Effect of leukemia inhibitory factor polymorphism on litter size traits in Thai commercial pig breeds https://doi.org/10.12982/VIS.2021.017
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Published:
Mar 8, 2021
Keywords:
LIF Pig Litter size SNPs
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Abstract
Leukemia inhibitory factor (LIF) is a crucial candidate gene that impacts on implantation process. In this study, the effects of the porcine LIF polymorphism on litter size traits were elucidated in Thai commercial pig populations. Genotyping of three single nucleotide polymorphisms (SNPs) of the porcine LIF gene was detected in coding and 3ˊ-untranslated regions. The porcine LIF c.*24C>T was segregating in Large White, Landrace, and Large White × Landrace (LW × LR) crossbred sows. No polymorphisms at two non-synonymous SNPs loci (LIF c.28C>A and LIF c.161A>G) were found in this study. The porcine LIF c.*24C>T was significantly associated with the total number born (TNB), the number born alive (NBA), and the number of piglets weaned alive (NWA) traits in Large White and Landrace sows. Moreover, the porcine LIF c.*24C>T was associated with the NBA and NWA traits in LW × LR crossbred sows. The favorable LIF c.*24C allele was positively correlated with the litter size traits. These findings indicated that the polymorphism of the porcine LIF gene was associated with litter size traits and confirms the significance of porcine LIF as a candidate gene for litter size traits in pig breeding. Thus, the porcine LIF gene could be used for improving prolific traits in these Thai commercial pig populations
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How to Cite
Norseeda, W. ., Liu, G. ., Teltathum, T. ., Sringarm, K. ., Naraballobh, W. ., Khamlor, T. ., & Mekchay, S. . (2021). Effect of leukemia inhibitory factor polymorphism on litter size traits in Thai commercial pig breeds: https://doi.org/10.12982/VIS.2021.017. Veterinary Integrative Sciences, 19(2), 185–196. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/249670
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References
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Blitek, A., Morawska, E., Ziecik, A.J., 2012. Regulation of expression and role of leukemia inhibitory factor and interleukin-6 in the uterus of early pregnant pigs. Theriogenology 78, 951-964.
Buske, B., Sternstein, I., Brockmann, G., 2006. QTL and candidate genes for fecundity in sows. Anim. Reprod. Sci. 95, 167-183.
Chen, X., Li, A., Chen, W., Wei, J., Fu, J., Wang, A., 2015. Differential gene expression in uterine endometrium during implantation in pigs. Biol. Reprod. 92, 1-14.
Cheng, J.G., Chen, J.R., Hernandez, L., Alvord, W.G., Stewart, C.L., 2001. Dual control of LIF expression and LIF receptor function regulate Stat3 activation at the onset of uterine receptivity and embryo implantation. Proc. Natl Acad. Sci. U.S.A. 98, 8680-8685.
Cullinan, E.B., Abbondanzo, S.J., Anderson, P.S., Pollard, J.W., Lessey, B.A., Stewart, C.L., 1996. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine paracrine function in regulating embryo implantation. Proc. Natl. Acad. Sci. U.S.A. 93, 3115-3120.
Devjak, R., Burnik Papler, T., Verdenik, I., Fon Tacer, K., Vrtačnik Bokal, E., 2016. Embryo quality predictive models based on cumulus cells gene expression. Balkan J. Med. Genet. 19, 5-12.
Ding, Y., Ding, C., Wu, X.D., Wu, C., Qian, L., Li, D., Zhang, W., Wang, Y., Li, Yang, M., Wang L., Ding, J., Zhang, X., Gao, Y., Yin, Z., 2020. Porcine LIF gene polymorphisms and their association with litter size traits in four pig breeds. Can. J. Anim. Sci. 100, 85-92.
Dunglison, D.F., Barlow, D.H., Sargent, I.L., 1996. Leukaemia inhibitory factor significantly enhances the blastocyst formation rates of human embryos cultured in serum-free medium. Hum. Reprod. 11, 191-196.
Falconer, D.S., Mackay, T.F.C., 1996. Introduction to Quantitative Genetics. 4 th edition. Longman, Essex, England.
Fouladi-Nashta, A.A., Jones, C.J., Nijjar, N., Mohamet, L., Smith, A., Chambers, I., Kimber, S.J., 2005. Characterization of the uterine phenotype during the peri-implantation period for LIF-null, MF1 strain mice. Dev. Biol. 281, 1-21.
Haines, B.P., Voyle, R.B., Rathjen, P.D., 2000. Intracellular and extracellular leukemia inhibitory factor proteins have different cellular activities that are mediated by distinct protein motifs. Mol. Biol. Cell. 11, 1369-1383.
Kim, M., Seo, H., Choi, Y., Yoo, I., Seo, M., Lee, C.K., Kim, H., Ka, H., 2015. Analysis of stage-specific gene expression profiles in the uterine endometrium during pregnancy in pigs. PLoS One 10, e0143436.
Kobayashi, R., Terakawa, J., Kato, Y., Azimi, S., Inoue, N., Ohmori, Y., Hondo, E., 2014. The contribution of leukemia inhibitory factor (LIF) for embryo implantation differs among strains of mice. Immunobiology 219, 512-521.
Leduc, K., Bourassa, V., Asselin, E., Leclerc, P., Lafond, J., Reyes-Moreno, C., 2012. Leukemia inhibitory factor regulates differentiation of trophoblastlike BeWo cells through the activation of JAK/STAT and MAPK3/1 MAP kinase-signaling pathways. Biol. Reprod. 86, 54.
Lee, D.S., Yanagimoto Ueta, Y., Xuan, X., Igarashi, I., Fujisaki, K., Sugimoto, C., Toyoda, Y., Suzuki, H., 2005. Expression patterns of the implantation-associated genes in the uterus during the estrous cycle in mice. J. Reprod. Dev. 51, 787-798.
Lei, T., Yang, Z.Q., Xia, T., Gan, L., Chen, X.D., Yuan, J.H., Zhu, Y., 2004. Stage-specific expression of leukaemia inhibitory factor and its receptor in rabbit pre-implantation embryo and uterine epithelium during early pregnancy. Reprod. Domest. Anim. 39, 13-8.
Leonova, M.A., Getmantseva, L.V., Vasilenko, V.N., Klimenko, A.I., Usatov, A.V., Yu, B.S., Yu, K.A., Shirockova, N.V., 2015. Leukemia inhibitory factor (LIF) gene polymorphism and its impact on reproductive traits of pigs. Am. J. Anim. Vet. Sci. 10, 212-216.
Lin, H.C., Liu, G.F., Wang, A.G., Kong, L.J., Wang, X.F., Fu, J.L., 2009. Effect of polymorphism in the leukemia inhibitory factor gene on litter size in Large White pigs. Mol. Biol. Rep. 36, 1833-1838.
Mathieu, M.E., Saucourt, C., Mournetas, V., Gauthereau, X., Thézé, N., Praloran, V., Thiébaud, P., Bœuf, H., 2012. LIF-dependent signaling: new pieces in the Lego. Stem Cell Rev. Rep. 8, 1-15.
Mikolajczyk, M., Wirstlein, P., Skrzypczak, J., 2007. The impact of leukemia inhibitory factor in uterine flushing on the reproductive potential of infertile women-a prospective study. Am. J. Reprod. Immunol. 58, 65-74.
Mojarrad, M., Hassanzadeh-Nazarabadi, M., Tafazoli, N., 2013. Polymorphism of genes and implantation failure. Int. J. Mol. Cell Med. 2, 1-8.
Moodley, D., Mody, G.M., Chuturgoon, A.A., 2010. Functional analysis of the p53 codon 72 polymorphism in black South Africans with rheumatoid arthritis a pilot study. Clin. Rheumatol. 29, 1099-1105.
Mucha, A., Ropka-Molik, K., Piorkowska, K., Tyra, M., Oczkowicz, M., 2013. Effect of EGF, AREG and LIF genes polymorphisms on reproductive traits in pigs. Anim. Reprod. Sci. 137, 88-92.
Muñoz, G., Ovilo, C., Estellé, J., Silió, L., Fernández, A., Rodriguez, C., 2007. Association with litter size of new polymorphisms on ESR1 and ESR2 genes in a Chinese-European pig line. Genet. Sel. Evol. 39, 195-206.
Nachtigall, M.J., Kliman, H.J., Feinberg, R.F., Olive, D.L., Engin, O., Arici, A., 1996. The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation. J. Clin. Endocrinol. Metab. 81, 801-806.
Nielsen, B., Su, G., Lund, M.S., Madsen, P., 2013. Selection for increased number of piglets at d 5 after farrowing has increased litter size and reduced piglet mortality. J. Anim. Sci. 91, 2575-2582.
Onteru, S.K., Fan, B., Du, Z.Q., Garrick, D.J., Stalder, K.J., Rothschild, M.F., 2012. A whole-genome association study for pig reproductive traits. Anim. Genet. 43, 18-26.
Paiva, P., Menkhorst, E., Salamonsen, L., Dimitriadis, E., 2009. Leukemia inhibitory factor and interleukin-11: critical regulators in the establishment of pregnancy. Cytokine Growth Factor Rev. 20, 319-328.
Raheem, K.A., 2017. Cytokines, growth factors and macromolecules as mediators of implantation in mammalian species. Int. J. Vet. Sci. Med. 6, S6-S14.
Robb, L., Dimitriadis, E., Li, R., Salamonsen, L.A., 2002. Leukemia inhibitory factor and interleukin-11: cytokines with key roles in implantation. J. Reprod. Immunol. 57, 129-141.
Rodríguez, A., De Frutos, C., Díez, C., Caamaño, J. N., Facal, N., Duque, P., García-Ochoa, C., Gómez, E., 2007. Effects of human versus mouse leukemia inhibitory factor on the in vitro development of bovine embryos. Theriogenology 67, 1092-1095.
Salleh, N., Giribabu, N., 2014. Leukemia inhibitory factor: roles in embryo implantation and in nonhormonal contraception. Sci. World J. 2014, 201514.
Schneider, J.F., Rempel, L.A., Snelling, W.M., Wiedmann, R.T., Nonneman, D.J., Rohrer, G.A., 2012. Genome-wide association study of swine farrowing traits. Part II: Bayesian analysis of marker data. J. Anim. Sci. 90, 3360-3367.
Spötter, A., Distl, O., 2006. Genetic approaches to the improvement of fertility traits in the pig. Vet. J. 172, 234-247.
Spötter, A., Drögemüller, C., Hamann, H., Distl, O., 2005. Evidence of a new leukemia inhibitory factor-associated genetic marker for litter size in a synthetic pig line. J. Anim. Sci. 83, 2264-2270.
Spötter, A., Muller, S., Hamann, H., Distl, O., 2009. Effect of polymorphisms in the genes for LIF and RBP4 on litter size in two German pig lines. Reprod. Domest. Anim. 44, 100-105.
Steck, T., Giess, R., Suetterlin, M.W., Bolland, M., Wiest, S., Poehls, U.G., Dietl, J., 2004. Leukaemia inhibitory factor (LIF) gene mutations in women with unexplained infertility and recurrent failure of implantation after IVF and embryo transfer. Eur. J. Obstet. Gynecol. Reprod. Biol. 112, 69-73.
Stewart, C.L., 1994. Leukaemia inhibitory factor and the regulation of pre-implantation development of the mammalian embryo. Mol. Reprod. Dev. 39, 233-238.
Stewart, C.L., Kaspar, P., Brunet, L.J., Bhatt, H., Gadi, I., Köntgen, F., Abbondanzo, S.J., 1992. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76-79.
Suman, P., Malhotra. S.S., Gupta. S.K., 2013. LIF-STAT signaling and trophoblast biology. JAKSTAT. 2, e25155.
Walsh, P.S., Metzger, D.A., Higushi, R., 2013. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 54, 134-139.
Yoo, I., Chae, S., Han, J., Lee, S., Kim, H.J., Ka, H., 2019. Leukemia inhibitory factor and its receptor: expression and regulation in the porcine endometrium throughout the estrous cycle and pregnancy. Asian-Australas. J. Anim. Sci. 32, 192-200
Blitek, A., Morawska, E., Ziecik, A.J., 2012. Regulation of expression and role of leukemia inhibitory factor and interleukin-6 in the uterus of early pregnant pigs. Theriogenology 78, 951-964.
Buske, B., Sternstein, I., Brockmann, G., 2006. QTL and candidate genes for fecundity in sows. Anim. Reprod. Sci. 95, 167-183.
Chen, X., Li, A., Chen, W., Wei, J., Fu, J., Wang, A., 2015. Differential gene expression in uterine endometrium during implantation in pigs. Biol. Reprod. 92, 1-14.
Cheng, J.G., Chen, J.R., Hernandez, L., Alvord, W.G., Stewart, C.L., 2001. Dual control of LIF expression and LIF receptor function regulate Stat3 activation at the onset of uterine receptivity and embryo implantation. Proc. Natl Acad. Sci. U.S.A. 98, 8680-8685.
Cullinan, E.B., Abbondanzo, S.J., Anderson, P.S., Pollard, J.W., Lessey, B.A., Stewart, C.L., 1996. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine paracrine function in regulating embryo implantation. Proc. Natl. Acad. Sci. U.S.A. 93, 3115-3120.
Devjak, R., Burnik Papler, T., Verdenik, I., Fon Tacer, K., Vrtačnik Bokal, E., 2016. Embryo quality predictive models based on cumulus cells gene expression. Balkan J. Med. Genet. 19, 5-12.
Ding, Y., Ding, C., Wu, X.D., Wu, C., Qian, L., Li, D., Zhang, W., Wang, Y., Li, Yang, M., Wang L., Ding, J., Zhang, X., Gao, Y., Yin, Z., 2020. Porcine LIF gene polymorphisms and their association with litter size traits in four pig breeds. Can. J. Anim. Sci. 100, 85-92.
Dunglison, D.F., Barlow, D.H., Sargent, I.L., 1996. Leukaemia inhibitory factor significantly enhances the blastocyst formation rates of human embryos cultured in serum-free medium. Hum. Reprod. 11, 191-196.
Falconer, D.S., Mackay, T.F.C., 1996. Introduction to Quantitative Genetics. 4 th edition. Longman, Essex, England.
Fouladi-Nashta, A.A., Jones, C.J., Nijjar, N., Mohamet, L., Smith, A., Chambers, I., Kimber, S.J., 2005. Characterization of the uterine phenotype during the peri-implantation period for LIF-null, MF1 strain mice. Dev. Biol. 281, 1-21.
Haines, B.P., Voyle, R.B., Rathjen, P.D., 2000. Intracellular and extracellular leukemia inhibitory factor proteins have different cellular activities that are mediated by distinct protein motifs. Mol. Biol. Cell. 11, 1369-1383.
Kim, M., Seo, H., Choi, Y., Yoo, I., Seo, M., Lee, C.K., Kim, H., Ka, H., 2015. Analysis of stage-specific gene expression profiles in the uterine endometrium during pregnancy in pigs. PLoS One 10, e0143436.
Kobayashi, R., Terakawa, J., Kato, Y., Azimi, S., Inoue, N., Ohmori, Y., Hondo, E., 2014. The contribution of leukemia inhibitory factor (LIF) for embryo implantation differs among strains of mice. Immunobiology 219, 512-521.
Leduc, K., Bourassa, V., Asselin, E., Leclerc, P., Lafond, J., Reyes-Moreno, C., 2012. Leukemia inhibitory factor regulates differentiation of trophoblastlike BeWo cells through the activation of JAK/STAT and MAPK3/1 MAP kinase-signaling pathways. Biol. Reprod. 86, 54.
Lee, D.S., Yanagimoto Ueta, Y., Xuan, X., Igarashi, I., Fujisaki, K., Sugimoto, C., Toyoda, Y., Suzuki, H., 2005. Expression patterns of the implantation-associated genes in the uterus during the estrous cycle in mice. J. Reprod. Dev. 51, 787-798.
Lei, T., Yang, Z.Q., Xia, T., Gan, L., Chen, X.D., Yuan, J.H., Zhu, Y., 2004. Stage-specific expression of leukaemia inhibitory factor and its receptor in rabbit pre-implantation embryo and uterine epithelium during early pregnancy. Reprod. Domest. Anim. 39, 13-8.
Leonova, M.A., Getmantseva, L.V., Vasilenko, V.N., Klimenko, A.I., Usatov, A.V., Yu, B.S., Yu, K.A., Shirockova, N.V., 2015. Leukemia inhibitory factor (LIF) gene polymorphism and its impact on reproductive traits of pigs. Am. J. Anim. Vet. Sci. 10, 212-216.
Lin, H.C., Liu, G.F., Wang, A.G., Kong, L.J., Wang, X.F., Fu, J.L., 2009. Effect of polymorphism in the leukemia inhibitory factor gene on litter size in Large White pigs. Mol. Biol. Rep. 36, 1833-1838.
Mathieu, M.E., Saucourt, C., Mournetas, V., Gauthereau, X., Thézé, N., Praloran, V., Thiébaud, P., Bœuf, H., 2012. LIF-dependent signaling: new pieces in the Lego. Stem Cell Rev. Rep. 8, 1-15.
Mikolajczyk, M., Wirstlein, P., Skrzypczak, J., 2007. The impact of leukemia inhibitory factor in uterine flushing on the reproductive potential of infertile women-a prospective study. Am. J. Reprod. Immunol. 58, 65-74.
Mojarrad, M., Hassanzadeh-Nazarabadi, M., Tafazoli, N., 2013. Polymorphism of genes and implantation failure. Int. J. Mol. Cell Med. 2, 1-8.
Moodley, D., Mody, G.M., Chuturgoon, A.A., 2010. Functional analysis of the p53 codon 72 polymorphism in black South Africans with rheumatoid arthritis a pilot study. Clin. Rheumatol. 29, 1099-1105.
Mucha, A., Ropka-Molik, K., Piorkowska, K., Tyra, M., Oczkowicz, M., 2013. Effect of EGF, AREG and LIF genes polymorphisms on reproductive traits in pigs. Anim. Reprod. Sci. 137, 88-92.
Muñoz, G., Ovilo, C., Estellé, J., Silió, L., Fernández, A., Rodriguez, C., 2007. Association with litter size of new polymorphisms on ESR1 and ESR2 genes in a Chinese-European pig line. Genet. Sel. Evol. 39, 195-206.
Nachtigall, M.J., Kliman, H.J., Feinberg, R.F., Olive, D.L., Engin, O., Arici, A., 1996. The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation. J. Clin. Endocrinol. Metab. 81, 801-806.
Nielsen, B., Su, G., Lund, M.S., Madsen, P., 2013. Selection for increased number of piglets at d 5 after farrowing has increased litter size and reduced piglet mortality. J. Anim. Sci. 91, 2575-2582.
Onteru, S.K., Fan, B., Du, Z.Q., Garrick, D.J., Stalder, K.J., Rothschild, M.F., 2012. A whole-genome association study for pig reproductive traits. Anim. Genet. 43, 18-26.
Paiva, P., Menkhorst, E., Salamonsen, L., Dimitriadis, E., 2009. Leukemia inhibitory factor and interleukin-11: critical regulators in the establishment of pregnancy. Cytokine Growth Factor Rev. 20, 319-328.
Raheem, K.A., 2017. Cytokines, growth factors and macromolecules as mediators of implantation in mammalian species. Int. J. Vet. Sci. Med. 6, S6-S14.
Robb, L., Dimitriadis, E., Li, R., Salamonsen, L.A., 2002. Leukemia inhibitory factor and interleukin-11: cytokines with key roles in implantation. J. Reprod. Immunol. 57, 129-141.
Rodríguez, A., De Frutos, C., Díez, C., Caamaño, J. N., Facal, N., Duque, P., García-Ochoa, C., Gómez, E., 2007. Effects of human versus mouse leukemia inhibitory factor on the in vitro development of bovine embryos. Theriogenology 67, 1092-1095.
Salleh, N., Giribabu, N., 2014. Leukemia inhibitory factor: roles in embryo implantation and in nonhormonal contraception. Sci. World J. 2014, 201514.
Schneider, J.F., Rempel, L.A., Snelling, W.M., Wiedmann, R.T., Nonneman, D.J., Rohrer, G.A., 2012. Genome-wide association study of swine farrowing traits. Part II: Bayesian analysis of marker data. J. Anim. Sci. 90, 3360-3367.
Spötter, A., Distl, O., 2006. Genetic approaches to the improvement of fertility traits in the pig. Vet. J. 172, 234-247.
Spötter, A., Drögemüller, C., Hamann, H., Distl, O., 2005. Evidence of a new leukemia inhibitory factor-associated genetic marker for litter size in a synthetic pig line. J. Anim. Sci. 83, 2264-2270.
Spötter, A., Muller, S., Hamann, H., Distl, O., 2009. Effect of polymorphisms in the genes for LIF and RBP4 on litter size in two German pig lines. Reprod. Domest. Anim. 44, 100-105.
Steck, T., Giess, R., Suetterlin, M.W., Bolland, M., Wiest, S., Poehls, U.G., Dietl, J., 2004. Leukaemia inhibitory factor (LIF) gene mutations in women with unexplained infertility and recurrent failure of implantation after IVF and embryo transfer. Eur. J. Obstet. Gynecol. Reprod. Biol. 112, 69-73.
Stewart, C.L., 1994. Leukaemia inhibitory factor and the regulation of pre-implantation development of the mammalian embryo. Mol. Reprod. Dev. 39, 233-238.
Stewart, C.L., Kaspar, P., Brunet, L.J., Bhatt, H., Gadi, I., Köntgen, F., Abbondanzo, S.J., 1992. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76-79.
Suman, P., Malhotra. S.S., Gupta. S.K., 2013. LIF-STAT signaling and trophoblast biology. JAKSTAT. 2, e25155.
Walsh, P.S., Metzger, D.A., Higushi, R., 2013. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 54, 134-139.
Yoo, I., Chae, S., Han, J., Lee, S., Kim, H.J., Ka, H., 2019. Leukemia inhibitory factor and its receptor: expression and regulation in the porcine endometrium throughout the estrous cycle and pregnancy. Asian-Australas. J. Anim. Sci. 32, 192-200