Mammalian sperm capacitation: In vivo and in vitro juxtaposition https://doi.org/10.12982/VIS.2022.026
Article Sidebar
Main Article Content
Abstract
The development of assisted reproductive technologies (ART) in mammalian species such as in vitro embryo production (IVEP) has the potential to provide great benefits for significant population increase, improve genetic performance and advancement, and reduce transmission of venereal diseases. Correspondingly, in vitro capacitation of sperm is also paramount, related to the ability of sperm to fertilize oocytes, and was created to imitate in vivo conditions in the female reproductive tract. Amid in vitro capacitation developments, studies on how far in vitro capacitation has progressed in mimicking in vivo scenes have not been thoroughly reviewed as a comparative form. Therefore, the present study outlined the series of alterations in mammalian sperm capacitation during their journey in the female reproductive tract by exploring and juxtaposing processes under in vivo and in vitro conditions. Several essential aspects that become gaps between in vivo and in vitro were also identified and elaborated comprehensively in this systematic literature review. We noted that although in vitro capacitation procedures in certain mammalian species have made promising progress and improvements, it is still poorly successful in other species like horses. Our findings further postulated that the occurrence of cryocapacitation, the high ratio of capacitated sperm/oocyte required for successful fertilization, and the incidence of polyspermy cause capacitation under in vitro settings is less efficient and not yet fully comparable to in vivo. This work is therefore proposed
several aspects that need to be bettered from in vitro milieu to make it analogous to in vivo environments in modulating sperm capacitation.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Publishing an article with open access in Veterinary Integrative Sciences leaves the copyright with the author. The article is published under the Creative Commons Attribution License 4.0 (CC-BY 4.0), which allows users to read, copy, distribute and make derivative works from the material, as long as the author of the original work is cited.
References
Agarwal, A., Sharma, R., Beydola, T., 2014. Sperm preparation and selection techniques. In: Agarwal, A., Sharma, R., Beydola, T., Medical and Surgical Management of Male infertility, Jaypee Brothers Medical Publishers (P) Ltd., New Delhi, pp. 244–244.
Aitken, R. J., 2011. The capacitation-apoptosis highway: Oxysterols and mammalian sperm function. Biol. Reprod. 85(1), 9–12.
Aitken, R. J., Nixon, B., 2013. Sperm capacitation: A distant landscape glimpsed but unexplored. Mol. Hum. Reprod. 19(12), 785–793.
Aitken, R. J., 2017. Reactive oxygen species as mediators of sperm capacitation and pathological damage. Mol. Reprod. Dev. 84(10), 1039–1052.
Ali, S., 2021. Advances in Bovine Follicular Aspiration Technique. World Sci. News, 157(April),169–188.
Ardon, F., Markello, R. D., Hu, L., Deutsch, Z. I., Tung, C. K., Wu, M., Suarez, S. S., 2016. Dynamics of bovine sperm interaction with epithelium differ between oviductal isthmus and ampulla. Biol. Reprod. 95(4), 1–7.
Armon, L., Eisenbach. M., 2011. Behavioral mechanism during human sperm chemotaxis: Involvement of hyperactivation. PLoS ONE. 6(12), 1-9
Arroyo-Salvo, C., Sanhueza, F., Fuentes, F., Treulén, F., Arias, M. E., Cabrera, P., Silva, M.,Felmer, R., 2019. Effect of human tubal fluid medium and hyperactivation inducers on stallion sperm capacitation and hyperactivation. Reprod. Domest. Anim. 54(2),184–194.
Austin, C. R., 1951. Observations on the penetration of the sperm in the mammalian egg. Aust.J. Biol. Sci. 4(4), 581–596.
Austin, C. R., 1952. The ‘Capacitation’ of the mammalian sperm. Nature. 170(4321), 326.
Bailey, J. L., Bilodeau, J. F., Cormier, N., 2000. Semen cryopreservation in domestic animals: A damaging and capacitating phenomenon. J. Androl. 21(1), 1–7.
Ballester, L., Romero-Aguirregomezcorta, J., Soriano-Úbeda, C., Matás, C., Romar, R., Coy,P., 2014. Timing of oviductal fluid collection, steroid concentrations, and sperm preservation method affect porcine in vitro fertilization efficiency. Fertil. Steril. 102(6), 1762-1768.
Battistone, M. A., Da Ros, V. G., Salicioni, A. M., Navarrete, F. A., Krapf, D., Visconti, P. E., Cuasnicú, P. S., 2013. Functional human sperm capacitation requires both bicarbonate-dependent PKA activation and down-regulation of Ser/Thr phosphatases by Src family kinases. Mol. Hum. Reprod. 19(9), 570–580.
Baumber, J., Sabeur, K., Vo, A., Ball, B. A., 2003. Reactive oxygen species promote tyrosine phosphorylation and capacitation in equine spermatozoa. Theriogenology. 60(7),1239–1247.
Bedford, J. M., 1970. Sperm Capacitation and Fertilization in Mammals. Biol. Reprod. 158,128–158.
Bernecic, N. C., Gadella, B. M., Leahy, T., de Graaf, S., P. 2019. Novel methods to detect capacitation-related changes in spermatozoa. Theriogenology. 137, 56–66.
Blengini, C. S., Teves, M. E., Uñates, D. R., Guidobaldi, H. A., Gatica, L. V., Giojalas, L. C., 2011. Human sperm pattern of movement during chemotactic re-orientation towards a progesterone source. Asian J. Androl. 13(5), 769–773.
Boerke, A., Tsai, P. S., Garcia-Gil, N., Brewis, I. A., Gadella, B. M., 2008. Capacitationdependent reorganization of microdomains in the apical sperm head plasma membrane: Functional relationship with zona binding and the zona-induced acrosome reaction. Theriogenology. 70(8), 1188–1196.
Boerke, A., Brouwers, J. F., Olkkonen, V. M., van de Lest, C. H. A., Sostaric, E., Schoevers, E. J., Helms, J. B., Gadella, B. M., 2013. Involvement of bicarbonate-induced radical signaling in oxysterol formation and sterol depletion of capacitating mammalian sperm during in vitro fertilization. Biol. Reprod. 88(1), 1–18.
Boryshpolets, S., Pérez-Cerezales, S., Eisenbach, M., 2015. Behavioral mechanism of human sperm in thermotaxis: a role for hyperactivation. Hum. Reprod. 30(4), 884–892.
Brackett, B. G., Oliphant, G., 1975. Capacitation of Rabbit Spermatozoa in vitro. Biol. Reprod.12(2), 260–274.
Brukman, N. G., Nuñez, S. Y., Puga Molina, L. del C., Buffone, M. G., Darszon, A., Cuasnicu, P. S., Da Ros, V. G., 2019. Tyrosine phosphorylation signaling regulates Ca 2+ entry by affecting intracellular pH during human sperm capacitation. J. Cell. Physiol. 234(4),5276–5288.
Calvo, L., Dennison-lagos, L., Banks, S. M., Fugger, E. F., Sherins, R. J., 1993. Chemical composition and protein source in the capacitation medium significantly affect the ability of human spermatozoa to undergo follicular fluid induced acrosome reaction. Hum. Reprod. 8(4), 575–580.
Carlson, A. E., Hille, B., Babcock, D. F., 2007. External Ca2+ acts upstream of adenylyl cyclase SACY in the bicarbonate signaled activation of sperm motility. Dev. Biol. 312(1),183–192.
Carlson, A. E., Quill, T. A., Westenbroek, R. E., Schuh, S. M., Hille, B., Babcock, D. F., 2005. Identical phenotypes of CatSper1 and CatSper2 null sperm. J. Biol. Chem. 280(37),32238–32244.
Castillo, J., Bogle, O. A., Jodar, M., Torabi, F., Delgado-Dueñas, D., Estanyol, J. M., Ballescà, J. L., Miller, D., Oliva, R., 2019. Proteomic Changes in Human Sperm During Sequential In vitro Capacitation and Acrosome Reaction. Front. Cell. Dev. Biol. 7,1–16.
Chang, H., Suarez, S. S., 2010. Rethinking the Relationship Between Hyperactivation and Chemotaxis in Mammalian Sperm1. Biol. Reprod. 83(4), 507–513.
Chang, H., Suarez, S. S., 2011. Two Distinct Ca 2+ signaling pathways modulate sperm flagellar beating patterns in mice. Biol. Reprod. 85(2), 296–305.
Chang, H., Suarez, S. S., 2012. Unexpected flagellar movement patterns and epithelial binding behavior of mouse: Sperm in the oviduct. Biol. Reprod. 86(5), 1–8.
Chang, M. C., 1951. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature. 168(4277), 697–698.
Chaves, B. R., Pavaneli, A. P. P., Blanco-Prieto, O., Pinart, E., Bonet, S., Zangeronimo, M. G.,Rodríguez-Gil, J. E., Yeste, M., 2021. Exogenous albumin is crucial for pig sperm to elicit in vitro capacitation whereas bicarbonate only modulates its efficiency. Biology.10(11).
Coy, P., García-Vázquez, F. A., Visconti, P. E., Avilés, M., 2012. Roles of the oviduct in mammalian fertilization. Reproduction. 144(6), 649–660.
Coy, P., Lloyd, R., Romar, R., Satake, N., Matas, C., Gadea, J., Holt, W. V., 2010. Effects of porcine pre-ovulatory oviductal fluid on boar sperm function. Theriogenology. 74(4),632–642.
Coy, P., Avilés, M., 2010. What controls polyspermy in mammals, the oviduct or the oocyte?. Biol. Rev. 85(3), 593–605.
de Lamirande, E., Gagnon, C., 1993. Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic. Biol. Med. 14(2), 157–166.
de Lamirande, E., Gagnon, C., 1995. Capacitation-associated production of superoxide anion by human spermatozoa. Free Radic. Biol. Med. 18(3), 487–495.
Ded, L., Dorosh, A., Dostalova, P., Peknicova, J., 2010. Effect of estrogens on sperm capacitation and acrosome reaction in vitro. J. Reprod. Immunol. 87, 1-11.
Ded, L., Dorosh, A., Peknicova, J., 2019. Fluorescent Analysis of Boar Sperm Capacitation Process In vitro. Biol. Reprod. 109(2019), 1-11.
Del Olmo, E., García-Álvarez, O., Maroto-Morales, A., Ramón, M., Iniesta-Cuerda, M., Martinez-Pastor, F., Montoro, V., Soler, A. J., Garde, J. J., Fernández-Santos, M. R., 2016. Oestrous sheep serum balances ROS levels to supply in vitro capacitation of ram spermatozoa. Reprod. Domest. Anim. 51(5), 743–750.
Domínguez-Rebolledo, Á. E., Fernández-Santos, M. R., Bisbal, A., Ros-Santaella, J. L., Ramón, M., Carmona, M., Martínez-Pastor, F., Garde, J. J., 2010. Improving the effect of incubation and oxidative stress on thawed spermatozoa from red deer by using different antioxidant treatments. Reprod. Fertil. Dev. 22(5), 856–870.
Du Plessis, S. S., Agarwal, A., Mohanty, G., Van Der Linde, M., 2015. Oxidative phosphorylation versus glycolysis: What fuel do spermatozoa use?. Asian J. Androl.17(2), 230–235.
Dukelow, W. R., Chernoff, H. N., 1969. Primate sperm survival and capacitation in a foreign uterine environment. Am. J. Physiol. 216(3), 682–686.
Edwards, R. G., Talbert, L., Israelstam, D., Nino, H. V., Johnson, M. H., 1968. Diffusion chamber for exposing spermatozoa to human uterine secretions. Am. J. Obstet. Gynecol. 102(3), 388–396.
El-Shahat, K. H., Taysser, M. I., Badr, M. R., Zaki, K. A., 2016. Effect of heparin, caffeine and calcium ionophore A23187 on in vitro induction of the acrosome reaction of fresh ram spermatozoa. Asian Pac. J. Reprod. 5(2), 148–155.
El-Shahat, K. H., Taysser, M. I., Badr, M. R., Zaki, K. A., 2017. Effects of penicillamine, hypotaurine, and epinephrine on motility, hyperactivity, acrosome reaction of fresh ram sperm. Asian Pac. J. Reprod. 6(6), 283–288.
Fàbrega, A., Puigmulé, M., Bonet, S., Pinart, E., 2012. Epididymal maturation and ejaculation are key events for further in vitro capacitation of boar spermatozoa. Theriogenology.78(4), 867–877.
Flesch, F. M., Brouwers, J. F. H. M., Nievelstein, P. F. E. M., Verkleij, A. J., van Golde, L. M. G., Colenbrander, B., Gadella, B. M., 2001. Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J. Cell. Sci. 114(19), 3543–3555.
Florman, H. M., Jungnickel, M. K., Sutton, K. A., 2008. Regulating the acrosome reaction. Int.J. Dev. Biol. 52(5–6), 503–510.
Fraser, L. R., 1998. Sperm capacitation and the acrosome reaction. Hum. Reprod. 13(S1), 9–19.
Fujinoki, M., 2013. Progesterone-enhanced sperm hyperactivation through IP3-PKC and PKA signals. Reprod. Med. Biol. 12(1), 27–33.
Gadella, B. M., Luna, C., 2014. Cell biology and functional dynamics of the mammalian sperm surface. Theriogenology. 81(1), 74–84.
García-Álvarez, O., Maroto-Morales, A., Jiménez-Rabadán, P., Ramón, M., del Olmo, E.,Iniesta-Cuerda, M., Anel-López, L., Fernández-Santos, M. R., Garde, J. J., Soler, A. J.,2015. Effect of different media additives on capacitation of frozen-thawed ram spermatozoa as a potential replacement for estrous sheep serum. Theriogenology.84(6), 948–955.
García-Álvarez, O., Maroto-Morales, A., Ramón, M., Del Olmo, E., Jiménez-Rabadán, P.,Fernández-Santos, M. R., Anel-López, L., Garde, J. J., Soler, A. J., 2014. Dynamics of sperm subpopulations based on motility and plasma membrane status in thawed ram spermatozoa incubated under conditions that support in vitro capacitation and fertilisation. Reprod. Fertil. Dev. 26(5), 725–732.
García-Herreros, M., Leal, C. L. V., 2014. Sperm volumetric dynamics during in vitro capacitation process in bovine spermatozoa. Animals. 9(6), 1016–1024.
Gautier, C., Barrier-Battut, I., Guénon, I., Goux, D., Delalande, C., Bouraïma-Lelong, H., 2016. Implication of the estrogen receptors GPER, ESR1, ESR2 in post-testicular maturations of equine spermatozoa. Gen. Comp. Endocrinol. 233, 100–108.
Gibb, Z., Lambourne, S. R., Aitken, R. J., 2014. The paradoxical relationship between stallion fertility and oxidative stress. Biol. Reprod. 91(3), 1–10.
Gibb, Z., Lambourne, S. R., Curry, B. J., Hall, S. E., Aitken, R. J., 2016. Aldehyde dehydrogenase plays a pivotal role in the maintenance of stallion sperm motility. Biol. Reprod. 94(6), 1–11.
Gil, M., Sar-Shalom, V., Sivira, Y. M., Carreras, R., Checa, M. A., 2013. Sperm selection using magnetic activated cell sorting (MACS) in assisted reproduction: a systematic review and meta-analysis. J. Assist. Reprod. Genet. 30(4), 479–485.
Gimeno-Martos, S., Santorromán-Nuez, M., Cebrián-Pérez, J. A., Muiño-Blanco, T., Pérez-Pé, R., Casao, A., 2021. Involvement of progesterone and estrogen receptors in the ram sperm acrosome reaction. Domest. Anim. Endocrinol. 74, 1-10.
Gimeno-Martos, S., Casao, A., Yeste, M., Cebrián-Pérez, J. A., Muiño-Blanco, T., Pérez-Pé, R., 2018. Melatonin reduces cAMP-stimulated capacitation of ram spermatozoa. Reprod. Fertil. Deve. 31(2), 420–431.
Gohil, V. M., Sheth, S. A., Nilsson, R., Wojtovich, A. P., Lee, J. H., Perocchi, F., Chen, W.,Clish, C. B., Ayata, C., Brookes, P. S., Mootha, V. K., 2010. Nutrient-sensitized screening for drugs that shift energy metabolism from mitochondrial respiration to glycolysis. Nat. Biotechnol. 28(3), 249–255.
Gonçalves, F. S., Barretto, L. S. S., Arruda, R. P., Perri, S. H. V., Mingoti, G. Z., 2014. Heparin and penicillamine-hypotaurine-epinephrine (PHE) solution during bovine in vitro fertilization procedures impair the quality of spermatozoa but improve normal oocyte fecundation and early embryonic development. In vitro Cell. Dev. Biol. Anim. 50(1),39–47.
Hasegawa, A., Mochida, K., Tomishima, T., Inoue, K., Ogura, A., 2014. Microdroplet in vitro fertilization can reduce the number of spermatozoa necessary for fertilizing oocytes.J. Reprod. Dev. 60(3), 187–193.
Henkel, R. R., Schill, W. B., 2003. Sperm preparation for ART. Reprod. Biol. Endocrinol. 1,1–22.
Hernández-Silva, G., López-Torres, A. S., Maldonado-Rosas, I., Mata-Martínez, E., Larrea, F.,Torres-Flores, V., Treviño, C. L., Chirinos, M., 2020. Effects of semen processing on sperm function: Differences between swim-up and density gradient centrifugation. World J. Mens Health. 38(4), 1–10.
Hino, T., Muro, Y., Tamura-nakano, M., Okabe, M., Tateno, H., 2016. The behavior and acrosomal status of mouse spermatozoa in vitro, and within the oviduct during fertilization after nnatural mating. Biol. Reprod. 95, 1–11.
Holt, W. V., Van Look, K. J. W., 2004. Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory test of semen quality.Reproduction. 127(5), 527–535.
Hunter, R. H., Dziuk, P. J., 1968. Sperm penetration of pig eggs in relation to the timing of ovulation and insemination. J. Reprod. Fertil. 15(2), 199–208.
Hunter, R. H. F., 2012. Temperature gradients in female reproductive tissues. Reprod. Biomed. Online. 24(4), 377–380.
Hyakutake, T., Mori, K., Sato, K., 2018. Effects of surrounding fluid on motility of hyperactivated bovine sperm. J. Biomech. 71, 183–189.
Ickowicz, D., Finkelstein, M., Breitbart, H., 2012. Mechanism of sperm capacitation and the acrosome reaction: role of protein kinases. Asian J. Androl. 14(6), 816–821.
Inoue, N., Ikawa, M., Nakanishi, T., Matsumoto, M., Nomura, M., Seya, T., Okabe, M., 2003.Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm. Mol. Cell. Biol. 23(7), 2614–2622.
Jin, J., Jin, N., Zheng, H., Ro, S., Tafolla, D., Sanders, K. M., Yan, W., 2007. Catsper3 and Catsper4 are essential for sperm hyperactivated motility and male fertility in the mouse. Biol. Reprod. 77(1), 37–44.
Jin, M., Fujiwara, E., Kakiuchi, Y., Okabe, M., Satouh, Y., Baba, S. A., 2011. Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc. Natl. Acad. Sci. U.S.A. 108(2011),4892–4896.
Kadirvel, G., Kathiravan, P., Kumar, S., 2011. Protein tyrosine phosphorylation and zona binding ability of in vitro capacitated and cryopreserved buffalo spermatozoa. Theriogenology, 75(9), 1630–1639.
Kang, S. S., Koyama, K., Huang, W., Yang, Y., Yanagawa, Y., Takahashi, Y., Nagano, M., 2015.Addition of D-penicillamine, hypotaurine, and epinephrine (PHE) mixture to IVF medium maintains motility and longevity of bovine sperm and enhances stable production of blastocysts in vitro. J. Reprod. Dev., 61(2), 99–105.
Kerns, K., Zigo, M., Drobnis, E. Z., Sutovsky, M., Sutovsky, P., 2018. Zinc ion flux during mammalian sperm capacitation. Nat. Commun. 9(1), 1-10
Kim, D. E., Youn, Y. C., Kim, Y. K., Hong, K. M., Lee, C. S., 2009. Glycyrrhizin prevents 7-ketocholesterol toxicity against differentiated pc12 cells by suppressing mitochondrial membrane permeability change. Neurochem. Res. 34(8), 1433–1442.
Kirton, K. T., Hafs, H. D., 1965. Sperm capacitation by uterine fluid or beta-amylase in vitro. Science. 150(3696), 618–619.
Kumaresan, A., Johannisson, A., Humblot, P., Bergqvist, A. S., 2019. Effect of bovine oviductal fluid on motility, tyrosine phosphorylation, and acrosome reaction in cryopreserved bull spermatozoa. Theriogenology. 124, 48–56.
Kumaresan, A., Siqueira, A. P., Hossain, M. S., Johannisson, A., Eriksson, I., Wallgren, M.,Bergqvist, A. S., 2012. Quantification of kinetic changes in protein tyrosine phosphorylation and cytosolic Ca2+ concentration in boar spermatozoa during cryopreservation. Reprod. Fertil. Dev. 24(4), 531–542.
Kwon, W. S., Shin, D. H., Ryu, D. Y., Khatun, A., Rahman, M. S., Pang, M. G., 2018. Applications of capacitation status for litter size enhancement in various pig breeds. Asian-Australas. J. Anim. Sci. 31(6), 842–850.
Lamy, J., Corbin, E., Blache, M. C., Garanina, A. S., Uzbekov, R., Mermillod, P., Saint-Dizier, M., 2017. Steroid hormones regulate sperm–oviduct interactions in the bovine. Reproduction. 154(4), 497–508.
Langlais, J., Kan, F. W. K., Granger, L., Raymond, L., Bleau, G., Roberts, K. D., 1988. Identification of sterol acceptors that stimulate cholesterol efflux from human spermatozoa during in vitro capacitation. Gamete Res. 20(2), 185–201.
Leahy, T., Gadella, B. M., 2015. New insights into the regulation of cholesterol efflux from the sperm membrane. Asian J. Androl. 17(4), 561–567.
Leemans, B., Stout, T. A. E., De Schauwer, C., Heras, S., Nelis, H., Hoogewijs, M., Van Soom, A., Gadella, B. M., 2019. Update on mammalian sperm capacitation: how much does the horse differ from other species?. Reproduction. 157(5), R181–R197.
Leese, H. J., Hugentobler, S. A., Gray, S. M., Morris, D. G., Sturmey, R. G., Whitear, S.-L., Sreenan, J. M., 2008. Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod. Fertil. Dev. 20(1), 1-8
Li, H. G., Ding, X. F., Liao, A. H., Kong, X. B., Xiong, C. L., 2007. Expression of CatSper family transcripts in the mouse testis during post-natal development and human ejaculated spermatozoa: Relationship to sperm motility. Mol. Hum. Reprod. 13(5),299–306.
Liu, H., Wang, T., Huang, K., 2009. Cholestane-3β,5α,6β-triol-induced reactive oxygen species production promotes mitochondrial dysfunction in isolated mice liver mitochondria. Chem. Biol. Interact. 179(2–3), 81–87.
López-González, I., Torres-Rodríguez, P., Sánchez-Carranza, O., Solís-López, A., Santi, C.M., Darszon, A., Treviño, C. L., 2014. Membrane hyperpolarization during human sperm capacitation. Mol. Hum. Reprod. 20(7), 619–629.
López-Torres, A. S., Chirinos, M., 2017. Modulation of human sperm capacitation by progesterone, estradiol, and luteinizing hormone. Reprod. Sci. 24(2), 193–201.
Losano, J. D. A., Padín, J. F., Méndez-López, I., Angrimani, D. S. R., García, A. G., Barnabe, V. H., Nichi, M., 2017. The stimulated glycolytic pathway is able to maintain ATP levels and kinetic patterns of bovine epididymal sperm subjected to mitochondrial uncoupling. Oxid. Med. Cell. Longev. 2017, 1-8.
Lukoseviciute, K., Zilinskas, H., Januskauskas, A., 2004. Effect of exogenous progesterone on post-thaw capacitation and acrosome reaction of bovine spermatozoa. Reprod.Domest. Anim. 39(3), 154–161.
Machado, S. A., Sharif, M., Wang, H., Bovin, N., Miller, D. J., 2019. Release of Porcine sperm from oviduct cells is stimulated by progesterone and requires CatSper. Sci. Rep. 9(1),1–11.
Macías-García, B., Gonzalez-Fernandez, L., Loux, S. C., Rocha, A. M., Guimarães, T., Pena,F. J., Varner, D. D., Hinrichs, K., 2015. Effect of calcium, bicarbonate, and albumin on capacitation-related events in equine sperm. Reproduction. 149(1), 87–99.
Mahé, C., Zlotkowska, A. M., Reynaud, K., Tsikis, G., Mermillod, P., Druart, X., Schoen, J.,Saint-Dizier, M., 2021. Sperm migration, selection, survival, and fertilizing ability in the mammalian oviduct. Biol. Reprod. 105(2), 317–331.
Maia, M. da S., Bicudo, S. D., Sicherle, C. C., Rodello, L., Gallego, I. C. S., 2010. Lipid peroxidation and generation of hydrogen peroxide in frozen-thawed ram semen cryopreserved in extenders with antioxidants. Anim. Reprod. Sci. 122(1–2), 118–123.
Marquez, B., Suarez, S. S., 2004. Different Signaling Pathways in Bovine Sperm Regulate Capacitation. Biol. Reprod. 1626–1633.
Marquez, B., Suarez, S. S., 2007. Bovine sperm hyperactivation is promoted by alkalinestimulated Ca2+ influx. Biol. Reprod. 660–665.
Marroquin, L. D., Hynes, J., Dykens, J. A., Jamieson, J. D., Will, Y., 2007. Circumventing the crabtree effect: Replacing media glucose with galactose increases susceptibility of hepG2 cells to mitochondrial toxicants. Toxicol. Sci. 97(2), 539–547.
Martin-Hidalgo, D., Gil, M. C., Hurtado De Llera, A., Perez, C. J., Bragado, M. J.,Garcia-Marin, L. J., 2018. Boar sperm hyperactivated motility is induced by temperature via an intracellular calcium-dependent pathway. Reprod. Fertil. Dev.30(11), 1462–1471.
Mattner, P. E., 1963. Capacitation of ram spermatozoa and penetration of the ovine egg. Nature. 199(4895), 772–773.
Maxwell, W. M. C., Evans, G., Rhodes, S. L., Hillard, M. A., Bindon, B. M., 1993. Fertility of superovulated ewes after intrauterine or oviducal insemination with low numbers of fresh or frozen-thawed spermatozoa. Reprod. Fertil. Dev. 5(1), 57–63.
Miki, K., Clapham, D. E., 2013. Rheotaxis guides mammalian sperm. Curr. Biol. 23(6), 443–452.
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.
Mondal, M. A., Takagi, Y., Baba, S. A., Hamano, K., 2017. Involvement of calcium channels and intracellular calcium in bull sperm thermotaxis. J. Reprod. Dev. 63(2), 143–148.
Moody, M. A., Cardona, C., Simpson, A. J., Smith, T. T., Travis, A. J., Ostermeier, G. C., 2017. Validation of a laboratory-developed test of human sperm capacitation. Mol. Reprod. Dev. 84(5), 408–422.
Mukai, C., Okuno, M., 2004. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol. Reprod. 71(2), 540–547.
Muro, Y., Hasuwa, H., Isotani, A., Miyata, H., Yamagata, K., Ikawa, M., Yanagimachi, R.,Okabe, M., 2016. Behavior of mouse spermatozoa in the female reproductive tract from soon after mating to the beginning of fertilization. Biol. Reprod. 94(4), 1–7.
Nadalini, M., Tarozzi, N., Di Santo, M., Borini, A., 2014. Annexin V magnetic-activated cell sorting versus swim-up for the selection of human sperm in ART: Is the new approach better then the traditional one?. J. Assist. Reprod. Genet. 31(8), 1045–1051.
Nagata, M. P. B., Endo, K., Ogata, K., Yamanaka, K., Egashira, J., Katafuchi, N., Yamanouchi, T., Matsuda, H., Goto, Y., Sakatani, M., Hojo, T., Nishizono, H., Yotsushima, K., Takenouchi, N., Hashiyada, Y., Yamashita, K., 2018. Live births from artificial insemination of microfluidic-sorted bovine spermatozoa characterized by trajectories correlated with fertility. Proc. Natl. Acad. Sci. U.S.A. 115(14), E3087–E3096.
Navarrete, F. A., García-Vázquez, F. A., Alvau, A., Escoffier, J., Krapf, D., Sánchez-Cárdenas, C., Salicioni, A. M., Darszon, A., Visconti, P. E., 2015. Biphasic role of calcium in mouse sperm capacitation signaling pathways. J. Cell. Physiol. 230(8), 1758–1769.
Navarro-Serna, S., París-Oller, E., Simonik, O., Romar, R., Gadea, J., 2021. Replacement of albumin by preovulatory oviductal fluid in swim-up sperm preparation method modifies boar sperm parameters and improves in vitro penetration of oocytes. Animals. 11(5), 1-14.
Neild, D. N., Gadella, B. M., Agüero, A., Stout, T. A. E., Colenbrander, B., 2005. Capacitation, acrosome function and chromatin structure in stallion sperm. Anim. Reprod. Sci. 89,47–56.
Ng, K. Y. B., Mingels, R., Morgan, H., Macklon, N., Cheong, Y., 2018. In vivo oxygen,temperature and pH dynamics in the female reproductive tract and their importance in human conception: A systematic review. Hum. Reprod. Update. 24(1), 15–34.
O’Flaherty, C., 2015. Redox regulation of mammalian sperm capacitation. Asian J. Androl.17(4), 583–590.
Olivares, C. C. S., da Fonseca, J. F., de Almeida Camargo, L. S., de Souza-Fabjan, J. M. G.,Rodrigues, A. L. R., Brandão, F. Z., 2015. Comparison of different methods of goat sperm selection and capacitation for optimization of assisted reproductive technologies. Small. Rumin. Res. 127, 44–49.
Oseguera-López, I., Ruiz-Díaz, S., Ramos-Ibeas, P., Pérez-Cerezales, S., 2019. Novel techniques of sperm selection for improving IVF and ICSI outcomes. Front. Cell.Dev. Biol. 7, 1-23.
Parrish, J. J., Susko-Parrish, J. L., First, N. L., 1989. Capacitation of bovine sperm by heparin: Inhibitory effect of glucose and role of intracellular pH. Biol. Reprod. 41(4),683–699.
Parrish, J. J., Susko-Parrish, J., Winer, M. A., First, N. L., 1988. Capacitation of bovine sperm by heparin. Biol. Reprod. 38(5), 1171–1180.
Parrish, J. J., 2014. Bovine in vitro fertilization: In vitro oocyte maturation and sperm capacitation with heparin. Theriogenology. 81(1), 67–73.
Pessoa, G. A., Martini, A. P., Trentin, J. M., Minela, T., Fiorenza, M. F., Rubin, M. I. B., 2017.Response to cooling of pony stallion semen selected by glass wool filtration. Andrologia. 49(10), 1–6.
Pick, E., Keisari, Y., 1980. A simple colorimetric method for the measurement of hydrogen peroxide produced by cells in culture. J. Immunol. Methods. 38(1–2), 161–170.
Pickworth, S., Change, M. C., 1969. Fertilization of Chinese hamster eggs in vitro. J. Reprod. Fert. 19(2), 371–374.
Pini, T., De Graaf, S. P., Druart, X., Tsikis, G., Labas, V., Teixeira-Gomes, A. P., Gadella, B.M., Leahy, T., 2018. Binder of sperm proteins 1 and 5 have contrasting effects on the capacitation of ram spermatozoa. Biol. Reprod. 98(6), 765–775.
Pommer, A. C., Rutllant, J., Meyers, S. A., 2003. Phosphorylation of protein tyrosine residues in fresh and cryopreserved stallion spermatozoa under capacitating conditions. Biol.Reprod. 68(4), 1208–1214.
Qi, H., Moran, M. M., Navarro, B., Chong, J. A., Krapivinsky, G., Krapivinsky, L., Kirichok, Y., Ramsey, I. S., Quill, T. A., Clapham, D. E., 2007. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc.Natl. Acad. Sci. U.S.A. 104(4), 1219–1223.
Rahman, M. S., Kwon, W., Pang, M., 2014. Calcium Influx and Male Fertility in the Context of the Sperm Proteome: An Update. Biomed. Res. Int. 2014, 1–13.
Ramalho-Santos, J., Moreno, R. D., Sutovsky, P., Chan, A. W. S., Hewitson, L., Wessel, G. M.,Simerly, C. R., Schatten, G., 2000. SNAREs in mammalian sperm: Possible implications for fertilization. Dev. Biol. 223(1), 54–69.
Rathi, R., Colenbrander, B., Bevers, M. M., Gadella, B. M., 2001. Evaluation of in vitro capacitation of stallion spermatozoa. Biol. Reprod. 65(2), 462–470.
Rodriguez-Martinez, H., 2007. Role of the oviduct in sperm capacitation. Theriogenology. 68,138–146.
Ruiz-Díaz, S., Oseguera-López, I., De La Cuesta-Díaz, D., García-López, B., Serres, C.,Sanchez-Calabuig, M. J., Gutiérrez-Adán, A., Perez-Cerezales, S., 2020. The presence of d-penicillamine during the in vitro capacitation of stallion spermatozoa prolongs hyperactive-like motility and allows for sperm selection by thermotaxis. Animals. 10(9), 1–18.
Runcan, E. E., Pozor, M. A., Zambrano, G. L., Benson, S., Macpherson, M. L., 2014. Use of two conventional staining methods to assess the acrosomal status of stallion spermatozoa. Equine. Vet. J. 46(4), 503–506.
Ryan, L., O’Callaghan, Y. C., O’Brien, N. M., 2005. The role of the mitochondria in apoptosis induced by 7β-hydroxycholesterol and cholesterol-5β,6β-epoxide. Br. J. Nutr. 94(4),519–525.
Ryu, D. Y., Song, W. H., Pang, W. K., Yoon, S. J., Rahman, M. S., Pang, M. G., 2019.Freezability biomarkers in bull epididymal spermatozoa. Sci. Rep. 9(1), 1–9.
Sagare-Patil, V., Vernekar, M., Galvankar, M., Modi, D., 2013. Progesterone utilizes the PI3K-AKT pathway in human spermatozoa to regulate motility and hyperactivation but not acrosome reaction. Mol. Cell. Endocrinol. 374(1–2), 82–91.
Said, T. M., Land, J. A., 2011. Effects of advanced selection methods on sperm quality and ART outcome: A systematic review. Hum. Reprod. Update. 17(6), 719–733.
Sajeevadathan, M., Pettitt, M. J., Buhr, M., 2019. Interaction of ouabain and progesterone on induction of bull sperm capacitation. Theriogenology. 126, 191–198.
Sebkova, N., Cerna, M., Ded, L., Peknicova, J., Dvorakova-Hortova, K., 2012. The slower the better: How sperm capacitation and acrosome reaction is modified in the presence of estrogens. Reproduction. 143(3), 297–307.
Shannon, P., Vishwanath, R., 1995. The effect of optimal and suboptimal concentrations of sperm on the fertility of fresh and frozen bovine semen and a theoretical model to explain the fertility differences. Anim. Reprod. Sci. 39(1), 1–10.
Sharma, R., Kattoor, A. J., Ghulmiyyah, J., Agarwal, A., 2015. Effect of sperm storage and selection techniques on sperm parameters. Syst. Biol. Reprod. Med. 61(1), 1–12.
Simons, J., Fauci, L., 2018. A model for the acrosome reaction in mammalian sperm. Bull. Math. Biol. 80(9), 2481–2501.
Singh, A. P., Rajender, S., 2015. CatSper channel, sperm function and male fertility. Reprod. Biomed. Online. 30(1), 28–38.
Spina, F. A. La, Molina, L. C. P., Romarowski, A., Vitale, A. M., Falzone, L., Krapf, D., Hirohashi, N., Buffone, M. G., Investigaciones, C. N. De, Aires, B., Aires, B., Aires, B., Station, M. B., 2017. Mouse sperm begin to undergo acrosomal exocytosis in the upper isthmus of the oviduct. Dev. Biol. 411(2), 172–182.
Strauss, F., 1956. The Time and Place of Fertilization of the Golden Hamster Egg. Development. 4(1), 42–56.
Suarez, S. S., 2008. Control of hyperactivation in sperm. Hum. Reprod. Update. 14(6),647–657.
Suarez, S. S., 2016. Mammalian sperm interactions with the female reproductive tract. Cell. Tissue. Res. 363(1), 185–194.
Sumigama, S., Mansell, S., Miller, M., Lishko, P. V., Cherr, G. N., Meyers, S. A., Tollner, T.,2015. Progesterone accelerates the completion of sperm capacitation and activates catsper channel in spermatozoa from the rhesus macaque. Biol. Reprod. 93(6), 1–11.
Sun, X. hong, Zhu, Y. ying, Wang, L., Liu, H. ling, Ling, Y., Li, Z. li, Sun, L. bo., 2017. The Catsper channel and its roles in male fertility: A systematic review. Reprod. Biol. Endocrinol. 15(1), 1–12.
Suzuki, K., Eriksson, B., Rodriguez-Martinez, H., 1999. Effect of hyaluronan on penetration of porcine oocytes in vitro by frozen-thawed ejaculated spermatozoa. Theriogenology. 51(1), 333.
Suzuki, K., Mori, T., Shimizu, H., 1994. In vitro fertilization of porcine oocytes in chemically defined medium. Theriogenology. 42(8), 1357–1368.
Takahashi, Y., First, N. L., 1992. In vitro development of bovine one-cell embryos: Influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology. 37(5),963–978.
Tamburrino, L., Marchiani, S., Minetti, F., Forti, G., Muratori, M., Baldi, E., 2014. The CatSper calcium channel in human sperm: Relation with motility and involvement in progesterone-induced acrosome reaction. Hum. Reprod. 29(3), 418–428.
Teijeiro, J. M., Cabada, M. O., Marini, P. E., 2008. Sperm binding glycoprotein (SBG) produces calcium and bicarbonate dependent alteration of acrosome morphology and protein tyrosine phosphorylation on boar sperm. J. Cell. Biochem. 103(5),1413–1423.
Teijeiro, J. M., Dapino, D. G., 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(4), 329–337.
Teijeiro, J. M., Marini, P. E., 2012. The effect of oviductal deleted in malignant brain tumor 1 over porcine sperm is mediated by a signal transduction pathway that involves pro-AKAP4 phosphorylation. Reproduction. 143(6), 773–785.
Thérien, I., Manjunath, P., 2003. Effect of progesterone on bovine sperm capacitation and acrosome reaction. Biol. Reprod. 69(4), 1408–1415.
Thongkham, M., Thaworn, W., Pattanawong, W., Teepatimakorn, S., Mekchay, S., Sringarm, K., 2021. Spermatological parameters of immunologically sexed bull semen assessed by imaging flow cytometry, and dairy farm trial. Reprod. Biol. 21(2).
Umehara, T., Kawai, T., Goto, M., Richards, J. A. S., Shimada, M., 2018. Creatine enhances the duration of sperm capacitation: a novel factor for improving in vitro fertilization with small numbers of sperm. Hum. Reprod. 33(6), 1117–1129.
Vadnais, M. L., Galantino-Homer, H. L., Althouse, G. C., 2007. Current concepts of molecular events during bovine and porcine spermatozoa capacitation. Arch. Androl. 53(3),109–123.
van Gestel, R. A., Brewis, I. A., Ashton, P. R., Helms, J. B., Brouwers, J. F., Gadella, B. M., 2005. Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. Mol. Hum. Reprod. 11(8), 583–590.
Visconti, P. E., Krapf, D., De La Vega-Beltrán, J. L., Acevedo, J. J., Darszon, A., 2011. Ion channels, phosphorylation and mammalian sperm capacitation. Asian J. Androl. 13(3), 395–405.
Volpes, A., Sammartano, F., Rizzari, S., Gullo, S., Marino, A., Allegra, A., 2016. The pellet swim-up is the best technique for sperm preparation during in vitro fertilization procedures. J. Assist. Reprod. Genet. 33(6), 765–770.
Watson, P. F., 1995. Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod. Fertil. Dev. 7(4),871–891.
Watson, P. F., 2000. The causes of reduced fertility with cryopreserved semen. Anim. Reprod. Sci. 60–61, 481–492.
Witte, T. S., Schäfer-Somi, S., 2007. Involvement of cholesterol, calcium and progesterone in the induction of capacitation and acrosome reaction of mammalian spermatozoa.Anim. Reprod. Sci. 102(3–4), 181–193.
Yanagimachi, R., 1969. In vitro capacitation of hamster spermatozoa by follicular fluid. J. Reprod. Fert. 18, 275–286.
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., 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(4), 729–747.
Yeste, M., 2015. Recent advances in boar sperm cryopreservation: State of the art and current perspectives. Reprod. Domest. Anim. 50, 71–79.
Zapata‐Carmona, H., Soriano‐Úbeda, C., París‐Oller, E., Matás, C., 2020. Periovulatory oviductal fluid decreases sperm protein kinase A activity, tyrosine phosphorylation, and in vitro fertilization in pig. Andrology. 8(3), 756–768.
Zhang, Z., Liu, J., Meriano, J., Ru, C., Xie, S., Luo, J., Sun, Y., 2016. Human sperm rheotaxis: A passive physical process. Sci. Rep. 6, 1–8.
Zhu, Z., Kawai, T., Umehara, T., Hoque, S. A. M., Zeng, W., Shimada, M., 2019a. Negative effects of ROS generated during linear sperm motility on gene expression and ATP generation in boar sperm mitochondria. Free. Radic. Biol. Med. 141(22), 159–171.
Zhu, Z., Umehara, T., Okazaki, T., Goto, M., Fujita, Y., Hoque, S. A. M., Kawai, T., Zeng, W., Shimada, M., 2019b. Gene expression and protein synthesis in mitochondria enhance the duration of high-speed linear motility in boar sperm. Front. Physiol. 10, 1–13.