Vitamins and hormones, volume 98

Cover photo credit: Nicola, J.P., Carrasco, N., Masini-Repiso, A.M Dietary IÀ Absorption: Expression and Regulation of the Na+/IÀ Symporter in the Intestine Vitamins and Hormones (2015) 98, pp 1–32 Academic Press is an imprint of Elsevier 225 Wyman Street, Waltham, MA 02451, USA 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 125 London Wall, London, EC2Y 5AS, UK The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK First edition 2015 Copyright © 2015 Elsevier Inc All rights reserved No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: 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operation of any methods, products, instructions, or ideas contained in the material herein ISBN: 978-0-12-803008-0 ISSN: 0083-6729 For information on all Academic Press publications visit our website at store.elsevier.com Former Editors ROBERT S HARRIS KENNETH V THIMANN Newton, Massachusetts University of California Santa Cruz, California JOHN A LORRAINE University of Edinburgh Edinburgh, Scotland PAUL L MUNSON University of North Carolina Chapel Hill, North Carolina JOHN GLOVER University of Liverpool Liverpool, England GERALD D AURBACH Metabolic Diseases Branch National Institute of Diabetes and Digestive and Kidney Diseases National Institutes of Health Bethesda, Maryland IRA G WOOL University of Chicago Chicago, Illinois EGON DICZFALUSY Karolinska Sjukhuset Stockholm, Sweden ROBERT OLSEN School of Medicine State University of New York at Stony Brook Stony Brook, New York DONALD B MCCORMICK Department of Biochemistry Emory University School of Medicine, Atlanta, Georgia CONTRIBUTORS Yasaman Aghazadeh The Research Institute of the McGill University Health Centre, and Department of Medicine, McGill University, Montreal, Quebec, Canada Denovan P Begg School of Psychology, University of New South Wales (UNSW, Australia), Sydney, New South Wales, Australia Liliana G Bianciotti Ca´tedra de Fisiopatologı´a, Facultad de Farmacia y Bioquı´mica, Universidad de Buenos Aires, Instituto de Inmunologı´a, Gene´tica y Metabolismo (INIGEM-CONICET), Buenos Aires, Argentina Nabila Boukelmoune Department of Integrative Biology and Pharmacology, The University of Texas Health Science Center at Houston, Houston, Texas, USA Rafael Brito Program of Neurosciences, Fluminense Federal University, Nitero´i, Rio de Janeiro, Brazil David A Buckley Department of Pharmacy, School of Applied Sciences, University of Huddersfield, Huddersfield, United Kingdom Nancy Carrasco Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut, USA Narattaphol Charoenphandhu Center of Calcium and Bone Research (COCAB), and Department of Physiology, Faculty of Science, Mahidol University, Bangkok, Thailand Lihe Chen Graduate School of Biomedical Sciences, The University of Texas Health Science Center at Houston, and Division of Renal Diseases and Hypertension, Department of Internal Medicine, University of Texas Medical School at Houston, Houston, Texas, USA Na´dia A de Oliveira Program of Neurosciences, Fluminense Federal University, Nitero´i, Rio de Janeiro, Brazil Alexandre dos Santos-Rodrigues Program of Neurosciences, Fluminense Federal University, Nitero´i, Rio de Janeiro, Brazil Peying Fong Department of Anatomy and Physiology, Kansas State University College of Veterinary Medicine, Manhattan, Kansas, USA xiii xiv Contributors Peter A Friedman Department of Pharmacology & Chemical Biology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA Jyothsna Gattineni Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, Texas, USA J€ urg Gertsch Institute of Biochemistry and Molecular Medicine, NCCR TransCure, University of Bern, Bern, Switzerland Marı´a J Guil Ca´tedra de Fisiologı´a e Instituto de la Quı´mica y Metabolismo del Fa´rmaco (IQUIMEFACONICET), Facultad de Farmacia y Bioquı´mica, Universidad de Buenos Aires, Buenos Aires, Argentina Sandra I Hope Ca´tedra de Fisiologı´a e Instituto de la Quı´mica y Metabolismo del Fa´rmaco (IQUIMEFACONICET), Facultad de Farmacia y Bioquı´mica, Universidad de Buenos Aires, Buenos Aires, Argentina Masahiro Ikeda Department of Veterinary Pharmacology, University of Miyazaki, Miyazaki, Japan Eric Madden Department of Integrative Biology and Pharmacology, The University of Texas Health Science Center at Houston, Houston, Texas, USA Mykola Mamenko Department of Integrative Biology and Pharmacology, The University of Texas Health Science Center at Houston, Houston, Texas, USA Ana Marı´a Masini-Repiso Departamento de Bioquı´mica Clı´nica, Facultad de Ciencias Quı´micas, Universidad Nacional de Co´rdoba, Co´rdoba, Argentina Toshiyuki Matsuzaki Department of Anatomy and Cell Biology, Gunma University Graduate School of Medicine, Maebashi, Japan Patrick C McHugh Department of Pharmacy, School of Applied Sciences, University of Huddersfield, Huddersfield, United Kingdom Juan Pablo Nicola Departamento de Bioquı´mica Clı´nica, Facultad de Ciencias Quı´micas, Universidad Nacional de Co´rdoba, Co´rdoba, Argentina Simon Nicolussi Institute of Biochemistry and Molecular Medicine, NCCR TransCure, University of Bern, Bern, Switzerland Roberto Paes-de-Carvalho Program of Neurosciences, Fluminense Federal University, Nitero´i, Rio de Janeiro, Brazil Contributors xv Vassilios Papadopoulos The Research Institute of the McGill University Health Centre; Department of Medicine; Department of Biochemistry, and Department of Pharmacology & Therapeutics, McGill University, Montreal, Quebec, Canada Mariana R Pereira Program of Neurosciences, Fluminense Federal University, Nitero´i, Rio de Janeiro, Brazil Oleh Pochynyuk Department of Integrative Biology and Pharmacology, The University of Texas Health Science Center at Houston, Houston, Texas, USA Matthias Quick Department of Psychiatry, Division of Molecular Therapeutics, Columbia University College of Physicians and Surgeons, New York State Psychiatric Institute, New York, USA Lei Shi Department of Physiology and Biophysics, Institute for Computational Biomedicine, Weill Medical College of Cornell University, New York, USA Andrey Sorokin Division of Nephrology, Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA Alexander Staruschenko Department of Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin, USA Marcelo S Vatta Ca´tedra de Fisiologı´a e Instituto de la Quı´mica y Metabolismo del Fa´rmaco (IQUIMEFA-CONICET), Facultad de Farmacia y Bioquı´mica, Universidad de Buenos Aires, Buenos Aires, Argentina Kannikar Wongdee Office of Academic Management, Faculty of Allied Health Sciences, Burapha University, Chonburi, and Center of Calcium and Bone Research (COCAB), Faculty of Science, Mahidol University, Bangkok, Thailand Oleg Zaika Department of Integrative Biology and Pharmacology, The University of Texas Health Science Center at Houston, Houston, Texas, USA Wenzheng Zhang Graduate School of Biomedical Sciences, The University of Texas Health Science Center at Houston, and Division of Renal Diseases and Hypertension, Department of Internal Medicine, University of Texas Medical School at Houston, Houston, Texas, USA Xi Zhang Division of Renal Diseases and Hypertension, Department of Internal Medicine, University of Texas Medical School at Houston, Houston, Texas, USA Barry R Zirkin Department of Biochemistry and Molecular Biology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Maryland, USA PREFACE Movements of hormones and ions through intracellular membranes and through the plasma membrane to the cell exterior and movement of these substances from the bloodstream into other cells require the agency of molecular transporters The functionality of these transporters is essential to the actions of hormones, such as insulin, norepinephrine, and dopamine, or to the actions of ions, such as sodium, calcium, phosphate, and iodide, or to the actions of other substances, such as cholesterol, vitamins, adenosine, endogenous cannabinoids (one is anandamide), and even water molecules If a transporter is not functioning properly, a disease condition may follow If there is an excess of a substance being transported and the availability of that substance needs to be reduced, a transporter can become a target for chemotherapy Of the many steps in the mechanisms of all of these critical molecules or atoms, the transporters themselves become vital regulators In this volume, the latest research is reviewed on these many topics To open this area, the transporters involved in the formation and action of thyroid hormones are considered The first topic is that of J.P Nicola, N Carrasco, and A.M Masini-Repiso on “Dietary IÀ Absorption: Expression and Regulation of the Na+/IÀ Symporter in the Intestine.” “Apical Iodide Efflux in Thyroid” is reviewed by P Fong D Braun and U Schweitzer contribute “Thyroid Hormone Transport and Transporters.” A discussion of the movement of sodium ion and the comovement of other molecules, in some cases, occurs through the following reviews M Quick and L Shi offer “The Sodium/Multivitamin Transporter: A Multipotent System with Therapeutic Implications.” “Regulation of αENaC Transcription” is authored by L Chen, X Zhang, and W Zhang M Mamenko, O Zaika, M Boukelmoune, E Madden, and O Pochynyuk write on “Control of ENaC-Mediated Sodium Reabsorption in the Distal Nephron by Bradykinin.” This topic is concluded with “Inhibition of ENaC by Endothelin-1,” a report by A Sorokin and A Staruschenko There are many other systems to be considered Of these, Y Aghazadeh, B.R Zirkin, and V Papadopoulos describe “Pharmacological Regulation of the Cholesterol Transport Machinery in Steroidogenic Cells of the Testis.” D.P Begg has written on “Insulin Transport into the Brain and Cerebrospinal Fluid.” “Regulation of Hormone-Sensitive Renal Phosphate Transport” is the focus of J Gattineni and P.A Friedman M Ikeda and xvii xviii Preface T Matsuzaki review “Regulation of Aquaporins by Vasopressin in the Kidney.” D.A Buckley and P.C McHugh contribute “The Structure and Function of the Dopamine Transporter and Its Role in CNS Diseases.” M.S Vatta, L.G Bianciotti, M.J Guil, and S.I Hope are the authors of “Regulation of the Norepinephrine Transporter by Endothelins: A Potential Therapeutic Target.” K Wongdee and N Charoenphandhu cover “Vitamin D-Enhanced Duodenal Calcium Transport.” “Endocannabinoid Transport Revisited” is the subject of S Nicolussi and J Gertsch The final contribution is that of A dos Santos-Rodrigues, M.R Pereira, R Brito, N.A de Oliveira, and R Paes-de-Carvalho who describe “Adenosine Transporters and Receptors: Key Elements for Retinal Function and Neuroprotection.” As always, Helene Kabes of Elsevier (Oxford, UK) and Vignesh Tamilselvvan of Elsevier (Chennai, India) have expedited the final preparations for the publication of this volume The cover illustration is taken from Fig of chapter entitled “Dietary IÀ Absorption: Expression and Regulation of the Na+/IÀ Symporter in the Intestine” by J.P Nicola, N Carrasco, and A.M Masini-Repiso GERALD LITWACK North Hollywood, California October 23, 2014 CHAPTER ONE Dietary I2 Absorption: Expression and Regulation of the Na+/I2 Symporter in the Intestine Juan Pablo Nicola*, Nancy Carrasco†,1, Ana María Masini-Repiso*,1 *Departamento de Bioquı´mica Clı´nica, Facultad de Ciencias Quı´micas, Universidad Nacional de Co´rdoba, Co´rdoba, Argentina † Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut, USA Corresponding authors: e-mail address: nancy.carrasco@yale.edu; amasini@fcq.unc.edu.ar Contents The Importance of Iodide in Human Health The Na+/IÀ Symporter 2.1 Molecular identification of NIS 2.2 NIS-mediated transport: Substrates and stoichiometry 2.3 The role of physiological Na+ concentrations in NIS affinity for IÀ NIS Expression Beyond the Thyroid Targeting of NIS to the Plasma Membrane Hormonal Regulation of NIS Expression Dietary IÀ Absorption Regulation of Intestinal NIS Expression Conclusions and Future Directions Acknowledgments References 2 10 11 13 19 24 25 26 Abstract Thyroid hormones are critical for the normal development, growth, and functional maturation of several tissues, including the central nervous system Iodine is an essential constituent of the thyroid hormones, the only iodine-containing molecules in vertebrates Dietary iodide (IÀ) absorption in the gastrointestinal tract is the first step in IÀ metabolism, as the diet is the only source of IÀ for land-dwelling vertebrates The Na+/IÀ symporter (NIS), an integral plasma membrane glycoprotein located in the brush border of enterocytes, constitutes a central component of the IÀ absorption system in the small intestine In this chapter, we review the most recent research on structure/ function relations in NIS and the protein's IÀ transport mechanism and stoichiometry, with a special focus on the tissue distribution and hormonal regulation of NIS, as well as the role of NIS in mediating IÀ homeostasis We further discuss recent findings concerning the autoregulatory effect of IÀ on IÀ metabolism in enterocytes: high Vitamins and Hormones, Volume 98 ISSN 0083-6729 http://dx.doi.org/10.1016/bs.vh.2014.12.002 # 2015 Elsevier Inc All rights reserved Juan Pablo Nicola et al intracellular IÀ concentrations in enterocytes decrease NIS-mediated uptake of IÀ through a complex array of posttranscriptional mechanisms, e.g., downregulation of NIS expression at the plasma membrane, increased NIS protein degradation, and reduction of NIS mRNA stability leading to decreased NIS mRNA levels Since the molecular identification of NIS, great progress has been made not only in understanding the role of NIS in IÀ homeostasis but also in developing protocols for NIS-mediated imaging and treatment of various diseases THE IMPORTANCE OF IODIDE IN HUMAN HEALTH Iodide (IÀ) uptake in the thyroid gland is the first step in the biosynthesis of thyroid hormones—triiodothyronine (T3) and thyroxine (T4) (Portulano, Paroder-Belenitsky, & Carrasco, 2014) Thyroid hormones are the only iodine-containing hormones in vertebrates and are required for the development and maturation of the central nervous system, skeletal muscle, and lungs in the fetus and the newborn They are also primary regulators of intermediate metabolism and effect pleiotropic modulation in virtually all organs and tissues throughout life (Yen, 2001) Iodine is an extremely scarce element in the environment and is supplied to the body exclusively through the diet Insufficient dietary IÀ intake may cause mild to severe hypothyroidism and subsequently goiter, stunted growth, retarded psychomotor development, and even cretinism (impairment of physical growth and irreversible mental retardation due to severe thyroid hormone deficiency during childhood) (Zimmermann, 2009) IÀ deficiency-associated diseases are the most common preventable cause of mental retardation in the world and were slated for global eradication by iodination of table salt by the year 1990 by the World Health Organization Although significant progress has been made, there were still an estimated 1.88 billion people suffering from insufficient IÀ intake in 2011 (Andersson, Karumbunathan, & Zimmermann, 2012) As iodine is an irreplaceable component of thyroid hormones, normal thyroid physiology relies on adequate dietary IÀ intake, gastrointestinal IÀ absorption, and proper IÀ accumulation in thyrocytes Therefore, the evolution of a highly efficient system to avidly accumulate IÀ appears to be a physiological adaptation to compensate for the environmental scarcity of iodine THE Na+/I2 SYMPORTER The thyroid gland has developed a remarkably efficient system to ensure an adequate supply of IÀ for thyroid hormone biosynthesis Under Intestinal Na+/IÀ Symporter physiological conditions, the thyroid concentrates IÀ approximately 40-fold with respect to the plasma concentration (Wolff & Maurey, 1961) Moreover, the ability of the thyroid to concentrate IÀ has provided the molecular basis for the use of radioiodide in the diagnosis, treatment, and follow-up of thyroid pathology (Bonnema & Hegedus, 2012; Reiners, Hanscheid, Luster, Lassmann, & Verburg, 2011) A major breakthrough in the field—as important as the introduction of radioactive IÀ isotopes into the study of thyroid physiology near the middle of the twentieth century (Hertz, Roberts, Means, & Evans, 1940)—was the identification of the complementary DNA (cDNA) encoding the Na+/IÀ symporter (NIS), the protein that mediates IÀ transport in the thyroid (Dai, Levy, & Carrasco, 1996) The identification of NIS started a new era of intensive IÀ research 2.1 Molecular identification of NIS The journey toward the identification of NIS began with the isolation of poly(A+) RNA from FRTL-5 cells, a line of highly differentiated rat thyroid-derived cells which, microinjected into Xenopus laevis oocytes, produced Na+-dependent IÀ transport (Vilijn & Carrasco, 1989) Thereafter, the cDNA encoding NIS was isolated by expression cloning in X laevis oocytes using cDNA libraries generated from FRTL-5 cells (Dai et al., 1996) The full nucleotide sequence revealed an open reading frame of 1,854 nucleotides encoding a protein of 618 amino acids Shortly thereafter, the screening of a human thyroid cDNA library with rat NIS probes enabled the identification of human NIS (Smanik et al., 1996), which exhibits 84% identity and 93% similarity to rat NIS The human NIS gene was mapped to chromosome 19p13.11 and comprises 15 exons with an open reading frame of 1,929 nucleotides, giving rise to a protein of 643 amino acids (Smanik, Ryu, Theil, Mazzaferri, & Jhiang, 1997) NIS is an intrinsic plasma membrane glycoprotein The current, experimentally tested NIS secondary structure model shows a hydrophobic protein with 13 transmembrane segments (TMSs), an extracellular amino terminus and an intracellular carboxy terminus (Levy et al., 1997, 1998; Fig 1A) Moreover, NIS is a highly N-glycosylated protein, although N-glycosylation is not essential for IÀ transport or NIS trafficking to the plasma membrane (Levy et al., 1998) NIS-driven active transport of IÀ into the thyroid is electrogenic and relies on the driving force of the Na+ gradient generated by the Na+/K+ ATPase and the electrical potential across the plasma membrane By ... concerning the autoregulatory effect of IÀ on IÀ metabolism in enterocytes: high Vitamins and Hormones, Volume 98 ISSN 0083-6729 http://dx.doi.org/10.1016/bs.vh.2014.12.002 # 2015 Elsevier Inc... University, Chonburi, and Center of Calcium and Bone Research (COCAB), Faculty of Science, Mahidol University, Bangkok, Thailand Oleg Zaika Department of Integrative Biology and Pharmacology, The... Biochemistry and Molecular Biology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Maryland, USA PREFACE Movements of hormones and ions through intracellular membranes and through