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  • 1
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    Adaptive evolution of voltage-gated sodium channels : the first 800 million years (2012)
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    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2012. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 109 (2012): 10619-10625, doi:10.1073/pnas.1201884109.
    Description: Voltage-gated Na+-permeable (Nav) channels form the basis for electrical excitability in animals. Nav channels evolved from Ca2+ channels and were present in the common ancestor of choanoflagellates and animals although this channel was likely permeable to both Na+ and Ca2+. Thus, like many other neuronal channels and receptors, Nav channels predated neurons. Invertebrates possess two Nav channels (Nav1, Nav2), whereas vertebrate Nav channels are of the Nav1 family. Approximately 500 MYA in early chordates Nav channels evolved a motif that allowed them to cluster at axon initial segments, 50MY later with the evolution of myelin, Nav channels “capitalized” on this property and clustered at nodes of Ranvier. The enhancement of conduction velocity along with the evolution of jaws likely made early gnathostomes fierce predators and the dominant vertebrates in the ocean. Later in vertebrate evolution, the Nav channel gene family expanded in parallel in tetrapods and teleosts (~9-10 genes in amniotes, 8 in teleosts). This expansion occurred during or after the late Devonian extinction when teleosts and tetrapods each diversified in their respective habitats and coincided with an increase in the number of telencephalic nuclei in both groups. The expansion of Nav channels may have allowed for more sophisticated neural computation and tailoring of Nav channel kinetics with potassium channel kinetics to enhance energy savings. Nav channels show adaptive sequence evolution for increasing diversity in communication signals (electric fish), in protection against lethal Nav channel toxins (snakes, newts, pufferfish, insects), and in specialized habitats (naked mole rats).
    Description: Much of the work from my laboratory discussed in this article was funded by NIH R01 NS025513.
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 2
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    Expansion of voltage-dependent Na+ channel gene family in early tetrapods coincided with the emergence of terrestriality and increased brain complexity (2010)
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    Publication Date: 2022-05-25
    Description: Author Posting. © The Authors, 2010. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in Molecular Biology and Evolution 28 (2011): 1415-1424, doi:10.1093/molbev/msq325.
    Description: Mammals have 10 voltage-dependent sodium (Nav) channel genes. Nav channels are expressed in different cell types with different sub-cellular distributions and are critical for many aspects of neuronal processing. The last common ancestor of teleosts and tetrapods had four Nav channel genes presumably on four different chromosomes. In the lineage leading to mammals a series of tandem duplications on two of these chromosomes more than doubled the number of Nav channel genes. It is unknown when these duplications occurred, whether they occurred against a backdrop of duplication of flanking genes on their chromosomes, or as an expansion of ion channel genes in general. We estimated key dates of the Nav channel gene family expansion by phylogenetic analysis using teleost, elasmobranch, lungfish, amphibian, avian, lizard, and mammalian Nav channel sequences, as well as chromosomal synteny for tetrapod genes. We tested, and exclude, the null hypothesis that Nav channel genes reside in regions of chromosomes prone to duplication by demonstrating the lack of duplication or duplicate retention of surrounding genes. We also find no comparable expansion in other voltage dependent ion channel gene families of tetrapods following the teleost-tetrapod divergence. We posit a specific expansion of the Nav channel gene family in the Devonian and Carboniferous periods when tetrapods evolved, diversified, and invaded the terrestrial habitat. During this time the amniote forebrain evolved greater anatomical complexity and novel tactile sensory receptors appeared. The duplication of Nav channel genes allowed for greater regional specialization in Nav channel expression, variation in sub-cellular localization, and enhanced processing of somatosensory input.
    Description: This work was funded by the National Science Foundation (IBN 0236147 to H.H.Z and M.C.J), and the National Institutes of Health (R01GM084879 to H.H.Z).
    Keywords: Sodium channel ; Tetrapods ; Amniotes ; Terrestriality ; Gene duplication ; Brain
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 3
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    The evolution of the four subunits of voltage-gated calcium channels : ancient roots, increasing complexity, and multiple losses (2014)
    Oxford University Press
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Genome Biology and Evolution 6 (2014): 2210-2217, doi:10.1093/gbe/evu177.
    Description: The alpha subunits of voltage-gated calcium channels (Cavs) are large transmembrane proteins responsible for crucial physiological processes in excitable cells. They are assisted by three auxiliary subunits that can modulate their electrical behavior. Little is known about the evolution and roles of the various subunits of Cavs in nonbilaterian animals and in nonanimal lineages. For this reason, we mapped the phyletic distribution of the four channel subunits and reconstructed their phylogeny. Although alpha subunits have deep evolutionary roots as ancient as the split between plants and opistokonths, beta subunits appeared in the last common ancestor of animals and their close-relatives choanoflagellates, gamma subunits are a bilaterian novelty and alpha2/delta subunits appeared in the lineage of Placozoa, Cnidaria, and Bilateria. We note that gene losses were extremely common in the evolution of Cavs, with noticeable losses in multiple clades of subfamilies and also of whole Cav families. As in vertebrates, but not protostomes, Cav channel genes duplicated in Cnidaria. We characterized by in situ hybridization the tissue distribution of alpha subunits in the sea anemone Nematostella vectensis, a nonbilaterian animal possessing all three Cav subfamilies common to Bilateria. We find that some of the alpha subunit subtypes exhibit distinct spatiotemporal expression patterns. Further, all six sea anemone alpha subunit subtypes are conserved in stony corals, which separated from anemones 500 MA. This unexpected conservation together with the expression patterns strongly supports the notion that these subtypes carry unique functional roles.
    Keywords: Voltage-gated calcium channel ; Ion channel ; Cnidaria ; Nematostella vectensis ; Evolution of nervous system
    Repository Name: Woods Hole Open Access Server
    Type: Article
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