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Eptatretus Stoutii) CARDIAC CONTROL IN THE PACIFIC HAGFISH (EPTATRETUS STOUTII) by Christopher Mark Wilson B.Sc., University of Manchester, 2007 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in The Faculty of Graduate and Postdoctoral Studies (Zoology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) October 2014 © Christopher Mark Wilson, 2014 ABSTRACT The Pacific hagfish (Eptatretus stoutii), being an extant ancestral craniate, possesses the most ancestral craniate-type heart with valved chambers, a response to increased filling pressure with increased stroke volume (Frank-Starling mechanism), and myogenic contractions. Unlike all other known craniate hearts, this heart receives no direct neural stimulation. Despite this, heart rate can vary four-fold during a prolonged, 36-h anoxic challenge followed by a normoxic recovery period, with heart rate decreasing in anoxia, and increasing beyond routine rates during recovery, a remarkable feat for an aneural heart. This thesis is a study of how the hagfish can regulate heart rate without the assistance of neural stimulation. A major role of hyperpolarization-activated cyclic nucleotide-activated (HCN) channels in heartbeat initiation was indicated by pharmacological application of zatebradine to spontaneously contracting, isolated hearts, which stopped atrial contraction and vastly reduced ventricular contraction. Tetrodotoxin inhibition of voltage-gated Na+ channels induced an atrioventricular block suggesting these channels play a role in cardiac conduction. Partial cloning of HCN channel mRNA extracted from hagfish hearts revealed six HCN isoforms, two hagfish representatives of vertebrate HCN2 (HCN2a and HCN2b), three of HCN3 (HCN3a, HCN3b and HCN3c) and one HCN4. Two paralogs of HCN3b were discovered, however, HCN3a dominated the expression of ii HCN isoforms followed by HCN4. All HCN isoforms bar HCN3b were dominantly expressed in the atrium, likely to support greater atrial excitability ensuring synchronous contractions. Phylogenetic analysis suggested that HCN3 is the ancestral isoform supporting previous observations. Studies with β-adrenoreceptor agonists and antagonists in isolated, spontaneously beating hearts showed that the routine normoxic heart rate may involve maximal catecholamine stimulation of heart rate through cAMP stimulation of HCN channels via transmembrane adenylyl cyclase (tmAC). Loss of this tonic β-adrenorecptor cardiac stimulation during anoxia reduces heart rate, but restoring β-adrenoreceptor stimulation during normoxic recovery does not produce the previously observed increase above routine heart rate in vivo. Instead, bicarbonate-stimulated, soluble adenylyl cyclase (sAC) mediated cAMP production was found to produce this tachycardia in addition to the reinstated tmAC produced cAMP. This is the first time sAC has been implicated in heart rate control. iii PREFACE This work represents original research conducted by the author (Wilson, C.M.) primarily at the University of British Columbia, Point Grey Campus (UBC), Bamfield Marine Sciences Centre, Bamfield (BMSC), and the University of British Columbia and Department of Fisheries and Oceans Canada, Centre for Aquaculture and Environmental Research, West Vancouver (WVL). A version of Chapter 2 has been published [Wilson, C.M., Farrell, A.P., 2012. Pharmacological characterization of the heartbeat in an extant vertebrate ancestor, the Pacific hagfish, Eptatretus stoutii. Comp. Biochem. Physiol. 164A:258-263]. All experimental work was conducted at BMSC and WVL by C.M. Wilson, who also produced the first draft of the manuscript, designed apparatus, analyzed data and produced the figures. As supervisor, A.P. Farrell assisted C.M. Wilson in experimental concept formation, experimental design, result interpretation and manuscript edits. A version Chapter 3 has been published as part of a collaboration with the University of Oslo, Norway (UO), with experiments being conducted at BMSC, WVL and UO [Wilson, C.M., Stecyk, J.A.W., Couturier, C.S., Nilsson, G.E., Farrell, A.P., 2013. Phylogeny and effects of anoxia on hyperpolarization-activated, cyclic nucleotide- gated channel gene expression in the heart of a primitive chordate, the Pacific hagfish (Eptatretus stoutii). J. Exp. Biol. 216:4462-4472]. As lead investigator, C.M. iv Wilson contributed to experimental design, primer design, performed all experiments, analyzed data, and produced both the figures and the first draft of the manuscript. J.A.W. Stecyk contributed to experimental design. C.S. Couturier assisted with data analysis and, with J.A.W. Stecyk, assisted with primer design and taught C.M. Wilson real-time PCR and phylogenetic analyses under the supervision of G.E. Nilsson. A.P. Farrell conceived the investigation and contributed to experimental design and production of the first draft of the manuscript. All authors contributed to data interpretation and manuscript edits. Chapter 4 was a collaboration between UBC, the Scripps Institution of Oceanography, University of California San Diego (UCSD) with experiments being conducted at UBC, BMSC, WVL and UCSD. As lead investigator, C.M. Wilson designed the experiment and apparatus, conducted all experiments bar immunofluorescence and cAMP production assay, analyzed the data and produced the figures and first draft of the manuscript. J. Roa taught C.M. Wilson molecular techniques and conducted bar immunofluorescence and cAMP production assay experiments. Figures 4.3 and 4.4 were produced using data obtained by J. Roa in these experiments. Molecular experiments were conducted under the supervision of M. Tresguerres who also assisted in experimental design and teaching. Plasma pH was measured by G.C. Cox. As supervisor, A.P. Farrell contributed to experimental concept formation, experimental design, result interpretation and manuscript edits. v TABLE OF CONTENTS ABSTRACT ................................................................................................................ ii PREFACE .................................................................................................................. iv TABLE OF CONTENTS ............................................................................................ vi LIST OF TABLES ...................................................................................................... xi LIST OF FIGURES ................................................................................................... xii LIST OF SYMBOLS AND ABBREVIATIONS ......................................................... xiv ACKNOWLEDGEMENTS ...................................................................................... xvii DEDICATION........................................................................................................... xix CHAPTER 1: INTRODUCTION ................................................................................. 1 1.1 Preface ...................................................................................................... 1 1.2 The initiation of the craniate heartbeat: Funny currents vs. calcium clocks .............................................................................................................. 4 1.2.1 The membrane clock ................................................................... 7 1.2.2 The calcium clock ........................................................................ 8 1.2.3 Integrated model of cardiac pacemaking ..................................... 9 1.3 Cardiac pacemaking in fish ..................................................................... 10 1.4 Initiation of the hagfish heartbeat ............................................................ 11 1.4.1 Hyperpolarization-activated cyclic nucleotide-gated channels ... 12 1.5 Regulating heart rate with HCN ............................................................... 14 1.5.1 HCN gating by cAMP ................................................................. 14 vi 1.5.2 Modulation of adenylyl cyclase activity by the autonomic nervous system and catecholamines ............................................................... 15 1.5.3 The variable heart rate of the aneural Pacific hagfish heart ...... 19 1.6 Overview of thesis questions and working hypotheses ........................... 20 1.7 Initiation of the heartbeat ......................................................................... 21 1.7.1 Does the membrane clock set intrinsic heart rate in Pacific hagfish? .............................................................................................. 21 1.8 Synchronization of cardiac contraction .................................................... 22 1.8.1 Are HCN channels involved in synchronous beating of the cardiac chambers in the Pacific hagfish? ........................................... 22 1.9 Control of heart rate ................................................................................ 25 1.9.1 Does varying HCN mRNA expression during anoxia and subsequent recovery suggest that HCN channel expression may have a role in heart rate control under these conditions? ............................ 25 1.9.2 Does varying tmAC activation modulate heart rate? .................. 26 1.9.3 Are there other mechanisms of HCN gating with cAMP? .......... 27 1.10 My proposed model of heartbeat control in an aneural heart ..... 28 CHAPTER 2: PHARMACOLOGICAL CHARACTERIZATION OF THE HEARTBEAT IN AN EXTANT VERTEBRATE ANCESTOR, THE PACIFIC HAGFISH, EPTATRETUS STOUTII.......................................................................
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