Membrane hyperpolarization removes inactivation of Ca2+ channels, leading to Ca2+ influx and subsequent initiation of sperm motility in the common carp

Z. Krasznai, T. Márián, Hiroko Izumi, S. Damjanovich, L. Balkay, L. Trón, Masaaki Morisawa

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135 Citations (Scopus)

Abstract

Change of osmolality surrounding spawned sperm from isotonic to hypotonic causes the initiation of sperm motility in the common carp. Here we show that membrane-permeable cAMP does not initiate motility of carp sperm that is quiescent in isotonic solution, and that motility of the demembranated sperm can be reactivated without cAMP. Furthermore, the cAMP level does not change during the initiation of sperm motility, and inhibitors of protein kinase do not affect sperm motility, suggesting that no cAMP- dependent system is necessary for the regulation of sperm motility. Sperm motility could not be initiated in Ca2+-free hypoosmotic solutions, and significant increase in the intracellular Ca2+ level was observed by a Ca- sensitive fluorescence dye during hypoosmolality-induced active motion period. The demembranated sperm cells were fully reactivated in the solutions containing 10-7 to 10-5 M Ca2+. Ca2+ channel blockers such as verapamil and ω-conotoxin reversibly inhibited the initiation of sperm motility, suggesting that Ca2+ influx is the prerequisite for the initiation of carp sperm motility. Motility of intact sperm was completely blocked; however, that of the demembranated sperm was not inhibited by the calmodulin inhibitor W7, suggesting that the calmodulin bound close to the plasma membrane participated in the initiation of sperm motility. Flow cytometric membrane potential measurements and spectrophotometric measurements by using fluorescence dyes showed transient membrane hyperpolarization on hypoosmolality-induced motility. This article discusses the role of membrane hyperpolarization on removal of inactivation of Ca2+ channels, leading to Ca2+ influx at the initiation of carp sperm motility.

Original languageEnglish
Pages (from-to)2052-2057
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume97
Issue number5
DOIs
Publication statusPublished - 2000

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Carps
Sperm Motility
Membranes
Spermatozoa
Calmodulin
Coloring Agents
Molecular Motor Proteins
Fluorescence
Conotoxins
Isotonic Solutions
Verapamil
Membrane Potentials
Osmolar Concentration
Protein Kinases
Cell Membrane

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

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title = "Membrane hyperpolarization removes inactivation of Ca2+ channels, leading to Ca2+ influx and subsequent initiation of sperm motility in the common carp",
abstract = "Change of osmolality surrounding spawned sperm from isotonic to hypotonic causes the initiation of sperm motility in the common carp. Here we show that membrane-permeable cAMP does not initiate motility of carp sperm that is quiescent in isotonic solution, and that motility of the demembranated sperm can be reactivated without cAMP. Furthermore, the cAMP level does not change during the initiation of sperm motility, and inhibitors of protein kinase do not affect sperm motility, suggesting that no cAMP- dependent system is necessary for the regulation of sperm motility. Sperm motility could not be initiated in Ca2+-free hypoosmotic solutions, and significant increase in the intracellular Ca2+ level was observed by a Ca- sensitive fluorescence dye during hypoosmolality-induced active motion period. The demembranated sperm cells were fully reactivated in the solutions containing 10-7 to 10-5 M Ca2+. Ca2+ channel blockers such as verapamil and ω-conotoxin reversibly inhibited the initiation of sperm motility, suggesting that Ca2+ influx is the prerequisite for the initiation of carp sperm motility. Motility of intact sperm was completely blocked; however, that of the demembranated sperm was not inhibited by the calmodulin inhibitor W7, suggesting that the calmodulin bound close to the plasma membrane participated in the initiation of sperm motility. Flow cytometric membrane potential measurements and spectrophotometric measurements by using fluorescence dyes showed transient membrane hyperpolarization on hypoosmolality-induced motility. This article discusses the role of membrane hyperpolarization on removal of inactivation of Ca2+ channels, leading to Ca2+ influx at the initiation of carp sperm motility.",
author = "Z. Krasznai and T. M{\'a}ri{\'a}n and Hiroko Izumi and S. Damjanovich and L. Balkay and L. Tr{\'o}n and Masaaki Morisawa",
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T1 - Membrane hyperpolarization removes inactivation of Ca2+ channels, leading to Ca2+ influx and subsequent initiation of sperm motility in the common carp

AU - Krasznai, Z.

AU - Márián, T.

AU - Izumi, Hiroko

AU - Damjanovich, S.

AU - Balkay, L.

AU - Trón, L.

AU - Morisawa, Masaaki

PY - 2000

Y1 - 2000

N2 - Change of osmolality surrounding spawned sperm from isotonic to hypotonic causes the initiation of sperm motility in the common carp. Here we show that membrane-permeable cAMP does not initiate motility of carp sperm that is quiescent in isotonic solution, and that motility of the demembranated sperm can be reactivated without cAMP. Furthermore, the cAMP level does not change during the initiation of sperm motility, and inhibitors of protein kinase do not affect sperm motility, suggesting that no cAMP- dependent system is necessary for the regulation of sperm motility. Sperm motility could not be initiated in Ca2+-free hypoosmotic solutions, and significant increase in the intracellular Ca2+ level was observed by a Ca- sensitive fluorescence dye during hypoosmolality-induced active motion period. The demembranated sperm cells were fully reactivated in the solutions containing 10-7 to 10-5 M Ca2+. Ca2+ channel blockers such as verapamil and ω-conotoxin reversibly inhibited the initiation of sperm motility, suggesting that Ca2+ influx is the prerequisite for the initiation of carp sperm motility. Motility of intact sperm was completely blocked; however, that of the demembranated sperm was not inhibited by the calmodulin inhibitor W7, suggesting that the calmodulin bound close to the plasma membrane participated in the initiation of sperm motility. Flow cytometric membrane potential measurements and spectrophotometric measurements by using fluorescence dyes showed transient membrane hyperpolarization on hypoosmolality-induced motility. This article discusses the role of membrane hyperpolarization on removal of inactivation of Ca2+ channels, leading to Ca2+ influx at the initiation of carp sperm motility.

AB - Change of osmolality surrounding spawned sperm from isotonic to hypotonic causes the initiation of sperm motility in the common carp. Here we show that membrane-permeable cAMP does not initiate motility of carp sperm that is quiescent in isotonic solution, and that motility of the demembranated sperm can be reactivated without cAMP. Furthermore, the cAMP level does not change during the initiation of sperm motility, and inhibitors of protein kinase do not affect sperm motility, suggesting that no cAMP- dependent system is necessary for the regulation of sperm motility. Sperm motility could not be initiated in Ca2+-free hypoosmotic solutions, and significant increase in the intracellular Ca2+ level was observed by a Ca- sensitive fluorescence dye during hypoosmolality-induced active motion period. The demembranated sperm cells were fully reactivated in the solutions containing 10-7 to 10-5 M Ca2+. Ca2+ channel blockers such as verapamil and ω-conotoxin reversibly inhibited the initiation of sperm motility, suggesting that Ca2+ influx is the prerequisite for the initiation of carp sperm motility. Motility of intact sperm was completely blocked; however, that of the demembranated sperm was not inhibited by the calmodulin inhibitor W7, suggesting that the calmodulin bound close to the plasma membrane participated in the initiation of sperm motility. Flow cytometric membrane potential measurements and spectrophotometric measurements by using fluorescence dyes showed transient membrane hyperpolarization on hypoosmolality-induced motility. This article discusses the role of membrane hyperpolarization on removal of inactivation of Ca2+ channels, leading to Ca2+ influx at the initiation of carp sperm motility.

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U2 - 10.1073/pnas.040558097

DO - 10.1073/pnas.040558097

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