Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Seminal plasma and cryopreservation alter ram sperm surface carbohydrates and interactions with neutrophils

Taylor Pini A B , Tamara Leahy A and Simon Paul de Graaf A
+ Author Affiliations
- Author Affiliations

A School of Life and Environmental Sciences, Faculty of Science, University of Sydney, Camperdown, NSW 2006, Australia.

B Corresponding author. Email: taylor.pini@sydney.edu.au

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17251
Submitted: 3 July 2017  Accepted: 18 September 2017   Published online: 25 October 2017

Abstract

Spermatozoa deposited vaginally must navigate the physical, chemical and immune barriers of the cervix to reach the site of fertilisation. Characteristics that favour successful cervical transit remain largely unknown beyond the obvious factors of motility and viability. Epididymal and cryopreserved ram spermatozoa demonstrate poor cervical transit, for unknown reasons. We hypothesised that seminal plasma exposure and cryopreservation alter the surface sugars of these sperm populations and, consequently, their interaction with immune cells, both potential factors for successful cervical transit. The carbohydrate profiles of epididymal, ejaculated and frozen–thawed ram spermatozoa were assessed by flow cytometry and western blotting using lectins for galactose, sialic acid, N-acetylglucosamine and mannose. Seminal plasma exposure and cryopreservation caused significant changes to the relative amounts of surface sugars detected by flow cytometry and lectin blotting. Immune cell interaction was characterised using a neutrophil-binding assay. Seminal plasma acted as a robust protective mechanism, limiting binding of spermatozoa, whereas the media used for cryopreservation caused a significant disruption to opsonin-mediated binding. We were unable to demonstrate a link between changes to surface sugars and neutrophil susceptibility. Seminal plasma and cryopreservation clearly alter the sperm glycocalyx, as well as the interaction of spermatozoa with immune cells.

Additional keywords: cervix, immune, ovine.


References

Alghamdi, A. S., and Foster, D. N. (2005). Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps. Biol. Reprod. 73, 1174–1181.
Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps.CrossRef | 1:CAS:528:DC%2BD2MXht1KqsLrP&md5=539fbd8e1369ed33767c99f14d9542aeCAS |

Alghamdi, A. S., Foster, D. N., and Troedsson, M. H. T. (2004). Equine seminal plasma reduces sperm binding to polymorphonuclear neutrophils (PMNs) and improves the fertility of fresh semen inseminated into inflamed uteri. Reproduction 127, 593–600.
Equine seminal plasma reduces sperm binding to polymorphonuclear neutrophils (PMNs) and improves the fertility of fresh semen inseminated into inflamed uteri.CrossRef | 1:CAS:528:DC%2BD2cXkvFOqu7o%3D&md5=5ca863755493b7fefef055b2573853fbCAS |

Alghamdi, A. S., Lovaas, B. J., Bird, S. L., Lamb, G. C., Rendahl, A. K., Taube, P. C., and Foster, D. N. (2009). Species-specific interaction of seminal plasma on sperm–neutrophil binding. Anim. Reprod. Sci. 114, 331–344.
Species-specific interaction of seminal plasma on sperm–neutrophil binding.CrossRef | 1:CAS:528:DC%2BD1MXosVGhtbY%3D&md5=fe2aca08e06cc1905819e789238a8769CAS |

Aloé, S., Weber, F., Behr, B., Sauter-Louis, C., and Zerbe, H. (2012). Modulatory effects of bovine seminal plasma on uterine inflammatory processes. Reprod. Domest. Anim. 47, 12–19.
Modulatory effects of bovine seminal plasma on uterine inflammatory processes.CrossRef |

Athamna, A., Ofek, I., Keisari, Y., Markowitz, S., Dutton, G. G., and Sharon, N. (1991). Lectinophagocytosis of encapsulated Klebsiella pneumonia-mediated by surface lectins of guinea pig alveolar macrophages and human monocyte-derived macrophages. Infect. Immun. 59, 1673–1682.
| 1:CAS:528:DyaK3MXkvFSmsrc%3D&md5=39d7f30e1e4c768afa2337dd6963ad69CAS |

Baumber, J., Vo, A., Sabeur, K., and Ball, B. A. (2002). Generation of reactive oxygen species by equine neutrophils and their effect on motility of equine spermatozoa. Theriogenology 57, 1025–1033.
Generation of reactive oxygen species by equine neutrophils and their effect on motility of equine spermatozoa.CrossRef | 1:STN:280:DC%2BD38zgtVantA%3D%3D&md5=8b0c1bd7849373d4a18fcddf8f33ee58CAS |

Bawa, S. R., Pabst, M. A., Werner, G., and Bains, H. K. (1993). Capacitated and acrosome reacted spermatozoa of goat (Capra indicus): a fluorescence and electron microscopic study. Andrologia 25, 123–135.
Capacitated and acrosome reacted spermatozoa of goat (Capra indicus): a fluorescence and electron microscopic study.CrossRef | 1:STN:280:DyaK3s3pslOnug%3D%3D&md5=7db0bb300193564d927ffa174e131c17CAS |

Binks, S., and Pockley, A. G. (1999). Modulation of leukocyte phagocytic and oxidative burst responses by human seminal plasma. Immunol. Invest. 28, 353–364.
Modulation of leukocyte phagocytic and oxidative burst responses by human seminal plasma.CrossRef | 1:STN:280:DC%2BD3c%2FjvFOqsg%3D%3D&md5=d4e64eec2c73d8f5581e90d2ce2cd14bCAS |

Chatterjee, S., and Gagnon, C. (2001). Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing. Mol. Reprod. Dev. 59, 451–458.
Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing.CrossRef | 1:CAS:528:DC%2BD3MXltVWmsb4%3D&md5=99c8558c0b7d280948c868493cd3f062CAS |

Clark, G. F., and Schust, D. J. (2013). Manifestations of immune tolerance in the human female reproductive tract. Front. Immunol. 4, 26.
Manifestations of immune tolerance in the human female reproductive tract.CrossRef | 1:CAS:528:DC%2BC3sXms1CrtLc%3D&md5=85912b52b14e6c6e60c43fee2844568eCAS |

Cone, R. A. (2009). Barrier properties of mucus. Adv. Drug Deliv. Rev. 61, 75–85.
Barrier properties of mucus.CrossRef | 1:CAS:528:DC%2BD1MXit1Ohtrs%3D&md5=d65f93cc90e5932e67b32be8e8497029CAS |

Constantinescu, A. A., Vink, H., and Spaan, J. A. E. (2001). Elevated capillary tube hematocrit reflects degradation of endothelial cell glycocalyx by oxidized LDL. Am. J. Physiol. Heart Circ. Physiol. 280, H1051–H1057.
| 1:CAS:528:DC%2BD3MXjtV2gt7o%3D&md5=e4173642ff01c1d0fb59ba1082a2bb97CAS |

Coulter, G. H., Foote, R. H., Schiavo, J. J., and Braun, R. K. (1976). Antibodies to egg yolk in blood serum of rabbits and cattle and cervical mucus of cattle inseminated artificially. Theriogenology 6, 585–589.
Antibodies to egg yolk in blood serum of rabbits and cattle and cervical mucus of cattle inseminated artificially.CrossRef | 1:STN:280:DyaE2s3gsFaitA%3D%3D&md5=e9378e0a7650a45835253e91af638150CAS |

Crestani, B., Rolland, C., Petiet, A., Colas-Linhart, N., and Aubier, M. (1993). Cell surface carbohydrates modulate neutrophil adherence to alveolar type II cells in vitro. Am. J. Physiol. Lung Cell. Mol. Physiol. 264, L391–L400.
| 1:CAS:528:DyaK3sXksVOgsLY%3D&md5=6f135b95a74b50a857a9bb2d5a48b8b0CAS |

Cropp, A. R. (2006) Interaction of bovine seminal proteins with neutrophils. M.Sc. Thesis, The University of Arizona, Ann Arbor.

D’Cruz, O. J., and Haas, G. G. (1995). Beta 2-integrin (CD11b/CD18) is the primary adhesive glycoprotein complex involved in neutrophil-mediated immune injury to human sperm. Biol. Reprod. 53, 1118–1130.
Beta 2-integrin (CD11b/CD18) is the primary adhesive glycoprotein complex involved in neutrophil-mediated immune injury to human sperm.CrossRef | 1:CAS:528:DyaK2MXoslynurY%3D&md5=4b020db64a6315e54cf0baa7991cfb7fCAS |

Denison, F. C., Grant, V. E., Calder, A. A., and Kelly, R. W. (1999). Seminal plasma components stimulate interleukin-8 and interleukin-10 release. Mol. Hum. Reprod. 5, 220–226.
Seminal plasma components stimulate interleukin-8 and interleukin-10 release.CrossRef | 1:CAS:528:DyaK1MXitFamu7g%3D&md5=aab51d698727c662106a0381432486fcCAS |

Dostàlovà, Z., Calvete, J. J., Sanz, L., and Töpfer-Petersen, E. (1994). Quantitation of boar spermadhesins in accessory sex gland fluids and on the surface of epididymal, ejaculated and capacitated spermatozoa. Biochim. Biophys. Acta, Gen. Subj. 1200, 48–54.
Quantitation of boar spermadhesins in accessory sex gland fluids and on the surface of epididymal, ejaculated and capacitated spermatozoa.CrossRef |

Doty, A., Buhi, W. C., Benson, S., Scoggin, K. E., Pozor, M., Macpherson, M., Mutz, M., and Troedsson, M. H. T. (2011). Equine CRISP3 modulates interaction between spermatozoa and polymorphonuclear neutrophils. Biol. Reprod. 85, 157–164.
Equine CRISP3 modulates interaction between spermatozoa and polymorphonuclear neutrophils.CrossRef | 1:CAS:528:DC%2BC3MXotFOlsL8%3D&md5=4d63dbd87d5b05d97522c3fcca4d507cCAS |

Eriksen, G. V., Carlstedt, I., Uldbjerg, N., and Ernst, E. (1998). Cervical mucins affect the motility of human spermatozoa in vitro. Fertil. Steril. 70, 350–354.
Cervical mucins affect the motility of human spermatozoa in vitro.CrossRef | 1:STN:280:DyaK1czlvFChsA%3D%3D&md5=8cee724e9192771e47e5ac0b545e8104CAS |

Fischer, C., Kelm, S., Ruch, B., and Schauer, R. (1991). Reversible binding of sialidase-treated rat lymphocytes by homologous peritoneal macrophages. Carbohydr. Res. 213, 263–273.
Reversible binding of sialidase-treated rat lymphocytes by homologous peritoneal macrophages.CrossRef | 1:CAS:528:DyaK3MXltFalsLk%3D&md5=d3a0c9487c9e7e7f4511e1a1a4f7337eCAS |

Futosi, K., Fodor, S., and Mócsai, A. (2013). Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int. Immunopharmacol. 17, 638–650.
Neutrophil cell surface receptors and their intracellular signal transduction pathways.CrossRef | 1:CAS:528:DC%2BC3sXhslWhu7jF&md5=dad7495e17f14682c7bdd2e958859b90CAS |

Gadella, B. M., and Boerke, A. (2016). An update on post-ejaculatory remodeling of the sperm surface before mammalian fertilization. Theriogenology 85, 113–124.
An update on post-ejaculatory remodeling of the sperm surface before mammalian fertilization.CrossRef | 1:CAS:528:DC%2BC2MXhtlOmt7vF&md5=cb578498211f559b318426192a2c2ea5CAS |

Gilbert, R. O., and Fales, M. H. (1996). The effect of bovine seminal plasma on the function and integrity of bovine neutrophils. Theriogenology 46, 649–658.
The effect of bovine seminal plasma on the function and integrity of bovine neutrophils.CrossRef | 1:STN:280:DC%2BD28zgtVKrtg%3D%3D&md5=054c4912126a882b4e1de8f7bb7ad81eCAS |

Gillan, L., Evans, G., and Maxwell, W. M. C. (1997). Capacitation status and fertility of fresh and frozen–thawed ram spermatozoa. Reprod. Fertil. Dev. 9, 481–487.
Capacitation status and fertility of fresh and frozen–thawed ram spermatozoa.CrossRef | 1:STN:280:DyaK1c%2FnvVOrtw%3D%3D&md5=9600c1305cfd624fdcda5a88282bedceCAS |

Griffin, J. F. T., Nunn, W. R., and Hartigan, P. J. (1971). An immune response to egg-yolk semen diluent in dairy cows. J. Reprod. Fertil. 25, 193–199.
An immune response to egg-yolk semen diluent in dairy cows.CrossRef | 1:STN:280:DyaE3M3lt1CqtA%3D%3D&md5=f98cf7cc26471476b825c1967be330faCAS |

Gwathmey, T. M., Ignotz, G. G., and Suarez, S. S. (2003). PDC-109 (BSP-A1/A2) promotes bull sperm binding to oviductal epithelium in vitro and may be involved in forming the oviductal sperm reservoir. Biol. Reprod. 69, 809–815.
PDC-109 (BSP-A1/A2) promotes bull sperm binding to oviductal epithelium in vitro and may be involved in forming the oviductal sperm reservoir.CrossRef | 1:CAS:528:DC%2BD3sXmvVeitL8%3D&md5=3797ab36bc1fafd3aa6e8878c5ba4169CAS |

Halbert, G. W., Dobson, H., Walton, J. S., and Buckrell, B. C. (1990). The structure of the cervical canal of the ewe. Theriogenology 33, 977–992.
The structure of the cervical canal of the ewe.CrossRef | 1:STN:280:DC%2BD283pvFGmtQ%3D%3D&md5=381656fba8f537b480097e0cadebb935CAS |

Harris, C. L., Mizuno, M., and Morgan, B. P. (2006). Complement and complement regulators in the male reproductive system. Mol. Immunol. 43, 57–67.
Complement and complement regulators in the male reproductive system.CrossRef | 1:CAS:528:DC%2BD2MXms1Ogu7o%3D&md5=c6e987aabeab119f84a9791c14dbcacdCAS |

He, Y., Wang, K., Zhao, X., Zhang, Y., Ma, Y., and Hu, J. (2016). Differential proteome association study of freeze–thaw damage in ram sperm. Cryobiology 72, 60–68.
Differential proteome association study of freeze–thaw damage in ram sperm.CrossRef | 1:CAS:528:DC%2BC2MXhvFCltrzE&md5=fedf426e8a1e6cb19ebab67baf28710eCAS |

Holt, W. V. (1980). Surface-bound sialic acid on ram and bull spermatozoa: deposition during epididymal transit and stability during washing. Biol. Reprod. 23, 847–857.
Surface-bound sialic acid on ram and bull spermatozoa: deposition during epididymal transit and stability during washing.CrossRef | 1:CAS:528:DyaL3MXivVagtQ%3D%3D&md5=8f47a29be9811e56d3907a7e4f845d46CAS |

Jiménez, I., González-Márquez, H., Ortiz, R., Betancourt, M., Herrera, J., and Fierro, R. (2002). Expression of lectin receptors on the membrane surface of sperm of fertile and subfertile boars by flow cytometry. Arch. Androl. 48, 159–166.

Kotilainen, T., Huhtinen, M., and Katila, T. (1994). Sperm-induced leukocytosis in the equine uterus. Theriogenology 41, 629–636.
Sperm-induced leukocytosis in the equine uterus.CrossRef | 1:STN:280:DC%2BD28zgtVWktA%3D%3D&md5=5d5fb13f26dc0410752193fda470fbf6CAS |

Kovalski, N. N., de Lamirande, E., and Gagnon, C. (1992). Reactive oxygen species generated by human neutrophils inhibit sperm motility: protective effect of seminal plasma and scavengers. Fertil. Steril. 58, 809–816.
Reactive oxygen species generated by human neutrophils inhibit sperm motility: protective effect of seminal plasma and scavengers.CrossRef | 1:STN:280:DyaK3s%2FltVaqtA%3D%3D&md5=45290ccdb20bb8e1f4983aec1e07e30eCAS |

Kurpisz, M., and Alexander, N. J. (1995). Carbohydrate moieties on sperm surface: physiological relevance. Fertil. Steril. 63, 158–165.
Carbohydrate moieties on sperm surface: physiological relevance.CrossRef | 1:STN:280:DyaK2M7gsVCruw%3D%3D&md5=83e8d2b50a9f17642d6db2a8144ca5c9CAS |

Leahy, T., Rickard, J. P., Aitken, R. J., and de Graaf, S. P. (2016). Penicillamine prevents ram sperm agglutination in media that support capacitation. Reproduction 151, 167–177.
Penicillamine prevents ram sperm agglutination in media that support capacitation.CrossRef | 1:CAS:528:DC%2BC28XivVaktLk%3D&md5=bac0a1b55871a6dd031f0ff9c12f612aCAS |

Li, J. C., and Funahashi, H. (2010). Effect of blood serum, caffeine and heparin on in vitro phagocytosis of frozen–thawed bull sperm by neutrophils derived from the peripheral blood of cows. Theriogenology 74, 691–698.
Effect of blood serum, caffeine and heparin on in vitro phagocytosis of frozen–thawed bull sperm by neutrophils derived from the peripheral blood of cows.CrossRef | 1:CAS:528:DC%2BC3cXhtVersLnI&md5=9c7f7646e58c17a9408b2883debed185CAS |

Li, J. C., Yamaguchi, S., and Funahashi, H. (2012). Boar seminal plasma or hen’s egg yolk decrease the in vitro chemotactic and phagocytotic activities of neutrophils when co-incubated with boar or bull sperm. Theriogenology 77, 73–80.
Boar seminal plasma or hen’s egg yolk decrease the in vitro chemotactic and phagocytotic activities of neutrophils when co-incubated with boar or bull sperm.CrossRef | 1:CAS:528:DC%2BC3MXhsF2rt7vK&md5=a6a0872405fc98d158f7e78882f5e996CAS |

Lightfoot, R. J., and Salamon, S. (1970). Fertility of ram spermatozoa frozen by the pellet method. J. Reprod. Fertil. 22, 385–398.
Fertility of ram spermatozoa frozen by the pellet method.CrossRef | 1:STN:280:DyaE3c3ns1emuw%3D%3D&md5=4323f63f6510da3ea1cd00215e45e972CAS |

López-Revuelta, A., Sánchez-Gallego, J. I., García-Montero, A. C., Hernández-Hernández, A., Sánchez-Yagüe, J., and Llanillo, M. (2007). Membrane cholesterol in the regulation of aminophospholipid asymmetry and phagocytosis in oxidized erythrocytes. Free Radic. Biol. Med. 42, 1106–1118.
Membrane cholesterol in the regulation of aminophospholipid asymmetry and phagocytosis in oxidized erythrocytes.CrossRef |

Ma, X., Pan, Q., Feng, Y., Choudhury, B. P., Ma, Q., Gagneux, P., and Ma, F. (2016). Sialylation facilitates the maturation of mammalian sperm and affects its survival in female uterus. Biol. Reprod. 94, 123.
Sialylation facilitates the maturation of mammalian sperm and affects its survival in female uterus.CrossRef |

Magargee, S. F., Kunze, E., and Hammerstedt, R. H. (1988). Changes in lectin-binding features of ram sperm surfaces associated with epididymal maturation and ejaculation. Biol. Reprod. 38, 667–685.
Changes in lectin-binding features of ram sperm surfaces associated with epididymal maturation and ejaculation.CrossRef | 1:CAS:528:DyaL1cXitVansLg%3D&md5=4dd978bd6fc709eb5f0224e160a00836CAS |

Mahmoud, A. I., and Parrish, J. J. (1996). Oviduct fluid and heparin induce similar surface changes in bovine sperm during capacitation: a flow cytometric study using lectins. Mol. Reprod. Dev. 43, 554–560.
Oviduct fluid and heparin induce similar surface changes in bovine sperm during capacitation: a flow cytometric study using lectins.CrossRef | 1:CAS:528:DyaK28XitVGjsLk%3D&md5=81e102d92719f0732997004da056d8d8CAS |

Martínez-Rodríguez, C., Alvarez, M., López-Urueña, E., Gomes-Alves, S., Anel-López, L., Chamorro, C. A., Anel, L., and de Paz, P. (2015). Ram spermatozoa migrating through artificial mucus in vitro have reduced mitochondrial membrane potential but retain their viability. Reprod. Fertil. Dev. 27, 852–864.
Ram spermatozoa migrating through artificial mucus in vitro have reduced mitochondrial membrane potential but retain their viability.CrossRef |

Matthijs, A., Harkema, W., Engel, B., and Woelders, H. (2000). In vitro phagocytosis of boar spermatozoa by neutrophils from peripheral blood of sows. J. Reprod. Fertil. 120, 265–273.
| 1:CAS:528:DC%2BD3cXovVajur0%3D&md5=c7d65dea8f97425aa3999ae5b8265ae5CAS |

Mattner, P. E. (1969). Differential leucocytic responses to spermatozoa in the cervix and the uterus in ewes. J. Reprod. Fertil. 18, 297–303.
Differential leucocytic responses to spermatozoa in the cervix and the uterus in ewes.CrossRef | 1:STN:280:DyaF1M3hvFGjtA%3D%3D&md5=514c32567ac154eb34a6e5dbc198eae6CAS |

Maxwell, W. M. C., and Hewitt, L. J. (1986). A comparison of vaginal, cervical and intrauterine insemination of sheep. J. Agric. Sci. 106, 191–193.
A comparison of vaginal, cervical and intrauterine insemination of sheep.CrossRef |

Maxwell, W. M. C., Evans, G., Mortimer, S. T., Gillan, L., Gellatly, E. S., and McPhie, C. A. (1999). Normal fertility in ewes after cervical insemination with frozen–thawed spermatozoa supplemented with seminal plasma. Reprod. Fertil. Dev. 11, 123–126.
Normal fertility in ewes after cervical insemination with frozen–thawed spermatozoa supplemented with seminal plasma.CrossRef | 1:STN:280:DC%2BD3c7pslKjsQ%3D%3D&md5=aa8ff7565f86dc6ab91f651336b00f78CAS |

Miró, J., Vilés, K., García, W., Jordana, J., and Yeste, M. (2013). Effect of donkey seminal plasma on sperm movement and sperm–polymorphonuclear neutrophils attachment in vitro. Anim. Reprod. Sci. 140, 164–172.
Effect of donkey seminal plasma on sperm movement and sperm–polymorphonuclear neutrophils attachment in vitro.CrossRef |

Naresh, S., and Atreja, S. K. (2015). The protein tyrosine phosphorylation during in vitro capacitation and cryopreservation of mammalian spermatozoa. Cryobiology 70, 211–216.
The protein tyrosine phosphorylation during in vitro capacitation and cryopreservation of mammalian spermatozoa.CrossRef | 1:CAS:528:DC%2BC2MXlsFemt70%3D&md5=71cd66b177c823387840de8c350f0318CAS |

Ofek, I., and Sharon, N. (1988). Lectinophagocytosis: a molecular mechanism of recognition between cell surface sugars and lectins in the phagocytosis of bacteria. Infect. Immun. 56, 539–547.
| 1:CAS:528:DyaL1cXht12lur0%3D&md5=8c1a54efa60c76cc0c55521117670ce1CAS |

O’Leary, S., Jasper, M. J., Warnes, G. M., Armstrong, D. T., and Robertson, S. A. (2004). Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction 128, 237–247.
Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig.CrossRef | 1:CAS:528:DC%2BD2cXntFeit70%3D&md5=d321a74d6bd0595d7a3d38c3e799265bCAS |

Oren-Benaroya, R., Kipnis, J., and Eisenbach, M. (2007). Phagocytosis of human post-capacitated spermatozoa by macrophages. Hum. Reprod. 22, 2947–2955.
Phagocytosis of human post-capacitated spermatozoa by macrophages.CrossRef | 1:CAS:528:DC%2BD2sXht1Shu7bI&md5=e84cd322c7e4637e1c2b05e015e698d1CAS |

Paris, L. L., Chihara, R. K., Sidner, R. A., Joseph Tector, A., and Burlak, C. (2012). Differences in human and porcine platelet oligosaccharides may influence phagocytosis by liver sinusoidal cells in vitro. Xenotransplantation 19, 31–39.
Differences in human and porcine platelet oligosaccharides may influence phagocytosis by liver sinusoidal cells in vitro.CrossRef |

Pérez, L. J., Valcárcel, A., de las Heras, M. A., Moses, D., and Baldassarre, H. (1996). Evidence that frozen/thawed ram spermatozoa show accelerated capacitation in vitro as assessed by chlortetracycline assay. Theriogenology 46, 131–140.
Evidence that frozen/thawed ram spermatozoa show accelerated capacitation in vitro as assessed by chlortetracycline assay.CrossRef |

Pfister, R. R., Haddox, J. L., Dodson, R. W., and Deshazo, W. F. (1984). Polymorphonuclear leukocytic inhibition by citrate, other metal chelators, and trifluoperazine. Evidence to support calcium binding protein involvement. Invest. Ophthalmol. Vis. Sci. 25, 955–970.
| 1:CAS:528:DyaL2cXls1eltLk%3D&md5=10ba2e99dcb140db38aa3f043fc20233CAS |

Pini, T., Leahy, T., Soleilhavoup, C., Tsikis, G., Labas, V., Combes-Soia, L., Harichaux, G., Rickard, J. P., Druart, X., and de Graaf, S. P. (2016). Proteomic investigation of ram spermatozoa and the proteins conferred by seminal plasma. J. Proteome Res. 15, 3700–3711.
Proteomic investigation of ram spermatozoa and the proteins conferred by seminal plasma.CrossRef | 1:CAS:528:DC%2BC28XhsFWmtbrE&md5=74accf04e6df63334961c61afa9ef236CAS |

Portus, B. J., Reilas, T., and Katila, T. (2005). Effect of seminal plasma on uterine inflammation, contractility and pregnancy rates in mares. Equine Vet. J. 37, 515–519.
Effect of seminal plasma on uterine inflammation, contractility and pregnancy rates in mares.CrossRef | 1:STN:280:DC%2BD2MngvFOiuw%3D%3D&md5=aab91b3e37d81f89062232bba2cffa7cCAS |

Rehm, M., Bruegger, D., Christ, F., Conzen, P., Thiel, M., Jacob, M., Chappell, D., Stoeckelhuber, M., Welsch, U., Reichart, B., Peter, K., and Becker, B. F. (2007). Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation 116, 1896–1906.
Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia.CrossRef | 1:CAS:528:DC%2BD2sXhtFKmu7fL&md5=8ec73434c31fd5c4644d0ae6e25c10d2CAS |

Rickard, J. P., Pini, T., Soleilhavoup, C., Cognie, J., Bathgate, R., Lynch, G. W., Evans, G., Maxwell, W. M. C., Druart, X., and de Graaf, S. P. (2014). Seminal plasma aids the survival and cervical transit of epididymal ram spermatozoa. Reproduction 148, 469–478.
Seminal plasma aids the survival and cervical transit of epididymal ram spermatozoa.CrossRef | 1:CAS:528:DC%2BC2cXhvFyhtr%2FJ&md5=748bf6dc6b824ad729746bbcbe3f4284CAS |

Robertson, S. A., Mau, V. J., Tremellen, K. P., and Seamark, R. F. (1996). Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J. Reprod. Fertil. 107, 265–277.
Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice.CrossRef | 1:CAS:528:DyaK28XmsFGgtrY%3D&md5=955b63afebef7c2ee6a784e726d6089bCAS |

Robertson, S. A., Ingman, W. V., O’Leary, S., Sharkey, D. J., and Tremellen, K. P. (2002). Transforming growth factor β – a mediator of immune deviation in seminal plasma. J. Reprod. Immunol. 57, 109–128.
Transforming growth factor β – a mediator of immune deviation in seminal plasma.CrossRef | 1:CAS:528:DC%2BD38XnvVOmsr8%3D&md5=05d93a659e76980cb74e17cf0a3a8dd4CAS |

Rodriguez-Martinez, H., Saravia, F., Wallgren, M., Martinez, E. A., Sanz, L., Roca, J., Vazquez, J. M., and Calvete, J. J. (2010). Spermadhesin PSP-I/PSP-II heterodimer induces migration of polymorphonuclear neutrophils into the uterine cavity of the sow. J. Reprod. Immunol. 84, 57–65.
Spermadhesin PSP-I/PSP-II heterodimer induces migration of polymorphonuclear neutrophils into the uterine cavity of the sow.CrossRef | 1:CAS:528:DC%2BC3cXkt1aqtA%3D%3D&md5=091f531959881fd1c7b2a1f28c060816CAS |

Rubio-Gayosso, I., Platts, S. H., and Duling, B. R. (2006). Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 290, H2247–H2256.
Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury.CrossRef | 1:CAS:528:DC%2BD28XlvVeksb8%3D&md5=54667f1167dde069885bf30cb2d1bd86CAS |

Santiani, A., Evangelista, S., Sepúlveda, N., Risopatrón, J., Villegas, J., and Sánchez, R. (2014). Addition of superoxide dismutase mimics during cooling process prevents oxidative stress and improves semen quality parameters in frozen/thawed ram spermatozoa. Theriogenology 82, 884–889.
Addition of superoxide dismutase mimics during cooling process prevents oxidative stress and improves semen quality parameters in frozen/thawed ram spermatozoa.CrossRef | 1:CAS:528:DC%2BC2cXhtlCjt7%2FO&md5=10c0b6f9e93e92034f2d2326b3d9a1faCAS |

Schauer, R., Shukla, A. K., Schroder, C., and Müller, E. (1984). The anti-recognition function of sialic acids: studies with erythrocytes and macrophages. Pure Appl. Chem. 56, 907–921.
The anti-recognition function of sialic acids: studies with erythrocytes and macrophages.CrossRef | 1:CAS:528:DyaL2cXlsV2mtL8%3D&md5=3cb53c90397bf15a46a1a2844bc9d246CAS |

Schembri, M. A., Major, D. A., Maxwell, W. M. C., Suttie, J. J., and Evans, G. (2002). Capacitation-like changes in equine spermatoza throughout the cryopreservation process. Reprod. Fertil. Dev. 14, 225–233.
Capacitation-like changes in equine spermatoza throughout the cryopreservation process.CrossRef | 1:STN:280:DC%2BD38vmtFajtQ%3D%3D&md5=122a0eed2d99820655c5963ec3992c50CAS |

Scott, J. L., Ketheesan, N., and Summers, P. M. (2006). Leucocyte population changes in the reproductive tract of the ewe in response to insemination. Reprod. Fertil. Dev. 18, 627–634.
Leucocyte population changes in the reproductive tract of the ewe in response to insemination.CrossRef |

Scott, J. L., Ketheesan, N., and Summers, P. M. (2009). Spermatozoa and seminal plasma induce a greater inflammatory response in the ovine uterus at oestrus than dioestrus. Reprod. Fertil. Dev. 21, 817–826.
Spermatozoa and seminal plasma induce a greater inflammatory response in the ovine uterus at oestrus than dioestrus.CrossRef | 1:CAS:528:DC%2BD1MXhtVartbfL&md5=6664caba508a819137a01464695900c1CAS |

Sharkey, D. J., Macpherson, A. M., Tremellen, K. P., and Robertson, S. A. (2007). Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells. Mol. Hum. Reprod. 13, 491–501.
Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells.CrossRef | 1:CAS:528:DC%2BD2sXotl2qurY%3D&md5=f25a90ab2fe152c906e8e9a40239881eCAS |

Sharkey, D. J., Tremellen, K. P., Jasper, M. J., Gemzell-Danielsson, K., and Robertson, S. A. (2012). Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J. Immunol. 188, 2445–2454.
Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus.CrossRef | 1:CAS:528:DC%2BC38XisVGrt7o%3D&md5=0b0fb5182b610695c45cf13d66d2d94eCAS |

Sheth, C. C., Hall, R., Lewis, L., Brown, A. J. P., Odds, F. C., Erwig, L. P., and Gow, N. A. R. (2011). Glycosylation status of the C. albicans cell wall affects the efficiency of neutrophil phagocytosis and killing but not cytokine signaling. Med. Mycol. 49, 513–524.
| 1:CAS:528:DC%2BC3MXnsFKrs74%3D&md5=295b571b390370b6cf2ee965f4ca83c0CAS |

Singh, A., Ramnath, R. D., Foster, R. R., Wylie, E. C., Fridén, V., Dasgupta, I., Haraldsson, B., Welsh, G. I., Mathieson, P. W., and Satchell, S. C. (2013). Reactive oxygen species modulate the barrier function of the human glomerular endothelial glycocalyx. PLoS One 8, e55852.
Reactive oxygen species modulate the barrier function of the human glomerular endothelial glycocalyx.CrossRef | 1:CAS:528:DC%2BC3sXjtl2qsbg%3D&md5=b54f34cc8e9f4efc0fa7dda98b2a4494CAS |

Soleilhavoup, C., Tsikis, G., Labas, V., Harichaux, G., Kohnke, P. L., Dacheux, J. L., Guerin, Y., Gatti, J. L., de Graaf, S. P., and Druart, X. (2014). Ram seminal plasma proteome and its impact on liquid preservation of spermatozoa. J. Proteomics 109, 245–260.
Ram seminal plasma proteome and its impact on liquid preservation of spermatozoa.CrossRef | 1:CAS:528:DC%2BC2cXht1OitrnL&md5=37028c495508cd972c9a675a20003c2dCAS |

Taitzoglou, I. A., Kokoli, A. N., and Killian, G. J. (2007). Modifications of surface carbohydrates on bovine spermatozoa mediated by oviductal fluid: a flow cytometric study using lectins. Int. J. Androl. 30, 108–114.
Modifications of surface carbohydrates on bovine spermatozoa mediated by oviductal fluid: a flow cytometric study using lectins.CrossRef | 1:CAS:528:DC%2BD2sXltFKktL4%3D&md5=752a2cd820224af2593bfedaf49bdd49CAS |

Tammi, R., Rönkkö, S., Agren, U. M., and Tammi, M. (1994). Distribution of hyaluronan in bull reproductive organs. J. Histochem. Cytochem. 42, 1479–1486.
Distribution of hyaluronan in bull reproductive organs.CrossRef | 1:CAS:528:DyaK2cXmvFOls70%3D&md5=c10340c808e9835f1369c63200ac8241CAS |

Taylor, U., Schuberth, H. J., Rath, D., Michelmann, H. W., Sauter-Louis, C., and Zerbe, H. (2009). Influence of inseminate components on porcine leucocyte migration in vitro and in vivo after pre- and post-ovulatory insemination. Reprod. Domest. Anim. 44, 180–188.
Influence of inseminate components on porcine leucocyte migration in vitro and in vivo after pre- and post-ovulatory insemination.CrossRef | 1:STN:280:DC%2BD1M3jsVOisA%3D%3D&md5=14bdd80338b7091ae0b39f2ff1d93754CAS |

Tecle, E., and Gagneux, P. (2015). Sugar-coated sperm: unraveling the functions of the mammalian sperm glycocalyx. Mol. Reprod. Dev. 82, 635–650.
Sugar-coated sperm: unraveling the functions of the mammalian sperm glycocalyx.CrossRef | 1:CAS:528:DC%2BC2MXps12qtbg%3D&md5=f80b76cf6dc0da252ab91a6bf25055ebCAS |

Thompson, L. A., Barratt, C. L. R., Bolton, A. E., and Cooke, I. D. (1992). The leukocytic reaction of the human uterine cervix. Am. J. Reprod. Immunol. 28, 85–89.
The leukocytic reaction of the human uterine cervix.CrossRef | 1:STN:280:DyaK3s7lvFGksw%3D%3D&md5=72c5d926eecc9fa3fa245d57522ce3d0CAS |

Tollner, T. L., Yudin, A. I., Tarantal, A. F., Treece, C. A., Overstreet, J. W., and Cherr, G. N. (2008a). Beta-defensin 126 on the surface of macaque sperm mediates attachment of sperm to oviductal epithelia. Biol. Reprod. 78, 400–412.
Beta-defensin 126 on the surface of macaque sperm mediates attachment of sperm to oviductal epithelia.CrossRef | 1:CAS:528:DC%2BD1cXisFSltb0%3D&md5=be7fdb5fb5c0079584fb4dce16229ff5CAS |

Tollner, T. L., Yudin, A. I., Treece, C. A., Overstreet, J. W., and Cherr, G. N. (2008b). Macaque sperm coating protein DEFB126 facilitates sperm penetration of cervical mucus. Hum. Reprod. 23, 2523–2534.
Macaque sperm coating protein DEFB126 facilitates sperm penetration of cervical mucus.CrossRef | 1:CAS:528:DC%2BD1cXht1Ois73E&md5=2535ffadb58dadfd781b54fbace08c0bCAS |

Tomlinson, M. J., White, A., Barratt, C. L. R., Bolton, A. E., and Cooke, I. D. (1992). The removal of morphologically abnormal sperm forms by phagocytes: a positive role for seminal leukocytes? Hum. Reprod. 7, 517–522.
The removal of morphologically abnormal sperm forms by phagocytes: a positive role for seminal leukocytes?CrossRef | 1:STN:280:DyaK38zpsFSqug%3D%3D&md5=dcf09efba0f35c9c822b7d99dfb2954cCAS |

Toshimori, K., Araki, S., Öra, C., and Eddy, E. M. (1991). Loss of sperm surface sialic acid induces phagocytosis: an assay with a monoclonal antibody T21, which recognizes a 54K sialoglycoprotein. Arch. Androl. 27, 79–86.
| 1:CAS:528:DyaK3MXmslKmurc%3D&md5=5db256dfc54fbd646c06bf609c79ecceCAS |

Toshimori, K., Araki, S., Tanii, I., and Oura, C. (1992). Masking the cryptodeterminant on the 54-kilodalton mouse sperm surface antigen. Biol. Reprod. 47, 1161–1167.
Masking the cryptodeterminant on the 54-kilodalton mouse sperm surface antigen.CrossRef | 1:CAS:528:DyaK3sXjs1erug%3D%3D&md5=919c4ea898f15d8b53787df0307234f5CAS |

Troedsson, M. H. T., Desvousges, A., Alghamdi, A. S., Dahms, B., Dow, C. A., Hayna, J., Valesco, R., Collahan, P. T., Macpherson, M. L., Pozor, M., and Buhi, W. C. (2005). Components in seminal plasma regulating sperm transport and elimination. Anim. Reprod. Sci. 89, 171–186.
Components in seminal plasma regulating sperm transport and elimination.CrossRef | 1:CAS:528:DC%2BD2MXhtVart77F&md5=1f1ba030d914800ea622271ea2973d4dCAS |

Tulsiani, D. R. P. (2006). Glycan-modifying enzymes in luminal fluid of the mammalian epididymis: an overview of their potential role in sperm maturation. Mol. Cell. Endocrinol. 250, 58–65.
Glycan-modifying enzymes in luminal fluid of the mammalian epididymis: an overview of their potential role in sperm maturation.CrossRef | 1:CAS:528:DC%2BD28XksVGjtrY%3D&md5=12fcaea41ab5c5f95fedaf170369d27fCAS |

Vega, V. L., and De Maio, A. (2005). Increase in phagocytosis after geldanamycin treatment or heat shock: role of heat shock proteins. J. Immunol. 175, 5280–5287.
Increase in phagocytosis after geldanamycin treatment or heat shock: role of heat shock proteins.CrossRef | 1:CAS:528:DC%2BD2MXhtVylsbfM&md5=83e988b0bf626aed40fb19659ac0e17bCAS |

Vink, H., Constantinescu, A. A., and Spaan, J. A. E. (2000). Oxidized lipoproteins degrade the endothelial surface layer: implications for platelet–endothelial cell adhesion. Circulation 101, 1500–1502.
Oxidized lipoproteins degrade the endothelial surface layer: implications for platelet–endothelial cell adhesion.CrossRef | 1:CAS:528:DC%2BD3cXivVyhsbo%3D&md5=81a7da013e6149cf1244cda1606f0e7aCAS |

Voglmayr, J. K., Fairbanks, G., and Lewis, R. G. (1983). Surface glycoprotein changes in ram spermatozoa during epididymal maturation. Biol. Reprod. 29, 767–775.
Surface glycoprotein changes in ram spermatozoa during epididymal maturation.CrossRef | 1:CAS:528:DyaL3sXlslelurk%3D&md5=f2364a90a9a0614116060e72d3713697CAS |

Westfalewicz, B., Dietrich, M. A., and Ciereszko, A. (2015). Impact of cryopreservation on bull (Bos taurus) semen proteome. J. Anim. Sci. 93, 5240–5253.
Impact of cryopreservation on bull (Bos taurus) semen proteome.CrossRef | 1:CAS:528:DC%2BC28XktlOgtr8%3D&md5=13187c353bb586520d01ce2d36c81bb4CAS |

Xin, A.-J., Cheng, L., Diao, H., Wang, P., Gu, Y.-H., Wu, B., Wu, Y.-C., Chen, G.-W., Zhou, S.-M., Guo, S.-J., Shi, H.-J., and Tao, S.-C. (2014). Comprehensive profiling of accessible surface glycans of mammalian sperm using a lectin microarray. Clin. Proteomics 11, 10.
Comprehensive profiling of accessible surface glycans of mammalian sperm using a lectin microarray.CrossRef |

Yeste, M. (2016). Sperm cryopreservation update: cryodamage, markers, and factors affecting the sperm freezability in pigs. Theriogenology 85, 47–64.
Sperm cryopreservation update: cryodamage, markers, and factors affecting the sperm freezability in pigs.CrossRef | 1:CAS:528:DC%2BC2MXhslSjsb%2FN&md5=1347619d07f97ac293b6bf0f14c03230CAS |

Yudin, A. I., Treece, C. A., Tollner, T. L., Overstreet, J. W., and Cherr, G. N. (2005). The carbohydrate structure of DEFB126, the major component of the cynomolgus macaque sperm plasma membrane glycocalyx. J. Membr. Biol. 207, 119–129.
The carbohydrate structure of DEFB126, the major component of the cynomolgus macaque sperm plasma membrane glycocalyx.CrossRef | 1:CAS:528:DC%2BD28XislWksbg%3D&md5=0eb18c1c197cee872f7be2245903d5c7CAS |



Export Citation

View Altmetrics