Evolutionary and comparative aspects of nitric oxide, carbon monoxide and hydrogen sulfide

Olson, Kenneth R.; Donald, John A.; Dombkowski, Ryan A.; Perry, Steve F.

doi:10.1016/j.resp.2012.04.004

Cited by 101 publications

(78 citation statements)

References 101 publications

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“…Curiously, these gases are also postulated to be involved in the endosymbionic event that gave rise to the mitochondria. As categorically reported by Olson et al (246) in their recent review article, using the same authors' words: "over the first 2 gasotransmitters as well as the complexities of their implementation" (246).…”

Section: Gaseous Signaling Moleculesmentioning

confidence: 95%

Gaseous Mediators in Temperature Regulation

Branco

Soriano

Steiner

2014

Comprehensive Physiology

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Deep body temperature (Tb) is kept relatively constant despite a wide range of ambient temperature variation. Nevertheless, in particular situations it is beneficial to decrease or to increase Tb in a regulated manner. Under hypoxia for instance a regulated drop in Tb (anapyrexia) is key to reduce oxygen demand of tissues when oxygen availability is diminished, leading to an increased survival rate in a number of species when experiencing low levels of inspired oxygen. On the other hand, a regulated rise in Tb (fever) assists the healing process. These regulated changes in Tb are mediated by the brain, where afferent signals converge and the most important regions for the control of Tb are found. The brain (particularly some hypothalamic structures located in the preoptic area) modulates efferent activities that cause changes in heat production (modulating brown adipose tissue activity and perfusion, for instance) and heat loss (modulating tail skin vasculature blood flow, for instance). This review highlights key advances about the role of the gaseous neuromodulators nitric oxide (NO), carbon monoxide (CO), and hydrogen sulfide (H2S) in thermoregulation, acting both on the brain and the periphery.

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Section: Gaseous Signaling Moleculesmentioning

confidence: 95%

Gaseous Mediators in Temperature Regulation

Branco

Soriano

Steiner

2014

Comprehensive Physiology

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“…The HO-1/CO system, however, has been well conserved throughout all vertebrates. The amino acid protein sequence of zebrafish (D. rerio) HO-1 bears an 86% identity with goldfish (Carassius auratus; Wang et al, 2008), 60% with Xenopus (Shi et al, 2008) and approximately 50% when compared with mammalian and avian protein sequences (reviewed in Olson et al, 2012). Furthermore, the amino acid sequence of the 'HO signature motif', believed to be important for heme binding and catabolism, shares 92-96% similarity between all vertebrate species investigated to date (Wang et al, 2008).…”

Section: Ho-1/co System In Other Vertebratesmentioning

confidence: 99%

“…Therefore, the HO-1/CO system appears to be a well conserved signalling pathway throughout all extant vertebrates. The reader is referred to a comprehensive review of the HO/CO system by Olson et al (2012) for an in-depth comparison of the function of the HO/CO system in vertebrates.…”

Section: Ho-1/co System In Other Vertebratesmentioning

confidence: 99%

Evidence for a role of heme oxygenase-1 in the control of cardiac function in zebrafish (Danio rerio) larvae exposed to hypoxia

Tzaneva

Perry

2016

Journal of Experimental Biology

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Carbon monoxide (CO) is a gaseous neurotransmitter produced from the breakdown of heme via heme oxygenase-1 (HO-1; hypoxiainducible isoform) and heme oxygenase-2 (HO-2; constitutively expressed isoform). In mammals, CO is involved in modulating cardiac function. The role of the HO-1/CO system in the control of heart function in fish, however, is unknown and investigating its physiological function in lower vertebrates will provide a better understanding of the evolution of this regulatory mechanism. We explored the role of the HO-1/CO system in larval zebrafish (Danio rerio) in vivo by investigating the impact of translational gene knockdown of HO-1 on cardiac function. Immunohistochemistry revealed the presence of HO-1 in the pacemaker cells of the heart at 4 days post-fertilization and thus the potential for CO production at these sites. Sham-treated zebrafish larvae (experiencing normal levels of HO-1) significantly increased heart rate ( f H ) when exposed to hypoxia (Pw O2 =30 mmHg). Zebrafish larvae lacking HO-1 expression after morpholino knockdown (morphants) exhibited significantly higher f H under normoxic (but not hypoxic) conditions when compared with sham-treaded fish. The increased f H in HO-1 morphants was rescued ( f H was restored to control levels) after treatment of larvae with a CO-releasing molecule (40 µmol l −1 CORM). The HO-1-deficient larvae developed significantly larger ventricles and when exposed to hypoxia they displayed higher cardiac output ( _ Q) and stroke volume (SV). These results suggest that under hypoxic conditions, HO-1 regulates _ Q and SV presumably via the production of CO. Overall, this study provides a better understanding of the role of the HO-1/CO system in controlling heart function in lower vertebrates. We demonstrate for the first time the ability for CO to be produced in presumptive pacemaker cells of the heart where it plays an inhibitory role in setting the resting cardiac frequency.

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“…in neonates) is unknown. Although there is an increasing awareness of the physiological significance of gasotransmitters in adult lower vertebrates (Fago et al, 2012;Olson et al, 2012), as in mammals, there are few data concerning their role during early development. To our knowledge, only two studies (Hedrick et al, 2005;Porteus et al, 2014) have systematically compared the interactive effects of gasotransmitters and developmental age and only one of these assessed the O 2 chemosensory response (Porteus et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

A role for nitric oxide in the control of breathing in zebrafish (Danio rerio)

Porteus

Pollack

Tzaneva

et al. 2015

Journal of Experimental Biology

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Nitric oxide (NO) is a gaseous neurotransmitter, which, in adult mammals, modulates the acute hypoxic ventilatory response; its role in the control of breathing in fish during development is unknown. We addressed the interactive effects of developmental age and NO in the control of piscine breathing by measuring the ventilatory response of zebrafish (Danio rerio) adults and larvae to NO donors and by inhibiting endogenous production of NO. In adults, sodium nitroprusside (SNP), a NO donor, inhibited ventilation; the extent of the ventilatory inhibition was related to the pre-existing ventilatory drive, with the greatest inhibition exhibited during exposure to hypoxia (P O2 =5.6 kPa). Inhibition of endogenous NO production using L-NAME suppressed the hypoventilatory response to hyperoxia, supporting an inhibitory role of NO in adult zebrafish. Neuroepithelial cells (NECs), the putative oxygen chemoreceptors of fish, contain neuronal nitric oxide synthase (nNOS). In zebrafish larvae at 4 days post-fertilization, SNP increased ventilation in a concentrationdependent manner. Inhibition of NOS activity with L-NAME or knockdown of nNOS inhibited the hypoxic (P O2 =3.5 kPa) ventilatory response. Immunohistochemistry revealed the presence of nNOS in the NECs of larvae. Taken together, these data suggest that NO plays an inhibitory role in the control of ventilation in adult zebrafish, but an excitatory role in larvae.

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Evolutionary and comparative aspects of nitric oxide, carbon monoxide and hydrogen sulfide

Cited by 101 publications

References 101 publications

Gaseous Mediators in Temperature Regulation

Gaseous Mediators in Temperature Regulation

Evidence for a role of heme oxygenase-1 in the control of cardiac function in zebrafish (Danio rerio) larvae exposed to hypoxia

A role for nitric oxide in the control of breathing in zebrafish (Danio rerio)

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