Abstract
Atrial and B-type natriuretic peptides (ANP and BNP) are cardiac hormones important for cardiovascular and body fluid regulation. In some teleost species, an additional member of the natriuretic peptide family, ventricular NP (VNP), has been identified. In this study, we examine tissue distribution of these three NPs in the eel heart. Quantitative real-time PCR showed that anp is almost exclusively expressed in atria, bnp equally in atria and ventricles and vnp three-fold more in ventricles than in atria. The amount of bnp transcript overall in the heart was 1/10 those of anp and vnp. There was no difference in transcript levels between freshwater and seawater-acclimated fishes. Immunohistochemistry using specific antisera and in situ hybridization using gene-specific probes showed that NP signals were detected in most atrial and ventricular myocytes with some regional differences in density. Because of high sequence similarity of the three NPs, each of the three NP antisera individually was pre-incubated with 10−8 M of the other two non-targeted cardiac NPs to increase the specificity. A few atrial myocytes contained all three NPs in the same cell. Immuno-electron microscopy identified many dense-core vesicles containing ANP in atria and VNP in ventricles and some vesicles contained both ANP and VNP as demonstrated using pre-absorbed antisera. Based on these data and those of previous studies, we suggest that in eels ANP is secreted from atria in a regulatory pathway and VNP from ventricles in a constitutive pathway. In addition, VNP, not BNP, is the principal ventricular hormone in eels.
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Arjamaa O, Sormunen R, Lehto VP, Vuolteenaho O (2000) Localization of salmon cardiac peptide (sCP) in the heart of salmon (Salmo salar L.) Gen Comp Endocrinol 120:276–282
Asano K, Masuda K, Okumura M, Kadosawa T, Fujinaga T (1999) Plasma atrial and brain natriuretic peptide levels in dogs with congestive heart failure. J Vet Med Sci 61:523–529
Broadhead CL, O’Sullivan UT, Deacon CF, Henderson IW (1992) Atrial natriuretic peptide in the eel, Anguilla anguilla L.: its cardiac distribution, receptors and actions on isolated branchial cells. J Mol Endocrinol 9:103–114
Chapeau C, Gutkawska J, Schiller PW, Milne RW, Thibault G, Garcia R, Genest J, Cantin M (1985) Localization of immunoreactive synthetic atrial natriuretic factor (ANF) in the heart of various animal species. J Histochem Cytochem 33:541–550
Cousins KL, Farrell AP (1996) Stretch-induced release of atrial natriuretic factor from the heart of rainbow trout (Oncorhynchus mykiss). Can J Zool 74:380–387
de Bold AJ, Borenstein HB, Veress AT, Sonnenberg H (1981) A rapid and potent natriuretic response to intravenous injection of atrial myocardial extracts in rats. Life Sci 28:89–94
Donald JA, Evans DH (1992) Immunohistochemical localization of natriuretic peptides in the heart and brain of the gulf toadfish, Opsanus beta. Cell Tiss Res 269:151–158
Duff DW, Olson KR (1986) Trout vascular and renal responses to atrial natriuretic factor and heart extracts. Am J Phys 251:R639–R642
Hansson M (2002) Natriuretic peptides in relation to the cardiac innervation and conduction system. Microsc Res Tech 58:378–386
Hirohama T, Uemura H, Nakamura S, Aoto T (1988) Atrial natriuretic peptide (ANP)-immunoreactivity and ultrastructures of cardiocytes in fish. Zool Sci 5:833–845
Inoue K, Naruse K, Yamagami S, Mitani H, Suzuki N, Takei Y (2003) Four functionally distinct C-type natriuretic peptides found in fish reveal evolutionary history of the natriuretic system. Proc Natl Acad Sci U S A 100:10079–10084
Inoue K, Sakamoto T, Yuge S, Iwatani H, Yamagami S, Tsutsumi M, Hori H, Cerra MC, Tota B, Suzuki N, Okamoto N, Takei Y (2005) Structural and functional evolution of three cardiac natriuretic peptides. Mol Biol Evol 22:2428–2434
Kaiya H, Takei Y (1996a) Atrial and ventricular natriuretic peptide concentrations in plasma of freshwater- and seawater-adapted eels. Gen Comp Endocrinol 102:183–190
Kaiya H, Takei Y (1996b) Osmotic and volaemic regulation of atrial and ventricular natriuretic peptide secretion in conscious eels. J Endocrinol 149:441–447
Kasahara M, Naruse K, Sasaki S et al (2007) The medaka draft genome and insights into vertebrate genome evolution. Nature 447:714–719
Kawakoshi A, Hyodo S, Inoue K, Kobayashi Y, Takei Y (2004) Four natriuretic peptides (ANP, BNP, VNP and CNP) coexist in the sturgeon: new evidence for the presence of BNP in fish lineage. J Mol Endocrinol 32:547–555
Kishimoto I, Tokudome T, Nakao K, Kangawa K (2011) Natriuretic peptide system: an overview of studies using genetically engineered animal models. FEBS J 278:1830–1841
Maldonado C, Forssmann WG, Aoki A (1992) Ultrastructural and immunocytochemical study of the myoendocrine cells of the fish Hypostomus cordovae. Anat Embryol 186:557–561
Miyanishi H, Nobata S, Takei Y (2011) Relative dipsogenic potencies of six natriuretic peptides in eels. Zool Sci 28:719–726
Miyanishi H, Okubo T, Kaneko T, Takei Y (2013a) Role of cardiac natriuretic peptides in seawater adaptation of medaka embryos as revealed by loss-of-function analysis. Am J Phys 304:R423–R434
Miyanishi H, Okubo K, Nobata S, Takei Y (2013b) Natriuretic peptides in developing medaka embryos: implications in cardiac development by loss-of-function studies. Endocrinology 154:410–420
Nakamura S, Naruse M, Naruse K, Kawata M, Nishikawa T, Hosoda S, Tanaka I, Yoshimi T, Yoshihara I, Inagami T, Uemura H, Demura H (1991) Atrial natriuretic peptide and brain natriuretic peptide coexist in the secretory granules of human cardiac myocytes. Am J Hypertens 4:909–912
Nishikimi T, Kuwahara K, Nakao K (2011) Current biochemistry, molecular biology, and clinical relevance of natriuretic peptides. J Cardiol 57:131–140
Nobata S, Ventura A, Kaiya H, Takei Y (2010) Diversified cardiovascular actions of six homologous natriuretic peptides (ANP, BNP, VNP, CNP1, CNP3 and CNP4) in conscious eels. Am J Phys 298:R1549–R1559
Olson KR, Farrell AP (2006) The cardiovascular system. In: Evans DH, Claiborne JB (eds) The physiology of fishes. CRC Press, Boca Raton, pp 119–153
Reinecke M, Nehls M, Forssmann WG (1985) Phylogenetic aspects of cardiac hormones as revealed by immunocytochemistry, electronmicroscopy, and bioassay. Peptides 6:321–331
Saito Y (2011) Roles of atrial natriuretic peptide and its therapeutic use. J Cardiol 56:262–270
Scott JN, Jennes L (1987) Distribution of atrial natriuretic factor in fetal rat atria and ventricles. Cell Tissue Res 248:479–481
Solc D (2007) The heart and heart conducting system in the kingdom of animals: a comparative approach to its evolution. Exp Clin Cardiol 12:113–118
Takei Y, Balment RJ (1993) Biochemistry and physiology of a family of eel natriuretic peptides. Fish Physiol Biochem 11:183–188
Takei Y, Hirose S (2002) The natriuretic peptide system in eel: a key endocrine system for euryhalinity? Am J Phys 282:R940–R951
Takei Y, Ando K, Kawakami M (1992) Atrial natriuretic peptide in eel plasma, heart and brain characterized by homologous radioimmunoassay. J Endocrinol 135:325–331
Takei Y, Takahashi A, Watanabe TX, Nakajima K, Ando K (1994) Eel ventricular natriuretic peptide: isolation of low-molecular size form and characterization of plasma form by homologous radioimmunoassay. J Endocrinol 141:81–89
Takei Y, Inoue K, Trajanovska S, Donald JA (2011) B-type natriuretic peptide (BNP), but not ANP, is the basic cardiac natriuretic peptide in vertebrates. Gen Comp Endocrinol 171:258–266
Takei Y, Hiroi J, Takahashi T, Sakamoto T (2014) Diverse mechanisms of body fluid regulation in teleost fishes. Am J Phys 307:R778–R792
Toshimori H, Toshimori K, Oura C, Matsuo H (1987) Immunohistochemical study of atrial natriuretic polypeptides in the embryonic, fetal and neonatal rat heart. Cell Tissue Res 248:627–633
Trajanovska S, Inoue K, Takei Y, Donald JA (2007) Genomic analyses and cloning of novel chicken natriuretic peptide genes reveal new insights into natriuretic peptide evolution. Peptides 28:2155–2163
Trevonen V, Ruskoaho H, Lecklin T, Ilves M, Vuolteenaho O (2002) Salmon cardiac natriuretic peptide is a volume-regulating hormone. Am J Phys 283:R353–R361
Tsukada T, Takei Y (2006) Integrative approach to osmoregulatory action of atrial natriuretic peptide in seawater eels. Gen Comp Endocrinol 147:31–38
Uemura H, Naruse M, Hirohama T, Nakamura S, Kasuya Y, Aoto T (1990) Immunoreactive atrial natriuretic peptide in the fish heart and blood plasma examined by electron microscopy, immunohistochemistry and radioimmunoassay. Cell Tissue Res 260:235–247
Ventura A, Kawakoshi A, Inoue K, Takei Y (2006) Multiple natriuretic peptides coexist in the most primitive extant ray-finned fish, bichir Polypterus endlicheri. Gen Comp Endocrinol 146:251–256
Yousaf MN, Amin AB, Koppang EO, Vuolteenaho O, Powell MD (2012) Localization of natriuretic peptides in the cardiac pacemaker of Atlantic salmon (Salmo salar L.) Acta Hitochem 114:819–824
Acknowledgements
We cordially thank Ms. Aya Shiozawa who performed the experiment of molecular biology under the guidance of M. K. We are grateful to Dr. Christopher A. Loretz of the State University of New York at Buffalo for his careful editing of this manuscript. This research was supported by Grant-in-Aid for Scientific Research (A) from the Japan Society for the Promotion of Science to Y. T. (23247010).
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Takei, Y., Nemoto, N., Kameya, T. et al. Distribution and co-localization of diversified natriuretic peptides in the eel heart. Cell Tissue Res 373, 367–377 (2018). https://doi.org/10.1007/s00441-018-2833-y
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DOI: https://doi.org/10.1007/s00441-018-2833-y