Desensitisation of chromaffin cell nicotinic receptors does not impede catecholamine secretion during acute hypoxia in rainbow trout (Oncorhynchus mykiss)

2000 ◽  
Vol 203 (10) ◽  
pp. 1589-1597 ◽  
Author(s):  
K.N. Lapner ◽  
C.J. Montpetit ◽  
S.F. Perry
Keyword(s):  
Nicotinic Receptor ◽  
Nicotinic Receptors ◽  
Acute Hypoxia ◽  
Plasma Catecholamine ◽  
Cardinal Vein ◽  
Plasma Adrenaline ◽  
Rainbow Trout Oncorhynchus Mykiss ◽  
Posterior Cardinal Vein ◽  
Receptor Desensitisation

Experiments were performed on adult rainbow trout (Oncorhynchus mykiss) in vivo using chronically cannulated fish and in situ using a perfused posterior cardinal vein preparation (i) to characterise the desensitisation of chromaffin cell nicotinic receptors and (ii) to assess the ability of fish to secrete catecholamines during acute hypoxia with or without functional nicotinic receptors. Intra-arterial injection of nicotine (6.0×10(−)(7)mol kg(−)(1)) caused a rapid increase in plasma adrenaline and noradrenaline levels; the magnitude of this response was unaffected by an injection of nicotine given 60 min earlier. Evidence for nicotinic receptor desensitisation, however, was provided during continuous intravenous infusion of nicotine (1.3×10(−)(5)mol kg(−)(1)h(−)(1)) in which plasma catecholamine levels increased initially but then returned to baseline levels. To ensure that the decline in circulating catecholamine concentrations during continuous nicotine infusion was not related to changes in storage levels or altered rates of degradation/clearance, in situ posterior cardinal vein preparations were derived from fish previously experiencing 60 min of saline or nicotine infusion. Confirmation of nicotinic receptor desensitisation was provided by demonstrating that the preparations derived from nicotine-infused fish were unresponsive to nicotine (10(−)(5)mol l(−)(1)), yet remained responsive to angiotensin II (500 pmol kg(−)(1)). The in situ experiments demonstrated that desensitisation of the nicotinic receptor occurred within 5 min of receptor stimulation and that resensitisation was established 40 min later. The ability to elevate plasma catecholamine levels during acute hypoxia (40–45 mmHg; 5.3-6.0 kPa) was not impaired in fish experiencing nicotinic receptor desensitisation. Indeed, peak plasma adrenaline levels were significantly higher in the desensitised fish during hypoxia than in controls (263+/−86 versus 69+/−26 nmol l(−)(1); means +/− s.e.m., N=6-9). Thus, the results of the present study demonstrate that activation of preganglionic sympathetic cholinergic nerve fibres and the resultant stimulation of nicotinic receptors is not the sole mechanism for eliciting catecholamine secretion during hypoxia.

scholarly journals Vasoactive intestinal polypeptide- and pituitary adenylate cyclase activating polypeptide-mediated control of catecholamine release from chromaffin tissue in the rainbow trout, Oncorhynchus mykiss

2000 ◽  
Vol 166 (3) ◽  
pp. 705-714 ◽  
Author(s):  
CJ Montpetit ◽  
SF Perry
Keyword(s):  
Rainbow Trout ◽  
Chromaffin Cells ◽  
Catecholamine Secretion ◽  
Cardinal Vein ◽  
Rainbow Trout Oncorhynchus Mykiss ◽  
Neuronal Control ◽  
Pituitary Adenylate Cyclase ◽  
Posterior Cardinal Vein ◽  
Chromaffin Tissue

The aim of the present investigation was to assess the relative contributions of cholinergic (acetylcholine) and non-cholinergic vasoactive intestinal polypeptide (VIP), and pituitary adenylate cyclase activating polypeptide (PACAP) neurotransmitters in the neuronal control of catecholamine secretion from the chromaffin tissue lining the posterior cardinal vein of the rainbow trout (Oncorhynchus mykiss). Using an in situ saline-perfused posterior cardinal vein preparation, it was demonstrated that exogenous administration of chicken VIP or human PACAP-27 caused a dose-dependent increase in adrenaline secretion; noradrenaline secretion was unaffected. Analysis of dose-response curves indicated that VIP and PACAP stimulated the secretion of adrenaline with a similar degree of potency (ED(50) for VIP=1.90x10(-11) mol/kg; ED(50) for PACAP=1.03x10(-11) mol/kg). The VIP/PACAP-elicited secretion was diminished in the presence of the VIP receptor antagonist, VIP 6-28, but was unaffected by the PACAP receptor antagonist, PACAP 6-27, or the cholinergic antagonists, hexamethonium and atropine. Thus, this is the first study to demonstrate a direct stimulatory role for VIP or PACAP in catecholamine secretion from piscine chromaffin cells. The relative contribution of cholinergic and non-cholinergic neurotransmitters in the neuronal control of catecholamine secretion from the chromaffin tissue was evaluated using an in situ nerve-stimulating technique previously validated by us in the rainbow trout. This was accomplished by comparing catecholamine secretion in the presence or absence of cholinergic and the VIP and PACAP receptor antagonists during different levels of electrical stimulation. The results demonstrated that cholinergic stimulation predominated during high frequency of electrical stimulation (20 Hz) while the non-cholinergic component prevailed at low frequency (1 Hz). Overall, the results of the present investigation demonstrate that VIP and/or PACAP may directly stimulate adrenaline secretion from trout chromaffin cells at low levels of neuronal activity. Therefore, the neuronal control of catecholamine secretion in teleosts may not be confined to cholinergic-evoked events.

scholarly journals The effects of acute hypoxia on chemically or neuronally induced catecholamine secretion in rainbow trout (Oncorhynchus mykiss) in situ and in vivo

2000 ◽  
Vol 203 (9) ◽  
pp. 1487-1495 ◽  
Author(s):  
S.F. Perry ◽  
C.J. Montpetit ◽  
M. Borowska
Keyword(s):  
Rainbow Trout ◽  
Oncorhynchus Mykiss ◽  
Muscarinic Receptor ◽  
Acute Hypoxia ◽  
Catecholamine Secretion ◽  
Cardinal Vein ◽  
Rainbow Trout Oncorhynchus Mykiss ◽  
Catecholamine Levels

The potential direct and modulating effects of acute hypoxia on catecholamine secretion in rainbow trout (Oncorhynchus mykiss) were assessed in situ, using a perfused cardinal vein preparation, and in vivo, using chronically cannulated fish. Acute (10 min) perfusion with hypoxic (P(O2)<10 mmHg) saline or homologous hypoxic blood did not have a statistically significant effect on basal (non-stimulated) catecholamine secretion. A field stimulation technique was used to excite the sympathetic nerves innervating the chromaffin cells electrically in situ under conditions of high-P(O2) (saline P(O2)=152 mmHg; 1 mmHg=0.133 kPa) or low-P(O2) (saline P(O2)<10 mmHg) perfusion at constant P(CO2) (2.3 mmHg). The results demonstrated that neuronally evoked catecholamine secretion was significantly lowered by 50 % during perfusion with hypoxic saline. To assess whether the inhibitory effect of hypoxia during neuronal stimulation in situ resulted from modulation of nicotinic and/or muscarinic receptor-linked pathways, perfused posterior cardinal vein preparations were injected with selective nicotinic (10(−)(7) or 10(−)(6)mol kg(−)(1) nicotine) or muscarinic (10(−)(3)mol kg(−)(1) methacholine) receptor agonists. For both doses of nicotine, catecholamine secretion was significantly lowered during hypoxia by 55 %. During muscarinic receptor stimulation, perfusion with hypoxic saline caused a 42 % reduction in the rate of catecholamine secretion. In contrast, catecholamine secretion elicited by depolarising levels of KCl (60 mmol l(−)(1)) was unaffected by the oxygen status of the perfusate. In vivo, intra-arterial injections of nicotine (300–600 nmol kg(−)(1)) into normoxic (water P(O2)=155 mmHg) or moderately hypoxic fish (water P(O2)=80 mmHg) caused a dose-dependent elevation of circulating catecholamine levels. However, despite the inhibitory influence of localised hypoxia on chromaffin cell responsiveness previously demonstrated in situ, the increase in plasma catecholamine levels after intra-arterial injection of nicotine was significantly enhanced in the hypoxic fish. The differences between the results from the in vivo and in situ experiments may reflect the contribution of higher control centres and modulating factors in vivo that are absent in situ.

The role of angiotensin II in regulating catecholamine secretion during hypoxia in rainbow troutOncorhynchus mykiss

2001 ◽  
Vol 204 (23) ◽  
pp. 4169-4176
Author(s):  
Katherine N. Lapner ◽  
Steve F. Perry
Keyword(s):  
Nicotinic Receptor ◽  
Nicotinic Receptors ◽  
Renin Angiotensin System ◽  
Catecholamine Release ◽  
Plasma Catecholamine ◽  
Converting Enzyme ◽  
Angiotensin System ◽  
Renin Angiotensin ◽  
Catecholamine Levels ◽  
Receptor Desensitisation

SUMMARYExperiments were performed in vivo on chronically cannulated adult rainbow trout (Oncorhynchus mykiss) to assess the involvement of serotonergic or muscarinic receptor stimulation or activation of the renin–angiotensin system in eliciting catecholamine release during acute hypoxia during periods of nicotinic receptor desensitisation.Despite nicotinic receptor desensitisation induced by intravenous infusion of nicotine (1.3×10–5 mol kg–1 h–1), plasma catecholamine levels were increased to levels (adrenaline plus noradrenaline 125–200 nmol l–1) similar to those in control fish during severe hypoxia (40–45 mmHg; 5.3–6.0 kPa). Blockade of serotonergic receptors using methysergide or of muscarinic receptors using atropine did not affect the ability of fish to elevate circulating catecholamine levels during hypoxia. However, selective blockade of the renin–angiotensin system, using lisinopril to inhibit angiotensin-converting enzyme, prevented the elevation of both angiotensin II and circulating catecholamine levels in acutely hypoxic fish experiencing nicotinic receptor desensitisation. In fish possessing functional nicotinic receptors, angiotensin-converting enzyme blockade attenuated but did not prevent the elevation of plasma catecholamine levels during hypoxia. The results of this study indicate that the renin–angiotensin system is activated during hypoxia and plays a role in eliciting catecholamine release that is secondary to activation of nicotinic receptors. However, under conditions of nicotinic receptor desensitisation, activation of the renin–angiotensin system during hypoxia is a prerequisite for catecholamine release.

THE EFFECTS OF ACCLIMATION TEMPERATURE ON THE DYNAMICS OF CATECHOLAMINE RELEASE DURING ACUTE HYPOXIA IN THE RAINBOW TROUT ONCORHYNCHUS MYKISS

1994 ◽  
Vol 186 (1) ◽  
pp. 289-307 ◽  
Author(s):  
S. Perry ◽  
S. Reid
Keyword(s):  
Rainbow Trout ◽  
Acute Hypoxia ◽  
Catecholamine Release ◽  
Acclimation Temperature ◽  
Plasma Catecholamine ◽  
Blood Oxygen ◽  
Rainbow Trout Oncorhynchus Mykiss ◽  
Arterial Blood ◽  
The Difference ◽  
Catecholamine Levels

The response of cannulated rainbow trout (Oncorhynchus mykiss) to acute hypoxia was studied in fish acclimated to two temperatures (5 and 15 °C). Blood/water respiratory variables and plasma catecholamine levels were measured before and 15 min after exposure to hypoxic water varying between 4.0 and 10.7 kPa (30–80 mmHg) oxygen partial pressure (PwO2). Arterial blood PO2 (PaO2) and oxygen content (CaO2) fell during hypoxia in a similar manner at both temperatures, although the changes in CaO2 were often more pronounced in the fish acclimated to 15 °C. Regardless of acclimation temperature, plasma catecholamine levels were consistently elevated at PwO2 values below 8.0 kPa (60 mmHg); the largest increases in plasma catecholamine levels occurred below PwO2=5.3 kPa (40 mmHg). Adrenaline was the predominant catecholamine released into the circulation. Adrenaline was released at PwO2 values of 8.0 kPa or below, whereas noradrenaline was released at PwO2 values of 6.7 kPa or below. The construction of in vivo oxygen dissociation curves demonstrated an obvious effect of acclimation temperature on haemoglobin (Hb) oxygen-affinity; the P50 values at 15 °C and 5 °C were 3.6 kPa (26.7 mmHg) and 1.9 kPa (14.0 mmHg), respectively. At 15 °C, catecholamines were released into the circulation abruptly at a PaO2 threshold of 4.6 kPa (34.5 mmHg) while at 5 °C the catecholamine release threshold was lowered to 3.3 kPa (24.5 mmHg). The difference in the PaO2 catecholamine release thresholds was roughly equivalent to the difference in the P50 values at the two distinct temperatures. Catecholamine release thresholds, calculated on the basis of arterial blood oxygen-saturation (expressed as CaO2/[Hb]), were similar at both temperatures and were approximately equal to 53–55 % Hb O2-saturation. The results support the contention that the lowering of blood oxygen content/saturation rather than PO2 per se is the proximate stimulus/signal causing catecholamine release in rainbow trout during acute hypoxia.

Hydrogen sulfide stimulates catecholamine secretion in rainbow trout (Oncorhynchus mykiss)

2009 ◽  
Vol 296 (1) ◽  
pp. R133-R140 ◽  
Author(s):  
Steve F. Perry ◽  
Brian McNeill ◽  
Eshay Elia ◽  
Ashish Nagpal ◽  
Branka Vulesevic
Keyword(s):  
Hydrogen Sulfide ◽  
Rainbow Trout ◽  
Chromaffin Cells ◽  
Acute Hypoxia ◽  
Electrical Field Stimulation ◽  
Catecholamine Secretion ◽  
Cardinal Vein ◽  
Posterior Cardinal Vein ◽  
Stimulation Of

We tested the hypothesis that endogenously produced hydrogen sulfide (H2S) can potentially contribute to the adrenergic stress response in rainbow trout by initiating catecholamine secretion from chromaffin cells. During acute hypoxia (water Po2 = 35 mmHg), plasma H2S levels were significantly elevated concurrently with a rise in circulating catecholamine concentrations. Tissues enriched with chromaffin cells (posterior cardinal vein and anterior kidney) produced H2S in vitro when incubated with l-cysteine. In both tissues, the production of H2S was eliminated by adding the cystathionine β-synthase inhibitor, aminooxyacetate. Cystathionine β-synthase and cystathionine γ-lyase were cloned and sequenced and the results of real-time PCR demonstrated that with the exception of white muscle, mRNA for both enzymes was broadly distributed within the tissues that were examined. Electrical field stimulation of an in situ saline-perfused posterior cardinal vein preparation caused the appearance of H2S and catecholamines in the outflowing perfusate. Perfusion with the cholinergic receptor agonist carbachol (1 × 10−6 M) or depolarizing levels of KCl (1 × 10−2 M) caused secretion of catecholamines without altering H2S output, suggesting that neuronal excitation is required for H2S release. Addition of H2S (at concentrations exceeding 5 × 10−7 M) to the perfusion fluid resulted in a marked stimulation of catecholamine secretion that was not observed when Ca2+-free perfusate was used. These data, together with the finding that H2S-induced catecholamine secretion was unaltered by the nicotinic receptor blocker hexamethonium, suggest that H2S is able to directly elicit catecholamine secretion via membrane depolarization followed by Ca2+-mediated exocytosis.

scholarly journals Control of Catecholamine Release In Vivo and In Situ in the Atlantic Cod (Gadus Morhua) During Hypoxia

1991 ◽  
Vol 155 (1) ◽  
pp. 549-566 ◽  
Author(s):  
STEVE F. PERRY ◽  
REGINA FRITSCHE ◽  
RICHARD KINKEAD ◽  
STEFAN NILSSON
Keyword(s):  
Gadus Morhua ◽  
Atlantic Cod ◽  
Head Kidney ◽  
Plasma Catecholamine ◽  
Plasma Adrenaline ◽  
Catecholamine Levels ◽  
Chromaffin Tissue ◽  
Stimulation Of

We have characterized the elevation of circulating catecholamines in the intact Atlantic cod (Gadus morhua) during graded acute (30 min) hypoxia. The potential mechanisms contributing to the mobilization of catecholamines during hypoxia were then assessed in vivo using nerve sectioning and pharmacological techniques and in situ using a perfused head kidney preparation. Pre-branchial plasma adrenaline concentrations were significantly elevated at all levels of aquatic hypoxia utilised [water Po2 (PWO2) = 10 kPa (75 mmHg), 7.3kPa (55 mmHg) or 5.3 kPa (40 mmHg)], whereas noradrenaline levels did not increase significantly in these particular experiments in which PWWOWO2 was lowered gradually over a 30 min period. All subsequent experiments were performed using a more rapid induction of hypoxia to reach a final PWWOWO2 of 5.3 kPa within the first 57–10 min of exposure. Blood withdrawn from pre-branchial (ventral aortic) and post-branchial (dorsal aortic) cannulae after 30 min revealed pronounced reductions in POO2 and O2 content (CO2) as well as elevated pH. These data support the notion that blood acidosis is not a prerequisite for catecholamine mobilization during hypoxia. Bilateral sectioning of spinal nerves 17-4 innervating the head kidney prevented the elevation of noradrenaline during rapidly induced hypoxia, but had no effect on the rise in plasma adrenaline concentration. After each experiment, fish were exposed to air for 3 min to induce severe stress. Plasma catecholamine levels were significantly reduced during stress, suggesting that the sectioning of the spinal nerves to the head kidney was indeed effective. These results indicated that mechanisms other than neural stimulation of head kidney chromaffin tissue were contributing to the rise in plasma adrenaline level during hypoxia. Neuronal overflow into the circulation, however, was an unlikely possibility since the increase of adrenaline could not be prevented by treating denervated fish with bretylium (an inhibitor of catecholamine release from adrenergic nerve terminals). These data suggested a local direct stimulatory effect of blood hypoxaemia on adrenaline release from chromaffin tissue. This hypothesis was confirmed using a blood-perfused head kidney preparation in which hypoxaemia markedly stimulated adrenaline overflow into the effluent blood. Further experiments using a Ringer-perfused head kidney preparation were designed to test the hypothesis that blood catecholamine levels in vivo are, in part, controlled by the concentration of catecholamines in the blood entering the head kidney. The results show conclusively that overflow of a particular catecholamine during cholinergic stimulation of the head kidney is controlled independently by the inflowing concentration of that catecholamine. We suggest that this mechanism of ‘auto-inhibition’ of catecholamine overflow is a functional negative feedback mechanism involved in the control of plasma catecholamine levels in the cod.

Plasma Concentrations of Catecholamines in Two Strains of Spontaneously Hypertensive Rats at Different Ages

1981 ◽  
Vol 61 (s7) ◽  
pp. 199s-202s ◽  
Author(s):  
P. Ferrari ◽  
G. B. Picotti ◽  
E. Minotti ◽  
G. P. Bondiolotti ◽  
A. M. Caravaggi ◽  
...  
Keyword(s):  
Blood Pressure ◽  
Plasma Concentrations ◽  
Plasma Catecholamine ◽  
Hypertensive Rats ◽  
Adult Rats ◽  
Plasma Adrenaline ◽  
Spontaneously Hypertensive ◽  
Wistar Kyoto ◽  
Normotensive Strain ◽  
Noradrenaline And Adrenaline

1. Blood pressure was measured and plasma levels of noradrenaline and adrenaline were determined radioenzymatically under basal conditions and after 10% blood volume reduction in blood drawn through catheters previously implanted in young and adult rats of two different genetically hypertensive strains: the Kyoto strain (SHR) and the Milan strain (MHS), and in their respective controls: Wistar—Kyoto strain (WKY) and Milan normotensive strain (MNS). 2. Under basal conditions no differences were observed between plasma noradrenaline and adrenaline levels in SHR and MHS rats and in the controls, at any age. Haemorrhage produced a greater fall in the blood pressure (P < 0.01) of young and adult hypertensive strains (SHR-MHS) than in WKY and MNS rats, and a greater rise in plasma adrenaline (P < 0.01). 3. These results suggest that: (a) there may be differences in involvement of the sympathetic nervous system in the pathogenesis of hypertension in SHR and MHS rats but not such as to cause differences in plasma catecholamine levels in either young or adult rats; (b) haemorrhage activates the sympatho—adrenal systems more in SHR and MHS rats, than in controls, and the greater percentage fall in blood pressure is probably due to a difference in reflex venoconstriction.

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