A novel mutation from gene splicing of a voltage-gated sodium channel in a marine copepod and its potential effect on channel function
The saxitoxins (STX), a group of potent neurotoxins produced by some marine algae (dinoflagellates and cyanobacteria), block voltage-gated sodium channels, inhibiting nerve-signal transmission in consumers of STX-bearing prey. Populations of grazers (clams and copepods) persistently exposed to the S...
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Published in | Journal of experimental marine biology and ecology Vol. 469; pp. 131 - 142 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier B.V
01.08.2015
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Abstract | The saxitoxins (STX), a group of potent neurotoxins produced by some marine algae (dinoflagellates and cyanobacteria), block voltage-gated sodium channels, inhibiting nerve-signal transmission in consumers of STX-bearing prey. Populations of grazers (clams and copepods) persistently exposed to the STX-bearing dinoflagellate Alexandrium fundyense are less susceptible to STX than naïve ones. Adaptation to STX in clams is linked to a point mutation at the STX-binding site in the sodium channel, which dramatically lowers the sensitivity to the toxin (STX resistance). The present study tested if a similar mechanism of STX resistance occurs in the copepod Acartia hudsonica. Our cloning and sequencing results indicate that two full-length cDNA variants (AhNaV1 and AhNaV2) of the sodium channel exist in A. hudsonica, which result from alternative splicing of the single coding gene. Both variants have identical nucleotide sequences except that AhNav1 (the putative mutant isoform) contains a three-amino-acid (GRD) insertion and a single adjacent aa-substitution (A to V) close to the inactivation gate on the cytoplasmic linker between domains III and IV of the sodium channel. All individuals express both AhNaV1 and AhNaV2 in varying proportions. The functional consequences of the mutation were studied by inserting the three-amino acid codons into a rat (rNav1.2) sodium channel expressed in both Xenopus oocytes and HEK cells. Currents carried by construct rNav1.2 bearing the GRD insertion did not inactivate as completely, and recovered faster from inactivation than rNav1.2. These two rNav1.2 constructs were, however, equally sensitive to STX, suggesting that the GRD variation does not confer STX resistance on the rat sequence of Nav1.2. These results render unlikely the hypothesis that this novel mutation is responsible for the adaptation (via resistance) of A. hudsonica to STX-bearing prey.
•The cDNA sequence of a voltage-gated Na+ channel for a marine copepod is reported.•Gene-splicing results in two isoforms of the copepod, Acartia hudsonica, Na+ channel.•The mutant Na+ channel isoform contains a GRD aa insertion and an A to V aa-substitution.•Na+ channel isoforms differ in inactivation and recovery from inactivation.•Both Na+ channel isoforms are, however, equally sensitive to STX. |
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AbstractList | The saxitoxins (STX), a group of potent neurotoxins produced by some marine algae (dinoflagellates and cyanobacteria), block voltage-gated sodium channels, inhibiting nerve-signal transmission in consumers of STX-bearing prey. Populations of grazers (clams and copepods) persistently exposed to the STX-bearing dinoflagellate Alexandrium fundyense are less susceptible to STX than naïve ones. Adaptation to STX in clams is linked to a point mutation at the STX-binding site in the sodium channel, which dramatically lowers the sensitivity to the toxin (STX resistance). The present study tested if a similar mechanism of STX resistance occurs in the copepod Acartia hudsonica. Our cloning and sequencing results indicate that two full-length cDNA variants (AhNaV1 and AhNaV2) of the sodium channel exist in A. hudsonica, which result from alternative splicing of the single coding gene. Both variants have identical nucleotide sequences except that AhNav1 (the putative mutant isoform) contains a three-amino-acid (GRD) insertion and a single adjacent aa-substitution (A to V) close to the inactivation gate on the cytoplasmic linker between domains III and IV of the sodium channel. All individuals express both AhNaV1 and AhNaV2 in varying proportions. The functional consequences of the mutation were studied by inserting the three-amino acid codons into a rat (rNav1.2) sodium channel expressed in both Xenopus oocytes and HEK cells. Currents carried by construct rNav1.2 bearing the GRD insertion did not inactivate as completely, and recovered faster from inactivation than rNav1.2. These two rNav1.2 constructs were, however, equally sensitive to STX, suggesting that the GRD variation does not confer STX resistance on the rat sequence of Nav1.2. These results render unlikely the hypothesis that this novel mutation is responsible for the adaptation (via resistance) of A. hudsonica to STX-bearing prey.
•The cDNA sequence of a voltage-gated Na+ channel for a marine copepod is reported.•Gene-splicing results in two isoforms of the copepod, Acartia hudsonica, Na+ channel.•The mutant Na+ channel isoform contains a GRD aa insertion and an A to V aa-substitution.•Na+ channel isoforms differ in inactivation and recovery from inactivation.•Both Na+ channel isoforms are, however, equally sensitive to STX. The saxitoxins (STX), a group of potent neurotoxins produced by some marine algae (dinoflagellates and cyanobacteria), block voltage-gated sodium channels, inhibiting nerve-signal transmission in consumers of STX-bearing prey. Populations of grazers (clams and copepods) persistently exposed to the STX-bearing dinoflagellate Alexandrium fundyense are less susceptible to STX than naive ones. Adaptation to STX in clams is linked to a point mutation at the STX-binding site in the sodium channel, which dramatically lowers the sensitivity to the toxin (STX resistance). The present study tested if a similar mechanism of STX resistance occurs in the copepod Acartia hudsonica. Our cloning and sequencing results indicate that two full-length cDNA variants (AhNaV1 and AhNaV2) of the sodium channel exist in A. hudsonica, which result from alternative splicing of the single coding gene. Both variants have identical nucleotide sequences except that AhNav1 (the putative mutant isoform) contains a three-amino-acid (GRD) insertion and a single adjacent aa-substitution (A to V) close to the inactivation gate on the cytoplasmic linker between domains III and IV of the sodium channel. All individuals express both AhNaV1 and AhNaV2 in varying proportions. The functional consequences of the mutation were studied by inserting the three-amino acid codons into a rat (rNav1.2) sodium channel expressed in both Xenopus oocytes and HEK cells. Currents carried by construct rNav1.2 bearing the GRD insertion did not inactivate as completely, and recovered faster from inactivation than rNav1.2. These two rNav1.2 constructs were, however, equally sensitive to STX, suggesting that the GRD variation does not confer STX resistance on the rat sequence of Nav1.2. These results render unlikely the hypothesis that this novel mutation is responsible for the adaptation (via resistance) of A. hudsonica to STX-bearing prey. |
Author | Bouchard, Christelle Avery, David E. Zhang, Huan Lin, Senjie Chen, Lihua Dam, Hans G. Bobkov, Yuriy Finiguerra, Michael Anderson, Peter A.V. |
Author_xml | – sequence: 1 givenname: Lihua surname: Chen fullname: Chen, Lihua organization: Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, CT 06340, United States – sequence: 2 givenname: Huan surname: Zhang fullname: Zhang, Huan organization: Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, CT 06340, United States – sequence: 3 givenname: Michael surname: Finiguerra fullname: Finiguerra, Michael organization: Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, CT 06340, United States – sequence: 4 givenname: Yuriy surname: Bobkov fullname: Bobkov, Yuriy organization: The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St. Augustine, FL 32080, United States – sequence: 5 givenname: Christelle surname: Bouchard fullname: Bouchard, Christelle organization: The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St. Augustine, FL 32080, United States – sequence: 6 givenname: David E. surname: Avery fullname: Avery, David E. organization: Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, CT 06340, United States – sequence: 7 givenname: Peter A.V. surname: Anderson fullname: Anderson, Peter A.V. organization: The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St. Augustine, FL 32080, United States – sequence: 8 givenname: Senjie surname: Lin fullname: Lin, Senjie organization: Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, CT 06340, United States – sequence: 9 givenname: Hans G. surname: Dam fullname: Dam, Hans G. email: hans.dam@uconn.edu organization: Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, CT 06340, United States |
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SubjectTerms | Acartia hudsonica Alexandrium fundyense Alternative splicing Copepod Cyanobacteria Electrophysiology Marine Saxitoxin Sodium channel |
Title | A novel mutation from gene splicing of a voltage-gated sodium channel in a marine copepod and its potential effect on channel function |
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