Comparative analyses of QTLs influencing obesity and metabolic phenotypes in pigs and humans

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Pant, Sameer D ^a,g   Karlskov Mortensen, Peter ^a   Jacobsen, Mette J ^a   Cirera, Susanna ^a   Kogelman, Lisette J A ^a   Bruun, Camilla S ^a   Mark, Thomas ^a   Jørgensen, Claus B ^a   Grarup, Niels ^b   Appel, Emil V R ^b   Galjatovic, Ehm A A ^b   Hansen, Torben ^b   Pedersen, Oluf ^b   Guerin, Maryse ^c,d,e   Huby, Thierry ^c,d,e   Lesnik, Philipppe ^c,d,e   Meuwissen, Theo H E ^f   Kadarmideen, Haja N ^a   Fredholm, Merete ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Capital Region   (Denmark)

^c Sorbonne Universités   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^f NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^g CHARLES STURT UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BOAR (MALE PIG); BODY COMPOSITION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DUROC PIG; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENOTYPE; GILT (SWINE); GLUCOSE BLOOD LEVEL; GOTTINGEN MINIPIG; HUMAN; MALE; METABOLIC DISORDER; NONHUMAN; OBESITY; PHENOTYPE; QUANTITATIVE TRAIT LOCUS; SOW (SWINE); SPECIES COMPARISON; SYNTENY; YORKSHIRE PIG; ANIMAL; BODY MASS; BREEDING; CHROMOSOMAL MAPPING; DISEASE MODEL; GENETIC LINKAGE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MOUSE; PATHOPHYSIOLOGY; PHOTON ABSORPTIOMETRY; PIG;

ABSORPTIOMETRY, PHOTON; ANIMALS; BODY COMPOSITION; BODY MASS INDEX; BREEDING; CHROMOSOME MAPPING; DISEASE MODELS, ANIMAL; GENETIC LINKAGE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; METABOLIC DISEASES; MICE; OBESITY; PHENOTYPE; QUANTITATIVE TRAIT LOCI; SUS SCROFA;

EID: 84944400509     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137356     Document Type: Article

References (57)

1. Cawley J, Meyerhoefer C. The medical care costs of obesity: an instrumental variables approach. Journal of health economics. 2012;31(1):219-30. doi: 10.1016/j.jhealeco.2011.10.003 PMID: 22094013.
2. Whitlock G, Lewington S, Sherliker P, Clarke R, Emberson J, Halsey J, et al. Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. Lancet. 2009;373(9669):1083-96. doi: 10.1016/S0140-6736 (09) 60318-4 PMID: 19299006; PubMed Central PMCID: PMC2662372.
3. Maes HH, Neale MC, Eaves LJ. Genetic and environmental factors in relative body weight and human adiposity. Behavior genetics. 1997;27(4):325-51. PMID: 9519560.
4. Speliotes EK, Willer CJ, Berndt SI, Monda KL, Thorleifsson G, Jackson AU, et al. Association analyses of 249, 796 individuals reveal 18 new loci associated with body mass index. Nature genetics. 2010;42(11):937-48. doi: 10.1038/ng.686 PMID: 20935630; PubMed Central PMCID: PMC3014648.
5. Arner P. Resistin: yet another adipokine tells us that men are not mice. Diabetologia. 2005;48(11):2203-5. doi: 10.1007/s00125-005-1956-3 PMID: 16193286.
6. Heinritz SN, Mosenthin R, Weiss E. Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutrition research reviews. 2013;26(2):191-209. doi: 10.1017/S0954422413000152 PMID: 24134811.
7. Spurlock ME, Gabler NK. The development of porcine models of obesity and the metabolic syndrome. The Journal of nutrition. 2008;138(2):397-402. PMID: 18203910.
8. Meuwissen T, Goddard M. The use of family relationships and linkage disequilibrium to impute phase and missing genotypes in up to whole-genome sequence density genotypic data. Genetics. 2010;185(4):1441-9. doi: 10.1534/genetics.110.113936 PMID: 20479147; PubMed Central PMCID: PMC2927768.
9. Welter D, MacArthur J, Morales J, Burdett T, Hall P, Junkins H, et al. The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic acids research. 2014;42(Database issue):D1001-6. doi: 10.1093/nar/gkt1229 PMID: 24316577; PubMed Central PMCID: PMC3965119.
10. Hu ZL, Park CA, Wu XL, Reecy JM. Animal QTLdb: an improved database tool for livestock animal QTL/association data dissemination in the post-genome era. Nucleic acids research. 2013;41(Database issue):D871-9. doi: 10.1093/nar/gks1150 PMID: 23180796; PubMed Central PMCID: PMC3531174.
11. Lee JM, Sonnhammer EL. Genomic gene clustering analysis of pathways in eukaryotes. Genome research. 2003;13(5):875-82. doi: 10.1101/gr.737703 PMID: 12695325; PubMed Central PMCID: PMC430880.
12. Fox CS, Liu Y, White CC, Feitosa M, Smith AV, Heard-Costa N, et al. Genome-wide association for abdominal subcutaneous and visceral adipose reveals a novel locus for visceral fat in women. PLoS genetics. 2012;8(5):e1002695. doi: 10.1371/journal.pgen. 1002695 PMID: 22589738; PubMed Central PMCID: PMC3349734.
13. Wang KS, Liu X, Zheng S, Zeng M, Pan Y, Callahan K. A novel locus for body mass index on 5p15.2: a meta-analysis of two genome-wide association studies. Gene. 2012;500(1):80-4. doi: 10.1016/j.gene. 2012.03.046 PMID: 22446040.
14. Velez Edwards DR, Naj AC, Monda K, North KE, Neuhouser M, Magvanjav O, et al. Gene-environment interactions and obesity traits among postmenopausal African-American and Hispanic women in the Women's Health Initiative SHARe Study. Human genetics. 2013;132(3):323-36. doi: 10.1007/s00439-012-1246-3 PMID: 23192594; PubMed Central PMCID: PMC3704217.
15. Melen E, Granell R, Kogevinas M, Strachan D, Gonzalez JR, Wjst M, et al. Genome-wide association study of body mass index in 23 000 individuals with and without asthma. Clinical and experimental allergy: journal of the British Society for Allergy and Clinical Immunology. 2013;43(4):463-74. doi: 10. 1111/cea.12054 PMID: 23517042; PubMed Central PMCID: PMC3608930.
16. Comuzzie AG, Cole SA, Laston SL, Voruganti VS, Haack K, Gibbs RA, et al. Novel genetic loci identified for the pathophysiology of childhood obesity in the Hispanic population. PloS one. 2012;7(12):e51954. doi: 10.1371/journal.pone.0051954 PMID: 23251661; PubMed Central PMCID: PMC3522587.
17. Irvin MR, Shrestha S, Chen YD, Wiener HW, Haritunians T, Vaughan LK, et al. Genes linked to energy metabolism and immunoregulatory mechanisms are associated with subcutaneous adipose tissue distribution in HIV-infected men. Pharmacogenetics and genomics. 2011;21(12):798-807. doi: 10.1097/FPC.0b013e32834b68f9 PMID: 21897333; PubMed Central PMCID: PMC3210910.
18. Lowe JK, Maller JB, Pe'er I, Neale BM, Salit J, Kenny EE, et al. Genome-wide association studies in an isolated founder population from the Pacific Island of Kosrae. PLoS genetics. 2009;5(2):e1000365. doi: 10.1371/journal.pgen. 1000365 PMID: 19197348; PubMed Central PMCID: PMC2628735.
19. Johansson A, Marroni F, Hayward C, Franklin CS, Kirichenko AV, Jonasson I, et al. Linkage and genome-wide association analysis of obesity-related phenotypes: association of weight with the MGAT1 gene. Obesity. 2010;18(4):803-8. doi: 10.1038/oby.2009.359 PMID: 19851299.
20. Melka MG, Bernard M, Mahboubi A, Abrahamowicz M, Paterson AD, Syme C, et al. Genome-wide scan for loci of adolescent obesity and their relationship with blood pressure. The Journal of clinical endocrinology and metabolism. 2012;97(1):E145-50. doi: 10.1210/jc.2011-1801 PMID: 22013104.
21. Replication DIG, Meta-analysis C, Asian Genetic Epidemiology Network Type 2 Diabetes C, South Asian Type 2 Diabetes C, Mexican American Type 2 Diabetes C, Type 2 Diabetes Genetic Exploration by Nex-generation sequencing in muylti-Ethnic Samples C, et al. Genome-wide trans-ancestry metaanalysis provides insight into the genetic architecture of type 2 diabetes susceptibility. Nature genetics. 2014;46(3):234-44. doi: 10.1038/ng.2897 PMID: 24509480; PubMed Central PMCID: PMC3969612.
22. Voight BF, Scott LJ, Steinthorsdottir V, Morris AP, Dina C, Welch RP, et al. Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nature genetics. 2010;42(7):579-89. doi: 10.1038/ng.609 PMID: 20581827; PubMed Central PMCID: PMC3080658.
23. Soleimani M. SLC26 Cl-/HCO3-exchangers in the kidney: roles in health and disease. Kidney international. 2013;84(4):657-66. doi: 10.1038/ki.2013.138 PMID: 23636174.
24. Flannick J, Thorleifsson G, Beer NL, Jacobs SB, Grarup N, Burtt NP, et al. Loss-of-function mutations in SLC30A8 protect against type 2 diabetes. Nature genetics. 2014;46(4):357-63. doi: 10.1038/ng. 2915 PMID: 24584071; PubMed Central PMCID: PMC4051628.
25. Berndt SI, Gustafsson S, Magi R, Ganna A, Wheeler E, Feitosa MF, et al. Genome-wide meta-analysis identifies 11 new loci for anthropometric traits and provides insights into genetic architecture. Nature genetics. 2013;45(5):501-12. doi: 10.1038/ng.2606 PMID: 23563607; PubMed Central PMCID: PMC3973018.
26. Fox CS, Heard-Costa N, Cupples LA, Dupuis J, Vasan RS, Atwood LD. Genome-wide association to body mass index and waist circumference: the Framingham Heart Study 100K project. BMC medical genetics. 2007;8 Suppl 1:S18. doi: 10.1186/1471-2350-8-S1-S18 PMID: 17903300; PubMed Central PMCID: PMC1995618.
27. Kempen KP, Saris WH, Kuipers H, Glatz JF, Van Der Vusse GJ. Skeletal muscle metabolic characteristics before and after energy restriction in human obesity: fibre type, enzymatic beta-oxidative capacity and fatty acid-binding protein content. European journal of clinical investigation. 1998;28(12):1030-7. PMID: 9893016.
28. Makowski L, Hotamisligil GS. The role of fatty acid binding proteins in metabolic syndrome and atherosclerosis. Current opinion in lipidology. 2005;16(5):543-8. PMID: 16148539; PubMed Central PMCID: PMC3904771.
29. Zou L, Chatham JC. The role of STIM1 and store operated calcium entry in glucose-induced insulin secretion. The FASEB Journal. 2013;27(1-MeetingAbstracts):701.7.
30. Ding H, Benslimane F, Marei I, Triggle CR. High Glucose Increases Acetylcholine-InducedCa2 Entry and Protein Expression of STIM1. International Science Index. 2012;6(4). waset.org/Publication/8247.
31. Estrada IA, Donthamsetty R, Debski P, Zhou MH, Zhang SL, Yuan JX, et al. STIM1 restores coronary endothelial function in type 1 diabetic mice. Circulation research. 2012;111(9):1166-75. doi: 10.1161/CIRCRESAHA.112.275743 PMID: 22896585; PubMed Central PMCID: PMC3627729.
32. Shackelford DB, Shaw RJ. The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nature Reviews Cancer. 2009;9(8):563-75. doi: 10.1038/nrc2676 PMID: 19629071
33. Arai A, Spencer JA, Olson EN. STARS, a striated muscle activator of Rho signaling and serum response factor-dependent transcription. The Journal of biological chemistry. 2002;277(27):24453-9. doi: 10.1074/jbc. M202216200 PMID: 11983702.
34. Nofer JR, Feuerborn R, Levkau B, Sokoll A, Seedorf U, Assmann G. Involvement of Cdc42 signaling in apoA-I-induced cholesterol efflux. The Journal of biological chemistry. 2003;278(52):53055-62. doi: 10.1074/jbc. M305673200 PMID: 14563854.
35. Chen G, Ramos E, Adeyemo A, Shriner D, Zhou J, Doumatey AP, et al. UGT1A1 is a major locus influencing bilirubin levels in African Americans. European journal of human genetics: EJHG. 2012;20(4):463-8. doi: 10.1038/ejhg.2011.206 PMID: 22085899; PubMed Central PMCID: PMC3306855.
36. Jones DP, Sosa FR, Shartsis J, Shah PT, Skromak E, Beher WT. Serum cholesterol esterifying and cholesteryl ester hydrolyzing activities in liver diseases: relationships to cholesterol, bilirubin, and bile salt concentrations. The Journal of clinical investigation. 1971;50(2):259-65. doi: 10.1172/JCI106490 PMID: 5540164; PubMed Central PMCID: PMC291919.
37. Reue K, Zhang P. The lipin protein family: dual roles in lipid biosynthesis and gene expression. FEBS letters. 2008;582(1):90-6. doi: 10.1016/j.febslet.2007.11.014 PMID: 18023282; PubMed Central PMCID: PMC2848953.
38. Phan J, Reue K. Lipin, a lipodystrophy and obesity gene. Cell metabolism. 2005;1(1):73-83. doi: 10. 1016/j.cmet.2004.12.002 PMID: 16054046.
39. Chang YC, Chang LY, Chang TJ, Jiang YD, Lee KC, Kuo SS, et al. The associations of LPIN1 gene expression in adipose tissue with metabolic phenotypes in the Chinese population. Obesity. 2010;18(1):7-12. doi: 10.1038/oby.2009.198 PMID: 19543209.
40. Fajas L, Auboeuf D, Raspe E, Schoonjans K, Lefebvre AM, Saladin R, et al. The organization, promoter analysis, and expression of the human PPARgamma gene. The Journal of biological chemistry. 1997;272(30):18779-89. PMID: 9228052.
41. Maeda K, Okubo K, Shimomura I, Funahashi T, Matsuzawa Y, Matsubara K. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (AdiPose Most abundant Gene transcript 1). Biochemical and biophysical research communications. 1996;221(2):286-9. doi: 10.1006/bbrc.1996. 0587 PMID: 8619847.
42. Akiyama TE, Sakai S, Lambert G, Nicol CJ, Matsusue K, Pimprale S, et al. Conditional disruption of the peroxisome proliferator-activated receptor gamma gene in mice results in lowered expression of ABCA1, ABCG1, and apoE in macrophages and reduced cholesterol efflux. Molecular and cellular biology. 2002;22(8):2607-19. PMID: 11909955; PubMed Central PMCID: PMC133709.
43. Evans RM, Barish GD, Wang YX. PPARs and the complex journey to obesity. Nature medicine. 2004;10(4):355-61. doi: 10.1038/nm1025 PMID: 15057233.
44. Zhang J, Fu M, Cui T, Xiong C, Xu K, Zhong W, et al. Selective disruption of PPARgamma 2 impairs the development of adipose tissue and insulin sensitivity. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(29):10703-8. doi: 10.1073/pnas.0403652101 PMID: 15249658; PubMed Central PMCID: PMC489998.
45. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nature medicine. 2002;8(11):1288-95. doi: 10.1038/nm788 PMID: 12368907.
46. Kallen JA, Schlaeppi JM, Bitsch F, Geisse S, Geiser M, Delhon I, et al. X-ray structure of the hRORalpha LBD at 1.63 A: structural and functional data that cholesterol or a cholesterol derivative is the natural ligand of RORalpha. Structure. 2002;10(12):1697-707. PMID: 12467577.
47. Willson TM. RORalpha: an orphan nuclear receptor on a high-cholesterol diet. Structure. 2002;10(12):1605-6. PMID: 12467566.
48. Bitsch F, Aichholz R, Kallen J, Geisse S, Fournier B, Schlaeppi JM. Identification of natural ligands of retinoic acid receptor-related orphan receptor alpha ligand-binding domain expressed in Sf9 cells-a mass spectrometry approach. Analytical biochemistry. 2003;323(1):139-49. PMID: 14622968.
49. Pathak P, Li T, Chiang JY. Retinoic acid-related orphan receptor alpha regulates diurnal rhythm and fasting induction of sterol 12alpha-hydroxylase in bile acid synthesis. The Journal of biological chemistry. 2013;288(52):37154-65. doi: 10.1074/jbc. M113.485987 PMID: 24226095; PubMed Central PMCID: PMC3873570.
50. Kathiresan S, Manning AK, Demissie S, D'Agostino RB, Surti A, Guiducci C, et al. A genome-wide association study for blood lipid phenotypes in the Framingham Heart Study. BMC medical genetics. 2007;8 Suppl 1:S17. doi: 10.1186/1471-2350-8-S1-S17 PMID: 17903299; PubMed Central PMCID: PMC1995614.
51. Johansen T, Hansen HS, Richelsen B, Malmlof R. The obese Gottingen minipig as a model of the metabolic syndrome: dietary effects on obesity, insulin sensitivity, and growth hormone profile. Comparative medicine. 2001;51(2):150-5. PMID: 11922179.
52. Kogelman LJ, Kadarmideen HN, Mark T, Karlskov-Mortensen P, Bruun CS, Cirera S, et al. An f2 pig resource population as a model for genetic studies of obesity and obesity-related diseases in humans: design and genetic parameters. Frontiers in genetics. 2013;4:29. doi: 10.3389/fgene.2013.00029 PMID: 23515185; PubMed Central PMCID: PMC3600696.
53. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clinical chemistry. 1972;18(6):499-502. PMID: 4337382
54. Guérin M, Dolphin PJ, Chapman MJ. A new in vitro method for the simultaneous evaluation of cholesteryl ester exchange and mass transfer between HDL and apoB-containing lipoprotein subspecies. Identification of preferential cholesteryl ester acceptors in human plasma. Arteriosclerosis, Thrombosis, and Vascular Biology. 1994;14(2):199-206.
55. Gilmour AR, Gogel B, Cullis B, Thompson R. ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead, UK. 2009.
56. Badke YM, Bates RO, Ernst CW, Schwab C, Steibel JP. Estimation of linkage disequilibrium in four US pig breeds. BMC genomics. 2012;13:24. doi: 10.1186/1471-2164-13-24 PMID: 22252454; PubMed Central PMCID: PMC3269977.
57. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, et al. The human genome browser at UCSC. Genome research. 2002;12(6):996-1006. doi: 10.1101/gr.229102 Article published online before print in May 2002. PMID: 12045153; PubMed Central PMCID: PMC186604.