Abstract
Outflow tract abnormalities are the most frequent congenital heart defects. These are due to the absence or dysfunction of the two main cell types, i.e., neural crest cells and secondary heart field cells that migrate in opposite directions at the same stage of development. These cells directly govern aortic arch patterning and development, ascending aorta dilatation, semi-valvular and coronary artery development, aortopulmonary septation abnormalities, persistence of the ductus arteriosus, trunk and proximal pulmonary arteries, sub-valvular conal ventricular septal/rotational defects, and non-compaction of the left ventricle. In some cases, depending on the functional defects of these cells, additional malformations are found in the expected spatial migratory area of the cells, namely in the pharyngeal arch derivatives and cervico-facial structures. Associated non-cardiovascular anomalies are often underestimated, since the multipotency and functional alteration of these cells can result in the modification of multiple neural, epidermal, and cervical structures at different levels. In most cases, patients do not display the full phenotype of abnormalities, but congenital cardiac defects involving the ventricular outflow tract, ascending aorta, aortic arch and supra-aortic trunks should be considered as markers for possible impaired function of these cells. Neural crest cells should not be considered as a unique cell population but on the basis of their cervical rhombomere origins R3-R5 or R6-R7-R8 and specific migration patterns: R3-R4 towards arch II, R5-R6 arch III and R7-R8 arch IV and VI. A better understanding of their development may lead to the discovery of unknown associated abnormalities, thereby enabling potential improvements to be made to the therapeutic approach.
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Source: original figure). Left posterolateral view of human developing embryo at embryonic day 29, corresponding to Carnegie stage CS11. Migration of neural crest cells in humans occurs from the neural crest to the cardiovascular structure, between Carnegie stages 10–13 for a 4-week period. At this time, the brain (in blue) is composed of 3 continuous structures: prosencephalon (Forebrain—PE), mesencephalon (Midbrain—ME), rhombencephalon (Hindbrain—RE). The neural crest (in green) comprises two longitudinal structures that develop bilaterally on the dorsal-lateral part of all neural structures at day 25 (CS9). Cardiac neural crests are derived from cervical neural crest cells that are located between the cranial neural crest cells and the trunk neural crest cells. The majority of NCCc come from R6-R7-R8 with a spatial postotic vesicle (OV) migration: NCCc from R6 through arch III, NCCc from R7 and R8 through arch IV and then through VI when developed. Recent studies have shown that NCC from more proximal rhombomers R3 and R4 (i.e., with preotic vesicle migration) migrate through arches II towards the heart. NCC from R5 have a specific intracrest migration to R4 and R6 and become NCCc at respective rhombomeres. RV right ventricle, LV left ventricle, BC Bulbus cordis, PA1-4 pharyngeal arch 1–4, OV otic vesicle
Source: Figure from Simoes-Costa (Simoes-Costa et al. 2014)]. Neural crest cells are generated in the ectodermal germ layer during gastrulation and initially reside in two neural plate border territories, which are located at the two lateral edges of the central nervous system in contact with the ectodermal epidermis (a). During neurulation, these border territories approach one another along the dorsal line (b) when the neural plate closes to form the neural tube (c). After neural tube closure, the NCC leave the central nervous system (i.e., delamination) via an epithelial to mesenchymal transition (EMT) that is accompanied by an alteration of cell contact with neural plate cells and enhanced migration capability (d)
Source: Figure adapted from M. Simoes-Costa (Simoes-Costa et al. 2014) and D. Meulenans (Meulemans and Bronner-Fraser 2004)] giving special consideration to cardiac Neural crest cells (NCCc). The initiation of neural crest genes in the lateral part of neural plate cells is induced by the presence of high levels of FGF and NOTCH and intermediate levels of BMP and Wnt signaling. The FGF and Wnt are secreted by lateral structures [i.e., epidermis (gray box)] and induce epidermal differentiation, while their inhibitors are secreted by medial structures such as the neural plate (blue box). The intermediate gradient of BMP and Wnt between neural cells and epidermal cells may explain the appearance of neural crest cells (green box). In the non-neural ectoderm, a high level of BMP activates the epidermal program. During neural crest induction, there is firstly the amplification of a set of transcription factors that initiate and maintain the neural plate border zone. These are referred to as neural plate border specifier transcription factors (b). The activation of this module of transcription factors leads to the activation of a new set of transcription factors (i.e., the neural crest specifier module) (c) that further determines the unique capabilities of these cells while maintaining their multipotency and characteristics of the neural crest. Activation of the neural crest specifier module leads to activation of Epithelial-Mesenchymal-Transdifferentiation (EMT) that is crucial for cell delamination and acquisition of mesenchymal phenotype. The neural crest specifier module also activates a new set of transcription factors (i.e., Neural crest migration specifiers) that is necessary for cell migration and maintenance of multipotency during migration (d). Ets1 and Sox9 (yellow star) are crucial regulators of the migratory module of the cranial neural crest for the establishment of cranial crest cephalic identity and for mediating mass delamination from the neural tube resulting in the wave-like migration pattern. The expression of neural specifier genes such as FoxD3, Ets1 and Sox9/10 is maintained in all migrating NCCc. Furthermore, there is a positive loop for Sox, especially Sox9, in migrating NCCc. Cardiac neural stem cell multipotency is already determined at the time of cell “egression” from the neural tube
Source: original figure). Anteroposterior crosssection through developing right ventricle/bulbus cordis/aortic sac at human embryonic day 32 (CS14). (A1) Enlargement view. Cardiac neural crest cells (in green) are attracted to the right ventricle outflow tract by SHCc that are initially present at this location (blue) and that will pattern all outflow track development. In chicken, and possibly mice, R8 (and possibly R7) anomalies are associated with aortopulmonary septation. This observation needs confirmation in humans. The NCCc migrate through the newly developed right and left arches of VI, which fuse on the midline to form the pulmonary trunk and participate in aortopulmonary septation. The direction of migration of NCCc in the outflow track is determined by a direct physical interaction with the posterior mesodermal flow divider (PMFD), which is a mesodermal structure that develops in the wall of the posterior part of the proximal developing right ventricle. The posterior migrating contingent of secondary heart field cells (blue arrow 2) provides an important cellular component for this structure as well as the valvular intercalated cushions (ICC). The interaction of PMFD has two main effects on the migration of cardiac neural crest cells: 1) by dividing and directing their flow towards the anterior and posterior conotruncal cushions (CTC), thus enabling their fusion, 2) by provoking a 90° rotation of the outflow tract (purple arrow). This rotation helps in the closure of the sub-valvular conal aortopulmonary septum, by narrowing the ventricle part of the conotruncal cushions, and in the fusion with the developing atrioventricular cushion. PMFD posterior mesodermal neural crest cell flow divider, VI-R or VI-L right or left VI arterial arches, RV right ventricle, LV left ventricle, migration of secondary heart field cells: (1) anterior or (2) posterior, CTC conotruncal cushions (ant/post), ICC intercalated cardiac cushions (right/left)
Source: original figure). Cross-section at level of endocardial cushions in the outflow tract at human embryonic day 32. The aortic (AV) and pulmonary (PV) valves develop from embryonic days 26–41 from 4 cushions: two lateral intercalated cushions (ICC) (yellow) with local restricted development in the outflow tract, and two anterior and posterior conotruncal cushions (CTC) s(brown). The endothelium monolayer covering the endoluminal surface of the outflow track is represented by a continuous green line. CTC are derived from local transdifferentiation of endothelial to mesenchymal differentiation, while ICC are mesodermal structure derivatives with an additional important contingent coming from secondary heart field cells (yellow circles). Migration of NCCc (green circles) provokes the fusion of anterior and posterior CTC on the midline, which is then followed by fusion between different formations on each side (large blue arrows). Then the partition and maturation of the valve occurs to form fine, stratified and mature tricuspid aortic and pulmonary valves. In chicken, arterial outflow tract valves are derived from cells originating from rhombomeres R6, R7 and R8 (Etchevers et al. 2001). Absence of fusion will give rise to a persistent arterial trunk, which is the genetic abnormality most commonly related to neural crest ablation abnormalities. Preotic NCCc (green rectangles) from R3-R4, as described in quail and mice, have a predominant distribution for CTC cushions, the coronaries, conotruncal and septal regions. ICC-R/ICC-L right or left intercalated cushion, CTC-ant/post: medial conotruncal cushion anterior or posterior, AV future tricuspid aortic valve, PV future tricuspid pulmonary valve
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References
Abdul-Wajid S, Demarest BL, Yost HJ (2018) Loss of embryonic neural crest derived cardiomyocytes causes adult onset hypertrophic cardiomyopathy in zebrafish. Nat Commun 9(1):4603. https://doi.org/10.1038/s41467-018-07054-8
Agarwal A, Khandheria BK, Paterick TE, Treiber SC, Bush M, Tajik AJ (2013) Left ventricular noncompaction in patients with bicuspid aortic valve. J Am Soc Echocardiogr 26(11):1306–1313. https://doi.org/10.1016/j.echo.2013.08.003
Aggarwal VS, Morrow BE (2008) Genetic modifiers of the physical malformations in velo-cardio-facial syndrome/DiGeorge syndrome. Dev Disabil Res Rev 14(1):19–25. https://doi.org/10.1002/ddrr.4
Anderson RH (2016) Rotation of the ventricular outflow tracts. Eur J Cardiothorac Surg 50(3):585. https://doi.org/10.1093/ejcts/ezw088
Anderson RH, Mori S, Spicer DE, Brown NA, Mohun TJ (2016) Development and morphology of the ventricular outflow tracts. World J Pediatr Congenit Heart Surg 7(5):561–577. https://doi.org/10.1177/2150135116651114
Anderson RH, Chaudhry B, Mohun TJ, Bamforth SD, Hoyland D, Phillips HM, Webb S, Moorman AF, Brown NA, Henderson DJ (2012) Normal and abnormal development of the intrapericardial arterial trunks in humans and mice. Cardiovasc Res 95(1):108–115. https://doi.org/10.1093/cvr/cvs147
Aoto K, Sandell LL, Butler Tjaden NE, Yuen KC, Watt KE, Black BL, Durnin M, Trainor PA (2015) Mef2c-F10N enhancer driven beta-galactosidase (LacZ) and Cre recombinase mice facilitate analyses of gene function and lineage fate in neural crest cells. Dev Biol 402(1):3–16. https://doi.org/10.1016/j.ydbio.2015.02.022
Arima Y, Miyagawa-Tomita S, Maeda K, Asai R, Seya D, Minoux M, Rijli FM, Nishiyama K, Kim KS, Uchijima Y, Ogawa H, Kurihara Y, Kurihara H (2012) Preotic neural crest cells contribute to coronary artery smooth muscle involving endothelin signalling. Nat Commun 3:1267. https://doi.org/10.1038/ncomms2258
Baardman ME, Zwier MV, Wisse LJ, Gittenberger-de Groot AC, Kerstjens-Frederikse WS, Hofstra RM, Jurdzinski A, Hierck BP, Jongbloed MR, Berger RM, Plosch T, DeRuiter MC (2016) Common arterial trunk and ventricular non-compaction in Lrp2 knockout mice indicate a crucial role of LRP2 in cardiac development. Dis Model Mech 9(4):413–425. https://doi.org/10.1242/dmm.022053
Bajolle F, Zaffran S, Meilhac SM, Dandonneau M, Chang T, Kelly RG, Buckingham ME (2008) Myocardium at the base of the aorta and pulmonary trunk is prefigured in the outflow tract of the heart and in subdomains of the second heart field. Dev Biol 313(1):25–34. https://doi.org/10.1016/j.ydbio.2007.09.023
Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, Helms J, Chang CP, Zhao Y, Swigut T, Wysocka J (2010) CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463(7283):958–962. https://doi.org/10.1038/nature08733
Bergman JE, Janssen N, van der Sloot AM, de Walle HE, Schoots J, Rendtorff ND, Tranebjaerg L, Hoefsloot LH, van Ravenswaaij-Arts CM, Hofstra RM (2012) A novel classification system to predict the pathogenic effects of CHD7 missense variants in CHARGE syndrome. Hum Mutat 33(8):1251–1260. https://doi.org/10.1002/humu.22106
Bergwerff M, Verberne ME, DeRuiter MC, Poelmann RE, Gittenberger-de Groot AC (1998) Neural crest cell contribution to the developing circulatory system: implications for vascular morphology? Circ Res 82(2):221–231. https://doi.org/10.1161/01.res.82.2.221
Betancur P, Bronner-Fraser M, Sauka-Spengler T (2010) Genomic code for Sox10 activation reveals a key regulatory enhancer for cranial neural crest. Proc Natl Acad Sci USA 107(8):3570–3575. https://doi.org/10.1073/pnas.0906596107
Brickner ME, Hillis LD, Lange RA (2000) Congenital heart disease in adults. Second of two parts. N Engl J Med 342(5):334–342. https://doi.org/10.1056/NEJM200002033420507
Brown CB, Feiner L, Lu MM, Li J, Ma X, Webber AL, Jia L, Raper JA, Epstein JA (2001) PlexinA2 and semaphorin signaling during cardiac neural crest development. Development 128(16):3071–3080
Byrd NA, Meyers EN (2005) Loss of Gbx2 results in neural crest cell patterning and pharyngeal arch artery defects in the mouse embryo. Dev Biol 284(1):233–245. https://doi.org/10.1016/j.ydbio.2005.05.023
Calmont A, Ivins S, Van Bueren KL, Papangeli I, Kyriakopoulou V, Andrews WD, Martin JF, Moon AM, Illingworth EA, Basson MA, Scambler PJ (2009) Tbx1 controls cardiac neural crest cell migration during arch artery development by regulating Gbx2 expression in the pharyngeal ectoderm. Development 136(18):3173–3183. https://doi.org/10.1242/dev.028902
Canga Y, Ozcan KS, Emre A, Kul S, Guvenc TS, Durmus G, Kirbas V, Ilhan E, Karatas MB, Oz D, Terzi S, Yesilcimen K (2012) Coronary artery fistula: review of 54 cases from single center experience. Cardiol J 19(3):278–286
Chai M, Sanosaka T, Okuno H, Zhou Z, Koya I, Banno S, Andoh-Noda T, Tabata Y, Shimamura R, Hayashi T, Ebisawa M, Sasagawa Y, Nikaido I, Okano H, Kohyama J (2018) Chromatin remodeler CHD7 regulates the stem cell identity of human neural progenitors. Genes Dev 32(2):165–180. https://doi.org/10.1101/gad.301887.117
Chambers D, McGonnell IM (2002) Neural crest: facing the facts of head development. Trends Genet 18(8):381–384
Chapnik E, Sasson V, Blelloch R, Hornstein E (2011) Dgcr8 controls neural crest cells survival in cardiovascular development. Dev Biol 362(1):50–56. https://doi.org/10.1016/j.ydbio.2011.11.008
Chen H, Jiang L, Xie Z, Mei L, He C, Hu Z, Xia K, Feng Y (2010) Novel mutations of PAX3, MITF, and SOX10 genes in Chinese patients with type I or type II Waardenburg syndrome. Biochem Biophys Res Commun 397(1):70–74. https://doi.org/10.1016/j.bbrc.2010.05.066
Chen HI, Poduri A, Numi H, Kivela R, Saharinen P, McKay AS, Raftrey B, Churko J, Tian X, Zhou B, Wu JC, Alitalo K, Red-Horse K (2014) VEGF-C and aortic cardiomyocytes guide coronary artery stem development. J Clin Investig 124(11):4899–4914. https://doi.org/10.1172/JCI77483
Chen JF, Murchison EP, Tang R, Callis TE, Tatsuguchi M, Deng Z, Rojas M, Hammond SM, Schneider MD, Selzman CH, Meissner G, Patterson C, Hannon GJ, Wang DZ (2008) Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc Natl Acad Sci USA 105(6):2111–2116. https://doi.org/10.1073/pnas.0710228105
Conway SJ, Henderson DJ, Copp AJ (1997a) Pax3 is required for cardiac neural crest migration in the mouse: evidence from the splotch (Sp2H) mutant. Development 124(2):505–514
Conway SJ, Henderson DJ, Kirby ML, Anderson RH, Copp AJ (1997b) Development of a lethal congenital heart defect in the splotch (Pax3) mutant mouse. Cardiovasc Res 36(2):163–173
Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D (2009) miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460(7256):705–710. https://doi.org/10.1038/nature08195
Corsten-Janssen N, Kerstjens-Frederikse WS, du Marchie Sarvaas GJ, Baardman ME, Bakker MK, Bergman JE, Hove HD, Heimdal KR, Rustad CF, Hennekam RC, Hofstra RM, Hoefsloot LH, Van Ravenswaaij-Arts CM, Kapusta L (2013) The cardiac phenotype in patients with a CHD7 mutation. Circ Cardiovasc Genet 6(3):248–254. https://doi.org/10.1161/CIRCGENETICS.113.000054
Couly G, Grapin-Botton A, Coltey P, Ruhin B, Le Douarin NM (1998) Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 125(17):3445–3459
Dai X, Jiang W, Zhang Q, Xu L, Geng P, Zhuang S, Petrich BG, Jiang C, Peng L, Bhattacharya S, Evans SM, Sun Y, Chen J, Liang X (2013) Requirement for integrin-linked kinase in neural crest migration and differentiation and outflow tract morphogenesis. BMC Biol 11:107. https://doi.org/10.1186/1741-7007-11-107
Demir M (2013) Left ventricular systolic and diastolic function in subjects with a bicuspid aortic valve without significant valvular dysfunction. Exp Clin Cardiol 18(1):e1–4
Dupin E, Le Douarin NM (2014) The neural crest, a multifaceted structure of the vertebrates. Birth Defects Res C 102(3):187–209. https://doi.org/10.1002/bdrc.21080
Eichmann A, Grapin-Botton A, Kelly L, Graf T, Le Douarin NM, Sieweke M (1997) The expression pattern of the mafB/kr gene in birds and mice reveals that the kreisler phenotype does not represent a null mutant. Mech Dev 65(1–2):111–122
Engleka KA, Gitler AD, Zhang M, Zhou DD, High FA, Epstein JA (2005) Insertion of Cre into the Pax3 locus creates a new allele of Splotch and identifies unexpected Pax3 derivatives. Dev Biol 280(2):396–406. https://doi.org/10.1016/j.ydbio.2005.02.002
Escot S, Blavet C, Faure E, Zaffran S, Duband JL, Fournier-Thibault C (2016) Disruption of CXCR4 signaling in pharyngeal neural crest cells causes DiGeorge syndrome-like malformations. Development 143(4):582–588. https://doi.org/10.1242/dev.126573
Etchevers HC, Vincent C, Le Douarin NM, Couly GF (2001) The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128(7):1059–1068
Ezin AM, Sechrist JW, Zah A, Bronner M, Fraser SE (2010) Early regulative ability of the neuroepithelium to form cardiac neural crest. Dev Biol 349(2):238–249. https://doi.org/10.1016/j.ydbio.2010.10.032
Feng X, Krebs LT, Gridley T (2010) Patent ductus arteriosus in mice with smooth muscle-specific Jag1 deletion. Development 137(24):4191–4199. https://doi.org/10.1242/dev.052043
Fernandez B, Duran AC, Fernandez-Gallego T, Fernandez MC, Such M, Arque JM, Sans-Coma V (2009) Bicuspid aortic valves with different spatial orientations of the leaflets are distinct etiological entities. J Am Coll Cardiol 54(24):2312–2318. https://doi.org/10.1016/j.jacc.2009.07.044
Folkersen L, Wagsater D, Paloschi V, Jackson V, Petrini J, Kurtovic S, Maleki S, Eriksson MJ, Caidahl K, Hamsten A, Michel JB, Liska J, Gabrielsen A, Franco-Cereceda A, Eriksson P (2010) Unraveling divergent gene expression profiles in bicuspid and tricuspid aortic valve patients with thoracic aortic dilatation: the ASAP study. Mol Med 17(11–12):1365–1373. https://doi.org/10.2119/molmed.2011.00286
Frisdal A, Trainor PA (2014) Development and evolution of the pharyngeal apparatus. Wiley Interdiscip Rev Dev Biol 3(6):403–418. https://doi.org/10.1002/wdev.147
Gao Z, Kim GH, Mackinnon AC, Flagg AE, Bassett B, Earley JU, Svensson EC (2010) Ets1 is required for proper migration and differentiation of the cardiac neural crest. Development 137(9):1543–1551. https://doi.org/10.1242/dev.047696
George L, Dunkel H, Hunnicutt BJ, Filla M, Little C, Lansford R, Lefcort F (2016) In vivo time-lapse imaging reveals extensive neural crest and endothelial cell interactions during neural crest migration and formation of the dorsal root and sympathetic ganglia. Dev Biol 413(1):70–85. https://doi.org/10.1016/j.ydbio.2016.02.028
Ghislain J, Desmarquet-Trin-Dinh C, Gilardi-Hebenstreit P, Charnay P, Frain M (2003) Neural crest patterning: autoregulatory and crest-specific elements co-operate for Krox20 transcriptional control. Development 130(5):941–953
Green SA, Simoes-Costa M, Bronner ME (2015) Evolution of vertebrates as viewed from the crest. Nature 520(7548):474–482. https://doi.org/10.1038/nature14436
Grewal N, Gittenberger-de Groot AC, Poelmann RE, Klautz RJ, Lindeman JH, Goumans MJ, Palmen M, Mohamed SA, Sievers HH, Bogers AJ, DeRuiter MC (2014) Ascending aorta dilation in association with bicuspid aortic valve: a maturation defect of the aortic wall. J Thorac Cardiovasc Surg 148(4):1583–1590. https://doi.org/10.1016/j.jtcvs.2014.01.027
Grossfeld PD, Mattina T, Lai Z, Favier R, Jones KL, Cotter F, Jones C (2004) The 11q terminal deletion disorder: a prospective study of 110 cases. Am J Med Genet A 129A(1):51–61. https://doi.org/10.1002/ajmg.a.30090
High FA, Zhang M, Proweller A, Tu L, Parmacek MS, Pear WS, Epstein JA (2007) An essential role for Notch in neural crest during cardiovascular development and smooth muscle differentiation. J Clin Investig 117(2):353–363. https://doi.org/10.1172/JCI30070
High FA, Jain R, Stoller JZ, Antonucci NB, Lu MM, Loomes KM, Kaestner KH, Pear WS, Epstein JA (2009) Murine Jagged1/Notch signaling in the second heart field orchestrates Fgf8 expression and tissue-tissue interactions during outflow tract development. J Clin Investig 119(7):1986–1996. https://doi.org/10.1172/JCI38922
Hinton RB, Martin LJ, Rame-Gowda S, Tabangin ME, Cripe LH, Benson DW (2009) Hypoplastic left heart syndrome links to chromosomes 10q and 6q and is genetically related to bicuspid aortic valve. J Am Coll Cardiol 53(12):1065–1071. https://doi.org/10.1016/j.jacc.2008.12.023
Hong SH, Fang S, Lu BC, Nofsinger R, Kawakami Y, Castro GL, Yin Y, Lin C, Yu RT, Downes M, Izpisua Belmonte JC, Shilatifard A, Evans RM (2018) Corepressor SMRT is required to maintain Hox transcriptional memory during somitogenesis. Proc Natl Acad Sci USA 115(41):10381–10386. https://doi.org/10.1073/pnas.1809480115
Hu N, Strobl-Mazzulla P, Sauka-Spengler T, Bronner ME (2012) DNA methyltransferase3A as a molecular switch mediating the neural tube-to-neural crest fate transition. Genes Dev 26(21):2380–2385. https://doi.org/10.1101/gad.198747.112
Hu N, Strobl-Mazzulla PH, Bronner ME (2014) Epigenetic regulation in neural crest development. Dev Biol 396(2):159–168. https://doi.org/10.1016/j.ydbio.2014.09.034
Huang ZP, Chen JF, Regan JN, Maguire CT, Tang RH, Dong XR, Majesky MW, Wang DZ (2010) Loss of microRNAs in neural crest leads to cardiovascular syndromes resembling human congenital heart defects. Arterioscler Thromb Vasc Biol 30(12):2575–2586. https://doi.org/10.1161/ATVBAHA.110.213306
Hurle JM, Colvee E, Blanco AM (1980) Development of mouse semilunar valves. Anat Embryol (Berl) 160(1):83–91
Huynh T, Chen L, Terrell P, Baldini A (2007) A fate map of Tbx1 expressing cells reveals heterogeneity in the second cardiac field. Genesis 45(7):470–475. https://doi.org/10.1002/dvg.20317
Ivey KN, Sutcliffe D, Richardson J, Clyman RI, Garcia JA, Srivastava D (2008) Transcriptional regulation during development of the ductus arteriosus. Circ Res 103(4):388–395. https://doi.org/10.1161/CIRCRESAHA.108.180661
Jain R, Engleka KA, Rentschler SL, Manderfield LJ, Li L, Yuan L, Epstein JA (2011) Cardiac neural crest orchestrates remodeling and functional maturation of mouse semilunar valves. J Clin Investig 121(1):422–430. https://doi.org/10.1172/JCI44244
Jia Q, McDill BW, Li SZ, Deng C, Chang CP, Chen F (2007) Smad signaling in the neural crest regulates cardiac outflow tract remodeling through cell autonomous and non-cell autonomous effects. Dev Biol 311(1):172–184. https://doi.org/10.1016/j.ydbio.2007.08.044
Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cardiac neural crest. Development 127(8):1607–1616
Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM (2002) Tissue origins and interactions in the mammalian skull vault. Dev Biol 241(1):106–116. https://doi.org/10.1006/dbio.2001.0487
Jiao J, Xiong W, Wang L, Yang J, Qiu P, Hirai H, Shao L, Milewicz D, Chen YE, Yang B (2016) Differentiation defect in neural crest-derived smooth muscle cells in patients with aortopathy associated with bicuspid aortic valves. EBioMedicine 10:282–290. https://doi.org/10.1016/j.ebiom.2016.06.045
Kaartinen V, Dudas M, Nagy A, Sridurongrit S, Lu MM, Epstein JA (2004) Cardiac outflow tract defects in mice lacking ALK2 in neural crest cells. Development 131(14):3481–3490. https://doi.org/10.1242/dev.01214
Kelly RG (2012) The second heart field. Curr Top Dev Biol 100:33–65. https://doi.org/10.1016/B978-0-12-387786-4.00002-6
Kelly RG, Buckingham ME, Moorman AF (2014) Heart fields and cardiac morphogenesis. Cold Spring Harb Perspect Med. https://doi.org/10.1101/cshperspect.a015750
Kelsh RN, Erickson CA (2013) Neural crest: origin, migration and differentiation. Wiley, Chister, pp 1–10
Keyte A, Hutson MR (2012) The neural crest in cardiac congenital anomalies. Differentiation 84(1):25–40. https://doi.org/10.1016/j.diff.2012.04.005
Kirby ML, Gale TF, Stewart DE (1983) Neural crest cells contribute to normal aorticopulmonary septation. Science 220(4601):1059–1061
Kirby ML, Hutson MR (2010) Factors controlling cardiac neural crest cell migration. Cell Adhes Migr 4(4):609–621
Kowalski WJ, Dur O, Wang Y, Patrick MJ, Tinney JP, Keller BB, Pekkan K (2013) Critical transitions in early embryonic aortic arch patterning and hemodynamics. PLoS ONE 8(3):e60271. https://doi.org/10.1371/journal.pone.0060271
Krispin S, Nitzan E, Kassem Y, Kalcheim C (2010) Evidence for a dynamic spatiotemporal fate map and early fate restrictions of premigratory avian neural crest. Development 137(4):585–595. https://doi.org/10.1242/dev.041509
Kulesa P, Ellies DL, Trainor PA (2004) Comparative analysis of neural crest cell death, migration, and function during vertebrate embryogenesis. Dev Dyn 229(1):14–29. https://doi.org/10.1002/dvdy.10485
Kusakabe T, Hoshi N, Kimura S (2006) Origin of the ultimobranchial body cyst: T/ebp/Nkx2.1 expression is required for development and fusion of the ultimobranchial body to the thyroid. Dev Dyn 235(5):1300–1309. https://doi.org/10.1002/dvdy.20655
Le Douarin NM, Brito JM, Creuzet S (2007) Role of the neural crest in face and brain development. Brain Res Rev 55(2):237–247. https://doi.org/10.1016/j.brainresrev.2007.06.023
Lecoin L, Sii-Felice K, Pouponnot C, Eychene A, Felder-Schmittbuhl MP (2004) Comparison of maf gene expression patterns during chick embryo development. Gene Expr Patterns 4(1):35–46
Lescroart F, Wang X, Lin X, Swedlund B, Gargouri S, Sanchez-Danes A, Moignard V, Dubois C, Paulissen C, Kinston S, Gottgens B, Blanpain C (2018) Defining the earliest step of cardiovascular lineage segregation by single-cell RNA-seq. Science 359(6380):1177–1181. https://doi.org/10.1126/science.aao4174
Lewis JL, Bonner J, Modrell M, Ragland JW, Moon RT, Dorsky RI, Raible DW (2004) Reiterated Wnt signaling during zebrafish neural crest development. Development 131(6):1299–1308. https://doi.org/10.1242/dev.01007
Li W, Xiong Y, Shang C, Twu KY, Hang CT, Yang J, Han P, Lin CY, Lin CJ, Tsai FC, Stankunas K, Meyer T, Bernstein D, Pan M, Chang CP (2013) Brg1 governs distinct pathways to direct multiple aspects of mammalian neural crest cell development. Proc Natl Acad Sci USA 110(5):1738–1743. https://doi.org/10.1073/pnas.1218072110
Liang D, Wang X, Mittal A, Dhiman S, Hou SY, Degenhardt K, Astrof S (2014) Mesodermal expression of integrin alpha5beta1 regulates neural crest development and cardiovascular morphogenesis. Dev Biol 395(2):232–244. https://doi.org/10.1016/j.ydbio.2014.09.014
Lin CJ, Lin CY, Chen CH, Zhou B, Chang CP (2012) Partitioning the heart: mechanisms of cardiac septation and valve development. Development 139(18):3277–3299. https://doi.org/10.1242/dev.063495
Liu NM, Yokota T, Maekawa S, Lu P, Zheng YW, Taniguchi H, Yokoyama U, Kato T, Minamisawa S (2013) Transcription profiles of endothelial cells in the rat ductus arteriosus during a perinatal period. PLoS ONE 8(9):e73685. https://doi.org/10.1371/journal.pone.0073685
Losee JE, Kirschner RE (2009) Embryology of orofacial clefting. McGraw-Hill Medical, New York, pp 7–19
Makki N, Capecchi MR (2010) Hoxa1 lineage tracing indicates a direct role for Hoxa1 in the development of the inner ear, the heart, and the third rhombomere. Dev Biol 341(2):499–509. https://doi.org/10.1016/j.ydbio.2010.02.014
Martin LJ, Hinton RB, Zhang X, Cripe LH, Benson DW (2011) Aorta measurements are heritable and influenced by bicuspid aortic valve. Front Genet 2:61. https://doi.org/10.3389/fgene.2011.00061
Martin PS, Kloesel B, Norris RA, Lindsay MM (2015) Embryonic development of the bicuspid aortic valve. J Cardiovasc DevDis 2(4):248–272
Mayor R, Aybar MJ (2001) Induction and development of neural crest in Xenopus laevis. Cell Tissue Res 305(2):203–209. https://doi.org/10.1007/s004410100369
McBride KL, Zender GA, Fitzgerald-Butt SM, Koehler D, Menesses-Diaz A, Fernbach S, Lee K, Towbin JA, Leal S, Belmont JW (2009) Linkage analysis of left ventricular outflow tract malformations (aortic valve stenosis, coarctation of the aorta, and hypoplastic left heart syndrome). Eur J Hum Genet 17(6):811–819. https://doi.org/10.1038/ejhg.2008.255
McElhinney DB, Krantz ID, Bason L, Piccoli DA, Emerick KM, Spinner NB, Goldmuntz E (2002) Analysis of cardiovascular phenotype and genotype-phenotype correlation in individuals with a JAG1 mutation and/or Alagille syndrome. Circulation 106(20):2567–2574. https://doi.org/10.1161/01.cir.0000037221.45902.69
McElhinney DB, Driscoll DA, Levin ER, Jawad AF, Emanuel BS, Goldmuntz E (2003) Chromosome 22q11 deletion in patients with ventricular septal defect: frequency and associated cardiovascular anomalies. Pediatrics 112(6 Pt 1):e472
McKinney MC, Fukatsu K, Morrison J, McLennan R, Bronner ME, Kulesa PM (2013) Evidence for dynamic rearrangements but lack of fate or position restrictions in premigratory avian trunk neural crest. Development 140(4):820–830. https://doi.org/10.1242/dev.083725
Meindl C, Achatz B, Huber D, Baessler A, Hubauer U, Meisinger C, Hengstenberg C, Erdmann J, Buchner S, Maier L, Schunkert H, Debl K, Fischer M (2016) Coronary artery ectasia are frequently observed in patients with bicuspid aortic valves with and without dilatation of the ascending aorta. Circ Cardiovasc Interv. https://doi.org/10.1161/CIRCINTERVENTIONS.116.004092
Meulemans D, Bronner-Fraser M (2004) Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7(3):291–299. https://doi.org/10.1016/j.devcel.2004.08.007
Midgett M, Thornburg K, Rugonyi S (2017) Blood flow patterns underlie developmental heart defects. Am J Physiol Heart Circ Physiol 312(3):H632–H642. https://doi.org/10.1152/ajpheart.00641.2016
Mifflin JJ, Dupuis LE, Alcala NE, Russell LG, Kern CB (2018) Intercalated cushion cells within the cardiac outflow tract are derived from the myocardial troponin T type 2 (Tnnt2) Cre lineage. Dev Dyn 247(8):1005–1017. https://doi.org/10.1002/dvdy.24641
Milgrom-Hoffman M, Michailovici I, Ferrara N, Zelzer E, Tzahor E (2014) Endothelial cells regulate neural crest and second heart field morphogenesis. Biol Open 3(8):679–688. https://doi.org/10.1242/bio.20148078
Minoux M, Holwerda S, Vitobello A, Kitazawa T, Kohler H, Stadler MB, Rijli FM (2017) Gene bivalency at Polycomb domains regulates cranial neural crest positional identity. Science. https://doi.org/10.1126/science.aal2913
Mittal A, Pulina M, Hou SY, Astrof S (2010) Fibronectin and integrin alpha 5 play essential roles in the development of the cardiac neural crest. Mech Dev 127(9–12):472–484. https://doi.org/10.1016/j.mod.2010.08.005
Miyagawa-Tomita S, Arima Y, Kurihara H (2018) The "Cardiac Neural Crest" concept revisited cellular interaction to morphology. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54628-3_30
Monsoro-Burq AH (2015) PAX transcription factors in neural crest development. Semin Cell Dev Biol 44:87–96. https://doi.org/10.1016/j.semcdb.2015.09.015
Mostefa-Kara M, Bonnet D, Belli E, Fadel E, Houyel L (2015) Anatomy of the ventricular septal defect in outflow tract defects: similarities and differences. J Thorac Cardiovasc Surg 149(3):682–688. https://doi.org/10.1016/j.jtcvs.2014.11.087
Mostefa Kara M, Houyel L, Bonnet D (2019) A new anatomic approach of the ventricular septal defect in the interruption of the aortic arch. J Anat 234(2):193–200. https://doi.org/10.1111/joa.12911
Motahari Z, Moody SA, Maynard TM, LaMantia AS (2019) In the line-up: deleted genes associated with DiGeorge/22q11.2 deletion syndrome: are they all suspects? J Neurodev Disord 11(1):7. https://doi.org/10.1186/s11689-019-9267-z
Nataatmadja M, West M, West J, Summers K, Walker P, Nagata M, Watanabe T (2003) Abnormal extracellular matrix protein transport associated with increased apoptosis of vascular smooth muscle cells in marfan syndrome and bicuspid aortic valve thoracic aortic aneurysm. Circulation. https://doi.org/10.1161/01.cir.0000087660.82721.15
Nie S, Bronner ME (2015) Dual developmental role of transcriptional regulator Ets1 in Xenopus cardiac neural crest vs. heart mesoderm. Cardiovasc Res 106(1):67–75. https://doi.org/10.1093/cvr/cvv043
Nie X, Wang Q, Jiao K (2011) Dicer activity in neural crest cells is essential for craniofacial organogenesis and pharyngeal arch artery morphogenesis. Mech Dev 128(3–4):200–207. https://doi.org/10.1016/j.mod.2010.12.002
Nishibatake M, Kirby ML, Van Mierop LH (1987) Pathogenesis of persistent truncus arteriosus and dextroposed aorta in the chick embryo after neural crest ablation. Circulation 75(1):255–264
O'Rahilly R, Muller F (2007) The development of the neural crest in the human. J Anat 211(3):335–351. https://doi.org/10.1111/j.1469-7580.2007.00773.x
Odelin G, Faure E, Coulpier F, Di Bonito M, Bajolle F, Studer M, Avierinos JF, Charnay P, Topilko P, Zaffran S (2018a) Krox20 defines a subpopulation of cardiac neural crest cells contributing to arterial valves and bicuspid aortic valve. Development. https://doi.org/10.1242/dev.151944
Odelin G, Faure E, Kober F, Maurel-Zaffran C, Theron A, Coulpier F, Guillet B, Bernard M, Avierinos JF, Charnay P, Topilko P, Zaffran S (2018b) Loss of Krox20 results in aortic valve regurgitation and impaired transcriptional activation of fibrillar collagen genes. Cardiovasc Res 104(3):443–455. https://doi.org/10.1093/cvr/cvu233
Okamoto N, Akimoto N, Hidaka N, Shoji S, Sumida H (2010) Formal genesis of the outflow tracts of the heart revisited: previous works in the light of recent observations. Congenit Anom (Kyoto) 50(3):141–158. https://doi.org/10.1111/j.1741-4520.2010.00286.x
Olaopa M, Zhou HM, Snider P, Wang J, Schwartz RJ, Moon AM, Conway SJ (2011) Pax3 is essential for normal cardiac neural crest morphogenesis but is not required during migration nor outflow tract septation. Dev Biol 356(2):308–322. https://doi.org/10.1016/j.ydbio.2011.05.583
Osumi-Yamashita N, Ninomiya Y, Doi H, Eto K (1996) Rhombomere formation and hind-brain crest cell migration from prorhombomeric origins in mouse embryos. Dev Growth Differ 38:107–118
Padang R, Bannon PG, Jeremy R, Richmond DR, Semsarian C, Vallely M, Wilson M, Yan TD (2013) The genetic and molecular basis of bicuspid aortic valve associated thoracic aortopathy: a link to phenotype heterogeneity. Ann Cardiothorac Surg 2(1):83–91. https://doi.org/10.3978/j.issn.2225-319X.2012.11.17
Paloschi V, Kurtovic S, Folkersen L, Gomez D, Wagsater D, Roy J, Petrini J, Eriksson MJ, Caidahl K, Hamsten A, Liska J, Michel JB, Franco-Cereceda A, Eriksson P (2011) Impaired splicing of fibronectin is associated with thoracic aortic aneurysm formation in patients with bicuspid aortic valve. Arterioscler Thromb Vasc Biol 31(3):691–697. https://doi.org/10.1161/ATVBAHA.110.218461
Papangeli I, Scambler PJ (2012) Tbx1 genetically interacts with the transforming growth factor-beta/bone morphogenetic protein inhibitor Smad7 during great vessel remodeling. Circ Res 112(1):90–102. https://doi.org/10.1161/CIRCRESAHA.112.270223
Parker HJ, Pushel I, Krumlauf R (2018) Coupling the roles of Hox genes to regulatory networks patterning cranial neural crest. Dev Biol. https://doi.org/10.1016/j.ydbio.2018.03.016
Payne S, Burney MJ, McCue K, Popal N, Davidson SM, Anderson RH, Scambler PJ (2015) A critical role for the chromatin remodeller CHD7 in anterior mesoderm during cardiovascular development. Dev Biol 405(1):82–95. https://doi.org/10.1016/j.ydbio.2015.06.017
Perez-Pomares JM, de la Pompa JL, Franco D, Henderson D, Ho SY, Houyel L, Kelly RG, Sedmera D, Sheppard M, Sperling S, Thiene G, van den Hoff M, Basso C (2016) Congenital coronary artery anomalies: a bridge from embryology to anatomy and pathophysiology—a position statement of the development, anatomy, and pathology ESC Working Group. Cardiovasc Res 109(2):204–216. https://doi.org/10.1093/cvr/cvv251
Phillippi JA, Klyachko EA, Kenny JP, Eskay MA, Gorman RC, Gleason TG (2009) Basal and oxidative stress-induced expression of metallothionein is decreased in ascending aortic aneurysms of bicuspid aortic valve patients. Circulation 119(18):2498–2506. https://doi.org/10.1161/CIRCULATIONAHA.108.770776
Phillips HM, Mahendran P, Singh E, Anderson RH, Chaudhry B, Henderson DJ (2013) Neural crest cells are required for correct positioning of the developing outflow cushions and pattern the arterial valve leaflets. Cardiovasc Res 99(3):452–460. https://doi.org/10.1093/cvr/cvt132
Pierpont ME, Basson CT, Benson DW Jr, Gelb BD, Giglia TM, Goldmuntz E, McGee G, Sable CA, Srivastava D, Webb CL (2007) Genetic basis for congenital heart defects: current knowledge: a scientific statement from the American Heart Association Congenital Cardiac Defects Committee, Council on Cardiovascular Disease in the Young: endorsed by the American Academy of Pediatrics. Circulation 115(23):3015–3038. https://doi.org/10.1161/CIRCULATIONAHA.106.183056
Plein A, Calmont A, Fantin A, Denti L, Anderson NA, Scambler PJ, Ruhrberg C (2015) Neural crest-derived SEMA3C activates endothelial NRP1 for cardiac outflow tract septation. J Clin Investig 125(7):2661–2676. https://doi.org/10.1172/JCI79668
Pong SK, Gullerova M (2018) Noncanonical functions of microRNA pathway enzymes—Drosha, DGCR8, Dicer and Ago proteins. FEBS Lett 592(17):2973–2986. https://doi.org/10.1002/1873-3468.13196
Prasad MS, Charney RM, Garcia-Castro MI (2019) Specification and formation of the neural crest: perspectives on lineage segregation. Genesis 57(1):e23276. https://doi.org/10.1002/dvg.23276
Prescott K, Ivins S, Hubank M, Lindsay E, Baldini A, Scambler P (2005) Microarray analysis of the Df1 mouse model of the 22q11 deletion syndrome. Hum Genet 116(6):486–496. https://doi.org/10.1007/s00439-005-1274-3
Quimonez SC, Innis JW (2014) Human Hox gene disorders. Mol Genet Metab 111:4–15
Rada-Iglesias A, Bajpai R, Prescott S, Brugmann SA, Swigut T, Wysocka J (2012) Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest. Cell Stem Cell 11(5):633–648. https://doi.org/10.1016/j.stem.2012.07.006
Rao A, LaBonne C (2018) Histone deacetylase activity has an essential role in establishing and maintaining the vertebrate neural crest. Development. https://doi.org/10.1242/dev.163386
Richarte AM, Mead HB, Tallquist MD (2007) Cooperation between the PDGF receptors in cardiac neural crest cell migration. Dev Biol 306(2):785–796. https://doi.org/10.1016/j.ydbio.2007.04.023
Roux M, Laforest B, Capecchi M, Bertrand N, Zaffran S (2015) Hoxb1 regulates proliferation and differentiation of second heart field progenitors in pharyngeal mesoderm and genetically interacts with Hoxa1 during cardiac outflow tract development. Dev Biol 406(2):247–258. https://doi.org/10.1016/j.ydbio.2015.08.015
Roux M, Laforest B, Eudes N, Bertrand N, Stefanovic S, Zaffran S (2016) Hoxa1 and Hoxb1 are required for pharyngeal arch artery development. Mech Dev 143:1–8. https://doi.org/10.1016/j.mod.2016.11.006
Roux M, Zaffran S (2016a) Hox genes in cardiovascular development and diseases. Dev Biol 4(14):5–12
Roux M, Zaffran S (2016b) Hox genes in cardiovascular developpment and diseases. Dev Biol 4:1–14
Sanchez-Castro M, Pichon O, Briand A, Poulain D, Gournay V, David A, Le Caignec C (2014) Disruption of the SEMA3D gene in a patient with congenital heart defects. Hum Mutat 36(1):30–33. https://doi.org/10.1002/humu.22702
Sanchez-Vasquez E, Bronner ME, Strobl-Mazzulla PH (2019) Epigenetic inactivation of miR-203 as a key step in neural crest epithelial-to-mesenchymal transition. Development. https://doi.org/10.1242/dev.171017
Sawada H, Rateri DL, Moorleghen JJ, Majesky MW, Daugherty A (2017) Smooth muscle cells derived from second heart field and cardiac neural crest reside in spatially distinct domains in the media of the ascending aorta. Arterioscler Thromb Vasc Biol. https://doi.org/10.1161/ATVBAHA.117.309599
Scambler PJ (2010) 22q11 deletion syndrome: a role for TBX1 in pharyngeal and cardiovascular development. Pediatr Cardiol 31(3):378–390. https://doi.org/10.1007/s00246-009-9613-0
Scheppke L, Murphy EA, Zarpellon A, Hofmann JJ, Merkulova A, Shields DJ, Weis SM, Byzova TV, Ruggeri ZM, Iruela-Arispe ML, Cheresh DA (2012) Notch promotes vascular maturation by inducing integrin-mediated smooth muscle cell adhesion to the endothelial basement membrane. Blood 119(9):2149–2158. https://doi.org/10.1182/blood-2011-04-348706
Schleich JM, Abdulla T, Summers R, Houyel L (2013) An overview of cardiac morphogenesis. Arch Cardiovasc Dis 106(11):612–623. https://doi.org/10.1016/j.acvd.2013.07.001
Scholl AM, Kirby ML (2009) Signals controlling neural crest contributions to the heart. Wiley Interdiscip Rev Syst Biol Med 1(2):220–227
Shaheen R, Al Hashem A, Alghamdi MH, Seidahmad MZ, Wakil SM, Dagriri K, Keavney B, Goodship J, Alyousif S, Al-Habshan FM, Alhussein K, Almoisheer A, Ibrahim N, Alkuraya FS (2015) Positional mapping of PRKD1, NRP1 and PRDM1 as novel candidate disease genes in truncus arteriosus. J Med Genet 52(5):322–329. https://doi.org/10.1136/jmedgenet-2015-102992
Shprintzen RJ (2008) Velo-cardio-facial syndrome: 30 years of study. Dev Disabil Res Rev 14(1):3–10. https://doi.org/10.1002/ddrr.2
Simoes-Costa M, Bronner ME (2015) Establishing neural crest identity: a gene regulatory recipe. Development 142(2):242–257. https://doi.org/10.1242/dev.105445
Simoes-Costa M, Tan-Cabugao J, Antoshechkin I, Sauka-Spengler T, Bronner ME (2014) Transcriptome analysis reveals novel players in the cranial neural crest gene regulatory network. Genome Res 24(2):281–290. https://doi.org/10.1101/gr.161182.113
Simoes-Costa MS, McKeown SJ, Tan-Cabugao J, Sauka-Spengler T, Bronner ME (2013) Dynamic and differential regulation of stem cell factor FoxD3 in the neural crest is Encrypted in the genome. PLoS Genet 8(12):e1003142. https://doi.org/10.1371/journal.pgen.1003142
Singh N, Trivedi CM, Lu M, Mullican SE, Lazar MA, Epstein JA (2011) Histone deacetylase 3 regulates smooth muscle differentiation in neural crest cells and development of the cardiac outflow tract. Circ Res 109(11):1240–1249. https://doi.org/10.1161/CIRCRESAHA.111.255067
Sizarov A, Lamers WH, Mohun TJ, Brown NA, Anderson RH, Moorman AF (2012) Three-dimensional and molecular analysis of the arterial pole of the developing human heart. J Anat 220(4):336–349. https://doi.org/10.1111/j.1469-7580.2012.01474.x
Sperber GH, Sperber SM (2013) Embryogenetics od cleft lip and palate, 3rd edn. Springer-Verlag, Berlin, pp 3–33
Stalmans I, Lambrechts D, De Smet F, Jansen S, Wang J, Maity S, Kneer P, von der Ohe M, Swillen A, Maes C, Gewillig M, Molin DG, Hellings P, Boetel T, Haardt M, Compernolle V, Dewerchin M, Plaisance S, Vlietinck R, Emanuel B, Gittenberger-de Groot AC, Scambler P, Morrow B, Driscol DA, Moons L, Esguerra CV, Carmeliet G, Behn-Krappa A, Devriendt K, Collen D, Conway SJ, Carmeliet P (2003) VEGF: a modifier of the del22q11 (DiGeorge) syndrome? Nat Med 9(2):173–182. https://doi.org/10.1038/nm819
Stankunas K, Shang C, Twu KY, Kao SC, Jenkins NA, Copeland NG, Sanyal M, Selleri L, Cleary ML, Chang CP (2008) Pbx/Meis deficiencies demonstrate multigenetic origins of congenital heart disease. Circ Res 103(7):702–709. https://doi.org/10.1161/CIRCRESAHA.108.175489
Stoetzel C, Riehm S, Bennouna Greene V, Pelletier V, Vigneron J, Leheup B, Marion V, Helle S, Danse JM, Thibault C, Moulinier L, Veillon F, Dollfus H (2009) Confirmation of TFAP2A gene involvement in branchio-oculo-facial syndrome (BOFS) and report of temporal bone anomalies. Am J Med Genet A 149A(10):2141–2146. https://doi.org/10.1002/ajmg.a.33015
Strobl-Mazzulla PH, Bronner ME (2012) A PHD12-Snail2 repressive complex epigenetically mediates neural crest epithelial-to-mesenchymal transition. J Cell Biol 198(6):999–1010. https://doi.org/10.1083/jcb.201203098
Sun X, Zhang R, Lin X, Xu X (2008) Wnt3a regulates the development of cardiac neural crest cells by modulating expression of cysteine-rich intestinal protein 2 in rhombomere 6. Circ Res 102(7):831–839. https://doi.org/10.1161/CIRCRESAHA.107.166488
Sylva M, van den Hoff MJ, Moorman AF (2014) Development of the human heart. Am J Med Genet A 164A(6):1347–1371. https://doi.org/10.1002/ajmg.a.35896
Tang Y, Urs S, Boucher J, Bernaiche T, Venkatesh D, Spicer DB, Vary CP, Liaw L (2010) Notch and transforming growth factor-beta (TGFbeta) signaling pathways cooperatively regulate vascular smooth muscle cell differentiation. J Biol Chem 285(23):17556–17563. https://doi.org/10.1074/jbc.M109.076414
Tani-Matsuhana S, Vieceli FM, Gandhi S, Inoue K, Bronner ME (2018) Transcriptome profiling of the cardiac neural crest reveals a critical role for MafB. Dev Biol. https://doi.org/10.1016/j.ydbio.2018.09.015
Tassabehji M, Newton VE, Read AP (1994) Waardenburg syndrome type 2 caused by mutations in the human microphthalmia (MITF) gene. Nat Genet 8(3):251–255. https://doi.org/10.1038/ng1194-251
Torroglosa A, Villalba-Benito L, Luzon-Toro B, Fernandez RM, Antinolo G, Borrego S (2019) Epigenetic mechanisms in hirschsprung disease. Int J Mol Sci. https://doi.org/10.3390/ijms20133123
Toyofuku T, Yoshida J, Sugimoto T, Yamamoto M, Makino N, Takamatsu H, Takegahara N, Suto F, Hori M, Fujisawa H, Kumanogoh A, Kikutani H (2008) Repulsive and attractive semaphorins cooperate to direct the navigation of cardiac neural crest cells. Dev Biol 321(1):251–262. https://doi.org/10.1016/j.ydbio.2008.06.028
Turner CJ, Badu-Nkansah K, Crowley D, van der Flier A, Hynes RO (2015) alpha5 and alphav integrins cooperate to regulate vascular smooth muscle and neural crest functions in vivo. Development 142(4):797–808. https://doi.org/10.1242/dev.117572
Valdembri D, Regano D, Maione F, Giraudo E, Serini G (2016) Class 3 semaphorins in cardiovascular development. Cell Adhes Migr 10(6):641–651. https://doi.org/10.1080/19336918.2016.1212805
van den Hoff MJ, Moorman AF, Ruijter JM, Lamers WH, Bennington RW, Markwald RR, Wessels A (1999) Myocardialization of the cardiac outflow tract. Dev Biol 212(2):477–490. https://doi.org/10.1006/dbio.1999.9366
Van Otterloo E, Li H, Jones KL, Williams T (2017) AP-2alpha and AP-2beta cooperatively orchestrate homeobox gene expression during branchial arch patterning. Development. https://doi.org/10.1242/dev.157438
Vieux-Rochas M, Mascrez B, Krumlauf R, Duboule D (2013) Combined function of HoxA and HoxB clusters in neural crest cells. Dev Biol 382(1):293–301. https://doi.org/10.1016/j.ydbio.2013.06.027
Villanueva S, Glavic A, Ruiz P, Mayor R (2002) Posteriorization by FGF, Wnt, and retinoic acid is required for neural crest induction. Dev Biol 241(2):289–301. https://doi.org/10.1006/dbio.2001.0485
Voiculescu O, Charnay P, Schneider-Maunoury S (2000) Expression pattern of a Krox-20/Cre knock-in allele in the developing hindbrain, bones, and peripheral nervous system. Genesis 26(2):123–126. https://doi.org/10.1002/(SICI)1526-968X(200002)26:2%3c123:AID-GENE7%3e3.0.CO;2-O
Wagsater D, Paloschi V, Hanemaaijer R, Hultenby K, Bank RA, Franco-Cereceda A, Lindeman JH, Eriksson P (2013) Impaired collagen biosynthesis and cross-linking in aorta of patients with bicuspid aortic valve. J Am Heart Assoc 2(1):e000034. https://doi.org/10.1161/JAHA.112.000034
Waldo K, Miyagawa-Tomita S, Kumiski D, Kirby ML (1998) Cardiac neural crest cells provide new insight into septation of the cardiac outflow tract: aortic sac to ventricular septal closure. Dev Biol 196(2):129–144. https://doi.org/10.1006/dbio.1998.8860
Wang J, Nagy A, Larsson J, Dudas M, Sucov HM, Kaartinen V (2006) Defective ALK5 signaling in the neural crest leads to increased postmigratory neural crest cell apoptosis and severe outflow tract defects. BMC Dev Biol 6:51. https://doi.org/10.1186/1471-213X-6-51
Wang JJ, Liu HX, Song L, Li HR, Yang YP, Zhang T, Jing Y (2019) Isl-1 positive pharyngeal mesenchyme subpopulation and its role in the separation and remodeling of the aortic sac in embryonic mouse heart. Dev Dyn 248(9):771–783. https://doi.org/10.1002/dvdy.68
Wang X, Astrof S (2015) Neural crest cell-autonomous roles of fibronectin in cardiovascular development. Development 143(1):88–100. https://doi.org/10.1242/dev.125286
Ward C (2000) Clinical significance of the bicuspid aortic valve. Heart 83(1):81–85
Ward C, Stadt H, Hutson M, Kirby ML (2005) Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev Biol 284(1):72–83. https://doi.org/10.1016/j.ydbio.2005.05.003
Weiner AMJ (2018) MicroRNAs and the neural crest: from induction to differentiation. Mech Dev. https://doi.org/10.1016/j.mod.2018.05.009
Xie CH, Zhao ZY, Zhou YB, Gong FQ (2007) Single coronary artery with fistula, right aortic arch, bicuspid aortic valve, and pulmonary stenosis: a rare combination. Pediatr Cardiol 28(4):286–288. https://doi.org/10.1007/s00246-006-0003-6
Yarboro MT, Durbin MD, Herington JL, Shelton EL, Zhang T, Ebby CG, Stoller JZ, Clyman RI, Reese J (2018) Transcriptional profiling of the ductus arteriosus: comparison of rodent microarrays and human RNA sequencing. Semin Perinatol 42(4):212–220. https://doi.org/10.1053/j.semperi.2018.05.003
Yashiro K, Shiratori H, Hamada H (2007) Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch. Nature 450(7167):285–288. https://doi.org/10.1038/nature06254
Zaidi S, Brueckner M (2017) Genetics and genomics of congenital heart disease. Circ Res 120(6):923–940. https://doi.org/10.1161/CIRCRESAHA.116.309140
Zehir A, Hua LL, Maska EL, Morikawa Y, Cserjesi P (2010) Dicer is required for survival of differentiating neural crest cells. Dev Biol 340(2):459–467. https://doi.org/10.1016/j.ydbio.2010.01.039
Zhao F, Weismann CG, Satoda M, Pierpont ME, Sweeney E, Thompson EM, Gelb BD (2001) Novel TFAP2B mutations that cause Char syndrome provide a genotype-phenotype correlation. Am J Hum Genet 69(4):695–703. https://doi.org/10.1086/323410
Zhou J, Pashmforoush M, Sucov HM (2012) Endothelial neuropilin disruption in mice causes DiGeorge syndrome-like malformations via mechanisms distinct to those caused by loss of Tbx1. PLoS ONE 7(3):e32429. https://doi.org/10.1371/journal.pone.0032429
Zou Y, Chen Z, Jennings BL, Zhao G, Gu Q, Bhattacharya A, Cui Y, Yu B, Malik KU, Yue J (2018) Deletion of DGCR8 in VSMCs of adult mice results in loss of vascular reactivity, reduced blood pressure and neointima formation. Sci Rep 8(1):1468. https://doi.org/10.1038/s41598-018-19660-z
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Schussler, O., Gharibeh, L., Mootoosamy, P. et al. Cardiac Neural Crest Cells: Their Rhombomeric Specification, Migration, and Association with Heart and Great Vessel Anomalies. Cell Mol Neurobiol 41, 403–429 (2021). https://doi.org/10.1007/s10571-020-00863-w
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DOI: https://doi.org/10.1007/s10571-020-00863-w