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Vascular Effects of Obestatin in Lean and Obese Subjects

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Vascular Effects of Obestatin in Lean and Obese Subjects 1214 Diabetes Volume 66, May 2017 Vascular Effects of Obestatin in Lean and Obese Subjects Francesca Schinzari,1 Augusto Veneziani,2 Nadia Mores,3 Angela Barini,4 Nicola Di Daniele,5 Carmine Cardillo,1 and Manfredi Tesauro5 Diabetes 2017;66:1214–1221 | DOI: 10.2337/db16-1067 Obese patients have impaired vasodilator reactivity and tone, predominantly resulting from enhanced endothe- increased endothelin 1 (ET-1)–mediated vasoconstriction, lin (ET)-1 activity (2,3), has been shown to importantly two abnormalities contributing to vascular dysfunction. contribute to their vascular dysfunction and damage. Obestatin, a product of the ghrelin gene, in addition to fa- Obestatin was identified in 2005 as a ghrelin-associ- vorable effects on glucose and lipid metabolism, has shown ated peptide derived from alternative splicing of the nitric oxide (NO)–dependent vasodilator properties in exper- common precursor prepro-ghrelin and was originally re- imental models. Given these premises, we compared the ported to reduce food intake and gastric emptying through fl effects of exogenous obestatin on forearm ow in lean activation of the G-protein–coupled receptor (GPCR) GPR39 fl – and obese subjects and assessed its in uence on ET-1 (4). Even though these effects on feeding behavior and gas- dependent vasoconstrictor tone in obesity. In both lean trointestinal motion have been subsequently disputed and and obese participants, infusion of escalating doses of the precise identity of its cognate receptor(s) is still a obestatin resulted in a progressive increase in blood flow matter of debate (5), obestatin indisputably exerts a from baseline (both P < 0.001). This vasodilation was pre- dominantly mediated by enhanced NO activity, because variety of effects in different cell types, including pan- G creatic b-cells, where it increases survival and prolifer- N -monomethyl-L-arginine markedly blunted the flow re- fl sponse to obestatin in both groups (both P < 0.05 vs. saline). ation by inhibiting apoptosis and in ammation (6,7). In line with these actions, other favorable effects of In obese subjects, antagonism of ETA receptors by BQ-123 OBESITY STUDIES increased forearm flow during saline (P < 0.001) but did not obestatin have been observed on glucose and lipid me- induce additional vasodilation (P > 0.05) during obestatin. tabolism, such as increased glucose uptake and insulin Circulating obestatin levels were not different between lean sensitivity as well as inhibition of lipolysis in human and obese participants (P =0.41).Ourfindings indicate that adipocytes (7,8). obestatin causes NO-dependent vasodilation in the human Interestingly, in addition to its helpful metabolic circulation. This effect is preserved in obesity, where it is properties, obestatin has been shown to provide vascular accompanied by reduced ET-1–mediated vasoconstriction. benefits in experimental models. Thus, in rat aorta and These latter observations make obestatin a promising tar- the superior mesenteric artery, Agnew et al. (9) have dem- get for vascular prevention in obesity and diabetes. onstrated that obestatin favorably affects endothelial function, inducing nitric oxide (NO)–dependent relaxa- tion via an adenylate cyclase–linked GPCR. These findings According to the current figures of the World Health have been more recently confirmed in the mouse cerebral Organization, the worldwide prevalence of obesity is still artery, where obestatin induces NO-dependent vasodila- on the rise, carrying an increased burden of type 2 diabetes tion, which is maintained during ghrelin receptor antag- and other untoward consequences, especially cardiovascular onism (10). This effect is also present in animals with complications. Impaired vasodilator reactivity has been increased superoxide generation caused by ghrelin recep- recognized as an early hemodynamic abnormality character- tor knockout, hence suggesting an additional mechanism istic of these patients (1), but also increased vasoconstrictor for the vascular protection afforded by obestatin (10). 1Department of Internal Medicine, Catholic University, Rome, Italy This article contains Supplementary Data online at http://diabetes 2Department of Surgery, Catholic University, Rome, Italy .diabetesjournals.org/lookup/suppl/doi:10.2337/db16-1067/-/DC1. 3 Department of Pharmacology, Catholic University, Rome, Italy © 2017 by the American Diabetes Association. Readers may use this article as 4 Department of Biochemistry, Catholic University, Rome, Italy long as the work is properly cited, the use is educational and not for profit, and the 5 Department of Internal Medicine, University of Rome Tor Vergata, Rome, Italy work is not altered. More information is available at http://www.diabetesjournals Corresponding author: Carmine Cardillo, [email protected]. .org/content/license. Received 31 August 2016 and accepted 29 January 2017. diabetes.diabetesjournals.org Schinzari and Associates 1215 Owing to the advantageous metabolic and vascular actions (12), all female participants were studied within the first observed in preclinical models, we hypothesized that obe- week from the beginning of their menstrual cycle. The statin might become an interesting target for cardiovascular study protocol was approved by the institutional review disease prevention in human obesity and diabetes. To this boards of the University of Rome Tor Vergata and Cath- purpose, the current study was designed to compare the olic University, and all participants gave written informed effects of obestatin on forearm flow in lean and obese consent before their participation in the study. subjects and to investigate whether inhibition of ET-1– dependent vasoconstriction might be an additional mecha- Protocols of Vascular Reactivity Studies nism of the vascular action of obestatin in obese individuals. All studies were performed in a quiet room with a temper- ature of ;22°C (Supplementary Figs. 1 and 2). Each study RESEARCH DESIGN AND METHODS consisted of infusions of drugs into the brachial artery and Study Subjects measurement of forearm blood flow by means of strain-gauge The study recruited lean subjects (BMI ,25 kg/m2, nor- venous occlusion plethysmography. All drugs used in this mal waist circumference) and individuals with central study were prepared by the local pharmaceutical service fol- obesity (waist circumference $102 cm for men lowing specific procedures to ensure accurate bioavailability or $88 cm for women) (Table 1), without or with the and sterility of the solutions. Participants were asked to fast metabolic syndrome (defined according to the National for at least 8 h before the study. While participants were Cholesterol Education Program’s Adult Treatment Panel supine, a 20-gauge Teflon catheter (Arrow Inc., Limerick, PA) III) (11). All participants had no history or current evi- was inserted into the brachial artery of the nondominant arm dence of cardiovascular disease (coronary artery disease, (left in most cases) for drug infusion. Another 20-gauge cath- cerebrovascular or peripheral occlusive arterial disease, eter (Abbott Laboratories, Abbott Park, IL) was inserted into a coagulopathy, vasculitis) or any other systemic condition. deep antecubital vein of the same arm for blood sampling. In obese participants taking antihypertensive and/or The extended arm was positioned slightly above the level lipid-lowering drugs, treatment was discontinued for at of the right atrium and a Hg-filled strain gauge was placed least 1 week before the vascular study. Blood pressure around the widest part of the forearm. The strain gauge was was repeatedly measured during this time, and when connected to a plethysmograph (model EC-6; Hokanson needed, treatment was restarted with the exclusion of Inc., Bellevue, WA) calibrated to measure the percentage the subject from the study. No participants smoked, and change in volume and connected to a personal computer all were asked to refrain from drinking alcohol and bev- through an analog-to-digital converter. For each measure- erages containing caffeine for at least 24 h before the ment, a cuff placed around the upper arm was inflated to study. The participants were not engaged in programs 40 mmHg with a rapid cuff inflator (model E-10; Hokanson of regular physical activity. Because of the possible effects Inc.) to occlude venous outflow from the extremity. A of sex hormones on vascular activity of the ET-1 system wrist cuff was inflated to suprasystolic pressures 1 min Table 1—Clinical characteristics of the study population Obese subjects Lean subjects No metabolic syndrome Metabolic syndrome (n = 14) (n = 13) (n = 11) P value Sex Male 7 5 6 Female 7 8 5 Age, years 40 6 3386 3416 3 0.74 BMI, kg/m2 23 6 1386 2* 42 6 2* ,0.001 Waist, cm 82 6 4 122 6 5* 117 6 3* ,0.001 Blood pressure, mmHg Systolic 116 6 2 124 6 3* 133 6 3*# 0.01 Diastolic 74 6 4796 3846 4 0.17 Glucose, mg/dL 88 6 3896 2956 5 0.30 Cholesterol, mg/dL Total 162 6 8 199 6 13 191 6 13 0.07 HDL 49 6 3486 3406 2 0.15 Triglycerides, mg/dL 92 6 8 117 6 17 164 6 26* 0.02 Insulin, mU/mL 8 6 1196 3* 18 6 3* 0.008 Data are expressed as number of subjects or as mean 6 SEM. Comparisons were performed by one-way ANOVA. There were no differences between the subgroups of lean or obese subjects participating in the two different protocols. *P , 0.05 vs. lean subjects. #P , 0.05 vs. no metabolic syndrome at the Holm-Sídák post hoc test for multiple comparisons. 1216 Vascular Effects of Obestatin Diabetes Volume 66, May 2017 before each measurement to exclude the hand circulation. administration was maintained, the BQ-123 infusion was Flow measurements were recorded for ;7 s every 15 s. Seven repeated as before. readings were obtained for each mean value. Blood pressure Analytical Procedures was recorded with the use of a standard Hg manometer. Plasma levels of obestatin and total ghrelin (acylated and Throughout all studies, volumes infused were matched by desacylated) were measured by enzyme immunosorbent administration of variable amounts of saline.
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