Exploring the Mediators That Promote Carotid Body Dysfunction in Type 2 Diabetes and Obesity Related Syndromes

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Exploring the Mediators That Promote Carotid Body Dysfunction in Type 2 Diabetes and Obesity Related Syndromes International Journal of Molecular Sciences Review Exploring the Mediators that Promote Carotid Body Dysfunction in Type 2 Diabetes and Obesity Related Syndromes 1 1,2, 1, 1 Joana F. Sacramento , Kryspin Andrzejewski y , Bernardete F. Melo y, Maria J. Ribeiro , Ana Obeso 3 and Silvia V. Conde 1,* 1 CEDOC (Chronic Disease Research Center), NOVA Medical School, Faculdade de Ciências Médicas, Universidade Nova de Lisboa, 1150-082 Lisbon, Portugal; [email protected] (J.F.S.); [email protected] (K.A.); [email protected] (B.F.M.); [email protected] (M.J.R.) 2 Department of Respiration Physiology, Mossakowski Medical Research Centre, Polish Academy of Sciences, Pawi´nskiego5, 02-106 Warsaw, Poland 3 Departamento de Bioquímica y Biología Molecular y Fisiología, Universidad de Valladolid, Facultad de Medicina, Instituto de Biología y Genética Molecular, CSIC, Ciber de Enfermedades Respiratorias, CIBERES, Instituto de Salud Carlos III, 47005 Valladolid, Spain; [email protected] * Correspondence: [email protected]; Tel.: +351-218803100 (ext. 26022) Both authors contributed equally as second authors to the present manuscript. y Received: 1 July 2020; Accepted: 30 July 2020; Published: 3 August 2020 Abstract: Carotid bodies (CBs) are peripheral chemoreceptors that sense changes in blood O2, CO2, and pH levels. Apart from ventilatory control, these organs are deeply involved in the homeostatic regulation of carbohydrates and lipid metabolism and inflammation. It has been described that CB dysfunction is involved in the genesis of metabolic diseases and that CB overactivation is present in animal models of metabolic disease and in prediabetes patients. Additionally, resection of the CB-sensitive nerve, the carotid sinus nerve (CSN), or CB ablation in animals prevents and reverses diet-induced insulin resistance and glucose intolerance as well as sympathoadrenal overactivity, meaning that the beneficial effects of decreasing CB activity on glucose homeostasis are modulated by target-related efferent sympathetic nerves, through a reflex initiated in the CBs. In agreement with our pre-clinical data, hyperbaric oxygen therapy, which reduces CB activity, improves glucose homeostasis in type 2 diabetes patients. Insulin, leptin, and pro-inflammatory cytokines activate the CB. In this manuscript, we review in a concise manner the putative pathways linking CB chemoreceptor deregulation with the pathogenesis of metabolic diseases and discuss and present new data that highlight the roles of hyperinsulinemia, hyperleptinemia, and chronic inflammation as major factors contributing to CB dysfunction in metabolic disorders. Keywords: carotid body; obesity related syndromes; type 2 diabetes; glucose; insulin; leptin; inflammation; sympathetic overactivation 1. Introduction Metabolic diseases such as obesity, metabolic syndrome, and type 2 diabetes are some of the most common non-communicable diseases whose prevalence continues to increase, contributing to significant morbidity and mortality worldwide and considered worldwide epidemics [1,2]. The increasing incidence of these diseases is mainly due to lifestyle changes such as the sedentary lifestyle and the increase in the consumption of hypercaloric diets. The sympathetic nervous system is known to play a role in the generation of metabolic diseases [3,4] and several factors have been postulated to be responsible for this increased sympathetic activation, such as hyperinsulinemia, hyperleptinemia, Int. J. Mol. Sci. 2020, 21, 5545; doi:10.3390/ijms21155545 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 5545 2 of 22 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 21 andmediators inflammatory responsible cytokines for it. [5 ].Additi However,onally, there afferent is no consensuspathways onand the th majore stimuli mediators that trigger responsible afferent for it.activation Additionally, are poorly afferent studied. pathways and the stimuli that trigger afferent activation are poorly studied. CarotidCarotid bodies (CBs), (CBs), located located bi bilaterallylaterally atat the the bifurcation bifurcation of ofeach each common common carotid carotid artery, artery, are peripheral chemoreceptors that classically sense changes in arterial blood O2, CO2, and pH levels. In are peripheral chemoreceptors that classically sense changes in arterial blood O2, CO2, and pH levels. response to hypoxia (O2 deprivation), hypercapnia (CO2 retention), and acidosis (pH drop), type I In response to hypoxia (O2 deprivation), hypercapnia (CO2 retention), and acidosis (pH drop), type I cells,cells, thethe CBCB chemosensorychemosensory unit,unit, releaserelease neurotransmittersneurotransmitters that act onon thethe nervenerve terminalsterminals ofof thethe CBCB sensitivesensitive nerve,nerve, thethe carotid carotid sinus sinus nerve nerve (CSN), (CSN), to to generate generate action action potentials potentials or toor inhibitto inhibit its activityits activity [6]. CSN[6]. CSN activity activity is integrated is integrated in the in brainstem the brainstem to induce to ainduce set of respiratorya set of respiratory reflexes aimed, reflexes primarily, aimed, atprimarily, normalizing at normalizing the altered bloodthe altered gases blood via hyperventilation gases via hyperventilation [6] and regulating [6] and blood regulating pressure blood and cardiacpressure performance and cardiac viaperformance sympathetic via nervoussympathetic system nerv activationous system [7 ].activation Besides [7]. its roleBesides as an its oxygen role as sensor,an oxygen in the sensor, last few in the years, last the few CB years, has also the beenCB has proposed also been to beproposed a metabolic to be sensor a metabolic implicated sensor in theimplicated control ofin carbohydratethe control of and carbohydrate lipid metabolism and lipid [8–11 metabolism] and in the [8–11] regulation and ofin peripheralthe regulation insulin of sensitivityperipheral andinsulin glucose sensitivity homeostasis and glucose [8,9,12 homeostasis–17] (Figure 1[8,9,12–17]a). Recently, (Figure we showed 1a). Recently, that CB we activity showed is increasedthat CB activity in prediabetes is increased and type in prediabetes 2 diabetes animal and type models 2 diabetes [13,18– 20animal] and patientsmodels [[13,18–20]21] (Figure and1a) andpatients that [21] the abolishment(Figure 1a) and of CB that activity the abolishment in animals, of via CB chronic activity resection in animals, of thevia CSNchronic or CBresection ablation, of preventsthe CSN or and CB reverses ablation, dysmetabolism prevents and reverses in rodent dysm modelsetabolism of metabolic in rodent disease models [13 of, 15metabolic,16] (Figure disease1b) by[13,15,16] positively (Figure impacting 1b) by glucosepositively uptake impacting and insulin glucos signalinge uptake and in the insulin liver signaling and in the in visceral the liver adipose and in tissuethe visceral [15]. Additionally, adipose tissue we [15]. have Additionally, previously shown we have that CSNpreviously resection shown in animal that CSN models resection prevents in andanimal restores models the prevents heightened and sympathetic restores the activity, heightened measured sympathetic as increased activity, plasma measured and adrenal as increased medulla catecholaminesplasma and adrenal levels medulla and increased catecholamines LF bands levels and and LF increased/HF ratio LF in heartbands rateand variabilityLF/HF ratio analysis, in heart whichrate variability is characteristic analysis, of which metabolic is characteristic diseases [13 ,of15 ].metabolic In agreement diseases with [13,15]. this heightened In agreement sympathetic with this activity,heightened electrophysiological sympathetic activity, recordings electrophysiological at the superior cervicalrecordings chain at confirmedthe superior the overactivationcervical chain ofconfirmed the sympathetic the overactivation nervous system of the sympathetic in rodent models nervous of system dysmetabolism in rodent thatmodels disappear of dysmetabolism with CSN resectionthat disappear [19]. Altogether, with CSN these resection results [19]. mean Altogeth that CBer, dysfunction these results is involved mean that in theCB development dysfunction ofis metabolicinvolved in diseases the development via an overactivation of metabolic of diseases the sympathetic via an overactivation nervous system of the (Figure sympathetic1a). nervous system (Figure 1a). Figure 1. Schematic representation of the carotid body (CB) involvement in the development of Figure 1. Schematic representation of the carotid body (CB) involvement in the development of obesity, insulin resistance, and glucose intolerance through an increase in sympathetic nervous obesity, insulin resistance, and glucose intolerance through an increase in sympathetic nervous system activity. (A) Hypercaloric diets and intermittent hypoxia promote an increase in CB activity system activity. (A) Hypercaloric diets and intermittent hypoxia promote an increase in CB activity that contributes to the augmentation of sympathetic nervous system activity, leading to metabolic that contributes to the augmentation of sympathetic nervous system activity, leading to metabolic dysfunction. (B) Modulation of CB activity through the carotid sinus nerve (CSN) resection or via dysfunction. (B) Modulation of CB activity through the carotid sinus nerve (CSN) resection or via hyperbaric oxygen therapy, normalized sympathetic nervous system activity, improving dysmetabolism. hyperbaric oxygen therapy, normalized
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