Skip to main content
NCBI 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 May 24;91(11):4912–4914. doi: 10.1073/pnas.91.11.4912

The calcitonin gene is expressed in salmon gills.

K Martial 1, L Maubras 1, J Taboulet 1, A Jullienne 1, M Berry 1, G Milhaud 1, A A Benson 1, M S Moukhtar 1, M Cressent 1
PMCID: PMC43899  PMID: 8197156

Abstract

Calcitonin is an important physiological regulator of salmon gills. Although the calcitonin receptor was found in salmon gills, the critical question concerning the source of the hormone remained unanswered. In this communication, evidence is presented for expression of calcitonin mRNA and its encoded peptide in gills of the pink salmon, Oncorhynchus gorbuscha. The expression of calcitonin gene transcripts was demonstrated by reverse transcription-polymerase chain reaction, Southern hybridization, and sequencing. The sequencing identified a sequence corresponding to that of exon 4 of the salmon calcitonin gene. Expression of the encoded calcitonin gene in gills was detected by radioimmunoassay in gill extracts. This synthesis of calcitonin in gills, which also possess specific receptors to the peptide, suggests function of an autocrine or paracrine process producing calcitonin in this tissue. These observations confirm and extend previous reports on the physiological role of calcitonin in fish gills.

Full text

PDF
4912

Images in this article

4913Image
on p.4913
4913Image
on p.4913

Selected References

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

  1. Amara S. G., Jonas V., Rosenfeld M. G., Ong E. S., Evans R. M. Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature. 1982 Jul 15;298(5871):240–244. doi: 10.1038/298240a0. [DOI] [PubMed] [Google Scholar]
  2. Arlot-Bonnemains Y., Fouchereau-Peron M., Moukhtar M. S., Milhaud G. Characterization of target organs for calcitonin in lower and higher vertebrates. Comp Biochem Physiol A Comp Physiol. 1983;76(2):377–380. doi: 10.1016/0300-9629(83)90340-7. [DOI] [PubMed] [Google Scholar]
  3. COPP D. H., CAMERON E. C., CHENEY B. A., DAVIDSON A. G., HENZE K. G. Evidence for calcitonin--a new hormone from the parathyroid that lowers blood calcium. Endocrinology. 1962 May;70:638–649. doi: 10.1210/endo-70-5-638. [DOI] [PubMed] [Google Scholar]
  4. Chan D. K., Jones I. C., Smith R. N. The effect of mammalian calcitonin on the plasma levels of calcium and inorganic phosphate in the European eel (Anguilla anguilla L). Gen Comp Endocrinol. 1968 Aug;11(1):243–245. doi: 10.1016/0016-6480(68)90123-8. [DOI] [PubMed] [Google Scholar]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. Copp D. H., Cockcroft D. W., Kueh Y. Calcitonin from ultimobranchial glands of dogfish and chickens. Science. 1967 Nov 17;158(3803):924–925. doi: 10.1126/science.158.3803.924. [DOI] [PubMed] [Google Scholar]
  7. FOSTER G. V., MACINTYRE I., PEARSE A. G. CALCITONIN PRODUCTION AND THE MITOCHONDRION-RICH CELLS OF THE DOG THYROID. Nature. 1964 Sep 5;203:1029–1030. doi: 10.1038/2031029a0. [DOI] [PubMed] [Google Scholar]
  8. Fouchereau-Peron M., Arlot-Bonnemains Y., Maubras L., Milhaud G., Moukhtar M. S. Calcitonin variations in male and female trout, Salmo gairdneri, during the annual cycle. Gen Comp Endocrinol. 1990 May;78(2):159–163. doi: 10.1016/0016-6480(90)90001-3. [DOI] [PubMed] [Google Scholar]
  9. Fouchereau-Peron M., Arlot-Bonnemains Y., Taboulet J., Milhaud G., Moukhtar M. S. Distribution of calcitonin gene-related peptide and calcitonin-like immunoreactivity in trout. Regul Pept. 1990 Feb 4;27(2):171–179. doi: 10.1016/0167-0115(90)90037-w. [DOI] [PubMed] [Google Scholar]
  10. Jansz H. S., Zandberg J. Identification and partial characterization of the salmon calcitonin/CGRP gene by polymerase chain reaction. Ann N Y Acad Sci. 1992 Jun 30;657:63–69. doi: 10.1111/j.1749-6632.1992.tb22757.x. [DOI] [PubMed] [Google Scholar]
  11. Lausson S., Tracqui P., Toubiana L., Milhaud G., Perault-Staub A. M., Staub J. F. Regulation of plasma calcium and phosphate in calcitonin-infused rats. Am J Physiol. 1990 Sep;259(3 Pt 1):E370–E377. doi: 10.1152/ajpendo.1990.259.3.E370. [DOI] [PubMed] [Google Scholar]
  12. Maubras L., Cressent M., Minvielle S., Taboulet J., Jullienne A., Milhaud G., Moukhtar M. S. Expression of the calcitonin gene during migration of the Pacific salmon, Oncorhynchus gorbuscha. Biochem Biophys Res Commun. 1990 Dec 31;173(3):788–794. doi: 10.1016/s0006-291x(05)80856-3. [DOI] [PubMed] [Google Scholar]
  13. Maubras L., Taboulet J., Pidoux E., Lasmoles F., Julienne A., Milhaud G., Benson A. A., Moukhtar M. S., Cressent M. Expression of CGRP mRNAs in the pink salmon, Oncorhynchus gorbuscha. Peptides. 1993 Sep-Oct;14(5):977–981. doi: 10.1016/0196-9781(93)90074-q. [DOI] [PubMed] [Google Scholar]
  14. Milhaud G., Bolis L., Benson A. A. Calcitonin, a major gill hormone. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6935–6936. doi: 10.1073/pnas.77.11.6935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Milhaud G., Rankin J. C., Bolis L., Benson A. A. Calcitonin: Its hormonal action on the gill. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4693–4696. doi: 10.1073/pnas.74.10.4693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Minvielle S., Cressent M., Delehaye M. C., Segond N., Milhaud G., Jullienne A., Moukhtar M. S., Lasmoles F. Sequence and expression of the chicken calcitonin gene. FEBS Lett. 1987 Oct 19;223(1):63–68. doi: 10.1016/0014-5793(87)80510-0. [DOI] [PubMed] [Google Scholar]
  17. Pang P. K. Calcitonin and ultimobranchial glands in fishes. J Exp Zool. 1971 Sep;178(1):89–99. doi: 10.1002/jez.1401780111. [DOI] [PubMed] [Google Scholar]
  18. Pöschl E., Lindley I., Hofer E., Seifert J. M., Brunowsky W., Besemer J. The structure of procalcitonin of the salmon as deduced from its cDNA sequence. FEBS Lett. 1987 Dec 21;226(1):96–100. doi: 10.1016/0014-5793(87)80558-6. [DOI] [PubMed] [Google Scholar]
  19. Rosenfeld M. G., Mermod J. J., Amara S. G., Swanson L. W., Sawchenko P. E., Rivier J., Vale W. W., Evans R. M. Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature. 1983 Jul 14;304(5922):129–135. doi: 10.1038/304129a0. [DOI] [PubMed] [Google Scholar]
  20. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Steenbergh P. H., Höppener J. W., Zandberg J., Van de Ven W. J., Jansz H. S., Lips C. J. Calcitonin gene related peptide coding sequence is conserved in the human genome and is expressed in medullary thyroid carcinoma. J Clin Endocrinol Metab. 1984 Aug;59(2):358–360. doi: 10.1210/jcem-59-2-358. [DOI] [PubMed] [Google Scholar]
  22. Treilhou-Lahille F., Jullienne A., Aziz M., Beaumont A., Moukhtar M. S. Ultrastructural localization of immunoreactive calcitonin in the two cell types of the ultimobranchial gland of the common toad (Bufo bufo L.). Gen Comp Endocrinol. 1984 Feb;53(2):241–251. doi: 10.1016/0016-6480(84)90249-1. [DOI] [PubMed] [Google Scholar]
  23. Watts E. G., Copp D. H., Deftos L. J. Changes in plasma calcitonin and calcium during the migration of salmon. Endocrinology. 1975 Jan;96(1):214–218. doi: 10.1210/endo-96-1-214. [DOI] [PubMed] [Google Scholar]
  24. Yamauchi H., Matsuo M., Yoshida A., Orimo H. Effect of eel calcitonin on serum electrolytes in the eel Anguilla japonica. Gen Comp Endocrinol. 1978 Mar;34(3):343–346. doi: 10.1016/0016-6480(78)90258-7. [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