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Mannosylated glycoconjugates on the surface of activated sperm in the giant freshwater prawn are crucial for sperm binding with the egg vitelline envelop

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Abstract

The unusual morphology and poorly defined acrosome-like structure in the mature sperm of the giant freshwater prawn Macrobrachium rosenbergii has led to difficulties in identifying the state of sperm activation. Mature distal vas deferens sperm (dVSp) can be activated by the calcium ionophore A23187 to show acrosome reaction-like enzymatic activities that increase their binding and penetration capabilities. However, these short-lived enzymatic activities limit their usefulness as a marker of sperm activation for further qualitative and quantitative analyses, leading to our examining the alterations in the exposure of sperm surface glycoconjugates both as markers of sperm activation and for their role in gamete interaction. Our results showed that after A23187 treatment, there was an increased exposure of mannosylated glycoconjugates on the sperm surface revealed by significant Concanavalin A (Con A) staining. Furthermore, sodium metaperiodate pre-treatment, Con A pre-incubation, or co-incubation with α-mannose monosaccharides all significantly reduced A23187-induced dVSp binding to the egg vitelline envelop, demonstrating the importance of sperm surface mannosylated glycoconjugates in the binding process. These same pre-treatments of sperm also resulted in the inhibition of the binding of soluble vitelline envelop proteins (MrVE) to both the sperm surface and to mannosylated dVSp protein bands. Therefore, the present study demonstrated the importance of the exposure of mannosylated glycoconjugates on the surface of activated dVSp, both as a reliable marker of sperm activation and as a binding factor in the gamete interaction process. Furthermore, these findings allow for a better understanding of the surface glycoconjugate-mediated interaction process between gametes in this species of prawn.

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Acknowledgments

This work was supported by the Thailand Research Fund (TRF: Grant No. MRG6080113 to Atthaboon Watthammawut), Srinakharinwirot University Research Grant (493/2559), and Srinakharinwirot University Government Budget Grant (013/2561). The authors would also like to thank all AN104 DR-BIC lab members, all the scientists at the Center of Nanoimaging (CNI) and the Central Instrument Facility at the Faculty of Science, Mahidol University and the Central Lab Facility at the Faculty of Medicine, Srinakharinwirot University.

Funding

This study was funded by the Thailand Research Fund (MRG6080113—Dr. Atthaboon Watthammawut), the Srinakharinwirot University Grant (493/2559) and Government Grant (013/2561), and the Research Support Grant of the Faculty of Science, Mahidol University (Dr. Monsicha Somrit).

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Authors and Affiliations

  1. Department of Anatomy, Faculty of Science, Mahidol University, Rama VI Road, Bangkok, 10400, Thailand

    Monsicha Somrit, Wattana Weerachatyanukul & Somluk Asuvapongpatana

  2. Anatomy Unit, Department of Medical Science, Faculty of Science, Rangsit University, Pathum Thani, 12000, Thailand

    Wauranittha Timklay

  3. Department of Anatomy, Faculty of Medicine, Srinakharinwirot University, 114 Sukhumwit 23 Wattana, Bangkok, 10110, Thailand

    Atthaboon Watthammawut

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  1. Monsicha Somrit
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Contributions

Monsicha Somrit: conceptualization, visualization, investigation, data curation, validation, resources, funding acquisition; Wattana Weerachatyanukul: conceptualization, supervision, validation, resources, funding acquisition; Somluk Asuvapongpatana: conceptualization, supervision, validation, resources; funding acquisition; Wauranitha Timklay: visualization, investigation, data curation, validation; Atthaboon Watthammawut: conceptualization, methodology, visualization, investigation, data curation, formal analysis, validation, resources, funding acquisition, writing-reviewing and editing, project administration.

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Correspondence to Atthaboon Watthammawut.

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All procedures performed in this study involving prawn were in accordance with the ethical standards and guidelines of the National Research Council of Thailand, Seafish UK (Jacklin and Combes 2007) and the National Aquaculture Council of Australia (Johnston and Jungalwalla 2004). The study was approved by the Animal Care Committee, Mahidol University, Thailand (Animal Ethic No. MUSC61-026-428).

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Somrit, M., Weerachatyanukul, W., Asuvapongpatana, S. et al. Mannosylated glycoconjugates on the surface of activated sperm in the giant freshwater prawn are crucial for sperm binding with the egg vitelline envelop. Cell Tissue Res 384, 179–193 (2021). https://doi.org/10.1007/s00441-020-03324-4

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