Molecular Pathways and Animal Models of Ebstein's Anomaly.
AV canal
Alk2
Alk3
Atrioventricular canal
BMP
Bone morphogenetic protein
CTVM
Canine tricuspid valve malformation
Dogs
EPDCs
Ebstein’s anomaly
Endocardial cushion
Epicardial-derived cells
Fog2
GATA4
Hypoplastic left heart syndrome
Junctional myocardium
Knockout
Labradors
Left ventricular noncompaction
Mesenchyme
Mouse models
NKX2-5
PLD1
Posterior leaflet
Septal leaflet
TBX5
Transforming growth factor beta
Tricuspid valve
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2024
2024
Historique:
medline:
17
6
2024
pubmed:
17
6
2024
entrez:
17
6
2024
Statut:
ppublish
Résumé
Ebstein's anomaly is a congenital malformation of the tricuspid valve characterized by abnormal attachment of the valve leaflets, resulting in varying degrees of valve dysfunction. The anatomic hallmarks of this entity are the downward displacement of the attachment of the septal and posterior leaflets of the tricuspid valve. Additional intracardiac malformations are common. From an embryological point of view, the cavity of the future right atrium does not have a direct orifice connected to the developing right ventricle. This chapter provides an overview of current insight into how this connection is formed and how malformations of the tricuspid valve arise from dysregulation of molecular and morphological events involved in this process. Furthermore, mouse models that show features of Ebstein's anomaly and the naturally occurring model of canine tricuspid valve malformation are described and compared to the human model. Although Ebstein's anomaly remains one of the least understood cardiac malformations to date, the studies summarized here provide, in aggregate, evidence for monogenic and oligogenic factors driving pathogenesis.
Identifiants
pubmed: 38884760
doi: 10.1007/978-3-031-44087-8_58
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
915-928Informations de copyright
© 2024. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Schreiber C, Cook A, Ho SY, Augustin N, Anderson RH. Morphologic spectrum of Ebstein’s malformation: revisitation relative to surgical repair. J Thorac Cardiovasc Surg. 1999;117(1):148–55.
pubmed: 9869769
doi: 10.1016/S0022-5223(99)70480-0
Qureshi MY, O’Leary PW, Connolly HM. Cardiac imaging in Ebstein anomaly. Trends Cardiovasc Med. 2018;28(6):403–9.
pubmed: 29409687
doi: 10.1016/j.tcm.2018.01.002
Possner M, Gensini FJ, Mauchley DC, Krieger EV, Steinberg ZL. Ebstein’s anomaly of the tricuspid valve: an overview of pathology and management. Curr Cardiol Rep. 2020;22(12):157.
pubmed: 33037480
doi: 10.1007/s11886-020-01412-z
Leung MP, Baker EJ, Anderson RH, Zuberbuhler JR. Cineangiographic spectrum of Ebstein’s malformation: its relevance to clinical presentation and outcome. J Am Coll Cardiol. 1988;11(1):154–61.
pubmed: 3335691
doi: 10.1016/0735-1097(88)90182-9
Rusconi PG, Zuberbuhler JR, Anderson RH, Rigby ML. Morphologic-echocardiographic correlates of Ebstein’s malformation. Eur Heart J. 1991;12(7):784–90.
pubmed: 1889443
Zuberbuhler JR, Allwork SP, Anderson RH. The spectrum of Ebstein’s anomaly of the tricuspid valve. J Thorac Cardiovasc Surg. 1979;77(2):202–11.
pubmed: 762960
doi: 10.1016/S0022-5223(19)40958-6
Sanchez-Quintana D, Cabrera JA, Picazo-Angelin B, Cabrera A, Anderson RH. Histological examination of the potential arrhythmic substrates in the setting of Ebstein’s malformation. J Anat. 2020;237(1):155–65.
pubmed: 32115720
pmcid: 7309280
doi: 10.1111/joa.13179
Petersen SE, Jensen B, Aung N, Friedrich MG, McMahon CJ, Mohiddin SA, Pignatelli RH, Ricci F, Anderson RH Bluemke DA. Excessive trabeculation of the left ventricle: JACC: cardiovascular imaging expert panel paper. Cardiovascular Imaging. 2023;16(3):408–425.
pubmed: 36764891
Attenhofer Jost CH, Connolly HM, O’Leary PW, Warnes CA, Tajik AJ, Seward JB. Left heart lesions in patients with Ebstein anomaly. Mayo Clin Proc. 2005;80(3):361–8.
pubmed: 15757018
doi: 10.4065/80.3.361
Attenhofer Jost CH, Connolly HM, Warnes CA, O’Leary P, Tajik AJ, Pellikka PA, et al. Noncompacted myocardium in ebstein’s anomaly: initial description in three patients. J Am Soc Echocardiogr. 2004;17(6):677–80.
pubmed: 15163943
doi: 10.1016/j.echo.2004.02.013
Castaneda-Zuniga W, Nath HP, Moller JH, Edwards JE. Left-sided anomalies in Ebstein’s malformation of the tricuspid valve. Pediatr Cardiol. 1982;3(2):181–5.
pubmed: 7155954
doi: 10.1007/BF02312967
Daliento L, Angelini A, Ho SY, Frescura C, Turrini P, Baratella MC, et al. Angiographic and morphologic features of the left ventricle in Ebstein’s malformation. Am J Cardiol. 1997;80(8):1051–9.
pubmed: 9352977
doi: 10.1016/S0002-9149(97)00602-4
Gerlis LM, Ho SY, Sweeney AE. Mitral valve anomalies associated with Ebstein’s malformation of the tricuspid valve. Am J Cardiovasc Pathol. 1993;4(4):294–301.
pubmed: 8305192
Monibi AA, Neches WH, Lenox CC, Park SC, Mathews RA, Zuberbuhler JR. Left ventricular anomalies associated with Ebstein’s malformation of the tricuspid valve. Circulation. 1978;57(2):303–6.
pubmed: 145329
doi: 10.1161/01.CIR.57.2.303
Stähli BE, Gebhard C, Biaggi P, Klaassen S, Valsangiacomo Buechel E, Attenhofer Jost CH, et al. Left ventricular non-compaction: prevalence in congenital heart disease. Int J Cardiol. 2013;167(6):2477–81.
pubmed: 22704867
doi: 10.1016/j.ijcard.2012.05.095
van Engelen K, Postma AV, van de Meerakker JBA, Roos-Hesselink JW, Helderman-van den Enden ATJM, Vliegen HW, et al. Ebstein’s anomaly may be caused by mutations in the sarcomere protein gene MYH7. Neth Hear J. 2013;21(3):113–7.
doi: 10.1007/s12471-011-0141-1
Reyes A, 2nd, Bove EL, Mosca RS, Kulik TJ, Ludomirsky A. Tricuspid valve repair in children with hypoplastic left heart syndrome during staged surgical reconstruction. Circulation. 1997;96(9 Suppl):II-341–3; discussion II-4-5
Stamm C. The morphologically tricuspid valve in hypoplastic left heart syndrome. Eur J Cardiothorac Surg. 1997;12(4):587–92.
pubmed: 9370403
doi: 10.1016/S1010-7940(97)00184-X
Lamers WH, Virágh S, Wessels A, Moorman AFM, Anderson RH. Formation of the tricuspid valve in the human heart. Circulation. 1995;91(1):111–21.
pubmed: 7805192
doi: 10.1161/01.CIR.91.1.111
Lincoln J, Alfieri CM, Yutzey KE. Development of heart valve leaflets and supporting apparatus in chicken and mouse embryos. Dev Dyn. 2004;230(2):239–50.
pubmed: 15162503
doi: 10.1002/dvdy.20051
Armstrong EJ, Bischoff J. Heart valve development: endothelial cell signaling and differentiation. Circ Res. 2004;95(5):459–70.
pubmed: 15345668
pmcid: 2810618
doi: 10.1161/01.RES.0000141146.95728.da
Bressan M, Yang PB, Louie JD, Navetta AM, Garriock RJ, Mikawa T. Reciprocal myocardial-endocardial interactions pattern the delay in atrioventricular junction conduction. Development. 2014;141(21):4149–57.
pubmed: 25273084
pmcid: 4302900
doi: 10.1242/dev.110007
de Lange FJ, Moorman AFM, Anderson RH, Männer J, Soufan AT, Vries CG-d, et al. Lineage and morphogenetic analysis of the cardiac valves. Circ Res. 2004;95(6):645–54.
pubmed: 15297379
doi: 10.1161/01.RES.0000141429.13560.cb
Kanani M, Moorman AFM, Cook AC, Webb S, Brown NA, Lamers WH, et al. Development of the atrioventricular valves: clinicomorphological correlations. Ann Thorac Surg. 2005;79(5):1797–804.
pubmed: 15854992
doi: 10.1016/j.athoracsur.2004.06.122
Wessels A, Markman MWM, Vermeulen JLM, Anderson RH, Moorman AFM, Lamers WH. The development of the atrioventricular junction in the human heart. Circ Res. 1996;78(1):110–7.
pubmed: 8603493
doi: 10.1161/01.RES.78.1.110
Wessels A, Vermeulen JLM, Virágh SZ, Kálmán F, Morris GE, Man NT, et al. Spatial distribution of “tissue-specific” antigens in the developing human heart and skeletal muscle. I. An immunohistochemical analysis of creatine kinase isoenzyme expression patterns: CK ISOENZYMES IN HUMAN MUSCLE. Anat Rec. 1990;228(2):163–76.
pubmed: 2240609
doi: 10.1002/ar.1092280208
Faber JW, Hagoort J, Moorman AFM, Christoffels VM, Jensen B. Quantified growth of the human embryonic heart. Biol Open. 2021;10(2)
Sizarov A, Devalla HD, Anderson RH, Passier R, Christoffels VM, Moorman AF. Molecular analysis of patterning of conduction tissues in the developing human heart. Circ Arrhythm Electrophysiol. 2011;4(4):532–42.
pubmed: 21576278
doi: 10.1161/CIRCEP.111.963421
Wessels A, van den Hoff MJB, Adamo RF, Phelps AL, Lockhart MM, Sauls K, et al. Epicardially derived fibroblasts preferentially contribute to the parietal leaflets of the atrioventricular valves in the murine heart. Dev Biol. 2012;366(2):111–24.
pubmed: 22546693
pmcid: 3358438
doi: 10.1016/j.ydbio.2012.04.020
Dettman RW, Denetclaw W, Ordahl CP, Bristow J. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and Intermyocardial fibroblasts in the avian heart. Dev Biol. 1998;193(2):169–81.
pubmed: 9473322
doi: 10.1006/dbio.1997.8801
Gittenberger-de Groot AC, Vrancken Peeters M-PFM, Mentink MMT, Gourdie RG, Poelmann RE. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res. 1998;82(10):1043–52.
pubmed: 9622157
doi: 10.1161/01.RES.82.10.1043
Wessels A, Pérez-Pomares JM. The epicardium and epicardially derived cells (EPDCs) as cardiac stem cells: epicardially derived cells as cardiac stem cells. Anat Rec A: Discov Mol Cell Evol Biol. 2004;276A(1):43–57.
doi: 10.1002/ar.a.10129
Zhou B, von Gise A, Ma Q, Hu YW, Pu WT. Genetic fate mapping demonstrates contribution of epicardium-derived cells to the annulus fibrosis of the mammalian heart. Dev Biol. 2010;338(2):251–61.
pubmed: 20025864
doi: 10.1016/j.ydbio.2009.12.007
Rajagopal SK, Ma Q, Obler D, Shen J, Manichaikul A, Tomita-Mitchell A, et al. Spectrum of heart disease associated with murine and human GATA4 mutation. J Mol Cell Cardiol. 2007;43(6):677–85.
pubmed: 17643447
pmcid: 2573470
doi: 10.1016/j.yjmcc.2007.06.004
Flagg AE, Earley JU, Svensson EC. FOG-2 attenuates endothelial-to-mesenchymal transformation in the endocardial cushions of the developing heart. Dev Biol. 2007;304(1):308–16.
pubmed: 17274974
doi: 10.1016/j.ydbio.2006.12.035
Svensson EC, Huggins GS, Lin H, Clendenin C, Jiang F, Tufts R, et al. A syndrome of tricuspid atresia in mice with a targeted mutation of the gene encoding Fog-2. Nat Genet. 2000;25(3):353–6.
pubmed: 10888889
doi: 10.1038/77146
Lahrouchi N, Postma AV, Salazar CM, De Laughter DM, Tjong F, Piherova L, et al. Biallelic loss-of-function variants in PLD1 cause congenital right-sided cardiac valve defects and neonatal cardiomyopathy. J Clin Invest. 2021;131(5)
Ta-Shma A, Zhang K, Salimova E, Zernecke A, Sieiro-Mosti D, Stegner D, et al. Congenital valvular defects associated with deleterious mutations in the PLD1 gene. J Med Genet. 2017;54(4):278–86.
pubmed: 27799408
doi: 10.1136/jmedgenet-2016-104259
Ashraf H, Pradhan L, Chang EI, Terada R, Ryan NJ, Briggs LE, et al. A mouse model of human congenital heart disease: high incidence of diverse cardiac anomalies and ventricular noncompaction produced by heterozygous Nkx2-5 homeodomain missense mutation. Circ Cardiovasc Genet. 2014;7(4):423–33.
pubmed: 25028484
pmcid: 4140955
doi: 10.1161/CIRCGENETICS.113.000281
Kasahara H. Biochemical analyses of eight NKX2.5 homeodomain missense mutations causing atrioventricular block and cardiac anomalies. Cardiovasc Res. 2004;64(1):40–51.
pubmed: 15364612
doi: 10.1016/j.cardiores.2004.06.004
Choquet C, Nguyen THM, Sicard P, Buttigieg E, Tran TT, Kober F, et al. Deletion of Nkx2-5 in trabecular myocardium reveals the developmental origins of pathological heterogeneity associated with ventricular non-compaction cardiomyopathy. PLoS Genet. 2018;14(7):e1007502.
pubmed: 29979676
pmcid: 6051668
doi: 10.1371/journal.pgen.1007502
Wilsbacher L, McNally EM. Genetics of cardiac developmental disorders: cardiomyocyte proliferation and growth and relevance to heart failure. Annu Rev Pathol. 2016;11:395–419.
pubmed: 26925501
pmcid: 8978617
doi: 10.1146/annurev-pathol-012615-044336
Winston JB, Erlich JM, Green CA, Aluko A, Kaiser KA, Takematsu M, et al. Heterogeneity of genetic modifiers ensures normal cardiac development. Circulation. 2010;121(11):1313–21.
pubmed: 20212279
pmcid: 2953850
doi: 10.1161/CIRCULATIONAHA.109.887687
Winston JB, Schulkey CE, Chen I-BD, Regmi SD, Efimova M, Erlich JM, et al. Complex trait analysis of ventricular septal defects caused by Nkx2-5 mutation. Circulation. 2012;5(3):293–300.
pubmed: 22534315
Gaussin V, Morley GE, Cox L, Zwijsen A, Vance KM, Emile L, et al. Alk3/Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus Fibrosus. Circ Res. 2005;97(3):219–26.
pubmed: 16037571
pmcid: 2950023
doi: 10.1161/01.RES.0000177862.85474.63
Lyons KM, Pelton RW, Hogan BL. Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development. 1990;109(4):833–44.
pubmed: 2226202
doi: 10.1242/dev.109.4.833
Roelen BA, Goumans MJ, van Rooijen MA, Mummery CL. Differential expression of BMP receptors in early mouse development. Int J Dev Biol. 1997;41(4):541–9.
pubmed: 9303341
Kruithof BPT, Kruithof-De-Julio M, Poelmann RE, Gittenberger-De-Groot AC, Gaussin V, Goumans M-J. Remodeling of the myocardium in early trabeculation and cardiac valve formation; a role for TGFβ2. Int J Dev Biol. 2013;57(11–12):853–63.
pubmed: 24623077
doi: 10.1387/ijdb.130302bk
Cai X, Nomura-Kitabayashi A, Cai W, Yan J, Christoffels VM, Cai C-L. Myocardial Tbx20 regulates early atrioventricular canal formation and endocardial epithelial–mesenchymal transition via Bmp2. Dev Biol. 2011;360(2):381–90.
pubmed: 21983003
pmcid: 3217163
doi: 10.1016/j.ydbio.2011.09.023
Aanhaanen WT, Boukens BJ, Sizarov A, Wakker V, de Gier-de Vries C, van Ginneken AC, et al. Defective Tbx2-dependent patterning of the atrioventricular canal myocardium causes accessory pathway formation in mice. J Clin Invest. 2011;121(2):534–44.
pubmed: 21266775
pmcid: 3026729
doi: 10.1172/JCI44350
Rentschler S, Harris BS, Kuznekoff L, Jain R, Manderfield L, Lu MM, et al. Notch signaling regulates murine atrioventricular conduction and the formation of accessory pathways. J Clin Invest. 2011;121(2):525–33.
pubmed: 21266778
pmcid: 3026731
doi: 10.1172/JCI44470
Bonyadi M, Rusholme SAB, Cousins FM, Su HC, Biron CA, Farrall M, et al. Mapping of a major genetic modifier of embryonic lethality in TGFβ1 knockout mice. Nat Genet. 1997;15(2):207–11.
pubmed: 9020852
doi: 10.1038/ng0297-207
Michaëlsson M, Ho S. World Scientific Publishing Company; 2000.
Chetboul V, Tran D, Carlos C, Tessier D, Pouchelon JL. Les malformations congénitales de la valve tricuspide chez les carnivores domestiques: étude rétrospective de 50 cas: Kongenitale Missbildungen der Trikuspidalklappe bei domestizierten Karnivoren: Retrospektive Studie von 50 Fällen. Schweiz Arch Tierheilkd. 2004;146(6):265–75.
pubmed: 15248346
doi: 10.1024/0036-7281.146.6.265
Eyster GE, Anderson L, Evans AT, Chaffee A, Bender G, Johnston J, et al. Ebstein’s anomaly: a report of 3 cases in the dog. J Am Vet Med Assoc. 1977;170(7):709–13.
pubmed: 858686
Hoffmann G, Amberger CN, Seiler G, Lombard CW. Tricuspid valve dysplasia in fifteen dogs. Schweiz Arch Tierheilkd. 2000;142(5):268–77.
pubmed: 10850163
Kornreich BG, Moïse NS. Right atrioventricular valve malformation in dogs and cats: an electrocardiographic survey with emphasis on splintered QRS complexes. J Vet Intern Med. 1997;11(4):226–30.
pubmed: 9298477
doi: 10.1111/j.1939-1676.1997.tb00095.x
Liu N, Schoch K, Luo X, Pena LDM, Bhavana VH, Kukolich MK, et al. Functional variants in TBX2 are associated with a syndromic cardiovascular and skeletal developmental disorder. Hum Mol Genet. 2018;27(14):2454–65.
pubmed: 29726930
pmcid: 6030957
doi: 10.1093/hmg/ddy146
Famula TR, Siemens LM, Davidson AP, Packard M. Evaluation of the genetic basis of tricuspid valve dysplasia in Labrador retrievers. Am J Vet Res. 2002;63(6):816–20.
pubmed: 12061526
doi: 10.2460/ajvr.2002.63.816
Ohad DG, Avrahami A, Waner T, David L. The occurrence and suspected mode of inheritance of congenital subaortic stenosis and tricuspid valve dysplasia in Dogue de Bordeaux dogs. Vet J. 2013;197(2):351–7.
pubmed: 23434219
doi: 10.1016/j.tvjl.2013.01.012
Adin D. Tricuspid valve dysplasia. St. Louis: Saunders Elsevier; 2008.
Wright K. Tricuspid valve dysplasia. St. Louis: Mosby Elsevier; 2011.
Andelfinger G, Wright KN, Lee HS, Siemens LM, Benson DW. Canine tricuspid valve malformation, a model of human Ebstein anomaly, maps to dog chromosome 9. J Med Genet. 2003;40(5):320–4.
pubmed: 12746392
pmcid: 1735483
doi: 10.1136/jmg.40.5.320
Andelfinger G, Etter L, Dyment M, Hitte C, Galibert F, Kirkness E, et al. Radiation hybrid mapping and genomic organization of canine TBX2 and TBX4: brief notes. Anim Genet. 2003;34(4):307–9.
pubmed: 12873224
doi: 10.1046/j.1365-2052.2003.01018.x
Andelfinger G, Hitte C, Etter L, Guyon R, Bourque G, Tesler G, et al. Detailed four-way comparative mapping and gene order analysis of the canine ctvm locus reveals evolutionary chromosome rearrangements. Genomics. 2004;83(6):1053–62.
pubmed: 15177558
doi: 10.1016/j.ygeno.2003.12.009
Singh R, Hoogaars WM, Barnett P, Grieskamp T, Rana MS, Buermans H, et al. Tbx2 and Tbx3 induce atrioventricular myocardial development and endocardial cushion formation. Cell Mol Life Sci. 2012;69(8):1377–89.
pubmed: 22130515
doi: 10.1007/s00018-011-0884-2
Asimaki A, Syrris P, Wichter T, Matthias P, Saffitz JE, McKenna WJ. A novel dominant mutation in plakoglobin causes arrhythmogenic right ventricular cardiomyopathy. Am J Hum Genet. 2007;81(5):964–73.
pubmed: 17924338
pmcid: 2265660
doi: 10.1086/521633
Werner P, Raducha MG, Prociuk U, Ostrander EA, Spielman RS, Kirkness EF, et al. The keeshond defect in cardiac conotruncal development is oligogenic1. Hum Genet. 2005;116(5):368–77.
pubmed: 15711798
doi: 10.1007/s00439-004-1242-3