ANG II and baroreflex control of heart rate in embryonic chickens (Gallus gallus domesticus)

Abstract

Mueller CA, Burggren WW, Crossley II DA. ANG II and baroreflex control of heart rate in embryonic chickens (Gallus gallus domesticus). Am J Physiol Regul Integr Comp Physiol 305: R855-R863, 2013. First published September 4, 2013 doi:10.1152/ajpregu.00298.2013.-ANG II alters the short-term blood pressure buffering capacity of the baroreflex in many adult animals. In embryonic chickens, high plasma ANG II levels contribute to baseline mean arterial pressure (MAP, kPa) without changing heart rate (ƒH, beats/min). We hypothesized, on the basis of these features, that an ANG II-induced reduction in baroreflex sensitivity is present in embryonic chickens as in adults. We examined baroreflex function in day 19 embryonic chickens (Gallus gallus domesticus) after chronic depletion of endogenous ANG II via angiotensinconverting enzyme (ACE) inhibition with captopril (5 mg/kg) from days 5-18 of incubation. The correlation between MAP and ƒH was assessed using increasing doses of sodium nitroprusside, a vasodilator, and phenylephrine, a vasoconstrictor. We used two analytical methods to evaluate baroreflex function: a conventional "static" method, in which maximal MAP and ƒH responses were examined, and a "dynamic" method that assessed beat-to-beat changes during the response to pharmacological manipulation. Captopril-treated embryos were hypotensive by 19% with baroreflex slopes ϳ40% steeper and normalized gains ϳ50% higher than controls, and differences across treatments were similar using either analytical method. Furthermore, reintroduction of ANG II via infusion raised MAP back to control levels and decreased the baroreflex gain in captopril-treated embryos. Therefore, during typical chicken development, ANG II dampens the baroreflex regulatory capacity and chicken embryos can be used as a natural model of elevated ANG II for studying developmental cardiovascular function. This study is the first to demonstrate that reduction of embryonic ANG II alters normal baroreflex function.angiotensin-converting enzyme inhibitor; blood pressure; ANG II infusion; sodium nitroprusside; phenylephrine THE BAROREFLEX IS AN IMPORTANT compensatory mechanism that mitigates short-term changes in arterial pressure. Peripheral limb motor outputs adjust vascular resistance, and cardiac limb motor outputs adjust arterial pressure via heart rate (ƒ H , beats/ min) (37). In the case of the cardiac limb, this negative feedback loop produces an inverse relationship between arterial pressure and ƒ H . Barostatic reflexes are functional during the fetal and adult phases of life, with clear function demonstrated from ϳ60% of development in fetal sheep (5,32,46,49), from ϳ80% of incubation in embryonic chickens (1, 15), and from ϳ70% of incubation in embryonic American alligators (Alligator mississippiensis) (12). The common conclusion from each of these investigations is that baroreflex function is an important homeostatic mechanism during fetal or embryonic life. However, modulation of baroreflex function via systemic hormones and central neurope...

Cardio-respiratory development in bird embryos: new insights from a venerable animal model

“…Thus, most of normal embryonic development of the chicken is characterized by adrenergic cardiac control, with little or no involvement of vagal innervation Burggren and Crossley, 2002). Similar temporal displacement of the onset of numerous components of the renin-angiotensin system and its control of the cardiovascular system is evident from analysis of the literature of ANG II and its effects in chicken embryos Crossley et al, 2010;Mueller et al, 2013a;Mueller et al, 2014a).…”

“…As the embryo and its circulation grow (and in particular as the vessels of the chorioallantoic membrane become accessible), drug injection directly into the blood vessels of the chorioallantoic membrane can be through a "keyhole" in the shell, and in some cases through an indwelling catheter, e.g., Altimiras and Crossley (2000), Burggren and Crossley (2002), Crossley et al (2003a), Crossley et al (2003b), Crossley and Altimiras (2000), Lindgren et al (2011), Mueller et al (2013a, Mueller et al (2014a), and Tintu et al (2009).…”

“…In fact, numerous studies have revealed a temporal mismatch of the onset of functionality of the various regulatory components. For example, the neural and hormonal control of the heart in perinatal birds involves a complex interplay between vagal tone, sympathetic tone, locally acting hormones (e.g., nitric oxide) and circulating hormones such as catecholamines and angiotensin II Crossley and Altimiras, 2000;Burggren and Crossley, 2002;Crossley et al, 2003a;Crossley et al, 2003b;Chiba et al, 2004;Mueller et al, 2013a;Iversen et al, 2014;Mueller et al, 2014a). Both muscarinic and adrenergic receptors are present in the first few days of normal embryonic development in the chicken, potentially enabling both sympathetic and parasympathetic neural control.…”

The nonpharmacological sequence method provides a reliable evaluation of baroreflex sensitivity in fish

“…The baroreflex relies on negative feedback, where altered arterial blood pressure initiates proportional changes in cardiac pulse interval (PI) and systemic vascular conductance to restore pressure (Bagshaw, 1985; Chapleau, 2012; Hedrick et al, 2015; Sandblom & Axelsson, 2005; Van Vliet & West, 1994). Given its importance for cardiovascular regulation, the baroreflex has been characterized under a variety of circumstances in most groups of vertebrates (Armelin et al, 2014, 2016, 2019; Hagensen et al, 2010; La Rovere et al, 2008; Lee et al, 2002; Mueller et al, 2013; Zena et al, 2015; Zena, Dantonio, et al, 2016).…”

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“…It begins with the monitoring of arterial pressure by baroreceptors, which constantly provide the central nervous system with afferent information about the status of this variable. Any increase or decrease in arterial pressure relative to its normal state triggers autonomic responses, which are characterized by an inversely proportional change in heart rate (f H ) and systemic vascular resistance and which tend to restore pressure normality (Bagshaw 1985;Van Vliet and West 1994;Mueller et al 2013;Armelin et al 2014).…”