Mechanisms of retinoic acid signaling during cardiogenesis

Mechanisms of Development

Volumn 143, Issue , 2017, Pages 9-19

  Stefanovic, Sonia ^a   Zaffran, Stéphane ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Cell fate decisions; Heart development; Retinoic acid; Retinoic acid receptors

Indexed keywords

RETINOIC ACID; RETINOID X RECEPTOR; ALDEHYDE DEHYDROGENASE; HOMEODOMAIN PROTEIN; INSULIN GENE ENHANCER BINDING PROTEIN ISL-1; LIM HOMEODOMAIN PROTEIN; RALDH2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

CARDIAC MUSCLE CELL; CARDIAC STEM CELL; CELL DIFFERENTIATION; CORONARY BLOOD VESSEL; EMBRYONIC STEM CELL; GENE; GENE CONTROL; GENE EXPRESSION; HEART DEVELOPMENT; HISTONE ACETYLATION; HOXA1 GENE; HOXB1 GENE; HUMAN; NONHUMAN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; DROSOPHILA MELANOGASTER; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART; METABOLISM; MOUSE; ORGANOGENESIS; ZEBRA FISH;

ALDEHYDE OXIDOREDUCTASES; ANIMALS; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HOMEODOMAIN PROTEINS; HUMANS; LIM-HOMEODOMAIN PROTEINS; MICE; ORGANOGENESIS; RETINOID X RECEPTORS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRETINOIN; ZEBRAFISH;

EID: 85014324469     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2016.12.002     Document Type: Review

References (199)

1. Abu-Abed, S., Dolle, P., Metzger, D., Beckett, B., Chambon, P., Petkovich, M., The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev. 15 (2001), 226–240.
2. Adams, M.K., Belyaeva, O.V., Wu, L., Kedishvili, N.Y., The retinaldehyde reductase activity of DHRS3 is reciprocally activated by retinol dehydrogenase 10 to control retinoid homeostasis. J. Biol. Chem. 289 (2014), 14868–14880.
3. Amengual, J., Zhang, N., Kemerer, M., Maeda, T., Palczewski, K., Von Lintig, J., STRA6 is critical for cellular vitamin A uptake and homeostasis. Hum. Mol. Genet. 23 (2014), 5402–5417.
4. Arceci, R.J., King, A.A., Simon, M.C., Orkin, S.H., Wilson, D.B., Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol. Cell. Biol. 13 (1993), 2235–2246.
5. Azambuja, A.P., Portillo-Sanchez, V., Rodrigues, M.V., Omae, S.V., Schechtman, D., Strauss, B.E., Costanzi-Strauss, E., Krieger, J.E., Perez-Pomares, J.M., Xavier-Neto, J., Retinoic acid and VEGF delay smooth muscle relative to endothelial differentiation to coordinate inner and outer coronary vessel wall morphogenesis. Circ. Res. 107 (2010), 204–216.
6. Bernstein, B.E., Birney, E., Dunham, I., Green, E.D., Gunter, C., Snyder, M., An integrated encyclopedia of DNA elements in the human genome. Nature 489 (2012), 57–74.
7. Bertrand, N., Roux, M., Ryckebusch, L., Niederreither, K., Dolle, P., Moon, A., Capecchi, M., Zaffran, S., Hox genes define distinct progenitor sub-domains within the second heart field. Dev. Biol. 353 (2011), 266–274.
8. Bilbija, D., Haugen, F., Sagave, J., Baysa, A., Bastani, N., Levy, F.O., Sirsjo, A., Blomhoff, R., Valen, G., Retinoic acid signalling is activated in the postischemic heart and may influence remodelling. PLoS One, 7, 2012, e44740.
9. Billings, S.E., Pierzchalski, K., Butler Tjaden, N.E., Pang, X.Y., Trainor, P.A., Kane, M.A., Moise, A.R., The retinaldehyde reductase DHRS3 is essential for preventing the formation of excess retinoic acid during embryonic development. FASEB J. 27 (2013), 4877–4889.
10. Boergesen, M., Pedersen, T.A., Gross, B., van Heeringen, S.J., Hagenbeek, D., Bindesboll, C., Caron, S., Lalloyer, F., Steffensen, K.R., Nebb, H.I., Gustafsson, J.A., Stunnenberg, H.G., Staels, B., Mandrup, S., Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor alpha in mouse liver reveals extensive sharing of binding sites. Mol. Cell. Biol. 32 (2012), 852–867.
11. Boink, G.J., Christoffels, V.M., Robinson, R.B., Tan, H.L., The past, present, and future of pacemaker therapies. Trends Cardiovasc. Med. 25 (2015), 661–673.
12. Boudadi, E., Stower, H., Halsall, J.A., Rutledge, C.E., Leeb, M., Wutz, A., O'Neill, L.P., Nightingale, K.P., Turner, B.M., The histone deacetylase inhibitor sodium valproate causes limited transcriptional change in mouse embryonic stem cells but selectively overrides Polycomb-mediated Hoxb silencing. Epigenetics Chromatin., 6, 2013, 11.
13. Brade, T., Kumar, S., Cunningham, T.J., Chatzi, C., Zhao, X., Cavallero, S., Li, P., Sucov, H.M., Ruiz-Lozano, P., Duester, G., Retinoic acid stimulates myocardial expansion by induction of hepatic erythropoietin which activates epicardial Igf2. Development 138 (2011), 139–148.
14. Braitsch, C.M., Combs, M.D., Quaggin, S.E., Yutzey, K.E., Pod1/Tcf21 is regulated by retinoic acid signaling and inhibits differentiation of epicardium-derived cells into smooth muscle in the developing heart. Dev. Biol. 368 (2012), 345–357.
15. Briscoe, J., Small, S., Morphogen rules: design principles of gradient-mediated embryo patterning. Development 142 (2015), 3996–4009.
16. Bruneau, B.G., The developmental genetics of congenital heart disease. Nature 451 (2008), 943–948.
17. Bruneau, B.G., Nemer, G., Schmitt, J.P., Charron, F., Robitaille, L., Caron, S., Conner, D.A., Gessler, M., Nemer, M., Seidman, C.E., Seidman, J.G., A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106 (2001), 709–721.
18. Buckingham, M., Meilhac, S., Zaffran, S., Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 6 (2005), 826–835.
19. Cai, C.L., Liang, X., Shi, Y., Chu, P.H., Pfaff, S.L., Chen, J., Evans, S., Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 5 (2003), 877–889.
20. Cammas, L., Romand, R., Fraulob, V., Mura, C., Dolle, P., Expression of the murine retinol dehydrogenase 10 (Rdh10) gene correlates with many sites of retinoid signalling during embryogenesis and organ differentiation. Dev. Dyn. 236 (2007), 2899–2908.
21. Castello, A., Rodriguez-Manzaneque, J.C., Camps, M., Perez-Castillo, A., Testar, X., Palacin, M., Santos, A., Zorzano, A., Perinatal hypothyroidism impairs the normal transition of GLUT4 and GLUT1 glucose transporters from fetal to neonatal levels in heart and brown adipose tissue. Evidence for tissue-specific regulation of GLUT4 expression by thyroid hormone. J. Biol. Chem. 269 (1994), 5905–5912.
22. Chang, C.P., Stankunas, K., Shang, C., Kao, S.C., Twu, K.Y., Cleary, M.L., Pbx1 functions in distinct regulatory networks to pattern the great arteries and cardiac outflow tract. Development 135 (2008), 3577–3586.
23. Chatagnon, A., Veber, P., Morin, V., Bedo, J., Triqueneaux, G., Semon, M., Laudet, V., d'Alche-Buc, F., Benoit, G., RAR/RXR binding dynamics distinguish pluripotency from differentiation associated cis-regulatory elements. Nucleic Acids Res. 43 (2015), 4833–4854.
24. Chiba, H., Muramatsu, M., Nomoto, A., Kato, H., Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor. Nucleic Acids Res. 22 (1994), 1815–1820.
25. Chlon, T.M., Crispino, J.D., Combinatorial regulation of tissue specification by GATA and FOG factors. Development 139 (2012), 3905–3916.
26. Christoffels, V.M., Smits, G.J., Kispert, A., Moorman, A.F., Development of the pacemaker tissues of the heart. Circ. Res. 106 (2010), 240–254.
27. Clabby, M.L., Robison, T.A., Quigley, H.F., Wilson, D.B., Kelly, D.P., Retinoid X receptor alpha represses GATA-4-mediated transcription via a retinoid-dependent interaction with the cardiac-enriched repressor FOG-2. J. Biol. Chem. 278 (2003), 5760–5767.
28. Comptour, A., Rouzaire, M., Belville, C., Bouvier, D., Gallot, D., Blanchon, L., Sapin, V., Nuclear retinoid receptors and pregnancy: placental transfer, functions, and pharmacological aspects. Cell. Mol. Life Sci., 2016.
29. D'Aniello, E., Ravisankar, P., Waxman, J.S., Rdh10a Provides a Conserved Critical Step in the Synthesis of Retinoic Acid during Zebrafish Embryogenesis. PLoS One, 10, 2015, e0138588.
30. D'Aniello, E., Rydeen, A.B., Anderson, J.L., Mandal, A., Waxman, J.S., Depletion of retinoic acid receptors initiates a novel positive feedback mechanism that promotes teratogenic increases in retinoic acid. PLoS Genet., 9, 2013, e1003689.
31. D'Aniello, E., Waxman, J.S., Input overload: Contributions of retinoic acid signaling feedback mechanisms to heart development and teratogenesis. Dev. Dyn. 244 (2015), 513–523.
32. de Laat, W., Duboule, D., Topology of mammalian developmental enhancers and their regulatory landscapes. Nature 502 (2013), 499–506.
33. de The, H., Vivanco-Ruiz, M.M., Tiollais, P., Stunnenberg, H., Dejean, A., Identification of a retinoic acid responsive element in the retinoic acid receptor beta gene. Nature 343 (1990), 177–180.
34. Delacroix, L., Moutier, E., Altobelli, G., Legras, S., Poch, O., Choukrallah, M.A., Bertin, I., Jost, B., Davidson, I., Cell-specific interaction of retinoic acid receptors with target genes in mouse embryonic fibroblasts and embryonic stem cells. Mol. Cell. Biol. 30 (2010), 231–244.
35. Devalla, H.D., Schwach, V., Ford, J.W., Milnes, J.T., El-Haou, S., Jackson, C., Gkatzis, K., Elliott, D.A., Chuva de Sousa Lopes, S.M., Mummery, C.L., Verkerk, A.O., Passier, R., Atrial-like cardiomyocytes from human pluripotent stem cells are a robust preclinical model for assessing atrial-selective pharmacology. EMBO Mol Med. 7 (2015), 394–410.
36. Dickman, E.D., Smith, S.M., Selective regulation of cardiomyocyte gene expression and cardiac morphogenesis by retinoic acid. Dev. Dyn. 206 (1996), 39–48.
37. Diman, N.Y., Remacle, S., Bertrand, N., Picard, J.J., Zaffran, S., Rezsohazy, R., A retinoic acid responsive Hoxa3 transgene expressed in embryonic pharyngeal endoderm, cardiac neural crest and a subdomain of the second heart field. PLoS One, 6, 2011, e27624.
38. Dolle, P., Fraulob, V., Kastner, P., Chambon, P., Developmental expression of murine retinoid X receptor (RXR) genes. Mech. Dev. 45 (1994), 91–104.
39. Dolle, P., Ruberte, E., Leroy, P., Morriss-Kay, G., Chambon, P., Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 110 (1990), 1133–1151.
40. Dominguez, J.N., Meilhac, S.M., Bland, Y.S., Buckingham, M.E., Brown, N.A., Asymmetric fate of the posterior part of the second heart field results in unexpected left/right contributions to both poles of the heart. Circ. Res. 111 (2012), 1323–1335.
41. Dupe, V., Davenne, M., Brocard, J., Dolle, P., Mark, M., Dierich, A., Chambon, P., Rijli, F.M., In vivo functional analysis of the Hoxa-1 3′ retinoic acid response element (3′RARE). Development 124 (1997), 399–410.
42. Dupe, V., Matt, N., Garnier, J.M., Chambon, P., Mark, M., Ghyselinck, N.B., A newborn lethal defect due to inactivation of retinaldehyde dehydrogenase type 3 is prevented by maternal retinoic acid treatment. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 14036–14041.
43. Durand, B., Saunders, M., Leroy, P., Leid, M., Chambon, P., All-trans and 9-cis retinoic acid induction of CRABPII transcription is mediated by RAR-RXR heterodimers bound to DR1 and DR2 repeated motifs. Cell 71 (1992), 73–85.
44. Dyson, E., Sucov, H.M., Kubalak, S.W., Schmid-Schonbein, G.W., DeLano, F.A., Evans, R.M., Ross, J. Jr., Chien, K.R., Atrial-like phenotype is associated with embryonic ventricular failure in retinoid X receptor alpha −/− mice. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 7386–7390.
45. El Robrini, N., Etchevers, H.C., Ryckebusch, L., Faure, E., Eudes, N., Niederreither, K., Zaffran, S., Bertrand, N., Cardiac outflow morphogenesis depends on effects of retinoic acid signaling on multiple cell lineages. Dev. Dyn. 245 (2016), 388–401.
46. Emoto, Y., Wada, H., Okamoto, H., Kudo, A., Imai, Y., Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev. Biol. 278 (2005), 415–427.
47. Hale, F., The relation of vitamin A to anophthalmos in pigs. Am. J. Opthalmol. 18 (1935), 1087–1093.
48. Fahed, A.C., Gelb, B.D., Seidman, J.G., Seidman, C.E., Genetics of congenital heart disease: the glass half empty. Circ. Res. 112 (2013), 707–720.
49. Fan, X., Molotkov, A., Manabe, S., Donmoyer, C.M., Deltour, L., Foglio, M.H., Cuenca, A.E., Blaner, W.S., Lipton, S.A., Duester, G., Targeted disruption of Aldh1a1 (Raldh1) provides evidence for a complex mechanism of retinoic acid synthesis in the developing retina. Mol. Cell. Biol. 23 (2003), 4637–4648.
50. Feng, L., Hernandez, R.E., Waxman, J.S., Yelon, D., Moens, C.B., Dhrs3a regulates retinoic acid biosynthesis through a feedback inhibition mechanism. Dev. Biol. 338 (2010), 1–14.
51. Flajollet, S., Lefebvre, B., Cudejko, C., Staels, B., Lefebvre, P., The core component of the mammalian SWI/SNF complex SMARCD3/BAF60c is a coactivator for the nuclear retinoic acid receptor. Mol. Cell. Endocrinol. 270 (2007), 23–32.
52. Galli, D., Dominguez, J.N., Zaffran, S., Munk, A., Brown, N.A., Buckingham, M.E., Atrial myocardium derives from the posterior region of the second heart field, which acquires left-right identity as Pitx2c is expressed. Development 135 (2008), 1157–1167.
53. Gassanov, N., Er, F., Zagidullin, N., Jankowski, M., Gutkowska, J., Hoppe, U.C., Retinoid acid-induced effects on atrial and pacemaker cell differentiation and expression of cardiac ion channels. Differentiation 76 (2008), 971–980.
54. Gillespie, R.F., Gudas, L.J., Retinoid regulated association of transcriptional co-regulators and the polycomb group protein SUZ12 with the retinoic acid response elements of Hoxa1, RARbeta(2), and Cyp26A1 in F9 embryonal carcinoma cells. J. Mol. Biol. 372 (2007), 298–316.
55. Golzio, C., Martinovic-Bouriel, J., Thomas, S., Mougou-Zrelli, S., Grattagliano-Bessieres, B., Bonniere, M., Delahaye, S., Munnich, A., Encha-Razavi, F., Lyonnet, S., Vekemans, M., Attie-Bitach, T., Etchevers, H.C., Matthew-Wood syndrome is caused by truncating mutations in the retinol-binding protein receptor gene STRA6. Am. J. Hum. Genet. 80 (2007), 1179–1187.
56. Gruber, P.J., Kubalak, S.W., Pexieder, T., Sucov, H.M., Evans, R.M., Chien, K.R., RXR alpha deficiency confers genetic susceptibility for aortic sac, conotruncal, atrioventricular cushion, and ventricular muscle defects in mice. J. Clin. Invest. 98 (1996), 1332–1343.
57. Guadix, J.A., Ruiz-Villalba, A., Lettice, L., Velecela, V., Munoz-Chapuli, R., Hastie, N.D., Perez-Pomares, J.M., Martinez-Estrada, O.M., Wt1 controls retinoic acid signalling in embryonic epicardium through transcriptional activation of Raldh2. Development 138 (2011), 1093–1097.
58. Guillonneau, M., Jacqz-Aigrain, E., Teratogenic effects of vitamin A and its derivates. Arch. Pediatr. 4 (1997), 867–874.
59. Harrison, M.M., Jenkins, B.V., O'Connor-Giles, K.M., Wildonger, J., A CRISPR view of development. Genes Dev. 28 (2014), 1859–1872.
60. He, H., Chin, S., Zhuang, K., Hartong, R., Apriletti, J., Gick, G., Negative regulation of the rat Na-K-ATPase alpha 3-subunit gene promoter by thyroid hormone. Am. J. Phys. 271 (1996), C1750–C1756.
61. He, Y., Gong, L., Fang, Y., Zhan, Q., Liu, H.X., Lu, Y., Guo, G.L., Lehman-McKeeman, L., Fang, J., Wan, Y.J., The role of retinoic acid in hepatic lipid homeostasis defined by genomic binding and transcriptome profiling. BMC Genomics, 14, 2013, 575.
62. Hernandez, R.E., Putzke, A.P., Myers, J.P., Margaretha, L., Moens, C.B., Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development. Development 134 (2007), 177–187.
63. Hierck, B.P., Gittenberger-de Groot, A.C., van Iperen, L., Brouwer, A., Poelmann, R.E., Expression of the beta 4 integrin subunit in the mouse heart during embryonic development: retinoic acid advances beta 4 expression. Dev. Dyn. 207 (1996), 89–103.
64. Hochgreb, T., Linhares, V.L., Menezes, D.C., Sampaio, A.C., Yan, C.Y., Cardoso, W.V., Rosenthal, N., Xavier-Neto, J., A caudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field. Development 130 (2003), 5363–5374.
65. Huang, D., Chen, S.W., Langston, A.W., Gudas, L.J., A conserved retinoic acid responsive element in the murine Hoxb-1 gene is required for expression in the developing gut. Development 125 (1998), 3235–3246.
66. Huk, D.J., Hammond, H.L., Kegechika, H., Lincoln, J., Increased dietary intake of vitamin A promotes aortic valve calcification in vivo. Arterioscler. Thromb. Vasc. Biol. 33 (2013), 285–293.
67. Iyer, D., Gambardella, L., Bernard, W.G., Serrano, F., Mascetti, V.L., Pedersen, R.A., Sinha, S., Talasila, A., Robust derivation of epicardium and its differentiated smooth muscle cell progeny from human pluripotent stem cells. Development, 143, 2016, 904.
68. Janesick, A., Nguyen, T.T., Aisaki, K., Igarashi, K., Kitajima, S., Chandraratna, R.A., Kanno, J., Blumberg, B., Active repression by RARgamma signaling is required for vertebrate axial elongation. Development 141 (2014), 2260–2270.
69. Jenkins, K.J., Correa, A., Feinstein, J.A., Botto, L., Britt, A.E., Daniels, S.R., Elixson, M., Warnes, C.A., Webb, C.L., Noninherited risk factors and congenital cardiovascular defects: current knowledge: a scientific statement from the American Heart Association Council on Cardiovascular Disease in the Young: endorsed by the American Academy of Pediatrics. Circulation 115 (2007), 2995–3014.
70. Jonk, L.J., de Jonge, M.E., Vervaart, J.M., Wissink, S., Kruijer, W., Isolation and developmental expression of retinoic-acid-induced genes. Dev. Biol. 161 (1994), 604–614.
71. Kang, J.O., Sucov, H.M., Convergent proliferative response and divergent morphogenic pathways induced by epicardial and endocardial signaling in fetal heart development. Mech. Dev. 122 (2005), 57–65.
72. Kashyap, V., Gudas, L.J., Epigenetic regulatory mechanisms distinguish retinoic acid-mediated transcriptional responses in stem cells and fibroblasts. J. Biol. Chem. 285 (2010), 14534–14548.
73. Kastner, P., Grondona, J.M., Mark, M., Gansmuller, A., LeMeur, M., Decimo, D., Vonesch, J.L., Dolle, P., Chambon, P., Genetic analysis of RXR alpha developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 78 (1994), 987–1003.
74. Kawaguchi, R., Yu, J., Honda, J., Hu, J., Whitelegge, J., Ping, P., Wiita, P., Bok, D., Sun, H., A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 315 (2007), 820–825.
75. Keegan, B.R., Feldman, J.L., Begemann, G., Ingham, P.W., Yelon, D., Retinoic acid signaling restricts the cardiac progenitor pool. Science 307 (2005), 247–249.
76. Kelly, R.G., Brown, N.A., Buckingham, M.E., The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell 1 (2001), 435–440.
77. Kliewer, S.A., Umesono, K., Heyman, R.A., Mangelsdorf, D.J., Dyck, J.A., Evans, R.M., Retinoid X receptor-COUP-TF interactions modulate retinoic acid signaling. Proc. Natl. Acad. Sci. U. S. A. 89 (1992), 1448–1452.
78. Kostetskii, I., Yuan, S.Y., Kostetskaia, E., Linask, K.K., Blanchet, S., Seleiro, E., Michaille, J.J., Brickell, P., Zile, M., Initial retinoid requirement for early avian development coincides with retinoid receptor coexpression in the precardiac fields and induction of normal cardiovascular development. Dev. Dyn. 213 (1998), 188–198.
79. Kumar, S., Cunningham, T.J., Duester, G., Nuclear receptor corepressors Ncor1 and Ncor2 (Smrt) are required for retinoic acid-dependent repression of Fgf8 during somitogenesis. Dev. Biol., 2016.
80. Kumar, S., Duester, G., Retinoic acid controls body axis extension by directly repressing Fgf8 transcription. Development 141 (2014), 2972–2977.
81. Laforest, B., Bertrand, N., Zaffran, S., Genetic lineage tracing analysis of anterior Hox expressing cells. Methods Mol. Biol. 1196 (2014), 37–48.
82. Lalevee, S., Anno, Y.N., Chatagnon, A., Samarut, E., Poch, O., Laudet, V., Benoit, G., Lecompte, O., Rochette-Egly, C., Genome-wide in silico identification of new conserved and functional retinoic acid receptor response elements (direct repeats separated by 5 bp). J. Biol. Chem. 286 (2011), 33322–33334.
83. Lammer, E.J., Chen, D.T., Hoar, R.M., Agnish, N.D., Benke, P.J., Braun, J.T., Curry, C.J., Fernhoff, P.M., Grix, A.W. Jr., Lott, I.T., et al. Retinoic acid embryopathy. N. Engl. J. Med. 313 (1985), 837–841.
84. Lampron, C., Rochette-Egly, C., Gorry, P., Dolle, P., Mark, M., Lufkin, T., LeMeur, M., Chambon, P., Mice deficient in cellular retinoic acid binding protein II (CRABPII) or in both CRABPI and CRABPII are essentially normal. Development 121 (1995), 539–548.
85. Langston, A.W., Thompson, J.R., Gudas, L.J., Retinoic acid-responsive enhancers located 3′ of the Hox A and Hox B homeobox gene clusters. Functional analysis. J. Biol. Chem. 272 (1997), 2167–2175.
86. LaRosa, G.J., Gudas, L.J., Early retinoic acid-induced F9 teratocarcinoma stem cell gene ERA-1: alternate splicing creates transcripts for a homeobox-containing protein and one lacking the homeobox. Mol. Cell. Biol. 8 (1988), 3906–3917.
87. Lavine, K.J., Yu, K., White, A.C., Zhang, X., Smith, C., Partanen, J., Ornitz, D.M., Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell 8 (2005), 85–95.
88. Lee, E.R., Murdoch, F.E., Fritsch, M.K., High histone acetylation and decreased polycomb repressive complex 2 member levels regulate gene specific transcriptional changes during early embryonic stem cell differentiation induced by retinoic acid. Stem Cells 25 (2007), 2191–2199.
89. Leroy, P., Nakshatri, H., Chambon, P., Mouse retinoic acid receptor alpha 2 isoform is transcribed from a promoter that contains a retinoic acid response element. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 10138–10142.
90. Lescroart, F., Mohun, T., Meilhac, S.M., Bennett, M., Buckingham, M., Lineage tree for the venous pole of the heart: clonal analysis clarifies controversial genealogy based on genetic tracing. Circ. Res. 111 (2012), 1313–1322.
91. Li, E., Sucov, H.M., Lee, K.F., Evans, R.M., Jaenisch, R., Normal development and growth of mice carrying a targeted disruption of the alpha 1 retinoic acid receptor gene. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 1590–1594.
92. Li, P., Pashmforoush, M., Sucov, H.M., Retinoic acid regulates differentiation of the secondary heart field and TGFbeta-mediated outflow tract septation. Dev. Cell 18 (2010), 480–485.
93. Liang, X., Evans, S.M., Sun, Y., Insights into cardiac conduction system formation provided by HCN4 expression. Trends Cardiovasc. Med. 25 (2015), 1–9.
94. Liberatore, C.M., Searcy-Schrick, R.D., Yutzey, K.E., Ventricular expression of tbx5 inhibits normal heart chamber development. Dev. Biol. 223 (2000), 169–180.
95. Lin, S.C., Dolle, P., Ryckebusch, L., Noseda, M., Zaffran, S., Schneider, M.D., Niederreither, K., Endogenous retinoic acid regulates cardiac progenitor differentiation. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 9234–9239.
96. Lohnes, D., Kastner, P., Dierich, A., Mark, M., LeMeur, M., Chambon, P., Function of retinoic acid receptor gamma in the mouse. Cell 73 (1993), 643–658.
97. Loudig, O., Maclean, G.A., Dore, N.L., Luu, L., Petkovich, M., Transcriptional co-operativity between distant retinoic acid response elements in regulation of Cyp26A1 inducibility. Biochem. J. 392 (2005), 241–248.
98. Lufkin, T., Lohnes, D., Mark, M., Dierich, A., Gorry, P., Gaub, M.P., LeMeur, M., Chambon, P., High postnatal lethality and testis degeneration in retinoic acid receptor alpha mutant mice. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 7225–7229.
99. MacLean, G., Abu-Abed, S., Dolle, P., Tahayato, A., Chambon, P., Petkovich, M., Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech. Dev. 107 (2001), 195–201.
100. Mahmood, R., Flanders, K.C., Morriss-Kay, G.M., Interactions between retinoids and TGF beta s in mouse morphogenesis. Development 115 (1992), 67–74.
101. Mahony, S., Mazzoni, E.O., McCuine, S., Young, R.A., Wichterle, H., Gifford, D.K., Ligand-dependent dynamics of retinoic acid receptor binding during early neurogenesis. Genome Biol., 12, 2011, R2.
102. Makki, N., Capecchi, M.R., Cardiovascular defects in a mouse model of HOXA1 syndrome. Hum. Mol. Genet. 21 (2012), 26–31.
103. Mark, M., Ghyselinck, N.B., Chambon, P., Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu. Rev. Pharmacol. Toxicol. 46 (2006), 451–480.
104. Marshall, H., Studer, M., Popperl, H., Aparicio, S., Kuroiwa, A., Brenner, S., Krumlauf, R., A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature 370 (1994), 567–571.
105. Mendelsohn, C., Lohnes, D., Decimo, D., Lufkin, T., LeMeur, M., Chambon, P., Mark, M., Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120 (1994), 2749–2771.
106. Mendoza-Parra, M.A., Walia, M., Sankar, M., Gronemeyer, H., Dissecting the retinoid-induced differentiation of F9 embryonal stem cells by integrative genomics. Mol. Syst. Biol., 7, 2011, 538.
107. Merki, E., Zamora, M., Raya, A., Kawakami, Y., Wang, J., Zhang, X., Burch, J., Kubalak, S.W., Kaliman, P., Izpisua Belmonte, J.C., Chien, K.R., Ruiz-Lozano, P., Epicardial retinoid X receptor alpha is required for myocardial growth and coronary artery formation. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 18455–18460.
108. Metzger, D., Chambon, P., Contribution of targeted conditional somatic mutagenesis to deciphering retinoid X receptor functions and to generating mouse models of human diseases. Handb. Exp. Pharmacol., 2007, 511–524.
109. Mic, F.A., Haselbeck, R.J., Cuenca, A.E., Duester, G., Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 129 (2002), 2271–2282.
110. Mic, F.A., Molotkov, A., Fan, X., Cuenca, A.E., Duester, G., RALDH3, a retinaldehyde dehydrogenase that generates retinoic acid, is expressed in the ventral retina, otic vesicle and olfactory pit during mouse development. Mech. Dev. 97 (2000), 227–230.
111. Miyake, N., Mizuno, S., Okamoto, N., Ohashi, H., Shiina, M., Ogata, K., Tsurusaki, Y., Nakashima, M., Saitsu, H., Niikawa, N., Matsumoto, N., KDM6A point mutations cause Kabuki syndrome. Hum. Mutat. 34 (2013), 108–110.
112. Molkentin, J.D., Kalvakolanu, D.V., Markham, B.E., Transcription factor GATA-4 regulates cardiac muscle-specific expression of the alpha-myosin heavy-chain gene. Mol. Cell. Biol. 14 (1994), 4947–4957.
113. Molotkova, N., Molotkov, A., Duester, G., Role of retinoic acid during forebrain development begins late when Raldh3 generates retinoic acid in the ventral subventricular zone. Dev. Biol. 303 (2007), 601–610.
114. Moorman, A.F., Christoffels, V.M., Cardiac chamber formation: development, genes, and evolution. Physiol. Rev. 83 (2003), 1223–1267.
115. Mori, A.D., Zhu, Y., Vahora, I., Nieman, B., Koshiba-Takeuchi, K., Davidson, L., Pizard, A., Seidman, J.G., Seidman, C.E., Chen, X.J., Henkelman, R.M., Bruneau, B.G., Tbx5-dependent rheostatic control of cardiac gene expression and morphogenesis. Dev. Biol. 297 (2006), 566–586.
116. Moss, J.B., Xavier-Neto, J., Shapiro, M.D., Nayeem, S.M., McCaffery, P., Drager, U.C., Rosenthal, N., Dynamic patterns of retinoic acid synthesis and response in the developing mammalian heart. Dev. Biol. 199 (1998), 55–71.
117. Moutier, E., Ye, T., Choukrallah, M.A., Urban, S., Osz, J., Chatagnon, A., Delacroix, L., Langer, D., Rochel, N., Moras, D., Benoit, G., Davidson, I., Retinoic acid receptors recognize the mouse genome through binding elements with diverse spacing and topology. J. Biol. Chem. 287 (2012), 26328–26341.
118. Nagy, L., Kao, H.Y., Chakravarti, D., Lin, R.J., Hassig, C.A., Ayer, D.E., Schreiber, S.L., Evans, R.M., Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 89 (1997), 373–380.
119. Nam, Y.J., Lubczyk, C., Bhakta, M., Zang, T., Fernandez-Perez, A., McAnally, J., Bassel-Duby, R., Olson, E.N., Munshi, N.V., Induction of diverse cardiac cell types by reprogramming fibroblasts with cardiac transcription factors. Development 141 (2014), 4267–4278.
120. Niederreither, K., Abu-Abed, S., Schuhbaur, B., Petkovich, M., Chambon, P., Dolle, P., Genetic evidence that oxidative derivatives of retinoic acid are not involved in retinoid signaling during mouse development. Nat. Genet. 31 (2002), 84–88.
121. Niederreither, K., Dolle, P., Retinoic acid in development: towards an integrated view. Nat. Rev. Genet. 9 (2008), 541–553.
122. Niederreither, K., Fraulob, V., Garnier, J.M., Chambon, P., Dolle, P., Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech. Dev. 110 (2002), 165–171.
123. Niederreither, K., McCaffery, P., Drager, U.C., Chambon, P., Dolle, P., Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech. Dev. 62 (1997), 67–78.
124. Niederreither, K., Subbarayan, V., Dolle, P., Chambon, P., Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 21 (1999), 444–448.
125. Niederreither, K., Vermot, J., Le Roux, I., Schuhbaur, B., Chambon, P., Dolle, P., The regional pattern of retinoic acid synthesis by RALDH2 is essential for the development of posterior pharyngeal arches and the enteric nervous system. Development 130 (2003), 2525–2534.
126. Niederreither, K., Vermot, J., Messaddeq, N., Schuhbaur, B., Chambon, P., Dolle, P., Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development 128 (2001), 1019–1031.
127. Nolte, C., Jinks, T., Wang, X., Martinez Pastor, M.T., Krumlauf, R., Shadow enhancers flanking the HoxB cluster direct dynamic Hox expression in early heart and endoderm development. Dev. Biol. 383 (2013), 158–173.
128. Norden, J., Grieskamp, T., Lausch, E., van Wijk, B., van den Hoff, M.J., Englert, C., Petry, M., Mommersteeg, M.T., Christoffels, V.M., Niederreither, K., Kispert, A., Wt1 and retinoic acid signaling in the subcoelomic mesenchyme control the development of the pleuropericardial membranes and the sinus horns. Circ. Res. 106 (2010), 1212–1220.
129. Oosterveen, T., van Vliet, P., Deschamps, J., Meijlink, F., The direct context of a hox retinoic acid response element is crucial for its activity. J. Biol. Chem. 278 (2003), 24103–24107.
130. Osmond, M.K., Butler, A.J., Voon, F.C., Bellairs, R., The effects of retinoic acid on heart formation in the early chick embryo. Development 113 (1991), 1405–1417.
131. Paige, S.L., Thomas, S., Stoick-Cooper, C.L., Wang, H., Maves, L., Sandstrom, R., Pabon, L., Reinecke, H., Pratt, G., Keller, G., Moon, R.T., Stamatoyannopoulos, J., Murry, C.E., A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell 151 (2012), 221–232.
132. Pasutto, F., Sticht, H., Hammersen, G., Gillessen-Kaesbach, G., Fitzpatrick, D.R., Nurnberg, G., Brasch, F., Schirmer-Zimmermann, H., Tolmie, J.L., Chitayat, D., Houge, G., Fernandez-Martinez, L., Keating, S., Mortier, G., Hennekam, R.C., von der Wense, A., Slavotinek, A., Meinecke, P., Bitoun, P., Becker, C., Nurnberg, P., Reis, A., Rauch, A., Mutations in STRA6 cause a broad spectrum of malformations including anophthalmia, congenital heart defects, diaphragmatic hernia, alveolar capillary dysplasia, lung hypoplasia, and mental retardation. Am. J. Hum. Genet. 80 (2007), 550–560.
133. Pavan, M., Ruiz, V.F., Silva, F.A., Sobreira, T.J., Cravo, R.M., Vasconcelos, M., Marques, L.P., Mesquita, S.M., Krieger, J.E., Lopes, A.A., Oliveira, P.S., Pereira, A.C., Xavier-Neto, J., ALDH1A2 (RALDH2) genetic variation in human congenital heart disease. BMC Med. Genet., 10, 2009, 113.
134. Pereira, F.A., Qiu, Y., Zhou, G., Tsai, M.J., Tsai, S.Y., The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. Genes Dev. 13 (1999), 1037–1049.
135. Perez-Pomares, J.M., Phelps, A., Sedmerova, M., Carmona, R., Gonzalez-Iriarte, M., Munoz-Chapuli, R., Wessels, A., Experimental studies on the spatiotemporal expression of WT1 and RALDH2 in the embryonic avian heart: a model for the regulation of myocardial and valvuloseptal development by epicardially derived cells (EPDCs). Dev. Biol. 247 (2002), 307–326.
136. Prendiville, T., Jay, P.Y., Pu, W.T., Insights into the genetic structure of congenital heart disease from human and murine studies on monogenic disorders. Cold Spring Harb. Perspect. Med., 4, 2014.
137. Rana, M.S., Theveniau-Ruissy, M., De Bono, C., Mesbah, K., Francou, A., Rammah, M., Dominguez, J.N., Roux, M., Laforest, B., Anderson, R.H., Mohun, T., Zaffran, S., Christoffels, V.M., Kelly, R.G., Tbx1 coordinates addition of posterior second heart field progenitor cells to the arterial and venous poles of the heart. Circ. Res. 115 (2014), 790–799.
138. Ratajska, A., Zlotorowicz, R., Blazejczyk, M., Wasiutynski, A., Coronary artery embryogenesis in cardiac defects induced by retinoic acid in mice. Birth Defects Res. A Clin. Mol. Teratol. 73 (2005), 966–979.
139. Rhinn, M., Dolle, P., Retinoic acid signalling during development. Development 139 (2012), 843–858.
140. Rhinn, M., Schuhbaur, B., Niederreither, K., Dolle, P., Involvement of retinol dehydrogenase 10 in embryonic patterning and rescue of its loss of function by maternal retinaldehyde treatment. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 16687–16692.
141. Roberts, C., Ivins, S., Cook, A.C., Baldini, A., Scambler, P.J., Cyp26 genes a1, b1 and c1 are down-regulated in Tbx1 null mice and inhibition of Cyp26 enzyme function produces a phenocopy of DiGeorge Syndrome in the chick. Hum. Mol. Genet. 15 (2006), 3394–3410.
142. Rohrer, D.K., Hartong, R., Dillmann, W.H., Influence of thyroid hormone and retinoic acid on slow sarcoplasmic reticulum Ca2 + ATPase and myosin heavy chain alpha gene expression in cardiac myocytes. Delineation of cis-active DNA elements that confer responsiveness to thyroid hormone but not to retinoic acid. J. Biol. Chem. 266 (1991), 8638–8646.
143. Romand, R., Kondo, T., Cammas, L., Hashino, E., Dolle, P., Dynamic expression of the retinoic acid-synthesizing enzyme retinol dehydrogenase 10 (rdh10) in the developing mouse brain and sensory organs. J. Comp. Neurol. 508 (2008), 879–892.
144. Rousseau, E., Michaud, C., Lefebvre, D., Proteau, S., Decrouy, A., Reconstitution of ionic channels from inner and outer membranes of mammalian cardiac nuclei. Biophys. J. 70 (1996), 703–714.
145. Ruberte, E., Dolle, P., Chambon, P., Morriss-Kay, G., Retinoic acid receptors and cellular retinoid binding proteins. II. Their differential pattern of transcription during early morphogenesis in mouse embryos. Development 111 (1991), 45–60.
146. Ruberte, E., Dolle, P., Krust, A., Zelent, A., Morriss-Kay, G., Chambon, P., Specific spatial and temporal distribution of retinoic acid receptor gamma transcripts during mouse embryogenesis. Development 108 (1990), 213–222.
147. Ryckebusch, L., Wang, Z., Bertrand, N., Lin, S.C., Chi, X., Schwartz, R., Zaffran, S., Niederreither, K., Retinoic acid deficiency alters second heart field formation. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 2913–2918.
148. Rydeen, A.B., Waxman, J.S., Cyp26 enzymes are required to balance the cardiac and vascular lineages within the anterior lateral plate mesoderm. Development 141 (2014), 1638–1648.
149. Sakabe, M., Kokubo, H., Nakajima, Y., Saga, Y., Ectopic retinoic acid signaling affects outflow tract cushion development through suppression of the myocardial Tbx2-Tgfbeta2 pathway. Development 139 (2012), 385–395.
150. Sakai, Y., Meno, C., Fujii, H., Nishino, J., Shiratori, H., Saijoh, Y., Rossant, J., Hamada, H., The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes Dev. 15 (2001), 213–225.
151. Sandell, L.L., Lynn, M.L., Inman, K.E., McDowell, W., Trainor, P.A., RDH10 oxidation of Vitamin A is a critical control step in synthesis of retinoic acid during mouse embryogenesis. PLoS One, 7, 2012, e30698.
152. Sandell, L.L., Sanderson, B.W., Moiseyev, G., Johnson, T., Mushegian, A., Young, K., Rey, J.P., Ma, J.X., Staehling-Hampton, K., Trainor, P.A., RDH10 is essential for synthesis of embryonic retinoic acid and is required for limb, craniofacial, and organ development. Genes Dev. 21 (2007), 1113–1124.
153. Schilling, T.F., Nie, Q., Lander, A.D., Dynamics and precision in retinoic acid morphogen gradients. Curr. Opin. Genet. Dev. 22 (2012), 562–569.
154. Shimozono, S., Iimura, T., Kitaguchi, T., Higashijima, S., Miyawaki, A., Visualization of an endogenous retinoic acid gradient across embryonic development. Nature 496 (2013), 363–366.
155. Sirbu, I.O., Zhao, X., Duester, G., Retinoic acid controls heart anteroposterior patterning by down-regulating Isl1 through the Fgf8 pathway. Dev. Dyn. 237 (2008), 1627–1635.
156. Smith, S.M., Dickman, E.D., Thompson, R.P., Sinning, A.R., Wunsch, A.M., Markwald, R.R., Retinoic acid directs cardiac laterality and the expression of early markers of precardiac asymmetry. Dev. Biol. 182 (1997), 162–171.
157. Smith, W.C., Nakshatri, H., Leroy, P., Rees, J., Chambon, P., A retinoic acid response element is present in the mouse cellular retinol binding protein I (mCRBPI) promoter. EMBO J. 10 (1991), 2223–2230.
158. Snarr, B.S., O'Neal, J.L., Chintalapudi, M.R., Wirrig, E.E., Phelps, A.L., Kubalak, S.W., Wessels, A., Isl1 expression at the venous pole identifies a novel role for the second heart field in cardiac development. Circ. Res. 101 (2007), 971–974.
159. Sommer, A., Tarwotjo, I., Djunaedi, E., West, K.P. Jr., Loeden, A.A., Tilden, R., Mele, L., Impact of vitamin A supplementation on childhood mortality. A randomised controlled community trial. Lancet 1 (1986), 1169–1173.
160. Sorrell, M.R., Waxman, J.S., Restraint of Fgf8 signaling by retinoic acid signaling is required for proper heart and forelimb formation. Dev. Biol. 358 (2011), 44–55.
161. Stankunas, K., Shang, C., Twu, K.Y., Kao, S.C., Jenkins, N.A., Copeland, N.G., Sanyal, M., Selleri, L., Cleary, M.L., Chang, C.P., Pbx/Meis deficiencies demonstrate multigenetic origins of congenital heart disease. Circ. Res. 103 (2008), 702–709.
162. Stefanovic, S., Christoffels, V.M., GATA-dependent transcriptional and epigenetic control of cardiac lineage specification and differentiation. Cell. Mol. Life Sci. 72 (2015), 3871–3881.
163. Strate, I., Min, T.H., Iliev, D., Pera, E.M., Retinol dehydrogenase 10 is a feedback regulator of retinoic acid signalling during axis formation and patterning of the central nervous system. Development 136 (2009), 461–472.
164. Stuckmann, I., Evans, S., Lassar, A.B., Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation. Dev. Biol. 255 (2003), 334–349.
165. Studer, M., Popperl, H., Marshall, H., Kuroiwa, A., Krumlauf, R., Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science 265 (1994), 1728–1732.
166. Sucov, H.M., Dyson, E., Gumeringer, C.L., Price, J., Chien, K.R., Evans, R.M., RXR alpha mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev. 8 (1994), 1007–1018.
167. Tsuda, T., Philp, N., Zile, M.H., Linask, K.K., Left-right asymmetric localization of flectin in the extracellular matrix during heart looping. Dev. Biol. 173 (1996), 39–50.
168. Uehara, M., Yashiro, K., Mamiya, S., Nishino, J., Chambon, P., Dolle, P., Sakai, Y., CYP26A1 and CYP26C1 cooperatively regulate anterior-posterior patterning of the developing brain and the production of migratory cranial neural crest cells in the mouse. Dev. Biol. 302 (2007), 399–411.
169. Underwood, B.A., Vitamin A deficiency disorders: international efforts to control a preventable “pox”. J. Nutr. 134 (2004), 231S–236S.
170. Vakoc, C.R., Letting, D.L., Gheldof, N., Sawado, T., Bender, M.A., Groudine, M., Weiss, M.J., Dekker, J., Blobel, G.A., Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1. Mol. Cell 17 (2005), 453–462.
171. van der Wees, J., Matharu, P.J., de Roos, K., Destree, O.H., Godsave, S.F., Durston, A.J., Sweeney, G.E., Developmental expression and differential regulation by retinoic acid of Xenopus COUP-TF-A and COUP-TF-B. Mech. Dev. 54 (1996), 173–184.
172. Vilhais-Neto, G.C., Maruhashi, M., Smith, K.T., Vasseur-Cognet, M., Peterson, A.S., Workman, J.L., Pourquie, O., Rere controls retinoic acid signalling and somite bilateral symmetry. Nature 463 (2010), 953–957.
173. Vissers, L.E., van Ravenswaaij, C.M., Admiraal, R., Hurst, J.A., de Vries, B.B., Janssen, I.M., van der Vliet, W.A., Huys, E.H., de Jong, P.J., Hamel, B.C., Schoenmakers, E.F., Brunner, H.G., Veltman, J.A., van Kessel, A.G., Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat. Genet. 36 (2004), 955–957.
174. Vitobello, A., Ferretti, E., Lampe, X., Vilain, N., Ducret, S., Ori, M., Spetz, J.F., Selleri, L., Rijli, F.M., Hox and Pbx factors control retinoic acid synthesis during hindbrain segmentation. Dev. Cell 20 (2011), 469–482.
175. von Gise, A., Zhou, B., Honor, L.B., Ma, Q., Petryk, A., Pu, W.T., WT1 regulates epicardial epithelial to mesenchymal transition through beta-catenin and retinoic acid signaling pathways. Dev. Biol. 356 (2011), 421–431.
176. Waardenberg, A.J., Homan, B., Mohamed, S., Harvey, R.P., Bouveret, R., Prediction and validation of protein-protein interactors from genome-wide DNA-binding data using a knowledge-based machine-learning approach. Open Biol., 6, 2016.
177. Wamstad, J.A., Alexander, J.M., Truty, R.M., Shrikumar, A., Li, F., Eilertson, K.E., Ding, H., Wylie, J.N., Pico, A.R., Capra, J.A., Erwin, G., Kattman, S.J., Keller, G.M., Srivastava, D., Levine, S.S., Pollard, K.S., Holloway, A.K., Boyer, L.A., Bruneau, B.G., Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 151 (2012), 206–220.
178. Wang, G.F., Nikovits, W. Jr., Bao, Z.Z., Stockdale, F.E., Irx4 forms an inhibitory complex with the vitamin D and retinoic X receptors to regulate cardiac chamber-specific slow MyHC3 expression. J. Biol. Chem. 276 (2001), 28835–28841.
179. Wang, G.F., Nikovits, W. Jr., Schleinitz, M., Stockdale, F.E., A positive GATA element and a negative vitamin D receptor-like element control atrial chamber-specific expression of a slow myosin heavy-chain gene during cardiac morphogenesis. Mol. Cell. Biol. 18 (1998), 6023–6034.
180. Weston, A.D., Blumberg, B., Underhill, T.M., Active repression by unliganded retinoid receptors in development: less is sometimes more. J. Cell Biol. 161 (2003), 223–228.
181. White, R.J., Schilling, T.F., How degrading: Cyp26s in hindbrain development. Dev. Dyn. 237 (2008), 2775–2790.
182. Wiens, D.J., Mann, T.K., Fedderson, D.E., Rathmell, W.K., Franck, B.H., Early heart development in the chick embryo: effects of isotretinoin on cell proliferation, alpha-actin synthesis, and development of contractions. Differentiation 51 (1992), 105–112.
183. Wilson, J.G., Roth, C.B., Warkany, J., An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am. J. Anat. 92 (1953), 189–217.
184. Wilson, J.G., Warkany, J., Congenital anomalies of heart and great vessels in offspring of vitamin A-deficient rats. Am. J. Dis. Child., 79, 1950, 963.
185. Wobus, A.M., Kaomei, G., Shan, J., Wellner, M.C., Rohwedel, J., Ji, G., Fleischmann, B., Katus, H.A., Hescheler, J., Franz, W.M., Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 29 (1997), 1525–1539.
186. Wu, J., Garami, M., Cheng, T., Gardner, D.G., 1,25(OH)2 vitamin D3, and retinoic acid antagonize endothelin-stimulated hypertrophy of neonatal rat cardiac myocytes. J. Clin. Invest. 97 (1996), 1577–1588.
187. Wu, S.P., Cheng, C.M., Lanz, R.B., Wang, T., Respress, J.L., Ather, S., Chen, W., Tsai, S.J., Wehrens, X.H., Tsai, M.J., Tsai, S.Y., Atrial identity is determined by a COUP-TfiI regulatory network. Dev. Cell 25 (2013), 417–426.
188. Xavier-Neto, J., Neville, C.M., Shapiro, M.D., Houghton, L., Wang, G.F., Nikovits, W. Jr., Stockdale, F.E., Rosenthal, N., A retinoic acid-inducible transgenic marker of sino-atrial development in the mouse heart. Development 126 (1999), 2677–2687.
189. Xavier-Neto, J., Shapiro, M.D., Houghton, L., Rosenthal, N., Sequential programs of retinoic acid synthesis in the myocardial and epicardial layers of the developing avian heart. Dev. Biol. 219 (2000), 129–141.
190. Xavier-Neto, J., Sousa Costa, A.M., Figueira, A.C., Caiaffa, C.D., Amaral, F.N., Peres, L.M., da Silva, B.S., Santos, L.N., Moise, A.R., Castillo, H.A., Signaling through retinoic acid receptors in cardiac development: Doing the right things at the right times. Biochim. Biophys. Acta 1849 (2015), 94–111.
191. Yasmin, R., Yeung, K.T., Chung, R.H., Gaczynska, M.E., Osmulski, P.A., Noy, N., DNA-looping by RXR tetramers permits transcriptional regulation “at a distance”. J. Mol. Biol. 343 (2004), 327–338.
192. Yasui, H., Nakazawa, M., Morishima, M., Miyagawa-Tomita, S., Momma, K., Morphological observations on the pathogenetic process of transposition of the great arteries induced by retinoic acid in mice. Circulation 91 (1995), 2478–2486.
193. Yutzey, K.E., Rhee, J.T., Bader, D., Expression of the atrial-specific myosin heavy chain AMHC1 and the establishment of anteroposterior polarity in the developing chicken heart. Development 120 (1994), 871–883.
194. Zaffran, S., Kelly, R.G., New developments in the second heart field. Differentiation 84 (2012), 17–24.
195. Zaffran, S., Kelly, R.G., Meilhac, S.M., Buckingham, M.E., Brown, N.A., Right ventricular myocardium derives from the anterior heart field. Circ. Res. 95 (2004), 261–268.
196. Zaidi, S., Choi, M., Wakimoto, H., Ma, L., Jiang, J., Overton, J.D., Romano-Adesman, A., Bjornson, R.D., Breitbart, R.E., Brown, K.K., Carriero, N.J., Cheung, Y.H., Deanfield, J., DePalma, S., Fakhro, K.A., Glessner, J., Hakonarson, H., Italia, M.J., Kaltman, J.R., Kaski, J., Kim, R., Kline, J.K., Lee, T., Leipzig, J., Lopez, A., Mane, S.M., Mitchell, L.E., Newburger, J.W., Parfenov, M., Pe'er, I., Porter, G., Roberts, A.E., Sachidanandam, R., Sanders, S.J., Seiden, H.S., State, M.W., Subramanian, S., Tikhonova, I.R., Wang, W., Warburton, D., White, P.S., Williams, I.A., Zhao, H., Seidman, J.G., Brueckner, M., Chung, W.K., Gelb, B.D., Goldmuntz, E., Seidman, C.E., Lifton, R.P., De novo mutations in histone-modifying genes in congenital heart disease. Nature 498 (2013), 220–223.
197. Zhang, Q., Jiang, J., Han, P., Yuan, Q., Zhang, J., Zhang, X., Xu, Y., Cao, H., Meng, Q., Chen, L., Tian, T., Wang, X., Li, P., Hescheler, J., Ji, G., Ma, Y., Direct differentiation of atrial and ventricular myocytes from human embryonic stem cells by alternating retinoid signals. Cell Res. 21 (2011), 579–587.
198. Zhou, M.D., Sucov, H.M., Evans, R.M., Chien, K.R., Retinoid-dependent pathways suppress myocardial cell hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 7391–7395.
199. Zile, M.H., Vitamin A-not for your eyes only: requirement for heart formation begins early in embryogenesis. Nutrients 2 (2010), 532–550.