The echinoderm nervous system is the least well studied of all the major metazoan phyla. For a number of technical reasons, the structure and function of echinoderm nerves have been neglected. Analysis of the sea urchin genome has enabled an unprecedented glimpse into the neural and sensory functions and has revealed several novel molecular approaches to the study of echinoderm nervous systems ().
Genomic insights into sea urchin neurobiology.
The nervous systems of echinoderm larvae and adults are dispersed, but they are not simple nerve nets. This organization differs from both vertebrates, which do not have a dispersed nervous system, and hemichordates, which do have nerve nets (47
). Adult sea urchins have thousands of appendages, each with sensory neurons, ganglia, and motor neurons arranged in local reflex arcs. These peripheral appendages are connected to each other and to radial nerves, which provide overall control and coordination (47
Nearly all of the genes encoding known neurogenic transcription factors are present in the sea urchin genome, and several are expressed in neurogenic domains before gastrulation, which indicates that they may operate near the top of a conserved neural gene regulatory network (47
). Axon guidance molecules known from other metazoans are also expressed in the developing embryo. Unexpectedly, genes encoding the neurotrophin-Trk receptor system that were thought to be vertebrate-specific because they were not found in Ciona
, are present in sea urchin, which suggests a deuterostome origin and a potential loss in urochordates.
The genes required to construct neurons and to transmit signals are present, but the repertoire of neural genes and the initial characterization of expression of a number of them led to unexpected and surprising conclusions. There appear to be no genes encoding gap junction proteins, which suggests that communication among neurons depends on chemical synapses without ionic coupling. The repertoire of sea urchin neurotransmitters is large, but melatonin and adrenalin are lacking, as they are in ascidians (4
). Cannabinoid, lysophospholipid, and melanocortin receptors are not present in urchins, but orthologs were found in ascidians (4
). In contrast, some sets of genes thought to be chordate-specific have sea urchin orthologs, for example, insulin and insulin-like growth factors (IGFs) that are more similar to their chordate counterparts than those of other invertebrates (47
). Overall, the genome contains representatives of all five large superfamilies of GPCRs, including those that mediate signals from neuropeptides and peptide hormones. Both the secretin and rhodopsin superfamilies display marked lineage-specific expansions (13
There were 200 to 700 putative chemosensory genes that formed large clusters and lacked introns, which are features of chemosensory genes in vertebrates, but not in Caenorhabditis elegans
and Drosophila melanogaster
. Many of these genes encoded amino acid motifs that were characteristic of vertebrate chemosensory and odorant receptors (13
). Sea urchins had an elaborate collection of photoreceptor genes that quite surprisingly appeared to be expressed in tube feet (13
). These included many genes encoding transcription factors regulating retinal development and a photorhodopsin gene.
Human Usher syndromes are genetic diseases affecting hearing, balance, and retinitis pigmentosa (retinal photoreceptor degeneration). Most of the genes involved have been identified, and they encode a set of membrane and cytoskeletal proteins that form an interacting network that controls the arrangement of mechanosensory stereocilia in hair cells of the mammalian ear. Many or all of the proteins play some roles in photoreceptor organization and/or maintenance. Orthologs of virtually the entire set of membrane and cytoskeletal proteins of the Usher syndrome network were found in the sea urchin genome. These include the very large membrane proteins, usherin and VLGR-1 and large cadherins (Cadh23 and possibly Pcad15), all of which participate in forming links between stereocilia in mammalian hair cells, as well as myosin 7 and 15, two PDZ proteins (harmonin and whirlin) and another adaptor protein (SANS), which participate in linking these membrane proteins to the cytoskeleton. In addition, two membrane transporters, NBC (a candidate Usher syndrome target known to interact with harmonin) and TrpA1 (the mechanosensory channel connected to the tip links containing cadherin 23), have orthologs in the sea urchin genome. Sea urchins do not have ears or eyes, so they must deploy these proteins in other sensory processes. Sea urchins respond to light, touch, and displacement and probably use some of same sensory genes used by vertebrates.