Transcriptomic Analysis of Murine Embryos Lacking Endogenous Retinoic Acid Signaling

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Paschaki, Marie ^a   Schneider, Carole ^a   Rhinn, Muriel ^a   Thibault Carpentier, Christelle ^a   Dembélé, Doulaye ^a   Niederreither, Karen ^a   Dollé, Pascal ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RETINAL DEHYDROGENASE; RETINOIC ACID; TRANSCRIPTOME;

ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; EMBRYO; FEMALE; GENE; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RALDH2 GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; UPREGULATION;

ALDEHYDE OXIDOREDUCTASES; ANIMALS; CELL LINEAGE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, KNOCKOUT; PHENOTYPE; PREGNANCY; REGULATORY SEQUENCES, NUCLEIC ACID; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TRETINOIN;

MURINAE;

EID: 84876544937     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062274     Document Type: Article

References (83)

1. Balmer JE, Blomhoff R, (2005) A robust characterization of retinoic acid response elements based on a comparison of sites in three species. J Steroid Biochem Mol Biol 96: 347-354.
2. McCaffery P, Drager UC, (2000) Regulation of retinoic acid signaling in the embryonic nervous system: a master differentiation factor. Cytokine Growth Factor Rev 11: 233-249.
3. Balmer JE, Blomhoff R, (2002) Gene expression regulation by retinoic acid. J Lipid Res 43: 1773-1808.
4. Rochette-Egly C, Germain P, (2009) Dynamic and combinatorial control of gene expression by nuclear retinoic acid receptors (RARs). Nucl Recept Signal 7: e005.
5. Maden M, Sonneveld E, van der Saag PT, Gale E, (1998) The distribution of endogenous retinoic acid in the chick embryo: implications for developmental mechanisms. Development 125: 4133-4144.
6. Ribes V, Le Roux I, Rhinn M, Schuhbaur B, Dolle P, (2009) Early mouse caudal development relies on crosstalk between retinoic acid, Shh and Fgf signalling pathways. Development 136: 665-676.
7. Stern CD, (2001) Initial patterning of the central nervous system: how many organizers? Nat Rev Neurosci 2: 92-98.
8. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, et al. (2003) Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40: 65-79.
9. Sirbu IO, Duester G, (2006) Retinoic-acid signalling in node ectoderm and posterior neural plate directs left-right patterning of somitic mesoderm. Nat Cell Biol 8: 271-277.
10. Vermot J, Gallego Llamas J, Fraulob V, Niederreither K, Chambon P, et al. (2005) Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo. Science 308: 563-566.
11. Niederreither K, Vermot J, Schuhbaur B, Chambon P, Dolle P, (2000) Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 127: 75-85.
12. Gavalas A, (2002) ArRAnging the hindbrain. Trends Neurosci 25: 61-64.
13. Diez del Corral R, Storey KG, (2004) Opposing FGF and retinoid pathways: a signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis. Bioessays 26: 857-869.
14. Maden M, (2007) Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci 8: 755-765.
15. Niederreither K, Vermot J, Le Roux I, Schuhbaur B, Chambon P, et al. (2003) 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: 2525-2534.
16. Ryckebusch L, Wang Z, Bertrand N, Lin SC, Chi X, et al. (2008) Retinoic acid deficiency alters second heart field formation. Proc Natl Acad Sci U S A 105: 2913-2918.
17. Sirbu IO, Zhao X, Duester G, (2008) Retinoic acid controls heart anteroposterior patterning by down-regulating Isl1 through the Fgf8 pathway. Dev Dyn 237: 1627-1635.
18. Niederreither K, Vermot J, Messaddeq N, Schuhbaur B, Chambon P, et al. (2001) Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development 128: 1019-1031.
19. Ward SJ, Chambon P, Ong DE, Bavik C, (1997) A retinol-binding protein receptor-mediated mechanism for uptake of vitamin A to postimplantation rat embryos. Biol Reprod 57: 751-755.
20. Sapin V, Ward SJ, Bronner S, Chambon P, Dolle P, (1997) Differential expression of transcripts encoding retinoid binding proteins and retinoic acid receptors during placentation of the mouse. Dev Dyn 208: 199-210.
21. Napoli JL, (2012) Physiological insights into all-trans-retinoic acid biosynthesis. Biochim Biophys Acta 1821: 152-167.
22. Rhinn M, Dolle P, (2012) Retinoic acid signalling during development. Development 139: 843-858.
23. Pares X, Farres J, Kedishvili N, Duester G, (2008) Medium- and short-chain dehydrogenase/reductase gene and protein families: Medium-chain and short-chain dehydrogenases/reductases in retinoid metabolism. Cell Mol Life Sci 65: 3936-3949.
24. von Lintig J, Hessel S, Isken A, Kiefer C, Lampert JM, et al. (2005) Towards a better understanding of carotenoid metabolism in animals. Biochim Biophys Acta 1740: 122-131.
25. Niederreither K, McCaffery P, Drager UC, Chambon P, Dolle P, (1997) Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech Dev 62: 67-78.
26. Niederreither K, Subbarayan V, Dolle P, Chambon P, (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21: 444-448.
27. Wagner E, McCaffery P, Drager UC, (2000) Retinoic acid in the formation of the dorsoventral retina and its central projections. Dev Biol 222: 460-470.
28. Mic FA, Molotkov A, Molotkova N, Duester G, (2004) Raldh2 expression in optic vesicle generates a retinoic acid signal needed for invagination of retina during optic cup formation. Dev Dyn 231: 270-277.
29. Ribes V, Wang Z, Dolle P, Niederreither K, (2006) Retinaldehyde dehydrogenase 2 (RALDH2)-mediated retinoic acid synthesis regulates early mouse embryonic forebrain development by controlling FGF and sonic hedgehog signaling. Development 133: 351-361.
30. Li H, Wagner E, McCaffery P, Smith D, Andreadis A, et al. (2000) A retinoic acid synthesizing enzyme in ventral retina and telencephalon of the embryonic mouse. Mech Dev 95: 283-289.
31. Mic FA, Molotkov A, Fan X, Cuenca AE, Duester G, (2000) 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: 227-230.
32. Rossant J, Zirngibl R, Cado D, Shago M, Giguere V, (1991) Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev 5: 1333-1344.
33. Mic FA, Haselbeck RJ, Cuenca AE, Duester G, (2002) Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 129: 2271-2282.
34. Molotkova N, Molotkov A, Sirbu IO, Duester G, (2005) Requirement of mesodermal retinoic acid generated by Raldh2 for posterior neural transformation. Mech Dev 122: 145-155.
35. Houle M, Sylvestre JR, Lohnes D, (2003) Retinoic acid regulates a subset of Cdx1 function in vivo. Development 130: 6555-6567.
36. Ribes V, Stutzmann F, Bianchetti L, Guillemot F, Dolle P, et al. (2008) Combinatorial signalling controls Neurogenin2 expression at the onset of spinal neurogenesis. Dev Biol 321: 470-481.
37. Kawaguchi R, Yu J, Honda J, Hu J, Whitelegge J, et al. (2007) A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science. 315: 820-825.
38. Bouillet P, Sapin V, Chazaud C, Messaddeq N, Decimo D, et al. (1997) Developmental expression pattern of Stra6, a retinoic acid-responsive gene encoding a new type of membrane protein. Mech Dev 63: 173-186.
39. Feng L, Hernandez RE, Waxman JS, Yelon D, Moens CB, (2010) Dhrs3a regulates retinoic acid biosynthesis through a feedback inhibition mechanism. Dev Biol 338: 1-14.
40. Di W, Li XY, Datta S, Astrom A, Fisher GJ, et al. (1998) Keratinocyte-specific retinoid regulation of human cellular retinoic acid binding protein-II (hCRABPII) gene promoter requires an evolutionarily conserved DR1 retinoic acid-responsive element. J Invest Dermatol 111: 1109-1115.
41. Thomas MA, Hodgson MC, Loermans SD, Hooper J, Endersby R, et al. (2006) Transcriptional regulation of the homeobox gene NKX3.1 by all-trans retinoic acid in prostate cancer cells. J Cell Biochem 99: 1409-1419.
42. Yun K, Mantani A, Garel S, Rubenstein J, Israel MA, (2004) Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 131: 5441-5448.
43. Kobayashi M, Yu RT, Yasuda K, Umesono K, (2000) Cell-type-specific regulation of the retinoic acid receptor mediated by the orphan nuclear receptor TLX. Mol Cell Biol 20: 8731-8739.
44. Paschaki M, Lin SC, Wong RL, Finnell RH, Dolle P, et al. (2012) Retinoic acid-dependent signaling pathways and lineage events in the developing mouse spinal cord. PLoS One 7: e32447.
45. Pierani A, Moran-Rivard L, Sunshine MJ, Littman DR, Goulding M, et al. (2001) Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29: 367-384.
46. Hunter CS, Rhodes SJ, (2005) LIM-homeodomain genes in mammalian development and human disease. Mol Biol Rep 32: 67-77.
47. Finley KR, Tennessen J, Shawlot W, (2003) The mouse secreted frizzled-related protein 5 gene is expressed in the anterior visceral endoderm and foregut endoderm during early post-implantation development. Gene Expr Patterns 3: 681-684.
48. Mochida Y, Parisuthiman D, Kaku M, Hanai J, Sukhatme VP, et al. (2006) Nephrocan, a novel member of the small leucine-rich repeat protein family, is an inhibitor of transforming growth factor-beta signaling. J Biol Chem 281: 36044-36051.
49. Seo KW, Wang Y, Kokubo H, Kettlewell JR, Zarkower DA, et al. (2006) Targeted disruption of the DM domain containing transcription factor Dmrt2 reveals an essential role in somite patterning. Dev Biol 290: 200-210.
50. Lee HS, Han J, Lee SH, Park JA, Kim KW, (2010) Meteorin promotes the formation of GFAP-positive glia via activation of the Jak-STAT3 pathway. J Cell Sci 123: 1959-1968.
51. Williams ME, Lu X, McKenna WL, Washington R, Boyette A, et al. (2006) UNC5A promotes neuronal apoptosis during spinal cord development independent of netrin-1. Nat Neurosci 9: 996-998.
52. Burgess R, Rawls A, Brown D, Bradley A, Olson EN, (1996) Requirement of the paraxis gene for somite formation and musculoskeletal patterning. Nature 384: 570-573.
53. Soyer J, Flasse L, Raffelsberger W, Beucher A, Orvain C, et al. (2010) Rfx6 is an Ngn3-dependent winged helix transcription factor required for pancreatic islet cell development. Development 137: 203-212.
54. Rossner MJ, Oster H, Wichert SP, Reinecke L, Wehr MC, et al. (2008) Disturbed clockwork resetting in Sharp-1 and Sharp-2 single and double mutant mice. PLoS One 3: e2762.
55. Boudjelal M, Taneja R, Matsubara S, Bouillet P, Dolle P, et al. (1997) Overexpression of Stra13, a novel retinoic acid-inducible gene of the basic helix-loop-helix family, inhibits mesodermal and promotes neuronal differentiation of P19 cells. Genes Dev 11: 2052-2065.
56. Martinez-Gac L, Marques M, Garcia Z, Campanero MR, Carrera AC, (2004) Control of cyclin G2 mRNA expression by forkhead transcription factors: novel mechanism for cell cycle control by phosphoinositide 3-kinase and forkhead. Mol Cell Biol 24: 2181-2189.
57. Luque JM, Morante-Oria J, Fairen A, (2003) Localization of ApoER2, VLDLR and Dab1 in radial glia: groundwork for a new model of reelin action during cortical development. Brain Res Dev Brain Res 140: 195-203.
58. Jung S, Park RH, Kim S, Jeon YJ, Ham DS, et al. (2010) Id proteins facilitate self-renewal and proliferation of neural stem cells. Stem Cells Dev 19: 831-841.
59. Shi Y, Chichung Lie D, Taupin P, Nakashima K, Ray J, et al. (2004) Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 427: 78-83.
60. Elkouris M, Balaskas N, Poulou M, Politis PK, Panayiotou E, et al. (2011) Sox1 maintains the undifferentiated state of cortical neural progenitor cells via the suppression of Prox1-mediated cell cycle exit and neurogenesis. Stem Cells 29: 89-98.
61. Glaser T, Brustle O, (2005) Retinoic acid induction of ES-cell-derived neurons: the radial glia connection. Trends Neurosci 28: 397-400.
62. Gomez-Lopez S, Wiskow O, Favaro R, Nicolis SK, Price DJ, et al. (2011) Sox2 and Pax6 maintain the proliferative and developmental potential of gliogenic neural stem cells In vitro. Glia 59: 1588-1599.
63. Feng L, Hatten ME, Heintz N, (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12: 895-908.
64. de Hoon MJ, Imoto S, Nolan J, Miyano S, (2004) Open source clustering software. Bioinformatics 20: 1453-1454.
65. Sucov HM, Murakami KK, Evans RM, (1990) Characterization of an autoregulated response element in the mouse retinoic acid receptor type beta gene. Proc Natl Acad Sci U S A 87: 5392-5396.
66. Tang XH, Gudas LJ, (2011) Retinoids, retinoic acid receptors, and cancer. Annu Rev Pathol 6: 345-364.
67. Niederreither K, Dolle P, (2008) Retinoic acid in development: towards an integrated view. Nat Rev Genet 9: 541-553.
68. Duester G, (2008) Retinoic acid synthesis and signaling during early organogenesis. Cell 134: 921-931.
69. Olivera-Martinez I, Storey KG, (2007) Wnt signals provide a timing mechanism for the FGF-retinoid differentiation switch during vertebrate body axis extension. Development 134: 2125-2135.
70. Chen F, Desai TJ, Qian J, Niederreither K, Lu J, et al. (2007) Inhibition of Tgfβ signaling by endogenous retinoic acid isessential for primary lung bud induction. Development 134: 2969-2979.
71. Dubrulle J, Pourquie O, (2004) fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427: 419-422.
72. Moutier E, Ye T, Choukrallah MA, Urban S, Osz J, et al. (2012) Retinoic acid receptors recognize the mouse genome through binding elements with diverse spacing and topology. J Biol Chem 287: 26328-26341.
73. Kim M, Habiba A, Doherty JM, Mills JC, Mercer RW, et al. (2009) Regulation of mouse embryonic stem cell neural differentiation by retinoic acid. Dev Biol 328: 456-471.
74. Akanuma H, Qin XY, Nagano R, Win-Shwe TT, Imanishi S, et al. (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.
75. Delacroix L, Moutier E, Altobelli G, Legras S, Poch O, et al. (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.
76. Mahony S, Mazzoni EO, McCuine S, Young RA, Wichterle H, et al. (2011) Ligand-dependent dynamics of retinoic acid receptor binding during early neurogenesis. Genome Biol 12: R2.
77. Schug TT, Berry DC, Shaw NS, Travis SN, Noy N, (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129: 723-733.
78. Ho Sui SJ, Fulton DL, Arenillas DJ, Kwon AT, Wasserman WW, (2007) oPOSSUM: integrated tools for analysis of regulatory motif over-representation. Nucleic Acids Res 35: W245-252.
79. Kwon AT, Arenillas DJ, Worsley Hunt R, Wasserman WW, (2012) oPOSSUM-3: advanced analysis of regulatory motif over-representation across genes or ChIP-Seq datasets. G3 (Bethesda) 2: 987-1002.
80. Di Rocco G, Mavilio F, Zappavigna V, (1997) Functional dissection of a transcriptionally active, target-specific Hox-Pbx complex. Embo J 16: 3644-3654.
81. Serpente P, Tumpel S, Ghyselinck NB, Niederreither K, Wiedemann LM, et al. (2005) Direct crossregulation between retinoic acid receptor {beta} and Hox genes during hindbrain segmentation. Development 132: 503-513.
82. 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.
83. Chotteau-Lelievre A, Dolle P, Gofflot F, (2006) Expression analysis of murine genes using in situ hybridization with radioactive and nonradioactively labeled RNA probes. Methods Mol Biol 326: 61-87.