Analyze Diet
PloS one2023; 18(8); e0289066; doi: 10.1371/journal.pone.0289066

Genomic screening of allelic and genotypic transmission ratio distortion in horse.

Abstract: The phenomenon in which the expected Mendelian inheritance is altered is known as transmission ratio distortion (TRD). The TRD analysis relies on the study of the transmission of one of the two alleles from a heterozygous parent to the offspring. These distortions are due to biological mechanisms affecting gametogenesis, embryo development and/or postnatal viability, among others. In this study, TRD phenomenon was characterized in horses using SNP-by-SNP model by TRDscan v.2.0 software. A total of 1,041 Pura Raza Español breed horses were genotyped with 554,634 SNPs. Among them, 277 horses genotyped in trios (stallion-mare-offspring) were used to perform the TRD analysis. Our results revealed 140 and 42 SNPs with allelic and genotypic patterns, respectively. Among them, 63 displayed stallion-TRD and 41 exhibited mare-TRD, while 36 SNPs showed overall TRD. In addition, 42 SNPs exhibited heterosis pattern. Functional analyses revealed that the annotated genes located within the TRD regions identified were associated with biological processes and molecular functions related to spermatogenesis, oocyte division, embryonic development, and hormonal activity. A total of 10 functional candidate genes related to fertility were found. To our knowledge, this is the most extensive study performed to evaluate the presence of alleles and functional candidate genes with transmission ratio distortion affecting reproductive performance in the domestic horse.
Publication Date: 2023-08-09 PubMed ID: 37556504PubMed Central: PMC10411798DOI: 10.1371/journal.pone.0289066Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study explores the phenomenon known as transmission ratio distortion (TRD) in horses, particularly, the Pura Raza Español breed. By analyzing the transmission of alleles from parent to offspring, the researchers identified genes associated with reproductive performance and fertility in the horse.

Research Methodology

  • The researchers used a particular breed of horse, the Pura Raza Español, for this study. This breed was chosen specifically because they have a high severity of equine diseases.
  • Around 1,041 of these horses were genotyped with more than half a million Single Nucleotide Polymorphisms (SNPs). SNPs are variations at single spots in a DNA sequence and can act as biological markers, helping scientists discover genes associated with certain diseases.
  • Out of all the horses genotyped, 277 horses were genotyped in trios consisting of a stallion, a mare, and their offspring. These groups were used to carry out the TRD analysis.

Findings

  • The analysis revealed 140 and 42 SNPs with allelic and genotypic patterns, respectively. An allelic pattern represents a variation in a genetic sequence, while a genotypic pattern indicates a specific gene’s form.
  • Some of these SNPs displayed a trend among certain parent-offspring pairs: 63 showed a tendency towards transmission from the stallion (male horse), 41 from the mare (female horse), and 36 showed a general trend of TRD irrespective of the parent.
  • An additional 42 SNPs exhibited a heterosis pattern, which is a phenomenon where the offspring’s genetic traits are superior to those of both parents.

Interpretation and Implications

  • By analyzing these patterns, the researchers identified that the genes found within the TRD regions were associated with biological activities such as spermatogenesis, oocyte division, embryonic development, and hormonal activity. These processes and functions are directly related to reproductive performance and fertility.
  • Ten functional candidate genes related to fertility were identified. These genes could potentially play a significant role in modifying or improving reproductive performance in horses.
  • This study contributes the most comprehensive evaluation of alleles and functional candidate genes with transmission ratio distortion affecting reproductive performance in horses. The findings could have significant implications for breeding and veterinary practices in the future.

Cite This Article

APA
Laseca N, Cánovas Á, Valera M, Id-Lahoucine S, Perdomo-González DI, Fonseca PAS, Demyda-Peyrás S, Molina A. (2023). Genomic screening of allelic and genotypic transmission ratio distortion in horse. PLoS One, 18(8), e0289066. https://doi.org/10.1371/journal.pone.0289066

Publication

ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 18
Issue: 8
Pages: e0289066
PII: e0289066

Researcher Affiliations

Laseca, Nora
  • Department of Genetics, University of Cordoba, Córdoba, Spain.
Cánovas, Ángela
  • Center of Genetic Improvement of Livestock, Department of Animal Biosciences, University of Guelph, Guelph, Ontario, Canada.
Valera, Mercedes
  • Department of Agronomy, School of Agronomy Engineering, University of Seville, Seville, Spain.
Id-Lahoucine, Samir
  • Department of Animal and Veterinary Science, Scotland's Rural College, Aberdeen, Scotland, United Kingdom.
Perdomo-González, Davinia I
  • Department of Agronomy, School of Agronomy Engineering, University of Seville, Seville, Spain.
Fonseca, Pablo A S
  • Department of Animal Production, University of Leon, León, Spain.
Demyda-Peyrás, Sebastián
  • Department of Genetics, University of Cordoba, Córdoba, Spain.
Molina, Antonio
  • Department of Genetics, University of Cordoba, Córdoba, Spain.

MeSH Terms

  • Horses / genetics
  • Animals
  • Male
  • Female
  • Alleles
  • Inheritance Patterns
  • Genotype
  • Heterozygote
  • Genomics

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 76 references
  1. Pardo-Manuel de Villena F, de la Casa-Esperon E, Briscoe TL, Sapienza C. A genetic test to determine the origin of maternal transmission ratio distortion. Meiotic drive at the mouse Om locus.. Genetics 2000 Jan;154(1):333-42.
    doi: 10.1093/genetics/154.1.333pmc: PMC1460926pubmed: 10628992google scholar: lookup
  2. Casellas J, Gularte RJ, Farber CR, Varona L, Mehrabian M, Schadt EE, Lusis AJ, Attie AD, Yandell BS, Medrano JF. Genome scans for transmission ratio distortion regions in mice.. Genetics 2012 May;191(1):247-59.
    doi: 10.1534/genetics.111.135988pmc: PMC3338264pubmed: 22367040google scholar: lookup
  3. Fishman L, McIntosh M. Standard Deviations: The Biological Bases of Transmission Ratio Distortion.. Annu Rev Genet 2019 Dec 3;53:347-372.
  4. Seymour DK, Chae E, Arioz BI, Koenig D, Weigel D. Transmission ratio distortion is frequent in Arabidopsis thaliana controlled crosses.. Heredity (Edinb) 2019 Mar;122(3):294-304.
    doi: 10.1038/s41437-018-0107-9pmc: PMC6169738pubmed: 29955170google scholar: lookup
  5. Meyer WK, Arbeithuber B, Ober C, Ebner T, Tiemann-Boege I, Hudson RR, Przeworski M. Evaluating the evidence for transmission distortion in human pedigrees.. Genetics 2012 May;191(1):215-32.
    doi: 10.1534/genetics.112.139576pmc: PMC3338262pubmed: 22377632google scholar: lookup
  6. Casellas J, Manunza A, Mercader A, Quintanilla R, Amills M. A flexible bayesian model for testing for transmission ratio distortion.. Genetics 2014 Dec;198(4):1357-67.
    doi: 10.1534/genetics.114.169607pmc: PMC4256756pubmed: 25271302google scholar: lookup
  7. Casellas J, Cañas-Álvarez JJ, González-Rodríguez A, Puig-Oliveras A, Fina M, Piedrafita J, Molina A, Díaz C, Baró JA, Varona L. Bayesian analysis of parent-specific transmission ratio distortion in seven Spanish beef cattle breeds.. Anim Genet 2017 Feb;48(1):93-96.
    doi: 10.1111/age.12509pubmed: 27650416google scholar: lookup
  8. Abdalla EA, Id-Lahoucine S, Cánovas A, Casellas J, Schenkel FS, Wood BJ, Baes CF. Discovering lethal alleles across the turkey genome using a transmission ratio distortion approach.. Anim Genet 2020 Dec;51(6):876-889.
    doi: 10.1111/age.13003pmc: PMC7702127pubmed: 33006154google scholar: lookup
  9. Arends D, Kärst S, Heise S, Korkuc P, Hesse D, Brockmann GA. Transmission distortion and genetic incompatibilities between alleles in a multigenerational mouse advanced intercross line.. Genetics 2022 Jan 4;220(1).
    doi: 10.1093/genetics/iyab192pmc: PMC8733443pubmed: 34791189google scholar: lookup
  10. Huang LO, Labbe A, Infante-Rivard C. Transmission ratio distortion: review of concept and implications for genetic association studies.. Hum Genet 2013 Mar;132(3):245-63.
    doi: 10.1007/s00439-012-1257-0pubmed: 23242375google scholar: lookup
  11. Hastings IM. Germline selection: population genetic aspects of the sexual/asexual life cycle.. Genetics 1991 Dec;129(4):1167-76.
    doi: 10.1093/genetics/129.4.1167pmc: PMC1204780pubmed: 1783297google scholar: lookup
  12. Dyer KA, Charlesworth B, Jaenike J. Chromosome-wide linkage disequilibrium as a consequence of meiotic drive.. Proc Natl Acad Sci U S A 2007 Jan 30;104(5):1587-92.
    doi: 10.1073/pnas.0605578104pmc: PMC1785283pubmed: 17242362google scholar: lookup
  13. Zöllner S, Wen X, Hanchard NA, Herbert MA, Ober C, Pritchard JK. Evidence for extensive transmission distortion in the human genome.. Am J Hum Genet 2004 Jan;74(1):62-72.
    doi: 10.1086/381131pmc: PMC1181913pubmed: 14681832google scholar: lookup
  14. Wakasugi N. A genetically determined incompatibility system between spermatozoa and eggs leading to embryonic death in mice.. J Reprod Fertil 1974 Nov;41(1):85-96.
    doi: 10.1530/jrf.0.0410085pubmed: 4431024google scholar: lookup
  15. Naumova AK, Greenwood CM, Morgan K. Imprinting and deviation from Mendelian transmission ratios.. Genome 2001 Jun;44(3):311-20.
    doi: 10.1139/g01-013pubmed: 11444688google scholar: lookup
  16. Moore CS. Postnatal lethality and cardiac anomalies in the Ts65Dn Down syndrome mouse model.. Mamm Genome 2006 Oct;17(10):1005-12.
    doi: 10.1007/s00335-006-0032-8pubmed: 17019652google scholar: lookup
  17. Id-Lahoucine S, Cánovas A, Jaton C, Miglior F, Fonseca PAS, Sargolzaei M, Miller S, Schenkel FS, Medrano JF, Casellas J. Implementation of Bayesian methods to identify SNP and haplotype regions with transmission ratio distortion across the whole genome: TRDscan v.1.0.. J Dairy Sci 2019 Apr;102(4):3175-3188.
    doi: 10.3168/jds.2018-15296pubmed: 30738671google scholar: lookup
  18. Id-Lahoucine S, Casellas J, Fonseca PAS, Suárez-Vega A, Schenkel FS, Cánovas A. Deviations from Mendelian Inheritance on Bovine X-Chromosome Revealing Recombination, Sex-of-Offspring Effects and Fertility-Related Candidate Genes.. Genes (Basel) 2022 Dec 9;13(12).
    doi: 10.3390/genes13122322pmc: PMC9778079pubmed: 36553588google scholar: lookup
  19. Casellas J, Id-Lahoucine S, Cánovas A. Discriminating between allele- and genotype-specific transmission ratio distortion.. Anim Genet 2020 Dec;51(6):847-854.
    doi: 10.1111/age.13007pubmed: 32996622google scholar: lookup
  20. Id-Lahoucine S.n. Mendelian inheritance in the genomics and big data era: transmission ratio distortion phenomenon in cattle breeds.. Dissertation University of Guelph. 2020.
  21. Vázquez-Gómez M, Hijas-Villalba MM, Varona L, Ibañez-Escriche N, Rosas JP, Negro S, Noguera JL, Casellas J. Maternal Transmission Ratio Distortion in Two Iberian Pig Varieties.. Genes (Basel) 2020 Sep 5;11(9).
    doi: 10.3390/genes11091050pmc: PMC7563664pubmed: 32899475google scholar: lookup
  22. Gòdia M, Casellas J, Ruiz-Herrera A, Rodríguez-Gil JE, Castelló A, Sánchez A, Clop A. Whole genome sequencing identifies allelic ratio distortion in sperm involving genes related to spermatogenesis in a swine model.. DNA Res 2020 Dec 3;27(5).
    doi: 10.1093/dnares/dsaa019pmc: PMC7750926pubmed: 32931559google scholar: lookup
  23. Martin AAA, Id-Lahoucine S, Fonseca PAS, Rochus CM, Alcantara LM, Tulpan D, LeBlanc SJ, Miglior F, Casellas J, Cánovas A, Baes CF, Schenkel FS. Unravelling the genetics of non-random fertilization associated with gametic incompatibility.. Sci Rep 2022 Dec 24;12(1):22314.
    doi: 10.1038/s41598-022-26910-8pmc: PMC9789956pubmed: 36566278google scholar: lookup
  24. Todd ET, Thomson PC, Hamilton NA, Ang RA, Lindgren G, Viklund Å, Eriksson S, Mikko S, Strand E, Velie BD. A genome-wide scan for candidate lethal variants in Thoroughbred horses.. Sci Rep 2020 Aug 4;10(1):13153.
    doi: 10.1038/s41598-020-68946-8pmc: PMC7403398pubmed: 32753654google scholar: lookup
  25. 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.
  26. 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
  27. 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
  28. 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
  29. 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
  30. Sargolzaei M, Chesnais JP, Schenkel FS. A new approach for efficient genotype imputation using information from relatives.. BMC Genomics 2014 Jun 17;15(1):478.
    doi: 10.1186/1471-2164-15-478pmc: PMC4076979pubmed: 24935670google scholar: lookup
  31. Kass RE, Raftery AE. Bayes Factors. Journal of the American Statistical Association 1995;90(430):773–95.
  32. Spiegelhalter DJ, Best NG, Carlin BP, Van Der Linde A. Bayesian measures of model complexity and fit. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 2002;64(4):583–639.
    doi: 10.1111/1467-9868.00353google scholar: lookup
  33. Kinsella RJ, Kähäri A, Haider S, Zamora J, Proctor G, Spudich G, Almeida-King J, Staines D, Derwent P, Kerhornou A, Kersey P, Flicek P. Ensembl BioMarts: a hub for data retrieval across taxonomic space.. Database (Oxford) 2011;2011:bar030.
    doi: 10.1093/database/bar030pmc: PMC3170168pubmed: 21785142google scholar: lookup
  34. Cánovas A, Pena RN, Gallardo D, Ramírez O, Amills M, Quintanilla R. Segregation of regulatory polymorphisms with effects on the gluteus medius transcriptome in a purebred pig population.. PLoS One 2012;7(4):e35583.
  35. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S. AmiGO: online access to ontology and annotation data.. Bioinformatics 2009 Jan 15;25(2):288-9.
  36. Mi H, Muruganujan A, Ebert D, Huang X, Thomas PD. PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools.. Nucleic Acids Res 2019 Jan 8;47(D1):D419-D426.
    doi: 10.1093/nar/gky1038pmc: PMC6323939pubmed: 30407594google scholar: lookup
  37. Sherman BT, Hao M, Qiu J, Jiao X, Baseler MW, Lane HC, Imamichi T, Chang W. DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update).. Nucleic Acids Res 2022 Jul 5;50(W1):W216-W221.
    doi: 10.1093/nar/gkac194pmc: PMC9252805pubmed: 35325185google scholar: lookup
  38. Jeffreys H. Theory of Probability. Clarendon Press, Oxford, UK. 1984.
  39. Paterson AD, Waggott D, Schillert A, Infante-Rivard C, Bull SB, Yoo YJ, Pinnaduwage D. Transmission-ratio distortion in the Framingham Heart Study.. BMC Proc 2009 Dec 15;3 Suppl 7(Suppl 7):S51.
    doi: 10.1186/1753-6561-3-s7-s51pmc: PMC2795951pubmed: 20018044google scholar: lookup
  40. Flisikowski K, Venhoranta H, Nowacka-Woszuk J, McKay SD, Flyckt A, Taponen J, Schnabel R, Schwarzenbacher H, Szczerbal I, Lohi H, Fries R, Taylor JF, Switonski M, Andersson M. A novel mutation in the maternally imprinted PEG3 domain results in a loss of MIMT1 expression and causes abortions and stillbirths in cattle (Bos taurus).. PLoS One 2010 Nov 30;5(11):e15116.
  41. Schütz E, Wehrhahn C, Wanjek M, Bortfeld R, Wemheuer WE, Beck J, Brenig B. The Holstein Friesian Lethal Haplotype 5 (HH5) Results from a Complete Deletion of TBF1M and Cholesterol Deficiency (CDH) from an ERV-(LTR) Insertion into the Coding Region of APOB.. PLoS One 2016;11(4):e0154602.
  42. Wu X, Mesbah-Uddin M, Guldbrandtsen B, Lund MS, Sahana G. Haplotypes responsible for early embryonic lethality detected in Nordic Holsteins.. J Dairy Sci 2019 Dec;102(12):11116-11123.
    doi: 10.3168/jds.2019-16651pubmed: 31548059google scholar: lookup
  43. Mohamed Elshabrawy G, Masahide N. Haplotypes associated with fetal death and abortion in Holstein cows with special reference to the situation in Japan. J Animal Genetics 2018;46(1):25–30.
    doi: 10.5924/abgri.46.25google scholar: lookup
  44. Didion JP, Morgan AP, Clayshulte AM, Mcmullan RC, Yadgary L, Petkov PM, Bell TA, Gatti DM, Crowley JJ, Hua K, Aylor DL, Bai L, Calaway M, Chesler EJ, French JE, Geiger TR, Gooch TJ, Garland T Jr, Harrill AH, Hunter K, McMillan L, Holt M, Miller DR, O'Brien DA, Paigen K, Pan W, Rowe LB, Shaw GD, Simecek P, Sullivan PF, Svenson KL, Weinstock GM, Threadgill DW, Pomp D, Churchill GA, Pardo-Manuel de Villena F. A multi-megabase copy number gain causes maternal transmission ratio distortion on mouse chromosome 2.. PLoS Genet 2015 Feb;11(2):e1004850.
  45. Khatib H, Monson RL, Schutzkus V, Kohl DM, Rosa GJ, Rutledge JJ. Mutations in the STAT5A gene are associated with embryonic survival and milk composition in cattle.. J Dairy Sci 2008 Feb;91(2):784-93.
    doi: 10.3168/jds.2007-0669pubmed: 18218766google scholar: lookup
  46. Wang T, Gao H, Li W, Liu C. Essential Role of Histone Replacement and Modifications in Male Fertility.. Front Genet 2019;10:962.
    doi: 10.3389/fgene.2019.00962pmc: PMC6792021pubmed: 31649732google scholar: lookup
  47. Kafer GR, Lehnert SA, Pantaleon M, Kaye PL, Moser RJ. Expression of genes coding for histone variants and histone-associated proteins in pluripotent stem cells and mouse preimplantation embryos.. Gene Expr Patterns 2010 Sep;10(6):299-305.
    doi: 10.1016/j.gep.2010.06.003pubmed: 20601166google scholar: lookup
  48. Le Danvic C, Gérard O, Sellem E, Ponsart C, Chemineau P, Humblot P, Nagnan-Le Meillour P. Enhancing bull sexual behavior using estrus-specific molecules identified in cow urine.. Theriogenology 2015 Jun;83(9):1381-8.
  49. Nielsen BL, Jerôme N, Saint-Albin A, Thonat C, Briant C, Boué F, Rampin O, Maurin Y. A mixture of odorant molecules potentially indicating oestrus in mammals elicits penile erections in male rats.. Behav Brain Res 2011 Dec 1;225(2):584-9.
    doi: 10.1016/j.bbr.2011.08.026pubmed: 21884731google scholar: lookup
  50. Dwyer CM. Maternal behaviour and lamb survival: from neuroendocrinology to practical application.. Animal 2014 Jan;8(1):102-12.
    doi: 10.1017/S1751731113001614pubmed: 24103485google scholar: lookup
  51. Negishi Y, Takahashi H, Kuwabara Y, Takeshita T. Innate immune cells in reproduction.. J Obstet Gynaecol Res 2018 Nov;44(11):2025-2036.
    doi: 10.1111/jog.13759pubmed: 30058156google scholar: lookup
  52. Archana SS, Selvaraju S, Binsila BK, Arangasamy A, Krawetz SA. Immune regulatory molecules as modifiers of semen and fertility: A review.. Mol Reprod Dev 2019 Nov;86(11):1485-1504.
    doi: 10.1002/mrd.23263pubmed: 31518041google scholar: lookup
  53. Fujimoto VY, Kane JP, Ishida BY, Bloom MS, Browne RW. High-density lipoprotein metabolism and the human embryo.. Hum Reprod Update 2010 Jan-Feb;16(1):20-38.
    doi: 10.1093/humupd/dmp029pubmed: 19700490google scholar: lookup
  54. Arias A, Quiroz A, Santander N, Morselli E, Busso D. Implications of High-Density Cholesterol Metabolism for Oocyte Biology and Female Fertility.. Front Cell Dev Biol 2022;10:941539.
    doi: 10.3389/fcell.2022.941539pmc: PMC9518216pubmed: 36187480google scholar: lookup
  55. Kim N, Nakamura H, Masaki H, Kumasawa K, Hirano KI, Kimura T. Effect of lipid metabolism on male fertility.. Biochem Biophys Res Commun 2017 Apr 8;485(3):686-692.
    doi: 10.1016/j.bbrc.2017.02.103pubmed: 28235483google scholar: lookup
  56. Pfender S, Kuznetsov V, Pleiser S, Kerkhoff E, Schuh M. Spire-type actin nucleators cooperate with Formin-2 to drive asymmetric oocyte division.. Curr Biol 2011 Jun 7;21(11):955-60.
    doi: 10.1016/j.cub.2011.04.029pmc: PMC3128265pubmed: 21620703google scholar: lookup
  57. Laseca N, Demyda-Peyrás S, Valera M, Ramón M, Escribano B, Perdomo-González DI, Molina A. A genome-wide association study of mare fertility in the Pura Raza Español horse.. Animal 2022 Mar;16(3):100476.
    doi: 10.1016/j.animal.2022.100476pubmed: 35247706google scholar: lookup
  58. Reddy P, Adhikari D, Zheng W, Liang S, Hämäläinen T, Tohonen V, Ogawa W, Noda T, Volarevic S, Huhtaniemi I, Liu K. PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles.. Hum Mol Genet 2009 Aug 1;18(15):2813-24.
    doi: 10.1093/hmg/ddp217pubmed: 19423553google scholar: lookup
  59. Ge LQ, Xia T, Huang B, Song QS, Zhang HW, Stanley D, Yang GQ, Wu JC. Suppressing male spermatogenesis-associated protein 5-like gene expression reduces vitellogenin gene expression and fecundity in Nilaparvata lugens Stål.. Sci Rep 2016 Jun 16;6:28111.
    doi: 10.1038/srep28111pmc: PMC4910105pubmed: 27305948google scholar: lookup
  60. Sujit KM, Singh V, Trivedi S, Singh K, Gupta G, Rajender S. Increased DNA methylation in the spermatogenesis-associated (SPATA) genes correlates with infertility.. Andrology 2020 May;8(3):602-609.
    doi: 10.1111/andr.12742pubmed: 31838782google scholar: lookup
  61. Sujit KM, Sarkar S, Singh V, Pandey R, Agrawal NK, Trivedi S, Singh K, Gupta G, Rajender S. Genome-wide differential methylation analyses identifies methylation signatures of male infertility.. Hum Reprod 2018 Dec 1;33(12):2256-2267.
    doi: 10.1093/humrep/dey319pubmed: 30358834google scholar: lookup
  62. Intasqui P, Agarwal A, Sharma R, Samanta L, Bertolla RP. Towards the identification of reliable sperm biomarkers for male infertility: A sperm proteomic approach.. Andrologia 2018 Apr;50(3).
    doi: 10.1111/and.12919pubmed: 29205438google scholar: lookup
  63. Song H, Chen D, Bai R, Feng Y, Wu S, Wang T, Xia X, Li J, Miao YL, Zuo B, Li F. BCL2-associated athanogene 6 exon24 contributes to testosterone synthesis and male fertility in mammals.. Cell Prolif 2022 Jul;55(7):e13281.
    doi: 10.1111/cpr.13281pmc: PMC9251057pubmed: 35688694google scholar: lookup
  64. Naaby-Hansen S, Herr JC. Heat shock proteins on the human sperm surface.. J Reprod Immunol 2010 Jan;84(1):32-40.
    doi: 10.1016/j.jri.2009.09.006pmc: PMC2898571pubmed: 19962198google scholar: lookup
  65. Wang X, Xie W, Yao Y, Zhu Y, Zhou J, Cui Y, Guo X, Yuan Y, Zhou Z, Liu M. The heat shock protein family gene Hspa1l in male mice is dispensable for fertility.. PeerJ 2020;8:e8702.
    doi: 10.7717/peerj.8702pmc: PMC7098389pubmed: 32231871google scholar: lookup
  66. Liu W, Wang F, Xu Q, Shi J, Zhang X, Lu X, Zhao ZA, Gao Z, Ma H, Duan E, Gao F, Gao S, Yi Z, Li L. BCAS2 is involved in alternative mRNA splicing in spermatogonia and the transition to meiosis.. Nat Commun 2017 Jan 27;8:14182.
    doi: 10.1038/ncomms14182pmc: PMC5290162pubmed: 28128212google scholar: lookup
  67. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis.. Genes Dev 2002 Jul 15;16(14):1779-91.
    doi: 10.1101/gad.989402pmc: PMC186403pubmed: 12130538google scholar: lookup
  68. Guo T, Zhao S, Zhao S, Chen M, Li G, Jiao X, Wang Z, Zhao Y, Qin Y, Gao F, Chen ZJ. Mutations in MSH5 in primary ovarian insufficiency.. Hum Mol Genet 2017 Apr 15;26(8):1452-1457.
    doi: 10.1093/hmg/ddx044pmc: PMC5393145pubmed: 28175301google scholar: lookup
  69. Wyrwoll MJ, van Walree ES, Hamer G, Rotte N, Motazacker MM, Meijers-Heijboer H, Alders M, Meißner A, Kaminsky E, Wöste M, Krallmann C, Kliesch S, Hunt TJ, Clark AT, Silber S, Stallmeyer B, Friedrich C, van Pelt AMM, Mathijssen IB, Tüttelmann F. Bi-allelic variants in DNA mismatch repair proteins MutS Homolog MSH4 and MSH5 cause infertility in both sexes.. Hum Reprod 2021 Dec 27;37(1):178-189.
    doi: 10.1093/humrep/deab230pubmed: 34755185google scholar: lookup
  70. Linscott ML, Chung WCJ. TET1 regulates fibroblast growth factor 8 transcription in gonadotropin releasing hormone neurons.. PLoS One 2019;14(7):e0220530.
  71. Xu K, Tian Y, Weng X, Hu X, Heng D, Xia G, Zhang C. Effect of thyroid dysfunction on NOS expression in the female rat.. Cell Tissue Res 2020 Feb;379(2):291-300.
    doi: 10.1007/s00441-019-03090-ypubmed: 31463706google scholar: lookup
  72. Jasiński T, Zdrojkowski Ł, Kautz E, Juszczuk-Kubiak E, Ferreira-Dias G, Domino M. Equine Endometrosis Pathological Features: Are They Dependent on NF-κB Signaling Pathway?. Animals (Basel) 2021 Nov 4;11(11).
    pmc: PMC8614257pubmed: 34827882doi: 10.3390/ani11113151google scholar: lookup
  73. Jasiński T, Zdrojkowski Ł, Kautz E, Juszczuk-Kubiak E, Ferreira-Dias G, Domino M. The NF-κB-signalling pathway in mare's endometrium infiltrated with the inflammatory cells.. Reprod Domest Anim 2022 Jun;57(6):598-610.
    doi: 10.1111/rda.14099pmc: PMC9305511pubmed: 35182075google scholar: lookup
  74. Jasiński T, Zdrojkowski Ł, Ferreira-Dias G, Kautz E, Juszczuk-Kubiak E, Domino M. Molecular Mechanism of Equine Endometrosis: The NF-κB-Dependent Pathway Underlies the Ovarian Steroid Receptors' Dysfunction.. Int J Mol Sci 2022 Jul 1;23(13).
    pmc: PMC9266418pubmed: 35806363doi: 10.3390/ijms23137360google scholar: lookup
  75. Nilsson EE, Detzel C, Skinner MK. Platelet-derived growth factor modulates the primordial to primary follicle transition.. Reproduction 2006 Jun;131(6):1007-15.
    doi: 10.1530/rep.1.00978pubmed: 16735540google scholar: lookup
  76. Banerjee P, Rodning SP, Diniz WJS, Dyce PW. Co-Expression Network and Integrative Analysis of Metabolome and Transcriptome Uncovers Biological Pathways for Fertility in Beef Heifers.. Metabolites 2022 Jul 29;12(8).
    pmc: PMC9413342pubmed: 36005579doi: 10.3390/metabo12080708google scholar: lookup

Citations

This article has been cited 0 times.