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Reorganization of the Flagellum Scaffolding Induces a Sperm Standstill During Fertilization

Martina Jabloñski, Guillermina M. Luque, Matías D. Gómez-Elías, Claudia Sanchez-Cardenas, Xinran Xu, Jose Luis de la Vega-Beltran, View ORCID ProfileGabriel Corkidi, Alejandro Linares, Victor X. Abonza Amaro, Aquetzalli Arenas-Hernandez, María Del Pilar Ramos-Godinez, Alejandro López-Saavedra, View ORCID ProfileDario Krapf, View ORCID ProfileDiego Krapf, View ORCID ProfileAlberto Darszon, Adan Guerrero, View ORCID ProfileMariano G. Buffone
doi: https://doi.org/10.1101/2023.06.22.546073
Martina Jabloñski
1Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina
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Guillermina M. Luque
1Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina
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Matías D. Gómez-Elías
1Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina
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Claudia Sanchez-Cardenas
2Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
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Xinran Xu
3Department of Electrical and Computer Engineering and School of Biomedical Engineering, Colorado State University, Fort Collins, Colorado, USA
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Jose Luis de la Vega-Beltran
2Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
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Gabriel Corkidi
4Laboratorio de Imágenes y Visión por Computadora, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, México
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Alejandro Linares
2Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
6Laboratorio Nacional de Microscopía Avanzada, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
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Victor X. Abonza Amaro
2Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
6Laboratorio Nacional de Microscopía Avanzada, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
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Aquetzalli Arenas-Hernandez
7Departamento de Microscopía Electrónica, Instituto Nacional de Cancerología, Mexico City, Mexico
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María Del Pilar Ramos-Godinez
8Unidad de Aplicaciones Avanzadas en Microscopía, Instituto Nacional de Cancerología, Unidad de Investigación Biomédica en Cáncer, UNAM. Mexico City, Mexico
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Alejandro López-Saavedra
8Unidad de Aplicaciones Avanzadas en Microscopía, Instituto Nacional de Cancerología, Unidad de Investigación Biomédica en Cáncer, UNAM. Mexico City, Mexico
9Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud. Mexico City, Mexico
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Dario Krapf
5Instituto de Biología Molecular y Celular de Rosario (IBR), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Nacional de Rosario (UNR), Rosario, Argentina
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Diego Krapf
3Department of Electrical and Computer Engineering and School of Biomedical Engineering, Colorado State University, Fort Collins, Colorado, USA
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Alberto Darszon
2Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
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Adan Guerrero
2Departamento de Genética del Desarrollo y Fisiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
6Laboratorio Nacional de Microscopía Avanzada, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, Mexico
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Mariano G. Buffone
1Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina
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  • ORCID record for Mariano G. Buffone
  • For correspondence: [email protected]
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Abstract

Mammalian sperm delve into the female reproductive tract to fertilize the female gamete. The available information about how sperm regulate their motility during the final journey to the fertilization site is extremely limited. In this work, we investigated the structural and functional changes in the sperm flagellum after AE and during the interaction with the eggs. The evidence demonstrates that the double helix actin network surrounding the mitochondrial sheath of the midpiece undergoes structural changes prior to the motility cessation. This structural modification is accompanied by a decrease in diameter of the midpiece and is driven by intracellular calcium changes that occur concomitant with a reorganization of the actin helicoidal cortex. Midpiece contraction occurs in a subset of cells that undergo AE, live-cell imaging during in vitro fertilization showed that the midpiece contraction is required for motility cessation after fusion is initiated. These findings provide the first evidence of the F-actin network’s role in regulating sperm motility, adapting its function to meet specific cellular requirements during fertilization, and highlighting the broader significance of understanding sperm motility.

Significant statement In this work, we demonstrate that the helical structure of polymerized actin in the flagellum undergoes a rearrangement at the time of sperm-egg fusion. This process is driven by intracellular calcium and promotes a decrease in the sperm midpiece diameter as well as the arrest in motility, which is observed after the fusion process is initiated.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* Mariano G. Buffone Ph.D. Instituto de Biología y Medicina Experimental, CONICET. Vuelta de Obligado 2490 (1428), Buenos Aires, Argentina. Tel: (+5411)4783-2869. E-mail: mgbuffone{at}ibyme.conicet.gov.ar. Adan Guerrero Ph.D. Laboratorio Nacional de Microscopía Avanzada, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, México. Email: adan.guerrero{at}ibt.unam.mx.

  • We have included new experiments to support our conclusions. In particular, those related to show the midpiece contraction using alternative methods (not based in dyes).

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted July 02, 2024.
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Reorganization of the Flagellum Scaffolding Induces a Sperm Standstill During Fertilization
Martina Jabloñski, Guillermina M. Luque, Matías D. Gómez-Elías, Claudia Sanchez-Cardenas, Xinran Xu, Jose Luis de la Vega-Beltran, Gabriel Corkidi, Alejandro Linares, Victor X. Abonza Amaro, Aquetzalli Arenas-Hernandez, María Del Pilar Ramos-Godinez, Alejandro López-Saavedra, Dario Krapf, Diego Krapf, Alberto Darszon, Adan Guerrero, Mariano G. Buffone
bioRxiv 2023.06.22.546073; doi: https://doi.org/10.1101/2023.06.22.546073
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Reorganization of the Flagellum Scaffolding Induces a Sperm Standstill During Fertilization
Martina Jabloñski, Guillermina M. Luque, Matías D. Gómez-Elías, Claudia Sanchez-Cardenas, Xinran Xu, Jose Luis de la Vega-Beltran, Gabriel Corkidi, Alejandro Linares, Victor X. Abonza Amaro, Aquetzalli Arenas-Hernandez, María Del Pilar Ramos-Godinez, Alejandro López-Saavedra, Dario Krapf, Diego Krapf, Alberto Darszon, Adan Guerrero, Mariano G. Buffone
bioRxiv 2023.06.22.546073; doi: https://doi.org/10.1101/2023.06.22.546073

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