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Frontiers in veterinary science2022; 9; 754028; doi: 10.3389/fvets.2022.754028

Fine-Scale Analysis of Runs of Homozygosity Islands Affecting Fertility in Mares.

Abstract: The loss of genetic variability in livestock populations bred under strict selection processes is a growing concern, as it may lead to increased inbreeding values and lower fertility, as a consequence of the "inbreeding depression" effect. This is particularly important in horses, where inbreeding levels tend to rise as individuals become more and more closely related. In this study, we evaluated the effect of increased inbreeding levels on mare fertility by combining an SNP-based genomic approach using runs of homozygosity and the estimation of genetic breeding values for reproductive traits in a large population of Pura Raza Española mares. Our results showed a negative correlation between whole-genome homozygosity and fertility estimated breeding values (EBVs) at the genome level ( = -0.144). However, the analysis at chromosome level revealed a wide variability, with some chromosomes showing higher correlations than others. Interestingly, the correlation was stronger (-0.241) when we repeated the analysis in a reduced dataset including the 10% most and least fertile individuals, where the latter showed an increase in average inbreeding values (F) of around 30%. We also found 41 genomic regions (ROHi, runs of homozygosity islands) where homozygosity increased 100-fold, 13 of which were significantly associated with fertility after cross-validation. These regions encompassed 17 candidate genes previously related to oocyte and embryo development in several species. Overall, we demonstrated the relationship between increased homozygosis at the genomic level and fertility in mares. Our findings may help to deal with the occurrence of inbreeding depression, as well as further our understanding of the mechanisms underlying fertility in mares.
Publication Date: 2022-02-17 PubMed ID: 35252415PubMed Central: PMC8891756DOI: 10.3389/fvets.2022.754028Google Scholar: Lookup
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  • Journal Article

Summary

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This research explores the impact of inbreeding on fertility in the Pura Raza Española breed of mares based on runs of homozygosity (ROH). The study found that there’s a negative correlation between whole-genome ROH and fertility, with increased homozygosity linked to reduced fertility, especially in the least fertile subset of the population. Certain areas of the genome, known as ROH islands, exhibit a more pronounced impact on fertility.

Study Design and Analysis

  • The researchers evaluated the influence of increased inbreeding levels by integrating a technique examining runs of homozygosity, with the estimation of genetic breeding values for reproductive traits. The study group comprised a substantial population of Pura Raza Española mares.
  • They analyzed connections between fertility and whole-genome homozygosity, as well as correlations on a chromosomal level. This dual approach revealed that particular chromosomes held stronger correlations than others.
  • The team also assessed the data focusing on the top 10% most and least fertile mares. In this group, the correlation was more significant and the least fertile individuals demonstrated a 30% rise in average inbreeding values.

Identification of ROH Islands

  • The study identified 41 genomic regions, referred to as “runs of homozygosity islands” (ROHi), where homozygosity amplified 100-fold. These areas could potentially have a more profound impact on fertility.
  • Thirteen of the detected ROHi were notably associated with fertility after further cross-validation. This process provided more robust findings by reducing the risk of false associations.
  • These islands encompassed 17 genes previously linked with oocyte and embryo development across various species, supporting their potential role in impacting fertility.

Conclusions and Implications

  • Ultimately, the findings underscored the association between increased genomic level homozygosity and diminished fertility in mares. By understanding the regions of the genome most implicated in fertility, breeding programs could potentially be adjusted to mitigate the effects of inbreeding depression.
  • The 17 identified candidate genes and their correlation with fertility are also significant and may be subject to further exploration to grasp the underlying mechanisms of fertility in mares and other species.

Cite This Article

APA
Laseca N, Molina A, Ramón M, Valera M, Azcona F, Encina A, Demyda-Peyrás S. (2022). Fine-Scale Analysis of Runs of Homozygosity Islands Affecting Fertility in Mares. Front Vet Sci, 9, 754028. https://doi.org/10.3389/fvets.2022.754028

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 9
Pages: 754028
PII: 754028

Researcher Affiliations

Laseca, Nora
  • Laboratorio de Diagnóstico Genético Veterinario, Departamento de Genética, Universidad de Córdoba, Córdoba, Spain.
Molina, Antonio
  • Laboratorio de Diagnóstico Genético Veterinario, Departamento de Genética, Universidad de Córdoba, Córdoba, Spain.
Ramón, Manuel
  • Cersyra de Valdepeñas, Instituto Regional de Investigación y Desarrollo Agroalimentario y Forestal Castilla La Mancha, Tomelloso, Spain.
Valera, Mercedes
  • Departamento de Agronomía, Escuela Técnica Superior de Ingeniería Agronómica, Universidad de Sevilla, Sevilla, Spain.
Azcona, Florencia
  • IGEVET (UNLP-CONICET LA PLATA), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, La Plata, Argentina.
Encina, Ana
  • Departamento de Agronomía, Escuela Técnica Superior de Ingeniería Agronómica, Universidad de Sevilla, Sevilla, Spain.
  • Asociación Nacional de Criadores de Caballos de Pura Raza Española, Sevilla, Spain.
Demyda-Peyrás, Sebastián
  • Departamento de Producción Animal, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, Buenos Aires, Argentina.
  • Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET LA PLATA), La Plata, Argentina.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 64 references
  1. Leroy G. Inbreeding depression in livestock species: review and meta-analysis.. Anim Genet 2014 Oct;45(5):618-28.
    doi: 10.1111/age.12178pubmed: 24975026google scholar: lookup
  2. Keller LF, Waller DM. Inbreeding effects in wild populations. Trends Ecol Evol (2002) 17:230–41.
  3. Howard JT, Pryce JE, Baes C, Maltecca C. Invited review: Inbreeding in the genomics era: Inbreeding, inbreeding depression, and management of genomic variability.. J Dairy Sci 2017 Aug;100(8):6009-6024.
    doi: 10.3168/jds.2017-12787pubmed: 28601448google scholar: lookup
  4. Goszczynski D, Molina A, Terán E, Morales-Durand H, Ross P, Cheng H, Giovambattista G, Demyda-Peyrás S. Runs of homozygosity in a selected cattle population with extremely inbred bulls: Descriptive and functional analyses revealed highly variable patterns.. PLoS One 2018;13(7):e0200069.
  5. Perdomo-González DI, Sánchez-Guerrero MJ, Molina A, Valera M. Genetic Structure Analysis of the Pura Raza Español Horse Population through Partial Inbreeding Coefficient Estimation.. Animals (Basel) 2020 Aug 6;10(8).
    doi: 10.3390/ani10081360pmc: PMC7459874pubmed: 32781594google scholar: lookup
  6. Todd ET, Hamilton NA, Velie BD, Thomson PC. The effects of inbreeding on covering success, gestation length and foal sex ratio in Australian thoroughbred horses.. BMC Genet 2020 Apr 8;21(1):41.
    doi: 10.1186/s12863-020-00847-1pmc: PMC7140579pubmed: 32268877google scholar: lookup
  7. Azcona F, Valera M, Molina A, Trigo P, Peral García P, Solé M. Impact of reproductive biotechnologies on genetic variability of Argentine Polo horses. Livest Sci (2020) 231.
  8. Gambini A, Maserati M. A journey through horse cloning.. Reprod Fertil Dev 2017 Jan;30(1):8-17.
    doi: 10.1071/RD17374pubmed: 29539299google scholar: lookup
  9. Amos W, Wilmer JW, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T. The influence of parental relatedness on reproductive success.. Proc Biol Sci 2001 Oct 7;268(1480):2021-7.
    doi: 10.1098/rspb.2001.1751pmc: PMC1088844pubmed: 11571049google scholar: lookup
  10. Gómez MD, Sánchez MJ, Bartolomé E, Cervantes I, Poyato-Bonilla J, Demyda-Peyrás S, Valera M. Phenotypic and genetic analysis of reproductive traits in horse populations with different breeding purposes.. Animal 2020 Jul;14(7):1351-1361.
    doi: 10.1017/S1751731120000087pubmed: 32026801google scholar: lookup
  11. Laseca N, Anaya G, Peña Z, Pirosanto Y, Molina A, Demyda Peyrás S. Impaired Reproductive Function in Equines: From Genetics to Genomics.. Animals (Basel) 2021 Feb 3;11(2).
    doi: 10.3390/ani11020393pmc: PMC7913728pubmed: 33546520google scholar: lookup
  12. Mantovani R, Folla F, Pigozzi G, Tsuruta S, Sartori C. Genetics of Lifetime Reproductive Performance in Italian Heavy Draught Horse Mares.. Animals (Basel) 2020 Jun 23;10(6).
    doi: 10.3390/ani10061085pmc: PMC7341281pubmed: 32586061google scholar: lookup
  13. Perdomo-González DI, Molina A, Sánchez-Guerrero MJ, Bartolomé E, Varona L, Valera M. Genetic inbreeding depression load for fertility traits in Pura Raza Española mares.. J Anim Sci 2021 Dec 1;99(12).
    doi: 10.1093/jas/skab316pmc: PMC8645228pubmed: 34718615google scholar: lookup
  14. McGivney BA, Han H, Corduff LR, Katz LM, Tozaki T, MacHugh DE, Hill EW. Genomic inbreeding trends, influential sire lines and selection in the global Thoroughbred horse population.. Sci Rep 2020 Jan 16;10(1):466.
    doi: 10.1038/s41598-019-57389-5pmc: PMC6965197pubmed: 31949252google scholar: lookup
  15. Ricard A, Duluard A. Genomic analysis of gaits and racing performance of the French trotter.. J Anim Breed Genet 2021 Mar;138(2):204-222.
    doi: 10.1111/jbg.12526pmc: PMC7898598pubmed: 33249655google scholar: lookup
  16. Solé M, Ablondi M, Binzer-Panchal A, Velie BD, Hollfelder N, Buys N, Ducro BJ, François L, Janssens S, Schurink A, Viklund Å, Eriksson S, Isaksson A, Kultima H, Mikko S, Lindgren G. Inter- and intra-breed genome-wide copy number diversity in a large cohort of European equine breeds.. BMC Genomics 2019 Oct 22;20(1):759.
    doi: 10.1186/s12864-019-6141-zpmc: PMC6805398pubmed: 31640551google scholar: lookup
  17. Poyato-Bonilla J, Laseca N, Demyda-Peyrás S, Molina A, Valera M. 500 years of breeding in the Carthusian Strain of Pura Raza Español horse: An evolutional analysis using genealogical and genomic data.. J Anim Breed Genet 2022 Jan;139(1):84-99.
    doi: 10.1111/jbg.12641pubmed: 34363624google scholar: lookup
  18. Curik I, Ferencakovic M, Solkner J. Genomic dissection of inbreeding depression: a gate to new opportunities. Rev Brasil Zoot (2017) 46:773–82.
  19. McQuillan R, Leutenegger AL, Abdel-Rahman R, Franklin CS, Pericic M, Barac-Lauc L, Smolej-Narancic N, Janicijevic B, Polasek O, Tenesa A, Macleod AK, Farrington SM, Rudan P, Hayward C, Vitart V, Rudan I, Wild SH, Dunlop MG, Wright AF, Campbell H, Wilson JF. Runs of homozygosity in European populations.. Am J Hum Genet 2008 Sep;83(3):359-72.
    doi: 10.1016/j.ajhg.2008.08.007pmc: PMC2556426pubmed: 18760389google scholar: lookup
  20. Gorssen W, Meyermans R, Janssens S, Buys N. A publicly available repository of ROH islands reveals signatures of selection in different livestock and pet species.. Genet Sel Evol 2021 Jan 4;53(1):2.
    doi: 10.1186/s12711-020-00599-7pmc: PMC7784028pubmed: 33397285google scholar: lookup
  21. Grilz-Seger G, Druml T, Neuditschko M, Mesarič M, Cotman M, Brem G. Analysis of ROH patterns in the Noriker horse breed reveals signatures of selection for coat color and body size.. Anim Genet 2019 Aug;50(4):334-346.
    doi: 10.1111/age.12797pmc: PMC6617995pubmed: 31199540google scholar: lookup
  22. Nani JP, Peñagaricano F. Whole-genome homozygosity mapping reveals candidate regions affecting bull fertility in US Holstein cattle.. BMC Genomics 2020 May 4;21(1):338.
    doi: 10.1186/s12864-020-6758-ypmc: PMC7199307pubmed: 32366228google scholar: lookup
  23. Metzger J, Karwath M, Tonda R, Beltran S, Águeda L, Gut M, Gut IG, Distl O. Runs of homozygosity reveal signatures of positive selection for reproduction traits in breed and non-breed horses.. BMC Genomics 2015 Oct 9;16:764.
    doi: 10.1186/s12864-015-1977-3pmc: PMC4600213pubmed: 26452642google scholar: lookup
  24. Henderson CR. A simple method for computing the inverse of a numerator relationship matrix used in prediction of breeding values. Biometrics (1976) 32:69−83.
    doi: 10.2307/2529339pubmed: 0google scholar: lookup
  25. Misztal I, Tsuruta S, Strabel T, Auvray B, Druet T, Lee DH. BLUPF90 and related programs. 7th World Congress on Genetics Applied to Livestock Production, Montpellier, France (2002).
  26. Garrick DJ, Taylor JF, Fernando RL. Deregressing estimated breeding values and weighting information for genomic regression analyses.. Genet Sel Evol 2009 Dec 31;41(1):55.
    doi: 10.1186/1297-9686-41-55pmc: PMC2817680pubmed: 20043827google scholar: lookup
  27. Schaefer RJ, Schubert M, Bailey E, Bannasch DL, Barrey E, Bar-Gal GK, Brem G, Brooks SA, Distl O, Fries R, Finno CJ, Gerber V, Haase B, Jagannathan V, Kalbfleisch T, Leeb T, Lindgren G, Lopes MS, Mach N, da Câmara Machado A, MacLeod JN, McCoy A, Metzger J, Penedo C, Polani S, Rieder S, Tammen I, Tetens J, Thaller G, Verini-Supplizi A, Wade CM, Wallner B, Orlando L, Mickelson JR, McCue ME. Developing a 670k genotyping array to tag ~2M SNPs across 24 horse breeds.. BMC Genomics 2017 Jul 27;18(1):565.
    doi: 10.1186/s12864-017-3943-8pmc: PMC5530493pubmed: 28750625google scholar: lookup
  28. . Thermofisher Axiom CNV Summary Tool user manual 2013. .
  29. Meyermans R, Gorssen W, Buys N, Janssens S. How to study runs of homozygosity using PLINK? A guide for analyzing medium density SNP data in livestock and pet species.. BMC Genomics 2020 Jan 29;21(1):94.
    doi: 10.1186/s12864-020-6463-xpmc: PMC6990544pubmed: 31996125google scholar: lookup
  30. R-Core-Team. R: A language environment for statistical computing V4.1.0 “Camp Pontanezen”. In: V. R Foundation for Statistical Computing, Austria (Ed.), 2021.
  31. Biscarini F, Cozzi P, Gaspa G, Marras G. DetectRUNS: Detect runs of homozygosity and runs of heterozygosity in diploid genomes in R 2018. .
  32. Ranjan C, Najari V. nlcor: Compute Nonl-inear Correlations. ResearchGate (2020).
  33. Beeson SK, Schaefer RJ, Mason VC, McCue ME. Robust remapping of equine SNP array coordinates to Eq쪳.. Anim Genet 2019 Feb;50(1):114-115.
    doi: 10.1111/age.12745pmc: PMC6349531pubmed: 30421446google scholar: lookup
  34. Lawrence M, HelloRanges A. R package to introduce *Ranges to bedtools users (2021). .
  35. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.. Nat Protoc 2009;4(1):44-57.
    doi: 10.1038/nprot.2008.211pubmed: 19131956google scholar: lookup
  36. Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D, Thomas PD. PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements.. Nucleic Acids Res 2017 Jan 4;45(D1):D183-D189.
    doi: 10.1093/nar/gkw1138pmc: PMC5210595pubmed: 27899595google scholar: lookup
  37. Cothran EG, MacCluer JW, Weitkamp LR, Pfennig DW, Boyce AJ. Inbreeding and reproductive performance in standardbred horses.. J Hered 1984 May-Jun;75(3):220-4.
  38. Valera M, Blesa F, Dos Santos R, Molina A. Genetic study of gestation length in Andalusian and Arabian mares.. Anim Reprod Sci 2006 Sep;95(1-2):75-96.
  39. Sairanen J, Nivola K, Katila T, Virtala AM, Ojala M. Effects of inbreeding and other genetic components on equine fertility.. Animal 2009 Dec;3(12):1662-72.
    doi: 10.1017/S1751731109990553pubmed: 22443550google scholar: lookup
  40. Müller-Unterberg M, Wallmann S, Distl O. Effects of inbreeding and other systematic effects on fertility of Black Forest Draught horses in Germany.. Acta Vet Scand 2017 Oct 18;59(1):70.
    doi: 10.1186/s13028-017-0338-4pmc: PMC5648486pubmed: 29047357google scholar: lookup
  41. Poyato-Bonilla J, Perdomo-González DI, Sánchez-Guerrero MJ, Varona L, Molina A, Casellas J, Valera M. Genetic inbreeding depression load for morphological traits and defects in the Pura Raza Española horse.. Genet Sel Evol 2020 Oct 20;52(1):62.
    doi: 10.1186/s12711-020-00582-2pmc: PMC7576714pubmed: 33081691google scholar: lookup
  42. Frankham R. Inbreeding and extinction: a threshold effect. Conserv Biol (1995) 9:792–9.
  43. Bizarria Dos Santos W, Pimenta Schettini G, Fonseca MG, Pereira GL, Loyola Chardulo LA, Rodrigues Machado Neto O, Baldassini WA, Nunes de Oliveira H, Abdallah Curi R. Fine-scale estimation of inbreeding rates, runs of homozygosity and genome-wide heterozygosity levels in the Mangalarga Marchador horse breed.. J Anim Breed Genet 2021 Mar;138(2):161-173.
    doi: 10.1111/jbg.12508pubmed: 32949478google scholar: lookup
  44. Grilz-Seger G, Mesarič M, Cotman M, Neuditschko M, Druml T, Brem G. Runs of homozygosity and population history of three horse breeds with small population size. J. Equine Vet Sci (2018) 71:27–34.
  45. Velie BD, Solé M, Fegraeus KJ, Rosengren MK, Røed KH, Ihler CF, Strand E, Lindgren G. Genomic measures of inbreeding in the Norwegian-Swedish Coldblooded Trotter and their associations with known QTL for reproduction and health traits.. Genet Sel Evol 2019 May 27;51(1):22.
    doi: 10.1186/s12711-019-0465-7pmc: PMC6537210pubmed: 31132983google scholar: lookup
  46. Martikainen K, Sironen A, Uimari P. Estimation of intrachromosomal inbreeding depression on female fertility using runs of homozygosity in Finnish Ayrshire cattle.. J Dairy Sci 2018 Dec;101(12):11097-11107.
    doi: 10.3168/jds.2018-14805pubmed: 30316595google scholar: lookup
  47. Howard JT, Tiezzi F, Huang Y, Gray KA, Maltecca C. A heuristic method to identify runs of homozygosity associated with reduced performance in livestock.. J Anim Sci 2017 Oct;95(10):4318-4332.
    doi: 10.2527/jas2017.1664pubmed: 29108032google scholar: lookup
  48. Pryce JE, Haile-Mariam M, Goddard ME, Hayes BJ. Identification of genomic regions associated with inbreeding depression in Holstein and Jersey dairy cattle.. Genet Sel Evol 2014 Nov 18;46(1):71.
    doi: 10.1186/s12711-014-0071-7pmc: PMC4234836pubmed: 25407532google scholar: lookup
  49. Visscher PM, Wray NR, Zhang Q, Sklar P, McCarthy MI, Brown MA, Yang J. 10 Years of GWAS Discovery: Biology, Function, and Translation.. Am J Hum Genet 2017 Jul 6;101(1):5-22.
    doi: 10.1016/j.ajhg.2017.06.005pmc: PMC5501872pubmed: 28686856google scholar: lookup
  50. Kawai T, Yanaka N, Richards JS, Shimada M. De Novo-Synthesized Retinoic Acid in Ovarian Antral Follicles Enhances FSH-Mediated Ovarian Follicular Cell Differentiation and Female Fertility.. Endocrinology 2016 May;157(5):2160-72.
    doi: 10.1210/en.2015-2064pmc: PMC4870881pubmed: 27022678google scholar: lookup
  51. Ellederova Z, Kovarova H, Melo-Sterza F, Livingstone M, Tomek W, Kubelka M. Suppression of translation during in vitro maturation of pig oocytes despite enhanced formation of cap-binding protein complex eIF4F and 4E-BP1 hyperphosphorylation.. Mol Reprod Dev 2006 Jan;73(1):68-76.
    doi: 10.1002/mrd.20368pubmed: 16211600google scholar: lookup
  52. Romasko EJ, Amarnath D, Midic U, Latham KE. Association of maternal mRNA and phosphorylated EIF4EBP1 variants with the spindle in mouse oocytes: localized translational control supporting female meiosis in mammals.. Genetics 2013 Oct;195(2):349-58.
    doi: 10.1534/genetics.113.154005pmc: PMC3781964pubmed: 23852387google scholar: lookup
  53. Tomek W, Melo Sterza FA, Kubelka M, Wollenhaupt K, Torner H, Anger M, Kanitz W. Regulation of translation during in vitro maturation of bovine oocytes: the role of MAP kinase, eIF4E (cap binding protein) phosphorylation, and eIF4E-BP1.. Biol Reprod 2002 May;66(5):1274-82.
    doi: 10.1095/biolreprod66.5.1274pubmed: 11967187google scholar: lookup
  54. Rhoads RE. eIF4E: new family members, new binding partners, new roles.. J Biol Chem 2009 Jun 19;284(25):16711-16715.
    doi: 10.1074/jbc.R900002200pmc: PMC2719305pubmed: 19237539google scholar: lookup
  55. Lee J, Ogushi S, Saitou M, Hirano T. Condensins I and II are essential for construction of bivalent chromosomes in mouse oocytes.. Mol Biol Cell 2011 Sep;22(18):3465-77.
    doi: 10.1091/mbc.e11-05-0423pmc: PMC3172270pubmed: 21795393google scholar: lookup
  56. Zhou TP, Zhang D, Cai LB, Xu YX, Shao L, Liu KL. Expression of target genes in cumulus cells derived from human oocytes with and without blastocyst formation. Reprod Dev Med (2019) 3:84–8.
    doi: 10.4103/2096-2924.262387google scholar: lookup
  57. Yang ZM, Das SK, Wang J, Sugimoto Y, Ichikawa A, Dey SK. Potential sites of prostaglandin actions in the periimplantation mouse uterus: differential expression and regulation of prostaglandin receptor genes.. Biol Reprod 1997 Feb;56(2):368-79.
    doi: 10.1095/biolreprod56.2.368pubmed: 9116135google scholar: lookup
  58. El-Gammal Z, AlOkda A, El-Badri N. Role of human oocyte-enriched factors in somatic cell reprograming.. Mech Ageing Dev 2018 Oct;175:88-99.
    doi: 10.1016/j.mad.2018.05.009pubmed: 29890177google scholar: lookup
  59. Itami N, Kawahara-Miki R, Kawana H, Endo M, Kuwayama T, Iwata H. Age-associated changes in bovine oocytes and granulosa cell complexes collected from early antral follicles.. J Assist Reprod Genet 2014 Aug;31(8):1079-88.
    doi: 10.1007/s10815-014-0251-ypmc: PMC4130926pubmed: 24830789google scholar: lookup
  60. Laskowski D, Båge R, Humblot P, Andersson G, Sirard MA, Sjunnesson Y. Insulin during in vitro oocyte maturation has an impact on development, mitochondria, and cytoskeleton in bovine day 8 blastocysts.. Theriogenology 2017 Oct 1;101:15-25.
  61. Booth RA, Cummings C, Tiberi M, Liu XJ. GIPC participates in G protein signaling downstream of insulin-like growth factor 1 receptor.. J Biol Chem 2002 Feb 22;277(8):6719-25.
    doi: 10.1074/jbc.M108033200pubmed: 11751850google scholar: lookup
  62. Rai A, Poh QH, Fatmous M, Fang H, Gurung S, Vollenhoven B, Salamonsen LA, Greening DW. Proteomic profiling of human uterine extracellular vesicles reveal dynamic regulation of key players of embryo implantation and fertility during menstrual cycle.. Proteomics 2021 Jul;21(13-14):e2000211.
    doi: 10.1002/pmic.202000211pubmed: 33634576google scholar: lookup
  63. Feng C, Xu W, Zuo Z. Knockout of the regulatory factor X1 gene leads to early embryonic lethality.. Biochem Biophys Res Commun 2009 Sep 4;386(4):715-7.
    doi: 10.1016/j.bbrc.2009.06.111pmc: PMC2745335pubmed: 19559676google scholar: lookup
  64. Yoon H, Jang H, Kim EY, Moon S, Lee S, Cho M, Cho HJ, Ko JJ, Chang EM, Lee KA, Choi Y. Knockdown of PRKAR2B Results in the Failure of Oocyte Maturation.. Cell Physiol Biochem 2018;45(5):2009-2020.
    doi: 10.1159/000487978pubmed: 29518769google scholar: lookup

Citations

This article has been cited 2 times.
  1. Jiménez JM, Morales RM, Menéndez-Buxadera A, Demyda-Peyrás S, Laseca N, Molina A. Estimation of the Genetic Components of (Co)variance and Preliminary Genome-Wide Association Study for Reproductive Efficiency in Retinta Beef Cattle.. Animals (Basel) 2023 Jan 31;13(3).
    doi: 10.3390/ani13030501pubmed: 36766391google scholar: lookup
  2. Perdomo-González DI, Laseca N, Demyda-Peyrás S, Valera M, Cervantes I, Molina A. Fine-tuning genomic and pedigree inbreeding rates in equine population with a deep and reliable stud book: the case of the Pura Raza Española horse.. J Anim Sci Biotechnol 2022 Nov 7;13(1):127.
    doi: 10.1186/s40104-022-00781-5pubmed: 36336696google scholar: lookup