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Why Do We Have Purkinje Fibers Deep in Our Heart?

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Why Do We Have Purkinje Fibers Deep in Our Heart? Physiol. Res. 63 (Suppl. 1): S9-S18, 2014 REVIEW Why Do We Have Purkinje Fibers Deep in Our Heart? D. SEDMERA1,2, R. G. GOURDIE3,4,5 1Institute of Anatomy, First Faculty of Medicine, Charles University, Prague, Czech Republic, 2Department of Cardiovascular Morphogenesis, Institute of Physiology Academy of Sciences of the Czech Republic, Prague, Czech Republic, 3Virginia Tech Carilion Research Institute, Center for Heart and Regenerative Medicine Research, Roanoke, Virginia, USA, 4Virginia Tech School of Biomedical Engineering and Sciences, Roanoke, Virginia, USA, 5Department of Emergency Medicine, Virginia Tech Carilion School of Medicine, Roanoke, Virginia, USA Received October 21, 2013 Accepted October 29, 2013 Summary internodal tracts, the atrioventricular node, the Purkinje fibers were the first discovered component of the atrioventricular (His) bundle, its right and left branches, cardiac conduction system. Originally described in sheep in 1839 and the network of Purkinje fibers. While the functional as pale subendocardial cells, they were found to be present, equivalent of these components are present in some form although with different morphology, in all mammalian and avian in all vertebrate hearts (Sedmera et al. 2003), all hearts. Here we review differences in their appearance and morphologically distinct parts are present only in the extent in different species, summarize the current state of heart of mammals. While development of the CCS has knowledge of their function, and provide an update on markers been subject to numerous reviews (Gourdie et al. for these cells. Special emphasis is given to popular model 2003a,b, Christoffels et al. 2010, Burggren et al. 2013), species and human anatomy. little was written on the comparative morphology of its components in different species, with a few notable Key words exceptions (Davies 1930, Davies et al. 1952, 1994). The Cardiac conduction system • Specialized tracts • Gap junctions • goal of this overview is to put the Purkinje fibers into Connexin context of other CCS components, briefly describe the history of their discovery, provide functional insight into Corresponding author equivalent structures in the lower vertebrates, and then to D. Sedmera, Department of Cardiovascular Morphogenesis, focus in detail on their structure and function in the most Institute of Physiology, Academy of Sciences of the Czech popular model species of mammals and birds. Republic, Videnska 1083, 14220 Prague, Czech Republic. E-mail: [email protected] Function of individual CCS components Introduction The SA node is the principal pacemaker of the heart. Under normal conditions it is the cardiac tissue that The cardiac conduction system (CCS) is defined autonomously sets the rhythm of the heart beat. It is also as a network of specialized myocardial cells that subject to neurohumoral regulation, in particular by generates the cardiac rhythm and assures a coordinated autonomous nervous system. This allows the heart to propagation of the electrical impulse for efficient change its frequency in reaction to the functional status of contraction of the heart. In the adult mammalian heart, the organism. Morphologically, it is organized into a the CCS comprises the sinoatrial (SA) node, the three dimensionally complex compact structure PHYSIOLOGICAL RESEARCH • ISSN 0862-8408 (print) • ISSN 1802-9973 (online) © 2014 Institute of Physiology v.v.i., Academy of Sciences of the Czech Republic, Prague, Czech Republic Fax +420 241 062 164, e-mail: [email protected], www.biomed.cas.cz/physiolres S10 Sedmera and Gourdie Vol. 63 (Mommersteeg et al. 2007, Fedorov et al. 2010), with (Mommersteeg et al. 2007, Aanhaanen et al. 2009, 2010). specific connection points to the working atrial Electrophysiologically, this region shows a typical action myocardium. In lower vertebrates, its function is potential shape (Arguello et al. 1986) and has a level of contained in a compartment termed the sinus venosus automaticity, which can manifest even in the embryo (Koprla 1987, Jensen et al. 2012). New data on the when the sinoatrial node is perturbed (Raddatz 1997). cellular origin of the SA node from outside the traditional Interfaces between atria and node and node and His are heart fields and role of Wnt signaling in recruitment of marked by distinct transitions in connexin expression mesodermal cells into pacemaker lineage were recently (Coppen et al. 1999, Gourdie and Sedmera 2008). Such reported by the Mikawa lab (Bressan et al. 2013). abrupt changes in cellular coupling can play a role in AV delay generation in adult heart (Choi and Salama 1998). Atrial special conduction pathways The His bundle The morphological distinction of specialized intra-atrial and internodal conduction pathways is a Also known as the atrioventricular, or non- controversial topic. Some claim that there are tracts of branching bundle, it forms under normal conditions the Purkinje-like cells connecting the sinoatrial and only conductive pathway between the atria and the atrioventricular node (James and Sherf 1971), while other ventricles. It is a rapidly conducting tissue, with agree that the conduction through the atria is anisotropic, propagation velocity an order of magnitude faster than see the main reason in holes caused by the entrance the working myocardium. As it traverses the vessels (Betts et al. 2002, Ho et al. 2002). Our view is atrioventricular fibrous plane, the bundle is insulated that these preferential conduction pathways, the best from the rest of the myocardium except of its proximal example of which is the interatrial bundle of Bachmann connection with the AV node and distal bifurcation into (Sedmera et al. 2006) can be explained by tissue the left and right bundle branch. geometry (pectinate muscles), in agreement with previous experimental data (Komuro et al. 1986), but are open to a The bundle branches marker that would distinguish cells within those tracts from the remaining atrial myocytes. These form continuation of the His bundle, sharing many of its characteristics – rapid conduction The AV node speed, expression of gap junction protein connexin40 (without co-expression of connexin43) and fibrous The main function of the atrioventricular node is insulation from the working myocardium. This makes generation of a delay between activation (and ensuing these bundles well suited to act as electrical cables, contraction) of the atria and the ventricles. Due to its assuring rapid spread of the impulse through the prolonged refractory period, it also serves as a filter ventricles. There is a notable asymmetry between the left against propagation of atrial tachyarrhythmias to the and right bundle branch, the left being broad, in the ventricles. In mammals, it shows a distinct morphological mouse composed of multiple parallel isolated strands, organization with specific cell phenotypes (Efimov et al. while the right bundle being a narrow structure (Miquerol 1997, Aanhaanen et al. 2010). On the other hand, its et al. 2004). It is likely due to optimization of source:sink morphological localization in birds is still obscure ratio due to a marked asymmetry of the myocardial mass (Vicente-Steijn et al. 2011). In lower vertebrates, and between the left and right ventricle. during embryonic development, the function of delay generator is located in the atrioventricular canal region, a The Purkinje fibers slowly proliferating, conducting and contracting portion of the cardiac tube that apparently retains its “primitive” The Purkinje fibers are the terminal part of the phenotype – not following the pathway of chamber cardiac conduction system. They form a three- myocardium differentiation (Kirby 2007). The dimensional subendocardial network originating from the transcriptional regulation of these events has been bundle branches and their main function is to distribute recently uncovered, and Tbx2, BMP and Tbx3 are the depolarization signal rapidly to the working implicated in maintaining this transcription programme myocardium. 2014 Purkinje Fibers in Vertebrates S11 Discovery of CCS Differentiation of Purkinje fibers during development The historical sequence, in which various CCS components were discovered, is in reverse order to the It has been shown in experimental studies in the functional sequence of activation. In 1839 the Czech chick heart, that ventricular Purkinje fibers share scientist Jan Evangeliste Purkinje described a pale common origin with the surrounding ventricular network of cells in the sheep heart, and noted their myocytes and terminally differentiate during fetal period microscopic characteristics, including the presence of one (Gourdie et al. 1995). In the avian model, it was or two nuclei and cross striations, which made him, after convincingly demonstrated that the differentiation some discussion, consider them a special form muscular towards the conduction phenotype is time-sensitive, and tissue (Eliska 2006). It took more than fifty years before a locally produced endothelin-1 was demonstrated to be a Swiss physiologist His found the elusive connection key signaling molecule (Gourdie et al. 1998, Hyer et al. between the atrial and ventricular myocardium, first by a 1999, Takebayashi-Suzuki et al. 2000). The clonal series of cuts in the beating heart, then by detailed relationship between the working ventricular myocytes histological examination of the region, where such cuts and Purkinje myocytes observed in birds was confirmed led to atrioventricular block (Suma 2001). Over a decade recently
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