Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Aquaporin 11 is related to cryotolerance and fertilising ability of frozen–thawed bull spermatozoa

Roser Morató A E , Noelia Prieto-Martínez A , Rodrigo Muiño B , Carlos O. Hidalgo C , Joan E. Rodríguez-Gil D , Sergi Bonet A and Marc Yeste A E
+ Author Affiliations
- Author Affiliations

A Department of Biology, Institute of Food and Agricultural Technology, University of Girona, C/Maria Aurèlia Campany 69, Campus Montilivi, E-17071 Girona, Spain.

B Department of Animal Pathology, Avda. Carballo Calero s/n, University of Santiago de Compostela, E-15705 Lugo, Spain.

C Department of Animal Selection and Reproduction, The Regional Agri-Food Research and Development Service of Asturias (SERIDA), Camino de Rioseco 1225, La Olla, Deva, E-33394 Gijón, Spain.

D Department of Animal Medicine and Surgery, Autonomous University of Barcelona, Building V, Campus Bellaterra s/n, E-08193 Bellaterra (Barcelona), Spain.

E Corresponding authors. Email: rmoratomolet@gmail.com; marc.yeste@udg.edu

Reproduction, Fertility and Development 30(8) 1099-1108 https://doi.org/10.1071/RD17340
Submitted: 28 August 2017  Accepted: 20 December 2017   Published: 25 January 2018

Abstract

Aquaporins (AQPs) are channel proteins involved in the transport of water and solutes across biological membranes. In the present study we identified and localised aquaporin 11 (AQP11) in bull spermatozoa and investigated the relationship between the relative AQP11 content, sperm cryotolerance and the fertilising ability of frozen–thawed semen. Bull ejaculates were classified into two groups of good and poor freezability and assessed through immunofluorescence and immunoblotting analyses before and after cryopreservation. AQP11 was localised throughout the entire tail and along the sperm head. These findings were confirmed through immunoblotting, which showed a specific band of approximately 50 kDa corresponding to AQP11. The relative amount of AQP11 was significantly (P < 0.05) higher in both fresh and frozen–thawed spermatozoa from bull ejaculates with good freezability compared with those with poorer freezability. In addition, in vitro oocyte penetration rates and non-return rates 56 days after AI were correlated with the relative AQP11 content in fresh spermatozoa. In conclusion, AQP11 is present in the head and tail of bull spermatozoa and its relative amount in fresh and frozen–thawed spermatozoa is related to the resilience of the spermatozoa to withstand cryopreservation and the fertilising ability of frozen–thawed spermatozoa. Further research is needed to elucidate the actual role of sperm AQP11 in bovine fertility.

Additional keywords: AI, AQP11, cryopreservation, IVF.


References

Agre, P., King, L. S., Yasui, M., Guggino, W. B., Ottersen, O. P., Fujiyoshi, Y., Engel, A., and Nielsen, S. (2002). Aquaporin water channels – from atomic structure to clinical medicine. J. Physiol. 542, 3–16.
Aquaporin water channels – from atomic structure to clinical medicine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtVamu7w%3D&md5=4eedfffbbb9566e0c096a83ed30d5d38CAS |

Alves, M. G., Sá, R., Jesus, T. T., Sousa, M., and Oliveira, P. F. (2015). CFTR regulation of aquaporin-mediated water transport: a target in male fertility. Curr. Drug Targets 16, 993–106.
CFTR regulation of aquaporin-mediated water transport: a target in male fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFagu77J&md5=d02d2a57c47b3ee3b6a285b0b162cc9bCAS |

Boj, M., Chauvigné, F., and Cerdà, J. (2015). Aquaporin biology of spermatogenesis and sperm physiology in mammals and teleosts. Biol. Bull. 229, 93–108.
Aquaporin biology of spermatogenesis and sperm physiology in mammals and teleosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XnsFKlu70%3D&md5=566a9e6739e5070a237aa4dac30c695cCAS |

Bonilla-Correal, S., Noto, F., Garcia-Bonavila, E., Rodríguez-Gil, J. E., Yeste, M., and Miró, J. (2017). First evidence for the presence of aquaporins in stallion sperm. Reprod. Domest. Anim. 52, 61–64.
First evidence for the presence of aquaporins in stallion sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhslSksLzJ&md5=9765d8546d5c78424bc155731bbf0bf9CAS |

Filho, A. C., Brezinsky, R. M., Youngblood, R. C., Da Silva, L. D., Willard, S. T., Ryan, P. L., and Feugang, J. M. (2014). Differential expression of aquaporins and spermadhesins in frozen–thawed ‘good freezer’ and ‘poor freezer’ boar spermatozoa. Reprod. Fertil. Dev. 26, 141–142.
Differential expression of aquaporins and spermadhesins in frozen–thawed ‘good freezer’ and ‘poor freezer’ boar spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Gorelick, D. A., Praetorius, J., Tsunenari, T., Nielsen, S., and Agre, P. (2006). Aquaporin-11: a channel protein lacking apparent transport function expressed in brain. BMC Biochem. 7, 14.
Aquaporin-11: a channel protein lacking apparent transport function expressed in brain.Crossref | GoogleScholarGoogle Scholar |

Huang, H. F., He, R. H., Sun, C. C., Zhang, Y., Meng, Q. X., and Ma, Y. Y. (2006). Function of aquaporins in female and male reproductive systems. Hum. Reprod. Update 12, 785–795.
Function of aquaporins in female and male reproductive systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFeisbzL&md5=0ccbc7cd178e0c24c3a2fb06ad92925eCAS |

Ishibashi, K., Tanaka, Y., and Morishita, Y. (2014). The role of mammalian superaquaporins inside the cell. Biochim. Biophys. Acta 1840, 1507–1512.
The role of mammalian superaquaporins inside the cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsl2hu7jF&md5=bedcf0b80267d1d2ae82b8fdafe05dfdCAS |

Klein, C., Troedsson, M., and Rutllant, J. (2013). Region-specific expression of aquaporin subtypes in equine testis, epididymis and ductus deferens. Anat. Rec. (Hoboken) 296, 1115–1126.
Region-specific expression of aquaporin subtypes in equine testis, epididymis and ductus deferens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpslCgtbs%3D&md5=01217f107d4a7e7f5bba6c433c0e81daCAS |

Loo, D. D., Wright, E. M., and Zeuthen, T. (2002). Water pumps. J. Physiol. 542, 53–60.
Water pumps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtVamu7k%3D&md5=04f0b56919f79873195ff6bbc04d05b3CAS |

Madeira, A., Fernández-Veledo, S., Camps, M., Zorzano, A., Moura, T. F., Ceperuelo-Mallafré, V., Vendrell, J., and Soveral, G. (2014). Human aquaporin-11 is a water and glycerol channel and localizes in the vicinity of lipid droplets in human adipocytes. Obesity (Silver Spring) 22, 2010–2017.
Human aquaporin-11 is a water and glycerol channel and localizes in the vicinity of lipid droplets in human adipocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVOitLzN&md5=815af46ce5b3d45927f53ac8f6a72d77CAS |

Madeira, A., Moura, T. F., and Soveral, G. (2015). Aquaglyceroporins: implications in adipose biology and obesity. Cell. Mol. Life Sci. 72, 759–771.
Aquaglyceroporins: implications in adipose biology and obesity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVOntL3F&md5=7e153e21588c60b2e906b92fe6756095CAS |

Muiño, R., Tamargo, C., Hidalgo, C. O., and Peña, A. I. (2008). Identification of sperm subpopulations with defined motility characteristics in ejaculates from Holstein bulls: effects of cryopreservation and between-bull variation. Anim. Reprod. Sci. 109, 27–39.
Identification of sperm subpopulations with defined motility characteristics in ejaculates from Holstein bulls: effects of cryopreservation and between-bull variation.Crossref | GoogleScholarGoogle Scholar |

Petrunkina, A. M., Waberski, D., Bollwein, H., and Sieme, H. (2010). Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach. Theriogenology 73, 995–1000.
Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3gsVejtQ%3D%3D&md5=b304fcac21cf2aca6eedbd96077a3d3dCAS |

Prieto-Martínez, N., Vilagran, I., Morató, R., Rodríguez-Gil, J. E., Yeste, M., and Bonet, S. (2016). Aquaporins 7 and 11 in boar spermatozoa: detection, localisation and relationship with sperm quality. Reprod. Fertil. Dev. 28, 663–672.
Aquaporins 7 and 11 in boar spermatozoa: detection, localisation and relationship with sperm quality.Crossref | GoogleScholarGoogle Scholar |

Prieto-Martínez, N., Morató, R., Vilagran, I., Rodríguez-Gil, J. E., Bonet, S., and Yeste, M. (2017a). Aquaporins in boar spermatozoa. Part II: detection and localisation of aquaglyceroporin 3. Reprod. Fertil. Dev. 29, 703–711.
Aquaporins in boar spermatozoa. Part II: detection and localisation of aquaglyceroporin 3.Crossref | GoogleScholarGoogle Scholar |

Prieto-Martínez, N., Morató, R., Muiño, R., Hidalgo, C. O., Rodríguez-Gil, J. E., Bonet, S., and Yeste, M. (2017b). Aquaglyceroporins 3 and 7 in bull sperm: identification, localisation and their relationship with sperm cryotolerance. Reprod. Fertil. Dev. 29, 1249–1259.
Aquaglyceroporins 3 and 7 in bull sperm: identification, localisation and their relationship with sperm cryotolerance.Crossref | GoogleScholarGoogle Scholar |

Prieto-Martínez, N., Vilagran, I., Morató, R., Rivera del Álamo, M. M., Rodríguez-Gil, J. E., Bonet, S., and Yeste, M. (2017c). Relationship of aquaporins 3 (AQP3), 7 (AQP7), and 11 (AQP11) with boar sperm resilience to withstand freeze–thawing procedures. Andrology 5, 1153–1164.
Relationship of aquaporins 3 (AQP3), 7 (AQP7), and 11 (AQP11) with boar sperm resilience to withstand freeze–thawing procedures.Crossref | GoogleScholarGoogle Scholar |

Rato, L., Socorro, S., Cavaco, J. E., and Oliveira, P. F. (2010). Tubular fluid secretion in the seminiferous epithelium: ion transporters and aquaporins in Sertoli cells. J. Membr. Biol. 236, 215–224.
Tubular fluid secretion in the seminiferous epithelium: ion transporters and aquaporins in Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKhtbnF&md5=4ea1576c8fd76c4f60a15834de1ecb63CAS |

Rizos, D., Ward, F., Boland, M. P., and Lonergan, P. (2001). Effect of culture system on the yield and quality of bovine blastocysts as assessed by survival after vitrification. Theriogenology 56, 1–16.
Effect of culture system on the yield and quality of bovine blastocysts as assessed by survival after vitrification.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvhvV2qtg%3D%3D&md5=6c06936b877baffe403418714408285bCAS |

Shannonhouse, J. L., Urbanski, H. F., Woo, S. L., Fong, L. A., Goddard, S. D., Lucas, W. F., Jones, E. R., Wu, C., and Morgan, C. (2014). Aquaporin-11 control of testicular fertility markers in Syrian hamsters. Mol. Cell. Endocrinol. 391, 1–9.
Aquaporin-11 control of testicular fertility markers in Syrian hamsters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXoslCru78%3D&md5=caabff49a217b7748d59f7d826888f22CAS |

Utt, M. D. (2016). Prediction of bull fertility. Anim. Reprod. Sci. 169, 37–44.
Prediction of bull fertility.Crossref | GoogleScholarGoogle Scholar |

Vicente-Carrillo, A., Ekwall, H., Álvarez-Rodríguez, M., and Rodríguez-Martínez, H. (2016). Membrane stress during thawing elicits redistribution of aquaporin 7 but not of aquaporin 9 in boar spermatozoa. Reprod. Domest. Anim. 51, 665–679.
Membrane stress during thawing elicits redistribution of aquaporin 7 but not of aquaporin 9 in boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVylt7jE&md5=85f2c31b6c6f242f95826f81f814693dCAS |

Vilagran, I., Castillo, J., Bonet, S., Sancho, S., Yeste, M., Estanyol, J. M., and Oliva, R. (2013). Acrosin-binding protein (ACRBP) and triosephosphate isomerase (TPI) are good markers to predict boar sperm freezing capacity. Theriogenology 80, 443–450.
Acrosin-binding protein (ACRBP) and triosephosphate isomerase (TPI) are good markers to predict boar sperm freezing capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpsV2rurg%3D&md5=95001d01dd9724fd072587461614774aCAS |

Vilagran, I., Yeste, M., Sancho, S., Casas, I., Rivera del Álamo, M. M., and Bonet, S. (2014). The amounts of small heat-shock protein 10 (ODF1/HSPB10) and voltage-dependent anion channel 2 (VDAC2) and their relationship with boar ejaculate freezability. Theriogenology 82, 418–426.
The amounts of small heat-shock protein 10 (ODF1/HSPB10) and voltage-dependent anion channel 2 (VDAC2) and their relationship with boar ejaculate freezability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVWmtrnP&md5=f86050048d3adaf5ad3ed32bc6b3e651CAS |

Vilagran, I., Yeste, M., Sancho, S., Castillo, J., Oliva, R., and Bonet, S. (2015). Comparative analysis of boar seminal plasma proteome from different freezability ejaculates and identification of fibronectin 1 as a sperm freezability marker. Andrology 3, 345–356.
Comparative analysis of boar seminal plasma proteome from different freezability ejaculates and identification of fibronectin 1 as a sperm freezability marker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntFSgsbg%3D&md5=2e4d1a36fc5b1b9d5b2cabcd361cb50dCAS |

Walsh, S. W., Williams, E. J., and Evans, A. C. (2011). A review of the causes of poor fertility in high milk producing dairy cows. Anim. Reprod. Sci. 123, 127–138.
A review of the causes of poor fertility in high milk producing dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3gt1eguw%3D%3D&md5=bacaf80aa7f57e9b7ccceabdc39d9ac6CAS |

Wathes, D. C., Pollott, G. E., Johnson, K. F., Richardson, H., and Cooke, J. S. (2014). Heifer fertility and carry over consequences for life time production in dairy and beef cattle. Animal 8, 91–104.
Heifer fertility and carry over consequences for life time production in dairy and beef cattle.Crossref | GoogleScholarGoogle Scholar |

Yeste, M., Briz, M., Pinart, E., Sancho, S., Bussalleu, E., and Bonet, S. (2010). The osmotic tolerance of boar spermatozoa and its usefulness as sperm quality parameter. Anim. Reprod. Sci. 119, 265–274.
The osmotic tolerance of boar spermatozoa and its usefulness as sperm quality parameter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktVait74%3D&md5=b503115ed2fe65eb534c142c088c0ecdCAS |

Yeste, M., Flores, E., Estrada, E., Bonet, S., Rigau, T., and Rodríguez-Gil, J. E. (2013). Reduced glutathione and procaine hydrochloride protect the nucleoprotein structure of boar spermatozoa during freeze–thawing by stabilising disulfide bonds. Reprod. Fertil. Dev. 25, 1036–1050.
Reduced glutathione and procaine hydrochloride protect the nucleoprotein structure of boar spermatozoa during freeze–thawing by stabilising disulfide bonds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Gms7rM&md5=cc363ef4c55911fe02c47a35bf367bd0CAS |

Yeste, M., Estrada, E., Rivera Del Álamo, M. M., Bonet, S., Rigau, T., and Rodríguez-Gil, J. E. (2014). The increase in phosphorylation levels of serine residues of protein HSP70 during holding time at 17°C is concomitant with a higher cryotolerance of boar spermatozoa. PLoS One 9, e90887.
The increase in phosphorylation levels of serine residues of protein HSP70 during holding time at 17°C is concomitant with a higher cryotolerance of boar spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Yeste, M., Fernández-Novell, J. M., Ramió-Lluch, L., Estrada, E., Rocha, L. G., Cebrián-Pérez, J. A., Muiño-Blanco, T., Concha, I. I., Ramírez, A., and Rodríguez-Gil, J. E. (2015). Intracellular calcium movements of boar spermatozoa during ‘in vitro’ capacitation and subsequent acrosome exocytosis follow a multiple-storage place, extracellular calcium-dependent model. Andrology 3, 729–747.
Intracellular calcium movements of boar spermatozoa during ‘in vitro’ capacitation and subsequent acrosome exocytosis follow a multiple-storage place, extracellular calcium-dependent model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1GkurfN&md5=881f26f9d6c17ae23caf71dc0d5ee646CAS |

Yeste, M., Morató, R., Rodríguez-Gil, J. E., Bonet, S., and Prieto-Martínez, N. (2017). Aquaporins in the male reproductive tract and sperm: functional implications and cryobiology. Reprod. Domest. Anim. 52, 12–27.
Aquaporins in the male reproductive tract and sperm: functional implications and cryobiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhslSksLzF&md5=b746b50debddc3f2eefab20badaf2021CAS |

Yeung, C. H. (2010). Aquaporins in spermatozoa and testicular germ cells: identification and potential role. Asian J. Androl. 12, 490–499.
Aquaporins in spermatozoa and testicular germ cells: identification and potential role.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlSksrw%3D&md5=232eaa378da305b0edf6d5bd6f38205dCAS |

Yeung, C. H., and Cooper, T. G. (2010). Aquaporin AQP11 in the testis: molecular identity and association with the processing of residual cytoplasm of elongated spermatids. Reproduction 139, 209–216.
Aquaporin AQP11 in the testis: molecular identity and association with the processing of residual cytoplasm of elongated spermatids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWlsw%3D%3D&md5=82d02b442a14ea2f8374f45ef3df9b36CAS |

Yeung, C. H., Callies, C., Tüttelmann, F., Kliesch, S., and Cooper, T. G. (2010). Aquaporins in the human testis and spermatozoa – identification, involvement in sperm volume regulation and clinical relevance. Int. J. Androl. 33, 629–641.
| 1:CAS:528:DC%2BC3cXhtVOntbvO&md5=4602c6be20c3fc911371e092e2477b86CAS |

Zhu, C., Jiang, Z., Bazer, F. W., Johnson, G. A., Burghardt, R. C., and Wu, G. (2015). Aquaporins in the female reproductive system of mammals. Front. Biosci. (Landmark Ed.) 20, 838–871.
Aquaporins in the female reproductive system of mammals.Crossref | GoogleScholarGoogle Scholar |