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      Gastrointestinal distribution of chicken gastrin-cholecystokinin family transcript expression and response to short-term nutritive state

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      * ,
      General and Comparative Endocrinology
      Academic Press
      Satiety, Avian, Hormone, Feeding, Poultry

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          Highlights

          • Anatomical distributions of chicken CCK and GAST mRNA expression are resolved.

          • Expressional responses of CCK and GAST to short-term nutritive state are investigated.

          • CCK mRNA expression does not respond to acute satiety state.

          • GAST mRNA expression is upregulated under short-term fasting.

          Abstract

          The related peptide hormones cholecystokinin (CCK) and gastrin are conserved throughout vertebrate clades and implicated in energy homeostasis. CCK is generally accepted as a satiety hormone in poultry, but the role of gastrin remains poorly studied. Functional dissection of these ligands is required to characterise the molecular control of growth & satiety in the domestic chicken, for which there is an increasingly pressing mandate. There are limited descriptions of physiological distributions for the two genes in birds, and these are mostly reliant on immunohistochemistry which can prove problematic due to the shared structure of the targets. Therefore, we have defined the tissue distributions of CCK and gastrin in the chicken, focussing on the gastrointestinal tract, by using transcript-dependent techniques to improve reliability by increasing specificity. Though considerably more highly expressed in the brain, gastrointestinal CCK transcripts were dispersed throughout the small intestine and particularly around the proximal ileum. Gastrin expression was strictly limited to the gastric antrum region of the intestinal tract, albeit very highly expressed. We demonstrate that CCK mRNA expression does not respond as expected for a short-term satiety hormone, and that the short-term response of gastrin expression is paradoxical compared to its role in mammals. These results partially corroborate previous peptide distribution studies and initiate exploration of the nutrient-responsive roles of these hormones in avian energy balance.

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          Most cited references43

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          Identification of common molecular subsequences.

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            Cholecystokinin bioactivity in human plasma. Molecular forms, responses to feeding, and relationship to gallbladder contraction.

            A sensitive and specific bioassay for the measurement of cholecystokinin (CCK) in human plasma was developed to determine the molecular forms of CCK in circulation, CCK responses to feeding, and the physiologic role of CCK in gallbladder contraction. First, plasma was quantitatively extracted and concentrated with octadecylsilylsilica, and the extracts were then assayed for their ability to stimulate amylase release from isolated rat pancreatic acini. Acini were highly sensitive to CCK whereas gastrin reacted only weakly in this system. With the assay, plasma levels of cholecystokinin octapeptide (CCK-8) bioactivity as low as 0.2 pM were detectable. CCK bioactivity in plasma was inhibited by the CCK antagonist, bibutyryl cyclic guanosine monophosphate, and was eliminated by immunoadsorption with an antibody directed against the carboxyl terminus of CCK. Detection of fasting levels of CCK was possible in all individuals tested and averaged 1.0 +/- 0.2 pM (mean +/- SE, n = 22) CCK-8 equivalents. Plasma CCK biological activity was normal in patients with gastrin-secreting tumors. After being fed a mixed liquid meal, CCK levels rose within 15 min to 6.0 +/- 1.6 pM. The individual food components fat, protein, and amino acids were all potent stimulants of CCK secretion; in contrast, glucose caused a significant but smaller elevation in plasma CCK levels. Gel filtration studies identified three major forms of CCK bioactivity in human plasma: an abundant form that eluted with CCK-33, a smaller form that eluted with CCK-8, and an intermediate form that eluted between CCK-33 and CCK-8. Ultrasonic measurements of gallbladder volume indicated that this organ decreased 51% in size 30 min after feeding a mixed liquid meal. This contraction occurred coincidentally with the increase in plasma CCK levels. Next CCK-8 was infused to obtain CCK levels similar to postprandial levels. This infusion caused a decrease in gallbladder volume, similar to that seen with a meal. The present studies indicate, therefore, that CCK can be bioassayed in fasting and postprandial human plasma. These studies also suggest that CCK may be an important regulator of gallbladder contraction.
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              Cholecystokinin—From Local Gut Hormone to Ubiquitous Messenger

              Cholecystokinin (CCK) was discovered in 1928 in jejunal extracts as a gallbladder contraction factor. It was later shown to be member of a peptide family, which are all ligands for the CCK1 and CCK2 receptors. CCK peptides are known to be synthetized in small intestinal endocrine I-cells and cerebral neurons. But in addition, CCK is expressed in several endocrine glands (pituitary cells, thyroid C-cells, pancreatic islets, the adrenals, and the testes); in peripheral nerves; in cortical and medullary kidney cells; in cardial myocytes; and in cells of the immune system. CCK peptides stimulate pancreatic enzyme secretion and growth, gallbladder contraction, and gut motility, satiety and inhibit acid secretion from the stomach. Moreover, they are major neurotransmitters in the brain and the periphery. CCK peptides also stimulate calcitonin, insulin, and glucagon secretion, and they may act as natriuretic peptides in the kidneys. CCK peptides are derived from proCCK with a C-terminal bioactive YMGWMDFamide sequence, in which the Y-residue is partly O-sulfated. The plasma forms are CCK-58, -33, -22, and -8, whereas the small CCK-8 and -5 are potent neurotransmitters. Over the last decades, CCK expression has also been encountered in tumors (neuroendocrine tumors, cerebral astrocytomas, gliomas, acoustic neuromas, and specific pediatric tumors). Recently, a metastastic islet cell tumor was found to cause a specific CCKoma syndrome, suggesting that circulating CCK may be a useful tumor marker.
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                Author and article information

                Contributors
                Journal
                Gen Comp Endocrinol
                Gen. Comp. Endocrinol
                General and Comparative Endocrinology
                Academic Press
                0016-6480
                1095-6840
                01 January 2018
                01 January 2018
                : 255
                : 64-70
                Affiliations
                The Roslin Institute, University of Edinburgh, Easter Bush, Midlothian, Scotland EH25 9RG, UK
                Author notes
                [* ]Corresponding author. angus.reid@ 123456roslin.ed.ac.uk
                Article
                S0016-6480(17)30622-6
                10.1016/j.ygcen.2017.10.009
                5693036
                29061367
                49e22c23-cdc2-4f8d-b7cf-2bfaced249ec
                © 2017 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 6 September 2017
                : 16 October 2017
                : 19 October 2017
                Categories
                Article

                Endocrinology & Diabetes
                satiety,avian,hormone,feeding,poultry
                Endocrinology & Diabetes
                satiety, avian, hormone, feeding, poultry

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