Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T11:14:45.821Z Has data issue: false hasContentIssue false

Effect of polymorphism in the porcine cytochrome b5 (CYB5A) gene on androstenone and skatole concentrations and sexual development in Swedish pig populations

Published online by Cambridge University Press:  01 February 2008

G. Zamaratskaia*
Affiliation:
Department of Food Science, Swedish University of Agricultural Sciences, Box 7051, SE-750 07 Uppsala, Sweden
Y. Lou
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ont., Canada, N1G 2W1
J. Peacock
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ont., Canada, N1G 2W1
L. Rydhmer
Affiliation:
Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Box 7023, SE-750 07 Uppsala, Sweden
H. K. Andersson
Affiliation:
Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, Box 7023, SE-750 07 Uppsala, Sweden
R. K. Juneja
Affiliation:
Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Box 7023, SE-750 07 Uppsala, Sweden
G. Chen
Affiliation:
Department of Food Science, Swedish University of Agricultural Sciences, Box 7051, SE-750 07 Uppsala, Sweden
K. Lundström
Affiliation:
Department of Food Science, Swedish University of Agricultural Sciences, Box 7051, SE-750 07 Uppsala, Sweden
E. J. Squires
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ont., Canada, N1G 2W1
Get access

Abstract

The present study investigated the presence of a single-nucleotide polymorphism (G > T) at base −8 upstream of ATG in 5′ untranslated region of cytochrome b5 (CYB5A) gene in Swedish pig populations and evaluated the significance of this polymorphism for androstenone and skatole levels, sexual development and performance parameters in pigs. Frequencies of the T allele were 6.7% for Swedish Yorkshire × Landrace crossbred pigs (n = 245), 6.5% for Swedish Yorkshire (n = 99) and 12.8% for Landrace breed (n = 74). No deviations from Hardy–Weinberg equilibrium were observed in the investigated populations. In Swedish Yorkshire × Landrace crossbred entire male pigs (n = 193), plasma samples were analysed for skatole, androstenone, testosterone and oestrone sulphate, and fat samples were analysed for androstenone, skatole and free oestrone. Additionally, testis weight and bulbourethral gland length for crossbred pigs were recorded. Plasma androstenone levels were significantly lower in the G/T genotype at 90 kg live weight compared with the wild G/G genotype at the same live weight (P = 0.006). In heavier pigs, plasma androstenone levels did not differ between genotypes (P = 0.382). Fat androstenone levels were not affected by CYB5A genotype (P = 0.252). Skatole levels in the G/T genotype at 115 kg live weight were lower compared with those in the G/G genotype in plasma (P = 0.048) and fat (P = 0.028), although no differences were observed in lighter pigs. Testis weight, bulbourethral gland length, testosterone and oestrone sulphate levels in plasma, and oestrone levels in fat were not affected by genotype. We concluded that the presence of the T allele in the CYB5A gene resulted in lower androstenone levels in plasma, and lower skatole levels in fat and plasma; this reduction, however, was dependent on the live weight of the animals. Reproductive hormones and growth rate did not differ between the pigs of different genotypes, whereas a higher lean meat content was found in the G/T genotype in comparison with the G/G genotype. The practical application of those results in Sweden is doubtful because of lack of the effect on androstenone in fat and the low frequency of the T allele in the studied Swedish pig populations.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akhtar, MK, Kelly, SL, Kaderbhai, MA 2005. Cytochrome b5 modulation of 17α- hydroxylase and 17–20 lyase (CYP17) activities in steroidogenesis. Journal of Endocrinology 187, 267274.CrossRefGoogle ScholarPubMed
Andersson, HK, Andersson, K, Zamaratskaia, G, Rydhmer, L, Chen, G, Lundström, K 2005. Effect of single-sex or mixed raising and live weight on performance, technological meat quality and sexual maturity in entire male and female pigs fed raw potato starch. Acta Agriculturae Scandinavica 55, 8090.CrossRefGoogle Scholar
Babol, J, Zamaratskaia, G, Juneja, K, Lundström, K 2004. The effect of age on distribution of skatole and indole levels in entire male pigs in four breeds: Yorkshire, Landrace, Hampshire and Duroc. Meat Science 67, 351358.CrossRefGoogle ScholarPubMed
Bonneau, M 1987. Effects of age and live weight on fat 5 alpha-androstenone levels in young boars fed two planes of nutrition. Reproduction, Nutrition, Development 27, 413422.CrossRefGoogle ScholarPubMed
Booth, WD, White, CA 1988. The isolation, purification and some properties of pheromaxein, the pheromonal steroid-binding protein, in porcine submaxillary glands and saliva. Journal of Endocrinology 118, 4757.CrossRefGoogle ScholarPubMed
Chen, G, Zamaratskaia, G, Andersson, HK, Lundström, K 2007a. Effect of dietary supplement of raw potato starch and live weight on the levels of skatole, indole and androstenone measured by different methods. Food Chemistry 101, 439448.CrossRefGoogle Scholar
Chen G, Cue RA, Lundstrom K, Wood JD and Doran O 2007b. Regulation of cytochrome P450 2A6 protein expression by skatole, indole and testicular steroids in primary cultured pig hepatocytes. Drug Metabolism and Disposition, in press.CrossRefGoogle Scholar
Claus, R, Lösel, D, Lacorn, M, Mentschel, J, Schenkel, H 2003. Effects of butyrate on apoptosis in the pig colon and its consequences for skatole formation and tissue accumulation. Journal of Animal Science 81, 239248.CrossRefGoogle ScholarPubMed
Davis, SM, Squires, EJ 1999. Association of cytochrome b5 with 16-androstene steroid synthesis in the testis and accumulation in the fat of male pigs. Journal of Animal Science 77, 12301235.CrossRefGoogle ScholarPubMed
Diaz, GJ, Squires, EJ 2000. Metabolism of 3-methylindole by porcine liver microsomes: responsible cytochrome P450 enzymes. Toxicological Sciences 55, 284292.CrossRefGoogle ScholarPubMed
Doran, E, Whittington, FW, Wood, JD, McGivan, JD 2002. Cytochrome P450IIE1 (CYP2E1) is induced by skatole and this induction is blocked by androstenone in isolated pig hepatocytes. Chemico-Biological Interactions 140, 8192.CrossRefGoogle ScholarPubMed
Gower, DB 1972. 16-Unsaturated C 19 steroids. A review of their chemistry, biochemistry and possible physiological role. Journal of Steroid Biochemistry 3, 45103.CrossRefGoogle Scholar
Hansen, LL, Larsen, AE, Jensen, BB, Hansen-Møller, J, Barton-Gade, P 1994. Influence of stocking rate and faeces deposition in the pen at different temperatures on skatole concentration (boar taint) in subcutaneous fat. Animal Production 59, 99110.Google Scholar
Hansen, LL, Lundström, K, Laue, A, Jensen, MT, Agergaard, N, Bæk, 1997. Skatole and androstenone patterns during the growth period from 90 to 120 kg live weight in pigs with high or low skatole levels in back fat at slaughter. In Boar taint in entire male pigs (ed. M Bonneau, K Lundström and B Malmfors), EAAP publication no. 92, pp. 100103. Wageningen Pers, The Netherlands.Google Scholar
Lin, Z, Lou, Y, Peacock, J, Squires, EJ 2004a. Molecular cloning and functional analysis of porcine SULT1A1 gene and its variant: a single mutation SULT1A1 causes a significant decrease in sulfation activity. Mammalian Genome 5, 218226.CrossRefGoogle Scholar
Lin, Z, Lou, Y, Peacock, J, Squires, EJ 2004b. Molecular cloning, expression and functional characterization of the cytochrome P450 2A6 gene in pig liver. Animal Genetics 35, 314316.CrossRefGoogle ScholarPubMed
Lin, Z, Lou, Y, Peacock, J, Squires, EJ 2005. A novel polymorphism in the 5′ untranslated region of the porcine cytochrome b5 (CYB5) gene is associated with decreased fat androstenone level. Mammalian Genome 16, 367373.CrossRefGoogle ScholarPubMed
Lin, Z, Lou, Y, Squires, EJ 2006. Functional polymorphism in porcine CYP2E1 gene: Its association with skatole levels. Journal of Steroid Biochemistry and Molecular Biology 99, 231237.CrossRefGoogle ScholarPubMed
Lundström, K, Malmfors, B, Hansson, I, Edqvist, L-E, Gahne, B 1978. 5α-Androstenone and testosterone in boars. Swedish Journal of Agricultural Research 8, 171178.Google Scholar
Meadus, WJ, Mason, JI, Squires, EJ 1993. Cytochrome P450c17 from porcine and bovine adrenal catalyses the formation of 5,16 androstadien-3b-ol from pregnenolone in the presence of cytochrome b5. Journal of Steroid Biochemistry and Molecular Biology 46, 565572.CrossRefGoogle ScholarPubMed
Mortensen AB and Sørensen SE 1984. Relationship between boar taint and skatole determination with a new analysis method. Proceedings of 30th European Meeting of Meat Research Workers, Bristol, UK, pp. 394–396.Google Scholar
Pandey, AV, Miller, WL 2005. Regulation of 17,20 lyase activity by cytochrome b5 and by serine phosphorylation of P450c17. The Journal of Biological Chemistry 280, 1326513271.CrossRefGoogle ScholarPubMed
Peacock J, Lou Y, Lundström K and Squires EJ 2007. The effect of a −8G > T polymorphism on the expression of cytochrome b5 and boar taint in pigs. Animal Genetics, in press.CrossRef+T+polymorphism+on+the+expression+of+cytochrome+b5+and+boar+taint+in+pigs.+Animal+Genetics,+in+press.>Google Scholar
Pedersen, B 1998. Heritability of skatole in back fat. In Skatole and boar taint (ed. WK Jensen), pp. 129136. Roskilde, Denmark.Google Scholar
Quintanilla, R, Demeure, O, Bidanel, JP, Milan, D, Iannuccelli, N, Amigues, Y, Gruand, J, Renard, C, Chevalet, C, Bonneau, M 2003. Detection of quantitative trait loci for fat androstenone levels in pigs. Journal of Animal Science 81, 385394.CrossRefGoogle ScholarPubMed
Sellier, P 1998. Genetics of meat and carcass traits. In The genetics of the pig (ed. MF Rothschild and A Ruvinsky), pp. 463510. CAB International, Wallingford, Oxon, UK.Google Scholar
Sinclair, PA, Squires, EA, Raeside, JI, Britt, JH, Hedgpeth, VG 2001. The effect of early postnatal treatment with a gonadotropin-releasing hormone agonist on the developmental profiles of testicular steroid hormones in the intact male pig. Journal of Animal Science 79, 10031010.CrossRefGoogle ScholarPubMed
Skinner, TM, Doran, E, McGivan, JD, Haley, CS, Archibald, AL 2005. Cloning and mapping of the porcine cytochrome-p450 2E1 gene and its association with skatole levels in the domestic pig. Animal Genetics 36, 417422.CrossRefGoogle ScholarPubMed
Skinner, TM, Anderson, JA, Haley, CS, Archibald, AL 2006. Assessment of SULT1A1, CYP2A6 and CYP2C18 as candidate genes for elevated backfat skatole levels in commercial and experimental pig populations. Animal Genetics 37, 521522.CrossRefGoogle ScholarPubMed
Statistical Analysis Systems Institute 2004. Version 9.1. SAS Institute, Cary, NC, USA.Google Scholar
Tambyrajah, WS, Doran, E, Wood, JD, McGivan, JD 2004. The pig CYP2E1 promoter is activated by COUP-TF1 and HNF-1 and is inhibited by androstenone. Archives of Biochemistry and Biophysics 431, 252260.CrossRefGoogle ScholarPubMed
Walstra, P, Claudi-Magnussen, C, Chevillon, P, Von Seth, G, Diestre, A, Matthews, KR, Homer, DB, Bonneau, M 1999. An international study on the importance of androstenone and skatole for boar taint: levels of androstenone and skatole by country and season. Livestock Production Science 62, 1528.CrossRefGoogle Scholar
Xue, J, Dial, GD, Holton, EE, Vickers, Z, Squires, EJ, Lou, Y, Gotbout, D, Morel, N 1996. Breed differences in boar taint: relationship between tissue levels of boar taint compounds and sensory analysis of taint. Journal of Animal Science 74, 21702177.CrossRefGoogle ScholarPubMed
Zamaratskaia, G, Babol, J, Andersson, H, Lundström, K 2004a. Plasma skatole and androstenone levels in entire male pigs and relationship between boar taint compounds, sex steroids and thyroxine at various ages. Livestock Production Science 87, 9198.CrossRefGoogle Scholar
Zamaratskaia, G, Babol, J, Madej, A, Squires, EJ, Lundström, K 2004b. Age-related variation of plasma concentrations of skatole, androstenone, testosterone, oestradiol-17 beta, oestrone sulphate, dehydroepiandrosterone sulphate, triiodothyronine and IGF-1 in six entire male pigs. Reproduction in Domestic Animals 39, 168172.CrossRefGoogle ScholarPubMed
Zamaratskaia, G, Squires, EJ, Babol, J, Andersson, HK, Andersson, K, Lundström, K 2005a. Relationship between the activities of cytochromes P4502E1 and P4502A6 and skatole content in fat in entire male pigs fed with and without raw potato starch. Livestock Production Science 95, 8388.CrossRefGoogle Scholar
Zamaratskaia, G, Babol, J, Andersson, HK, Andersson, K, Lundström, K 2005b. Effect of live weight and dietary supplement of raw potato starch on the levels of skatole, androstenone, testosterone and oestrone sulphate in entire male pigs. Livestock Production Science 93, 235243.CrossRefGoogle Scholar
Zamaratskaia, G, Gilmore, WJ, Lundström, K, Squires, EJ 2007. Effect of testicular steroids on catalytic activities of cytochrome P450 enzymes in porcine liver microsomes. Food and Chemical Toxicology 45, 676681.CrossRefGoogle ScholarPubMed