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Gaseous Mediators in Temperature Regulation

Luiz G.S. Branco, Renato N. Soriano, Alexandre A. Steiner

10.1002/cphy.c130053

Source: Volume 4, Issue 4, October 2014

Published online: September 2014

Full Article on Wiley Online Library



Abstract

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. © 2014 American Physiological Society. Compr Physiol 4:1301‐1338, 2014.

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Figure 1. Figure 1. Relationship between ambient temperature and the activity of thermoeffectors in euthermia (A), fever (B), and anapyrexia (C). Values for temperature thresholds and preferred ambient temperatures are approximations based on the thermal biology of the laboratory rat (271). Arrows indicate the possible direction (or directions) of the change in thermoeffector activity. TNZ, thermoneutral zone.
Figure 2. Figure 2. The nitric oxide (NO) pathway and the pharmacological tools available to study the NO signaling pathway. NO arises from the cleavage of L‐arginine by NOS and acts mainly through sGC, cGMP, and PKG. Abbreviations: NOS, nitric oxide synthase; NO, nitric oxide; sGC, soluble guanylate cyclase; cGMP, cyclic guanosine monophosphate; PKG, protein kinase G.
Figure 3. Figure 3. Nitric oxide (NO) activates soluble guanylate cyclase (sGC), yielding increased levels of cyclic GMP (cGMP) and, consequently, vasodilation. Besides, NO may also cause vasodilation acting via potassium channels and hyperpolarization.
Figure 4. Figure 4. Role of NO in brown adipose tissue (BAT) thermogenesis. NO has been postulated to facilitate BAT thermogenesis through different actions: facilitating norepinephrine release onto brown adipocytes; causing vasodilation in arteries/arterioles that irrigate BAT, increasing BAT blood flow. Moreover, it has been shown that NO favors glucose breakdown, mitochondrial activity, and fatty‐acid oxidation in brown adipocytes.
Figure 5. Figure 5. Role of NO in skeletal muscle contractility. Skeletal muscles are known to generate heat mainly during shivering, thus functioning as a powerful thermoeffector that helps to maintain Tb when the animal is exposed to cold and to increase Tb to mount the febrile response to pyrogens or psychological stresses. Increased intracellular Ca2+ levels are normally observed when nicotinic receptors are activated to produce contraction. It is well known in other tissues that the increase in Ca2+ activates NOS, leading to heightened production of NO. In skeletal muscles is not different. Interesting are the facts that increased levels of NO inhibit skeletal muscle contraction despite favoring glucose transport and increasing blood flow to the muscle.
Figure 6. Figure 6. Effects of central NO on euthermic control of deep body temperature (Tb). Microinjection of L‐NAME (a nonselective NOS inhibitor) into the lateral ventricle (LV) has led to the conclusion that central NO has either no effect on Tb or causes a slight reduction in Tb. Interestingly, NO does not affect Tb when its production is inhibited with L‐NMMA (another nonselective NOS inhibitor) in the most caudal brain ventricle, that is, the fourth ventricle (4V).
Figure 7. Figure 7. Effects of central NO on fever induced by LPS. Microinjection of inhibitors of iNOS or nNOS into the lateral ventricle (LV) has led to the conclusion that central NO favors the occurrence of fever. Conversely, microinjection of a nonselective inhibitor of NOS into the fourth ventricle (4V) has suggested that NO does not alter LPS fever when its production is inhibited predominantly in the most caudal brain ventricle.
Figure 8. Figure 8. Effects of NO within specific regions of the brain. Microinjection of L‐NMMA (a nonselective NOS inhibitor) within the AVPO has led to the conclusion that AVPO NO attenuates LPS fever. Conversely, it has been demonstrated that locus coeruleus (LC) NO exacerbates LPS fever.
Figure 9. Figure 9. Role of preoptic area of the hypothalamus (POA) nitric oxide (NO) in lipopolysaccharide (LPS)‐induced fever. Systemic LPS has been shown to reduce NOS activity, diminishing the levels of NO in the POA. It is believed that lowered levels of NO in the POA relieve (dashed arrow) the activity of the intracellular cascade (COX‐2/mPGES‐1/PGE2) classically known as the responsible for fever generation. Interestingly, besides inducing fever, this cascade appears to downmodulate a cascade known to downmodulates fever: AC/cAMP/PKA, thus further favoring the febrile response. Reduced levels of POA NO downmodulate its classical cascade, which in the POA is a cascade that attenuates fever: NO/sGC/cGMP/PKG, thus facilitating the regulated increase in deep body temperature (Tb), that is, fever. Abbreviations: COX‐2, cyclooxygenase‐2; mPGES‐1, inducible microsomal PGE synthase‐1; PGE2, prostaglandin E2; AC, adenylate cyclase; cAMP, cyclic adenosine monophosphate; PKA, protein kinase A; NOS, nitric oxide synthase; NO, nitric oxide; sGC, soluble guanylate cyclase; cGMP, cyclic guanosine monophosphate; PKG, protein kinase G.
Figure 10. Figure 10. Effects of central NO on anapyrexia induced by hypoxia. Microinjection of L‐NAME (a nonselective NOS inhibitor) into the lateral ventricle (LV) has led to the conclusion that central NO seems to be essential to the occurrence of hypoxia‐induced anapyrexia.
Figure 11. Figure 11. Role of preoptic area of the hypothalamus (POA) nitric oxide (NO) in hypoxia‐induced anapyrexia. Reduced inspired levels of oxygen (hypoxia) stimulate the production of NO in the POA. Once the levels of NO are augmented in the POA, the intracellular cascade that favors the regulated drop in Tb (anapyrexia) is heightened. This intracellular cascade is composed basically of sGC, cGMP, and PKG. These molecules ultimately favor the occurrence of anapyrexia. Abbreviations: NOS, nitric oxide synthase; NO, nitric oxide; sGC, soluble guanylate cyclase; cGMP, cyclic guanosine monophosphate; PKG, protein kinase G.
Figure 12. Figure 12. The carbon monoxide (CO) pathway and the pharmacological tools available to study the CO signaling pathway. Metabolism of heme is catalyzed by the enzyme heme oxygenase (HO). Heme catabolism by (HO) yields biliverdin, iron, and CO. CO may activate the cyclic guanosine monophosphate (cGMP)‐synthesizing enzyme soluble guanylyl cyclase (sGC). Therefore, activation of sGC leads to elevated levels of cGMP, which in turn activates protein kinase G (PKG).
Figure 13. Figure 13. Role of central nervous system (CNS) carbon monoxide (CO) in febrile response to lipopolysaccharide (LPS). It is well known that systemic administration of a fever‐inducing dose of LPS induces in the CNS the following fever‐inducing signaling cascade: COX‐2/mPGES‐1/PGE2, which in the fever‐originating center of the brain, the preoptic area of the hypothalamus (POA), evokes appropriate thermoefferent signals that ultimately results in a regulated increase in deep body temperature (Tb), that is, fever. Systemic LPS seems to stimulate the enzyme heme oxygenase to increase the generation of CO in the CNS. Central CO, in region(s) other than the POA, has been suggested to act as a propyretic molecule. Abbreviations: COX‐2, cyclooxygenase‐2; mPGES‐1, inducible microsomal PGE synthase‐1; PGE2, prostaglandin E2.
Figure 14. Figure 14. Role of central carbon monoxide (CO) in hypoxia‐induced anapyrexia. Preoptic area of the hypothalamus (POA) CO has been shown not to participate in the control of anapyrexic response to hypoxia. Conversely, the results obtained from inhibition of heme oxygenase (HO), the CO‐synthesizing enzyme, in the cerebroventricular system suggests that central CO downmodulates hypoxia‐induced anapyrexia.
Figure 15. Figure 15. Biosynthesis of hydrogen sulfide (H2S). Three enzymatic pathways are involved in the biosynthesis of H2S. Cystathionine β‐synthase (CBS) produces H2S via the generation of cystathionine from homocysteine and L‐cysteine from cystathione. Cystathionine γ‐lyase (CSE) produces H2S by producing L‐cysteine from cystathionine. 3‐mercaptopyruvate sulfur transferase (3MST) produces H2S via the production of 3‐mercaptopyruvate (3MP) from α‐ketoglutarate (α‐KG) by cysteine aminotransferase (CAT). H2S, endogenously produced in the donor cell, seems to act predominantly via adenylate cyclase (AC)/cyclic adenosine monophosphate (cAMP) and/or modulating ATP‐dependent potassium (K+ATP) channels in the target cell.
Figure 16. Figure 16. Role of preoptic area of the hypothalamus (POA) hydrogen sulfide (H2S) in hypoxia‐induced anapyrexia. Exposure to hypoxia (7% oxygen in inspired air) is known to induce CBS activity, elevating H2S levels in the POA. Increased levels of POA H2S stimulates an intracellular cascade, composed of AC, cAMP, and PKA, which is believed to be essential to the occurrence of the anapyrexic response to hypoxia. Abbreviations: CBS, cystathionine β‐synthase; AC, adenylate cyclase; cAMP, cyclic adenosine monophosphate; PKA, protein kinase A.
Figure 17. Figure 17. Role of preoptic area of the hypothalamus (POA) hydrogen sulfide (H2S) in fever induced by systemic administration of lipopolysaccharide (LPS). Systemic LPS has been shown to suppress CBS activity, reducing H2S levels in the POA. It is believed that reduced levels of H2S in the POA relieve (gray dashed arrow) the activity of the intracellular cascade (COX‐2/mPGES‐1/PGE2) responsible for fever generation. It is well known that this cascade induces fever. Interestingly, besides inducing fever, this cascade appears to downmodulate the cascade known to downmodulate fever: AC/cAMP/PKA. Reduced levels of POA H2S are believed to downmodulate the latter cascade as well (gray, curved dashed arrow). Abbreviations: Tb, deep body temperature; COX‐2, cyclooxygenase‐2; mPGES‐1, inducible microsomal PGE synthase‐1; PGE2, prostaglandin E2; AC, adenylate cyclase; cAMP, cyclic adenosine monophosphate; PKA, protein kinase A.


Figure 1. Relationship between ambient temperature and the activity of thermoeffectors in euthermia (A), fever (B), and anapyrexia (C). Values for temperature thresholds and preferred ambient temperatures are approximations based on the thermal biology of the laboratory rat (271). Arrows indicate the possible direction (or directions) of the change in thermoeffector activity. TNZ, thermoneutral zone.


Figure 2. The nitric oxide (NO) pathway and the pharmacological tools available to study the NO signaling pathway. NO arises from the cleavage of L‐arginine by NOS and acts mainly through sGC, cGMP, and PKG. Abbreviations: NOS, nitric oxide synthase; NO, nitric oxide; sGC, soluble guanylate cyclase; cGMP, cyclic guanosine monophosphate; PKG, protein kinase G.


Figure 3. Nitric oxide (NO) activates soluble guanylate cyclase (sGC), yielding increased levels of cyclic GMP (cGMP) and, consequently, vasodilation. Besides, NO may also cause vasodilation acting via potassium channels and hyperpolarization.


Figure 4. Role of NO in brown adipose tissue (BAT) thermogenesis. NO has been postulated to facilitate BAT thermogenesis through different actions: facilitating norepinephrine release onto brown adipocytes; causing vasodilation in arteries/arterioles that irrigate BAT, increasing BAT blood flow. Moreover, it has been shown that NO favors glucose breakdown, mitochondrial activity, and fatty‐acid oxidation in brown adipocytes.


Figure 5. Role of NO in skeletal muscle contractility. Skeletal muscles are known to generate heat mainly during shivering, thus functioning as a powerful thermoeffector that helps to maintain Tb when the animal is exposed to cold and to increase Tb to mount the febrile response to pyrogens or psychological stresses. Increased intracellular Ca2+ levels are normally observed when nicotinic receptors are activated to produce contraction. It is well known in other tissues that the increase in Ca2+ activates NOS, leading to heightened production of NO. In skeletal muscles is not different. Interesting are the facts that increased levels of NO inhibit skeletal muscle contraction despite favoring glucose transport and increasing blood flow to the muscle.


Figure 6. Effects of central NO on euthermic control of deep body temperature (Tb). Microinjection of L‐NAME (a nonselective NOS inhibitor) into the lateral ventricle (LV) has led to the conclusion that central NO has either no effect on Tb or causes a slight reduction in Tb. Interestingly, NO does not affect Tb when its production is inhibited with L‐NMMA (another nonselective NOS inhibitor) in the most caudal brain ventricle, that is, the fourth ventricle (4V).


Figure 7. Effects of central NO on fever induced by LPS. Microinjection of inhibitors of iNOS or nNOS into the lateral ventricle (LV) has led to the conclusion that central NO favors the occurrence of fever. Conversely, microinjection of a nonselective inhibitor of NOS into the fourth ventricle (4V) has suggested that NO does not alter LPS fever when its production is inhibited predominantly in the most caudal brain ventricle.


Figure 8. Effects of NO within specific regions of the brain. Microinjection of L‐NMMA (a nonselective NOS inhibitor) within the AVPO has led to the conclusion that AVPO NO attenuates LPS fever. Conversely, it has been demonstrated that locus coeruleus (LC) NO exacerbates LPS fever.


Figure 9. Role of preoptic area of the hypothalamus (POA) nitric oxide (NO) in lipopolysaccharide (LPS)‐induced fever. Systemic LPS has been shown to reduce NOS activity, diminishing the levels of NO in the POA. It is believed that lowered levels of NO in the POA relieve (dashed arrow) the activity of the intracellular cascade (COX‐2/mPGES‐1/PGE2) classically known as the responsible for fever generation. Interestingly, besides inducing fever, this cascade appears to downmodulate a cascade known to downmodulates fever: AC/cAMP/PKA, thus further favoring the febrile response. Reduced levels of POA NO downmodulate its classical cascade, which in the POA is a cascade that attenuates fever: NO/sGC/cGMP/PKG, thus facilitating the regulated increase in deep body temperature (Tb), that is, fever. Abbreviations: COX‐2, cyclooxygenase‐2; mPGES‐1, inducible microsomal PGE synthase‐1; PGE2, prostaglandin E2; AC, adenylate cyclase; cAMP, cyclic adenosine monophosphate; PKA, protein kinase A; NOS, nitric oxide synthase; NO, nitric oxide; sGC, soluble guanylate cyclase; cGMP, cyclic guanosine monophosphate; PKG, protein kinase G.


Figure 10. Effects of central NO on anapyrexia induced by hypoxia. Microinjection of L‐NAME (a nonselective NOS inhibitor) into the lateral ventricle (LV) has led to the conclusion that central NO seems to be essential to the occurrence of hypoxia‐induced anapyrexia.


Figure 11. Role of preoptic area of the hypothalamus (POA) nitric oxide (NO) in hypoxia‐induced anapyrexia. Reduced inspired levels of oxygen (hypoxia) stimulate the production of NO in the POA. Once the levels of NO are augmented in the POA, the intracellular cascade that favors the regulated drop in Tb (anapyrexia) is heightened. This intracellular cascade is composed basically of sGC, cGMP, and PKG. These molecules ultimately favor the occurrence of anapyrexia. Abbreviations: NOS, nitric oxide synthase; NO, nitric oxide; sGC, soluble guanylate cyclase; cGMP, cyclic guanosine monophosphate; PKG, protein kinase G.


Figure 12. The carbon monoxide (CO) pathway and the pharmacological tools available to study the CO signaling pathway. Metabolism of heme is catalyzed by the enzyme heme oxygenase (HO). Heme catabolism by (HO) yields biliverdin, iron, and CO. CO may activate the cyclic guanosine monophosphate (cGMP)‐synthesizing enzyme soluble guanylyl cyclase (sGC). Therefore, activation of sGC leads to elevated levels of cGMP, which in turn activates protein kinase G (PKG).


Figure 13. Role of central nervous system (CNS) carbon monoxide (CO) in febrile response to lipopolysaccharide (LPS). It is well known that systemic administration of a fever‐inducing dose of LPS induces in the CNS the following fever‐inducing signaling cascade: COX‐2/mPGES‐1/PGE2, which in the fever‐originating center of the brain, the preoptic area of the hypothalamus (POA), evokes appropriate thermoefferent signals that ultimately results in a regulated increase in deep body temperature (Tb), that is, fever. Systemic LPS seems to stimulate the enzyme heme oxygenase to increase the generation of CO in the CNS. Central CO, in region(s) other than the POA, has been suggested to act as a propyretic molecule. Abbreviations: COX‐2, cyclooxygenase‐2; mPGES‐1, inducible microsomal PGE synthase‐1; PGE2, prostaglandin E2.


Figure 14. Role of central carbon monoxide (CO) in hypoxia‐induced anapyrexia. Preoptic area of the hypothalamus (POA) CO has been shown not to participate in the control of anapyrexic response to hypoxia. Conversely, the results obtained from inhibition of heme oxygenase (HO), the CO‐synthesizing enzyme, in the cerebroventricular system suggests that central CO downmodulates hypoxia‐induced anapyrexia.


Figure 15. Biosynthesis of hydrogen sulfide (H2S). Three enzymatic pathways are involved in the biosynthesis of H2S. Cystathionine β‐synthase (CBS) produces H2S via the generation of cystathionine from homocysteine and L‐cysteine from cystathione. Cystathionine γ‐lyase (CSE) produces H2S by producing L‐cysteine from cystathionine. 3‐mercaptopyruvate sulfur transferase (3MST) produces H2S via the production of 3‐mercaptopyruvate (3MP) from α‐ketoglutarate (α‐KG) by cysteine aminotransferase (CAT). H2S, endogenously produced in the donor cell, seems to act predominantly via adenylate cyclase (AC)/cyclic adenosine monophosphate (cAMP) and/or modulating ATP‐dependent potassium (K+ATP) channels in the target cell.


Figure 16. Role of preoptic area of the hypothalamus (POA) hydrogen sulfide (H2S) in hypoxia‐induced anapyrexia. Exposure to hypoxia (7% oxygen in inspired air) is known to induce CBS activity, elevating H2S levels in the POA. Increased levels of POA H2S stimulates an intracellular cascade, composed of AC, cAMP, and PKA, which is believed to be essential to the occurrence of the anapyrexic response to hypoxia. Abbreviations: CBS, cystathionine β‐synthase; AC, adenylate cyclase; cAMP, cyclic adenosine monophosphate; PKA, protein kinase A.


Figure 17. Role of preoptic area of the hypothalamus (POA) hydrogen sulfide (H2S) in fever induced by systemic administration of lipopolysaccharide (LPS). Systemic LPS has been shown to suppress CBS activity, reducing H2S levels in the POA. It is believed that reduced levels of H2S in the POA relieve (gray dashed arrow) the activity of the intracellular cascade (COX‐2/mPGES‐1/PGE2) responsible for fever generation. It is well known that this cascade induces fever. Interestingly, besides inducing fever, this cascade appears to downmodulate the cascade known to downmodulate fever: AC/cAMP/PKA. Reduced levels of POA H2S are believed to downmodulate the latter cascade as well (gray, curved dashed arrow). Abbreviations: Tb, deep body temperature; COX‐2, cyclooxygenase‐2; mPGES‐1, inducible microsomal PGE synthase‐1; PGE2, prostaglandin E2; AC, adenylate cyclase; cAMP, cyclic adenosine monophosphate; PKA, protein kinase A.
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Article Title: Gaseous Mediators in Temperature Regulation
 

How to Cite

Luiz G.S. Branco, Renato N. Soriano, Alexandre A. Steiner. Gaseous Mediators in Temperature Regulation. Compr Physiol 2014, 4: 1301-1338. doi: 10.1002/cphy.c130053