Integration of autonomic and local mechanisms in regulating cardiovascular responses to heating and cooling in a reptile (Crocodylus porosus)

SUMMARY In reptiles, accumulating evidence suggests that nitric oxide (NO) induces a potent relaxation in the systemic vasculature. However, very few studies have examined the source from which NO is derived. Therefore, the present study used both anatomical and physiological approaches to establish whether NO-mediated vasodilation is via an endothelial or neural NO pathway in the large arteries of the estuarine crocodile Crocodylus porosus. Specific endothelial nitric oxide synthase (NOS) staining was observed in aortic endothelial cells following nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) histochemistry and endothelial NOS immunohistochemistry (IHC), suggesting that an endothelial NO pathway is involved in vascular control. This finding was supported by in vitroorgan bath physiology, which demonstrated that the relaxation induced by acetylcholine (10-5 mol l-1) was abolished in the presence of the NOS inhibitor, N-omega-nitro-l-arginine(l-NNA; 10-4 mol l-1), the soluble guanylyl cyclase inhibitor, 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ;10-5 mol l-1), or when the endothelium was removed. Interestingly, evidence for a neural NO pathway was also identified in large arteries of the crocodile. Neural NOS was located in perivascular nerves of the major blood vessels following NADPH-d histochemistry and neural NOS IHC and in isolated aortic rings, l-NNA and ODQ, but not the removal of the endothelium, abolished the relaxation effect of the neural NOS agonist,nicotine (3×10-4 mol l-1). Thus, we conclude that the large arteries of C. porosus are potentially regulated by NO-derived from both endothelial and neural NOS.

Section: Discussionmentioning

confidence: 98%

Dual mechanisms for nitric oxide control of large arteries in the estuarine crocodile Crocodylus porosus

Broughton

Donald

2007

“…Hence, variation at lower frequencies in the power spectrum can be attributed to sympathetic responses, whereas high frequency peaks result from parasympathetic responses; peaks in the mid-frequency range may be either sympathetic or parasympathetic, and peaks at very low frequencies relate to changes in vasomotor tone brought about by local or blood-borne mediators such as angiotensin, for example (Akselrod et al, 1981). Based on previous work on autonomic control of heart rate in ectothermic vertebrates (Seebacher and Franklin, 2004), spectra were divided into four components: ultra low (0.000-0.021 Hz), very low (0.022-0.070 Hz), low , relating to local regulation, sympathetic regulation, sympathetic and/or parasympathetic regulation and parasympathetic regulation, respectively. Spectral analyses were conducted in Chart software (AD Instruments) on resting and maximum heart rate data for cold control and…”

Section: Spectral Analysismentioning

confidence: 99%

Thyroid hormone regulates cardiac performance during cold acclimation in Zebrafish (Danio rerio)

Little

Seebacher

2013

Self Cite

Limitations to oxygen transport reduce aerobic scope and thereby activity at thermal extremes. Oxygen transport in fish is facilitated to a large extent by cardiac function so that climate variability may reduce fitness by constraining the performance of the heart. In zebrafish (Danio rerio), thyroid hormone (TH) regulates skeletal muscle function and metabolism in response to thermal acclimation. Here, we aimed to determine whether TH also regulates cardiac function during acclimation. We used propylthiouracil and iopanoic acid to induce hypothyroidism in zebrafish over a 3 week acclimation period to either 18 or 28°C. We found that cold-acclimated fish had higher maximum heart rates and sarco-endoplasmic reticulum Ca 2+ -ATPase (SERCA) activity than warm-acclimated fish. Hypothyroid treatment significantly decreased these responses in the coldacclimated fish, but it did not affect the warm-acclimated fish. TH did not influence SERCA gene transcription, nor did it increase metabolic rate, of isolated whole hearts. To verify that physiological changes following hypothyroid treatment were in fact due to the action of TH, we supplemented hypothyroid fish with 3,5-diiodothryronine (T 2 ) or 3,5,3′-triiodothyronine (T 3 ). Supplementation of hypothyroid fish with T 2 or T 3 restored heart rate and SERCA activity to control levels. We also show that, in zebrafish, changes in cardiac output in response to warming are primarily mediated by heart rate, rather than by stroke volume. Thus, changes in heart rate are important for the overall aerobic capacity of the fish. In addition to its local effects on heart phenotype, we show that TH increases sympathetic tone on the heart at rest and during maximum exercise. Our findings reveal a new pathway through which fish can mitigate the limiting effects of temperature variability on oxygen transport to maintain aerobic scope and promote thermal tolerance.

“…Cardiovascular responses in reptiles and birds are principally mediated by autonomic mechanisms (Altimiras and Crossley, 2000;Galli et al, 2007;Seebacher and Franklin, 2007) (Fig. 3B), and may also be stimulated locally by nitric oxide and prostaglandins Seebacher and Franklin, 2004). The common pattern of autonomic regulation of cardiovascular responses in mammals and reptiles hint at a broader similarity of efferent thermoregulatory responses that may also encompass control of tissue metabolic capacities.…”

Section: Efferent Pathwaysmentioning

confidence: 99%

Responses to temperature variation: integration of thermoregulation and metabolism in vertebrates

Seebacher

2009

Self Cite

SummaryMany vertebrates regulate their body temperature in response to thermal variability of the environment. Endotherms maintain relatively stable body temperatures by adjusting metabolic heat production in response to varying environmental heat loads. Although most ectotherms do not display adaptive thermogenesis, they do acclimate cellular metabolism to compensate for environmental temperature variation. The components of the thermoregulatory systems in endotherms and ectotherms are evolutionarily conserved, and I suggest that metabolic acclimation in ectotherms relies on the same regulatory pathways as adaptive thermogenesis in endotherms. Both groups rely on transient receptor potential ion channels to sense environmental temperatures. Thermosensory (afferent) information is relayed to the hypothalamus, which initiates a sympathetic efferent response. Cardiovascular responses to heat are similar in ectothermic crocodiles and in mammals, and are mediated by the autonomic nervous system in both cases. The sympathetic nervous system also modulates cellular metabolism by inducing expression of the transcriptional regulator peroxisome proliferator activated receptor γ coactivator 1α (PGC-1α), which interacts with a range of transcription factors that control glycolysis, fatty acid oxidation, gluconeogenesis, mitochondrial biogenesis and bioenergetics, and metabolic rate. PGC-1α is best known from mammalian model species but there is increasing evidence that it is also instrumental in non-mammalian vertebrates. Hence, endothermic adaptive thermogenesis may result from the same regulatory pathways as ectothermic metabolic acclimation, and both could be considered as adaptive metabolic responses to temperature variation.