Genetic Adaptation of Fatty-Acid Metabolism: A Human-Specific Haplotype Increasing the Biosynthesis of Long-Chain Omega-3 and Omega-6 Fatty Acids

The American Journal of Human Genetics - Tập 90 - Trang 809-820 - 2012
Adam Ameur1, Stefan Enroth1, Åsa Johansson1, Ghazal Zaboli1, Wilmar Igl1, Anna C.V. Johansson1, Manuel A. Rivas2, Mark J. Daly2, Gerd Schmitz3, Andrew A. Hicks4, Thomas Meitinger5, Lars Feuk1, Cornelia van Duijn6, Ben Oostra7, Peter P. Pramstaller4,8,9, Igor Rudan10,11, Alan F. Wright12, James F. Wilson11, Harry Campbell11, Ulf Gyllensten1
1Department of Immunology, Genetics and Pathology, SciLifeLab Uppsala, Rudbeck Laboratory, Uppsala University, SE-751 85 Uppsala, Sweden
2The Center for Human Genetic Research, Massachusetts General Hospital, and The Broad Institute of MIT and Harvard, Boston, MA 02114, USA
3Institute for Clinical Chemistry and Laboratory Medicine, University Hospital Regensburg, 93042 Regensburg, Germany
4Center for Biomedicine, European Academy Bozen/Bolzano, 39100 Bolzano, Italy; affiliated institute of the University of Lübeck, 23562 Lübeck, Germany
5Helmholtz Zentrum München, D-85764 Neuherberg, Germany
6Department of Epidemiology, Erasmus University Medical Center, 3015 GE, Rotterdam, The Netherlands
7Department of Clinical Genetics, Erasmus University Medical Center, 3015 GE Rotterdam, the Netherlands
8Department of Neurology, General Central Hospital, 39100 Bolzano, Italy
9Department of Neurology, University of Lubeck, 23538 Lubeck, Germany
10Croatian Centre for Global Health, Faculty of Medicine, University of Split, 21000 Split, Croatia
11Centre for Population Health Sciences, University of Edinburgh, Teviot Place, Edinburgh EH8 9AG, UK
12Medical Research Council Human Genetics Unit, Medical Research Council Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh EH4 2XU, UK

Tài liệu tham khảo

Leonard, 2010, Evolutionary Perspectives on Fat Ingestion and Metabolism in Humans Darios, 2006, Omega-3 and omega-6 fatty acids stimulate cell membrane expansion by acting on syntaxin 3, Nature, 440, 813, 10.1038/nature04598 Marszalek, 2005, Docosahexaenoic acid, fatty acid-interacting proteins, and neuronal function: Breastmilk and fish are good for you, Annu. Rev. Cell Dev. Biol., 21, 633, 10.1146/annurev.cellbio.21.122303.120624 Ratnayake, 2009, Fat and fatty acid terminology, methods of analysis and fat digestion and metabolism: A background review paper, Ann. Nutr. Metab., 55, 8, 10.1159/000228994 Nakamura, 2004, Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases, Annu. Rev. Nutr., 24, 345, 10.1146/annurev.nutr.24.121803.063211 Aulchenko, 2009, Loci influencing lipid levels and coronary heart disease risk in 16 European population cohorts, Nat. Genet., 41, 47, 10.1038/ng.269 Hicks, 2009, Genetic determinants of circulating sphingolipid concentrations in European populations, PLoS Genet., 5, e1000672, 10.1371/journal.pgen.1000672 Kathiresan, 2009, Common variants at 30 loci contribute to polygenic dyslipidemia, Nat. Genet., 41, 56, 10.1038/ng.291 Sabatti, 2009, Genome-wide association analysis of metabolic traits in a birth cohort from a founder population, Nat. Genet., 41, 35, 10.1038/ng.271 Tanaka, 2009, Genome-wide association study of plasma polyunsaturated fatty acids in the InCHIANTI Study, PLoS Genet., 5, e1000338, 10.1371/journal.pgen.1000338 Bokor, 2010, Single nucleotide polymorphisms in the FADS gene cluster are associated with delta-5 and delta-6 desaturase activities estimated by serum fatty acid ratios, J. Lipid Res., 51, 2325, 10.1194/jlr.M006205 Malerba, 2008, SNPs of the FADS gene cluster are associated with polyunsaturated fatty acids in a cohort of patients with cardiovascular disease, Lipids, 43, 289, 10.1007/s11745-008-3158-5 Schaeffer, 2006, Common genetic variants of the FADS1 FADS2 gene cluster and their reconstructed haplotypes are associated with the fatty acid composition in phospholipids, Hum. Mol. Genet., 15, 1745, 10.1093/hmg/ddl117 Zietemann, 2010, Genetic variation of the FADS1 FADS2 gene cluster and n-6 PUFA composition in erythrocyte membranes in the European Prospective Investigation into Cancer and Nutrition-Potsdam study, Br. J. Nutr., 104, 1748, 10.1017/S0007114510002916 Caspi, 2007, Moderation of breastfeeding effects on the IQ by genetic variation in fatty acid metabolism, Proc. Natl. Acad. Sci. USA, 104, 18860, 10.1073/pnas.0704292104 Lattka, 2011, Am. J. Clin. Nutr., 93, 382, 10.3945/ajcn.110.004515 Moltó-Puigmartí, 2010, FADS1 FADS2 gene variants modify the association between fish intake and the docosahexaenoic acid proportions in human milk, Am. J. Clin. Nutr., 91, 1368, 10.3945/ajcn.2009.28789 Martinelli, 2008, FADS genotypes and desaturase activity estimated by the ratio of arachidonic acid to linoleic acid are associated with inflammation and coronary artery disease, Am. J. Clin. Nutr., 88, 941, 10.1093/ajcn/88.4.941 Cordain, 2001, Fatty acid composition and energy density of foods available to African hominids. Evolutionary implications for human brain development, World Rev. Nutr. Diet., 90, 144, 10.1159/000059813 Crawford, 1999, Evidence for the unique function of docosahexaenoic acid during the evolution of the modern hominid brain, Lipids, 34, S39, 10.1007/BF02562227 Bansal, 2010, Statistical analysis strategies for association studies involving rare variants, Nat. Rev. Genet., 11, 773, 10.1038/nrg2867 Johansson, 2009, Common variants in the JAZF1 gene associated with height identified by linkage and genome-wide association analysis, Hum. Mol. Genet., 18, 373, 10.1093/hmg/ddn350 McQuillan, 2008, Runs of homozygosity in European populations, Am. J. Hum. Genet., 83, 359, 10.1016/j.ajhg.2008.08.007 Rudan, 1999, Genetic epidemiological studies of eastern Adriatic Island isolates, Croatia: Objective and strategies, Coll. Antropol., 23, 531 Vitart, 2006, 3000 years of solitude: Extreme differentiation in the island isolates of Dalmatia, Croatia, Eur. J. Hum. Genet., 14, 478, 10.1038/sj.ejhg.5201589 Pattaro, 2007, The genetic study of three population microisolates in South Tyrol (MICROS): Study design and epidemiological perspectives, BMC Med. Genet., 8, 29, 10.1186/1471-2350-8-29 Aulchenko, 2004, Linkage disequilibrium in young genetically isolated Dutch population, Eur. J. Hum. Genet., 12, 527, 10.1038/sj.ejhg.5201188 Mascalzoni, 2010, Comparison of participant information and informed consent forms of five European studies in genetic isolated populations, Eur. J. Hum. Genet., 18, 296, 10.1038/ejhg.2009.155 Liebisch, 1999, Quantitative measurement of different ceramide species from crude cellular extracts by electrospray ionization tandem mass spectrometry (ESI-MS/MS), J. Lipid Res., 40, 1539, 10.1016/S0022-2275(20)33398-8 Liebisch, 2004, High-throughput quantification of phosphatidylcholine and sphingomyelin by electrospray ionization tandem mass spectrometry coupled with isotope correction algorithm, Biochim. Biophys. Acta, 1686, 108, 10.1016/j.bbalip.2004.09.003 Demirkan, 2012, Genome-Wide Association Study Identifies Novel Loci Associated with Circulating Phospho- and Sphingolipid Concentrations, PLoS Genet., 8, e1002490, 10.1371/journal.pgen.1002490 Li, 2009, Genotype imputation, Annu. Rev. Genomics Hum. Genet., 10, 387, 10.1146/annurev.genom.9.081307.164242 Scheet, 2006, A fast and flexible statistical model for large-scale population genotype data: Applications to inferring missing genotypes and haplotypic phase, Am. J. Hum. Genet., 78, 629, 10.1086/502802 Aulchenko, 2007, GenABEL: An R library for genome-wide association analysis, Bioinformatics, 23, 1294, 10.1093/bioinformatics/btm108 Chen, 2007, Family-based association tests for genomewide association scans, Am. J. Hum. Genet., 81, 913, 10.1086/521580 Barrett, 2005, Haploview: Analysis and visualization of LD and haplotype maps, Bioinformatics, 21, 263, 10.1093/bioinformatics/bth457 Zaboli, 2012, Sequencing of high-complexity DNA pools for identification of nucleotide and structural variants in regions associated with complex traits, Eur. J. Hum. Genet., 20, 77, 10.1038/ejhg.2011.138 Neale, 2011, Testing for an unusual distribution of rare variants, PLoS Genet., 7, e1001322, 10.1371/journal.pgen.1001322 Li, 2008, Worldwide human relationships inferred from genome-wide patterns of variation, Science, 319, 1100, 10.1126/science.1153717 Altshuler, 2010, Integrating common and rare genetic variation in diverse human populations, Nature, 467, 52, 10.1038/nature09298 Durbin, 2010, A map of human genome variation from population-scale sequencing, Nature, 467, 1061, 10.1038/nature09534 Reich, 2010, Genetic history of an archaic hominin group from Denisova Cave in Siberia, Nature, 468, 1053, 10.1038/nature09710 Green, 2010, A draft sequence of the Neandertal genome, Science, 328, 710, 10.1126/science.1188021 Li, 2009, The Sequence Alignment/Map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 Roach, 2010, Analysis of genetic inheritance in a family quartet by whole-genome sequencing, Science, 328, 636, 10.1126/science.1186802 Schuster, 2010, Complete Khoisan and Bantu genomes from southern Africa, Nature, 463, 943, 10.1038/nature08795 Rasmussen, 2010, Ancient human genome sequence of an extinct Palaeo-Eskimo, Nature, 463, 757, 10.1038/nature08835 Rasmussen, 2011, An Aboriginal Australian genome reveals separate human dispersals into Asia, Science, 334, 94, 10.1126/science.1211177 Schliep, 2011, phangorn: Phylogenetic analysis in R, Bioinformatics, 27, 592, 10.1093/bioinformatics/btq706 Drummond, 2007, BEAST: Bayesian evolutionary analysis by sampling trees, BMC Evol. Biol., 7, 214, 10.1186/1471-2148-7-214 Scott, 1989, Membrane docosahexaenoate is supplied to the developing brain and retina by the liver, Proc. Natl. Acad. Sci. USA, 86, 2903, 10.1073/pnas.86.8.2903 Schadt, 2008, Mapping the genetic architecture of gene expression in human liver, PLoS Biol., 6, e107, 10.1371/journal.pbio.0060107 Teslovich, 2010, Biological, clinical and population relevance of 95 loci for blood lipids, Nature, 466, 707, 10.1038/nature09270 Sabeti, 2007, Genome-wide detection and characterization of positive selection in human populations, Nature, 449, 913, 10.1038/nature06250 Nielsen, 2005, Genomic scans for selective sweeps using SNP data, Genome Res., 15, 1566, 10.1101/gr.4252305 Williamson, 2007, Localizing recent adaptive evolution in the human genome, PLoS Genet., 3, e90, 10.1371/journal.pgen.0030090 Pickrell, 2009, Signals of recent positive selection in a worldwide sample of human populations, Genome Res., 19, 826, 10.1101/gr.087577.108 Abi-Rached, 2011, The shaping of modern human immune systems by multiregional admixture with archaic humans, Science, 334, 89, 10.1126/science.1209202 Titus-Trachtenberg, 1994, Analysis of HLA class II haplotypes in the Cayapa Indians of Ecuador: A novel DRB1 allele reveals evidence for convergent evolution and balancing selection at position 86, Am. J. Hum. Genet., 55, 160 Wang, 2007, Genetic variation and population structure in native Americans, PLoS Genet., 3, e185, 10.1371/journal.pgen.0030185 Mathias, 2011, The impact of FADS genetic variants on ω6 polyunsaturated fatty acid metabolism in African Americans, BMC Genet., 12, 50, 10.1186/1471-2156-12-50 Martinelli, 2009, A ‘desaturase hypothesis’ for atherosclerosis: Janus-faced enzymes in omega-6 and omega-3 polyunsaturated fatty acid metabolism, J Nutrigenet Nutrigenomics, 2, 129, 10.1159/000238177 Sergeant, 2012, Differences in arachidonic acid levels and fatty acid desaturase (FADS) gene variants in African Americans and European Americans with diabetes or the metabolic syndrome, Br. J. Nutr., 107, 547, 10.1017/S0007114511003230 Koletzko, 2008, Genetically determined variation in polyunsaturated fatty acid metabolism might result in different dietary requirements, Nestle Nutr. Workshop Ser. Pediatr. Program., 62, 35, 10.1159/000146246 Birney, 2007, Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project, Nature, 447, 799, 10.1038/nature05874 Matsuzaka, 2002, Dual regulation of mouse Delta(5)- and Delta(6)-desaturase gene expression by SREBP-1 and PPARalpha, J. Lipid Res., 43, 107, 10.1016/S0022-2275(20)30193-0