Recombinant β-defensin 126 promotes bull sperm binding to bovine oviductal epithelia
A. Lyons A , F. Narciandi B , E. Donnellan A , J. Romero-Aguirregomezcorta A , C. O’ Farrelly B , P. Lonergan C , K. G. Meade D and S. Fair A E
+ Author Affiliations
- Author Affiliations
A Laboratory of Animal Reproduction, Department of Biological Sciences, School of Natural Sciences, Faculty of Science and Engineering, University of Limerick, Limerick, V94 T9PX,Ireland.
B Trinity Biomedical Sciences Institute, Trinity College, Dublin 2, Dublin, D02 R590, Ireland.
C School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Dublin, D04 N2E5, Ireland.
D Animal & Bioscience Research Department, Animal & Grassland Research and Innovation Centre, Teagasc, Grange, Meath, C15 PW93, Ireland.
E Corresponding author. Email: sean.fair@ul.ie
Reproduction, Fertility and Development 30(11) 1472-1481 https://doi.org/10.1071/RD17415
Submitted: 9 October 2017 Accepted: 12 April 2018 Published: 18 May 2018
Abstract
Primate β-defensin 126 regulates the ability of spermatozoa to bind to oviductal epithelial cells in vitro. Bovine β-defensin 126 (BBD126) exhibits preferential expression in the cauda epididymis of the bull, but there have been few studies on its functional role in cattle. The aim of the present study was to examine the role of BBD126 in bull sperm binding to bovine oviductal epithelial cell (BOEC) explants. BBD126 has been shown to be highly resistant to the standard methods of dissociation used in other species and, as a result, corpus epididymal spermatozoa, which have not been exposed to the protein, were used to study the functional role of BBD126. Corpus epididymal spermatozoa were incubated with recombinant (r) BBD126 in the absence or presence of anti-BBD126 antibody. Addition of rBBD126 significantly enhanced the ability of epididymal spermatozoa to bind to BOEC explants (P < 0.05). Anti-BBD126 antibody blocked the BBD126-mediated increase in sperm binding capacity. Ejaculated spermatozoa, which are coated with native BBD126 protein but also a large number of seminal plasma proteins in vivo, were incubated with rBBD126 in the absence or presence of the anti-BBD126 antibody. Addition of rBBD126 significantly enhanced the ability of ejaculated spermatozoa to bind to BOEC explants (P < 0.05), whereas rBBD126 also reduced corpus sperm agglutination (P < 0.05). These results suggest that, similar to the role of its analogue in the macaque, spermatozoa with more BBD126 in their acrosome may represent spermatozoa with more oviduct binding capacity.
Additional keyword: oviduct.
References
Al Naib, A., Hanrahan, J. P., Lonergan, P., and Fair, S. (2011). In vitro assessment of sperm from bulls of high and low field fertility. Theriogenology 76, 161–167.| In vitro assessment of sperm from bulls of high and low field fertility.Crossref | GoogleScholarGoogle Scholar |
Boilard, M., Reyes-Moreno, C., Lachance, C., Massicotte, L., Bailey, J. L., Sirard, M. A., and Leclerc, P. (2004). Localization of the chaperone proteins GRP78 and HSP60 on the luminal surface of bovine oviduct epithelial cells and their association with spermatozoa. Biol. Reprod. 71, 1879–1889.
| Localization of the chaperone proteins GRP78 and HSP60 on the luminal surface of bovine oviduct epithelial cells and their association with spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Cornwall, G. A. (2014). Role of posttranslational protein modifications in epididymal sperm maturation and extracellular quality control. Adv. Exp. Med. Biol. 759, 159–180.
| Role of posttranslational protein modifications in epididymal sperm maturation and extracellular quality control.Crossref | GoogleScholarGoogle Scholar |
Coy, P., García-Vázquez, F. A., Visconti, P. E., and Avilés, M. (2012). Roles of the oviduct in mammalian fertilization. Reproduction 144, 649–660.
| Roles of the oviduct in mammalian fertilization.Crossref | GoogleScholarGoogle Scholar |
Dacheux, J. L., Paquignon, M., and Combarnous, Y. (1983). Head-to-head agglutination of ram and boar epididymal spermatozoa and evidence for an epididymal antagglutinin. J. Reprod. Fertil. 67, 181–189.
| Head-to-head agglutination of ram and boar epididymal spermatozoa and evidence for an epididymal antagglutinin.Crossref | GoogleScholarGoogle Scholar |
DeMott, R. P., Lefebvre, R., and Suarez, S. S. (1995). Carbohydrates mediate the adherence of hamster sperm to oviductal epithelium. Biol. Reprod. 52, 1395–1403.
| Carbohydrates mediate the adherence of hamster sperm to oviductal epithelium.Crossref | GoogleScholarGoogle Scholar |
Dorin, J. R., and Barratt, C. L. (2014). Importance of β-defensins in sperm function. Mol. Hum. Reprod. 20, 821–826.
| Importance of β-defensins in sperm function.Crossref | GoogleScholarGoogle Scholar |
Druart, X., Gatti, J. L., Huet, S., Dacheux, J. L., and Humblot, P. (2009). Hypotonic resistance of boar spermatozoa: sperm subpopulations and relationship with epididymal maturation and fertility. Reproduction 137, 205–213.
| Hypotonic resistance of boar spermatozoa: sperm subpopulations and relationship with epididymal maturation and fertility.Crossref | GoogleScholarGoogle Scholar |
Fernandez-Fuertes, B., Narciandi, F., O’ Farrelly, C., Meade, K. G., Fair, S., and Lonergan, P. (2016). Cauda epididymis-specific beta-defensin 126 promotes sperm motility but not fertilizing ability in cattle. Biol. Reprod. 95, 122.
| Cauda epididymis-specific beta-defensin 126 promotes sperm motility but not fertilizing ability in cattle.Crossref | GoogleScholarGoogle Scholar |
Girouard, J., Frenette, G., and Sullivan, R. (2011). Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. Int. J. Androl. 34, e475–e486.
| Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis.Crossref | GoogleScholarGoogle Scholar |
Gualtieri, R., Mollo, V., Barbato, V., and Talevi, R. (2010). Ability of sulfated glycoconjugates and disulfide-reductants to release bovine epididymal sperm bound to the oviductal epithelium in vitro. Theriogenology 73, 1037–1043.
| Ability of sulfated glycoconjugates and disulfide-reductants to release bovine epididymal sperm bound to the oviductal epithelium in vitro.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Gwathmey, T. M., Ignotz, G. G., Mueller, J. L., Manjunath, P., and Suarez, S. S. (2006). Bovine seminal plasma proteins PDC-109, BSP-A3, and BSP-30-kDa share functional roles in storing sperm in the oviduct. Biol. Reprod. 75, 501–507.
| Bovine seminal plasma proteins PDC-109, BSP-A3, and BSP-30-kDa share functional roles in storing sperm in the oviduct.Crossref | GoogleScholarGoogle Scholar |
Hall, T. J., McQuillan, C., Finlay, E. K., O’Farrelly, C., Fair, S., and Meade, K. G. (2017). Comparative genomic identification and validation of β-defensin genes in the Ovis aries genome. BMC Genomics 18, 278.
| Comparative genomic identification and validation of β-defensin genes in the Ovis aries genome.Crossref | GoogleScholarGoogle Scholar |
Holden, S. A., Fernandez-Fuertes, B., Murphy, C., Whelan, H., O’Gorman, A., Brennan, L., Butler, S. T., Lonergan, P., and Fair, S. (2017). Relationship between in vitro sperm functional assessments, seminal plasma composition, and field fertility after AI with either non-sorted or sex-sorted bull semen. Theriogenology 87, 221–228.
| Relationship between in vitro sperm functional assessments, seminal plasma composition, and field fertility after AI with either non-sorted or sex-sorted bull semen.Crossref | GoogleScholarGoogle Scholar |
Holt, W. V., and Fazeli, A. (2010). The oviduct as a complex mediator of mammalian sperm function and selection. Mol. Reprod. Dev. 77, 934–943.
| The oviduct as a complex mediator of mammalian sperm function and selection.Crossref | GoogleScholarGoogle Scholar |
Holt, W. V., and Fazeli, A. (2015). Do sperm possess a molecular passport? Mechanistic insights into sperm selection in the female reproductive tract. MHR: Basic Science of Reproductive Medicine 21, 491–501.
Hunter, R. H. (2008). Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory graafian follicles. Mol. Reprod. Dev. 75, 167–174.
| Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory graafian follicles.Crossref | GoogleScholarGoogle Scholar |
Hunter, R. H. F. (2012). Components of oviduct physiology in eutherian mammals. Biol. Rev. Camb. Philos. Soc. 87, 244–255.
| Components of oviduct physiology in eutherian mammals.Crossref | GoogleScholarGoogle Scholar |
Hunter, R. H., Flechon, B., and Flechon, J. E. (1991). Distribution, morphology and epithelial interactions of bovine spermatozoa in the oviduct before and after ovulation: a scanning electron microscope study. Tissue Cell 23, 641–656.
| Distribution, morphology and epithelial interactions of bovine spermatozoa in the oviduct before and after ovulation: a scanning electron microscope study.Crossref | GoogleScholarGoogle Scholar |
Ignotz, G. G., Cho, M. Y., and Suarez, S. S. (2007). Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir. Biol. Reprod. 77, 906–913.
| Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir.Crossref | GoogleScholarGoogle Scholar |
Johnson, G. P., Lloyd, A. T., O’Farrelly, C., Meade, K. G., and Fair, S. (2015). Comparative genomic identification and expression profiling of a novel β-defensin gene cluster in the equine reproductive tract. Reprod. Fertil. Dev. 28, 1499–1508.
| Comparative genomic identification and expression profiling of a novel β-defensin gene cluster in the equine reproductive tract.Crossref | GoogleScholarGoogle Scholar |
Kiernan, M., Fahey, A. G., and Fair, S. (2013). The effect of the in vitro supplementation of exogenous long-chain fatty acids on bovine sperm cell function. Reprod. Fertil. Dev. 25, 947–954.
| The effect of the in vitro supplementation of exogenous long-chain fatty acids on bovine sperm cell function.Crossref | GoogleScholarGoogle Scholar |
Lefebvre, R., Chenoweth, P. J., Drost, M., LeClear, C. T., MacCubbin, M., Dutton, J. T., and Suarez, S. S. (1995). Characterization of the oviductal sperm reservoir in cattle. Biol. Reprod. 53, 1066–1074.
| Characterization of the oviductal sperm reservoir in cattle.Crossref | GoogleScholarGoogle Scholar |
Lefebvre, R., Lo, M. C., and Suarez, S. S. (1997). Bovine sperm binding to oviductal epithelium involves fucose recognition. Biol. Reprod. 56, 1198–1204.
| Bovine sperm binding to oviductal epithelium involves fucose recognition.Crossref | GoogleScholarGoogle Scholar |
Légaré, C., Akintayo, A., Blondin, P., Calvo, E., and Sullivan, R. (2017). Impact of male fertility status on the transcriptome of the bovine epididymis. Mol. Hum. Reprod. 23, 355–369.
| Impact of male fertility status on the transcriptome of the bovine epididymis.Crossref | GoogleScholarGoogle Scholar |
Lodish, H., Berk, A., Matsudaira, P., Kaiser, C., and Krieger, M. (2008). Molecular cell biology. In ‘Biologia celular Y molecular’. (6th edn) pp. 924–930. (WH Freeman: New York)
Meade, K. G., Cormican, P., Narciandi, F., Lloyd, A., and O’Farrelly, C. (2014). Bovine β-defensin gene family: opportunities to improve animal health? Physiol. Genomics 46, 17–28.
| Bovine β-defensin gene family: opportunities to improve animal health?Crossref | GoogleScholarGoogle Scholar |
Miller, D. J. (2015). Regulation of sperm function by oviduct fluid and the epithelium: insight into the role of glycans. Reprod. Domest. Anim. 50, 31–39.
| Regulation of sperm function by oviduct fluid and the epithelium: insight into the role of glycans.Crossref | GoogleScholarGoogle Scholar |
Nagdas, S. K., McLean, E. L., Richardson, L. P., and Raychoudhury, S. (2014). Identification and characterization of TEX101 in bovine epididymal spermatozoa. Biochem. Res. Int. 2014, 573293.
Narciandi, F., Lloyd, A. T., Chapwanya, A., O’Farrelly, C., and Meade, K. G. (2011). Reproductive tissue-specific expression profiling and genetic variation across a 19 gene bovine β-defensin cluster. Immunogenetics 63, 641–651.
| Reproductive tissue-specific expression profiling and genetic variation across a 19 gene bovine β-defensin cluster.Crossref | GoogleScholarGoogle Scholar |
Narciandi, F., Fernandez-Fuertes, B., Fair, S., Lonergan, P., Jahns, H., King, D., Mok, K., Finlay, E., O’ Farrelly, C., and Meade, K. G. (2016). Sperm-coating beta-defensin 126 is a dissociation-resistant dimer produced by epididymal epithelium in the bovine reproductive tract. Biol. Reprod. 95, 121.
| Sperm-coating beta-defensin 126 is a dissociation-resistant dimer produced by epididymal epithelium in the bovine reproductive tract.Crossref | GoogleScholarGoogle Scholar |
Nauc, V., and Manjunath, P. (2000). Radioimmunoassays for bull seminal plasma proteins (BSP-A1/-A2, BSP-A3, and BSP-30-kilodaltons), and their quantification in seminal plasma and sperm. Biol. Reprod. 63, 1058–1066.
| Radioimmunoassays for bull seminal plasma proteins (BSP-A1/-A2, BSP-A3, and BSP-30-kilodaltons), and their quantification in seminal plasma and sperm.Crossref | GoogleScholarGoogle Scholar |
Netzel-Arnett, S., Bugge, T. H., Hess, R. A., Carnes, K., Stringer, B. W., Scarman, A. L., Hooper, J. D., Tonks, I. D., Kay, G. F., and Antalis, T. M. (2009). The glycosylphosphatidylinositol-anchored serine protease PRSS21 (testisin) imparts murine epididymal sperm cell maturation and fertilizing ability. Biol. Reprod. 81, 921–932.
| The glycosylphosphatidylinositol-anchored serine protease PRSS21 (testisin) imparts murine epididymal sperm cell maturation and fertilizing ability.Crossref | GoogleScholarGoogle Scholar |
Osycka-Salut, C. E., Castellano, L., Fornes, D., Beltrame, J. S., Alonso, C. A. I., Jawerbaum, A., Franchi, A., Diaz, E. S., and Perez Martinez, S. (2017). Fibronectin from oviductal cells fluctuates during the estrous cycle and contributes to sperm–oviduct interaction in cattle. J. Cell. Biochem. 118, 4095–4108.
| Fibronectin from oviductal cells fluctuates during the estrous cycle and contributes to sperm–oviduct interaction in cattle.Crossref | GoogleScholarGoogle Scholar |
Peyrin-Biroulet, L., Beisner, J., Wang, G., Nuding, S., Oommen, S. T., Kelly, D., Parmentier-Decrucq, E., Dessein, R., Merour, E., Chavatte, P., Grandjean, T., Bressenot, A., Desreumaux, P., Colombel, J. F., Desvergne, B., Stange, E. F., Wehkamp, J., and Chamaillard, M. (2010). Peroxisome proliferator-activated receptor gamma activation is required for maintenance of innate antimicrobial immunity in the colon. Proc. Natl Acad. Sci. USA 107, 8772–8777.
| Peroxisome proliferator-activated receptor gamma activation is required for maintenance of innate antimicrobial immunity in the colon.Crossref | GoogleScholarGoogle Scholar |
Sass, V., Schneider, T., Wilmes, M., Korner, C., Tossi, A., Novikova, N., Shamova, O., and Sahl, H. G. (2010). Human β-defensin 3 inhibits cell wall biosynthesis in staphylococci. Infect. Immun. 78, 2793–2800.
| Human β-defensin 3 inhibits cell wall biosynthesis in staphylococci.Crossref | GoogleScholarGoogle Scholar |
Schröter, S., Osterhoff, C., McArdle, W., and Ivell, R. (1999). The glycocalyx of the sperm surface. Hum. Reprod. Update 5, 302–313.
| The glycocalyx of the sperm surface.Crossref | GoogleScholarGoogle Scholar |
Semple, F., MacPherson, H., Webb, S., Kilanowski, F., Lettice, L., McGlasson, S. L., Wheeler, A. P., Chen, V., Millhauser, G. L., Melrose, L., Davidson, D. J., and Dorin, J. R. (2015). Human β-D-3 exacerbates MDA5 but suppresses TLR3 responses to the viral molecular pattern mimic polyinosinic : polycytidylic acid. PLoS Genet. 11, e1005673.
| Human β-D-3 exacerbates MDA5 but suppresses TLR3 responses to the viral molecular pattern mimic polyinosinic : polycytidylic acid.Crossref | GoogleScholarGoogle Scholar |
Sinowatz, F., Friess, A. E., and Wrobel, K. H. (1984). Glycoproteins of bovine epididymal spermatozoa – a cytochemical study. Acta Histochem. Suppl. 29, 113–120.
Srivastav, A., Singh, B., Chandra, A., Jamal, F., Khan, M. Y., and Chowdhury, S. R. (2004). Partial characterization, sperm association and significance of N- and O-linked glycoproteins in epididymal fluid of rhesus monkeys (Macaca mulatta). Reproduction 127, 343–357.
| Partial characterization, sperm association and significance of N- and O-linked glycoproteins in epididymal fluid of rhesus monkeys (Macaca mulatta).Crossref | GoogleScholarGoogle Scholar |
Suarez, S. S. (2001). Carbohydrate-mediated formation of the oviductal sperm reservoir in mammals. Cells Tissues Organs 168, 105–112.
| Carbohydrate-mediated formation of the oviductal sperm reservoir in mammals.Crossref | GoogleScholarGoogle Scholar |
Suarez, S. S. (2002). Formation of a reservoir of sperm in the oviduct. Reprod. Domest. Anim. 37, 140–143.
| Formation of a reservoir of sperm in the oviduct.Crossref | GoogleScholarGoogle Scholar |
Suarez, S. S. (2016). Mammalian sperm interactions with the female reproductive tract. Cell Tissue Res. 363, 185–194.
| Mammalian sperm interactions with the female reproductive tract.Crossref | GoogleScholarGoogle Scholar |
Suarez, S. S., and Pacey, A. A. (2006). Sperm transport in the female reproductive tract. Hum. Reprod. Update 12, 23–37.
| Sperm transport in the female reproductive tract.Crossref | GoogleScholarGoogle Scholar |
Teijeiro, J. M., Dapino, D. G., and Marini, P. E. (2011). Porcine oviduct sperm binding glycoprotein and its deleterious effect on sperm: a mechanism for negative selection of sperm? Biol. Res. 44, 329–337.
| Porcine oviduct sperm binding glycoprotein and its deleterious effect on sperm: a mechanism for negative selection of sperm?Crossref | GoogleScholarGoogle Scholar |
Thys, M., Nauwynck, H., Maes, D., Hoogewijs, M., Vercauteren, D., Rijsselaere, T., Favoreel, H., and Van Soom, A. (2009). Expression and putative function of fibronectin and its receptor (integrin α5β1) in male and female gametes during bovine fertilization in vitro. Reproduction 138, 471–482.
| Expression and putative function of fibronectin and its receptor (integrin α5β1) in male and female gametes during bovine fertilization in vitro.Crossref | GoogleScholarGoogle Scholar |
Tollner, T. L., Yudin, A. I., Treece, C. A., Overstreet, J. W., and Cherr, G. N. (2004). Macaque sperm release ESP13.2 and PSP94 during capacitation: the absence of ESP13.2 is linked to sperm–zona recognition and binding. Mol. Reprod. Dev. 69, 325–337.
| Macaque sperm release ESP13.2 and PSP94 during capacitation: the absence of ESP13.2 is linked to sperm–zona recognition and binding.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Tollner, T. L., Venners, S. A., Hollox, E. J., Yudin, A. I., Liu, X., Tang, G., Xing, H., Kays, R. J., Lau, T., Overstreet, J. W., Xu, X., Bevins, C. L., and Cherr, G. N. (2011). A common mutation in the defensin DEFB126 causes impaired sperm function and subfertility. Sci. Transl. Med. 3, 92ra65.
| A common mutation in the defensin DEFB126 causes impaired sperm function and subfertility.Crossref | GoogleScholarGoogle Scholar |
Tollner, T. L., Bevins, C. L., and Cherr, G. N. (2012). Multifunctional glycoprotein DEFB126 – a curious story of defensin-clad spermatozoa. Nat. Rev. Urol. 9, 365–375.
| Multifunctional glycoprotein DEFB126 – a curious story of defensin-clad spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Wagner, A., Ekhlasi-Hundrieser, M., Hettel, C., Petrunkina, A., Waberski, D., Nimtz, M., and Topfer-Petersen, E. (2002). Carbohydrate-based interactions of oviductal sperm reservoir formation – studies in the pig. Mol. Reprod. Dev. 61, 249–257.
| Carbohydrate-based interactions of oviductal sperm reservoir formation – studies in the pig.Crossref | GoogleScholarGoogle Scholar |
Walter, I. (1995). Culture of bovine oviduct epithelial cells (BOEC). Anat. Rec. 243, 347–356.
| Culture of bovine oviduct epithelial cells (BOEC).Crossref | GoogleScholarGoogle Scholar |
Whiston, R., Finlay, E. K., McCabe, M. S., Cormican, P., Flynn, P., Cromie, A., Hansen, P. J., Lyons, A., Fair, S., Lonergan, P., O’Farrelly, C., and Meade, K. G. (2017). A dual targeted β-defensin and exome sequencing approach to identify, validate and functionally characterise genes associated with bull fertility. Sci. Rep. 7, 12287.
| A dual targeted β-defensin and exome sequencing approach to identify, validate and functionally characterise genes associated with bull fertility.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Yudin, A. I., Tollner, T. L., Treece, C. A., Kays, R., Cherr, G. N., Overstreet, J. W., and Bevins, C. L. (2008). β-Defensin 22 is a major component of the mouse sperm glycocalyx. Reproduction 136, 753–765.
| β-Defensin 22 is a major component of the mouse sperm glycocalyx.Crossref | GoogleScholarGoogle Scholar |
Zhou, C. X., Zhang, Y. L., Xiao, L., Zheng, M., Leung, K. M., Chan, M. Y., Lo, P. S., Tsang, L. L., Wong, H. Y., Ho, L. S., Chung, Y. W., and Chan, H. C. (2004). An epididymis-specific β-defensin is important for the initiation of sperm maturation. Nat. Cell Biol. 6, 458–464.
| An epididymis-specific β-defensin is important for the initiation of sperm maturation.Crossref | GoogleScholarGoogle Scholar |
