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10 Molecular Regulation of Cardiogenesis 10 Molecular Regulation of Cardiogenesis VISHAL NIGAM AND DEEPAK SRIVASTAVA ongenital heart malformations, the most common of all human destined to contribute to speci( c chambers of the future heart (reviewed Cbirth defects, occur in almost 1% of the population worldwide, in Srivastava and Olson, 2000). However, such studies could not regardless of race (Hoffman and Kaplan, 2002). An additional determine the clonal contributions of individual cells (Meilhac 1%–2% of the population harbor more subtle cardiac developmental et al., 2004). More recent studies using Cre-lox technologies to mark anomalies that only become apparent as age-dependent phenomena progenitor cells and all their descendents indicate—in stark contrast reveal the underlying pathology. With more than 1 million survivors to previous models—that the heart tube derived from the FHF may of congenital heart disease (CHD) in the United States, it is becoming predominantly provide a scaffold which enables a second population apparent that genetic disruptions which predispose to developmental of cells to migrate and expand into cardiac chambers (Buckingham defects can have ongoing consequences in the maintenance of speci( c et al., 2005). These additional cells arise from an area often referred cell types and cellular processes over decades (Srivastava, 2004). A to as the “second heart ( eld (SHF)” or “anterior heart ( eld” based on more precise understanding of the causes of CHD is imperative for its location anterior and medial to the crescent-shaped primary heart the recognition and potential intervention of progressive degenerative ( eld (Kelly et al., 2001; Mjaatvedt et al., 2001; Waldo et al., 2001; conditions among the survivors of CHD. Fig. 10–1). Both heart ( elds appear to be regulated by complex posi- Although genetic approaches have been important in understand- tive and negative signaling networks involving members of the bone ing human CHD, detailed molecular analysis of cardiac development morphogenetic protein (Bmp), sonic hedgehog (Shh), ( broblast growth in humans has been dif( cult. The recognition that genetic pathways factor (Fgf), Wnt and Notch proteins. Such signals often arise from the which dictate cardiac development are highly conserved across vastly adjacent endoderm, although the precise nature and role of these sig- diverse species ranging from * ies to man has resulted in a rapid nals remain unknown (reviewed in Schultheiss et al., 1997; Marvin expansion of information from the studies in more tractable biologi- et al., 2001; Schneider and Mercola, 2001; Zaffran and Frasch, cal models (Srivastava and Olson, 2000; Chien and Olson, 2002). 2002). SHF cells remain in an undifferentiated progenitor state until Despite the diversity of body plans adopted by different species, there incorporation into the heart, and this may in part be due to the closer seems to exist a common genetic program for the early formation of proximity to inhibitory Wnt signals emanating from the midline. a circulatory system. Cardiovascular systems seem to have developed Recent work has raised the possibility that the Tbx18 may be required increasing complexity to adapt to speci( c environments. In a simpli- for the formation of a venous pole, which contributes portions of the ( ed view, it appears that higher organisms have retained the morpho- atria and venous structures (Christoffels et al., 2006). logic steps used by lower organisms and have built complexity into the As the heart tube forms, the SHF cells migrate into the midline and heart as needed. In particular, the speci( cation of chamber structures position themselves dorsal to the heart tube in the pharyngeal meso- and the advent of a parallel circulation through chamber duplication derm. Upon rightward looping of the heart tube, SHF cells cross the and out* ow tract division by neural crest derivatives have facilitated pharyngeal mesoderm into the anterior and posterior portions, popu- the development of larger, air-breathing organisms using complex cir- lating a large portion of the out* ow tract, future right ventricle and culatory systems. In such a scheme, defects in particular regions of the atria (Cai et al., 2003; Fig. 10–1). Precursors of the left ventricle are heart may arise from speci( c genetic and environmental effects dur- sparsely populated by the SHF and appear to be largely derived from ing discrete developmental windows of time. To simplify the complex the FHF. In contrast to the FHF, SHF cells do not differentiate into events of cardiogenesis and CHD, different regions of the developing cardiac cells until they are positioned within the heart. Once within the heart will be considered individually in the context described earlier, heart, FHF and SHF cells appear to proliferate in response to endocar- weaving knowledge from model systems and human genetics when dial-derived signals such as neuregulin and epicardial signals depen- available. dent on retinoic acid, although the mechanisms through which these noncell autonomous events occur remain poorly understood (Garratt ORIGIN OF CARDIOMYOCYTE PRECURSORS et al., 2003; Stuckmann et al., 2003). Despite decades of cell lineage tracings and descriptive embryology CARDIOMYOCYTE AND HEART TUBE FORMATION of the heart’s origins, a more complete and accurate picture of cardio- genesis emerged only recently (reviewed in Buckingham et al., 2005; Fruit* ies have a primitive heart-like structure known as the dorsal ves- Srivastava, 2006). Two distinct mesodermal heart ( elds that share a sel that is analogous to the straight heart tube of the vertebrate embryo. common origin appear to contribute cells to the developing heart in a It contracts rhythmically and pumps hemolymph through an open temporally and spatially speci( c manner. The well-studied “( rst heart circulatory system. Formation of the dorsal vessel in * ies is depen- ( eld” (FHF) is derived from cells in the anterior lateral plate meso- dent on a protein, tinman, whose name is based on the Wizard of Oz derm, which align in a crescent shape at approximately embryonic day character that lacks a heart (Bodmer, 1993). Tinman belongs to the 7.5 (E7.5) in the mouse embryo, roughly corresponding to week 2 of homeodomain family of proteins, and was initially described to play human gestation (Fig. 10–1). By mouse E8.0, or 3 weeks in humans, a role in establishing the regional identity of cells and organs during these cells coalesce along the ventral midline to form a primitive heart embryogenesis. tube that consists of an interior layer of endocardial cells and an exte- In contrast to the requirement of tinman for heart formation in * ies, rior layer of myocardial cells, separated by the extracellular matrix its mammalian ortholog, Nkx2.5, is not essential for speci( cation of the necessary for reciprocal signaling between the two layers. The tubular cardiac lineage in mice, suggesting either that other genes may share heart initiates rhythmic contractions at about day 23 in humans. functions with Nkx2.5 or that cardiogenesis in * ies and vertebrates dif- Previous lineage tracings using dye-labeling techniques suggested fers with respect to its dependence on this family of homeobox genes that cells along the anterior–posterior (AP) axis of the heart tube were (Lyons et al., 1995; Tanaka et al., 1999). The possibility of functional 124 110-Epstein-Chap10.indd0-Epstein-Chap10.indd 112424 88/21/2007/21/2007 88:35:16:35:16 PPMM Molecular Regulation of Cardiogenesis 125 miR1-1 miR1-2 h ht v a A B Figure 10–1. Illustration of cardiac development. Illustrations depict cardiac aortic arch arteries (III, IV, and VI) and aortic sac, which together contrib- development, with morphologically related regions color-coded, seen from a ute to speci( c segments of the mature aortic arch, also color-coded. (C, D) ventral view. (A) Two distinct cardiogenic precursor ( elds form a crescent Mesenchymal cells form the cardiac valves from the conotruncal (CT) and that is speci( ed to form speci( c regions of the heart tube (A, artery; V, ven- atrioventricular valve (AVV) segments, which divide into separate left- and tricle), which is patterned to form the various regions and chambers of the right-sided valves. Corresponding days of human embryonic development looped and mature heart. (B) The secondary heart ( eld (SHF) contributes are indicated. Ao, aorta; DA, ductus arteriosus; LA, left atrium; LCC, left to much of the right ventricle and out* ow tract as the heart loops. (C) Each common carotid; LSCA, left subclavian artery; LV, left ventricle; PA, pul- cardiac chamber balloons from the outer curvature of the looped heart tube monary artery; RA, right atrium; RCC, right common carotid; RSCA, right in a segmental fashion. Neural crest cells populate the bilaterally symmetric subclavian artery; RV, right ventricle. redundancy between Nkx2.5 and other cardiac-expressed homeobox outer curvature of the heart (Biben and Harvey, 1997; Thomas et al., genes in vertebrates is supported by the ability of dominant-negative 1998). Remodeling of the inner curvature occurs, allowing migration versions of Nkx2.5 to block cardiogenesis in frog and zebra( sh embryos of the in* ow tract to the right and out* ow tract to the left, facilitating (Fu et al., 1998; Grow and Krieg, 1998). Similarly, the transcriptional proper alignment and separation of right- and left-sided circulations. co-activator, myocardin, is necessary and suf( cient in frogs for cardiac Defects of inner curvature remodeling may underlie a host of human gene expression, likely through the activation of serum response fac- congenital heart malformations that involve improper alignment of the tor (SRF)-dependent genes (Wang et al., 2001; Small et al., 2005). atria, ventricles and out* ow tract, and are often observed in the setting Combinations of these transcription factors along with Mef2, Gata, of abnormalities of left–right (LR) asymmetry. Other cardiac defects Hand, and Tbx family members appear to form core regulatory circuits are a result of genetic defects that cause disruption of discrete devel- that control early events during cardiogenesis (reviewed in Srivastava opmental events, making it useful to consider the molecular processes et al., 2006).
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