Large scale genome-wide association and LDLA mapping study identifies QTLs for boar taint and related sex steroids

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Grindflek, Eli ^a   Lien, Sigbjørn ^b   Hamland, Hanne ^a,b   Hansen, Marianne H S ^a,b   Kent, Matthew ^b   van Son, Maren ^a   Meuwissen, Theo H E ^b  

^a Norsvin   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROSTENONE; ESTRADIOL; ESTROGEN; ESTRONE SULFATE; INDOLE; SEX HORMONE; SKATOLE; TESTOSTERONE; UNCLASSIFIED DRUG; ANDROST 16 EN 3 ONE; ANDROST-16-EN-3-ONE; ANDROSTANE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; BREED; CONTROLLED STUDY; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC LINKAGE; GENOTYPE; MALE; NONHUMAN; PHENOTYPE; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; SUBCUTANEOUS FAT; SWINE; ANIMAL; BREEDING; GENETICS; GENOME; MEAT; METABOLISM; STANDARD;

SUIDAE; SUS;

ANDROSTENES; ANIMALS; BREEDING; GENETIC LINKAGE; GENOME; GENOME-WIDE ASSOCIATION STUDY; GONADAL STEROID HORMONES; LINKAGE DISEQUILIBRIUM; MALE; MEAT; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SKATOLE; SWINE;

EID: 79960142302     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-362     Document Type: Article

References (63)

1. Babol J, Squires EJ. Quality of meat from entire male pigs. Food Research International 1995, 28(3):201-212.
2. Dijksterhuis GB, Engel B, Walstra P, Font i Furnols M, Agerhem H, Fischer K, Oliver MA, Claudi-Magnussen C, Siret F, Béague MP, Homer DB, Bonneau M. An international study on the importance of androstenone and skatole for boar taint: II. Sensory evaluation by trained panels in seven European countries. Meat Science 2000, 54(3):261-269.
3. Grindflek E, Meuwissen T, Aasmundstad T, Hamland H, Hansen M, Nome T, Kent M, Torjesen P, Lien S. Revealing genetic relationships between compounds affecting boar taint and reproduction in pigs. J Anim Sci 2011, 89(3):680-692. 10.2527/jas.2010-3290, 21346135.
4. Sellier P, Le Roy P, Fouilloux MN, Gruand J, Bonneau M. Responses to restricted index selection and genetic parameters for fat androstenone level and sexual maturity status of young boars. Livstestock Production Science 2000, 63:265-274.
5. Gower DB. 16-Unsaturated C 19 steroids. A review of their chemistry, biochemistry and possible physiological role. Journal of Steroid Biochemistry 1972, 3:45-103. 10.1016/0022-4731(72)90011-8, 4561286.
6. Hess RA. Estrogen in the adult male reproductive tract: a review. Reprod Biol Endocrinol 2003, 1:52. 10.1186/1477-7827-1-52, 179885, 12904263.
7. Zamaratskaia G, Madej A, Babol J, Squires E, Lundstrom K. Free oestrone in adipose tissue and its relation to androstenone and skatole in entire male pigs. Reprod Domest Anim 2005, 40(2):156-160. 10.1111/j.1439-0531.2005.00573.x, 15819967.
8. Zamaratskaia G, Rydhmer L, Chen G, Madej A, Andersson HK, Lundstrom K. Boar taint is related to endocrine and anatomical changes at puberty but not to aggressive behaviour in entire male pigs. Reprod Domest Anim 2005, 40(6):500-506. 10.1111/j.1439-0531.2005.00613.x, 16324073.
9. Walker WH. Non-classical actions of testosterone and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010, 365(1546):1557-1569. 10.1098/rstb.2009.0258, 2871922, 20403869.
10. Yokoyama MT, Carlson JR. Microbial metabolites of tryptophan in the intestinal tract with special reference to skatole. Am J Clin Nutr 1979, 32(1):173-178.
11. Lundström K, Malmfors B, Malmfors G, Petersson H, Stern S, Mortensen A, Sorensen S. Boar taint and bitter taste as affected by androstenone and skatole. 30th Eur Meeting of Meat Res Workers Bristol Proc 30th Eur Meeting of Meat Res Workers 1984, 379-398.
12. Vold E. Fleischproduktionseigenschaften bei ebern und kastraten. Meldinger fra Norges Landbrukshøgskole 1970, 49:1-25.
13. Rasmussen MK, Zamaratskaia G, Ekstrand B. In vivo effect of dried chicory root (Cichorium intybus L.) on xenobiotica metabolising cytochrome P450 enzymes in porcine liver. Toxicol Lett 2010,
14. Quintanilla R, Demeure O, Bidanel JP, Milan D, Iannuccelli N, Amigues Y, Gruand J, Renard C, Chevalet C, Bonneau M. Detection of quantitative trait loci for fat androstenone levels in pigs. J Anim Sci 2003, 81(2):385-394.
15. Lee GJ, Archibald AL, Law AS, Lloyd S, Wood J, Haley CS. Detection of quantitative trait loci for androstenone, skatole and boar taint in a cross between Large White and Meishan pigs. Anim Genet 2005, 36(1):14-22. 10.1111/j.1365-2052.2004.01214.x, 15670126.
16. Varona L, Vidal O, Quintanilla R, Gil M, Sánchez A, Folch J, Hortos M, Rius M, Amills M, Noguera J. Bayesian analysis of quantitative trait loci for boar taint in a Landrace outbred population. J Anim Sci 2005, 83(2):301-307.
17. Duijvesteijn N, Knol EF, Merks JW, Crooijmans RP, Groenen MA, Bovenhuis H, Harlizius B. A genome-wide association study on androstenone levels in pigs reveals a cluster of candidate genes on chromosome 6. BMC Genet 2010, 11(1):42. 2889844, 20487517.
18. Ramos AM, Crooijmans R, Affara NA, Amaral AJ, Archibald AL, Beever JE, Bendixen C, Churcher C, Clark R, Dehais P, Hansen MS, Hedegaard J, Hu ZL, Kerstens HH, Law AS, Megens HJ, Milan D, Nonneman DJ, Rohrer GA, Rothschild MF, Smith TPL, Schnabel RD, Van Tassell CP, Taylor JF, Wiedmann RT, Schook LB, Groenen MAM. Design of a High Density SNP Genotyping Assay in the Pig Using SNPs Identified and Characterized by Next Generation Sequencing Technology. PLoS One 2009, 4(8).
19. Gregersen V, Panitz F, Vingborg R, Sorensen K, Stengaard H, Buije Z, Hoj A, Grindflek E, Moe M, Lien S, Archibald A, Hastings N, Humphrey S, Rogers J, Dunham A, Bendixen C. Performance of a Genome-Wide 7 K Porcine SNP Chip. The 3rd International Symposium on Animal Functional Genomics: 7-9 April 2008; Edinburgh 2008,
20. Moe M, Meuwissen T, Lien S, Bendixen C, Wang X, Conley LN, Berget I, Tajet H, Grindflek E. Gene expression profiles in testis of pigs with extreme high and low levels of androstenone. BMC Genomics 2007, 8:405. 10.1186/1471-2164-8-405, 2204014, 17988377.
21. Moe M, Lien S, Bendixen C, Hedegaard J, Hornshoj H, Berget I, Meuwissen TH, Grindflek E. Gene expression profiles in liver of pigs with extreme high and low levels of androstenone. BMC Vet Res 2008, 4:29. 10.1186/1746-6148-4-29, 2535776, 18684314.
22. Tuomola M, Harpio R, Knuuttila P, Mikola H, Løvgren T. Time-resolved fluoroimmunoassay for the measurement of androstenone in porcine serum and fat samples. Journal of agricultural food chemistry 1997, 45:3529-3534.
23. Andresen T. Development of radioimunoassay for 5alpha-adrost-16-en-3-one in pig peripheral plasma. Acta endochrinologia 1974, 76:377-387.
24. Tuomola M, Vahva M, Kallio H. High-Performance liquid chromatography determination of skatole and indole levels in pig serum, subcutaneous fat and submaxillary salivary glands. Journal of agricultur food chemistry 1996, 44:1265-1270.
25. Green P, Falls K, Crooks S. Documentation for CRI-MAP, version 2.4. Washington University School of Medicine, St Louis, MO 1990,
26. Meuwissen TH, Goddard ME. Multipoint identity-by-descent prediction using dense markers to map quantitative trait loci and estimate effective population size. Genetics 2007, 176(4):2551-2560. 10.1534/genetics.107.070953, 1950654, 17565953.
27. Patterson H, Thompson R. Recovery of inter-block information when block sizes are unequal. Biometrika 1971, 58(3):545-554.
28. Piepho HP. A quick method for computing approximate thresholds for quantitative trait loci detection. Genetics 2001, 157(1):425-432. 1461497, 11139522.
29. R-Development-Core-Team R:A Language and Environment for Statistical Computing. R Foundation for Statistical Computing 2011, R-Development-Core-Team., http://www.R-project.org
30. Le Mignon G, Iannuccelli N, Robic A, Billon Y, Bidanel JP, Larzul C. Fine Mapping Of Quantitative Trait Loci For Androstenone And Skatole Levels In Pig. 9th WCGALP, 1-6 August, Leipzig, Germany 2010,
31. De Fabiani E, Mitro N, Gilardi F, Crestani M. Sterol-protein interactions in cholesterol and bile acid synthesis. Subcell Biochem 2010, 51:109-135. 10.1007/978-90-481-8622-8_4, 20213542.
32. Rodriguez-Agudo D, Ren S, Wong E, Marques D, Redford K, Gil G, Hylemon P, Pandak WM. Intracellular cholesterol transporter StarD4 binds free cholesterol and increases cholesteryl ester formation. J Lipid Res 2008, 49(7):1409-1419. 10.1194/jlr.M700537-JLR200, 2431108, 18403318.
33. Hu J, Zhang Z, Shen WJ, Azhar S. Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones. Nutr Metab (Lond) 2010, 7:47.
34. Gumus ZH, Du B, Kacker A, Boyle JO, Bocker JM, Mukherjee P, Subbaramaiah K, Dannenberg AJ, Weinstein H. Effects of tobacco smoke on gene expression and cellular pathways in a cellular model of oral leukoplakia. Cancer Prev Res (Phila) 2008, 1(2):100-111.
35. Diaz GJ, Squires EJ. Metabolism of 3-methylindole by porcine liver microsomes: responsible cytochrome P450 enzymes. Toxicol Sci 2000, 55(2):284-292. 10.1093/toxsci/55.2.284, 10828259.
36. Fan J, Traore K, Li W, Amri H, Huang H, Wu C, Chen H, Zirkin B, Papadopoulos V. Molecular mechanisms mediating the effect of mono-(2-ethylhexyl) phthalate on hormone-stimulated steroidogenesis in MA-10 mouse tumor Leydig cells. Endocrinology 2010, 151(7):3348-3362. 10.1210/en.2010-0010, 2903930, 20463053.
37. Horibata Y, Sugimoto H. StarD7 mediates the intracellular trafficking of phosphatidylcholine to mitochondria. J Biol Chem 2010, 285(10):7358-7365. 10.1074/jbc.M109.056960, 2844184, 20042613.
38. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21(2):263-265. 10.1093/bioinformatics/bth457, 15297300.
39. Bray JE, Marsden BD, Oppermann U. The human short-chain dehydrogenase/reductase (SDR) superfamily: a bioinformatics summary. Chem Biol Interact 2009, 178(1-3):99-109. 10.1016/j.cbi.2008.10.058, 19061874.
40. Payne AH, Hales DB. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 2004, 25(6):947-970. 10.1210/er.2003-0030, 15583024.
41. Lee JJ, Widmaier EP. Gene array analysis of the effects of chronic adrenocorticotropic hormone in vivo on immature rat adrenal glands. J Steroid Biochem Mol Biol 2005, 96(1):31-44. 10.1016/j.jsbmb.2005.01.026, 15890514.
42. Amills M, Vidal O, Varona L, Tomas A, Gil M, Sanchez A, Noguera JL. Polymorphism of the pig 2,4-dienoyl CoA reductase 1 gene (DECR1) and its association with carcass and meat quality traits. J Anim Sci 2005, 83(3):493-498.
43. Opperman LA, Saunders TJ, Bruns DE, Boyd JC, Mills SE, Bruns ME. Estrogen inhibits calbindin-D28k expression in mouse uterus. Endocrinology 1992, 130(3):1728-1735. 10.1210/en.130.3.1728, 1537319.
44. Stuart EB, Thompson JM, Rhees RW, Lephart ED. Steroid hormone influence on brain calbindin-D(28 K) in male prepubertal and ovariectomized rats. Brain Res Dev Brain Res 2001, 129(2):125-133.
45. Moeller G, Adamski J. Multifunctionality of human 17beta-hydroxysteroid dehydrogenases. Mol Cell Endocrinol 2006, 248(1-2):47-55. 10.1016/j.mce.2005.11.031, 16413960.
46. Wang J, Chai X, Eriksson U, Napoli JL. Activity of human 11-cis-retinol dehydrogenase (Rdh5) with steroids and retinoids and expression of its mRNA in extra-ocular human tissue. Biochem J 1999, 338(Pt 1):23-27. 1220019, 9931293.
47. Crawford RJ, Hammond VE, Connell JM, Coghlan JP. The structure and activity of two cytochrome P450c21 proteins encoded in the ovine adrenal cortex. J Biol Chem 1992, 267(23):16212-16218.
48. Picado-Leonard J, Miller WL. Cloning and sequence of the human gene for P450c17 (steroid 17 alpha-hydroxylase/17,20 lyase): similarity with the gene for P450c21. DNA 1987, 6(5):439-448. 10.1089/dna.1987.6.439, 3500022.
49. New MI. Steroid 21-hydroxylase deficiency (congenital adrenal hyperplasia). Am J Med 1995, 98(1A):2S-8S.
50. Grindflek E, Berget I, Moe M, Oeth P, Lien S. Transcript profiling of candidate genes in testis of pigs exhibiting large differences in androstenone levels. BMC Genet 2010, 11:4. 2823645, 20100319.
51. Cassady JP, Johnson RK, Pomp D, Rohrer GA, Van Vleck LD, Spiegel EK, Gilson KM. Identification of quantitative trait loci affecting reproduction in pigs. J Anim Sci 2001, 79(3):623-633.
52. Lanza D, Yost G. Selective dehydrogenation/oxygenation of 3-methylindole by cytochrome P450 enzymes. Drug Metabolism and Disposition 2001, 29(7):950-953.
53. Miller WL. Mitochondrial specificity of the early steps in steroidogenesis. J Steroid Biochem Mol Biol 1995, 55(5-6):607-616. 10.1016/0960-0760(95)00212-X, 8547188.
54. Wiebe MS, Nichols RJ, Molitor TP, Lindgren JK, Traktman P. Mice deficient in the serine/threonine protein kinase VRK1 are infertile due to a progressive loss of spermatogonia. Biol Reprod 2010, 82(1):182-193. 10.1095/biolreprod.109.079095, 2802121, 19696012.
55. Bahn A, Ljubojevic M, Lorenz H, Schultz C, Ghebremedhin E, Ugele B, Sabolic I, Burckhardt G, Hagos Y. Murine renal organic anion transporters mOAT1 and mOAT3 facilitate the transport of neuroactive tryptophan metabolites. Am J Physiol-Cell Physiol 2005, 289(5):C1075-C1084. 10.1152/ajpcell.00619.2004, 15944205.
56. Burckhardt BC, Burckhardt G. Transport of organic anions across the basolateral membrane of proximal tubule cells. Rev Physiol Biochem Pharmacol 2003, 146:95-158. 10.1007/s10254-002-0003-8, 12605306.
57. Li C, Tang Y, Li F, Turner S, Li K, Zhou X, Centola M, Yan X, Cao W. 17beta-estradiol (betaE2) protects human retinal Muller cell against oxidative stress in vitro: evaluation of its effects on gene expression by cDNA microarray. Glia 2006, 53(4):392-400. 10.1002/glia.20291, 16342170.
58. Babol J, Squires E, Lundström K. Hepatic metabolism of skatole in pigs by cytochrome P4502E1. J Anim Sci 1998, 76(3):822-828.
59. Skinner T, Doran E, McGivan J, Haley C, Archibald A. Cloning and mapping of the porcine cytochrome-p450 2E1 gene and its association with skatole levels in the domestic pig. Animal Genetics 2005, 36(5):417-422. 10.1111/j.1365-2052.2005.01342.x, 16167985.
60. Moe M, Lien S, Aasmundstad T, Meuwissen THE, Hansen MHS, Bendixen C, Grindflek E. Association between SNPs within candidate genes and compounds related to boar taint and reproduction. BMC Genetics 2009, 10(32).
61. Karacaören B, de Koning DJ, Velander I, Petersen S, Haley CS, Archibald AL. Alternative Association Analyses on Boar Taint using Discordant Sib Pairs Experimental Design. Proc 60th EAAP, Barcelona, Spain 2009,
62. Christoffersen BO, Gade LP, Golozoubova V, Svendsen O, Raun K. Influence of castration-induced testosterone and estradiol deficiency on obesity and glucose metabolism in male Gottingen minipigs. Steroids 2010, 75(10):676-684. 10.1016/j.steroids.2010.04.004, 20420845.
63. Christenson LK, Strauss JF. Steroidogenic acute regulatory protein (StAR) and the intramitochondrial translocation of cholesterol. Biochim Biophys Acta 2000, 1529(1-3):175-187.