ECB-ART-49840
Front Endocrinol (Lausanne)
2020 Jan 01;11:225. doi: 10.3389/fendo.2020.00225.
Show Gene links
Show Anatomy links
Comparative and Evolutionary Physiology of Vasopressin/ Oxytocin-Type Neuropeptide Signaling in Invertebrates.
Odekunle EA
,
Elphick MR
.
Abstract
The identification of structurally related hypothalamic hormones that regulate blood pressure and diuresis (vasopressin, VP; CYFQNCPRG-NH2) or lactation and uterine contraction (oxytocin, OT; CYIQNCPLG-NH2) was a major advance in neuroendocrinology, recognized in the award of the Nobel Prize for Chemistry in 1955. Furthermore, the discovery of central actions of VP and OT as regulators of reproductive and social behavior in humans and other mammals has broadened interest in these neuropeptides beyond physiology into psychology. VP/OT-type neuropeptides and their G-protein coupled receptors originated in a common ancestor of the Bilateria (Urbilateria), with invertebrates typically having a single VP/OT-type neuropeptide and cognate receptor. Gene/genome duplications followed by gene loss gave rise to variety in the number of VP/OT-type neuropeptides and receptors in different vertebrate lineages. Recent advances in comparative transcriptomics/genomics have enabled discovery of VP/OT-type neuropeptides in an ever-growing diversity of invertebrate taxa, providing new opportunities to gain insights into the evolution of VP/OT-type neuropeptide function in the Bilateria. Here we review the comparative physiology of VP/OT-type neuropeptides in invertebrates, with roles in regulation of reproduction, feeding, and water/salt homeostasis emerging as common themes. For example, we highlight recent reports of roles in regulation of oocyte maturation in the sea-squirt Ciona intestinalis, extraoral feeding behavior in the starfish Asterias rubens and energy status and dessication resistance in ants. Thus, VP/OT-type neuropeptides are pleiotropic regulators of physiological processes, with evolutionarily conserved roles that can be traced back to Urbilateria. To gain a deeper understanding of the evolution of VP/OT-type neuropeptide function it may be necessary to not only determine the actions of the peptides but also to characterize the transcriptomic/proteomic/metabolomic profiles of cells expressing VP/OT-type precursors and/or VP/OT-type receptors within the framework of anatomically and functionally identified neuronal networks. Furthermore, investigation of VP/OT-type neuropeptide function in a wider range of invertebrate species is now needed if we are to determine how and when this ancient signaling system was recruited to regulate diverse physiological and behavioral processes in different branches of animal phylogeny and in contrasting environmental contexts.
PubMed ID: 32362874
PMC ID: PMC7181382
Article link: Front Endocrinol (Lausanne)
Grant support: [+]
Article Images: [+] show captions
References [+] :
ACHER,
[The structure of bovine vasopressin].
1954, Pubmed
ACHER, [The structure of bovine vasopressin]. 1954, Pubmed
Acher, Molecular evolution of fish neurohypophysial hormones: neutral and selective evolutionary mechanisms. 1996, Pubmed
Acher, Unique evolution of neurohypophysial hormones in cartilaginous fishes: possible implications for urea-based osmoregulation. 1999, Pubmed
Adams, The genome sequence of Drosophila melanogaster. 2000, Pubmed
Aikins, Vasopressin-like peptide and its receptor function in an indirect diuretic signaling pathway in the red flour beetle. 2008, Pubmed
Alevizos, Synaptic actions of identified peptidergic neuron R15 in Aplysia. I. Activation of respiratory pumping. 1991, Pubmed
Alevizos, Synaptic actions of identified peptidergic neuron R15 in Aplysia. III. Activation of the large hermaphroditic duct. 1991, Pubmed
Amare, Neuropeptide precursors in Tribolium castaneum. 2007, Pubmed
Arletti, Oxytocin inhibits food and fluid intake in rats. 1990, Pubmed
Baines, Pharmacological analysis of the cholinergic input to the locust VPLI neuron from an extraocular photoreceptor system. 1994, Pubmed
Baines, Analysis of the peptide content of the locust vasopressin-like immunoreactive (VPLI) neurons. 1995, Pubmed
Balment, Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. 2006, Pubmed
Banerjee, Structural and functional diversity of nonapeptide hormones from an evolutionary perspective: A review. 2017, Pubmed
Barberis, Structural bases of vasopressin/oxytocin receptor function. 1998, Pubmed
Bardou, Distribution of oxytocin-like and vasopressin-like immunoreactivities within the central nervous system of the cuttlefish, Sepia officinalis. 2009, Pubmed
Bardou, Vasopressin/oxytocin-related peptides influence long-term memory of a passive avoidance task in the cuttlefish, Sepia officinalis. 2010, Pubmed
Bauknecht, Large-Scale Combinatorial Deorphanization of Platynereis Neuropeptide GPCRs. 2015, Pubmed
Beets, Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. elegans. 2012, Pubmed
Beets, Ancient neuromodulation by vasopressin/oxytocin-related peptides. 2013, Pubmed
Burke, A genomic view of the sea urchin nervous system. 2006, Pubmed , Echinobase
C. elegans Sequencing Consortium, Genome sequence of the nematode C. elegans: a platform for investigating biology. 1998, Pubmed
Cannon, Xenacoelomorpha is the sister group to Nephrozoa. 2016, Pubmed
Chen, Neuropeptide precursors and neuropeptides in the sea cucumber Apostichopus japonicus: a genomic, transcriptomic and proteomic analysis. 2019, Pubmed , Echinobase
Christie, Peptidergic signaling in the crab Cancer borealis: Tapping the power of transcriptomics for neuropeptidome expansion. 2016, Pubmed
Chérasse, Measuring inotocin receptor gene expression in chronological order in ant queens. 2017, Pubmed
Coast, A comparison of the effects of two putative diuretic hormones from Locusta migratoria on isolated locust malpighian tubules. 1993, Pubmed
Cruz, Invertebrate vasopressin/oxytocin homologs. Characterization of peptides from Conus geographus and Conus straitus venoms. 1987, Pubmed
DU VIGNEAUD, The sequence of amino acids in oxytocin, with a proposal for the structure of oxytocin. 1953, Pubmed
Dale, On some physiological actions of ergot. 1906, Pubmed
Dale, The Action of Extracts of the Pituitary Body. 1909, Pubmed
De Oliveira, Extensive conservation of the proneuropeptide and peptide prohormone complement in mollusks. 2019, Pubmed
Di Giglio, Development of a human vasopressin V1a-receptor antagonist from an evolutionary-related insect neuropeptide. 2017, Pubmed
Dickinson, To what extent may peptide receptor gene diversity/complement contribute to functional flexibility in a simple pattern-generating neural network? 2019, Pubmed
Donaldson, Oxytocin, vasopressin, and the neurogenetics of sociality. 2008, Pubmed
Dubos, Characterization of a tachykinin signalling system in the bivalve mollusc Crassostrea gigas. 2018, Pubmed
Elphick, NGFFFamide and echinotocin: structurally unrelated myoactive neuropeptides derived from neurophysin-containing precursors in sea urchins. 2009, Pubmed , Echinobase
Elphick, NG peptides: a novel family of neurophysin-associated neuropeptides. 2010, Pubmed , Echinobase
Forsling, Diurnal rhythms in neurohypophysial function. 2000, Pubmed
Garrison, Oxytocin/vasopressin-related peptides have an ancient role in reproductive behavior. 2012, Pubmed
Gavilán, The digestive system of xenacoelomorphs. 2019, Pubmed
Gruber, Physiology of invertebrate oxytocin and vasopressin neuropeptides. 2014, Pubmed
Gruber, Discovery of defense- and neuropeptides in social ants by genome-mining. 2012, Pubmed
Gwee, Characterization of the neurohypophysial hormone gene loci in elephant shark and the Japanese lamprey: origin of the vertebrate neurohypophysial hormone genes. 2009, Pubmed
Hasse, Three consecutive generations of nephridia occur during development of Platynereis dumerilii (Annelida, Polychaeta). 2010, Pubmed
Hejnol, Xenacoelomorpha's significance for understanding bilaterian evolution. 2016, Pubmed
Hejnol, Assessing the root of bilaterian animals with scalable phylogenomic methods. 2009, Pubmed
Henry, Identification and expression of two oxytocin/vasopressin-related peptides in the cuttlefish Sepia officinalis. 2013, Pubmed
Howell, THE PHYSIOLOGICAL EFFECTS OF EXTRACTS OF THE HYPOPHYSIS CEREBRI AND INFUNDIBULAR BODY. 1898, Pubmed
In, Reproductive neuropeptides that stimulate spawning in the Sydney Rock Oyster (Saccostrea glomerata). 2016, Pubmed
Jékely, Global view of the evolution and diversity of metazoan neuropeptide signaling. 2013, Pubmed
Jékely, The long and the short of it - a perspective on peptidergic regulation of circuits and behaviour. 2018, Pubmed
Jönsson, Cell Biology of the Tardigrades: Current Knowledge and Perspectives. 2019, Pubmed
Kanda, Single exon structures of the oxytocin/vasopressin superfamily peptides of octopus. 2003, Pubmed
Kanda, Cloning of Octopus cephalotocin receptor, a member of the oxytocin/vasopressin superfamily. 2003, Pubmed
Kanda, Novel evolutionary lineages of the invertebrate oxytocin/vasopressin superfamily peptides and their receptors in the common octopus (Octopus vulgaris). 2005, Pubmed
Kawada, Identification of a novel receptor for an invertebrate oxytocin/vasopressin superfamily peptide: molecular and functional evolution of the oxytocin/vasopressin superfamily. 2004, Pubmed
Kawada, Characterization of a novel vasopressin/oxytocin superfamily peptide and its receptor from an ascidian, Ciona intestinalis. 2008, Pubmed
Koehbach, Insights into the molecular evolution of oxytocin receptor ligand binding. 2013, Pubmed
Koene, Neuro-endocrine control of reproduction in hermaphroditic freshwater snails: mechanisms and evolution. 2010, Pubmed
Koto, Oxytocin/vasopressin-like peptide inotocin regulates cuticular hydrocarbon synthesis and water balancing in ants. 2019, Pubmed
Koziol, Precursors of neuropeptides and peptide hormones in the genomes of tardigrades. 2018, Pubmed
Lagman, The vertebrate ancestral repertoire of visual opsins, transducin alpha subunits and oxytocin/vasopressin receptors was established by duplication of their shared genomic region in the two rounds of early vertebrate genome duplications. 2013, Pubmed
Leng, The osmoresponsiveness of oxytocin and vasopressin neurones: Mechanisms, allostasis and evolution. 2019, Pubmed
Li, Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. 2008, Pubmed
Lin, CRISPR/Cas9-mediated genome editing in sea urchins. 2019, Pubmed , Echinobase
Lin, Cellular localization of relaxin-like gonad-stimulating peptide expression in Asterias rubens: New insights into neurohormonal control of spawning in starfish. 2017, Pubmed , Echinobase
Liutkeviciute, Global map of oxytocin/vasopressin-like neuropeptide signalling in insects. 2016, Pubmed
Liutkevičiūtė, Oxytocin-like signaling in ants influences metabolic gene expression and locomotor activity. 2018, Pubmed
Lockard, Oxytocin mediated behavior in invertebrates: An evolutionary perspective. 2017, Pubmed
Lukowiak, Vasopressin increases the central nervous system suppressive control over gill reflex behaviours and associated neural activity in Aplysia. 1980, Pubmed
Makki, The development and functions of oenocytes. 2014, Pubmed
Marder, Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. 2007, Pubmed
Marks, Neuropeptides in helminths: occurrence and distribution. 2010, Pubmed
Martinez-Padrón, Localization of vasopressin-like immunoreactivity in the CNS of Aplysia californica. 1992, Pubmed
Martínez-Padrón, Conopressin G, a molluscan vasopressin-like peptide, alters gill behaviors in Aplysia. 1992, Pubmed
Matsubara, The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates. 2019, Pubmed
Mayorova, Localization of Neuropeptide Gene Expression in Larvae of an Echinoderm, the Starfish Asterias rubens. 2016, Pubmed , Echinobase
McVeigh, Parasite neuropeptide biology: Seeding rational drug target selection? 2012, Pubmed
McVeigh, Neuropeptide signalling systems in flatworms. 2005, Pubmed
Mennigen, The nonapeptide isotocin in goldfish: Evidence for serotonergic regulation and functional roles in the control of food intake and pituitary hormone release. 2017, Pubmed
Minakata, Oxytocin/vasopressin and gonadotropin-releasing hormone from cephalopods to vertebrates. 2010, Pubmed
Mirabeau, Molecular evolution of peptidergic signaling systems in bilaterians. 2013, Pubmed
Mita, A relaxin-like peptide purified from radial nerves induces oocyte maturation and ovulation in the starfish, Asterina pectinifera. 2009, Pubmed , Echinobase
Mizuno, Phylogenetic study of the arginine-vasotocin/arginine-vasopressin-like immunoreactive system in invertebrates. 1988, Pubmed , Echinobase
Moore, An arginine vasotocin-like neuropeptide is present in the nervous system of the marine mollusc Aplysia californica. 1981, Pubmed
Mousley, Neuropeptide physiology in helminths. 2010, Pubmed
Ocampo Daza, The oxytocin/vasopressin receptor family has at least five members in the gnathostome lineage, inclucing two distinct V2 subtypes. 2012, Pubmed
Odekunle, Ancient role of vasopressin/oxytocin-type neuropeptides as regulators of feeding revealed in an echinoderm. 2019, Pubmed , Echinobase
Oliphant, Transcriptomic analysis of crustacean neuropeptide signaling during the moult cycle in the green shore crab, Carcinus maenas. 2018, Pubmed
Oliver, On the Physiological Action of Extracts of Pituitary Body and certain other Glandular Organs: Preliminary Communication. 1895, Pubmed
Oumi, Annetocin: an oxytocin-related peptide isolated from the earthworm, Eisenia foetida. 1994, Pubmed
Oumi, Annetocin, an annelid oxytocin-related peptide, induces egg-laying behavior in the earthworm, Eisenia foetida. 1996, Pubmed
Pani, Ancient deuterostome origins of vertebrate brain signalling centres. 2012, Pubmed
Philippe, Acoelomorph flatworms are deuterostomes related to Xenoturbella. 2011, Pubmed , Echinobase
Philippe, Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria. 2019, Pubmed , Echinobase
Proux, Identification of an arginine vasopressin-like diuretic hormone from Locusta migratoria. 1987, Pubmed
Proux, Evidence of vasopressin-like molecule in migratory locust. Radioimmunological measurements in different tissues: correlation with various states of hydration. 1980, Pubmed
Proux, Enhancement of excretion across locust malpighian tubules by a diuretic vasopressin-like hormone. 1982, Pubmed
Reich, A new peptide of the oxytocin/vasopressin family isolated from nerves of the cephalopod Octopus vulgaris. 1992, Pubmed
Richards, The genome of the model beetle and pest Tribolium castaneum. 2008, Pubmed
Rémy, Vertebrate neuropeptide-like substances in the suboesophageal ganglion of two insects: Locusta migratoria R. and F. (Orthoptera) and Bombyx mori L. (Lepidoptera). Immunocytological investigation. 1979, Pubmed
Saetan, Molecular cloning and distribution of oxytocin/vasopressin-like mRNA in the blue swimming crab, Portunus pelagicus, and its inhibitory effect on ovarian steroid release. 2018, Pubmed
Sakamoto, Osmotic/ionic status of body fluids in the euryhaline cephalopod suggest possible parallel evolution of osmoregulation. 2015, Pubmed
Salzet, Isolation, structural characterization and biological function of a lysine-conopressin in the central nervous system of the pharyngobdellid leech Erpobdella octoculata. 1993, Pubmed
Satake, Evidence for conservation of the vasopressin/oxytocin superfamily in Annelida. 1999, Pubmed
Sawyer, Evolution of neurohypophyseal hormones and their receptors. 1977, Pubmed
Sawyer, Immunological and biological characteristics of the vasotocin-like activity in the head ganglia of gastropod molluscs. 1984, Pubmed
Schot, Immunocytochemical demonstration of peptidergic neurons in the central nervous system of the pond snail Lymnaea stagnalis with antisera raised to biologically active peptides of vertebrates. 1981, Pubmed
Scott, An oxytocin-dependent social interaction between larvae and adult C. elegans. 2017, Pubmed
Semmens, Transcriptomic identification of starfish neuropeptide precursors yields new insights into neuropeptide evolution. 2016, Pubmed , Echinobase
Simakov, Hemichordate genomes and deuterostome origins. 2015, Pubmed , Echinobase
Smith, The neuropeptidome of the Crown-of-Thorns Starfish, Acanthaster planci. 2017, Pubmed , Echinobase
Sodergren, The genome of the sea urchin Strongylocentrotus purpuratus. 2006, Pubmed , Echinobase
Stafflinger, Cloning and identification of an oxytocin/vasopressin-like receptor and its ligand from insects. 2008, Pubmed
Stewart, Neuropeptides encoded by the genomes of the Akoya pearl oyster Pinctata fucata and Pacific oyster Crassostrea gigas: a bioinformatic and peptidomic survey. 2014, Pubmed
Suwansa-Ard, Transcriptomic discovery and comparative analysis of neuropeptide precursors in sea cucumbers (Holothuroidea). 2018, Pubmed , Echinobase
TUPPY, The amino-acid sequence in oxytocin. 1953, Pubmed
TURNER, The purification and the amino acid content of vasopressin preparations. 1951, Pubmed
Takahama, Immunohistochemical Localization of Annetocin, an Earthworm Oxytocin-Related Peptide, and Identification and Ultrastructural Characteristics of the Annetocin-Secretory Cells in the Oligochaete Earthworm Eisenia foetida. 1998, Pubmed
Takuwa-Kuroda, Octopus, which owns the most advanced brain in invertebrates, has two members of vasopressin/oxytocin superfamily as in vertebrates. 2003, Pubmed
Telford, Phylogenomic analysis of echinoderm class relationships supports Asterozoa. 2014, Pubmed , Echinobase
Telford, Zoology: War of the Worms. 2016, Pubmed
Tessmar-Raible, Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. 2007, Pubmed
Thompson, The vasopressin-like immunoreactive (VPLI) neurons of the locust, Locusta migratoria. I. Anatomy. 1991, Pubmed
Thompson, The vasopressin-like immunoreactive (VPLI) neurons of the locust, Locusta migratoria. II. Physiology. 1991, Pubmed
Thornhill, Arginine vasotocin, an endogenous neuropeptide of Aplysia, suppresses the gill withdrawal reflex and reduces the evoked synaptic input to central gill motor neurons. 1981, Pubmed
Tyrer, Morphology of the vasopressin-like immunoreactive (VPLI) neurons in many species of grasshopper. 1993, Pubmed
Ukena, Unique form and osmoregulatory function of a neurohypophysial hormone in a urochordate. 2008, Pubmed
Van Kesteren, Structural and functional evolution of the vasopressin/oxytocin superfamily: vasopressin-related conopressin is the only member present in Lymnaea, and is involved in the control of sexual behavior. 1995, Pubmed
Veenstra, The contribution of the genomes of a termite and a locust to our understanding of insect neuropeptides and neurohormones. 2014, Pubmed
Wagenaar, A hormone-activated central pattern generator for courtship. 2010, Pubmed
Williams, Synaptic and peptidergic connectome of a neurosecretory center in the annelid brain. 2017, Pubmed
Williams, Neuronal cell types in the annelid Platynereis dumerilii. 2019, Pubmed
Wood, Neuropeptidergic Systems in Pluteus Larvae of the Sea Urchin Strongylocentrotus purpuratus: Neurochemical Complexity in a "Simple" Nervous System. 2018, Pubmed , Echinobase
Yao, Cis-regulatory architecture of a brain signaling center predates the origin of chordates. 2016, Pubmed
Zandawala, Discovery of novel representatives of bilaterian neuropeptide families and reconstruction of neuropeptide precursor evolution in ophiuroid echinoderms. 2017, Pubmed , Echinobase
de Bree, Structure-function relationships of the vasopressin prohormone domains. 1998, Pubmed
van Kesteren, A novel G protein-coupled receptor mediating both vasopressin- and oxytocin-like functions of Lys-conopressin in Lymnaea stagnalis. 1995, Pubmed
van Kesteren, Evolution of the vasopressin/oxytocin superfamily: characterization of a cDNA encoding a vasopressin-related precursor, preproconopressin, from the mollusc Lymnaea stagnalis. 1992, Pubmed
van Kesteren, A vasopressin-related peptide in the mollusc Lymnaea stagnalis: peptide structure, prohormone organization, evolutionary and functional aspects of Lymnaea conopressin. 1992, Pubmed