Polymorphisms within the IGF1 and IGF1R genes associated with superovulation-related traits in Holstein dairy cows managed in a semiarid environment

Adriana Rodríguez-Borbón; Juan F. Medrano; Milton G. Thomas; R. Mark Enns; Scott E. Speidel; Jose F. Torres-Simental; Fernando Rivera-Acuña; Juan F. Hernández-Chávez; Pablo Luna-Nevárez

doi:10.31893/jabb.23029

Keywords:

Abstract

Embryo transfer (ET) is an artificial reproductive technology used for the genetic improvement of cattle. High variation has been observed in superovulation (SPO) and embryo flush recovery, which appear to be influenced by donor cow genetics. Then, the objective was to identify single nucleotide polymorphisms (SNPs) from the genes IGF1 and IGF1R associated with reproductive traits related to SPO response in dairy cows raised in a semiarid region. Sixty-four Holstein cows were subjected to SPO, artificial insemination, and nonsurgical embryo collection. Individual blood samples were collected and used to genotype 13 SNPs from the genes IGF1 and IGF1R. Additional blood samples were collected to measure anti-Mullerian hormone (AMH) concentrations. Ovarian and embryo traits related to SPO response were evaluated. A mixed-effects model was used to identify associations between SNPs and SPO-related traits. A regression model was implemented to calculate allele substitution effects. From 13 SNPs, the SNP rs109763947 in the gene IGF1 and the SNPs rs110343126 and rs208140993 in the gene IGF1R were predictors for six traits evaluated in superovulated cows. The most favorable genotypes for these SNPs were CC, AA and GG, respectively. A linear trend was detected, suggesting an additive effect of the genes. Moreover, all traits evaluated in the current study improved as the number of favorable SNP genotypes increased, confirming a positive contribution of the SNP genes. In conclusion, three SNPs in the genes IGF1 and IGF1R were marker predictors for reproductive traits related to SPO response and embryo production in Holstein cows managed in a semiarid region.
References
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This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

How to cite

Rodríguez-Borbón, A., Medrano, J. F., Thomas, M. G., Enns, R. M., Speidel, S. E., Torres-Simental, J. F., Rivera-Acuña, F., Hernández-Chávez, J. F., & Luna-Nevárez, P. (2023). Polymorphisms within the IGF1 and IGF1R genes associated with superovulation-related traits in Holstein dairy cows managed in a semiarid environment. Journal of Animal Behaviour and Biometeorology, 11(4), 2023029. https://doi.org/10.31893/jabb.23029

[1] Alward KJ, Cockrum RR, Ealy AD (2023) Associations of antral follicle count with fertility in cattle: A review. JDS Communications 4(2):132-137. doi: 10.3168/jdsc.2022-0283.

[2] Balboula AZ, Aboelenain M, Sakatani M, Yamanaka KI, Bai H, Shirozu T, Kawahara M, Hegab AEO, Zaabel SM, Takahashi M (2022) Effect of E-64 Supplementation during In vitro maturation on the developmental competence of bovine OPU-derived oocytes. Genes (Basel) 13(2):324. doi: 10.3390/genes13020324.

[3] Batista EO, Guerreiro BM, Freitas BG, Silva JC, Vieira LM, Ferreira RM, Rezende RG, Basso AC, Lopes RN, Rennó FP, Souza AH, Baruselli PS (2016) Plasma anti-Müllerian hormone as a predictive endocrine marker to select Bos taurus (Holstein) and Bos indicus (Nelore) calves for in vitro embryo production. Domestic Animal Endocrinology 54:1-9.

[4] Baumgarten SC, Armouti M, Ko C, Stocco C (2017) IGF1R Expression in ovarian granulosa cells is essential for steroidogenesis, follicle survival, and fertility in female mice. Endocrinology 158(7):2309-2318. doi: 10.1210/en.2017-00146.

[5] Boldt HB, Glerup S, Overgaard MT, Sottrup-Jensen L, Oxvig C (2006) Definition, expression, and characterization of a protein domain in the N-terminus of pregnancy-associated plasma protein-A distantly related to the family of laminin G-like modules. Protein Expression and Purification 48(2):261-73. doi: 10.1016/j.pep.2006.01.024.

[6] Cartes D, Strappini A, Matamala F, Held-Montaldo R, Sepúlveda-Varas P (2021) Responses of outdoor housed dairy cows to shade access during the prepartum period under temperate summer conditions. Animals (Basel) 11(10):2911. doi: 10.3390/ani11102911.

[7] Center K, Dixon D, Looney C, Rorie R (2018) Anti-mullerian hormone and follicle counts as predictors of superovulatory response and embryo production in beef cattle. Advances in Reproductive Science 6:22-33. doi: 10.4236/arsci.2018.61003

[8] Chinchilla-Vargas J, Jahnke MM, Dohlman TM, Rothschild MF, Gunn PJ (2018) Climatic factors affecting quantity and quality grade of in vivo derived embryos of cattle. Animal Reproduction Science 192:53-60. doi: 10.1016/j.anireprosci.2018.02.012.

[9] Cochran SD, Cole JB, Null DJ, Hansen PJ (2013) Discovery of single nucleotide polymorphisms in candidate genes associated with fertility and production traits in Holstein cattle. BMC Genetics 7:14:49. doi: 10.1186/1471-2156-14-49.

[10] Dai S, Zhang H, Yang F, Shang W, Zeng S (2022) Effects of IGF-1 on the three-dimensional culture of ovarian preantral follicles and superovulation rates in mice. Biology (Basel) 29:11(6):833. doi: 10.3390/biology11060833.

[11] DeAtley KL, Rincon G, Farber CR, Medrano JF, Luna-Nevarez P, Enns RM, VanLeeuwen DM, Silver GA, Thomas MG (2011) Genetic analyses involving microsatellite ETH10 genotypes on bovine chromosome 5 and performance trait measures in Angus- and Brahman-influenced cattle. Journal of Animal Science 89(7):2031-41. doi: 10.2527/jas.2010-3293.

[12] Falconer DS, Mackay, TFC (1996) Introduction to quantitative genetics. 4th, Ed. Longman Scientific and Technical, New York, NY.

[13] Faylon MP, Baumgard LH, Rhoads RP, Spurlock DM (2015) Effects of acute heat stress on lipid metabolism of bovine primary adipocytes. Journal of Dairy Science 98(12):8732-4870. doi: 10.3168/jds.2015-9692.

[14] Gobikrushanth M, Purfield DC, Colazo MG, Butler ST, Wang Z, Ambrose DJ (2018) The relationship between serum anti-Müllerian hormone concentrations and fertility, and genome-wide associations for anti-Müllerian hormone in Holstein cows. Journal of Dairy Science 101:7563–7574. doi: 10.3168/jds.2017-13940.

[15] Grala TM, Price MD, Kuhn-Sherlock B, Burke CR, Meier S (2021) Investigating anogenital distance and antral follicle count as novel markers of fertility within a herd of cows with positive or negative genetic merit for fertility traits. Journal of Dairy Science 104(12):12939-12952. doi: 10.3168/jds.2020-19948.

[16] Grigoletto L, Santana MHA, Bressan FF, Eler JP, Nogueira MFG, Kadarmideen HN, Baruselli PS, Ferraz JBS, Brito LF (2020) Genetic parameters and genome-wide association studies for anti-müllerian hormone levels and antral follicle populations measured after estrus synchronization in Nellore cattle. Animals (Basel) 13:10(7):1185. doi: 10.3390/ani10071185.

[17] Hahn GL (1999) Dynamic responses of cattle to thermal heat loads. Journal of Dairy Science 77(suppl. 2):10–20. doi: 10.2527/1997.77suppl_210x.

[18] Hansen PJ (2020) The incompletely fulfilled promise of embryo transfer in cattle-why aren't pregnancy rates greater and what can we do about it? Journal of Animal Science 98:288. doi: 10.1093/jas/skaa288.

[19] Hansen P., Drost M, Rivera RM, Paula-Lopes FF, AI-Katananit YM, Krininger I, Chase CC Jr (2001) Adverse impact of heat stress on embryo production: causes and strategies for mitigation. Theriogenology 55, 91-103. doi: 10.1016/s0093-691x(00)00448-9.

[20] Hasler JF (2014) Forty years of embryo transfer in cattle: A review focusing on the journal Theriogenology, the growth of the industry in North America, and personal reminisces. Theriogenology 81:152–169. doi: 10.1016/j.theriogenology.2013.09.010.

[21] IETS (International Embryo Transfer Society). 2010. Manual of the International Embryo Transfer Society: A procedural guide and general information for the use of embryo transfer technology emphasizing sanitary precautions. Stringfellow DA, Givens MD (editors). 4th. Ed. Champaign, IL.

[22] Ireland JL, Scheetz D, Jimenez-Krassel F, Themmen AP, Ward F, Lonergan P, Smith GW, Perez GI, Evans AC, Ireland JJ (2008) Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biology of Reproduction 79:1219-1225. doi: 10.1095/biolreprod.108.071670.

[23] Jaton C, Schenkel FS, Sargolzaei M, Cánovas A, Malchiodi F, Price CA, Baes C, Miglior F (2018) Genome-wide association study and in silico functional analysis of the number of embryos produced by Holstein donors. Journal of Dairy Science 101:7248–7257. doi: 10.3168/jds.2017-13848.

[24] Kirkpatrick BW, Morris CA (2015) A major gene for bovine ovulation rate. PLoS One 10(6):e0129025. doi: 10.1371/journal.pone.0129025.

[25] Leyva-Corona JC, Reyna-Granados JR, Zamorano-Algandar R, Sanchez-Castro MA, Thomas MG, Enns RM, Speidel SE, Medrano JF, Rincon G, Luna-Nevarez P (2018) Polymorphisms within the prolactin and growth hormone/insulin-like growth factor-1 functional pathways associated with fertility traits in Holstein cows raised in a hot-humid climate. Tropical Animal Health and Production 50(8):1913-1920. doi: 10.1007/s11250-018-1645-0.

[26] Littell RC, StroupWW, Freund RJ (2002) SAS for linear models, 4th Ed. SAS Institute Inc., Cary, NC.

[27] Loi P, Toschi P, Zacchini F, Ptak G, Scapolo PA, Capra E, Stella A, Marsan PA, Williams JL (2016) Synergies between assisted reproduction technologies and functional genomics. Genetics Selection Evolution 48(1):53. doi: 10.1186/s12711-016-0231-z.

[28] Mossa F, Ireland JJ (2019) Physiology and endocrinology symposium: Anti-Müllerian hormone: a biomarker for the ovarian reserve, ovarian function, and fertility in dairy cows. Journal of Animal Science 97:1255-1264. doi: 10.1093/jas/skz022.

[29] Mossa F, Jimenez-Krassel F, Scheetz D, Weber-Nielsen M, Evans ACO, Ireland J (2017) Anti-Müllerian hormone (AMH) and fertility management in agricultural species. Reproduction 154, R1-R11. doi: 10.1530/REP-17-0104.

[30] Nabenishi H, Kitahara G, Takagi S, Yamazaki A, Osawa T (2017) Relationship between plasma anti-Müllerian hormone concentrations during the rearing period and subsequent embryo productivity in Japanese black cattle. Domestic Animal Endocrinology 60:19-24. doi: 10.1016/j.domaniend.2017.01.002.

[31] Nawaz MY, Jimenez-Krassel F, Steibel JP, Lu Y, Baktula A, Vukasinovic N, Neuder L, Ireland JLH, Ireland JJ, Tempelman RJ (2018) Genomic heritability and genome-wide association analysis of anti-Müllerian hormone in Holstein dairy heifers. Journal of Dairy Science 101:8063–8075. doi: 10.3168/jds.2018-14798.

[32] Parker Gaddis KL, Dikmen S, Null DJ, Cole JB, Hansen P (2017) Evaluation of genetic components in traits related to superovulation, in vitro fertilization, and embryo transfer in Holstein cattle. Journal of Dairy Science 100(4):2877-2891. doi: 10.3168/jds.2016-11907.

[33] Rico C, Drouilhet, Salvetti P, Dalbiès-Tran R, Jarrier P, Touzé JL, Pillet E, Ponsart C, Fabre S, Monniaux D (2012) Determination of Anti-Müllerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm. Reproduction, Fertility and Development 24(7):932-44. doi: 10.1071/RD11290.

[34] Rocha JC, Passalia F, Matos FD, Maserati MP Jr, Alves MF, Almeida TG, Cardoso BL, Basso AC, Nogueira MF (2016) Methods for assessing the quality of mammalian embryos: How far we are from the gold standard? JBRA Assisted Reproduction 20(3):150-8. doi: 10.5935/1518-0557.20160033.

[35] Roth Z (2015) Physiology and Endocrinology Symposium: Cellular and molecular mechanisms of heat stress related to bovine ovarian function. Journal of Animal Science 93:2034-44. doi: 10.2527/jas.2014-8625.

[36] Sigdel A, Bisinotto RS, Peñagaricano F (2021) Genes and pathways associated with pregnancy loss in dairy cattle. Scientific Reports 11(1):13329. doi: 10.1038/s41598-021-92525-0.

[37] Sherman EL, Nkrumah JD, Li C, Bartusiak R, Murdoch B, Moore SS (2009) Fine mapping quantitative trait loci (QTL) for feed intake and feed efficiency in beef cattle. Journal of Animal Science 87:37-45. doi: 10.2527/jas.2008-0876.

[38] Souza AH, Carvalho PD, Rozner AE, Vieira LM, Hackbart KS, Bender RW, Dresch AR, Verstegen JP, Shaver RD, Wiltbank MC (2015) Relationship between circulating anti-Müllerian hormone (AMH) and superovulatory response of high-producing dairy cows. Journal of Dairy Science 98:169-178. doi: 10.3168/jds.2014-8182.

[39] Thomasen JR, Willam A, Egger-Danner C, Sørensen AC (2016) Reproductive technologies combine well with genomic selection in dairy breeding programs. Journal of Dairy Science 99(2):1331-1340. doi: 10.3168/jds.2015-9437.

[40] Torres-Simental JF, Peña-Calderón C, Avendaño-Reyes L, Correa-Calderón A, Macías-Cruz U, Rodríguez-Borbón A, Leyva-Corona JC, Rivera-Acuña F, Thomas MG, Luna-Nevárez P (2021) Predictive markers for superovulation response and embryo production in beef cattle managed in northwest Mexico are influenced by climate. Livestock Science 250:104590. https://doi.org/10.1016/j.livsci.2021.104590.

[41] Umer S, Zhao SJ, Sammad A, Weldegebriall Sahlu B, Yunwei P, Zhu H (2019) AMH: Could it be used as a biomarker for fertility and superovulation in domestic animals? Genes (Basel) 10(12):1009. doi: 10.3390/genes10121009.

[42] Weir BS (2001) Forensics. In: Balding DG, Bishop M, Cannings C (eds). Handbook of Statistical Genetics. John Wiley and Sons, LTD, New York, NY.

[43] Velazquez MA, Zaraza J, Oropeza A, Webb R, Niemann H (2009) The role of IGF1 in the in vivo production of bovine embryos from superovulated donors. Reproduction 37(2):161-80. doi: 10.1530/REP-08-0362.

[44] Yang WC, Yang LG, Riaz H, Tang KQ, Chen L, Li SJ (2013) Effects in cattle of genetic variation within the IGF1R gene on the superovulation performance and pregnancy rates after embryo transfer. Animal Reproduction Science 143(1-4):24-9. doi: 10.1016/j.anireprosci.2013.10.008.

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