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Retinoic Acid-Regulated Target Genes During Development: Integrative Genomics Analysis

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The Biochemistry of Retinoid Signaling III

Part of the book series: Subcellular Biochemistry ((SCBI,volume 95))

Abstract

Retinoic acid (RA), a major natural active metabolite of vitamin A (VA) is well known to play critical roles in embryonic development. The effects of RA are mediated by nuclear receptors (RARs), which regulate the expression of gene batteries involved in cell growth and differentiation. Since the early 1990s several laboratories have focused on understanding how RA-regulated genes and RAR binding sites operate by studying the differentiation of embryonal carcinoma cells and embryonic stem cells. The development of hybridization-based microarray technology and high performance software analysis programs has allowed the characterization of thousands of RA-regulated genes. During the two last decades, publication of the genome sequence of various organisms has allowed advances in massive parallel sequencing and bioinformatics analysis of genome-wide data sets. These new generation sequencing (NGS) technologies have revolutionized the field by providing a global integrated picture of RA-regulated gene networks and the regulatory programs involved in cell fate decisions during embryonal carcinoma and embryonic stem cells differentiation. Now the challenge is to reconstruct the RA-regulated gene networks at the single cell level during the development of specialized embryonic tissues.

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Abbreviations

CRABP:

Cellular Retinoic Acid Binding Protein

ChIP:

Chromatin Immunoprecipitation

ChIp-Chip:

ChIP-on-chip

ChIP-seq:

ChIP coupled to massive parallel sequencing

DNA-chip:

DNA microarrays

ECC:

Embryonal carcinoma cell

ESC:

Embryonic Stem Cell

KO:

Knock Out

NGS:

Next Generation Sequencing

PCR:

Polymerase Chain Reaction

RT-PCR:

Reverse Transcriptase PCR

qPCR:

Quantitative PCR

RNA-seq:

RNA sequencing (whole transcriptome sequencing using NGS)

RA:

Retinoic Acid

RAR:

Retinoic Acid Receptor

RARE:

Retinoic Acid Response Element

RXR:

Retinoid X Receptor

TF:

Transcription factor

Transcriptome:

All transcribed RNAs produced in one or a population of cells

VAD:

Vitamin A deficiency

WT:

Wild Type

References

  • Akanuma H, Qin XY, Nagano R, Win-Shwe TT, Imanishi S, Zaha H, Yoshinaga J, Fukuda T, Ohsako S, Sone H (2012) Identification of stage-specific gene expression signatures in response to retinoic acid during the neural differentiation of mouse embryonic stem cells. Front Genet 3:141

    Article  PubMed  PubMed Central  Google Scholar 

  • Al Tanoury Z, Gaouar S, Piskunov A, Ye T, Urban S, Jost B, Keime C, Davidson I, Dierich A, Rochette-Egly C (2014) Phosphorylation of the retinoic acid receptor RARgamma2 is crucial for the neuronal differentiation of mouse embryonic stem cells. J Cell Sci 127:2095–2105

    Article  CAS  PubMed  Google Scholar 

  • Al Tanoury Z, Piskunov A, Rochette-Egly C (2013) Vitamin A and retinoid signaling: genomic and nongenomic effects: thematic review series: fat-soluble vitamins: vitamin A. J Lipid Res 54:1761–1775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altmann CR, Bell E, Sczyrba A, Pun J, Bekiranov S, Gaasterland T, Brivanlou AH (2001) Microarray-based analysis of early development in Xenopus laevis. Dev Biol 236:64–75

    Article  CAS  PubMed  Google Scholar 

  • Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP (2002) Gene expression during the life cycle of Drosophila melanogaster. Science 297:2270–2275

    Article  CAS  PubMed  Google Scholar 

  • Arima K, Shiotsugu J, Niu R, Khandpur R, Martinez M, Shin Y, Koide T, Cho KW, Kitayama A, Ueno N, Chandraratna RA, Blumberg B (2005) Global analysis of RAR-responsive genes in the Xenopus neurula using cDNA microarrays. Dev Dyn 232:414–431

    Article  CAS  PubMed  Google Scholar 

  • Bakken TE, Hodge RD, Miller JA, Yao Z, Nguyen TN, Aevermann B, Barkan E, Bertagnolli D, Casper T, Dee N, Garren E, Goldy J, Graybuck LT, Kroll M, Lasken RS, Lathia K, Parry S, Rimorin C, Scheuermann RH, Schork NJ et al (2018) Single-nucleus and single-cell transcriptomes compared in matched cortical cell types. PLoS ONE 13:e0209648

    Article  PubMed  PubMed Central  Google Scholar 

  • Balmer JE, Blomhoff R (2002) Gene expression regulation by retinoic acid. J Lipid Res 43:1773–1808

    Article  CAS  PubMed  Google Scholar 

  • Belton JM, McCord RP, Gibcus JH, Naumova N, Zhan Y, Dekker J (2012) Hi-C: a comprehensive technique to capture the conformation of genomes. Methods 58:268–276

    Article  CAS  PubMed  Google Scholar 

  • Benbrook DM, Chambon P, Rochette-Egly C, Asson-Batres MA (2014) History of retinoic acid receptors. Subcell Biochem 70:1–20

    Article  CAS  PubMed  Google Scholar 

  • Bibel M, Richter J, Schrenk K, Tucker KL, Staiger V, Korte M, Goetz M, Barde YA (2004) Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat Neurosci 7:1003–1009

    Article  CAS  PubMed  Google Scholar 

  • Blat Y, Kleckner N (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98:249–259

    Article  CAS  PubMed  Google Scholar 

  • Bouillet P, Chazaud C, Oulad-Abdelghani M, Dolle P, Chambon P (1995a) Sequence and expression pattern of the Stra7 (Gbx-2) homeobox-containing gene induced by retinoic acid in P19 embryonal carcinoma cells. Dev Dyn 204: 372-82

    Google Scholar 

  • Bouillet P, Oulad-Abdelghani M, Vicaire S, Garnier JM, Schuhbaur B, Dolle P, Chambon P (1995b) Efficient cloning of cDNAs of retinoic acid-responsive genes in P19 embryonal carcinoma cells and characterization of a novel mouse gene, Stra1 (mouse LERK-2/Eplg2). Dev Biol 170: 420-33

    Google Scholar 

  • Bouillet P, Oulad-Abdelghani M, Ward SJ, Bronner S, Chambon P, Dolle P (1996) A new mouse member of the Wnt gene family, mWnt-8, is expressed during early embryogenesis and is ectopically induced by retinoic acid. Mech Dev 58:141–152

    Article  CAS  PubMed  Google Scholar 

  • Bouillet P, Sapin V, Chazaud C, Messaddeq N, Decimo D, Dolle P, Chambon P (1997) Developmental expression pattern of Stra6, a retinoic acid-responsive gene encoding a new type of membrane protein. Mech Dev 63:173–186

    Article  CAS  PubMed  Google Scholar 

  • Briggs JA, Weinreb C, Wagner DE, Megason S, Peshkin L, Kirschner MW, Klein AM (2018) The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution. Science 360

    Google Scholar 

  • Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ (2013) Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10:1213–1218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buenrostro JD, Wu B, Litzenburger UM, Ruff D, Gonzales ML, Snyder MP, Chang HY, Greenleaf WJ (2015) Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523:486–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bumgarner R (2013) Overview of DNA microarrays: types, applications, and their future. Curr Protoc Mol Biol Chapter 22: Unit 22 1

    Google Scholar 

  • Buttitta L, Tanaka TS, Chen AE, Ko MS, Fan CM (2003) Microarray analysis of somitogenesis reveals novel targets of different WNT signaling pathways in the somitic mesoderm. Dev Biol 258:91–104

    Article  CAS  PubMed  Google Scholar 

  • Chambon P (1996) A decade of molecular biology of retinoic acid receptors. Faseb J 10:940–954

    Article  CAS  PubMed  Google Scholar 

  • Chatagnon A, Veber P, Morin V, Bedo J, Triqueneaux G, Semon M, Laudet V, d’Alche-Buc F, Benoit G (2015) RAR/RXR binding dynamics distinguish pluripotency from differentiation associated cis-regulatory elements. Nucleic Acids Res 43:4833–4854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chazaud C, Bouillet P, Oulad-Abdelghani M, Dolle P (1996) Restricted expression of a novel retinoic acid responsive gene during limb bud dorsoventral patterning and endochondral ossification. Dev Genet 19:66–73

    Article  CAS  PubMed  Google Scholar 

  • Chen A, Chen D, Chen Y (2018) Advances of DNase-seq for mapping active gene regulatory elements across the genome in animals. Gene 667:83–94

    Article  CAS  PubMed  Google Scholar 

  • Chen F, Desai TJ, Qian J, Niederreither K, Lu J, Cardoso WV (2007) Inhibition of Tgf beta signaling by endogenous retinoic acid is essential for primary lung bud induction. Development 134:2969–2979

    Article  CAS  PubMed  Google Scholar 

  • Cholley PE, Moehlin J, Rohmer A, Zilliox V, Nicaise S, Gronemeyer H, Mendoza-Parra MA (2018) Modeling gene-regulatory networks to describe cell fate transitions and predict master regulators. NPJ Syst Biol Appl 4:29

    Article  PubMed  PubMed Central  Google Scholar 

  • Cunningham TJ, Duester G (2015) Mechanisms of retinoic acid signalling and its roles in organ and limb development. Nat Rev Mol Cell Biol 16:110–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davidson EH (2002) A genomic regulatory network for development. Sci 295(5560):1669–1678

    Google Scholar 

  • Delacroix L, Moutier E, Altobelli G, Legras S, Poch O, Choukrallah MA, Bertin I, Jost B, Davidson I (2010) Cell-specific interaction of retinoic acid receptors with target genes in mouse embryonic fibroblasts and embryonic stem cells. Mol Cell Biol 30:231–244

    Article  CAS  PubMed  Google Scholar 

  • Dirks RA, Stunnenberg HG, Marks H (2016) Genome-wide epigenomic profiling for biomarker discovery. Clin Epigenetics 8:122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dolle P, Ruberte E, Kastner P, Petkovich M, Stoner CM, Gudas LJ, Chambon P (1989) Differential expression of genes encoding alpha, beta and gamma retinoic acid receptors and CRABP in the developing limbs of the mouse. Nature 342:702–705

    Article  CAS  PubMed  Google Scholar 

  • Dolle P, Ruberte E, Leroy P, Morriss-Kay G, Chambon P (1990) Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 110:1133–1151

    CAS  PubMed  Google Scholar 

  • Eifert C, Sangster-Guity N, Yu LM, Chittur SV, Perez AV, Tine JA, McCormick PJ (2006) Global gene expression profiles associated with retinoic acid-induced differentiation of embryonal carcinoma cells. Mol Reprod Dev 73:796–824

    Article  CAS  PubMed  Google Scholar 

  • Ernst J, Vainas O, Harbison CT, Simon I, Bar-Joseph Z (2007) Reconstructing dynamic regulatory maps. Mol Syst Biol 3:74

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fathi A, Hatami M, Hajihosseini V, Fattahi F, Kiani S, Baharvand H, Salekdeh GH (2011) Comprehensive gene expression analysis of human embryonic stem cells during differentiation into neural cells. PLoS ONE 6:e22856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freemantle SJ, Kerley JS, Olsen SL, Gross RH, Spinella MJ (2002) Developmentally-related candidate retinoic acid target genes regulated early during neuronal differentiation of human embryonal carcinoma. Oncogene 21:2880–2889

    Article  CAS  PubMed  Google Scholar 

  • Furey TS (2012) ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat Rev Genet 13:840–852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardini A (2017) Global Run-On Sequencing (GRO-Seq). Methods Mol Biol 1468:111–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giguere V, Lyn S, Yip P, Siu CH, Amin S (1990) Molecular cloning of cDNA encoding a second cellular retinoic acid-binding protein. Proc Natl Acad Sci U S A 87:6233–6237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giresi PG, Kim J, McDaniell RM, Iyer VR, Lieb JD (2007) FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Res 17:877–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris TM, Childs G (2002) Global gene expression patterns during differentiation of F9 embryonal carcinoma cells into parietal endoderm. Funct Integr Genomics 2:105–119

    Article  CAS  PubMed  Google Scholar 

  • Hermsen SA, Pronk TE, van den Brandhof EJ, van der Ven LT, Piersma AH (2013) Transcriptomic analysis in the developing zebrafish embryo after compound exposure: individual gene expression and pathway regulation. Toxicol Appl Pharmacol 272:161–171

    Article  CAS  PubMed  Google Scholar 

  • Hogan BL, Taylor A, Adamson E (1981) Cell interactions modulate embryonal carcinoma cell differentiation into parietal or visceral endoderm. Nature 291:235–237

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Gudas LJ (1990) Cyclic AMP analogs and retinoic acid influence the expression of retinoic acid receptor alpha, beta, and gamma mRNAs in F9 teratocarcinoma cells. Mol Cell Biol 10:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jarvinen AK, Hautaniemi S, Edgren H, Auvinen P, Saarela J, Kallioniemi OP, Monni O (2004) Are data from different gene expression microarray platforms comparable? Genomics 83:1164–1168

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Ryu J, Kiraly M, Duke K, Reinke V, Kim SK (2001) Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc Natl Acad Sci U S A 98:218–223

    Article  CAS  PubMed  Google Scholar 

  • Jin W, Tang Q, Wan M, Cui K, Zhang Y, Ren G, Ni B, Sklar J, Przytycka TM, Childs R, Levens D, Zhao K (2015) Genome-wide detection of DNase I hypersensitive sites in single cells and FFPE tissue samples. Nature 528:142–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones-Villeneuve EM, McBurney MW, Rogers KA, Kalnins VI (1982) Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J Cell Biol 94:253–262

    Article  CAS  PubMed  Google Scholar 

  • Jonk LJ, de Jonge ME, Vervaart JM, Wissink S, Kruijer W (1994) Isolation and developmental expression of retinoic-acid-induced genes. Dev Biol 161:604–614

    Article  CAS  PubMed  Google Scholar 

  • Kashyap V, Laursen KB, Brenet F, Viale AJ, Scandura JM, Gudas LJ (2013) RARgamma is essential for retinoic acid induced chromatin remodeling and transcriptional activation in embryonic stem cells. J Cell Sci 126:999–1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly DL, Rizzino A (2000) DNA microarray analyses of genes regulated during the differentiation of embryonic stem cells. Mol Reprod Dev 56:113–123

    Article  CAS  PubMed  Google Scholar 

  • Lalevee S, Anno YN, Chatagnon A, Samarut E, Poch O, Laudet V, Benoit G, Lecompte O, Rochette-Egly C (2011) Genome-wide in silico identification of new conserved and functional retinoic acid receptor response elements (direct repeats separated by 5 bp). J Biol Chem 286:33322–33334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaRosa GJ, Gudas LJ (1988) 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 8:3906–3917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linney E, Dobbs-McAuliffe B, Sajadi H, Malek RL (2004) Microarray gene expression profiling during the segmentation phase of zebrafish development. Comp Biochem Physiol C Toxicol Pharmacol 138:351–362

    Article  PubMed  CAS  Google Scholar 

  • Lo J, Lee S, Xu M, Liu F, Ruan H, Eun A, He Y, Ma W, Wang W, Wen Z, Peng J (2003) 15000 unique zebrafish EST clusters and their future use in microarray for profiling gene expression patterns during embryogenesis. Genome Res 13:455–466

    Article  PubMed  PubMed Central  Google Scholar 

  • Lockhart DJ, Dong H, Byrne MC, Follettie MT, Gallo MV, Chee MS, Mittmann M, Wang C, Kobayashi M, Horton H, Brown EL (1996) Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat Biotechnol 14:1675–1680

    Article  CAS  PubMed  Google Scholar 

  • Maden M (1982) Vitamin A and pattern formation in the regenerating limb. Nature 295:672–675

    Article  CAS  PubMed  Google Scholar 

  • Mahony S, Mazzoni EO, McCuine S, Young RA, Wichterle H, Gifford DK (2011) Ligand-dependent dynamics of retinoic acid receptor binding during early neurogenesis. Genome Biol 12:R2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendoza-Parra MA, Malysheva V, Mohamed Saleem MA, Lieb M, Godel A, Gronemeyer H (2016) Reconstructed cell fate-regulatory programs in stem cells reveal hierarchies and key factors of neurogenesis. Genome Res 26:1505–1519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendoza-Parra MA, Walia M, Sankar M, Gronemeyer H (2011) Dissecting the retinoid-induced differentiation of F9 embryonal stem cells by integrative genomics. Mol Syst Biol 7:538

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morris SA, Cahan P, Li H, Zhao AM, San Roman AK, Shivdasani RA, Collins JJ, Daley GQ (2014) Dissecting engineered cell types and enhancing cell fate conversion via Cell Net. Cell 158:889–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moutier E, Ye T, Choukrallah MA, Urban S, Osz J, Chatagnon A, Delacroix L, Langer D, Rochel N, Moras D, Benoit G, Davidson I (2012) Retinoic acid receptors recognize the mouse genome through binding elements with diverse spacing and topology. J Biol Chem 287:26328–26341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E, Dean W, Laue ED, Tanay A, Fraser P (2013) Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502:59–64

    Article  CAS  PubMed  Google Scholar 

  • Nomura M, Takihara Y, Yasunaga T, Shimada K (1994) One of the retinoic acid-inducible cDNA clones in mouse embryonal carcinoma F9 cells encodes a novel isoenzyme of fructose 1,6-bisphosphatase. FEBS Lett 348:201–205

    Article  CAS  PubMed  Google Scholar 

  • Oulad-Abdelghani M, Bouillet P, Decimo D, Gansmuller A, Heyberger S, Dolle P, Bronner S, Lutz Y, Chambon P (1996) Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J Cell Biol 135:469–477

    Article  CAS  PubMed  Google Scholar 

  • Oulad-Abdelghani M, Chazaud C, Bouillet P, Mattei MG, Dolle P, Chambon P (1998) Stra3/lefty, a retinoic acid-inducible novel member of the transforming growth factor-beta superfamily. Int J Dev Biol 42:23–32

    CAS  PubMed  Google Scholar 

  • Oulad-Abdelghani M, Chazaud C, Bouillet P, Sapin V, Chambon P, Dolle P (1997) Meis2, a novel mouse Pbx-related homeobox gene induced by retinoic acid during differentiation of P19 embryonal carcinoma cells. Dev Dyn 210:173–183

    Article  CAS  PubMed  Google Scholar 

  • Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12:87–98

    Article  CAS  PubMed  Google Scholar 

  • Padmarasu S, Himmelbach A, Mascher M, Stein N (2019) In Situ Hi-C for Plants: An Improved Method to Detect Long-Range Chromatin Interactions. Methods Mol Biol 1933:441–472

    Article  CAS  PubMed  Google Scholar 

  • Paschaki M, Schneider C, Rhinn M, Thibault-Carpentier C, Dembele D, Niederreither K, Dolle P (2013) Transcriptomic analysis of murine embryos lacking endogenous retinoic acid signaling. PLoS ONE 8:e62274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pickering J, Wali N, Towers M (2017) Transcriptional changes in chick wing bud polarization induced by retinoic acid. Dev Dyn 246:682–690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Preissl S, Fang R, Huang H, Zhao Y, Raviram R, Gorkin DU, Zhang Y, Sos BC, Afzal V, Dickel DE, Kuan S, Visel A, Pennacchio LA, Zhang K, Ren B (2018) Single-nucleus analysis of accessible chromatin in developing mouse forebrain reveals cell-type-specific transcriptional regulation. Nat Neurosci 21:432–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rochette-Egly C, Germain P (2009) Dynamic and combinatorial control of gene expression by nuclear retinoic acid receptors (RARs). Nucl Recept Signal 7:e005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rogers MB, Rosen V, Wozney JM, Gudas LJ (1992) Bone morphogenetic proteins-2 and -4 are involved in the retinoic acid-induced differentiation of embryonal carcinoma cells. Mol Biol Cell 3:189–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruberte E, Dolle P, Chambon P, Morriss-Kay G (1991) Retinoic acid receptors and cellular retinoid binding proteins. II. Their differential pattern of transcription during early morphogenesis in mouse embryos. Development 111:45–60

    CAS  PubMed  Google Scholar 

  • Ruberte E, Dolle P, Krust A, Zelent A, Morriss-Kay G, Chambon P (1990) Specific spatial and temporal distribution of retinoic acid receptor gamma transcripts during mouse embryogenesis. Development 108:213–222

    CAS  PubMed  Google Scholar 

  • Samarut E, Gaudin C, Hughes S, Gillet B, de Bernard S, Jouve PE, Buffat L, Allot A, Lecompte O, Berekelya L, Rochette-Egly C, Laudet V (2014) Retinoic acid receptor subtype-specific transcriptotypes in the early zebrafish embryo. Mol Endocrinol 28:260–272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470

    Article  CAS  PubMed  Google Scholar 

  • Serandour AA, Brown GD, Cohen JD, Carroll JS (2013) Development of an Illumina-based ChIP-exonuclease method provides insight into FoxA1-DNA binding properties. Genome Biol 14:R147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simandi Z, Balint BL, Poliska S, Ruhl R, Nagy L (2010) Activation of retinoic acid receptor signaling coordinates lineage commitment of spontaneously differentiating mouse embryonic stem cells in embryoid bodies. FEBS Lett 584:3123–3130

    Article  CAS  PubMed  Google Scholar 

  • Sinner D, Kirilenko P, Rankin S, Wei E, Howard L, Kofron M, Heasman J, Woodland HR, Zorn AM (2006) Global analysis of the transcriptional network controlling Xenopus endoderm formation. Development 133:1955–1966

    Article  CAS  PubMed  Google Scholar 

  • Skene PJ, Henikoff JG, Henikoff S (2018) Targeted in situ genome-wide profiling with high efficiency for low cell numbers. Nat Protoc 13:1006–1019

    Article  CAS  PubMed  Google Scholar 

  • Stocum DL (1991) Limb regeneration: a call to arms (and legs). Cell 67:5–8

    Article  CAS  PubMed  Google Scholar 

  • Strickland S, Mahdavi V (1978) The induction of differentiation in teratocarcinoma cells by retinoic acid. Cell 15:393–403

    Article  CAS  PubMed  Google Scholar 

  • Strickland S, Smith KK, Marotti KR (1980) Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell 21:347–355

    Article  CAS  PubMed  Google Scholar 

  • Su D, Gudas LJ (2008) Gene expression profiling elucidates a specific role for RARgamma in the retinoic acid-induced differentiation of F9 teratocarcinoma stem cells. Biochem Pharmacol 75:1129–1160

    Article  CAS  PubMed  Google Scholar 

  • Taher L, Collette NM, Murugesh D, Maxwell E, Ovcharenko I, Loots GG (2011) Global gene expression analysis of murine limb development. PLoS ONE 6:e28358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanay A, Regev A (2017) Scaling single-cell genomics from phenomenology to mechanism. Nature 541:331–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taneja R, Rochette-Egly C, Plassat JL, Penna L, Gaub MP, Chambon P (1997) Phosphorylation of activation functions AF-1 and AF-2 of RAR alpha and RAR gamma is indispensable for differentiation of F9 cells upon retinoic acid and cAMP treatment. EMBO J 16:6452–6465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thaller C, Eichele G (1987) Identification and spatial distribution of retinoids in the developing chick limb bud. Nature 327:625–628

    Article  CAS  PubMed  Google Scholar 

  • Tickle C, Alberts B, Wolpert L, Lee J (1982) Local application of retinoic acid to the limb bond mimics the action of the polarizing region. Nature 296:564–566

    Article  CAS  PubMed  Google Scholar 

  • Ton C, Stamatiou D, Dzau VJ, Liew CC (2002) Construction of a zebrafish cDNA microarray: gene expression profiling of the zebrafish during development. Biochem Biophys Res Commun 296:1134–1142

    Article  CAS  PubMed  Google Scholar 

  • Vasios G, Mader S, Gold JD, Leid M, Lutz Y, Gaub MP, Chambon P, Gudas L (1991) The late retinoic acid induction of laminin B1 gene transcription involves RAR binding to the responsive element. EMBO J 10:1149–1158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vasios GW, Gold JD, Petkovich M, Chambon P, Gudas LJ (1989) A retinoic acid-responsive element is present in the 5’ flanking region of the laminin B1 gene. Proc Natl Acad Sci U S A 86:9099–9103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner DE, Weinreb C, Collins ZM, Briggs JA, Megason SG, Klein AM (2018) Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo. Science 360:981–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SY, Gudas LJ (1988) Protein synthesis inhibitors prevent the induction of laminin B1, collagen IV (alpha 1), and other differentiation-specific mRNAs by retinoic acid in F9 teratocarcinoma cells. J Cell Physiol 136:305–311

    Article  CAS  PubMed  Google Scholar 

  • Warkany J, Schraffenberger E (1946) Congenital malformations induced in rats by maternal vitamin A deficiency; defects of the eye. Arch Ophthal 35:150–169

    Article  CAS  PubMed  Google Scholar 

  • Wei Y, Harris T, Childs G (2002) Global gene expression patterns during neural differentiation of P19 embryonic carcinoma cells. Differentiation 70:204–219

    Article  CAS  PubMed  Google Scholar 

  • Woo Y, Affourtit J, Daigle S, Viale A, Johnson K, Naggert J, Churchill G (2004) A comparison of cDNA, oligonucleotide, and Affymetrix GeneChip gene expression microarray platforms. J Biomol Tech 15:276–284

    PubMed  PubMed Central  Google Scholar 

  • Zelent A, Krust A, Petkovich M, Kastner P, Chambon P (1989) Cloning of murine alpha and beta retinoic acid receptors and a novel receptor gamma predominantly expressed in skin. Nature 339:714–717

    Article  CAS  PubMed  Google Scholar 

  • Zeng W, Mortazavi A (2012) Technical considerations for functional sequencing assays. Nat Immunol 13:802–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Rochette-Egly, C. (2020). Retinoic Acid-Regulated Target Genes During Development: Integrative Genomics Analysis. In: Asson-Batres, M., Rochette-Egly, C. (eds) The Biochemistry of Retinoid Signaling III. Subcellular Biochemistry, vol 95. Springer, Cham. https://doi.org/10.1007/978-3-030-42282-0_3

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