; SELENOPROTEINS;

EID: 84930719974     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv043     Document Type: Article

References (73)

1. Ahmad K, Khan ZI, Ashraf M, Shah ZA, Ejaz A, Valeem EE. 2009. Timecourse chages in selenium status of soil and forage in a pasture in Sargodha, Punjab, Pakistan. Pak J Bot. 41:2397-2401.
2. Allmang C, Wurth L, Krol A. 2009. The selenium to selenoprotein pathway in eukaryotes: more molecular partners than anticipated. Biochim Biophys Acta. 1790:1415-1423.
3. Andres AM, Dennis MY, Kretzschmar WW, Cannons JL, Lee-Lin SQ, Hurle B, Schwartzberg PL, Williamson SH, Bustamante CD, Nielsen R, et al. 2010. Balancing selection maintains a form of ERAP2 that undergoes nonsense-mediated decay and affects antigen presentation. PLoS Genet. 6:e1001157.
4. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc B. 57:289-300.
5. Bhutta ZA, Salam RA. 2012. Global nutrition epidemiology and trends. Ann Nutr Metab. 61(Suppl. 1): 19-27.
6. Bifano AL, Atassi T, Ferrara T, Driscoll DM. 2013. Identification of nucleotides and amino acids that mediate the interaction between ribosomal protein L30 and the SECIS element. BMC Mol Biol. 14:12.
7. Bubenik JL, Ladd AN, Gerber CA, Budiman ME, Driscoll DM. 2009. Known turnover and translation regulatory RNA-binding proteins interact with the 30 UTR of SECIS-binding protein 2. RNA Biol. 6: 73-83.
8. Burk RF, Hill KE. 2009. Selenoprotein P-expression, functions, and roles in mammals. Biochim Biophys Acta. 1790:1441-1447.
9. Caballero B. 2002. Global patterns of child health: the role of nutrition. Ann Nutr Metab. 46(Suppl. 1): 3-7.
10. Canani LH, Capp C, Dora JM, Meyer EL, Wagner MS, Harney JW, Larsen PR, Gross JL, Bianco AC, Maia AL. 2005. The type 2 deiodinase A/G (Thr92Ala) polymorphism is associated with decreased enzyme velocity and increased insulin resistance in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 90:3472-3478.
11. Cann HM, de Toma C, Cazes L, Legrand MF, Morel V, Piouffre L, Bodmer J, Bodmer WF, Bonne-Tamir B, Cambon-Thomsen A, et al. 2002. A human genome diversity cell line panel. Science 296:261-262.
12. Castellano S, Andres AM, Bosch E, Bayes M, Guigo R, Clark AG. 2009. Low exchangeability of selenocysteine, the 21st amino acid, in vertebrate proteins. Mol Biol Evol. 26:2031-2040.
13. Castellano S, Gladyshev VN, Guigo R, Berry MJ. 2008. SelenoDB 1. 0: A database of selenoprotein genes, proteins and SECIS elements. Nucleic Acids Res. 36:D332-D338.
14. Castellano S, Parra G, Sanchez-Quinto FA, Racimo F, Kuhlwilm M, Kircher M, Sawyer S, Fu Q, Heinze A, Nickel B, et al. 2014. Patterns of coding variation in the complete exomes of three Neandertals. Proc Natl Acad Sci U S A. 111:6666-6671.
15. Curran JE, Jowett JB, Elliott KS, Gao Y, Gluschenko K, Wang J, Abel Azim DM, Cai G, Mahaney MC, Comuzzie AG, et al. 2005. Genetic variation in selenoprotein S influences inflammatory response. Nat Genet. 37:1234-1241.
16. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 43:491-498.
17. Diamond J. 2002. Evolution, consequences and future of plant and animal domestication. Nature 418:700-707.
18. Dumitrescu AM, Liao XH, AbdullahMS, Lado-Abeal J, Majed FA, Moeller LC, Boran G, Schomburg L, Weiss RE, Refetoff S. 2005. Mutations in SECISBP2 result in abnormal thyroid hormone metabolism. Nat Genet. 37:1247-1252.
19. Fay JC, Wu CI. 2000. Hitchhiking under positive Darwinian selection. Genetics 155:1405-1413.
20. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, et al. 2013. Ensembl 2013. Nucleic Acids Res. 41:D48-D55.
21. Foster CB, Aswath K, Chanock SJ, McKay HF, Peters U. 2006. Polymorphism analysis of six selenoprotein genes: support for a selective sweep at the glutathione peroxidase 1 locus (3p21) in Asian populations. BMC Genet. 7:56.
22. Fu Q, Mittnik A, Johnson PL, Bos K, LariM, Bollongino R, Sun C, Giemsch L, Schmitz R, Burger J, et al. 2013. A revised timescale for human evolution based on ancient mitochondrial genomes. Curr Biol. 23: 553-559.
23. Gromer S, Johansson L, Bauer H, Arscott LD, Rauch S, Ballou DP, Williams CH Jr, Schirmer RH, Arner ES. 2003. Active sites of thioredoxin reductases: why selenoproteins? Proc Natl Acad Sci U S A. 100:12618-12623.
24. Guimaraes MJ, Peterson D, Vicari A, Cocks BG, Copeland NG, Gilbert DJ, Jenkins NA, Ferrick DA, Kastelein RA, Bazan JF, et al. 1996. Identification of a novel selD homolog from eukaryotes, bacteria, and archaea: is there an autoregulatory mechanism in selenocysteine metabolism? Proc Natl Acad Sci U S A. 93:15086-15091.
25. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5: e1000695.
26. Hamanishi T, Furuta H, Kato H, Doi A, Tamai M, Shimomura H, Sakagashira S, Nishi M, Sasaki H, Sanke T, et al. 2004. Functional variants in the glutathione peroxidase-1 (GPx-1) gene are associated with increased intima-media thickness of carotid arteries and risk of macrovascular diseases in japanese type 2 diabetic patients. Diabetes 53:2455-2460.
27. Hatfield DL, Berry MJ, Gladyshev VN. 2012. Selenium: its molecular biology and role in human health. New York: Springer.
28. Hodges E, Rooks M, Xuan Z, Bhattacharjee A, Benjamin Gordon D, Brizuela L, RichardMcCombieW, Hannon GJ. 2009. Hybrid selection of discrete genomic intervals on custom-designed microarrays for massively parallel sequencing. Nat Protoc. 4:960-974.
29. Hudson RR. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18:337-338.
30. Hurst R, Siyame EW, Young SD, ChilimbaAD, Joy EJ, Black CR, Ander EL, Watts MJ, Chilima B, Gondwe J, et al. 2013. Soil-Type influences human selenium status and underlies widespread selenium deficiency risks in Malawi. Sci Rep. 3:1425.
31. Keinan A, Mullikin JC, Patterson N, Reich D. 2007. Measurement of the human allele frequency spectrum demonstrates greater genetic drift in East Asians than in Europeans. Nat Genet. 39:1251-1255.
32. Keshan Disease Research Group of the Chinese Academy of Medical Sciences. 1979. Observations on effect of sodium selenite in prevention of Keshan disease. Chin Med J (Engl). 92:471-476.
33. Khan ZI, AshrafM, DanishM, Ahmad K, Valeem EE. 2008. Assessment of selenium content in pasture and ewes in Punjab, Pakistan. Pak J Bot. 40:1159-1162.
34. Khan ZI, Hussain A, Ashraf M, McDowell R. 2006. Mineral status of soils and forages in southwestern Punjab-Pakistan: micro-minerals. Asian-Aust J Anim Sci. 19:1139-1147.
35. Kircher M, Stenzel U, Kelso J. 2009. Improved base calling for the Illumina Genome Analyzer using machine learning strategies. Genome Biol. 10:R83.
36. Koivistoinen P, Huttunen JK. 1986. Selenium in food and nutrition in Finland. An overview on research and action. Ann Clin Res. 18:13-17.
37. Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigo R, Gladyshev VN. 2003. Characterization of mammalian selenoproteomes. Science 300:1439-1443.
38. Latreche L, Jean-Jean O, Driscoll DM, Chavatte L. 2009. Novel structural determinants in human SECIS elements modulate the translational recoding of UGA as selenocysteine. Nucleic Acids Res. 37:5868-5880.
39. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
40. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, Ramachandran S, Cann HM, Barsh GS, Feldman M, Cavalli-Sforza LL, et al. 2008. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319:1100-1104.
41. McDowell LR. 1976. Mineral deficiencies and toxicities and their effect on beef production in developing countries. In: Smith AJ, editor. Beef cattle production in developing countries. Edinburgh (United Kingdom): University of Edinburgh, Centre for Tropical Veterinary Medicine. p. 216-241.
42. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al. 2010. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20:1297-1303.
43. Meplan C, Hughes DJ, Pardini B, Naccarati A, Soucek P, Vodickova L, Hlavata I, Vrana D, Vodicka P, Hesketh JE. 2010. Genetic variants in selenoprotein genes increase risk of colorectal cancer. Carcinogenesis 31:1074-1079.
44. Mertz W. 1981. The essential trace elements. Science 213:1332-1338.
45. Meyer M, Kircher M. 2010. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc. 2010:pdb prot5448.
46. Moreno-Reyes R, Egrise D, Neve J, Pasteels JL, Schoutens A. 2001. Selenium deficiency-induced growth retardation is associated with an impaired bone metabolism and osteopenia. J Bone Miner Res. 16: 1556-1563.
47. Novakovic R, Cavelaars A, Geelen A, Nikolic M, Altaba II, Vinas BR, Ngo J, Golsorkhi M, Medina MW, Brzozowska A, et al. 2014. Socioeconomic determinants of micronutrient intake and status in Europe: A systematic review. Public Health Nutr. 17:1031-1045.
48. Novakovic R, Cavelaars AE, Bekkering GE, Roman-Vinas B, Ngo J, Gurinovic M, Glibetic M, Nikolic M, Golesorkhi M, Medina MW, et al. 2013. Micronutrient intake and status in Central and Eastern Europe compared with other European countries, results from the EURRECA network. Public Health Nutr. 16:824-840.
49. Oldfield JE. 2002. Selenium world atlas. Grimbergen (Belgium): STDA.
50. Paten B, Herrero J, Beal K, Fitzgerald S, Birney E. 2008. Enredo and Pecan: genome-wide mammalian consistency-based multiple alignment with paralogs. Genome Res. 18:1814-1828.
51. Pemberton TJ, Absher D, FeldmanMW, Myers RM, Rosenberg NA, Li JZ. 2012. Genomic patterns of homozygosity in worldwide human populations. Am J Hum Genet. 91:275-292.
52. Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R, Werner J, Villanea FA, Mountain JL, Misra R, et al. 2007. Diet and the evolution of human amylase gene copy number variation. Nat Genet. 39: 1256-1260.
53. Pruitt KD, Tatusova T, Klimke W, Maglott DR. 2009. NCBI Reference Sequences: current status, policy and new initiatives. Nucleic Acids Res. 37:D32-D36.
54. Rayman MP. 2012. Selenium and human health. Lancet 379: 1256-1268.
55. Romagne F, Santesmasses D, White L, Sarangi GK, Mariotti M, Hubler R, Weihmann A, Parra G, Gladyshev VN, Guigo R, et al. 2014. SelenoDB 2. 0: Annotation of selenoprotein genes in animals and their genetic diversity in humans. Nucleic Acids Res. 42:D437-D443.
56. Rosenberg NA. 2006. Standardized subsets of the HGDP-CEPH Human Genome Diversity Cell Line Panel, accounting for atypical and duplicated samples and pairs of close relatives. Ann Hum Genet. 70: 841-847.
57. Safaralizadeh R, Kardar GA, Pourpak Z, Moin M, Zare A, Teimourian S. 2005. Serum concentration of selenium in healthy individuals living in Tehran. Nutr J. 4:32.
58. Schomburg L, Schweizer U. 2009. Hierarchical regulation of selenoprotein expression and sex-specific effects of selenium. Biochim Biophys Acta. 1790:1453-1462.
59. Selinus O, Alloway BJ. 2005. Essentials of medical geology: impacts of the natural environment on public health. Amsterdam (The Netherlands): Elsevier Academic Press.
60. Snider GW, Ruggles E, Khan N, Hondal RJ. 2013. Selenocysteine confers resistance to inactivation by oxidation in thioredoxin reductase: comparison of selenium and sulfur enzymes. Biochemistry 52: 5472-5481.
61. Steinbrenner H, Sies H. 2009. Protection against reactive oxygen species by selenoproteins. Biochim Biophys Acta. 1790:1478-1485.
62. Steinmann D, Nauser T, Koppenol WH. 2010. Selenium and sulfur in exchange reactions: A comparative study. J Org Chem. 75: 6696-6699.
63. Stringer CB, Andrews P. 1988. Genetic and fossil evidence for the origin of modern humans. Science 239:1263-1268.
64. Sutherland A, Kim DH, Relton C, Ahn YO, Hesketh J. 2010. Polymorphisms in the selenoprotein S and 15-kDa selenoprotein genes are associated with altered susceptibility to colorectal cancer. Genes Nutr. 5:215-223.
65. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
66. Thomson CD. 2004. Selenium and iodine intakes and status in New Zealand and Australia. Br J Nutr. 91:661-672.
67. Thornton K. 2003. Libsequence: A C++ class library for evolutionary genetic analysis. Bioinformatics 19:2325-2327.
68. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, Silverman JS, Powell K, Mortensen HM, Hirbo JB, Osman M, et al. 2007. Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet. 39:31-40.
69. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population-structure. Evolution 38:1358-1370.
70. Wright S. 1951. The genetical structure of populations. Ann Eugen. 15: 323-354.
71. Xia Y, Hill KE, Byrne DW, Xu J, Burk RF. 2005. Effectiveness of selenium supplements in a low-selenium area of China. Am J Clin Nutr. 81: 829-834.
72. Xiong YM, Mo XY, Zou XZ, Song RX, Sun WY, Lu W, Chen Q, Yu YX, Zang WJ. 2010. Association study between polymorphisms in selenoprotein genes and susceptibility to Kashin-Beck disease. Osteoarthr Cartil. 18:817-824.
73. Yao Y, Pei F, Kang P. 2011. Selenium, iodine, and the relation with Kashin-Beck disease. Nutrition 27:1095-1100.