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

It has been suggested that the gene duplication that led to the formation of the vasopressin/oxytocin two-gene family occurred early during vertebrate evolution. However, the existence of both vasopressin- and oxytocin-related peptides in invertebrates suggests that this duplication may have occurred much earlier, although there is no evidence for the co-occurrence of vasopressin- and oxytocin-related peptides in the same invertebrate species. We report here that in Lymnaea only the vasopressin-related peptide Lys-conopressin, but not an oxytocin-related peptide, is present. Moreover, it is very likely that an oxytocin-like cDNA or gene is absent. The conopressin gene is expressed in neurons that control male sexual behavior, and its gene products are present in the penis nerve and the vas deferens. Conopressin induces muscular contractions of the vas deferens and inhibits central neurons that control female reproductive behavior. Thus, although structurally related to vasopressin, conopressin has functional and behavioral characteristics typical for oxytocin. Physiological and receptor binding data suggest that conopressin and [Ile8]-conopressin, a synthetic oxytocin-like analog of conopressin, are functionally equivalent in Lymnaea, and that the chemical nature of the amino acid residue at position 8 does not result in a functional difference. Therefore, we suggest that invertebrates contain only a single member of the vasopressin/oxytocin gene family and that the amino acid change that distinguishes vasopressin from oxytocin is functionally neutral in invertebrates.

[1]  W. Geraerts,et al.  Identification of a novel amide peptide, GLTPNMNSLFF-NH2, involved in the control of vas deferens motility in lymnaea stagnalis. , 1995, European journal of biochemistry.

[2]  M. Brown,et al.  cDNA Cloning of MCT2, a Second Monocarboxylate Transporter Expressed in Different Cells than MCT1 (*) , 1995, The Journal of Biological Chemistry.

[3]  H. Minakata,et al.  Annetocin: an oxytocin-related peptide isolated from the earthworm, Eisenia foetida. , 1994, Biochemical and biophysical research communications.

[4]  A. van Dorsselaer,et al.  Isolation, structural characterization and biological function of a lysine-conopressin in the central nervous system of the pharyngobdellid leech Erpobdella octoculata. , 1993, European journal of biochemistry.

[5]  R. Acher.  Neurohypophysial peptide systems: processing machinery, hydroosmotic regulation, adaptation and evolution , 1993, Regulatory Peptides.

[6]  A. Lasham,et al.  Direct sequencing of lambda DNA from crude lysates using an improved linear amplification technique. , 1993, Molecular and cellular probes.

[7]  J. Heierhorst,et al.  Presence of a member of the Tc1-like transposon family from nematodes and Drosophila within the vasotocin gene of a primitive vertebrate, the Pacific hagfish Eptatretus stouti. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. van Kesteren,et al.  Evolution of the vasopressin/oxytocin superfamily: characterization of a cDNA encoding a vasopressin-related precursor, preproconopressin, from the mollusc Lymnaea stagnalis. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[9]  A. Smit,et al.  Characterization of a cDNA clone encoding multiple copies of the neuropeptide APGWamide in the mollusk Lymnaea stagnalis , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  K. Lederis,et al.  A vasotocin-like peptide in Aplysia kurodai ganglia: HPLC and RIA evidence for its identity with Lys-conopressin G , 1992, Peptides.

[11]  J. Haefliger,et al.  Four novel members of the connexin family of gap junction proteins. Molecular cloning, expression, and chromosome mapping. , 1992, The Journal of biological chemistry.

[12]  G. Reich.  A new peptide of the oxytocin/vasopressin family isolated from nerves of the cephalopod Octopus vulgaris , 1992, Neuroscience Letters.

[13]  J. Battey,et al.  Structure of mouse vasopressin and oxytocin genes. , 1990, Brain research. Molecular brain research.

[14]  J. Heierhorst,et al.  Vasotocin genes of the teleost fish Catostomus commersoni: gene structure, exon-intron boundary, and hormone precursor organization. , 1990, Biochemistry.

[15]  E. Vreugdenhil,et al.  Expression of the egg-laying hormone genes in peripheral neurons and exocrine cells in the reproductive tract of the mollusc Lymnaea stagnalis , 1989, Neuroscience.

[16]  W. Geraerts,et al.  Dot immunobinding assay of high-performance liquid chromatographic fractions on poly(vinylidene difluoride) membranes. , 1989, Journal of chromatography.

[17]  T. Bouwmeester,et al.  Isolation, characterization, and evolutionary aspects of a cDNA clone encoding multiple neuropeptides involved in the stereotyped egg-laying behavior of the freshwater snail Lymnaea stagnalis , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  H. Kawauchi,et al.  Arginine vasotocin from the pituitary gland of the lamprey (Petromyzon marinus): isolation and amino acid sequence. , 1988, General and comparative endocrinology.

[19]  D. Schooley,et al.  Identification of an arginine vasopressin-like diuretic hormone from Locusta migratoria. , 1987, Biochemical and biophysical research communications.

[20]  S. Checkley,et al.  Changes in oxytocin and vasopressin secretion during sexual activity in men. , 1987, The Journal of clinical endocrinology and metabolism.

[21]  J. Burbach,et al.  Characterization of vasopressin and oxytocin immunoreactivity in the sheep and rat pineal gland: Absence of vasotocin and detection of a vasopressin-like peptide , 1987, Peptides.

[22]  S. Lightman,et al.  Oxytocin release during coitus in male and female rabbits: effect of opiate receptor blockade with naloxone , 1986, Psychoneuroendocrinology.

[23]  J. Battey,et al.  The human vasopressin gene is linked to the oxytocin gene and is selectively expressed in a cultured lung cancer cell line. , 1985, The Journal of biological chemistry.

[24]  G. Schütz,et al.  Recent gene conversion involving bovine vasopressin and oxytocin precursor genes suggested by nucleotide sequence , 1984, Nature.

[25]  R. Ivell,et al.  Structure and comparison of the oxytocin and vasopressin genes from rat. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[26]  G. Schütz,et al.  Deduced amino acid sequence from the bovine oxytocin–neurophysin I precursor cDNA , 1983, Nature.

[27]  D. Richter,et al.  Structural organization of the rat gene for the arginine vasopressin‐neurophysin precursor. , 1983, The EMBO journal.

[28]  R. Acher.  Molecular evolution of biologically active polypeptides , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[29]  K. Kits.  States of excitability in ovulation hormone producing neuroendocrine cells of Lymnaea stagnalis (gastropoda) and their relation to the egg-laying cycle. , 1980, Journal of neurobiology.

[30]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[31]  D. Swaab,et al.  Specificity of oxytocin and vasopressin immunofluorescence. , 1975, The Journal of endocrinology.

[32]  T. Chard.  THE POSTERIOR PITUITARY GLAND , 1975, Lancet.

[33]  H. Gainer,et al.  Peptide Regulation of Bursting Pacemaker Activity in a Molluscan Neurosecretory Cell , 1974, Science.

[34]  É. Barraud.  The copulatory behaviour of the freshwater snail (Limnaea stagnalis L.) , 1957 .

[35]  A. Smit,et al.  Neuropeptide Gene Families that Control Reproductive Behaviour and Growth in Molluscs , 1991 .

[36]  H. Sambrook.  Molecular cloning : a laboratory manual. Cold Spring Harbor, NY , 1989 .