Abstract
Connections between neurons called synapses are the key components underlying all nervous system functions of animals and humans. However, important genetic information on the formation and plasticity of one type, the electrical (gap junction-mediated) synapse, is understudied in many invertebrates. In the present study, we set forth to identify and characterize the gap junction-encoding gene innexin in the central nervous system (CNS) of the mollusk pond snail Lymnaea stagnalis. With PCR, 3′ and 5′ RACE, and BLAST searches, we identified eight innexin genes in the L. stagnalis genome, named Lst Inx1–Lst Inx8. Phylogenetic analysis revealed that the L. stagnalis innexin genes originated from a single copy in the common ancestor of molluskan species by multiple gene duplication events and have been maintained in L. stagnalis since they were generated. The paralogous innexin genes demonstrate distinct expression patterns among tissues. In addition, one paralog, Lst Inx1, exhibits heterogeneity in cells and ganglia, suggesting the occurrence of functional diversification after gene duplication. These results introduce possibilities to study an intriguing potential relationship between innexin paralog expression and cell-specific functional outputs such as heterogenic ability to form channels and exhibit synapse plasticity. The L. stagnalis CNS contains large neurons and functionally defined networks for behaviors; with the introduction of L. stagnalis in the gap junction gene field, we are providing novel opportunities to combine genetic research with direct investigations of functional outcomes at the cellular, synaptic, and behavioral levels.
Highlights
IntroductionFrom simple reflexes to high cognitive functions including learning and memory, all nervous system operations rely on two main forms of synaptic communication to efficiently transmit signals: chemical (transmitter-mediated) and electrical (gap junction-mediated; Ovsepian, 2017)
From simple reflexes to high cognitive functions including learning and memory, all nervous system operations rely on two main forms of synaptic communication to efficiently transmit signals: chemical and electrical
All invertebrate innexins share two strictly conserved cysteines in each extracellular loop and a YY(x)W region in the second transmembrane domain (Phelan and Starich, 2001); the eight innexin paralogs identified in L. stagnalis shared these conserved regions
Summary
From simple reflexes to high cognitive functions including learning and memory, all nervous system operations rely on two main forms of synaptic communication to efficiently transmit signals: chemical (transmitter-mediated) and electrical (gap junction-mediated; Ovsepian, 2017). The presence of innexin has been established in all invertebrates except for sponges and echinoderms (Watanabe, 1958; Skerrett and Williams, 2017); extensive studies of innexin genes encoding the gap junction-forming proteins have been severely restricted to a select few invertebrate model organisms, such as the fruit fly Drosophila melanogaster, the nematode Caenorhabditis elegans, and the medicinal leech Hirudo verbana (Phelan et al, 1998; Starich et al, 2001; Stebbings et al, 2002; Kandarian et al, 2012; Beyer and Berthoud, 2018) Such restrictions limit the extent to which evolutionary and functional analyses can be made; full genetic and molecular characterization of a gap junction system in a novel and easy-to-study invertebrate species is long overdue
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