Association of Variants in Innate Immune Genes TLR4 and TLR5 with Reproductive and Milk Production Traits in Czech Simmental Cattle
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
grant MZE-RO0718
Ministry of Agriculture of the Czech Republic
PubMed
38254914
PubMed Central
PMC10815032
DOI
10.3390/genes15010024
PII: genes15010024
Knihovny.cz E-zdroje
- Klíčová slova
- cattle, genotyping, immunity, inflammation, mammary gland, parturition, toll-like receptors,
- MeSH
- jednonukleotidový polymorfismus MeSH
- mléko MeSH
- přirozená imunita MeSH
- rozmnožování genetika MeSH
- skot genetika MeSH
- toll-like receptor 4 * genetika MeSH
- toll-like receptor 5 * genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- skot genetika MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Česká republika MeSH
- Názvy látek
- toll-like receptor 4 * MeSH
- toll-like receptor 5 * MeSH
Bovine genes TLR4 and TLR5, which encode antibacterial toll-like receptors, were screened for polymorphisms in Czech Red Pied (Czech Simmental) cattle to identify variants associated with reproduction, udder health, and milk production traits. Variants were discovered by hybrid resequencing of 164 bulls using HiSeq X-Ten and PacBio technologies and then individually genotyped. Nominal p-values < 0.05 for associations were detected in 18 combinations between 14 polymorphisms and 15 traits using one-way analysis of variance (ANOVA). The TLR4 variants g.610C>T (rs43578094) and g.10310T>G (rs8193072) in reference AC000135.1 were strictly associated with the index of early reproductive disorders and maternal calving ease, respectively, at false discovery rate (FDR) < 0.05. A highly permissive false discovery rate cutoff of 0.6 separated seventeen combinations in both genes comprising eight positives. In the case of the TLR4 variant g.9422T>C (rs8193060), indications were obtained for the association with as many as four reproductive traits: incidence of cystic ovaries, early reproductive disorders, calving ease, and production longevity. The permissive FDR interpretation for the TLR5 data indicated associations with cyst incidence and early reproduction disorders with maternal calving ease. Moreover, three TLR5 polymorphisms correlated with milk production traits. The discrepancy of the observed associations with the predicted impacts of the SNPs on protein function points to the role of haplotypes. Nevertheless, this question should be resolved on a larger scale. The observed associations are endorsed by independent evidence from the published functional roles in other species and by the published QTL mapping data.
Breeding Company CHD Impuls 592 55 Bohdalec Czech Republic
Department of Genetics and Microbiology Viničná 7 Charles University 128 43 Prague Czech Republic
Department of Genetics Czech University of Life Sciences Kamýcká 129 165 06 Prague Czech Republic
Zobrazit více v PubMed
Meuwissen T.H.E., Hayes B.J., Goddard M.E. Prediction of total genetic value using genome-wide dense marker maps. Genetics. 2001;157:1819–1829. doi: 10.1093/genetics/157.4.1819. PubMed DOI PMC
Capitan A., Michot P., Baur A., Saintilan R., Hoze C., Valour D., Guillaume F., Boichon D., Barbat A., Boichard D., et al. Genetic tools to improve reproduction traits in dairy cattle. Reprod. Fer. Dev. 2014;27:14–21. doi: 10.1071/RD14379. PubMed DOI
Boichard D., Ducrocq V., Fritz S. Sustainable dairy cattle selection in the genomic era. J. Anim. Breed. Genet. 2015;132:135–143. doi: 10.1111/jbg.12150. PubMed DOI
Jungi T.W., Farhat K., Burgener I.A., Werling D. Toll-like receptors in domestic animals. Cell Tissue Res. 2011;343:107–120. doi: 10.1007/s00441-010-1047-8. PubMed DOI
Jann O.C., Werling D., Chang J.S., Haig D., Glass E.J. Molecular evolution of bovine Toll-like receptor 2 suggests substitutions of functional relevance. BMC Evol. Biol. 2008;8:288. doi: 10.1186/1471-2148-8-288. PubMed DOI PMC
Seabury C.M., Seabury P.M., Decker J.E., Schnabel R.D., Taylor J.F., Womack J.E. Diversity and evolution of 11 innate immune genes in Bos taurus taurus and Bos taurus indicus cattle. Proc. Natl. Acad. Sci. USA. 2010;107:151–156. doi: 10.1073/pnas.0913006107. PubMed DOI PMC
Fisher C.A., Bhattarai E.K., Osterstock J.B., Dowd S.E., Seabury P.M., Vikram M., Whitlock R.H., Schukken Y.H., Schnabel R.D., Taylor J.F., et al. Evolution of the bovine TLR gene family and member associations with Mycobacterium avium subspecies paratuberculosis infection. PLoS ONE. 2011;6:11. doi: 10.1371/journal.pone.0027744. PubMed DOI PMC
Koets A., Santema W., Mertens H., Oostenrijk D., Keestra M., Overdijk M., Labouriau R., Franken P., Frijters A., Nielen M., et al. Susceptibility to paratuberculosis infection in cattle is associated with single nucleotide polymorphisms in Toll-like receptor 2 which modulate immune responses against Mycobacterium avium subspecies paratuberculosis. Prev. Vet. Med. 2010;93:305–315. doi: 10.1016/j.prevetmed.2009.11.008. PubMed DOI
Ruiz-Larrañaga O., Manzano C., Iriondo M., Garrido J.M., Molina E., Vazquez P., Juste R.A., Estonba A. Genetic variation of toll-like receptor genes and infection by Mycobacterium avium ssp. paratuberculosis in Holstein-Friesian cattle. J. Dairy Sci. 2011;94:3635–3641. doi: 10.3168/jds.2010-3788. PubMed DOI
Kannaki T.R., Shanmugam M., Verma P.C. Toll-like receptors and their role in animal reproduction. Anim. Reprod. Sci. 2011;125:1–12. doi: 10.1016/j.anireprosci.2011.03.008. PubMed DOI
Sharma B.S., Leyva I., Schenkel F., Karrow N.A. Association of toll-like receptor 4 polymorphisms with somatic cell score and lactation persistency in Holstein bulls. J. Dairy Sci. 2006;89:3626–3635. doi: 10.3168/jds.S0022-0302(06)72402-X. PubMed DOI
Beecher C., Daly M., Childs S., Berry D.P., Magee D.A., McCarthy T.V., Giblin L. Polymorphisms in bovine immune genes and their associations with somatic cell count and milk production in dairy cattle. BMC Genet. 2010;11:99. doi: 10.1186/1471-2156-11-99. PubMed DOI PMC
Bjelka M., Novák K. Association of TLR gene variants in a Czech Red Pied cattle population with reproductive traits. Vet. Immunol. Immunopathol. 2020;220:109997. doi: 10.1016/j.vetimm.2019.109997. PubMed DOI
White S.N., Taylor K.H., Abbey C.A. Haplotype variation in bovine Toll-like receptor 4 and computational prediction of a positively selected ligand-binding domain. Proc. Natl. Acad. Sci. USA. 2003;100:10364–10369. doi: 10.1073/pnas.1333957100. PubMed DOI PMC
Seabury C.M., Cargill E.J., Womack J.E. Sequence variability and protein domain architectures for bovine Toll-like receptors 1, 5, and 10. Genomics. 2007;90:502–515. doi: 10.1016/j.ygeno.2007.07.001. PubMed DOI
Novák K., Bjelka M., Samake K., Valčíková T. Potential of TLR-gene diversity in Czech indigenous cattle for resistance breeding as revealed by hybrid sequencing. Arch. Anim. Breed. 2019;62:477–490. doi: 10.5194/aab-62-477-2019. PubMed DOI PMC
Koren S., Schatz M.C., Walenz B.P., Martin J., Howard J.T., Ganapathy G., Wang Z., Rasko D.A., McCombie W.R., Jarvis E.D., et al. Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotech. 2012;30:692. doi: 10.1038/nbt.2280. PubMed DOI PMC
Sim N.L., Kumar P., Hu J., Henikoff S., Schneider G., Ng P.C. SIFT web server: Predicting effects of amino acid substitutions on proteins. Nucl. Acids Res. 2012;40:W452–W457. doi: 10.1093/nar/gks539. PubMed DOI PMC
Richardson I.W., Berry D.P., Wiencko H.L., Higgins I.M., More S.J., McClure J., Lynn D.J., Bradley D.G. A genome-wide association study for genetic susceptibility to Mycobacterium bovis infection in dairy cattle identifies a susceptibility QTL on chromosome 23. Genet. Sel. Evol. 2016;48:19. doi: 10.1186/s12711-016-0197-x. PubMed DOI PMC
Samaké K., Novák K. Haplotype disequilibrium in the TLR genes of Czech Red Pied cattle. Diversity. 2023;15:811. doi: 10.3390/d15070811. DOI
Benjamini Y., Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 1995;57:289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x. DOI
Meyer K. WOMBAT—A tool for mixed model analyses in quantitative genetics by restricted maximum likelihood (REML) J. Zhejiang Univ. Sci. B. 2007;8:815–821. doi: 10.1631/jzus.2007.B0815. PubMed DOI PMC
Sharma B.S., Mount J., Karrow N.A. Functional characterization of a single nucleotide polymorphism in the 5′-UTR region of the bovine toll-like receptor 4 gene. Dev. Biol. 2008;132:331–336. PubMed
Wang M.Q., Song H.L., Zhu X.R., Xing S.Y., Zhang M.R., Zhang H.M., Wang X.L., Yang Z.P., Ding X.D., Karrow N.A., et al. Toll-like receptor 4 gene polymorphisms influence milk production traits in Chinese Holstein cows. J. Dairy Res. 2018;85:407–411. doi: 10.1017/S0022029918000535. PubMed DOI
Hu J.X., Zhao H., Zhou H.H. False discovery rate control with groups. J. Am. Stat. Assoc. 2010;105:1215–1227. doi: 10.1198/jasa.2010.tm09329. PubMed DOI PMC
Balding D.J. A tutorial on statistical methods for population association studies. Nature Rev. Genet. 2006;7:781–791. doi: 10.1038/nrg1916. PubMed DOI
Opsal M.A., Lien S., Brenna-Hansen S., Olsen H.G., Våge D.I. Association analysis of the constructed linkage maps covering TLR2 and TLR4 with clinical mastitis in Norwegian Red cattle. J. Anim. Breed. Genet. 2008;125:110–118. doi: 10.1111/j.1439-0388.2007.00704.x. PubMed DOI
Abdel-Shafy H., Bortfeldt R.H., Regens J., Brockmann G.A. Single nucleotide polymorphism and haplotype effects associated with somatic cell score in German Holstein cattle. Genet. Sel. Evol. 2014;46:35. doi: 10.1186/1297-9686-46-35. PubMed DOI PMC
Novák K., Pikousová J., Czerneková V., Mátlová V. Diversity of the TLR4 immunity receptor in Czech native cattle breeds revealed using the Pacific Biosciences sequencing platform. Anim. Biotech. 2017;28:228–236. doi: 10.1080/10495398.2017.1279170. PubMed DOI
Mullen M.P., McClure M.C., Kearney J.F. Book of Abstracts of the 69th Annual Meeting of the European Federation of Animal Science, Dubrovnik, Croatia, 27–31 August 2018. Wageningen Academic Publishers; Wageningen, The Netherlands: 2018. Relationships between a TLR4 allele associated with IBK and production traits in dairy cattle; p. 611.
El-Domany W.B., Radwan H.A., Ateya A.I., Ramadan H.H., Marghani B.H., Nasr S.M. Genetic polymorphisms in LTF/EcoRI and TLR4/AluI loci as candidates for milk and reproductive performance assessment in Holstein cattle. Repr. Dom. Anim. 2019;54:678–686. doi: 10.1111/rda.13408. PubMed DOI
Sheldon I.M. Genes and environmental factors that influence disease resistance to microbes in the female reproductive tract of dairy cattle. Reprod. Fert. Dev. 2015;27:72–81. doi: 10.1071/RD14305. PubMed DOI
Bicalho M.L.S., Santin T., Rodrigues M.X., Marques C.E., Lima S.F., Bicalho R.C. Dynamics of the microbiota found in the vaginas of dairy cows during the transition period: Associations with uterine diseases and reproductive outcome. J. Dairy Sci. 2017;100:3043–3058. doi: 10.3168/jds.2016-11623. PubMed DOI
Lim R., Barker G., Lappas M. TLR2, TLR3 and TLR5 regulation of pro-inflammatory and pro-labour mediators in human primary myometrial cells. J. Reprod. Immunol. 2017;122:28–36. doi: 10.1016/j.jri.2017.08.004. PubMed DOI
Wahid H.H., Dorian C.L., Chin P.Y., Hutchinson M.R., Rice K.C., Olson D.M., Moldenhauer L.M., Robertson S.A. Toll-like receptor 4 is an essential upstream regulator of on-time parturition and perinatal viability in mice. Endocrinology. 2015;156:3828–3841. doi: 10.1210/en.2015-1089. PubMed DOI PMC
Elovitz M.A., Wang Z., Chien E.K., Rychlik D.F., Phillippe M. A new model for inflammation-induced preterm birth: The role of platelet-activating factor and Toll-like receptor-4. Am. J. Pathol. 2003;163:2103–2111. doi: 10.1016/S0002-9440(10)63567-5. PubMed DOI PMC
Kadam L., Gomez-Lopez N., Mial T.N., Kohan-Ghadr H.R., Drewlo S. Rosiglitazone regulates TLR4 and rescues HO-1 and NRF2 expression in myometrial and decidual macrophages in inflammation-induced preterm birth. Reprod. Sci. 2017;24:1590–1599. doi: 10.1177/1933719117697128. PubMed DOI PMC
Schjenken J.E., Glynn D.J., Sharkey D.J., Robertson S.A. Female tract response to seminal fluid in mice. Biol. Reprod. 2015;93:3. doi: 10.1095/biolreprod.114.125740. PubMed DOI
Cole J.B., Wiggans G.R., Ma L., Sonstegard T.S., Lawlor T.J., Jr., Crooker B.A., Van Tassell C.P., Yang J., Wang S., Matukumalli L.K., et al. Genome-wide association analysis of thirty one production, health, reproduction and body conformation traits in contemporary U.S. Holstein cows. BMC Genom. 2011;12:408. doi: 10.1186/1471-2164-12-408. PubMed DOI PMC
Purfield D.C., Bradley D.G., Evans R.D., Kearney F.J., Berry D.P. Genome-wide association study for calving performance using high-density genotypes in dairy and beef cattle. Genet. Sel. Evol. 2015;47:47. doi: 10.1186/s12711-015-0126-4. PubMed DOI PMC