Abstract
Three isoforms of calcitonin (CT) exist in salmonids. Isohormones I and II are expressed in the pink salmon Oncorhynchus gorbuscha. We report here the existence in this species of a CT gene and of its transcripts, which encode for a fourth isohormone, the salmon CT (sCT) IV. This new CT gene was identified by PCR from genomic DNA and by sequencing the amplified DNA. The expression of this CT gene was established in ultimobranchial body and brain, by reverse transcription-PCR, hybridization and sequencing. The sCT IV gene, like the sCT I gene, is a complex transcription unit, containing exons encoding for a CT as a calcitonin gene-related peptide (CGRP) molecule. The predicted peptide, sCT IV, has a greater homology with the eel CT and the sCT II than with the sCT I. Alignment of the sCT IV with other fish and chicken CT showed amino acid modifications in similar positions as those found during evolution. The predicted salmon CGRP IV peptide is highly homologous to the known CGRP molecules in other species, confirming the high conservation of the molecule during evolution. This identification of a new salmon CT gene is interesting both for the therapeutic potential represented by the new molecules encoded by this gene and for phylogenetic studies.
Full text
PDF




Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alevizaki M., Shiraishi A., Rassool F. V., Ferrier G. J., MacIntyre I., Legon S. The calcitonin-like sequence of the beta CGRP gene. FEBS Lett. 1986 Sep 29;206(1):47–52. doi: 10.1016/0014-5793(86)81338-2. [DOI] [PubMed] [Google Scholar]
- Amara S. G., Arriza J. L., Leff S. E., Swanson L. W., Evans R. M., Rosenfeld M. G. Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide. Science. 1985 Sep 13;229(4718):1094–1097. doi: 10.1126/science.2994212. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Conlon J. M., Tonon M. C., Vaudry H. Isolation and structural characterization of calcitonin gene-related peptide from the brain and intestine of the frog, Rana ridibunda. Peptides. 1993 May-Jun;14(3):581–586. doi: 10.1016/0196-9781(93)90148-a. [DOI] [PubMed] [Google Scholar]
- Fischer J. A., Tobler P. H., Henke H., Tschopp F. A. Salmon and human calcitonin-like peptides coexist in the human thyroid and brain. J Clin Endocrinol Metab. 1983 Dec;57(6):1314–1316. doi: 10.1210/jcem-57-6-1314. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Kanehisa M. Use of statistical criteria for screening potential homologies in nucleic acid sequences. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):203–213. doi: 10.1093/nar/12.1part1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lasmoles F., Jullienne A., Desplan C., Milhaud G., Moukhtar M. S. Structure of chicken calcitonin predicted by partial nucleotide sequence of its precursor. FEBS Lett. 1985 Jan 21;180(1):113–116. doi: 10.1016/0014-5793(85)80242-8. [DOI] [PubMed] [Google Scholar]
- Martial K., Maubras L., Taboulet J., Jullienne A., Berry M., Milhaud G., Benson A. A., Moukhtar M. S., Cressent M. The calcitonin gene is expressed in salmon gills. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4912–4914. doi: 10.1073/pnas.91.11.4912. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martial K., Maubras L., Taboulet J., Jullienne A., Milhaud G., Moukhtar M. S., Cressent M. Production of salmon calcitonin I in Oncorhynchus gorbuscha by alternative polyadenylation of two RNA species. Gene. 1994 Nov 18;149(2):277–281. doi: 10.1016/0378-1119(94)90161-9. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Niall H. D., Keutmann H. T., Copp D. H., Potts J. T., Jr Amino acid sequence of salmon ultimobranchial calcitonin. Proc Natl Acad Sci U S A. 1969 Oct;64(2):771–778. doi: 10.1073/pnas.64.2.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Otani M., Yamauchi H., Meguro T., Kitazawa S., Watanabe S., Orimo H. Isolation and characterization of calcitonin from pericardium and esophagus of eel. J Biochem. 1976 Feb;79(2):345–352. doi: 10.1093/oxfordjournals.jbchem.a131077. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
- 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]
- Sasayama Y., Ukawa K., Kai-Ya H., Oguro C., Takei Y., Watanabe T. X., Nakajima K., Sakakibara S. Goldfish calcitonin: purification, characterization, and hypocalcemic potency. Gen Comp Endocrinol. 1993 Feb;89(2):189–194. doi: 10.1006/gcen.1993.1023. [DOI] [PubMed] [Google Scholar]
- Steenbergh P. H., Höppener J. W., Zandberg J., Lips C. J., Jansz H. S. A second human calcitonin/CGRP gene. FEBS Lett. 1985 Apr 22;183(2):403–407. doi: 10.1016/0014-5793(85)80820-6. [DOI] [PubMed] [Google Scholar]
- 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]
- Steenbergh P. H., Höppener J. W., Zandberg J., Visser A., Lips C. J., Jansz H. S. Structure and expression of the human calcitonin/CGRP genes. FEBS Lett. 1986 Dec 1;209(1):97–103. doi: 10.1016/0014-5793(86)81091-2. [DOI] [PubMed] [Google Scholar]
- Suzuki N., Nosé Y., Kasé Y., Sasayama Y., Takei Y., Nagasawa H., Watanabe T. X., Nakajima K., Sakakibara S. Amino acid sequence of sardine calcitonin and its hypocalcemic activity in rats. Zoolog Sci. 1994 Oct;11(5):713–716. [PubMed] [Google Scholar]
- 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]
- 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]