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Alteration of the Cortical Actin Cytoskeleton Deregulates Ca(2+) Signaling, Monospermic Fertilization, and Sperm Entry

BACKGROUND: When preparing for fertilization, oocytes undergo meiotic maturation during which structural changes occur in the endoplasmic reticulum (ER) that lead to a more efficient calcium response. During meiotic maturation and subsequent fertilization, the actin cytoskeleton also undergoes drama...

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Autores principales: Puppo, A., Chun, Jong T., Gragnaniello, Giovanni, Garante, Ezio, Santella, Luigia
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2570615/
https://www.ncbi.nlm.nih.gov/pubmed/18974786
http://dx.doi.org/10.1371/journal.pone.0003588
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author Puppo, A.
Chun, Jong T.
Gragnaniello, Giovanni
Garante, Ezio
Santella, Luigia
author_facet Puppo, A.
Chun, Jong T.
Gragnaniello, Giovanni
Garante, Ezio
Santella, Luigia
author_sort Puppo, A.
collection PubMed
description BACKGROUND: When preparing for fertilization, oocytes undergo meiotic maturation during which structural changes occur in the endoplasmic reticulum (ER) that lead to a more efficient calcium response. During meiotic maturation and subsequent fertilization, the actin cytoskeleton also undergoes dramatic restructuring. We have recently observed that rearrangements of the actin cytoskeleton induced by actin-depolymerizing agents, or by actin-binding proteins, strongly modulate intracellular calcium (Ca(2+)) signals during the maturation process. However, the significance of the dynamic changes in F-actin within the fertilized egg has been largely unclear. METHODOLOGY/PRINCIPAL FINDINGS: We have measured changes in intracellular Ca(2+) signals and F-actin structures during fertilization. We also report the unexpected observation that the conventional antagonist of the InsP(3) receptor, heparin, hyperpolymerizes the cortical actin cytoskeleton in postmeiotic eggs. Using heparin and other pharmacological agents that either hypo- or hyperpolymerize the cortical actin, we demonstrate that nearly all aspects of the fertilization process are profoundly affected by the dynamic restructuring of the egg cortical actin cytoskeleton. CONCLUSIONS/SIGNIFICANCE: Our findings identify important roles for subplasmalemmal actin fibers in the process of sperm-egg interaction and in the subsequent events related to fertilization: the generation of Ca(2+) signals, sperm penetration, cortical granule exocytosis, and the block to polyspermy.
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spelling pubmed-25706152008-10-30 Alteration of the Cortical Actin Cytoskeleton Deregulates Ca(2+) Signaling, Monospermic Fertilization, and Sperm Entry Puppo, A. Chun, Jong T. Gragnaniello, Giovanni Garante, Ezio Santella, Luigia PLoS One Research Article BACKGROUND: When preparing for fertilization, oocytes undergo meiotic maturation during which structural changes occur in the endoplasmic reticulum (ER) that lead to a more efficient calcium response. During meiotic maturation and subsequent fertilization, the actin cytoskeleton also undergoes dramatic restructuring. We have recently observed that rearrangements of the actin cytoskeleton induced by actin-depolymerizing agents, or by actin-binding proteins, strongly modulate intracellular calcium (Ca(2+)) signals during the maturation process. However, the significance of the dynamic changes in F-actin within the fertilized egg has been largely unclear. METHODOLOGY/PRINCIPAL FINDINGS: We have measured changes in intracellular Ca(2+) signals and F-actin structures during fertilization. We also report the unexpected observation that the conventional antagonist of the InsP(3) receptor, heparin, hyperpolymerizes the cortical actin cytoskeleton in postmeiotic eggs. Using heparin and other pharmacological agents that either hypo- or hyperpolymerize the cortical actin, we demonstrate that nearly all aspects of the fertilization process are profoundly affected by the dynamic restructuring of the egg cortical actin cytoskeleton. CONCLUSIONS/SIGNIFICANCE: Our findings identify important roles for subplasmalemmal actin fibers in the process of sperm-egg interaction and in the subsequent events related to fertilization: the generation of Ca(2+) signals, sperm penetration, cortical granule exocytosis, and the block to polyspermy. Public Library of Science 2008-10-30 /pmc/articles/PMC2570615/ /pubmed/18974786 http://dx.doi.org/10.1371/journal.pone.0003588 Text en Puppo et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Puppo, A.
Chun, Jong T.
Gragnaniello, Giovanni
Garante, Ezio
Santella, Luigia
Alteration of the Cortical Actin Cytoskeleton Deregulates Ca(2+) Signaling, Monospermic Fertilization, and Sperm Entry
title Alteration of the Cortical Actin Cytoskeleton Deregulates Ca(2+) Signaling, Monospermic Fertilization, and Sperm Entry
title_full Alteration of the Cortical Actin Cytoskeleton Deregulates Ca(2+) Signaling, Monospermic Fertilization, and Sperm Entry
title_fullStr Alteration of the Cortical Actin Cytoskeleton Deregulates Ca(2+) Signaling, Monospermic Fertilization, and Sperm Entry
title_full_unstemmed Alteration of the Cortical Actin Cytoskeleton Deregulates Ca(2+) Signaling, Monospermic Fertilization, and Sperm Entry
title_short Alteration of the Cortical Actin Cytoskeleton Deregulates Ca(2+) Signaling, Monospermic Fertilization, and Sperm Entry
title_sort alteration of the cortical actin cytoskeleton deregulates ca(2+) signaling, monospermic fertilization, and sperm entry
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2570615/
https://www.ncbi.nlm.nih.gov/pubmed/18974786
http://dx.doi.org/10.1371/journal.pone.0003588
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