Abstract
A range of homologous (trout ANP, trout CNP, trout VNP) and heterologous (eel ANP, eel ANP-NH2, rat ANP, porcine CNP) NPs were tested for their effect on guanylyl cyclase in gill and kidney membrane preparations from freshwater and seawater-acclimated rainbow trout and Atlantic salmon. All NPs stimulated guanylyl cyclase at 1 μmol l−1in all preparations. ANP was the most potent stimulator of kidney guanylyl cyclase and CNP the most potent stimulator of guanylyl cyclase in gills. Some differences were apparent between the potencies of homologous and heterologous peptides at 1 μmol l−1: tANP was more potent than rANP in the SW trout kidney and tCNP was more potent than pCNP in FW salmon tissues. While eANP was more potent than tANP in trout gills, it was less potent than tANP in FW salmon gills. However, there was no significant difference between the potencies of eANP and eANP-NH2 in trout or salmon gills. Salinity did not affect guanylyl cyclase activity with the exception that trout ANP at 1 μmol l−1was more potent in SW trout kidneys than in FW trout kidneys. These results suggest a predomination of NPR-A in the kidney and NPR-B in the gill. It appears that salmonid NPR-A and NPR-B are relatively promiscuous in their ligand affinity, with few differences in the potencies of trout and mammalian NPs and only small differences in cGMP production where these differences do occur.
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Ando, M. and Hara, I. 1994. Alteration of sensitivity to various regulators in the intestine of the eel following seawater acclimation. Comp. Biochem. Physiol. 109A: 447–453.
Aller, S.G., Lombardo, I.D., Bhanot, S. and Forrest, J.N. Jr. 1999. Cloning, characterization, and functional expression of a CNP receptor regulating CFTR in the shark rectal gland. Am. J. Physiol. 276: C442:C449.
Barr, C.S., Rhodes, P. and Struthers, A.D. 1996. C-type natriuretic peptide. Peptides 17: 1243–1251.
Callahan, W., Forster, M. and Toop, T. 2000. Evidence of a guanylyl cyclase natriuretic peptide receptor in the gills of the New Zealand hagfish Eptatretus cirrhatus (Class Agnatha). J. Exp. Biol. 203: 2519–2528.
Callahan, W., Powell, M.D. and Toop, T. 2003. CNP is more potent than ANP as a stimulant of particulate guanylyl cyclase in the teleost gill. Comp. Biochem. Physiol. 134A: S48.
Conklin, D.J. and Olson, K.R. 1994. Compliance and smooth muscle reactivity of rainbow trout (Oncorhynchus mykiss) vessels in vitro. J. Comp. Physiol. B 163: 657–663.
Donald, J.A., Toop, T. and Evans, D.H. 1994. Localization and analysis of natriuretic peptide receptors in the gills of the toadfish, Opsanus beta (teleostei). Am. J. Physiol. 267: R1437–R1444.
Duff, D.W. and Conklin, D.J. 1997. Effect of atrial natriuretic peptide on fluid volume and glomerular filtration in the rainbow trout. J. Exp. Zool. 278: 215–220.
Duff, D.W. and Olson, K.R. 1986. Trout vascular and renal responses to atrial natriuretic factor and heart extracts. Am. J. Physiol. 251: R639–R642.
Evans, D.H. 2002. Cell signaling and ion transport across the fish gill epithelium. J. Exp. Zool. 293: 336–347.
Evans, D.H., Chipouras, E. and Payne, J.A. 1989. Immunoreactive atriopeptin in plasma of fishes: its potential role in gill hemodynamics. Am. J. Physiol. 257: R939–R945.
Evans, D.H., Roeser, J.M. and Stidham, J.D. 2002. Natriuretic peptide hormones do not inhibit NaCl transport across the opercular skin of the killifish Fundulus heteroclitus. Bull. Mt. Desert Isl. Biol. Lab. 41: 9.
Evans, D. H., Toop, T., Donald, J. and Forrest, J.N. Jr. 1993. C-Type natriuretic peptides are potent dilators of shark vascular smooth muscle. J. Exp. Zool. 265: 84–87
Fowkes, R.C. and McArdle, C.A. 2000. C-type natriuretic peptide: an important neuroendocrine regulator? TEM 11: 333–338.
Galli, S.M., Evans, D.H., Kimura, B. and Phillips, M.I. 1988. Changes in plasma and brain levels of atrial natriuretic peptide in fish adapting to fresh water and sea water. FASEB J. 2: A524.
Gunning, M., Cuero, C., Solomon, R. and Silva, P. 1993. C-type natriuretic peptide receptors and signaling in rectal gland of Squalus acanthias. Am. J. Physiol. 264: F300–F305.
Inoue, K., Russell, M. J., Olson, K. R., Takei, Y. 2003. C-type natriuretic peptide of rainbow trout (Oncorhynchus mykiss): primary structure and vasorelaxant activities. Gen. Comp. Endocrimol. 130: 185–192.
Kaiya, H. and Takei, Y. 1996. Changes in plasma atrial and ventricular natriuretic peptide concentrations after transfer of eels from freshwater to seawater or vice versa. Gen. Comp. Endocrinol. 104: 337–345.
Kashiwagi, M., Katafuchi, T., Kato, A., Inuyama, H., Ito, T., Hagiwara, H., Takei, Y. and Hirose, S. 1995. Cloning and properties of a novel natriuretic peptide receptor, NPR-D. Eur. J. Biochem. 233: 102–109.
Kashiwagi, M., Miyamoto, K., Takei, Y. and Hirose, S. 1999. Cloning, properties and tissue distribution of natriuretic peptide receptor-A of euryhaline eel, Anguilla japonica. Eur. J. Biochem. 259: 204–211.
Katafuchi, T., Takashima, A., Kashiwagi, M., Hagiwara, H., Takei, Y. and Hirose, S. 1994. Cloning and expression of eel natriuretic peptide receptor B (NPR-B) and comparison with its mammalian counterparts. Eur. J. Biochem. 222: 835–842.
Kawakoshi, A., Hyodo, S. and Takei, Y. 2001. CNP is the only natriuretic peptide in an elasmobranch fish, Triakis scyllia. Zool. Sci. 18: 861–868.
Lee, J. and Malvin, R.L. 1987. Natriuretic response to homologous heart extract in aglomerular toadfish. Am. J. Physiol. 252: R1055–R1058.
Loretz, C.A. 1996. Inhibition of goby posterior intestinal NaCl transport by natriuretic peptides and by cardiac extracts. J. Comp. Physiol. B 166: 484–491.
Loretz, C.A. and Pollina, C. 2000. Natriuretic peptides in fish physiology. Comp. Biochem. Physiol. 125A: 169–187
Maack, T. 1992. Receptors of atrial natriuretic factor. Annu. Rev. Physiol. 54: 11–27.
Mishina, S. and Takei, Y. 1997. Characterisation of natriuretic peptide receptors in eel gill. J. Endocrinol. 154: 415–422.
O'Grady, S.M. 1989. Cyclic nucleotide-mediated effects of ANF and VIP on flounder intestinal ion transport. Am. J. Physiol. 249: C142–C146.
Ohno, S, 1970. Evolution by Gene Duplication. Springer-Verlag, Berlin, Heidelberg, New York.
Perrott, M.N., Sainsbury, R.J. and Balment, R.J. 1993. Peptide hormone-stimulated second messenger production in the teleostean nephron. Gen. Comp. Endocrinol. 89: 387–395.
Sakaguchi, H., Suzuki, H., Hagiwara, H., Kaiya, H., Takei, Y., Ito, M., Shibabe, S. and Hirose, S. 1996. Whole body autoradiography and microautoradiography in eels after intra-arterial administration of 125I-labeled eel ANP. Am. J. Physiol. 271: R926–R935.
Sakamoto, T., Uchida, K. and Yokota, S. 2001. Regulation of the ion-transporting mitochondrion-rich cell during adaptation of teleost fishes to different salinities. Zool. Sci. 18: 1163–1174.
Smith, M.P., Takei, Y. and Olson, K.R. 2000. Similarity of vasorelaxant effects of natriuretic peptides in isolated blood vessels of salmonids. Physiol. Biochem. Zool. 73: 494–500.
Suga, S. I., Nakao, K., Hosoda, K., Mukoyama, M., Ogawa, Y., Shirakami, G., Arai, H., Saito, Y., Kambayashi, Y., Inouye, K. and Imura, H. 1992. Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-type natriuretic peptide. Endocrinol. 130: 229–239
Takashima, A., Katafuchi, T., Shibasaki, M., Kashiwagi, M., Hagiwara, H., Takei, Y. and Hirose, S. 1995. Cloning, properties, site-directed mutagenesis analysis of the subunit structure, tissue distribution and regulation of expression of the type-C eel natriuretic peptide receptor. Eur. J. Biochem. 227: 673–680.
Takeda, K. and Suzuki, N. 1999. Genomic structure and expression of the Medaka fish homolog of the mammalian guanylyl cyclase B. J. Biochem. 126(1): 104–114.
Takei, Y. and Balment, R.J. 1993. Natriuretic factors in nonmammalian vertebrates. In New Insights in Vertebrate Kidney Function. pp 351–385. Edited by J.A. Brown, R.J. Balment and J.C. Rankin. Cambridge University Press, Cambridge.
Takei, Y., Flik, G. and Hirose, S. 1999. Interaction of the natriuretic peptide system and the renin-angiotensin system in eel osmoregulation. In Recent Developments in Comparative Endocrinology and Neurobiology. pp. 144–148. Edited by E.W. Roubos, S.E. Wendelaar Bonga, H. Vaudry and A. De Loof. Shaker Publishing, Maastricht.
Takei, Y., Fukuzawa, A., Itahara, Y., Watanabe, T.X., Yoshizawa Kumagaye, K., Nakajima, K., Yasuda, A., Smith, M.P., Duff, D.W. and Olson, K.R. 1997a. A new natriuretic peptide isolated from cardiac atria of trout, Oncorhynchus mykiss. FEBS Letters 414: 377–380.
Takei, Y. and Hirose, S. 2002. The natriuretic peptide system in eels: a key endocrine system for euryhalinity? Am. J. Physiol. 282: R940–R951.
Takei, Y., Inoue, K., Ando, K., Ihara, T., Katafuchi, T., Kashiwagi, M. and Hirose, S. 2001. Enhanced expression and release of Ctype natriuretic peptide in freshwater eels. Am. J. Physiol. 280: R1727–R1735.
Takei, Y. and Kaiya, H. 1998. Antidiuretic effect of eel ANP infused at physiological doses in conscious, seawater-adapted eels, Anguilla japonica. Zool. Sci. 15: 399–404.
Takei, Y., Takahashi, A., Watanabe, T.X., Nakajima, K. and Sakakibara, S. 1989. Amino acid sequence and relative biological activity of eel atrial natriuretic peptide. Biochem. Biophys. Res. Commun. 164: 537–543.
Takei, Y., Takahashi, A., Watanabe, T.X., Nakajima, K., Sakakibara, S., Takao, T. and Shimonishi, Y. 1990. Amino acid sequence and relative biological activity of a natriuretic peptide isolated from eel brain. Biochem. Biophys. Res. Commun. 170: 883–891.
Takei, Y., Takano, M., Itahara, Y., Watanabe, T.X., Nakajima, K., Conklin, D.J., Duff, D.W. and Olson, K.R. 1994. Rainbow trout ventricular natriuretic peptide: isolation, sequencing, and determination of biological activity. Gen. Comp. Endocrinol. 96: 420–426.
Takei, Y., Ueki, M., Takahashi, A. and Nishizawa, T. 1997b. Cloning, sequence analysis, tissue-specific expression, and prohormone isolation of eel atrial natriuretic peptide. Zool. Sci. 14: 993–999.
Tervonen, V., Arjamaa, O., Kokkonen, K., Ruskoaho, H. and Vuolteenaho, O. 1998. A novel cardiac hormone related to A-, B-and C-type natriuretic peptides. Endocrinol. 139: 4021–4025.
Tervonen, V., Ruskoaho, H. and Vuolteenaho, O. 2000. Novel cardiac peptide hormone in several teleosts. J. Endocrinol. 166: 407–418.
Tervonen, V., Ruskoaho, H., Lecklin, T., Ilves, M. and Vuolteenaho, O. 2002. Salmon cardiac natriuretic peptide is a volumeregulating hormone. Am. J. Physiol. 283: E353–E361.
Toop, T., Grozdanovski, D. and Potter, I.C. 1998. Natriuretic peptide binding sites in the gills of the pouched lamprey Geotria australis. J. Exp. Biol. 201: 1799–1808.
Westenfelder, C., Birch, F.M., Baranowski, R.L., Rosenfeld, M.J., Shiozawa, D.K. and Kablitz, C. 1988. Atrial natriuretic factor and salt adaptation in the teleost fish Gila atraria. Am. J. Physiol. 255: F1281–F1286.
Yamagami, S., Suzuki, K., Suzuki, N. 2001. Expression and exon/intron organization of two medaka fish homologs of the mammalian guanylyl cyclase A. J. Biochem. 130: 39–50.
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Callahan, W., McWilliam, H., Powell, M.D. et al. Guanylyl cyclase stimulation by homologous and heterologous natriuretic peptides in salmonids. Fish Physiology and Biochemistry 26, 129–138 (2002). https://doi.org/10.1023/A:1025466000972
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DOI: https://doi.org/10.1023/A:1025466000972