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Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Implication of transcriptome profiling of spermatozoa for stallion fertility

Yara Suliman A , Frank Becker A C and Klaus Wimmers B
+ Author Affiliations
- Author Affiliations

A Institute for Reproductive Biology, Leibniz Institute for Farm Animal Biology Dummerstorf, D-18196 Dummerstorf, Wilhem-Stahl-Allee 2, Germany.

B Institute for Genome Biology, Leibniz Institute for Farm Animal Biology Dummerstorf, D-18196 Dummerstorf, Wilhelm-Stahl-Allee 2, Germany.

C Corresponding author. Email: becker@fbn-dummerstorf.de

Reproduction, Fertility and Development 30(8) 1087-1098 https://doi.org/10.1071/RD17188
Submitted: 9 July 2016  Accepted: 6 December 2017   Published: 14 March 2018

Journal Compilation © CSIRO 2018 Open Access CC BY-NC-ND

Abstract

Poor fertility of breeding stallions is a recognised problem in the equine industry. The aim of the present study was to detect molecular pathways using two groups of stallions that differed in pregnancy rates as well as in the proportion of normal and motile spermatozoa. RNA was isolated from spermatozoa of each stallion and microarray data were analysed to obtain a list of genes for which transcript abundance differed between the groups (P ≤0.05, fold change ≥1.2). In all, there were 437 differentially expressed (DE) genes between the two groups (P ≤ 0.05, fold change ≥1.2). Next, the DE genes were analysed using Database for Annotation, Visualisation, and Integrated Discovery (DAVID). Finally, ingenuity pathways analysis (IPA) was used to identify top biological functions and significant canonical pathways associated with the DE genes. Analysis using the DAVID database showed significant enrichment in the gene ontology (GO) term ‘RNA binding’ (P = 0.05) and in the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway cytokine–cytokine receptor interaction (P = 0.02). Furthermore, IPA analysis showed interconnected biological functions and canonical pathways involved in the regulation of spermatogenesis and male fertility. In addition, significantly enriched metabolic pathways were identified. In conclusion, the present study has identified, for the first time, molecular processes in stallion spermatozoa that could be associated with stallion fertility.

Additional keywords: microarray, sperm RNA, spermatogenesis.


References

Ashrafzadeh, A., Nathan, S., and Anuar Karsani, S. (2013). Comparative analysis of Mafriwal (Bos taurus × Bos indicus) and Kedah Kelantan (Bos indicus) sperm proteome identifies sperm proteins potentially responsible for higher fertility in a tropical climate. Int. J. Mol. Sci. 14, 15860–15877.
Comparative analysis of Mafriwal (Bos taurus × Bos indicus) and Kedah Kelantan (Bos indicus) sperm proteome identifies sperm proteins potentially responsible for higher fertility in a tropical climate.Crossref | GoogleScholarGoogle Scholar |

Balhorn, R., Weston, S., Thomas, C., and Wyrobek, A. (1984). DNA packaging in mouse spermatids. Synthesis of protamine variants and four transition proteins. Exp. Cell Res. 150, 298–308.
DNA packaging in mouse spermatids. Synthesis of protamine variants and four transition proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhtVSktbs%3D&md5=e4ef8ae04ec845d904daf2ea3ad3142eCAS |

Bansal, S. K., Gupta, N., Sankhwar, S. N., and Rajender, S. (2015). Differential genes expression between fertile and infertile spermatozoa revealed by transcriptome analysis. PLoS One 10, e0127007.
Differential genes expression between fertile and infertile spermatozoa revealed by transcriptome analysis.Crossref | GoogleScholarGoogle Scholar |

Bettegowda, A., and Wilkinson Miles, F. (2010). Transcription and post-transcriptional regulation of spermatogenesis. Phil. Trans. R. Soc. B. 365, 1637–1651.
Transcription and post-transcriptional regulation of spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaisrrI&md5=a171a274dd2603810749bf6e6a4dbdd8CAS |

Bissonnette, N., Le’vesque-Sergerie, J. P., Thibault, C., and Boissonneault, G. (2009). Spermatozoal transcriptome profiling for bull sperm motility: a potential tool to evaluate semen quality. Reproduction 138, 65–80.
Spermatozoal transcriptome profiling for bull sperm motility: a potential tool to evaluate semen quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFemsb0%3D&md5=a32b4746c7290058912952df52903d2eCAS |

Bizzarri  M.Dinicola  S.Bevilacqua  A.Cucina  A.(2016) . Broad spectrum anticancer activity of myo-inositol and inositol hexakisphosphate. Int. J. Endocrinol. 2016, 5616807.

Boerke, A., Dieleman, S. J., and Gadella, B. M. (2007). A possible role for sperm RNA in early embryo development. Theriogenology 68, S147–S155.
A possible role for sperm RNA in early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaitLc%3D&md5=65478b39c78a5c4b6ce4c086e7162853CAS |

Brazma, A., Hingamp, P., Quackenbush, J., Sherlock, G., Spellman, P., Stoeckert, C., Aach, J., Ansorge, W., Ball, C. A., Causton, H. C., et al. (2009). Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat. Genet. 29, 365–371.
Minimum information about a microarray experiment (MIAME)-toward standards for microarray data.Crossref | GoogleScholarGoogle Scholar |

Bright, L. A., Burgess, S. C., Chowdhary, B., Swiderski, C. E., and McCarthy, F. M. (2009). Structural and functional-annotation of an equine whole genome oligoarray. BMC Bioinformatics 10, S8.
Structural and functional-annotation of an equine whole genome oligoarray.Crossref | GoogleScholarGoogle Scholar |

Bukowska, D., Kempisty, B., Piotrowska, H., Sosinska, B., Wozna, M., Ciesiolka, S., Antosik, P., Jaskowski, J. M., Brüssow, K. P., and Nowicki, M. (2013). The structure and role of mammalian sperm RNA: a review. Vet Med (Praha) 2, 57–64.

Calogero, A. E., Gullo, G., La Vignera, S., and Condorelli, R. A. (2015). Myoinositol improves sperm parameters and serum reproductive hormones in patients with idiopathic infertility: a prospective double-blind randomized placebocontrolled study. Andrology 3, 491–495.
Myoinositol improves sperm parameters and serum reproductive hormones in patients with idiopathic infertility: a prospective double-blind randomized placebocontrolled study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpt1WqtL0%3D&md5=7f83b6fccc3cfe21d5cc332dea34903bCAS |

Carrell, D. T. (2008). Contributions of spermatozoa to embryogenesis: assays to evaluate their genetic and epigenetic fitness. Reprod. Biomed. Online 16, 474–484.
Contributions of spermatozoa to embryogenesis: assays to evaluate their genetic and epigenetic fitness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsFOqs70%3D&md5=50b7c226ce9afb8f2d6f1c44599bbc99CAS |

Chauvin, T. R., and Griswold, M. D. (2004). Characterization of the expression and regulation of genes necessary for myo-inositol biosynthesis and transport in the seminiferous epithelium. Biol. Reprod. 70, 744–751.
Characterization of the expression and regulation of genes necessary for myo-inositol biosynthesis and transport in the seminiferous epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Chsb4%3D&md5=4bc471ca670dd53c8db2ece25fcf9ea3CAS |

Colegrove-Otero, L. J., Minshall, N., and Standart, N. (2005). RNA-binding proteins in early development. Crit. Rev. Biochem. Mol. Biol. 40, 21–73.
RNA-binding proteins in early development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisl2ku7k%3D&md5=628245b16fde059ce49052efd32c8158CAS |

Colenbrander, B., Feitsma, H., and Grooten, H. J. (1993). Optimizing semen production for artificial insemination in swine. J. Reprod. Fertil. Suppl. 48, 207–215.
| 1:STN:280:DyaK2c7psVCltQ%3D%3D&md5=71b943a3f22e61fd1910f97f4234132dCAS |

Colenbrander, B., Gadella, B. M., and Stout, T. A. (2003). The predictive value of semen analysis in the evaluation of stallion fertility. Reprod. Domest. Anim. 38, 305–311.
The predictive value of semen analysis in the evaluation of stallion fertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svis1Srtw%3D%3D&md5=4db49265c54f0524fb81c38702eedc0cCAS |

Condorelli, R. A., La Vignera, S., Di Bari, F., Unfer, V., and Calogero, A. E. (2011). Effects of myoinositol on sperm mitochondrial function in-vitro. Eur. Rev. Med. Pharmacol. Sci. 15, 129–134.
| 1:STN:280:DC%2BC3M3psV2mtQ%3D%3D&md5=359e882290fa686e40485fcc23531c3fCAS |

Condorelli, R. A., La Vignera, S., Bellanca, S., Vigari, E., and Calogero, A. E. (2012). Myoinositol: does it improve sperm mitochondrial function and sperm motility? Urology 79, 1290–1295.
Myoinositol: does it improve sperm mitochondrial function and sperm motility?Crossref | GoogleScholarGoogle Scholar |

Dadoune, J. P. (2009). Spermatozoal RNAs: what about their functions? Microsc. Res. Tech. 72, 536–551.
Spermatozoal RNAs: what about their functions?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVOnurrF&md5=937f88ba85e7e2e40dc6e1afdcaed394CAS |

Das, P. J., Paria, N., Gustafson-Seabury, A., Vishnoi, M., and Chaki, S. P. (2010). Total RNA isolation from stallion sperm and testis biopsies. Theriogenology 74, 1099–1106.e2.
Total RNA isolation from stallion sperm and testis biopsies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWqtLbN&md5=73339f428a0e56e3a31b759a537e8c90CAS |

Das, P. J., McCarthy, F., Vishnoi, M., Paria, N., Gresham, C., Li, G., Kachroo, P., Sudderth, A. K., Teague, S., Love, C. C., Varner, D. D., Chowdhary, B. P., and Raudsepp, T. (2013). Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq. PLoS One 8, e56535.
Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtFKgsbc%3D&md5=6944150cea425b55af05ccf21956b158CAS |

Dowsett, K. F., and Pattie, W. A. (1982). Characteristics and fertility of stallion semen. J. Reprod. Fertil. Suppl. 32, 1–8.
| 1:STN:280:DyaL3s7mtl2gsg%3D%3D&md5=eea7914b9a6ec179e0b1db5448fd1c5aCAS |

Feugang, J. M., Rodriguez-Osorio, N., Kaya, A., Wang, H., and Page, G. (2010). Transcriptome analysis of bull spermatozoa: implications for male fertility. Reprod. Biomed. Online 21, 312–324.
Transcriptome analysis of bull spermatozoa: implications for male fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSgtbrJ&md5=582cfa217d99c76533cb9e7b5419ef07CAS |

Gamboa, S., and Ramalho-Santos, J. (2005). SNARE proteins and caveolin-1 in stallion spermatozoa: possible implications for fertility. Theriogenology 64, 275–291.
SNARE proteins and caveolin-1 in stallion spermatozoa: possible implications for fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlt1Ggu7g%3D&md5=73db0db020a1f6d99d79e356b3304c53CAS |

Giesecke, K., Hamann, H., Stock, K. F., Klewitz, J., Martinsson, G., Distl, O., and Sieme, H. (2011). Evaluation of ACE, SP17, and FSHB as candidates for stallion fertility in Hanoverian warmblood horses. Anim. Reprod. Sci. 126, 200–206.
Evaluation of ACE, SP17, and FSHB as candidates for stallion fertility in Hanoverian warmblood horses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFygurk%3D&md5=f3997bc60550cd924fe5a0bc01361fa7CAS |

Gilbert, I., Bissonnette, N., Boissonneault, G., Vallee, M., and Robert, C. (2007). A molecular analysis of the population of mRNA in bovine spermatozoa. Reproduction 133, 1073–1086.
A molecular analysis of the population of mRNA in bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGnu7k%3D&md5=e054e25b9956a92c0fc9496276748257CAS |

Hales, D. B., Diemer, T., and Hales, K. H. (1999). Role of cytokines in testicular function. Endocrine 10, 201–217.
Role of cytokines in testicular function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlt1Olsrk%3D&md5=f1cf4420780f2d122eee4104e377d01cCAS |

Hamann, H., Mertens, U., Sieme, H., Klug, E., and Distl, O. (2005). Einfluss des Besamungsmanagements auf Fruchtbarkeitsmerkmale in der Population des Hannoverschen Warmbluts. Züchtungskunde 77, 194–205.

Hamann, H., Jude, R., Sieme, H., Mertens, U., Töpfer-Petersen, E., Distl, O., and Leeb, T. (2007). A polymorphism within the equine CRISP3 gene is associated with stallion fertility in Hanoverian warmblood horses. Anim. Genet. 38, 259–264.
A polymorphism within the equine CRISP3 gene is associated with stallion fertility in Hanoverian warmblood horses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsVOisrg%3D&md5=e1c77cd96943e41b6bca30f4077a08a7CAS |

Hedger, M. P., and Meinhardt, A. (2003). Cytokines and the immune–testicular axis. J. Reprod. Immunol. 58, 1–26.
Cytokines and the immune–testicular axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVCntLo%3D&md5=42e27de69ac0c055c83b2825d588d97dCAS |

Hinton, B. T., White, R. W., and Setchell, B. P. (1980). Concentrations of myo-inositol in the luminal fluid of the mammalian testis and epididymis. J. Reprod. Fertil. 58, 395–399.
Concentrations of myo-inositol in the luminal fluid of the mammalian testis and epididymis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhslOqs7Y%3D&md5=0154c2aace91d5d1eaa617fa1f352b66CAS |

Hirano, Y., Shibahara, H., Obara, H., Suzuki, T., Takamizawa, S., and Yamaguchi, C. (2001). Relationships between sperm motility characteristics assessed by the computer-aided sperm analysis (CASA) and fertilization rates in vitro. J. Assist. Reprod. Genet. 18, 215–220.
Relationships between sperm motility characteristics assessed by the computer-aided sperm analysis (CASA) and fertilization rates in vitro.Crossref | GoogleScholarGoogle Scholar |

Hosken, D. J., and Hodgson, D. J. (2014). Why do sperm carry RNA? Relatedness, conflict, and control. Trends Ecol. Evol. 29, 451–455.
Why do sperm carry RNA? Relatedness, conflict, and control.Crossref | GoogleScholarGoogle Scholar |

Idler, R. K., and Yan, W. (2012). Control of messenger RNA fate by RNA-binding proteins: an emphasis on mammalian spermatogenesis. J. Androl. 33, 309–337.
Control of messenger RNA fate by RNA-binding proteins: an emphasis on mammalian spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOmt7%2FN&md5=e9f675eff118e9248531bc3d4dda6cbeCAS |

Ihsan, E. A. A. (2014). Evaluation of serum levels of pro-inflammatory cytokines (interleukins 2, 6, 8) in fertile and infertile men. DJMBR 1, 23–34.

Ingman, W. V., and Rebecca, L. J. (2008). Cytokine knockouts in reproduction: the use of gene ablation to dissect roles of cytokines in reproductive biology. Hum. Reprod. Update 14, 179–192.
Cytokine knockouts in reproduction: the use of gene ablation to dissect roles of cytokines in reproductive biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVKmu74%3D&md5=353da1138dc856326553156eb0269060CAS |

Jasko, D. J., Lein, D. H., and Foote, R. H. (1990a). Determination of the relationship between sperm morphologic classifications and fertility in stallions: 66 cases (1987–1988). J. Am. Vet. Med. Assoc. 197, 389–394.
| 1:STN:280:DyaK3czmtFGktQ%3D%3D&md5=6ee8d80141802be0fe03bd5deb0ee70cCAS |

Kane, M. T., Morgan, P. M., and Coonan, C. (1997). Peptide growth factors and preimplantation development. Hum. Reprod. Update 3, 137–157.
Peptide growth factors and preimplantation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVWmt70%3D&md5=f69492eb0dc82b6f1f52e80f0634c353CAS |

Kempisty, B., Antosik, P., Bukowska, D., Jackowska, M., and Lianeri, M. (2008). Analysis of selected transcript levels in porcine spermatozoa, oocytes, zygotes and two-cell stage embryos. Reprod. Fertil. Dev. 20, 513–518.
Analysis of selected transcript levels in porcine spermatozoa, oocytes, zygotes and two-cell stage embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFagsrs%3D&md5=c8a9f1657b2026806fe2d418a3050453CAS |

Krawetz, S. A. (2005). Paternal contribution: new insights and future challenges. Nat. Rev. Genet. 6, 633–642.
Paternal contribution: new insights and future challenges.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntFeqtbo%3D&md5=505a7c9dcacf8cce716459f2dfb60659CAS |

Kropp, J., Carillo, J. A., Namous, H., Daniels, A., Salih, S. M., Song, J., and Katib, H. (2017). Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genomics 18, 280–296.
Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |

Lalancette, C., Miller, D., Li, Y., and Krawetz, S. A. (2008). Paternal contributions: new functional insights for spermatozoal RNA. J. Cell. Biochem. 104, 1570–1579.
Paternal contributions: new functional insights for spermatozoal RNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvVOjt7w%3D&md5=19664600994c1098835d8850a26083bbCAS |

Lambard, S., Galeraud-Denis, I., Martin, G., Levy, R., Chocat, A., and Carreau, S. (2004). Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: relationship to sperm motility and capacitation. Mol. Hum. Reprod. 10, 535–541.
Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: relationship to sperm motility and capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVWnsr8%3D&md5=32b4a2953d5f363e0db7d22e7e6bd457CAS |

Martins, R. P., and Krawetz, S. A. (2005). RNA in human sperm. Asian J. Androl. 7, 115–120.
RNA in human sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXos1aluro%3D&md5=47681c406fb3ac80b9f9ba3f3b624c46CAS |

Menzies, P. I. (1999). Reproductive health management programs. In ‘Current Therapy in Large Animal Theriogenology’. (Ed. R. S. Youngquist.) pp. 643–649. (W. B. Saunders and Co.: Philadelphia, PA.)

Miller, D. (2000). Analysis and significance of messenger RNA in human ejaculated spermatozoa. Mol. Reprod. Dev. 56, 259–264.
Analysis and significance of messenger RNA in human ejaculated spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtFyrtrk%3D&md5=6902e779229ab96888eb7c689263cdf1CAS |

Miller, D., and Ostermeier, G. C. (2006). Towards a better understanding of RNA carriage by ejaculate spermatozoa. Hum. Reprod. Update 12, 757–767.
Towards a better understanding of RNA carriage by ejaculate spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFeisbzF&md5=6da137dd68eadc3509bcc144a75eda70CAS |

Miller, D., Briggs, D., Snowden, H., Hamlington, J., Rollinson, S., Lilford, R., and Krawetz, S. A. (1999). A complex population of RNAs exists in human ejaculate spermatozoa: implications for understanding molecular aspects of spermiogenesis. Gene 237, 385–392.
A complex population of RNAs exists in human ejaculate spermatozoa: implications for understanding molecular aspects of spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvVWlt7o%3D&md5=9645bc51a39e28c5d8ed4ccf25558adaCAS |

Morris, L. H. A., and Allen, W. R. (2002). Reproductive efficiency of intensively managed thoroughbred mares in Newmarket. Equine Vet. J. 34, 51–60.
Reproductive efficiency of intensively managed thoroughbred mares in Newmarket.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fptlequg%3D%3D&md5=93f3fdf6cacfa401d93f1026d2998a9bCAS |

Neganova, I., and Lako, M. (2008). G1 to S phase cell cycle transition in somatic and embryonic stem cells. J. Anat. 213, 30–44.
G1 to S phase cell cycle transition in somatic and embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslajsbw%3D&md5=f823863916467e8e9b7e6b9508ca1979CAS |

Novak, S., Smith, T. A., Paradis, F., Burwash, L., Dyck, M. K., Foxcroft, G. R., and Dixon, W. T. (2010). Biomarkers of in vivo fertility in sperm and seminal plasma of fertile stallions. Theriogenology 74, 956–967.
Biomarkers of in vivo fertility in sperm and seminal plasma of fertile stallions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWqtLbL&md5=8bf52c0c61ea8acedad059afa4473bb7CAS |

Ostermeier, G. C., Dix, D. J., Miller, D., Khatri, P., and Krawetz, S. A. (2002). Spermatozoal RNA profiles of normal fertile men. Lancet 360, 772–777.
Spermatozoal RNA profiles of normal fertile men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmsl2nsLg%3D&md5=edba25b46292df4b7eb91e6cdaf6e2d4CAS |

Paulesu, L., Jantra, S., Ietta, F., Brizzi, R., Avanzati, A. M., and Bigliardi, E. (2010). Cytokines in vertebrate reproduction. Herpetol. Conserv. Biol. 5, 335–340.

Platts, A. E., Dix, D. J., Chemes, H. E., Thompson, K. E., Goodrich, R., Rockett, J. C., Rawe, V. Y., Quintana, S., Diamond, M. P., Strader, L. F., and Krawetz, S. A. (2007). Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum. Mol. Genet. 16, 763–773.
Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsVWnsbk%3D&md5=d9aa10f6ab2344ecceda3f3dfb3cce92CAS |

Poltich, J. A., Tucker, L., Bowman, F. P., and Anderson, D. J. (2007). Concentrations and significance of cytokines and other immunologic factors in semen of healthy fertile men. Hum. Reprod. 22, 2928–2935.
Concentrations and significance of cytokines and other immunologic factors in semen of healthy fertile men.Crossref | GoogleScholarGoogle Scholar |

Robertson, S. A., Sjoblom, C., Jasper, M. J., Norman, R. J., and Seamark, R. F. (2001). Granulocyte–macrophage colony-stimulating factor promotes glucose transport and blastomere viability in murine preimplantation embryos. Biol. Reprod. 64, 1206–1215.
Granulocyte–macrophage colony-stimulating factor promotes glucose transport and blastomere viability in murine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1aru7c%3D&md5=1cd37869bf155797fdf0b433a3e1c7ebCAS |

Robertson, S. A., Care, A. S., and Skinner, R. J. (2007). Interleukin 10 regulates inflammatory cytokine synthesis to protect against lipopolysaccharide-induced abortion and fetal growth restriction in mice. Biol. Reprod. 76, 738–748.
Interleukin 10 regulates inflammatory cytokine synthesis to protect against lipopolysaccharide-induced abortion and fetal growth restriction in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXks1Ohs78%3D&md5=fabb94e785bd55750f0ad262c0e357f1CAS |

Ruwanpura, S. M., McLachlan, R. E., and Meachem, S. J. (2010). Hormonal regulation of male germ cell development. J. Endocrinol. 205, 117–131.
Hormonal regulation of male germ cell development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVCgs7s%3D&md5=7c028f2b82b89a6cdda67b75235caf3cCAS |

Sassone-Corsi, P. (2002). Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296, 2176–2178.
Unique chromatin remodeling and transcriptional regulation in spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvFGhsb8%3D&md5=7ff9f57aa74032f802913d151ad6cdb1CAS |

Schambony, A., Gentzel, M., Wolfes, H., Raida, M., Neumann, U., and Töpfer-Petersen, E. (1998). Equine CRISP-3: primary structure and expression in the male genital tract. Biochim. Biophys. Acta 1387, 206–216.
Equine CRISP-3: primary structure and expression in the male genital tract.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsl2gsbw%3D&md5=6075294d3e8fececbb0549b2fe147b10CAS |

Setchell, B. P., Dawson, R. M., and White, R. W. (1968). The high concentration of free myo-inositol in rete testis fluid from rams. J. Reprod. Fertil. 17, 219–220.
The high concentration of free myo-inositol in rete testis fluid from rams.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXis12jsQ%3D%3D&md5=c9e86ec0ced874993714b1d0e53e6516CAS |

Sharkey, A. (1998). Cytokines and implantation. Rev. Reprod. 3, 52–61.
Cytokines and implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1Wrsbw%3D&md5=787831dbd5ab906a17275ad93747c2ecCAS |

Simón, C., Valbuena, D., Krüssel, J. S., Bernal, A., and Murphy, C. R. (1998). Interleukin-1 receptor antagonist prevents embryonic implantation by a direct effect on the endometrial epithelium. Fertil. Steril. 70, 896–906.
Interleukin-1 receptor antagonist prevents embryonic implantation by a direct effect on the endometrial epithelium.Crossref | GoogleScholarGoogle Scholar |

Sjöblom, C., Wikland, M., and Robertson, S. A. (1999). Granulocyte–macrophage colony-stimulating factor promotes human blastocyst development in vitro. Hum. Reprod. 14, 3069–3076.
Granulocyte–macrophage colony-stimulating factor promotes human blastocyst development in vitro.Crossref | GoogleScholarGoogle Scholar |

Steger, K. (2001). Haploid spermatids exhibit translationally repressed mRNAs. Anat. Embryol. (Berl.) 203, 323–334.
Haploid spermatids exhibit translationally repressed mRNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosFChtrY%3D&md5=151cc34987058e181ffe5fcc91803c2bCAS |

Steger, K., Fink, L., Failing, K., Bohle, R. M., Kliesch, S., Weidner, W., and Bergmann, M. (2003). Decreased protamine1 transcript levels in testes from infertile men. Mol. Hum. Reprod. 9, 331–336.
Decreased protamine1 transcript levels in testes from infertile men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovVKhsLk%3D&md5=cf44e61527e40ed5db9f3f9e4e1ec857CAS |

Töpfer-Petersen, E., Ekhlasi-Hundrieser, M., Kirchhoff, C., Leeb, T., and Sieme, H. (2005). The role of stallion seminal proteins in fertilization. Anim. Reprod. Sci. 89, 159–170.
The role of stallion seminal proteins in fertilization.Crossref | GoogleScholarGoogle Scholar |

Voss, J. L., Pickett, B. W., and Squires, E. L. (1981). Stallion spermatozoal morphology and motility and their relationship to fertility. J. Am. Vet. Med. Assoc. 178, 287–289.
| 1:STN:280:DyaL3M7ptFOgtw%3D%3D&md5=8337f708b478d03e324f9fefa399d68aCAS |

Wolgemuth, D. J., Laurion, E., and Lele, K. M. (2002). Regulation of the mitotic and meiotic cell cycles in the male germ line. The Endocrine Society 365, 1653–1662.
Regulation of the mitotic and meiotic cell cycles in the male germ line.Crossref | GoogleScholarGoogle Scholar |

Wolgemuth, D. J., Manterola, M., and Vasileva, A. (2013). Role of cyclins in controlling progression of mammalian spermatogenesis. Int. J. Dev. Biol. 57, 159–168.
Role of cyclins in controlling progression of mammalian spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVersbjP&md5=3050e4b613b5ec818f5dc0048a23a344CAS |

Yang, C. C., Lin, Y. S., Hsu, C. C., Wu, S. C., and Lin, E. C. (2009). Identification and sequencing of remnant messenger RNAs found in domestic swine (Sus scrofa) fresh ejaculated spermatozoa. Anim. Reprod. Sci. 113, 143–155.
Identification and sequencing of remnant messenger RNAs found in domestic swine (Sus scrofa) fresh ejaculated spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFeltbo%3D&md5=bd553270ba9ca5cb88312716a9208c69CAS |

Zaabal, M. M., and Ahmed, W. M. (2010). Monitoring of gene markers associated with fertility in purebred Arabian stallions. J. Reprod. Infertil. 1, 41–44.

Zhao, Y., Li, Q., Yao, C., Wang, Z., Zhou, Y., Wang, Y., Liu, L., Wang, Y., Wang, L., and Qiao, Z. (2006). Characterization and quantification of mRNA transcripts in ejaculated spermatozoa of fertile men by serial analysis of gene expression. Hum. Reprod. 21, 1583–1590.
Characterization and quantification of mRNA transcripts in ejaculated spermatozoa of fertile men by serial analysis of gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntF2gu70%3D&md5=557635bb3d6b89061876e230242d3477CAS |