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2 Cardiac Development BRAD J. MARTINSEN, PhD AND JAMIE L. LOHR, MD CONTENTS INTRODUCTION TO HUMAN HEART EMBRYOLOGY AND DEVELOPMENT PRIMARY HEART FIELD AND LINEAR HEART TUBE FORMATION SECONDARY HEART FIELD, OUTFLOWTRACT FORMATION, AND CARDIAC LOOPING CARDIAC NEURAL CREST AND OUTFLOWTRACT AND ATRIAL AND VENTRICULARSEPTATION PROEPICARDIUM AND CORONARY ARTERY DEVELOPMENT CARDIAC MATURATION SUMMARY OF EMBRYONIC CONTRIBUTIONTO HEART DEVELOPMENT REFERENCES 1. INTRODUCTION TO HUMAN HEART human congenital heart disease (5). In addition, great strides EMBRYOLOGY AND DEVELOPMENT have also been made in our knowledge of the contribution of the cardiac neural crest and the epicardium to overall heart devel- The primary heart field, secondary heart field, cardiac neural opment. crest, and proepicardium are the four major embryonic regions involved in the process of vertebrate heart develop- 2. PRIMARY HEART FIELD ment (Fig. 1). They each make an important contribution to AND LINEAR HEART TUBE FORMATION overall cardiac development, which occurs with complex developmental timing and regulation. This chapter describes The cells that will become the heart are among the first cell how these regions interact to form the final structure of the heart lineages formed in the vertebrate embryo (6,7). By day 15 of in relationship to the generalized developmental timeline of human development, the primitive streak has formed (8), and human embryology (Table 1). the first mesodermal cells to migrate (gastrulate) through the The heart is the first organ to fully form and function during primitive streak are cells fated to become the heart (9,10) vertebrate development, and many of the underlying mecha- (Fig. 2). These mesodermal cells migrate to an anterior and nisms are considered molecularly and developmentally con- lateral position where they form bilateral primary heart fields served (1). The description presented here is based on heart (Fig. 1A) (11). Studies of chick development have not sup- development research from the chick, mouse, frog, and human ported the previously held notion of a medial cardiac crescent model systems. Importantly, numerous research findings have that bridges the two bilateral primary heart fields (12). Com- redefined the understanding of the primary heart field, which plete comparative molecular and developmental studies gives rise to the main structure of the heart (atria and ventricles) between the chick and mouse are required to confirm these and have led to exciting discoveries of the secondary heart field, results. The posterior border of the bilateral primary heart field which gives rise to the outflow tracts of the mature heart (2-4). reaches to the first somite in the lateral mesoderm on both sides These discoveries were a critical step in advancing our under- of the midline (Fig. 1A) (3,12). standing of how the outflow tracts of the heart form, an area in At day 18 of human development, the lateral plate meso- which many congenital heart defects arise, and thus have had derm is split into two layers: somatopleuric and splanchno- important implications for the understanding and prevention of pleuric (8). It is the splanchnopleuric mesoderm layer that From: Handbook of Cardiac Anatomy, Physiology, and Devices contains the myocardial and endocardial cardiogenic precur- Edited by: P. A. Iaizzo © Humana Press Inc., Totowa, NJ sors in the region of the primary heart fields as defined above. 15 16 PART I1: ANATOMY / MARTINSEN AND I.OHR Fig. 1. The four major contributors to heart development illustrated in the chick model system: primary heart field, secondary heart field, cardiac neural crest, and proepicardium. (A) Day 1 chick embryo (equivalent to day 20 of human development). Red denotes primary heart field cells. (B) Day 2.5 chick embryo (equivalent to -5 wk of human development). Green denotes cardiac neural crest cells; yellow denotes secondary heart field cells; blue denotes proepicardial cells. (C) Day 8 chick heart (equivalent to -9 wk of human development). Green dots represent derivatives of the cardiac neural crest; yellow dots represent derivatives of the secondary heart field; red dots represent derivatives of the primary heart fields; blue dots represent the derivatives of the proepicardium. Ao, aorta; APP, anterior parasympathetic plexis; Co, coronary vessels; E, eye; H, heart; IFT, inflow tract; LA, left atrium; LV, left ventricle; Mb, midbrain; NF, neural folds; OFT, outflow tract; Otc, otic placode; P, pulmonary artery; RA, right atrium; RV, right ventricle; T, trunk. CHAPTER 2 / C'ARDIAC DEVELOPMENT 17 Table 1 Developmental Timeline of Human Heart Embryology Days of human Developmental development process 0 Fertilization. 1-4 Cleavage and movement down the oviduct to the uterus. 5-12 Implantation of the embryo into the uterus. 13-14 Primitive streak formation (midstreak level contains precardiac cells). 15-17 Formation of the three primary germ layers (gastrulation): ectoderm, mesoderm, and endoderm. Midlevel primitive streak cells that migrate to an anterior and lateral position form the bilateral primary heart field. 17-18 Lateral plate mesoderm splits into the somatopleuric mesoderm and splanchnopleuric mesoderm. Splanchnopleuric mesoderm contains the myocardial and endocardial cardiogenic precursors in the region of the primary heart field. 18-26 Neurulation (formation of the neural tube) 20 Cephalocaudal and lateral folding brings the bilateral endocardial tubes into the ventral midline of the embryo. 21-22 Heart tube fusion. 22 Heart tube begins to beat. 22-28 (3-4 wk) Heart looping and the accretion of cells from the primary and secondary heart fields. 22-28 (3-4 wk) Proepicardial cells invest the outer layer of the heart tube and eventually form the epicardium and coronary vasculature. 22-28 (3-4 wk) Neural crest migration starts. 32-37 (5-6 wk) Cardiac neural crest migrates through the aortic arches and enters the outflow tract of the heart. 57+ (9 wk) Outflow tract and ventricular septation complete. Birth Functional septation of the atrial chambers as well as the pulmonary and systemic circulatory systems. Most of the human developmental timing information is from ref. 8, except for the human staging of the secondary heart field and proepicardium, which was correlated from other model systems (2~l,14). Neural fold Dorsal aorta Presumptive endocardial cells delaminate from the splanch- Somatopleuric nopleuric mesoderm and coalesce via vasculogenesis to form planchnopleuric two lateral endocardial tubes (Fig. 2A) (13). igrating During the third week of human development, two bilateral hnopleuric cells layers of myocardium surrounding the endocardial tubes are A Endocardial tube brought into the ventral midline during closure of the ventral foregut via cephalic and lateral folding of the embryo (Fig. 2A) (8). The lateral borders of the myocardial mesoderm layers are the first heart structures to fuse, followed by the fusion of the two endocardial tubes to form one endocardial tube surrounded by splanchnopleuric-derived myocardium (Fig. 2B,C). The medial borders of the myocardial mesoderm layers are the last g lateral to fuse (14). Thus, the early heart is continuous with noncardiac ardium splanchnopleuric mesoderm across the dorsal mesocardium (Fig. 2C). This will eventually partially break down to form the ventral aspect of the linear heart tube with a posterior inflow (venous pole) and anterior outflow (arterial pole), as well as the dorsal wall of the pericardial cavity (5,14). During the fusion of ~rest cells the endocardial tubes, the myocardium secretes an acellular y heart field matrix, forming the cardiac jelly layer that separates the myo- cardium and endocardium. 'sal By day 22 of human development, the linear heart tube ;ocardium begins to beat. As the human heart begins to fold and loop from days 22-28 (described in the next section), epicardial cells will endocardial invest the outer layer of the heart tube (Fig. 1B and Fig. 3A), resulting in a heart tube with four primary layers: endocardium, nyocardium cardiac jelly, myocardium, and epicardium (Fig. 3B) (8). 3. SECONDARY HEART FIELD, OUTFLOW TRACT Fig. 2. Cross-sectional view of human heart tube fusion: (A) Day 20, FORMATION, AND CARDIAC LOOPING cephalocaudal and lateral folding brings bilateral endocardial tubes into the ventral midline of the embryo. (B) Day 21, start of heart tube A cascade of signals identifying the left and right sides of the fusion. (C) Day 22, complete fusion, resulting in the beating primitive embryo are thought to initiate the process of primary linear heart tube. Ectoderm, dark gray; mesoderm, gray; endoderm, white. 18 PART I1: ANATOMY / MARTINSEN AND LOHR Mvocardium. Er pican rating Lrdial \ 'enosl Jm ~rsum A Fig. 3. Origin and migration of proepicardial cells. (A) Whole mount view of the looping human heart within the pericardial cavity at day 28. Proepicardial cells (dark gray dots, mesoderm origin) emigrate from the sinus venosus and possibly the septum transversum and then migrate out over the outer surface of the ventricles, eventually surrounding the entire heart. (B) Cross-sectional view of the looping heart showing the four layers of the heart: epicardium, myocardium, cardiac jelly, and endocardium. LV, left ventricle; RV, right ventricle. S Linear heart Looping & Septation tube Accretion Day 22 Day 28 9 weeks Fig. 4. Looping and septation of the human primary linear heart tube. Dark gray and white regions represent tissue added during the looping process from the primary and secondary
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