Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Feb 15;91(4):1342–1345. doi: 10.1073/pnas.91.4.1342

Structure, function, and phylogeny of [Arg8]vasotocin receptors from teleost fish and toad.

S Mahlmann 1, W Meyerhof 1, H Hausmann 1, J Heierhorst 1, C Schönrock 1, H Zwiers 1, K Lederis 1, D Richter 1
PMCID: PMC43154  PMID: 7509069

Abstract

[Arg8]Vasotocin (AVT) is considered to be the most primitive known vertebrate neurohypophyseal peptide of the vasopressin/oxytocin hormone family and may thus be ancestral to all the other vertebrate peptide hormones. The molecular evolution of the corresponding receptor family has now been studied by cloning an AVT receptor, consisting of 435 amino acid residues, from the teleost fish, the white sucker Catostomus commersoni. Frog oocytes injected with the AVT receptor-encoding cRNA respond to the application of AVT, but not to its structural and functional counterpart isotocin, by an induction of membrane chloride currents indicating the coupling of the AVT receptor to the inositol phosphate/calcium pathway. The pharmacological properties of the expressed AVT receptor show that it represents, or is closely related to, an ancestral nonapeptide receptor: oxytocin, aspargtocin, mesotocin, and vasopressin activated the receptor, but other members of the vasopressin/oxytocin family tested showed little or no potency; antagonists of the mammalian vasopressin V1 and oxytocin receptors blocked the AVT response. Comparison of AVT receptor sequences spanning transmembrane domains two to five, deduced by cloning cDNAs from the Pacific salmon Oncorhynchus kisutch, the cave-dwelling fish Astyanax fasciatus, and the anuran Xenopus laevis, with those of their mammalian counterparts emphasizes amino acid residues that are involved in hormone binding. The presence of a 5.0-kb transcript in various teleost tissues (pituitary, liver, gills, swim bladder, and lateral line) points to a physiological role for the fish AVT receptor in metabolic, osmoregulatory, and sensory processes.

Full text

PDF
1342

Images in this article

1345Image
on p.1345

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Acher R. Molecular evolution of biologically active polypeptides. Proc R Soc Lond B Biol Sci. 1980 Oct 29;210(1178):21–43. doi: 10.1098/rspb.1980.0116. [DOI] [PubMed] [Google Scholar]
  2. Birnbaumer M., Seibold A., Gilbert S., Ishido M., Barberis C., Antaramian A., Brabet P., Rosenthal W. Molecular cloning of the receptor for human antidiuretic hormone. Nature. 1992 May 28;357(6376):333–335. doi: 10.1038/357333a0. [DOI] [PubMed] [Google Scholar]
  3. Burgess W. H., Dionne C. A., Kaplow J., Mudd R., Friesel R., Zilberstein A., Schlessinger J., Jaye M. Characterization and cDNA cloning of phospholipase C-gamma, a major substrate for heparin-binding growth factor 1 (acidic fibroblast growth factor)-activated tyrosine kinase. Mol Cell Biol. 1990 Sep;10(9):4770–4777. doi: 10.1128/mcb.10.9.4770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carattoli A., Romano N., Ballario P., Morelli G., Macino G. The Neurospora crassa carotenoid biosynthetic gene (albino 3) reveals highly conserved regions among prenyltransferases. J Biol Chem. 1991 Mar 25;266(9):5854–5859. [PubMed] [Google Scholar]
  5. Charles C. H., Abler A. S., Lau L. F. cDNA sequence of a growth factor-inducible immediate early gene and characterization of its encoded protein. Oncogene. 1992 Jan;7(1):187–190. [PubMed] [Google Scholar]
  6. Cunningham E. T., Jr, Sawchenko P. E. Reflex control of magnocellular vasopressin and oxytocin secretion. Trends Neurosci. 1991 Sep;14(9):406–411. doi: 10.1016/0166-2236(91)90032-p. [DOI] [PubMed] [Google Scholar]
  7. Elands J., Barberis C., Jard S., Tribollet E., Dreifuss J. J., Bankowski K., Manning M., Sawyer W. H. 125I-labelled d(CH2)5[Tyr(Me)2,Thr4,Tyr-NH2(9)]OVT: a selective oxytocin receptor ligand. Eur J Pharmacol. 1988 Mar 1;147(2):197–207. doi: 10.1016/0014-2999(88)90778-9. [DOI] [PubMed] [Google Scholar]
  8. Heierhorst J., Morley S. D., Figueroa J., Krentler C., Lederis K., Richter D. Vasotocin and isotocin precursors from the white sucker, Catostomus commersoni: cloning and sequence analysis of the cDNAs. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5242–5246. doi: 10.1073/pnas.86.14.5242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kemp B. E., Pearson R. B. Protein kinase recognition sequence motifs. Trends Biochem Sci. 1990 Sep;15(9):342–346. doi: 10.1016/0968-0004(90)90073-k. [DOI] [PubMed] [Google Scholar]
  10. Kimura T., Tanizawa O., Mori K., Brownstein M. J., Okayama H. Structure and expression of a human oxytocin receptor. Nature. 1992 Apr 9;356(6369):526–529. doi: 10.1038/356526a0. [DOI] [PubMed] [Google Scholar]
  11. Lane T. F., Sower S. A., Kawauchi H. Arginine vasotocin from the pituitary gland of the lamprey (Petromyzon marinus): isolation and amino acid sequence. Gen Comp Endocrinol. 1988 Apr;70(1):152–157. doi: 10.1016/0016-6480(88)90104-9. [DOI] [PubMed] [Google Scholar]
  12. Lolait S. J., O'Carroll A. M., McBride O. W., Konig M., Morel A., Brownstein M. J. Cloning and characterization of a vasopressin V2 receptor and possible link to nephrogenic diabetes insipidus. Nature. 1992 May 28;357(6376):336–339. doi: 10.1038/357336a0. [DOI] [PubMed] [Google Scholar]
  13. Meyerhof W., Morley S., Schwarz J., Richter D. Receptors for neuropeptides are induced by exogenous poly(A)+ RNA in oocytes from Xenopus laevis. Proc Natl Acad Sci U S A. 1988 Feb;85(3):714–717. doi: 10.1073/pnas.85.3.714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Morel A., O'Carroll A. M., Brownstein M. J., Lolait S. J. Molecular cloning and expression of a rat V1a arginine vasopressin receptor. Nature. 1992 Apr 9;356(6369):523–526. doi: 10.1038/356523a0. [DOI] [PubMed] [Google Scholar]
  15. Nozaki M., Gorbman A. Immunocytochemical localization of somatostatin and vasotocin in the brain of the Pacific hagfish, Eptatretus stouti. Cell Tissue Res. 1983;229(3):541–550. doi: 10.1007/BF00207697. [DOI] [PubMed] [Google Scholar]
  16. Proux J. P., Miller C. A., Li J. P., Carney R. L., Girardie A., Delaage M., Schooley D. A. Identification of an arginine vasopressin-like diuretic hormone from Locusta migratoria. Biochem Biophys Res Commun. 1987 Nov 30;149(1):180–186. doi: 10.1016/0006-291x(87)91621-4. [DOI] [PubMed] [Google Scholar]
  17. Rouillé Y., Michel G., Chauvet M. T., Chauvet J., Acher R. Hydrins, hydroosmotic neurohypophysial peptides: osmoregulatory adaptation in amphibians through vasotocin precursor processing. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5272–5275. doi: 10.1073/pnas.86.14.5272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rurak D. W., Perks A. M. The pharmacological characterization of arginine vasotocin in the pituitary of the pacific hagfish (Polistotrema stoutii). Gen Comp Endocrinol. 1974 Apr;22(4):480–488. doi: 10.1016/0016-6480(74)90024-0. [DOI] [PubMed] [Google Scholar]
  19. Sawyer W. H., Grzonka Z., Manning M. Neurohypophysial peptides. Design of tissue-specific agonists and antagonists. Mol Cell Endocrinol. 1981 May;22(2):117–134. doi: 10.1016/0303-7207(81)90086-1. [DOI] [PubMed] [Google Scholar]
  20. Sharif M., Hanley M. R. Peptide receptors. Stepping up the pressure. Nature. 1992 May 28;357(6376):279–280. doi: 10.1038/357279a0. [DOI] [PubMed] [Google Scholar]
  21. Woodgett J. R., Gould K. L., Hunter T. Substrate specificity of protein kinase C. Use of synthetic peptides corresponding to physiological sites as probes for substrate recognition requirements. Eur J Biochem. 1986 Nov 17;161(1):177–184. doi: 10.1111/j.1432-1033.1986.tb10139.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES