Transcript profiling of candidate genes in testis of pigs exhibiting large differences in androstenone levels

BMC Genetics

Volumn 11, Issue , 2010, Pages

  Grindflek, Eli ^a   Berget, Ingunn ^b   Moe, Maren ^a   Oeth, Paul ^c   Lien, Sigbjørn ^b  

^a Norsvin   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c SEQUENOM INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

17BETA HYDROXYSTEROID DEHYDROGENASE 4; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ALDO KETO REDUCTASE FAMILY 1 MEMBER C4; ANDROSTENONE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYTOCHROME B5; CYTOCHROME P450C17; FERRITIN LIGHT POLYPEPTIDE; GENE PRODUCT; NUCLEAR RECEPTOR COACTIVATOR 4; PROGESTERONE RECEPTOR MEMBRANE COMPONENT 1; SEX HORMONE; SHORT CHAIN DEHYDROGENASE REDUCTASE FAMILY MEMBER 4; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELIN PHOSPHODIESTERASE 1; STEROID 21 MONOOXYGENASE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; SULFOTRANSFERASE FAMILY 2A DEHYDROEPIANDROSTERONE PREFERRING MEMBER 1; TESTOSTERONE 17BETA DEHYDROGENASE; UNCLASSIFIED DRUG; 3 (HEXADEC 2 YNYLSULFONYLMETHYL)ANDROST 5 EN 17 ONE; 3-(HEXADEC-2-YNYLSULFONYLMETHYL)ANDROST-5-EN-17-ONE; ANDROSTANE DERIVATIVE; COMPLEMENTARY DNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BOAR (MALE PIG); CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; MALE; NONHUMAN; POLYMERASE CHAIN REACTION; RNA EXTRACTION; SINGLE NUCLEOTIDE POLYMORPHISM; TISSUE LEVEL; UPREGULATION; ALLELE; ANIMAL; CHEMISTRY; DNA MICROARRAY; GENETICS; GENOTYPE; METABOLISM; PHENOTYPE; SWINE; TESTIS;

SUIDAE;

ALLELES; ANDROSTENES; ANIMALS; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDIES; GENOTYPE; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SUS SCROFA; TESTIS;

EID: 76949096894     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-11-4     Document Type: Article

References (66)

1. Claus R, Weiler U, Herzog A. Physiological aspects of androstenone and skatole formation in the boar--A review with experimental data. Meat Science 1994, 38(2):289-305.
2. 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.
3. Brooks RI, Pearson AM. Steroid hormone pathways in the pig, with special emphasis on boar odor: a review. J Anim Sci 1986, 62(3):632-645.
4. Willeke H. Possibilities of breeding for low 5α-androstenone content in pigs. Pigs news and information 1993, 14:31-33.
5. Tajet H, Andresen T, Meuwissen T. Prevention of boar taint in pig production: the 19th symposium of the nordic committee for veterinary scientific cooperation Gardermoen, Norway. Acta Veterinaria Scandinavica Supplement 2005, 48(Suppl 1):P1-6. S1-16.
6. Robic A, Larzul C, Bonneau M. Genetic and metabolic aspects of androstenone and skatole deposition in pig adipose tissue: a review. Genet Sel Evol 2008, 40(1):129-143. 2674915, 18096119.
7. Zamaratskaia G, Squires J. Biochemical, nutritional and genetic effects on boar taint in entire male pigs. Animal 2009, 3(11):1508-1521.
8. 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.
9. Morley M, Molony CM, Weber TM, Devlin JL, Ewens KG, Spielman RS, Cheung VG. Genetic analysis of genome-wide variation in human gene expression. Nature 2004, 430(7001):743-747. 10.1038/nature02797, 15269782.
10. Stranger BE, Forrest MS, Clark AG, Minichiello MJ, Deutsch S, Lyle R, Hunt S, Kahl B, Antonarakis SE, Tavare S, et al. Genome-wide associations of gene expression variation in humans. PLoS Genet 2005, 1(6):e78. 10.1371/journal.pgen.0010078, 1315281,1315281, 16362079.
11. 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). 2723134, 19575819.
12. Lo HS, Wang Z, Hu Y, Yang HH, Gere S, Buetow KH, Lee MP. Allelic variation in gene expression is common in the human genome. Genome Res 2003, 13(8):1855-1862. 403776, 12902379.
13. Katkov T, Gower DB. The biosynthesis of androst-16-enes in boar testis tissue. Biochem J 1970, 117(3):533-538. 1178957, 4392931.
14. Meadus W, Mason J, Squires E. Cytochrome P450c17 from porcine and bovine adrenal catalyses the formation of 5,16-androstadien-3 beta-ol from pregnenolone in the presence of cytochrome b5. J Steroid Biochem Mol Biol 1993, 46(5):565-572. 10.1016/0960-0760(93)90183-W, 8240978.
15. Lin Z, Lou Y, Peacock J, Squires EJ. A novel polymorphism in the 5' untranslated region of the porcine cytochrome b5 (CYB5) gene is associated with decreased fat androstenone level. Mamm Genome 2005, 16(5):367-373. 10.1007/s00335-004-2439-4, 16104384.
16. Davis S, Squires E. Association of cytochrome b5 with 16-androstene steroid synthesis in the testis and accumulation in the fat of male pigs. J Anim Sci 1999, 77(5).
17. Zamaratskaia G, Lou Y, Peacock J, Rydhmer L, Andersson HK, Juneja RK, Chen G, Lundstrom K, Squires EJ. Effect of polymorphism in the porcine cytochrome b5 (CYB5A) gene on androstenone and skatole concentrations and sexual development in Swedish pig populations. Animal 2008, 2(2):190-196.
18. VanDerMark PK, Steggles AW. The isolation and characterization of the soluble and membrane-bound porcine cytochrome b5 cDNAs. Biochem Biophys Res Commun 1997, 240(1):80-83. 10.1006/bbrc.1997.7599, 9367886.
19. Giordano SJ, Steggles AW. Differential expression of the mRNAs for the soluble and membrane-bound forms of rabbit cytochrome b5. Biochim Biophys Acta 1993, 1172(1-2):95-100.
20. Peacock J, Lou Y, Lundstrom K, Squires EJ. The effect of a c.-8G>T polymorphism on the expression of cytochrome b5A and boar taint in pigs. Anim Genet 2008, 39(1):15-21. 10.1111/j.1365-2052.2007.01674.x, 18162105.
21. Schenkman JB, Jansson I. The many roles of cytochrome b5. Pharmacol Ther 2003, 97(2):139-152. 10.1016/S0163-7258(02)00327-3, 12559387.
22. Bonfils C, Balny C, Maurel P. Direct evidence for electron transfer from ferrous cytochrome b5 to the oxyferrous intermediate of liver microsomal cytochrome P-450 LM2. J Biol Chem 1981, 256(18):9457-9465.
23. Hentze MW, Kuhn LC. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA 1996, 93(16):8175-8182. 10.1073/pnas.93.16.8175, 38642, 8710843.
24. Lin Z, Lou Y, Squires EJ. Identification of a single nucleotide polymorphism in porcine testis cytochrome P450-c17 (CYP17) and its effect on steroidogenesis. Biochem Genet 2005, 43(9-10):531-542. 10.1007/s10528-005-8169-9, 16341769.
25. Christenson LK, Strauss JF. Steroidogenic acute regulatory protein (StAR) and the intramitochondrial translocation of cholesterol. Biochim Biophys Acta 2000, 1529(1-3):175-187.
26. 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.
27. Pilon N, Daneau I, Brisson C, Ethier JF, Lussier JG, Silversides DW. Porcine and bovine steroidogenic acute regulatory protein (StAR) gene expression during gestation. Endocrinology 1997, 138(3):1085-1091. 10.1210/en.138.3.1085, 9048613.
28. Blomberg LA, Zuelke KA. Expression analysis of the steroidogenic acute regulatory protein (STAR) gene in developing porcine conceptuses. Mol Reprod Dev 2005, 72(4):419-429. 10.1002/mrd.20369, 16155961.
29. Irusta G, Parborell F, Peluffo M, Manna PR, Gonzalez-Calvar SI, Calandra R, Stocco DM, Tesone M. Steroidogenic acute regulatory protein in ovarian follicles of gonadotropin-stimulated rats is regulated by a gonadotropin-releasing hormone agonist. Biol Reprod 2003, 68(5):1577-1583. 10.1095/biolreprod.102.009944, 12606484.
30. Greger D, Antle S, Plath-Gabler A, Gutshall K, Mills E, Hammerstedt R, Hagen D, Baumrucker C. Identification of a porcine CYP11A1 polymorphism and associations with steroid concentrations and reproductive traits in pigs. Plant & Animal Genome IX Conference, San Diego, CA 2001,
31. 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.
32. Sinclair PA, Squires EJ. Testicular sulfoconjugation of the 16-androstene steroids by hydroxysteroid sulfotransferase: its effect on the concentrations of 5alpha-androstenone in plasma and fat of the mature domestic boar. J Anim Sci 2005, 83(2):358-365.
33. Sinclair P, Gilmore W, Lin Z, Lou Y, Squires E. Molecular cloning and regulation of porcine SULT2A1: relationship between SULT2A1 expression and sulfoconjugation of androstenone. J Mol Endocrinol 2006, 36(2):301-311. 10.1677/jme.1.01847, 16595701.
34. 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.
35. Carstensen JF, Tesdorpf JG, Kaufmann M, Markus MM, Husen B, Leenders F, Jakob F, de Launoit Y, Adamski J. Characterization of 17 beta-hydroxysteroid dehydrogenase IV. J Endocrinol 1996, 150(Suppl):S3-12.
36. Kaufmann M, Carstensen J, Husen B, Adamski J. The tissue distribution of porcine 17 beta-estradiol dehydrogenase and its induction by progesterone. J Steroid Biochem Mol Biol 1995, 55(5-6):535-539. 10.1016/0960-0760(95)00203-0, 8547179.
37. Adamski J, Normand T, Leenders F, Monte D, Begue A, Stehelin D, Jungblut PW, de Launoit Y. Molecular cloning of a novel widely expressed human 80 kDa 17 beta-hydroxysteroid dehydrogenase IV. Biochem J 1995, 311(Pt 2):437-443. 1136019, 7487879.
38. Chen G, Bourneuf E, Marklund S, Zamaratskaia G, Madej A, Lundstrom K. Gene expression of 3{beta}-hydroxysteroid dehydrogenase and 17{beta}-hydroxysteroid dehydrogenase in relation to androstenone, testosterone, and estrone sulphate in gonadally-intact male and castrated pigs. J Anim Sci 2007, 85(10):2457-2463. 10.2527/jas.2007-0087, 17609472.
39. Penning TM, Burczynski ME, Jez JM, Hung CF, Lin HK, Ma H, Moore M, Palackal N, Ratnam K. Human 3alpha-hydroxysteroid dehydrogenase isoforms (AKR1C1-AKR1C4) of the aldo-keto reductase superfamily: functional plasticity and tissue distribution reveals roles in the inactivation and formation of male and female sex hormones. Biochem J 2000, 351(Pt 1):67-77. 10.1042/0264-6021:3510067, 1221336, 10998348.
40. Penning TM. Molecular endocrinology of hydroxysteroid dehydrogenases. Endocr Rev 1997, 18(3):281-305. 10.1210/er.18.3.281, 9183566.
41. Matsunaga T, Endo S, Maeda S, Ishikura S, Tajima K, Tanaka N, Nakamura KT, Imamura Y, Hara A. Characterization of human DHRS4: an inducible short-chain dehydrogenase/reductase enzyme with 3beta-hydroxysteroid dehydrogenase activity. Arch Biochem Biophys 2008, 477(2):339-347. 10.1016/j.abb.2008.06.002, 18571493.
42. Michalik L, Auwerx J, Berger JP, Chatterjee VK, Glass CK, Gonzalez FJ, Grimaldi PA, Kadowaki T, Lazar MA, O'Rahilly S, et al. International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacol Rev 2006, 58(4):726-741. 10.1124/pr.58.4.5, 17132851.
43. Moe M, Grindflek E, Doran O. Expression of 3{beta}-hydroxysteroid dehydrogenase, cytochrome P450c17 and sulfotransferase 2B1 proteins in liver and testis of pigs of two breeds: relationship with adipose tissue androstenone concentration. J Anim Sci 2007, 85(11):2924-2931. 10.2527/jas.2007-0283, 17686889.
44. Xue J, Dial G, Holton E, Vickers Z, Squires E, Lou Y, Godbout D, Morel N. Breed differences in boar taint: relationship between tissue levels boar taint compounds and sensory analysis of taint. Journal of Anim Science 1996, 74(9):2170-2177.
45. Cue R, Nicolau-Solano S, McGivan J, Wood J, Doran O. Breed-associated variations in the sequence of the pig 3beta-hydroxysteroid dehydrogenase gene. Journal of Animal Science 2007, 85(3):571-576. 10.2527/jas.2006-366, 17060418.
46. Claus R, Hoffman B. Oestrogens, compared to other steroids of testicular origin, in bloodplasma of boars. Acta Endocrinologica 1980, 94:404-411.
47. Corbin CJ, Khalil MW, Conley AJ. Functional ovarian and placental isoforms of porcine aromatase. Mol Cell Endocrinol 1995, 113(1):29-37. 10.1016/0303-7207(95)03607-9, 8674811.
48. Cahill MA. Progesterone receptor membrane component 1: An integrative review. J Steroid Biochem Mol Biol 2007, 105(1-5):16-36. 10.1016/j.jsbmb.2007.02.002, 17583495.
49. 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.
50. 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.
51. New MI. Steroid 21-hydroxylase deficiency (congenital adrenal hyperplasia). Am J Med 1995, 98(1A):2S-8S. 10.1016/S0002-9343(99)80052-7, 7825636.
52. Payne AH, Youngblood GL. Regulation of expression of steroidogenic enzymes in Leydig cells. Biol Reprod 1995, 52(2):217-225. 10.1095/biolreprod52.2.217, 7711191.
53. Doran E, Whittington FM, Wood JD, McGivan JD. Characterisation of androstenone metabolism in pig liver microsomes. Chem Biol Interact 2004, 147(2):141-149. 10.1016/j.cbi.2003.12.002, 15013816.
54. Nicolau-Solano S, McGivan J, Whittington F, Nieuwhof G, Wood J, Doran O. Relationship between the expression of hepatic but not testicular 3beta-hydroxysteroid dehydrogenase with androstenone deposition in pig adipose tissue. J Anim Sci 2006, 84(10):2809-2817. 10.2527/jas.2005-595, 16971583.
55. Yeh S, Chang C. Cloning and characterization of a specific coactivator, ARA70, for the androgen receptor in human prostate cells. Proc Natl Acad Sci USA 1996, 93(11):5517-5521. 10.1073/pnas.93.11.5517, 39278, 8643607.
56. Yeh S, Miyamoto H, Shima H, Chang C. From estrogen to androgen receptor: a new pathway for sex hormones in prostate. Proc Natl Acad Sci USA 1998, 95(10):5527-5532. 10.1073/pnas.95.10.5527, 20411, 9576916.
57. Santana P, Llanes L, Hernandez I, Gallardo G, Quintana J, Gonzalez J, Estevez F, Ruiz de Galarreta C, Fanjul LF. Ceramide mediates tumor necrosis factor effects on P450-aromatase activity in cultured granulosa cells. Endocrinology 1995, 136(5):2345-2348. 10.1210/en.136.5.2345, 7720683.
58. Yan H, Yuan W, Velculescu VE, Vogelstein B, Kinzler KW. Allelic variation in human gene expression. Science 2002, 297(5584):1143. 10.1126/science.1072545, 12183620.
59. Agca C, Ries JE, Kolath SJ, Kim JH, Forrester LJ, Antoniou E, Whitworth KM, Mathialagan N, Springer GK, Prather RS, et al. Luteinization of porcine preovulatory follicles leads to systematic changes in follicular gene expression. Reproduction 2006, 132(1):133-145. 10.1530/rep.1.01163, 16816339.
60. 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.
61. Andresen T. Development of radioimunoassay for 5alpha-adrost-16-en-3-one in pig peripheral plasma. Acta endochrinologia 1974, 76:377-387.
62. Ding C, Cantor CR. A high-throughput gene expression analysis technique using competitive PCR and matrix-assisted laser desorption ionization time-of-flight MS. Proc Natl Acad Sci USA 2003, 100(6):3059-3064. 10.1073/pnas.0630494100, 152246, 12624187.
63. Elvidge G, Price T, Glenny L, Ragoussis J. Development and evaluation of real competitive PCR for high-throughput quantitative applications. Anal Biochem 2005, 339(2):231-241. 10.1016/j.ab.2005.01.040, 15797563.
64. Jurinke C, Oeth P, Boom D. MALDI-TOF mass spectrometry: a versatile tool for high-performance DNA analysis. Molecular Biotechnology 2004, 26:147-164. 10.1385/MB:26:2:147, 14764940.
65. SAS SAS 9.1.3. Help and Documentation. 2007, Cary, NC: SAS Institute Inc, SAS.
66. 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.