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Peptidergic, Purinergic and Adrenergic Neurotransmitters

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Peptidergic, Purinergic and Adrenergic Neurotransmitters PEPTIDERGIC, PURINERGIC AND ADRENERGIC NEUROTRANSMITTERS IN THE CONTROL OF THE CORONARY ARTERY by Laura Anne Corr Department of Anatomy and Developmental Biology and Centre for Neuroscience, University College London Gower Street, London WC1 and Department of Cardiac Medicine, National Heart and Lung Institute, Dovehouse Street, London SW3 Thesis submitted for the degree of Doctor of Philosophy University of London 1 ABSTRACT OF THESIS In addition to the "classical" transmitters, noradrenaline and acetylcholine, autonomic perivascular nerves are now known to contain several peptide and purine neurotransmitters. These may act directly on the vascular smooth muscle, as cotransmitters or neuromodulators, and may also stimulate endothelial responses. This thesis presents a study of the smooth muscle and endothelial responses of the coronary artery to such neurotransmitters. It also describes changes in the peptidergic innervation and in the responses to these neurotransmitters which occur under physiological and pathophysiological conditions. Acetylcholine produced endothelium-dependent relaxation of the rabbit epicardial coronary artery at low concentrations, but smooth muscle constriction dominated at higher concentrations. Noradrenaline relaxed this vessel by action on smooth muscle 0-adrenoceptors which were identified as 0j; the endothelium played no role in mediating responses to the 0-adrenergic agonists. There was very little alpha-receptor-mediated vasoconstrictor response to noradrenaline; ATP too was found to act directly as a vasodilator of the smooth muscle in this vessel, supporting the hypothesis that noradrenaline and ATP may be inhibitory co-transmitters in the coronary artery. Examination of the purinoceptor subtypes demonstrated not only Pj- but also P2y-purinoceptors on the smooth muscle and on the endothelium, while P2^-purinoceptors were found only on the smooth muscle. 2 The responses of the coronary arteries of female rabbits to these adrenergic and purinergic transmitters, as well as some of the more recently recognised peptidergic neurotransmitters, were found to undergo profound changes during development of sexual maturity. Coronary arteries from the New Zealand white (NZW) rabbits were compared with those from Watanabe Hereditable Hyperlipidaemic (WHHL) rabbits to assess the long-term effects of atherosclerosis on the responses to these agents. This study showed that endothelium-dependent responses were depressed in the young WHHL animals. Maturational changes in the atherosclerotic rabbits in the responses to non-endothelium-dependant agonists mirrored closely those seen in normal rabbits but the responses to the endothelium-dependant vasodilators differed markedly, showing a compensatory recovery during maturation while the response in the normal animals declined. Using guanethidine to produce long-term sympathectomy in neonatal rats, compensatory changes in peptide-containing nerves were examined using immunohistochemical and assay techniques. Non-sympathetic NPY-containing nerves were identified in the ileum, bladder, heart and vas deferens but blood vessels were supplied entirely by sympathetic NPY-containing nerves. Despite the reduction of sympathetic NPY, the non-sympathetic NPY-containing nerves did not proliferate to compensate for the loss of the sympathetic nerves. However, marked and selective increases were found in nerves immunoreactive for the sensory neurotransmitter calcitonin gene-related peptide, but not for substance P or vasoactive intestinal polypeptide. The pattern of receptors exhibited by the coronary artery and the changes in innervation and responses which were demonstrated in health and disease are discussed. 3 TO MY PARENTS, NUALA AND GERRY, WHOM I LOVE VERY MUCH ACKNOWLEDGEMENTS I am most grateful to my supervisors, Professor Geoffrey Burnstock and Professor Philip Poole-Wilson, for their interest, encouragement and advice which often extended to matters beyond the scope of this thesis. My thanks also to the many people who helped me during this period. In particular I thank my friend and collaborator Judy Aberdeen, with whom all the work in Chapters 10 and 11 was carried out; Jill Lincoln, who performed the catecholamine assays with HPLC in Chapters 10 and 11; Pam Milner, who assayed the peptides using an ELISA in Chapters 10 and 11; Sian Harding and Charles Hoyle who provided generous and helpful advice; Mollie White, Annie Evans and Rosie Cole for their friendly support and secretarial skills; Gill Knight for her cheerful companionship and practical help; Marie Phillips and Edith Quinn for their technical help and advice; Frances Cribben and Phillippa Chara tan for editorial assistance; the staff of the photographic department; the staff of the joint animal house; and the many other colleagues who provided practical support and helped make the time so personally rewarding. I am especially grateful to Bradford Marks for the love and laughter. I am indebted to the Medical Research Council for financial support. Other than the work in Chapters 10 and 11 acknowledged above, this thesis is entirely my own work. 5 CONTENTS Abstract ........................................................................................................................ 2 Acknowledgements......................................................................................................... 5 Contents .......................................................................................................................... 6 List of Tables ................................................................................................................ 15 List of Figures ............................................................................................................ 16 CHAPTER 1 INTRODUCTION ............................................................................ 17 CHAPTER 2 GENERAL BACKGROUND .......................................................... 21 2.1 A CLINICAL PERSPECTIVE .................................................................... 21 2.1.1 Coronary Heart Disease ......................................................................... 21 2.1.2 Changing Concepts ........................................................................... 22 2.1.3 The Role of Coronary Vasospasm .................................................. 23 2.2 STRUCTURE AND FUNCTION OF THE CORONARY ARTERIES . 26 2.2.1 The Coronary Circulation ............................................................... 26 2.2.2 Factors Controlling Coronary Blood Flow ...................................... 27 2.2.3 Structure of the Epicardial Coronary Artery ................................. 28 2.3 THE ROLE OF ENDOTHELIUM ................................................................ 30 2.3.1 Traditional Concepts ........................................................................ 30 2.3.2 New Concepts ................................................................................... 32 i Endothelial Control of Vasomotor Tone .......................... 32 ii The Endothelium as a Source of Vasoactive Agents ...... 34 6 2.4 THE ROLE OF THE AUTONOMIC NERVOUS SYSTEM 35 2.4.1 Sympathetic Nervous System .......................................................... 35 i Anatomy ............................................................................... 35 ii Autonomic Neuroeffector Junction .................................. 36 iii Sympathetic Neurotransmitters and Receptors - Classical View ................................................................... 38 iv New Concepts - Cotransmission and Neuromodulation ............................ 40 2.4.2 Parasympathetic Nervous System .................................................... 42 i Anatomy ............................................................................... 42 ii Parasympathetic Neurotransmitters and Receptors - Classical View ................................................................... 43 iii New Concepts ....................................................................... 45 2.4.3 Sensory-Motor Nervous System ...................................................... 47 i Anatomy ............................................................................... 47 ii Sensory-Motor Neurotransmitters and Receptors ........... 47 2.4.4 Intrinsic Nevous System .................................................................. 49 2.4.5 Neuronal Plasticity ........................................................................... 50 CHAPTER 3 GENERAL METHODOLOGY ......................................................... 54 3.1 PHARMACOLOGY ...................................................................................... 54 3.1.1 Choice of Preparation ....................................................................... 54 3.1.2 Method ............................................................................................... 56 3.1.3 Administration of Drugs .................................................................. 59 7 3.2 HISTOCHEMISTRY .................................................................................. 60 3.2.1 Fluorescence Histochemistry for Noradrenaline ........................... 60 i Introduction .......................................................................... 60 ii Method for Whole Mounts .................................................... 61 iii Method for Sections ............................................................ 62 iv Assessment of Innervation ...................................................
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