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Role of Bradykinins and Nitric Oxide in the AT2 Receptor-Mediated Hypotension

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Role of Bradykinins and Nitric Oxide in the AT2 Receptor-Mediated Hypotension Journal of Human Hypertension (2000) 14, Suppl 1, S40–S46 2000 Macmillan Publishers Ltd All rights reserved 0950-9240/00 $15.00 www.nature.com/jhh Role of bradykinins and nitric oxide in the AT2 receptor-mediated hypotension B Sosa-Canache1, M Cierco2, C Ine`s Gutierrez2 and A Israel3 1Clinical Pharmacology Unit, School of Medicine, Universidad “Centroccidental Lisandro Alvarado”; 2School of Medicine, Universidad “Francisco de Miranda” and 3School of Pharmacy, Universidad Central de Venezuela, Venezuela Footshocks increases mean arterial pressure and heart of angiotensin AT1 receptor antagonist. We studied the rate. Systemic or intracerebroventricular (IVT) adminis- role of kinins and nitric oxide in the vasodepressor tration of losartan, a specific angiotensin AT1 receptor response observed after footshocks. The decrease in antagonist, not only inhibited the pressor response to mean arterial pressure observed after footshocks in los- footshocks but resulted in vasodepression. Peripheral artan treated rats was blunted by systemic or IVT admin- or IVT administration of PD 123319, a specific angio- istration of icatibant (HOE 140) or NG-nitro-L-arginine- tensin AT2 receptor antagonist, did not alter the haemo- methyl ester, indicating that peripheral or brain kinins dynamic response to footshocks. However, simul- and nitric oxide are involved in the hypotensor response taneous blockade of angiotensin AT1 and AT2 receptors to footshocks during angiotensin AT1 receptor block- by combined systemic or central administration of los- ade. Our results suggest a role for angiotensin AT2 artan and PD 12319, eliminated the vasodepressor receptor in the regulation of arterial blood pressure, response to footshocks unmasked in losartan pre- possibly through the release of vasodilator autacoids treated rats. Our data suggest that activation of peri- such as bradykinins and nitric oxide. Journal of Human pheral or brain angiotensin AT2 receptor mediated the Hypertension (2000) 14, Suppl 1, S40–S46. vasodepressor response to footshocks in the presence Keywords: angiotensin AT2 receptor; losartan; PD 123319; kinins; nitric oxide synthase; footshocks Introduction antagonist may not be entirely due to blockade of the angiotensin AT1 receptor. Angiotensin receptors Angiotensin II, the primary effector hormone of the comprise two major subtypes, AT and AT .2 Since renin-angiotensin system, has a wide range of 1 2 the angiotensin AT2 receptor is not blocked by losar- physiological actions directed at target organs in the tan, it should be expected that the functions cardiovascular system. These include vasoconstric- mediated via this receptor might be enhanced dur- tion of peripheral blood vessels through activation ing angiotensin AT1 receptor blockade. When the of smooth muscle cell angiotensin AT1 receptors. In angiotensin AT receptor is blocked, plasma and addition to the direct vasoconstrictor action on 1 tissue renin and angiotensins increase markedly;6 vascular smooth muscle, angiotensin II influences angiotensin II may act on angiotensin AT receptors vascular tone due to its ability to enhance nor- 2 which could have an opposite effect such as adrenergic neuroeffector transmission. Findings vasodilation. Thus, one could predict that during from several studies indicate that angiotensin AT 1 footshock-stress, increased levels of angiotensin II receptors are involved in the enhancement of sym- pathetic transmission by angiotensin II.1,2 In effect, would bind to unblocked angiotensin AT2 receptors the angiotensin AT receptor antagonist losartan, but leading to a vasodepressor response. In fact, several 1 studies have demonstrated that angiotensin II can not the angiotensin AT2 receptor antagonist PD 123177, blocks the enhancement of vasoconstriction also induce endothelium-dependent relaxations in responses to renal sympathetic stimulation pro- some types of blood vessels. It has been reported 3 that angiotensin II can elicit a biphasic arterial duced by angiotensin II in the dog and in the pithed 7 8 rat vasculature,4 suggesting an action through stimu- pressure response in rabbits and rats. Furthermore, endothelium-dependent relaxations induced by lation of prejunctional angiotensin AT1 receptors. The concept of a functional role of angiotensin AT angiotensin II have been reported in a variety of 1 9 receptor in the regulation of sympathetic activity is experimental preparations such as the fowl aorta 10 supported by our previous findings showing that and canine renal and cerebral arteries. The hetero- central or peripheral administration of losartan geneity of the response to angiotensin II may be causes inhibition of the vasopressor response elic- related to modulatory effects of the vascular endo- ited by footshocks.5 thelium or stimulation of different angiotensin II Vascular actions of the angiotensin AT1 receptor receptor subtypes. A few studies in rats suggest that the endothelium-dependent vasorelaxation by angiotensin II is mediated by angiotensin AT2 recep- Correspondence: Anita Israel, Apartado postal 50176, Sabana tors thereby counteracting the vasoconstrictor action Grande 1050, Caracas, Venezuela of angiotensin II at the smooth muscle site. Indeed, AT2 receptor, kinins and nitric oxide in footshocks B Sosa-Canache et al S41 in anaesthetized rats blockade of angiotensin AT2 activated protein (MAP) kinases on catecholam- receptors enhances the angiotensin-induced pressor inergic neurons, functional interactions between the response.8 In addition, it has been shown that two receptor subtypes was proposed as the key in angiotensin II degradation products evoked angiotensin II-induced neuromodulatory actions.27 endothelium-dependent relaxations in rat and rabbit When brain AT1 receptors are blocked by losartan, cerebral arterioles, presumably through the acti- it should be expected that the functions mediated 11,12 vation of angiotensin AT2 receptor subtypes. via the AT2 receptor might be enhanced. Angiotensin II may act on angiotensin AT2 receptor Little is known about brain AT2 receptor subtype, either directly or via the release of auta- mediators mechanism underlying the actions of 13,14 coids such as kinins and nitric oxide. In this angiotensin II in vivo. It is known that AT2 receptor respect, it has been shown that in cultured endo- mediate activation of the kinin and nitric oxide (NO) thelial cells, angiotensin II increases nitric oxide- system. Evidence has accumulated for the existence dependent cyclic guanosine monophosphate of a brain kallikrein-kinin system28 and bradykinin (cGMP) production through the stimulation of the B2 receptors have been characterised in brain struc- angiotensin AT2 receptor, which in turn leads to an tures in which the renin-angiotensin system is enhanced release of bradykinin.15 expressed and known to participate in the regu- Some of the actions of angiotensin II are centrally lation of blood pressure.29 In addition, NOS is also mediated. Indeed, in brain angiotensin II has a wide expressed in the same brain regions in which the range of physiological actions which include renin-angiotensin system is localized, providing increase in blood pressure, arginine-vasopressin potential anatomical substrate for interactions release, promotion of drinking behaviour and natri- between angiotensin II and NO.30 Based on the ana- uresis.16 These actions have been attributed mainly tomical and functional evidence, it appears that to the activation of various signalling transduction angiotensin II actions may be mediated by an inter- pathways modulated by angiotensin type I receptor play of central mechanisms involving kinins and since they could be antagonized by AT1 receptor nitric oxide. blockers.2,17–19 Brain angiotensin also enhances In the present study, we tested the hypothesis that adrenergic tone by central activation and facilitation in losartan treated rats, footshocks would result in of sympathetic transmission20 and increasing cat- a vasodepressor response due not only to blockade 21 echolamine turnover in sympathetic brain nuclei. of the angiotensin AT1 receptor but also activation Since central blockade of AT1 receptor with losartan of the angiotensin AT2 sites and the release of nitric significantly attenuates the pressor response to sym- oxide or kinins. Toward this end, we assessed the pathetic stimulation-induced haemorrhage,22 immo- effect of systemic or intracerebroventricular admin- bilization stress23 and footshocks,5 a role for brain istration of losartan and/or PD123319, on the cardio- AT1 receptors has been suggested in the facilitation vascular response to footshocks. This experimental of noradrenergic transmission and pressor response model is known to cause sympathoadrenal and neu- to stress. Indeed, in various brain nuclei relevant to roendocrine activation.31 In addition, to ascertain cardiovascular control, AT1 receptor activation regu- the role of kinins or nitric oxide on the vasodep- lates uptake, synthesis and release of noradrenaline ressor responses to footshocks, experiments were and dopamine.21,24 performed in the presence of losartan and/or icatib- The role of brain angiotensin AT2 receptor is not ant (HOE 140), a kinin B2 receptor antagonist or G as clear as the angiotensin AT1 receptor, and no N —nitro-L-arginine-methyl ester (L-NAME) a nitric direct evidence for an involvement of central angio- oxide synthase inhibitor. tensin AT2 receptors in the sympathetic response to stress has been presented so far. AT2 receptor is expressed at very high levels in the developing
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