Species-Specific Gamete Interaction during Sea Urchin Fertilization: Roles of the Egg Jelly and Vitelline Layer

In sea urchins, the sequence of the cellular and molecular events characterizing the fertilization process has been intensively studied. We have learned that to activate the egg, the fertilizing sperm must undergo morphological modifications (the acrosome reaction, AR) upon reaching the outer gelati...

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Main Authors: Nunzia Limatola, Jong Tai Chun, Luigia Santella
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/11/19/2984
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author Nunzia Limatola
Jong Tai Chun
Luigia Santella
author_facet Nunzia Limatola
Jong Tai Chun
Luigia Santella
author_sort Nunzia Limatola
collection DOAJ
description In sea urchins, the sequence of the cellular and molecular events characterizing the fertilization process has been intensively studied. We have learned that to activate the egg, the fertilizing sperm must undergo morphological modifications (the acrosome reaction, AR) upon reaching the outer gelatinous layer enveloping the egg (egg jelly), which triggers the polymerization of F-actin on the sperm head to form the acrosomal process. The AR exposes bindin, an adhesive sperm protein essential for the species-specific interaction with the cognate receptor on the egg vitelline layer. To investigate the specific roles of the egg jelly and vitelline layer at fertilization of sea urchin eggs, <i>Paracentrotus lividus</i> eggs were incubated in acidic seawater, which removes the egg jelly, i.e., experimental conditions that should prevent the occurrence of the AR, and inseminated in the same medium. At variance with the prevailing view, our results have shown that these dejellied <i>P. lividus</i> eggs can still interact with sperm in acidic seawater, albeit with altered fertilization responses. In particular, the eggs deprived of the vitelline layer reacted with multiple sperm but with altered Ca<sup>2+</sup> signals. The results have provided experimental evidence that the plasma membrane, and not the vitelline layer, is where the specific recognition between gametes occurs. The vitelline layer works in unfertilized eggs to prevent polyspermy.
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spelling doaj.art-bd2d5600ea0445e3b4512a0ad81380ee2023-11-23T20:00:36ZengMDPI AGCells2073-44092022-09-011119298410.3390/cells11192984Species-Specific Gamete Interaction during Sea Urchin Fertilization: Roles of the Egg Jelly and Vitelline LayerNunzia Limatola0Jong Tai Chun1Luigia Santella2Department of Research Infrastructures for Marine Biological Resources, Stazione Zoologica Anton Dohrn, 80121 Napoli, ItalyDepartment of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, 80121 Napoli, ItalyDepartment of Research Infrastructures for Marine Biological Resources, Stazione Zoologica Anton Dohrn, 80121 Napoli, ItalyIn sea urchins, the sequence of the cellular and molecular events characterizing the fertilization process has been intensively studied. We have learned that to activate the egg, the fertilizing sperm must undergo morphological modifications (the acrosome reaction, AR) upon reaching the outer gelatinous layer enveloping the egg (egg jelly), which triggers the polymerization of F-actin on the sperm head to form the acrosomal process. The AR exposes bindin, an adhesive sperm protein essential for the species-specific interaction with the cognate receptor on the egg vitelline layer. To investigate the specific roles of the egg jelly and vitelline layer at fertilization of sea urchin eggs, <i>Paracentrotus lividus</i> eggs were incubated in acidic seawater, which removes the egg jelly, i.e., experimental conditions that should prevent the occurrence of the AR, and inseminated in the same medium. At variance with the prevailing view, our results have shown that these dejellied <i>P. lividus</i> eggs can still interact with sperm in acidic seawater, albeit with altered fertilization responses. In particular, the eggs deprived of the vitelline layer reacted with multiple sperm but with altered Ca<sup>2+</sup> signals. The results have provided experimental evidence that the plasma membrane, and not the vitelline layer, is where the specific recognition between gametes occurs. The vitelline layer works in unfertilized eggs to prevent polyspermy.https://www.mdpi.com/2073-4409/11/19/2984fertilizationsea urchin eggspolyspermyactinCa<sup>2+</sup> signalingacrosome reaction
spellingShingle Nunzia Limatola
Jong Tai Chun
Luigia Santella
Species-Specific Gamete Interaction during Sea Urchin Fertilization: Roles of the Egg Jelly and Vitelline Layer
Cells
fertilization
sea urchin eggs
polyspermy
actin
Ca<sup>2+</sup> signaling
acrosome reaction
title Species-Specific Gamete Interaction during Sea Urchin Fertilization: Roles of the Egg Jelly and Vitelline Layer
title_full Species-Specific Gamete Interaction during Sea Urchin Fertilization: Roles of the Egg Jelly and Vitelline Layer
title_fullStr Species-Specific Gamete Interaction during Sea Urchin Fertilization: Roles of the Egg Jelly and Vitelline Layer
title_full_unstemmed Species-Specific Gamete Interaction during Sea Urchin Fertilization: Roles of the Egg Jelly and Vitelline Layer
title_short Species-Specific Gamete Interaction during Sea Urchin Fertilization: Roles of the Egg Jelly and Vitelline Layer
title_sort species specific gamete interaction during sea urchin fertilization roles of the egg jelly and vitelline layer
topic fertilization
sea urchin eggs
polyspermy
actin
Ca<sup>2+</sup> signaling
acrosome reaction
url https://www.mdpi.com/2073-4409/11/19/2984
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AT jongtaichun speciesspecificgameteinteractionduringseaurchinfertilizationrolesoftheeggjellyandvitellinelayer
AT luigiasantella speciesspecificgameteinteractionduringseaurchinfertilizationrolesoftheeggjellyandvitellinelayer