Constitutive recycling of the store-operated Ca2+ channel Orai1 and its internalization during meiosis

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Abstract

The egg's competency to activate at fertilization and transition to embryogenesis is dependent on its ability to generate a fertilization-specific Ca2+ transient. To endow the egg with this capacity, Ca2+ signals remodel during oocyte maturation, including inactivation of the primary Ca2+ influx pathway store-operated Ca2+ entry (SOCE). SOCE inactivation is coupled to internalization of the SOCE channel, Orai1. In this study, we show that Orai1 internalizes during meiosis through a caveolin (Cav)- and dynamin-dependent endocytic pathway. Cav binds to Orai1, and we map a Cav consensus-binding site in the Orai1 N terminus, which is required for Orai1 internalization. Furthermore, at rest, Orai1 actively recycles between an endosomal compartment and the cell membrane through a Rho-dependent endocytic pathway. A significant percentage of total Orai1 is intracellular at steady state. Store depletion completely shifts endosomal Orai1 to the cell membrane. These results define vesicular trafficking mechanisms in the oocyte that control Orai1 subcellular localization at steady state, during meiosis, and after store depletion.

Original languageEnglish
Pages (from-to)523-535
Number of pages13
JournalJournal of Cell Biology
Volume191
Issue number3
DOIs
Publication statusPublished - 1 Nov 2010

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Caveolins
Meiosis
Recycling
Fertilization
Oocytes
Cell Membrane
Dynamins
Embryonic Development
Ovum
Binding Sites

ASJC Scopus subject areas

  • Cell Biology

Cite this

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title = "Constitutive recycling of the store-operated Ca2+ channel Orai1 and its internalization during meiosis",
abstract = "The egg's competency to activate at fertilization and transition to embryogenesis is dependent on its ability to generate a fertilization-specific Ca2+ transient. To endow the egg with this capacity, Ca2+ signals remodel during oocyte maturation, including inactivation of the primary Ca2+ influx pathway store-operated Ca2+ entry (SOCE). SOCE inactivation is coupled to internalization of the SOCE channel, Orai1. In this study, we show that Orai1 internalizes during meiosis through a caveolin (Cav)- and dynamin-dependent endocytic pathway. Cav binds to Orai1, and we map a Cav consensus-binding site in the Orai1 N terminus, which is required for Orai1 internalization. Furthermore, at rest, Orai1 actively recycles between an endosomal compartment and the cell membrane through a Rho-dependent endocytic pathway. A significant percentage of total Orai1 is intracellular at steady state. Store depletion completely shifts endosomal Orai1 to the cell membrane. These results define vesicular trafficking mechanisms in the oocyte that control Orai1 subcellular localization at steady state, during meiosis, and after store depletion.",
author = "Fang Yu and Lu Sun and Khaled Machaca",
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AU - Yu, Fang

AU - Sun, Lu

AU - Machaca, Khaled

PY - 2010/11/1

Y1 - 2010/11/1

N2 - The egg's competency to activate at fertilization and transition to embryogenesis is dependent on its ability to generate a fertilization-specific Ca2+ transient. To endow the egg with this capacity, Ca2+ signals remodel during oocyte maturation, including inactivation of the primary Ca2+ influx pathway store-operated Ca2+ entry (SOCE). SOCE inactivation is coupled to internalization of the SOCE channel, Orai1. In this study, we show that Orai1 internalizes during meiosis through a caveolin (Cav)- and dynamin-dependent endocytic pathway. Cav binds to Orai1, and we map a Cav consensus-binding site in the Orai1 N terminus, which is required for Orai1 internalization. Furthermore, at rest, Orai1 actively recycles between an endosomal compartment and the cell membrane through a Rho-dependent endocytic pathway. A significant percentage of total Orai1 is intracellular at steady state. Store depletion completely shifts endosomal Orai1 to the cell membrane. These results define vesicular trafficking mechanisms in the oocyte that control Orai1 subcellular localization at steady state, during meiosis, and after store depletion.

AB - The egg's competency to activate at fertilization and transition to embryogenesis is dependent on its ability to generate a fertilization-specific Ca2+ transient. To endow the egg with this capacity, Ca2+ signals remodel during oocyte maturation, including inactivation of the primary Ca2+ influx pathway store-operated Ca2+ entry (SOCE). SOCE inactivation is coupled to internalization of the SOCE channel, Orai1. In this study, we show that Orai1 internalizes during meiosis through a caveolin (Cav)- and dynamin-dependent endocytic pathway. Cav binds to Orai1, and we map a Cav consensus-binding site in the Orai1 N terminus, which is required for Orai1 internalization. Furthermore, at rest, Orai1 actively recycles between an endosomal compartment and the cell membrane through a Rho-dependent endocytic pathway. A significant percentage of total Orai1 is intracellular at steady state. Store depletion completely shifts endosomal Orai1 to the cell membrane. These results define vesicular trafficking mechanisms in the oocyte that control Orai1 subcellular localization at steady state, during meiosis, and after store depletion.

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