Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2019-0083
Animal Reproduction (AR)
Original Article

Lectin spatial immunolocalization during in vitro capacitation in Tursiops truncatus spermatozoa

Laura Robles-Gómez; María del Carmen Fuentes-Albero; Natalia Huerta-Retamal; Paula Sáez-Espinosa; Daniel García-Párraga; Alejandro Romero; María José Gómez-Torres

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Abstract

Abstract: Spermatozoa interactions with the female reproductive tract and oocyte are regulated by surface molecules such as glycocalyx. The capacitation process comprises molecular and structural modifications which increase zona pellucida binding affinity. Lectins allowed us to describe glycocalyx changes during maturation, capacitation and acrosome reaction. This study had as its aim to identify lectin binding patterns using four lectins with different carbohydrate affinity in bottlenose dolphin (Tursiops truncatus) spermatozoa both before and after in vitro capacitation. Two semen samples from the same dolphin obtained on consecutive days were used, with four different lectin binding patterns becoming visible in both samples before and after capacitation. A highly stained equatorial segment with prolongations at the edges appeared as the most frequent pattern with Wheat germ agglutinin (WGA) in uncapacitated spermatozoa. However, it was homogeneously distributed over the acrosomal region after capacitation. Instead, the use of Peanut agglutinin (PNA) resulted in most spermatozoa showing high labelling in the acrosomal periphery region before capacitation and a homogeneous staining in the acrosomal region within the population of capacitated spermatozoa. Nevertheless, the most representative patterns with Concavalin A (ConA) and Aleuria aurantia agglutinin (AAA) lectins did not change before and after capacitation, labelling the acrosomal region periphery. These findings could contribute to the understanding of the reproductive biology of cetaceans and the improvement of sperm selection techniques.

Keywords

bottlenose dolphin, sperm capacitation, lectin

References

Andrews B. Bottlenose dolphin management past, present and future. In: Duffield RT, Robeck TR editor. The Bottlenose Dolphin Breeding Workshop. Silver Springs: AZA Marine Mammal Taxon Advisory Group; 2000. p. 7-15

Bains HK, Pabst MA, Bawa SR. Changes in the lectin binding sites on the testicular, epididymal, vas, and ejaculated spermatozoon surface of dog. Andrologia. 1993;25(1):19-24. http://dx.doi.org/10.1111/j.1439-0272.1993.tb02676.x. PMid:8427417.

Baker SS, Thomas M, Thaler CD. Sperm membrane dynamics assessed by changes in lectin fluorescence before and after capacitation. J Androl. 2004;25(5):744-51. http://dx.doi.org/10.1002/j.1939-4640.2004.tb02850.x. PMid:15292105.

Bawa SR, Pabst MA, Werner G, Bains HK. Capacitated and acrosome reacted spermatozoa of goat (Capra indicus): a fluorescence and electron microscopic study. Andrologia. 1993;25(3):123-35. http://dx.doi.org/10.1111/j.1439-0272.1993.tb02694.x. PMid:8517552.

Bearer EL, Friend DS. Morphology of mammalian sperm membranes during differentiation, maturation, and capacitation. J Electron Microsc Tech. 1990;16(4):281-97. http://dx.doi.org/10.1002/jemt.1060160403. PMid:2250184.

Bhattacharyya L, Ceccarini C, Lorenzoni P, Brewer CF. Concanavalin a interactions with asparagine-linked glycopeptides. J Biol Chem. 1987;262(3):1288-93. PMid:3805020.

Cites.org [homepage on the Internet]. Ginebra: The Convention on International Trade in Endangered Species of Wild Fauna and Flora; 2019 [cited 2019 Jun 19]. Avaiable from: https://cites.org/esp/node/25478

Fierro R, Foliguet B, Grignon G, Daniel M, Bene MC, Faure GC, Barbarino-Monnier P. Lectin-binding sites on human sperm during acrosome reaction: modifications judged by electron microscopy/flow cytometry. Arch Androl. 1996;36(3):187-96. http://dx.doi.org/10.3109/01485019608987095. PMid:8743350.

Fleming AD, Yanagimachi R, Yanagimachi H. Spermatozoa of the Atlantic bottlenosed dolphin, Tursiops truncatus. Reproduction. 1981;63(2):509-14. http://dx.doi.org/10.1530/jrf.0.0630509. PMid:6895389.

Friend DS. Plasma-membrane diversity in a highly polarized cell. J Cell Biol. 1982;93(2):243-9. http://dx.doi.org/10.1083/jcb.93.2.243. PMid:7096437.

Gabriel LK, Franken DR, Van Der Horst G, Kruger TF, Oehninger SC. Wheat germ agglutinin receptors on human sperm membranes and sperm morphology. Andrologia. 1994;26(1):5-8. http://dx.doi.org/10.1111/j.1439-0272.1994.tb00745.x. PMid:8185062.

Gallagher JT, Morris A, Dexter TM. Identification of two binding sites for wheat-germ agglutinin on polylactosamine-type oligosaccharides. Biochem J. 1985;231(1):115-22. http://dx.doi.org/10.1042/bj2310115. PMid:3840682.

Gómez-Torres MJ, Avilés M, Girela JL, Murcia V, Fernández-Colom PJ, Romeu A, De Juan J. Characterization of the lectin binding pattern in human spermatozoa after swim-up selection. Histol Histopathol. 2012;27(12):1621-8. PMid:23059892.

Harrison RJ. Reproduction and reproductive organs. In: Yersen HT, editor. The biology of marine mammals. New York: Academic Press; 1969. p. 253-348.

Jiménez I, González-Márquez H, Ortiz R, Betancourt M, Herrera J, Fierro R. Expression of lectin receptors on the membrane surface of sperm of fertile and subfertile boars by flow cytometry. Arch Androl. 2002;48(2):159-66. http://dx.doi.org/10.1080/014850102317267481. PMid:11868630.

Keller KV. Training of the Atlantic bottlenose dolphins (Tursiops truncatus) for artificial insemination. Proceedings of the International Association for Aquatic Animal Medicine. 1986;14:22-4.

Kita S, Yoshioka M, Kashiwagi M, Ogawa S, Tobayama T. Comparative external morphology of cetacean spermatozoa. Fish Sci. 2001;67(3):482-92. http://dx.doi.org/10.1046/j.1444-2906.2001.00284.x.

Lassalle B, Testart J. Human zona pellucida recognition associated with removal of sialic. J Reprod Fertil. 1994;101(3):703-11. http://dx.doi.org/10.1530/jrf.0.1010703. PMid:7966029.

Lee SH, Ahuja KK. An investigation using lectins of glycocomponents of mouse spermatozoa during capacitation and sperm-zona binding. J Reprod Fertil. 1987;80(1):65-74. http://dx.doi.org/10.1530/jrf.0.0800065. PMid:3598974.

Lee MC, Damjanov I. Lectin binding sites on human sperm and spermatogenic cells. Anat Rec. 1985;212(3):282-7. http://dx.doi.org/10.1002/ar.1092120310. PMid:3933381.

Lotan R, Skutelsky E, Danon D, Sharon N. The purification, composition, and specificity of the anti-T lectin from peanut (Arachis hypogaea). J Biol Chem. 1975;250(21):8518-23. PMid:811657.

Magargee F, Kunze E, Hammerstedt RH. Changes in lectin-binding features of ram sperm surfaces associated with epididymal maturation and ejaculation. Biol Reprod. 1988;38(3):667-85. http://dx.doi.org/10.1095/biolreprod38.3.667. PMid:3378079.

Meisner AD, Klaus AV, O’Leary MA. Sperm head morphology in 36 species of Artiodactylans, Perissodactylans, and Cetaceans (Mammalia). J Morphol. 2005;263(2):179-202. http://dx.doi.org/10.1002/jmor.10297. PMid:15593320.

Migliorisi AL, Loureiro JP, Balbona JC, de la Sota RL, Loureiro JD. Estudios preliminares de los parámetros seminales de un delfín de nariz de botella (Tursiops truncatus gephyreus). In Abstracts of the 9º Simposio Internacional de Reproducción Animal; 2011; Córdoba, Argentina. Córdoba: IRAC; 2011.

Montano GA, Kraemer DC, Love CC, Robeck TR, O’Brien JK. Evaluation of motility, membrane status and DNA integrity of frozen-thawed bottlenose dolphin (Tursiops truncatus) spermatozoa after sex-sorting and recryopreservation. Reproduction. 2012;143(6):799-813. http://dx.doi.org/10.1530/REP-11-0490. PMid:22454530.

Navaneetham D, Sivashanmugam P, Rajalakshmi M. Changes in binding of lectins to epididymal, ejaculated, and capacitated spermatozoa of the rhesus monkey. Anat Rec. 1996;245(3):500-8. http://dx.doi.org/10.1002/(SICI)1097-0185(199607)245:3<500::AID-AR6>3.0.CO;2-V. PMid:8800408.

Nicolson GL, Usui N, Yanagimachi R, Yanagimachi H, Smith J. Lectin-binding sites on the plasma membranes of rabbit spermatozoa. J Cell Biol. 1977;74(3):950-62. http://dx.doi.org/10.1083/jcb.74.3.950. PMid:903374.

Osawa T, Tsuji T. Fractionation and structural assessment of oligosaccharides and glycopeptides by use of immobilized lectins. Annu Rev Biochem. 1987;56(1):21-42. http://dx.doi.org/10.1146/annurev.bi.56.070187.000321. PMid:3304133.

Peláez J, Long JA. Characterizing the glycocalyx of poultry spermatozoa: I. Identification and distribution of carbohydrate residues using flow cytometry and epifluorescence microscopy. J Androl. 2007;28(2):342-52. http://dx.doi.org/10.2164/jandrol.106.001073. PMid:17108364.

Purohit S, Laloraya M, Kumar PG. Distribution of N- and O-linked oligosaccharides on surface of spermatozoa from normal and infertile subjects. Andrologia. 2008;40(1):7-12. http://dx.doi.org/10.1111/j.1439-0272.2008.00801.x. PMid:18211295.

Robeck TR, McBain JF, Mathey S, Kraemer DC. Ultrasonographic evaluation of the effects of exogenous gonadotropins on follicular recruitment and ovulation induction in the Atlantic bottlenose dolphin (Tursiops truncatus). J Zoo Wildl Med. 1998;28(1):6-13. PMid:9638617.

Robeck TR, Steinman KJ, Yoshioka M, Jensen E, Obrien JK, Katsumata E, Gili C, McBain JF, Sweeney J, Monfort SL. Estrous cycle characterization and artificial insemination using frozen-thawed spermatozoa in the bottlenose dolphin (Tursiops truncatus). Reproduction. 2005;129(5):659-74. http://dx.doi.org/10.1530/rep.1.00516. PMid:15855629.

Schröter S, Osterhoff C, McArdle W, Ivell R. The glycocalyx of the sperm surface. Hum Reprod Update. 1999;5(4):302-13. http://dx.doi.org/10.1093/humupd/5.4.302. PMid:10465522.

Tecle E, Gagneux P. Sugar-coated sperm: unraveling the functions of the mammalian sperm glycocalyx. Mol Reprod Dev. 2015;82(9):635-50. http://dx.doi.org/10.1002/mrd.22500. PMid:26061344.

Töpfer-Petersen E. Carbohydrate-based interactions on the route of a spermatozoon to fertilization. Hum Reprod Update. 1999;5(4):314-29. http://dx.doi.org/10.1093/humupd/5.4.314. PMid:10465523.

van der Horst G, Medger K, Steckler D, Luther I, Bartels P. Bottlenose dolphin (Tursiops truncatus) sperm revisited: Motility, morphology and ultrastructure of fresh sperm of consecutive ejaculates. Anim Reprod Sci. 2018;195:309-20. http://dx.doi.org/10.1016/j.anireprosci.2018.06.009. PMid:29954651.

World Health Organization. WHO Laboratory manual for the examination and processing of human semen and sperm-cervical mucus interaction. 5. ed. Geneva: World Health Organization; 2010.
 

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