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      The effects of intra-stomach obestatin administration on intestinal contractility in neonatal piglets fed milk formula

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          Abstract

          A 23-amino acid peptide named obestatin is derived from the ghrelin gene. The aim of the experiment was to study the effects of enteral obestatin administration for a 6-day period on intestinal contractility in piglets fed milk formula. Pigs were treated with 0.9% NaCl (group C) or varying doses of obestatin: 2 μg/kg body weight (BW) (group O2), 10 μg/kg BW (O10) or 15 μg/kg BW (O15) every 8 hours via a stomach tube. Blood was sampled for assessment of obestatin concentration. Duodenal and middle jejunum whole-thickness preparations were studied in an organ bath for isometric recording under electric field stimulation (EFS) and increasing doses of acetylcholine (ACh), and in the presence of atropine and tetrodotoxin (TTX). Additionally, the measurement of intestinal muscularis layer and the immunodetection of Muscarinic Acetylcholine Receptors (M1 and M2) were performed. In comparison to C animals, the obestatin concentration in blood plasma was significantly increased in groups O10 and O15. In both studied intestinal segments, significant increases in the frequency and amplitude of spontaneous contractions were observed in O15 and C groups. In the duodenum and middle jejunum significant differences in responsiveness to EFS (0.5, 5 and 50 Hz) were observed between the groups. The addition of 10 −4 M ACh to the duodenum significantly increased the responsiveness in tissues. In contrast, in the middle jejunum a significant increase in the amplitude of contraction was observed after the addition of 10 −9 and 10 −6 M ACh (groups O15 and O10, respectively). Pretreatment with atropine and TTX resulted in a significant decrease in the responsiveness of the intestinal preparations from all groups, in both studied segments. The increased contractility was not dependent on the expression of muscarinic receptors. Results indicate the importance of enteral obestatin administration in the regulation of intestinal contractility in neonatal piglets.

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          Most cited references23

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          Obestatin, a peptide encoded by the ghrelin gene, opposes ghrelin's effects on food intake.

          Ghrelin, a circulating appetite-inducing hormone, is derived from a prohormone by posttranslational processing. On the basis of the bioinformatic prediction that another peptide also derived from proghrelin exists, we isolated a hormone from rat stomach and named it obestatin-a contraction of obese, from the Latin "obedere," meaning to devour, and "statin," denoting suppression. Contrary to the appetite-stimulating effects of ghrelin, treatment of rats with obestatin suppressed food intake, inhibited jejunal contraction, and decreased body-weight gain. Obestatin bound to the orphan G protein-coupled receptor GPR39. Thus, two peptide hormones with opposing action in weight regulation are derived from the same ghrelin gene. After differential modification, these hormones activate distinct receptors.
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            GPR39 signaling is stimulated by zinc ions but not by obestatin.

            GPR39 is an orphan member of the ghrelin receptor family that recently was suggested to be the receptor for obestatin, a peptide derived from the ghrelin precursor. Here, we compare the effect of obestatin to the effect of Zn(2+) on signal transduction and study the effect of obestatin on food intake. Although Zn(2+) stimulated inositol phosphate turnover, cAMP production, arrestin mobilization, as well as cAMP response element-dependent and serum response element-dependent transcriptional activity in GPR39-expressing cells as opposed to mock-transfected cells, no reproducible effect was obtained with obestatin in the GPR39-expressing cells. Moreover, no specific binding of obestatin could be detected in two different types of GPR39-expressing cells using three different radioiodinated forms of obestatin. By quantitative PCR analysis, GPR39 expression was readily detected in peripheral organs such as duodenum and kidney but not in the pituitary and hypothalamus, i.e. presumed central target organs for obestatin. Obestatin had no significant and reproducible effect on acute food intake in either freely fed or fasted lean mice. It is concluded that GPR39 is probably not the obestatin receptor. In contrast, the potency and efficacy of Zn(2+) in respect of activating signaling indicates that this metal ion could be a physiologically relevant agonist or modulator of GPR39.
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              Hormones and growth factors in milk.

              Research dealing with hormones/growth factors in milk has progressed rapidly during the last 10 yr from their identification in milk to their regulation of various functions in the maternal organism and in the neonate. Many hormones, growth factors, and bioactive substances present in the maternal organism are present in colostrum and milk, often exceeding concentrations that occur in maternal plasma. Some appear in milk in different, sometimes multiple, forms from that found in maternal serum, reflecting to some extent synthesis and posttranslational processing by mammary tissue. Recent research has indicated that many milk hormones/growth factors survive the environment of the gut of the neonate, become absorbed into the neonatal circulation, and exert important functions in the neonate.
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                Author and article information

                Contributors
                Role: Data curationRole: InvestigationRole: Writing – original draft
                Role: InvestigationRole: Writing – review & editing
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Resources
                Role: Resources
                Role: Investigation
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                23 March 2020
                2020
                : 15
                : 3
                : e0230190
                Affiliations
                [1 ] Department of Animal Physiology, Polish Academy of Sciences, The Kielanowski Institute of Animal Physiology and Nutrition, Jabłonna, Poland
                [2 ] Department of Animal Nutrition and Feed Sciences, National Research Institute of Animal Production, Balice, Poland
                [3 ] Department of Physiological Sciences, Faculty of Veterinary Medicine, Warsaw University of Life Sciences, Warsaw, Poland
                [4 ] Department of Dental Surgery, Medical University of Warsaw, Warsaw, Poland
                [5 ] Laboratory of Physiology, Institute for Environmental Sciences & Graduate School of Nutritional and Environmental Sciences, University of Shizuoka, Shizuoka, Japan
                [6 ] Department of Medical Biochemistry, Kobe Pharmaceutical University, Kobe, Japan
                Medical University of Vienna, AUSTRIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                ‡ These authors also contributed equally to this work.

                Author information
                http://orcid.org/0000-0001-8645-1045
                Article
                PONE-D-19-19879
                10.1371/journal.pone.0230190
                7089538
                32203550
                605262f0-b80e-4a77-a940-3a213af95d76
                © 2020 Słupecka-Ziemilska et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 10 August 2019
                : 24 February 2020
                Page count
                Figures: 4, Tables: 5, Pages: 13
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: Grant no. 2012/05/B/NZ9/00901
                Award Recipient :
                This research was supported by National Science Center [Grant no. 2012/05/B/NZ9/00901] ( https://www.ncn.gov.pl/). JW received the funding. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There was no additional external funding received for this study.
                Categories
                Research Article
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Body Weight
                Obesity
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Body Weight
                Obesity
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Swine
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Jejunum
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Jejunum
                Biology and Life Sciences
                Nutrition
                Diet
                Beverages
                Milk
                Medicine and Health Sciences
                Nutrition
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                Biology and Life Sciences
                Anatomy
                Body Fluids
                Milk
                Medicine and Health Sciences
                Anatomy
                Body Fluids
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                Biology and Life Sciences
                Physiology
                Body Fluids
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                Medicine and Health Sciences
                Physiology
                Body Fluids
                Milk
                Biology and Life Sciences
                Anatomy
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                Gastrointestinal Tract
                Duodenum
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Duodenum
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Body Weight
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
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                Biology and Life Sciences
                Physiology
                Muscle Physiology
                Muscle Contraction
                Medicine and Health Sciences
                Physiology
                Muscle Physiology
                Muscle Contraction
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