Changes in membrane carbohydrates distribution associated to epididymal sperm maturation during the prolonged sperm storage period of Corynorhinus mexicanus bat (Chiroptera: Vespertilionidae)

Ahiezer Rodríguez Tobón, Reyna Fierro, Miguel Angel León Galván, Adolfo Rosado, Edith Cortés Barberena, Edith Arenas Ríos


The Corynorhinus mexicanus bat provides an interesting experimental model for the study of epididymal sperm maturation because after testicular regression, this bat stores sperm in epididymal cauda for several months. Earlier research conducted by our group suggested that sperm maturation in this specie must be completed in the caudal region of the epididymis, although the precise factor linked with this phenomenon is unknown. Therefore, the aim of this work was to analyze changes in the distribution of N-acetylglucosamine and/or sialic acid, Fucose and Mannose carbohydrates in different membrane domains of sperm cells as they change from the caput to the cauda of the epididymis, as well as, their changes in different dates of capture. The sperm cells present a redistribution of N-acetylglucosamine and/or sialic when they arrived in the caudal region (September 11), but after storage until October 22 the distribution of N-acetylglucosamine and/or sialic acid changed. Mannose residues were found predominantly towards the acrosome during their entry into and transit through the three regions of the epididymis. The flow cytometry assay indicated that fluorescence intensity due to the presence of of N-acetylglucosamine and/or sialic acid on the sperm decreases as the sperm pass through the epididymal duct and as storage time in the cauda goes on. The Mannose fluorescence intensity, decreased in corpus and cauda from September 24 to October 8, though no differences appeared on the latter date. The presence of Fucuse was corroborated only by flow cytometry. In conclusion, the carbohydrate distribution on sperm membrane can be considered as part of the process of epididymal sperm maturation and is associated with the phenomenon of prolonged sperm storage that is characteristic of this specie. This adaptation allows the males to synchronize with the period of receptivity of the females, and then, carry out the matings.

Palabras clave

bats; epididymal sperm maturation; sperm storage; membrane carbohydrates; lectins

Texto completo:

PDF (English)


Arenas-Ríos, E., León-Galván, M. A., Mercado, P. E., Rosado A. (2005) Superoxide dismutase, catalase, and glutathione peroxidase during epididymal maturation and prolonged storage of spermatozoa in the Mexican big-eared bat (Corynorhinus mexicanus). Canadian Journal of Zoology, 83, 1556–1565.

Arenas, M. I., De Miguel, M. P., Bethencourt, F. R., Fraile, B., Royuela, M., Paniagua, R. (1996) Lectin histochemistry in the human epididymis. Journal of Reproduction and Fertility, 106, 313–320.

Baker, M. A., Hetherington, L., Weinberg, A., Naumovski, N., Velkov, T., Pelzing, M., Dolman, S., Condina, M. R., Aitken, R. J. (2012) Analysis of phosphopeptide changes as spermatozoa acquire functional competence in the epididymis demonstrates changes in the post-translational modification of Izumo1. Journal of Proteome Research, 11, 5252–5264.

Cervantes, M. I., Arenas-Rios, E., Leon-Galvan, M. A., Lopez-Wilchis, R., Ambriz, D., Rosado, A. (2008) Spermatozoa epididymal maturation in the Mexican big-eared bat (Corynorhinus mexicanus). Systems Biology in Reproductive Medicine, 54, 196–204.

Chandra, A., Srinivasan, K. R., Jamal, F., Mehrotra, P. K., Singh, R. L., Srivastav, A. (2008) Post-translational modifications in glycosylation status during epididymal passage and significance in fertility of a 33 kDa glycoprotein (MEF3) of rhesus monkey (Macaca mulatta). Reproduction, 135, 761–770.

Clermont, Y., Tang, X. M. (1985) Glycoprotein synthesis in the Golgi apparatus of spermatids during spermiogenesis of the rat. The Anatomical Record, 213, 33–43.

Cooper, T. G. (2011) The epididymis, cytoplasmic droplets and male fertility. Asian Journal of Andrology, 13, 130–138.

Dacheux, J. L., Belleannee, C., Guyonnet, B., Labas, V., Teixeira-Gomes, A. P., Ecroyd, H., Druart, X., Gatti, J. L., Dacheux, F. (2012) The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa. Systems Biology in Reproductive Medicine, 58, 197–210.

Damjanov, I. (1987) Biology of disease. Lectin cytochemistry and histochemistry. Laboratory Investigation, 57, 5–20.

De Maistre, E., Bene, M. C., Foliguet, B., Touati, F., Faure, G. C. (1996) Centrifugation on Percoll gradient enhances fluorescent lectin binding on human sperm: a flow cytometric analysis. Archives of Andrology, 37, 179–187.

Eddy, E., Vermon, R., Muller, C., Hahnel, A., Fenderson, B. (1985) Inmunodissection of sperm surface modification during epididymal maturation. American Journal of Anatomy, 174, 225–237.

Fierro, R., Foliguet, B., Grignon, G., Daniel, M., Bene, M. C., Faure, G. C., Barbarino-Monnier, P. (1996) Lectin-binding sites on human sperm during acrosome reaction: modifications judged by electron microscopy/flow cytometry. Archives of Andrology, 36, 187–196.

Flesch, F. M., Voorhout, W. F., Colenbrander, B., van Golde, L. M., Gadella, B. M. (1998) Use of lectins to characterize plasma membrane preparations from boar spermatozoa: a novel technique for monitoring membrane purity and quantity. Biology of Reproduction, 59, 1530–1539.

Harayama, H., Miyake, M., Shidara, O., Iwamoto, E., Kato, S. (1998) Effects of calcium and bicarbonate on head-to-head agglutination in ejaculated boar spermatozoa. Reproduction, Fertility and Development, 10, 445-450.

Holt, W. V. (1980) Surface-bound sialic acid on ram and bull spermatozoa: deposition during epididymal transit and stability during washing. Biology of Reproduction, 23, 847–857.

Jimenez, I., Fierro, R., Gonzalez-Marquez, H., Mendoza-Hernandez, G., Romo, S., Betancourt, M. (2006) Carbohydrate affinity chromatography indicates that arylsulfatase-A from capacitated boar sperm has mannose and N-acetylglucosamine/sialic acid residues. Archives of Andrology, 52, 455–462.

Kopecny, V., Flechon, J. E. (1981) Fate of acrosomal glycoproteins during the acrosomal reaction and fertilization: a light and electron microscope autoradiographic study. Biology of Reproduction, 24, 201–216.

Kumar, G. P, Laloraya, M., Agrawal, P., Laloraya, M. M. (1990) The involvement of surface sugars of mammalian spermatozoa in epididymal maturation and in vitro sperm-zona recognition. Andrologia, 22, 184–194.

León-Galván, M. A., López-Wilchis, R., Hernández-Pérez, O., Arenas-Ríos, E., Rosado, A. (2005) Male reproductive cycle of Mexican big-eared bats, Corynorhinus mexicanus (Chiroptera: Vespertilionidae). The Southwestern Naturalist, 50, 453–460.

Lewis, B., Aitken, R. J. (2001) Impact of epididymal maturation on the tyrosine phosphorylation patterns exhibited by rat spermatozoa. Biology of Reproduction, 64, 1545–1556.

Moore, H. D., Bedford, J. M. (1979) The differential absorptive activity of epithelial cells of the rat epididymus before and after castration. The Anatomical Record, 193, 313–327.

Navaneetham, D., Sivashanmugam, P., Rajalakshmi, M. (1996) Changes in binding of lectins to epididymal, ejaculated, and capacitated spermatozoa of the rhesus monkey. The Anatomical Record, 245, 500–508.

Olson, G. E., Danzo, B. J. (1981) Surface changes in rat spermatozoa during epididymal transit. Biology of Reproduction, 24, 431–443.

Racey, P. A., Entwistle, A. C. (2000) Life-history and reproductive strategies of bats, pp. 364–414. In: E. G. Crichton, P. H. Krutzsch (Eds.). Reproductive biology of bats. Academic Press, San Diego, CA. USA.

Rodríguez-Tobón, A., Fierro, R., León-Galván, M. A., Rosado, A., Cortés-Barberena, E., Arenas-Ríos, E. (2016) Tyrosine phosphorylation as evidence of epididymal cauda participation in the sperm maturation process of Corynorhinus mexicanus bat. Acta Zoologica (Stockholm), 97, 310–318.

Schroter, S., Osterhoff, C., McArdle, W., Ivell, R. (1999) The glycocalyx of the sperm surface. Human Reproduction Update, 5, 302–313.

SEMARNAT (2010) Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Protección Ambiental-Especies Nativas de México de Flora y Fauna Silvestres-Categorías de Riesgo y Especificaciones para su Inclusión, Exclusión o Cambio-Lista de Especies en Riesgo. Diario Oficial de la Federación. Aviable at (accessed on October 2019).

Sikes, R. S., Gannon, W. L. (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92, 235–253.

Sullivan, R., Frenette, G., Girouard, J. (2007) Epididymosomes are involved in the acquisition of new sperm proteins during epididymal transit. Asian Journal of Andrology, 9, 483–491.

Toshimori, K. (1998) Maturation of mammalian spermatozoa: modifications of the acrosome and plasma membrane leading to fertilization. Cell and Tissue Research, 293, 177–187.

Toyonaga, M., Morita, M., Hori, T., Tsutsui, T. (2011) Distribution of glycoproteins on feline testicular sperm, epididymal sperm and ejaculated sperm. The Journal of Veterinary Medical Science, 73, 827–829.

Tulsiani, D. R. (2003) Glycan modifying enzymes in luminal fluid of rat epididymis: are they involved in altering sperm surface glycoproteins during maturation? Microscopy Research and Technique, 61, 18–27.

Tulsiani, D. R. (2006) Glycan-modifying enzymes in luminal fluid of the mammalian epididymis: an overview of their potential role in sperm maturation. Molecular and Cell Endocrinology, 250, 58–65.

Vazquez, J. M., Martinez, E., Pastor, L. M., Roca, J., Matas, C., Calvo, A. (1996) Lectin histochemistry during in vitro capacitation and acrosome reaction in boar spermatozoa: new lectins for evaluating acrosomal status of boar spermatozoa. Acta Histochemica, 98, 93–100.

World Health Organization (2010) WHO Laboratory Manual for the Examination and Processing of Human Semen. World Health Organization. Geneva, Switzerland, 287 pp.


Enlaces refback

  • No hay ningún enlace refback.

Copyright (c) 2020 ACTA ZOOLÓGICA MEXICANA (N.S.)

Licencia de Creative Commons
Este obra está bajo una licencia de Creative Commons Reconocimiento-NoComercial-CompartirIgual 4.0 Internacional.

Acta Zoológica Mexicana (nueva serie), 2020, Vol. 36, es una publicación electrónica continua de acceso abierto, editada por el Instituto de Ecología, A.C. (INECOL), Carretera antigua a Coatepec 351, Col. El Haya, Xalapa, Ver. C.P. 91073, Tel. (228) 842-1800, extensión 4112 Editor responsable: Sergio Ibáñez-Bernal, Reservas de Derechos al Uso Exclusivo No. 04-2019-021314325500-203, versión on-line ISSN 2448-8445, [antes también impresa ISSN 0065-1737], con registros otorgados por el Instituto Nacional del Derecho de Autor. Responsable de la última actualización de este volumen, Sergio Ibáñez-Bernal, Carretera antigua a Coatepec, 351, Col. El Haya, Xalapa, Ver., C.P. 91073. Fecha de la última modificación: 09 de enero de 2020.


Reconocimiento –noComercial-Compartirigual