Polymorphism and Expression of HSD17β13 Gene and Its Association with Lamb Quality of Indonesian Sheep


Ratna Sholatia Harahap
Ronny Rachman Noor
Asep Gunawan


HSD17β13 (17beta 13-Hydroxysteroid dehydrogenases) are important enzymes in steroid metabolism. This study investigated the polymorphisms and expression of the HSD17β13 gene in lamb quality traits in Indonesian sheep. A total of 200 of rams of seven breeds administered in the study were Javanese fat-tailed (JFT), Javanese thin-tailed (JTT), Garut sheep (GS), Jonggol sheep (JS), Garut composite sheep (GCS), Compass agrinac sheep (CAS), Barbados cross sheep (BCS) aged 10-12 months and weighed 20-30 kg. The Polymerase Chain Reaction-Restriction Fragment Length Polymorphism (PCR-RFLP) and MspI enzyme restriction were performed to identify the polymorphism of the HSD17β13 gene. The lamb quality traits were measured for physical quality, flavor, odor, and fatty acid composition. The results showed that the HSD17β13 gene was polymorphic and had three genotypes i.e., CC, CT, and TT. The highest genotype frequency was the CC when compared to the other genotypes. The allele frequency of HSD17β13 gene was not in Hardy Weinberg Equilibrium. The polymorphism of HSD17β13 gene was significantly (P<0.05) associated with the fatty acid composition and Saturated Fatty Acid (SFA),  i.e., tridecanoic acid (C13:0), arachidic acid (C20:0), henecosanoic acid (C21:0), and tricosanoic acid (C23:0). The polymorphism was also significantly associated with the Monounsaturated Fatty Acid (MUFA) i.e. ginkgoleic acid (C17:1) and nervonoic acid (C24:1), and Polyunsaturated Fatty Acid (PUFA) i.e. eicosedienoic acid (C20:2). The level of expression of the HSD17β13 gene based on quantitative real time-PCR analysis results was not significantly different (P>0.05) among genotypes for lamb quality traits. It can be concluded that the polymorphism of HSD17β13 gene was associated with the fatty acid composition of lamb in Indonesian sheep.


How to Cite
Harahap, R. S., Noor, R. R., & Gunawan, A. (2021). Polymorphism and Expression of HSD17β13 Gene and Its Association with Lamb Quality of Indonesian Sheep. ANIMAL PRODUCTION, 23(1), 44-53. https://doi.org/10.20884/1.jap.2021.23.1.88


AOAC (Association of Analytical Chemist). 2005. Official Methods of Analysis of the Association of Official Analytical Chemist. Washington (USA): Association of Official Analytical Chemist.
OECD-FAO(Organization For Economic Co-Operation and Development-Food and Agriculture Organization on The United Nations). 2020. FAO AgricultureProduct.stats.oecd.org/viewhtml.aspx?datasetcode=HIGH_AGLINK_2019&lang=en#. (accessed: April 22, 2020).
Abul-Husn, N.S., X. Cheng, A.H. Li, Y. Xin, C. Schurmann, P. Stevis, Y. Liu, J. Kozlitina, S. Stender, G.C. Wood, A.N. Stepanchick, M.D. Still, S. McCarthy, C. O'Dushlaine, J.S. Packer, S. Balasubramanian, N. Gosalia, D. Esopi, S.Y. Kim, S. Mukherjee, A.E. Lopez, E.D. Fuller, J. Penn, X. Chu, J.Z. Luo, U.L. Mirshahi, D.J. Carey, C.D. Still, M.D. Feldman, A. Small, S.M. Damrauer, D.J. Rader, B. Zambrowicz, W. Olson, A.J. Murphy, I.B. Borecki, A.R. Shuldiner, J.G. Reid, J.D. Overton, G.D. Yancopoulos, H.H. Hobbs, J.C. Cohen, O. Gottesman, T.M. Teslovich, A. Baras, T. Mirshahi, J. Gromada and F.E. Dewey. 2018. A Protein-Truncating HSD17β13 Variant and Protection from Chronic Liver Disease. N Engl J Med. 378: 1096-1106.
Akers, M.D. 2018. Exploring, Analysing and Interpeting Data with Minitab 18. Compass Publishing.
Azizah, D., R.R. Noor, A. Gunawan. 2020. Investigasi Hubungan Keragaman Gen Leptin Receptor (LEPR) dengan Karakteristik Karkas dan Kualitas Daging Domba. JIPTHP. 8(3): 124-130.
Baker, M.E. 2001. Evolution of 17βeta-hydroxysteroid dehydrogenases and their role in androgen, estrogen and retinoid action. Mol Cell Endocrinol. 171: 211–215.
Cavanagh, C.R., E. Jonas, M. Hobbs, P.C. Thomson, I. Tammen and H.R. Raadsma. 2010. Mapping quantitative trait loci (QTL) in sheep. III. QTL for carcass composition traits derived from CT scans and aligned with a meta-assembly for sheep and cattle carcass QTL. Genet Sel Evol. 42(1): 36.
Duijvesteijn, N., S. Bolormaa, C. Gonro, C. Clark, M. Khansefid, N. Moghaddar, A. Swan, P. Storhard, H.D. Daetwyler, J.H.J. Van der Werf and I. Macleod. 2018. Genome-wide association study of meat quality traits using whole-genome sequence data in a multi-breed sheep population. In: Proceedings of the world congress on genetics applied to livestock production, vol methods and tools-GWAS. p 257.
Fukuda, I., A. Ito, G. Hirai, S. Nishimura, H. Kawasaki and H. Saitoh. 2009. Ginkgolic acid inhibits protein SUMOylation by blocking formation of the E1-SUMO intermediate. Chem Biol. 16, 133–140.
Gunawan, A., D. Anggrela, K. Listyarini, M.A. Abuzahra, Jakaria, M. Yamin, I. Inounu and C. Sumantri. 2018. Identification of single nucleotide polymorphism and pathway analysis of Apolipoprotein A5 (APOA5) related to fatty acid traits in Indonesian sheep. TASJ. 41(3): 165-173.
Gunawan, A., R.S. Harahap, K. Listyarini and C. Sumantri. 2019. Identification polymorphism of DGAT1 gene and its association with characteristic of carcass and fat traits in sheep. JITRO. 6(2): 259-266.
Harahap, R.S., A. Gunawan and R.R. Noor. 2020. Effect of CYP2E1 gene polymorphisms on lamb odor and flavour in indonesian sheep. In: The 3th International Conference of Animal Science and Technology (ICAST). Makassar, November 2020.
Hartl, D.L. and A.G. Clark. 1997. Principle of Population Genetic. Sinauer Associates, Sunderland, MA.
Horiguchi, Y., M. Araki and K. Motojima. 2008. 17beta-Hydroxysteroid dehydrogenase type 13 is a liver-specific lipid droplet-associated protein. Biochem Biophys Res Commun. 370: 235-238.
Hua, Z., C. Wu, G. Fan, Z. Tang and F Cao. 2017. The antibacterial activity and mechanism of ginkgolic acid C15:1. BMC Biotechnol. 17: 5.
Jo, J.L., J.H. Hwang, S.G. Kwon, D.H. Park, T.W. Kim, D.G. Kang, G.E. Yu, L.S. Kim, J. Ha and C.W. Kim. 2016. Association between a non-synonymous HSD17β4 single nucleotide polymorphism and meat-quality traits in Berkshire pigs. Genet Mol Res. 15(14): 1–9.
Karamichou, E., R.I. Richardson, G.R. Nute, K.A. McLean and S.C. Bishop. 2006. A partial genome scan to map quantitative trait loci for carcass composition, as assessed by X-ray computer tomography, and meat quality traits in Scottish Blackface Sheep. Anim Sci. 82: 301-309.
Karisa, J. Thomson, Z. Wang, H.L. Bruce, G.S. Plastow, S.S. Moore. 2013. Candidate genes and biological pathways associated with carcass quality traits in beef cattle. Can J Anim Sci. 93: 295306.
Li, J., A. Li, M. Li, Y. Liu, W. Zhao and D. Gao. 2018. Ginkgolic acid exerts an anti-inflammatory effect in human umbilical vein endothelial cells induced by ox-LDL. Pharmazie 73: 408–412.
Li, Q., J. Chen, X. Yu and J.M. Gao. 2019. A mini review of nervonic acid: Source, production, and biological functions. Food Chem. 301: 125286.
Listyarini, K., Jakaria, M.J. Uddin, C. Sumantri, and A. Gunawan. 2018. Association and expression of CYP2A6 and KIF12 genes related to lamb flavor and odor. TASJ. 41(2): 100-107.
Ma, Y., O.V. Belyaeva, P.M. Brown, K. Fujita, K. Valles, S. Karki, Y.S. de Boer, C. Koh, Y. Chen, X. Du and S.K. Handelman. 2019. 17- Beta Hydroxysteroid Dehydrogenase 13 Is a Hepatic Retinol Dehydrogenase Associated with Histological Features of Nonalcoholic Fatty Liver Disease. Hepatol J. 69: 1504-1519.
Moe, M., S. Lien, C. Bendixen and J. Hedegaard. 2008. Gene expression profiles in liver of pigs with extreme high and low levels of androstenone. BMC Vet Res. 4: 29.
Mortimer, S.I. and W. Przybylski. 2016. Breeding strategies for improving meat quality. In: Meat Quality Genetic and Environmental Factors Chapter 9. Przybylski W and Hopkins D (Ed). CRC Publishing. Boca Raton, Florida, United State. Pp: 267-270.
Munyaneza, J.P., A. Gunawan and R.R. Noor. 2019. Exploring effectsof betaine-homocysteine methyltransferase(BHMT) gene polymorphisms on fatty acid traits and cholesterol in sheep. JITAA. 44(3): 243-251.
Nei and Kumar. 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York.
Pfaffl, M.W. 2001. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29(9): e45.
Putranto, R.A. 2013. Studi transkriptomik untuk menghubungkan antara genom dan fungsi sebuah gen dalam tanaman. IBRIEC. 1(2): 25-28.
Silver, N., S. Best, J. Jiang and S.L. Thein. 2006. Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Biol. 7: 33.
Su, W., Y. Wang, X. Jia, W. Wu, L. Li, X. Tian, S. Li, C. Wang, H. Xu, J. Cao, Q. Han, S. Xu, Y. Chen, Y. Zhong, X. Zhang, P. Liu, J.A. Gustafsson, and Y. Guan. 2014. Comparative proteomic study reveals 17beta-HSD13 as a pathogenic protein in nonalcoholic fatty liver disease. Proc Natl Acad Sci U S A: 11437-11442.
Su, W., Z. Mao, Y. Liu, X. Zhang, W. Zhang, J.A. Gustafsson, and Y. Guan. 2019. Role of HSD17β13 in the liver physiology and pathophysiology. Mol Cell Endocrinol. 489: 119-125.
Sun, L., M. Bai, L. Xiang, G. Zhang, W. Ma and H. Jiang. 2016. Comparative transcriptome profiling of longissimus muscle tissue from Qianhua Mutton Merino and Small Tail Han sheep. Sci Rep. 6: 33586.
Walpole, R. 1995. Pengantar Statistika. PT Gramedia Pustaka Utama. Jakarta.
Wang, H., L. Zhang, J. Cao, M. Wu, X. Ma, Z. Liu, R. Liu, F. Zhao, C. Wei and L. Du. 2015. Genome-wide specific selection in three domestic sheep breeds. PloS One. 10(6): e0128688.
Walling, G.A., P.M. Visscher, A.D. Wilson, B.L. McTeir, G. Simm and S.C. Bishop. 2004. Mapping of quantitative trait loci for growth and carcass traits in commercial sheep populations. Anim Sci. 82: 2234-2245.
Weir, N., W. Guan, B. Steffen, L.M. Steffen, A.B.
Karger and M.Y. Tsai. 2018. Omega-6 eicosadienoic Acid is associated with lower HOMA-IR and incident T2D in participants from the MESA cohort. ADA J. 67 (1): 1560-P.
Wood, J.D., M. Enser, A.V. Fisher, G.R. Nute, P.R. Sheard, R.I. Richardson, S.I. Hughes, F.M. Whittingto. 2008. Fat deposition, fatty acid composition, and meat quality [review]. Meat Sci. 78: 343–358.
Zhang, L., J. Liu, F. Zhao, H. Ren, L. Xu, J. Lu, S. Zhang, X. Zhang, C. Wei, G. Lu, Y. Zheng and L. Du. 2013. Genome-wide association studies for growth and meat production traits in sheep. PloS One. 8: e66569.
Zhou, C., X. Li, W. Du, Y. Feng, X. Kong and Y. Li. 2010. Antitumor effects of ginkgolic acid in human cancer cell occur via cell cycle arrest and decrease the Bcl-2/Bax ratio to induce apoptosis. Chemother J. 56: 393–402.
Zlobin, A.S., N.A. Volkova, P.M. Borodin, T.I. Aksenovich and Y.A. Tsepilov. 2019. Recent advances in understanding genetic variants associated with growth, carcass, and meat productivity traits in sheep (Ovis Aries): an update. Arch Anim Breed. 62(2): 579-583.

DB Error: Unknown column 'Array' in 'where clause'