Skip to main content
SpringerLink
Log in

Reactivity of isolated toad aortic rings to angiotension II: the role of nitric oxide

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Little is known about the vascular actions of angiotensin II (Ang II) and nitric oxide (NO) in Amphibia. This study investigated (1) Ang II contractility, (2) NO concentrations, and (3) correlations between Ang II contractility, NO concentration and mean arterial pressure (MAP) in isolated Bufo arenarum toad aortic rings. Contractility was measured in isometric conditions, NO concentrations were determined by the Griess reaction, and MAP was determined by a direct method. In isolated toad aortic rings, Ang II produced a contractile response (292.7 ± 89.2 mg; n = 20). Furthermore, a contractile response to norepinephrine (NE) was also obtained. A significant correlation between both the Ang II and NE contractile responses was found (r = 0.89; n = 11; P < 0.01). Administration of Ang II increased MAP values (Basal 16.8 ± 1.7; n = 19 vs. Ang II 28.4 ± 1.8 mmHg; n = 19; P < 0.001), and the increase of MAP by Ang II was positively correlated with the Ang II contractile response (P < 0.01). Administration of L-NAME also increased MAP values, and this effect was higher in those toads that presented a lower pressure response to Ang II (Pearson r = −0.68; P < 0.05). NO was present in all aortic rings, and its concentrations were negatively related to the Ang II contractile response (P < 0.036) and pressure response (Pearson r = −7.08; P < 0.001). These findings suggest that, in the B. arenarum toad, the NO system contra-regulates both the contractile and pressure Ang II responses, although its action could be different in each specimen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alderton W, Cooper C, Knowles R (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615

    Article  PubMed  CAS  Google Scholar 

  • Basset A, Laude D, Laurent S, Elghozi J (2004) Contrasting circadian rhythms of blood pressure among inbred rat strains: recognition of dipper and non-dipper patterns. J Hypertens 22:727–737

    Article  PubMed  CAS  Google Scholar 

  • Broughton B, Donald J (2002) Nitric oxide regulation of the central aortae of the toad Bufo marinus occurs independently of the endothelium. J Exp Biol 205:3093–3100

    PubMed  CAS  Google Scholar 

  • Brown J, Cobb C, Frankling S, Rankin J (2005) Activation of the newly discovered cyclostome renin–angiotensin system in the river lamprey Lampetra fluviatilis. J Exp Biol 208:223–232

    Article  PubMed  CAS  Google Scholar 

  • Castel H, Jégou S, Tonon MC, Vaudry H (2000) Regulation of the GABA(A) receptor by nitric oxide in frog pituitary melanotrophs. Endocrinology 141:3451–3560

    Article  PubMed  CAS  Google Scholar 

  • Conklin DJ, Olson KR (1994) Angiotensin II relaxation of rainbow trout vessels in vitro. Am J Physiol Regul Integr Comp Physiol 266:R1856–R1860

    CAS  Google Scholar 

  • Coviello A (1972) Hydrosmotic effect of angiotensin II in isolated toad bladder. Acta Physiol Lat Am 22:218–226

    PubMed  CAS  Google Scholar 

  • Donald J, Broughton B (2005) Nitric oxide control of lower vertebrate blood vessels by vasomotor nerves. Comp Biochem Physiol A Mol Integr Physiol 142:188–197

    Article  PubMed  CAS  Google Scholar 

  • Fock E, Lavrova E, Bachteeva V, Chernigovskaya E, Parnova R (2004) Nitric oxide inhibits arginine-vasotocin-induced increase of water osmotic permeability in frog urinary bladder. Pflugers Arch 448:197–203

    Article  PubMed  CAS  Google Scholar 

  • Gamundi S (1983) Vascular responses to angiotensins in the toad. Role of the adrenergic system. Pharmacol Res Commun 15:529–543

    Article  PubMed  CAS  Google Scholar 

  • Goense J, Feng A (2005) Seasonal changes in frequency tuning and temporal processing in single neurons in the frog auditory midbrain. J Neurobiol 65:22–36

    Article  PubMed  Google Scholar 

  • Hamano K, Tierney ML, Ashida K, Takei Y, Hazon N (1998) Direct vasoconstrictor action of homologous angiotensin II on isolated arterial ring preparations in an elasmobranch fish. J Endocrinol 158:419–423

    Article  PubMed  CAS  Google Scholar 

  • Harper R, Stephens G (1985) Blockade of the pressor response to angiotensins. Gen Comp Endocrinol 60:227–235

    Article  PubMed  CAS  Google Scholar 

  • Higashi Y, Nakagawa K, Kimura M, Noma K, Hara K, Sasaki S, Goto C, Oshima T, Chayama K, Yoshizumi M (2002) Circadian variation of blood pressure and endothelial function in patients with essential hypertension: a comparison of dippers and non-dippers. J Am Coll Cardiol 40:2039–2043

    Article  PubMed  Google Scholar 

  • Jennings B, Bell J, Hyodo S, Toop T, Donald J (2007) Mechanisms of vasodilation in the dorsal aorta of the elephant fish Callorhinchus milii (Chimaeriformes: Holocephali). J Comp Physiol B 177:557–567

    Article  PubMed  CAS  Google Scholar 

  • Knight G, Burnstock G (1996) The involvement of the endothelium in the relaxation of the leopard frog (Rana pipiens) aorta in response to acetylcholine. Br J Pharmacol 118:1518–1522

    PubMed  CAS  Google Scholar 

  • Martinez-Sierra R, Lorenzo-Velazquez B (2005) Influence of temperature and seasons on H3-norepinephrine uptake by isolated strip ventricle of frog. Cell Mol Life Sci (CMLS) 28:1063–1065

    Article  Google Scholar 

  • Miller B, Vanhoutte P (1986) Endothelium-dependent responses in isolated blood vessels of lower vertebrates. Blood Vessels 23:225–235.33

    PubMed  CAS  Google Scholar 

  • Moris J (1982) Seasonal variation in responses of the toad renal vasculature to adrenaline. Naunyn-Schmiedeberg’s Arch Pharmacol 320:246–254

    Article  Google Scholar 

  • Mustafa T, Agnisola C (1988) Vasoactivity of adenosine in the trout (Oncorhynchus mykiss) coronary system: involvement of nitric oxide and interaction with noradrenaline. J Exp Biol 201:3075–3083

    Google Scholar 

  • Nolly H, Fasciolo J (1971) The renin-angiotensin system in Bufo arenarum and Bufo paracnemis. Comp Biochem Physiol 39A:823–831

    Article  Google Scholar 

  • Olson K, Villa J (1991) Evidence against nonprostanoid endothelium- derived relaxing factor(s) in trout vessels. Am J Physiol 260:925–933

    Google Scholar 

  • Peral de Bruno M, Coviello A (1992) Effects of atrial natriuretic peptide and toad heart extract on isolated toad Bufo arenarum aortic rings. Gen Comp Endocrinol 88:424–433

    Article  PubMed  CAS  Google Scholar 

  • Peral de Bruno M, Coviello A (1996) Effects of angiotensin II antagonists on the contractile and hydrosmotic effect of AT II and AT III in the toad (Bufo arenarum). J Comp Physiol B 166:565–570

    Article  Google Scholar 

  • Peral de Bruno M, Lebenshon de Chialvo P, Coviello A (1988) Effects of angiotensin II on isolated toad (Bufo arenarum) aortic rings. Comp Biochem Physiol 90:195–201

    CAS  Google Scholar 

  • Peral de Bruno M, Soria M, Coviello A (1992) Variación del efecto vasoconstrictor de la angiotensina II y la edad: Comparación con otros agonistas. Acta zool Lilloana 41:185–188

    Google Scholar 

  • Peral de Bruno M, Romano L, Coviello A (1996) Interaction between antagonist of angiotensin II and antidiuretic hormone in isolated toad tissues. Comp Biochem Physiol 113:307–314

    Article  Google Scholar 

  • Perry S, Gilmour K, Vulesevic B, McNeill S, Chew F (2005) Circulating catecholamines and cardiorespiratory responses in hypoxic lungfish (Protopterus dolloi): a comparison of aquatic and aerial hypoxia. Physiol Biochem Zool 78:325–334

    Article  PubMed  CAS  Google Scholar 

  • Privat C, Lantoine F, Bedioui F, Millanvoye van Brussel E, Devynck J, Devynck M-A (1997) Nitric oxide production by endothelial cells: comparison of three methods of quantification. Life Sci 61:1193–1202

    Article  PubMed  CAS  Google Scholar 

  • Rea M, Parsons R (2001) Evidence of nitric oxide and angiotensin II regulation of circulation and cutaneous drinking in Bufo marinus. Physiol Biochem Zool 74:127–133

    Article  PubMed  CAS  Google Scholar 

  • Rocha P, Branco L (1997) Cardiovascular, respiratory and metabolic responses to temperature and hypoxia of the winter frog Rana catesbeiana. Braz J Med Biol Res 30:125–131

    PubMed  CAS  Google Scholar 

  • Romano L, Coviello A, Jerez S, Peral de Bruno M (2002) Role of nitric oxide on the vasorelaxant effect of atrial natriuretic peptide on rabbit aorta basal tone. Can J Physiol Pharmacol 80:1022–1029

    Article  PubMed  CAS  Google Scholar 

  • Romero S, Pereira A, Rissato Garófalo M, Hoffmann A (2004) Effects of exercise on plasma catecholamine levels in the toad, Bufo paracnemis: Role of the adrenals and neural control. J Exp Zool Part A: Comp Exp Biol 301A:911–918

    Article  CAS  Google Scholar 

  • Rumbaut R, Mckay M, Huxley V (1995) Capillary hydraulic conductivity is decreased by nitric oxide synthase inhibition. Am J Physiol 37:1856–1861

    Google Scholar 

  • Slivkoff M, Warburton S (2003) An endocrinological update in toads: disparity between the cardiovascular effects of two angiotensin II analogs. Gen Comp End 132:125–132

    Article  CAS  Google Scholar 

  • Solari J, Pozzi A, Ceballos N (2002) Seasonal changes in the activity of cytochrome P450(C17) from the testis of Bufo arenarum. J Comp Physiol 172:685–690

    CAS  Google Scholar 

  • Soria M, Berman D, Coviello A (1987) Comparative effect of angiotensin II on osmotic water permeability in the toad Bufo arenarum. Comp Biochem Physiol 86:147–150

    Article  CAS  Google Scholar 

  • Stephens GA (1984) Angiotensin and norepinephrine effects on isolated vascular strips from a reptile. Gen Comp Endocrinol 54:175–180

    Article  PubMed  CAS  Google Scholar 

  • Taylor P, Scrop M, Tyler D (1982) An ontogenetic and interspecific study of the renin-angiotensin system in australian anuran amphibia. Comp Biochem Physiol 73:187–191

    Article  CAS  Google Scholar 

  • Toda N, Ayajiki K (2006) Phylogenesis of constitutively formed nitric oxide in non-mammals. Physiol Biochem Pharmacol 157:31–80

    CAS  Google Scholar 

  • West N, Kimmel P, Topor Z, Evered M (1998) The role of angiotensin in arterial blood pressure regulation in the toad Bufo marinus. J Exp Biol 201:2219–2224

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was sponsored by grants from the Consejo de Investigaciones de la Universidad Nacional de Tucumán (CIUNT) and the Consejo de Investigaciones Científicas y Técnicas de la República Argentina (CONICET). The experiments comply with the current laws of Tucumán, Argentina.

Author information

Authors and Affiliations

  1. Departmento Biomédico (Or. Fisiología), Facultad de Medicina, Universidad Nacional de Tucumán (UNT), INSIBIO-CONICET, Balcarce 32, 4000, Tucumán, Argentina

    Rodrigo O. Marañón, Claudio M. Joo Turoni & María Peral de Bruno

  2. Departmento de Bioingeniería, UNT, INSIBIO-CONICET, Balcarce 32, 4000, Tucumán, Argentina

    Alfredo Coviello

Authors
  1. Rodrigo O. Marañón
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudio M. Joo Turoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alfredo Coviello
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. María Peral de Bruno
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Peral de Bruno.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marañón, R.O., Joo Turoni, C.M., Coviello, A. et al. Reactivity of isolated toad aortic rings to angiotension II: the role of nitric oxide. J Comp Physiol B 179, 403–409 (2009). https://doi.org/10.1007/s00360-008-0325-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-008-0325-1

Keywords

Search

Navigation