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Andersons pediatric cardiology 108

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Single Gene Defects In the last few decades, human genetic studies have identified several genes that are mutated in those with inherited cardiac disease All of these are important regulators of cardiac morphogenesis, supporting the concept that the cardiac malformations are primarily a disease of abnormal embryonic organogenesis These findings have also cemented the notion that most lesions have a genetic origin In addition, these discoveries have clearly demonstrated that unrelated lesions can be caused by the same genetic defect, resulting in a need to reexamine epidemiologic studies from a different perspective In all cases, the mutations are autosomal dominant, as they affect only one of two alleles of the gene As yet, it is not fully known how dominant mutations in these genes result in profound aberrations in formation of the heart However, most are likely related to decreased dosage, while some mutations lead to gain of function effects It is of paramount importance to understand the molecular consequences of disease-causing mutations, and the mechanism underlying these events, in order to be able to design in rational fashion nonsurgical therapeutic interventions for those with congenitally malformed hearts The future of our understanding of the etiology of the lesions therefore lies in understanding how mutations in these important regulators lead to altered morphogenesis A few lessons from select mutations are described below Syndromic Mutations Mutations of TBX5 in Holt-Oram Syndrome Some genetic mutations have been identified in rare syndromes that include congenital cardiac malformations For example, mutations in TBX5 cause defects in the context of Holt-Oram syndrome.61–63 These defects are predominantly interatrial communications, usually within the oval fossa, muscular ventricular septal defects, and abnormalities of the conduction system, but mutations can also result in more diverse abnormalities, such as hypoplastic left heart syndrome, totally anomalous pulmonary venous connection, and common atrioventricular junction (Fig 4.1) The syndrome also includes defects in limb formation, specifically of the radial ray, the thumb, first digit, and radius Most defects of the limbs involve the thumbs, and range in severity from mild triphalangeal thumbs, up to complete phocomelia, with defects of intermediate severity such as missing thumbs, and hypoplastic radius FIG 4.1 Tbx5 expression and congenital heart defects in Holt-Oram syndrome (A) In situ hybridization of Tbx5 (red signal) in an E13.5 mouse embryo, with expression in the left and right atria (LA, ra), left ventricle (lv), and left side of the interventricular septum, and right ventricular (RV) trabeculae (B) Diagrammatic representation of Tbx5 expression in a mature heart and the location and type of congenital heart defects found in Holt-Oram syndrome patients Numbers in parentheses represent numbers of reported cases AA, Aortic atresia; ASD, atrial septal defect; CSD, conduction system defects; DORV, double-outlet right ventricle; ECD, endocardial cushion defect; HLH, hypoplastic left heart; MVP, mitral valve prolapse; PAA, pulmonary artery atresia; PDA, patent arterial duct; PLSVC, persistent left superior vena cava; TA, tricuspid atresia; TAPVR, total anomalous pulmonary venous return; TOF, tetralogy of Fallot; TRA, truncus arteriosus; TRAB, trabecular anomalies; VSD, ventricular septal defects (Modified from Bruneau BG The developing heart and congenital heart defects: a make or break situation Clin Genet 2003;63:252–261; and Bruneau BG, Logan M, Davis N, et al Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome Dev Biol 1999;211:100–108.) Mutations have been found throughout the TBX5 gene,63 although they predominantly cluster in the so-called “T-box” domain, which confers DNAbinding capabilities on the protein Early studies supported the concept of genotype-phenotype correlation, whereby mutations in one part of the gene were predominantly associated with families with severe cardiac defects, while mutations in a different part of the gene were found in families that had a predominance of severe limb, but not cardiac, defects.64 Subsequent findings, however, discounted this hypothesis It is now believed that the difference in manifestation of disease is more likely a result of genetic background.63,65,66 The observation by clinical geneticists that limb anomalies often coincide with cardiac defects have led some investigators to investigate TBX5 mutations for several related disorders This often does not yield positive correlations Recent work has strived to define the clinical criterion for the Holt-Oram syndrome in relation to the presence of TBX5 mutations Indeed, there is excellent concordance, as long as a strict definition is maintained for the components of the syndrome.67 Modelling of Holt-Oram syndrome in the mouse has revealed interesting and important features of the consequences of haploinsufficiency on downstream target gene regulation.68–70 In particular, it is clear that some genes in the heart are exquisitely sensitive to the dosage of Tbx5, explaining the occasional severity of defects in mice or humans with reduced dosage of this gene Some genes, such as the gap junction protein-encoding gene Gja5, also known as connexin 40, are targets that may explain some aspects of Holt-Oram syndrome, such as, in this case, the atrioventricular block In other cases, investigation of the mouse model has led to the intriguing observation that independent of structural lesions one can identify clear defects in diastolic function due to reduced Tbx5 activity These functional deficits are directly due to reduced function of the calcium pump, related to reduced activity of the Serca2a gene, which is directly regulated by Tbx5.70 These results, observed in the mouse, correlate to human patients with Holt-Oram syndrome, indicating that specific defects in cardiac function can accompany structural lesions while being unrelated to them except for their underlying genetic cause.70 Mutations of SALL4 in Okihiro Syndrome Mutations in the Spalt gene SALL4 have been found to underlie Okihiro syndrome, which, as with Holt-Oram syndrome, affects the limbs as well as the heart, although it also has a broad spectrum of ocular, renal, and other defects.66,71–75 The two syndromes are sometimes confused clinically due to very similar defects involving the heart and limbs, but molecular genetic studies have clearly outlined the distinction between the two.66 Using mouse models, it has been shown that Sall4 and Tbx5 genetically and physically interact to pattern the heart and limbs,76 thus explaining the reason for the similarities in

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