Summary
The distribution of natriuretic peptide immunoreactivity was determined in the heart and brain of the gulf toadfish Opsanus beta using the avidin-biotin peroxidase technique. Four antisera were used: the first raised against porcine brain natriuretic peptide which cross-reacts with atrial natriuretic and C-type natriuretic peptides (termed natriuretic peptide-like immunoreactivity); the second raised against porcine brain natriuretic peptide which cross-reacts with C-type natriuretic peptide but not with atrial natriuretic peptide (termed porcine brain natriuretic peptide-like immunoreactivity); the third raised against rat atrial natriuretic peptide; and the fourth raised against eel atrial natriuretic peptide. Natriuretic peptide- and porcine brain natriuretic peptide-like immunoreactivity was observed in all cardiac muscle cells of the atrium. In the ventricle, natriuretic peptide-like immunoreactivity was found in all cardiac muscle cells, however porcine brain natriuretic peptidelike immunoreactivity was confined to muscle cells adjacent to the epicardium. There was no discernible difference in the distribution of natriuretic peptide-like immunoreactivity and porcine brain natriuretic peptide-like immunoreactivity in the brain. Immunoreactive perikarya were observed only in the preoptic region of the diencephalon, and many immunoreactive fibres were found in the telencephalon, preoptic area, and rostral hypothalamus, lateral to the thalamic region. There was no immunoreactivity in any region of the hypophysis. A pair of distinct immunoreactive fibre tracts ran caudally from the preoptic area to the thalamic region, from which fibres extended to the posterior commissure, area praetectalis, dorsolateral regions of the midbrain tegmentum, and tectum. Many immunoreactive fibres were present in the rostral regions of the inferior lobes of the hypothalamus and in the dorsolateral and ventrolateral aspects of the rhombencephalon. No immunoreactivity was observed in the heart and brain using rat atrial natriuretic and eel natriuretic peptide antisera. Although the chemical structure of natriuretic peptides in the heart and brain of toadfish is unknown, these observations show that a component of the natriuretic peptide complement is similar to porcine brain natriuretic and/or porcine C-type natriuretic peptides. The presence of natriuretic peptides in the brain suggests that they could be important neuromodulators and/or neurotransmitters.
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References
Aburaya M, Minamino N, Kangawa K, Tanaka K, Matsuo H (1989a) Distribution and molecular forms of brain natriuretic peptide in porcine heart and blood. Biochem Biophys Res Comm 165:872–879
Aburaya M, Minamino N, Hino J, Kangawa K, Matsuo H (1989b) Distribution and molecular forms of brain natriuretic peptide in the central nervous system, heart and peripheral tissues of rat. Biochem Biophys Res Comm 165:880–887
Brody MJ, Johnson AK (1980) Role of the AV3V region in the fluid and electrolyte balance, arterial pressure regulation, and hypertension. In: Martini L. Ganong WF (eds) Frontiers in neuroendocrinology, vol 6. Oxford University Press, London, pp 249–292
Chapeau C, Gutkowska J, Schiller PW, Milne RW, Thibault G, Garcia R, Genest J, Cantin M (1985) Localisation of immunoreactive synthetic atrial natriuretic factor (ANF) in the heart of various animal species. J Histochem Cytochem 33:541–550
Davis RE, Northutt RG (1983) Fish neurobiology, vol 2. The University of Michigan Press, Ann Arbor
Donald JA, Vomachka AJ, Evans DH (1992) Immunohistochemical localisation of natriuretic peptides in tissues of teleost, elasmobranch, and cyclostome fish. Bull Mount Desert Island Biol Lab 31:120–121
Evans DH (1989) Immunoreactive atriopeptin in plasma and tissues of fishes: the effect of salinity change. Bull Mount Desert Island Biol Lab 28:39–41
Evans DH (1990) An emerging role for a cardiac peptide hormone in fish osmoregulation. Annu Rev Physiol 52:43–60
Evans DH, Chipouras E, Payne JA (1989) Immunoreactive atriopeptin in plasma of fishes: its potential role in gill hemodynamics. Am J Physiol 257:R939-R945
Evans DH, Toop T, Donald JA, Forrest JN (1992) C-type atrial natriuretic peptides are potent dilators of shark (Squalus acanthias) vascular smooth muscle. Bull Mount Desert Island Biol Lab 31:118–119
Furuya M, Takehisa M, Minamitake Y, Kitajima Y, Hayashi Y, Ohnuma N, Ishihara T, Minamino N, Kangawa K, Matsuo H (1990) Novel natriuretic peptide, CNP, potently stimulates cyclic GMP production in rat cultured vascular smooth muscle cells. Biochem Biophys Res Comm 170:201–208
Galli SM, Evans DH, Kimura B, Philips IM (1988) Changes in plasma and brain levels of atrial natriuretic peptide in fish adapting to fresh water and sea water. FASEB J 2:A524
Genest J, Cantin M (1988) The atrial natriuretic factor: its physiology and biochemistry. Rev Physiol Biochem Pharmacol 110:1–145
Gutkowska J, Nemer M (1989) Structure, expression and function of atrial natriuretic factor in extraatrial tissues. Endocrine Rev 10:519–536
Hino J, Taeyama H, Minamino N, Kangawa, Matsuo H (1990) Isolation and identification of human brain natriuretic peptides in cardiac atrium. Biochem Biophys Res Comm 167:693–700
Kambayashi Y, Nakao K, Mukoyama M, Saito Y, Ogawa Y, Shiono S, Inouye K, Yoshida N, Imura H (1990) Isolation and sequence determination of human brain natriuretic peptide in human atrium. FEBS Lett 259:341–345
Kawata M, Nakao K, Morii N, Kiso Y, Yamashita H, Imura H, Sano Y (1985) Atrial natriuretic polypeptide: topographical distribution in the rat brain by radioimmunoassay and immunohistochemistry. Neuroscience 16:521–546
Netchitailo P, Feuilloley M, Pelletier G, Leboulanger F, Cantin M, Gutkowska J, Vaudry H (1987) Atrial natriuretic factor-like immunoreactivity in the central nervous system of the frog. Neuroscience 22:341–359
Nishida Y, Hironobu M, Naoto M, Kangawa K, Matsuo H, Hosomi H (1990) Effects of brain natriuretic peptide on hemodynamics and renal function in dogs. Jpn J Physiol 40:531–540
Northcutt RG, Davis RE (1983) Fish neurobiology, vol 1. The University of Michigan Press, Ann Arbor
Price DA, Doble KE, Lee TD, Galli SM, Dunn BM, Parten B, Evans DH (1990) The sequencing, synthesis and biological actions of an ANP-like peptide isolated from the brain of the killifish, Fundulus heteroclitus. Biol Bull, Woods Hole 178:279–285
Reinecke M, Betzler D, Forssmann WG (1987a) Immunocytochemistry of cardiac polypeptide hormones (cardiodilatin/atrial natriuretic polypeptide) in brain and hearts of Myxine glutinosa (Cyclostomata). Histochemistry 86:233–239
Reinecke M, Betzler D, Forsmann WG, Thorndyke M, Askensten U, Falkmer S (1987b) Electronmicroscopical, immunohistochemical, immunocytochemical and biological evidence for the occurrence of cardiac hormones (ANP/CDD) in Chondrichthyes. Histochemistry 87:531–538
Saper CB, Stanaert DG, Currie MG, Schwartz D, Geller DM, Needleman P (1985) Atriopeptin-immunoreactive neurons in the brain: presence in cardiovascular regulatory areas. Science 227:1047–1049
Saper CB, Hurley KM, Moga MM, Holmes HR, Adams SA, Leahy KM, Needleman P (1989) Brain natriuretic peptides: differential localisation of a new family of neuropeptides. Neurosci Lett 96:29–34
Saper C, Kibbe M, Hurley KM, Spencer S, Holmes RH, Leahy KM, Needleman P (1990) Brain natriuretic peptide-like immunoreactive innervation of the cardiovascular and cerebrovascular systems in the rat. Circ Res 67:1345–1354
Schofield JP, Jones DSC, Forrest JN (1991) Identification of C-type natriuretic peptide in heart of the spiny dogfish shark (Squalus acanthias). Am J Physiol 261:F734-F739
Seilhamer JJ, Arfsten A, Miller JA, Lundquist P, Scarborough RM, Jewicki JA, Porter JG (1989) Human and canine gene homologs of porcine brain natriuretic peptide. Biochem Biophys Res Comm 165:650–658
Standaert DG, Needleman P, Saper CB (1986) Organisation of atriopeptin-like immunoreactive neurons in the centrla nervous system of the rat. J Comp Neurol 253:315–341
Sudoh T, Kangawa K, Minamino N, Matsuo H (1988) A new natriuretic peptide in porcine brain. Nature 332:78–81
Sudoh T, Minamino N, Kangawa K, Matsuo H (1990) C-type natriuretic peptide (CNP): A new member of the natriuretic peptide family identified in porcine brain. Biochem Biophys Res Comm 168:863–870
Suzuki R, Takahashi A, Hazon N, Takei Y (1991) Isolation of high-molecular-weight C-type natriuretic peptide from the heart of a cartilaginous fish (European dogfish, Scyliorhinus canicula). FEBS Lett 282:321–325
Takei Y, Takahashi A, Watanabe TX, Nakajima K, Sakakibara S (1989) Amino acid sequence and relative biological activity of eel atrial natriuretic peptide. Biochem Biophys Res Comm 164:537–543
Takei Y, Tamaki H, Ando K (1990a) Identification and partial characterisation of immunoreactive and bioactive atrial natriuretic peptide from eel heart. J Comp Physiol [B] 160:119–126
Takei Y, Takahashi A, Watanabe TX, Nakajima K, Sakakibara S, Takao T, Shimonishi Y (1990b) Amino acid sequence and relative biological activity of a natriuretic peptide isolated from eel brain. Biochem Biophys Res Comm 170:883–891
Uehara Y, Shimizu H, Shimomura Y, Kobayashi I, Kobayashi S (1990) Rat brain natriuretic peptide (BNP) reduces water intake following dehydration. Neurpeptides 17:107–110
Uemura H, Naruse M, Hirohama T, Nakamura S, Kasuya Y, Aoto T (1990) Immunoreactive atrial natriuretic peptide in the fish heart examined by electron microscopy, immunohistochemistry and radioimmunoassay. Cell Tissue Res 260:235–247
Vallarino M, Feuilloley M, Gutkowska J, Cantin M, Vaudry H (1990) Localisation of atrial natriuretic factor (ANF)-related peptides in the central nervous system of the elasmobranch fish Scyliorhinus canicula. Peptides 11:1175–1181
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Donald, J.A., Evans, D.H. Immunohistochemical localisation of natriuretic peptides in the heart and brain of the gulf toadfish Opsanus beta . Cell Tissue Res 269, 151–158 (1992). https://doi.org/10.1007/BF00384735
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DOI: https://doi.org/10.1007/BF00384735