Responses of the trout cardiac natriuretic peptide system to manipulation of salt and water balance

Abstract

Natriuretic peptides (NPs) are evolutionarily conserved hormones that affect blood pressure and fluid volume through membrane-bound guanylate cyclase (GC)-linked natriuretic peptide receptors-A and -B (NPR-A and NPR-B, respectively) in a variety of vascular, renal, and other tissues. The principal physiological stimulus for cardiac NPs in fish is somewhat debated between two prominent theories: regulation of salt balance (osmoregulatory hypothesis) or prevention of volume expansion (cardioprotective hypothesis). In the present study, we examined atrial and ventricular expression of trout NPs, atrial (ANP), brain (BNP), and ventricular (VNP) using Northern (mRNA), Western (NP pro-hormone), and qPCR (GC-NPR-A and -B mRNA) blot analysis following independent manipulation of plasma salt and volume levels after chronic exposure to freshwater (FW; volume loaded, salt depleted), saltwater (SW; volume depleted, salt loaded), or freshwater trout fed a high-salt diet (FW-HSD; volume and salt loaded). We also measured NP transcriptional response to acute (2 h) volume expansion with dialyzed plasma (VE; 80% blood vol) or volume depletion by hemorrhage (VD, 20% blood volume every 30 min for 2 h) with real-time PCR. In essentially all instances, increased expression of the NP system was associated with FW-HSD or plasma expansion. There were no differences in NP expression between chronically adapted FW and SW fish, and hemorrhage decreased atrial ANP and VNP mRNA. These results indicate that rainbow trout cardiac NPs and cardiovascular GC-NPRs respond principally to volume, not salt overload, and this suggests that the primary function of trout cardiac NP system is to protect the heart.

Endogenous vascular synthesis of B-type and C-type natriuretic peptides in the rainbow trout

“…A strong argument has been made that the piscine NP system is principally responsive to volume, and hence the physiological progenitor to the mammalian NP system (Farrell and Olson, 2000;Johnson and Olson, 2008;Johnson and Olson, 2009a;Johnson and Olson, 2009b). The results from the present study further extend the multiple functional similarities between the piscine and mammalian NP systems and indicate that the production of NPs in the vasculature is a fundamental property of the NP system that is found throughout vertebrates.…”

“…Although endogenous synthesis of NPs has been reported in the mammalian vasculature (Hartmann et al, 2008;Potter et al, 2009) and a ubiquitous vascular expression of the guanylate cyclase-linked NP receptors A and B has been previously identified in trout (Johnson and Olson, 2009a), to our knowledge this is the first description of NP synthesis in the teleost vasculature.…”

“…EBA, CMA and ACV), will effectively accomplish this. Pre-branchial NP synthesis in the vasculature, such as the VA and the heart (Johnson and Olson, 2009a;Johnson and Olson, 2009b), are likely modulators of R G (and to a lesser extent P VA ), the primary determinants of afterload. Clearly, exogenous CNP can effectively reduce R G (Fig.5) and thereby lower cardiac afterload.…”

“…The teleost NP system bears many striking functional similarities to the cardiovascular anti-hypertrophic and volume-regulating NP system found in mammals (Farrell and Olson, 2000;Johnson and Olson, 2008;Johnson and Olson, 2009a). However, empirical information on extra-cardiac NP synthesis sites such as the vasculature in fish is limited.…”

The response of non-traditional natriuretic peptide production sites to salt and water manipulations in the rainbow trout

“…In addition, ANP and CNP are both found in the vasculature of rats and humans (Kelsall et al, 2006;Woodard et al, 2002). The transmembrane guanylate-cyclase-linked NP receptors (NPRs) are represented by NPR-A (the principal target for ANP and BNP) and NPR-B (the principal target for CNP) and are ubiquitously distributed throughout the cardiovascular system and central nervous system (CNS) of mammals and fish (Johnson and Olson, 2009;Potter et al, 2009).…”