Active repression by RARγ signaling is required for vertebrate axial elongation

Development (Cambridge)

Volumn 141, Issue 11, 2014, Pages 2260-2270

  Janesick, Amanda ^a   Nguyen, Tuyen T L ^a   Aisaki, Ken Ichi ^b   Igarashi, Katsuhide ^b   Kitajima, Satoshi ^b   Chandraratna, Roshantha A S ^c   Kanno, Jun ^b   Blumberg, Bruce ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^c IO Therapeutics   (United States)

Author keywords

Active repression; Axial elongation; Chordoneural hinge; Posterior Hox; Presomitic mesoderm; Retinoic acid receptor

Indexed keywords

4 [2 [5,6 DIHYDRO 5,5 DIMETHYL 8 (4 METHYLPHENYL) 2 NAPHTHYL]ETHYNYL]BENZOIC ACID; CYTOCHROME P450 26A1; HOX PROTEIN; NRX205099; RETINOIC ACID RECEPTOR GAMMA; RETINOIC ACID RECEPTOR GAMMA 2; RETINOID; UNCLASSIFIED DRUG;

ARTICLE; AXIAL ELONGATION; AXIAL GROWTH; CELL DIFFERENTIATION; CHORDONEURAL HINGE; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; EMBRYONIC STRUCTURES; FEMALE; GENE ACTIVATION; GENE REPRESSION; GENETIC TRANSCRIPTION; HOX GENE; MESODERM; MICROARRAY ANALYSIS; NONHUMAN; PRESOMITIC MESODERM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL; TRUNK; VERTEBRATE; XENOPUS;

ACTIVE REPRESSION; AXIAL ELONGATION; CHORDONEURAL HINGE; POSTERIOR HOX; PRESOMITIC MESODERM; RETINOIC ACID RECEPTOR;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CO-REPRESSOR PROTEINS; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DOMINANT; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; NERVOUS SYSTEM; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, RETINOIC ACID; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SOMITES; TIME FACTORS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84901430985     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.103705     Document Type: Article

References (72)

1. Abu-Abed, S., Dollé, P., Metzger, D., Beckett, B., Chambon, P. and Petkovich, M. (2001). The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev. 15, 226-240.
2. Arima, K., Shiotsugu, J., Niu, R., Khandpur, R., Martinez, M., Shin, Y., Koide, T., Cho, K. W. Y., Kitayama, A., Ueno, N. et al. (2005). Global analysis of RARresponsive genes in the Xenopus neurula using cDNA microarrays. Dev. Dyn. 232, 414-431.
3. Beck, C.W. and Slack, J. M.W. (1998). Analysis of the developing Xenopus tail bud reveals separate phases of gene expression during determination and outgrowth. Mech. Dev. 72, 41-52.
4. Bevington, P. R. and Robinson, D. K. (2003). Data Reduction and Error Analysis for the Physical Sciences. New York: McGraw-Hill Education.
5. Blewitt, R. (2009). Enhancer of split-related-2 mRNA shows cyclic expression during somitogenesis in Xenopus laevis. Biosci. Horizons 2, 22-31.
6. Blumberg, B., Mangelsdorf, D. J., Dyck, J. A., Bittner, D. A., Evans, R. M. and De Robertis, E. M. (1992). Multiple retinoid-responsive receptors in a single cell: families of retinoid "X" receptors and retinoic acid receptors in the Xenopus egg. Proc. Natl. Acad. Sci. U.S.A. 89, 2321-2325.
7. Blumberg, B., Bolado, J., Jr, Derguini, F., Craig, A. G., Moreno, T. A., Chakravarti, D., Heyman, R. A., Buck, J. and Evans, R. M. (1996). Novel retinoic acid receptor ligands in Xenopus embryos. Proc. Natl. Acad. Sci. U.S.A. 93, 4873-4878.
8. Blumberg, B., Bolado, J., Jr, Moreno, T. A., Kintner, C., Evans, R. M. and Papalopulu, N. (1997). An essential role for retinoid signaling in anteroposterior neural patterning. Development 124, 373-379.
9. Blumberg, B., Kang, H., Bolado, J., Chen, H., Craig, A. G., Moreno, T. A., Umesono, K., Perlmann, T., De Robertis, E. M. and Evans, R. M. (1998). BXR, an embryonic orphan nuclear receptor activated by a novel class of endogenous benzoate metabolites. Genes Dev. 12, 1269-1277.
10. Bolce, M. E., Hemmati-Brivanlou, A., Kushner, P. D. and Harland, R. M. (1992). Ventral ectoderm of Xenopus forms neural tissue, including hindbrain, in response to activin. Development 115, 681-688.
11. Bradley, L. C., Snape, A., Bhatt, S. and Wilkinson, D. G. (1993). The structure and expression of the Xenopus Krox-20 gene: conserved and divergent patterns of expression in rhombomeres and neural crest. Mech. Dev. 40, 73-84.
12. Buchberger, A., Bonneick, S. and Arnold, H.-H. (2000). Expression of the novel basic-helix-loop-helix transcription factor cMespo in presomitic mesoderm of chicken embryos. Mech. Dev. 97, 223-226.
13. Cambray, N. and Wilson, V. (2002). Axial progenitors with extensive potency are localised to the mouse chordoneural hinge. Development 129, 4855-4866.
14. Cambray, N. and Wilson, V. (2007). Two distinct sources for a population of maturing axial progenitors. Development 134, 2829-2840.
15. Chakravarti, D., LaMorte, V. J., Nelson, M. C., Nakajima, T., Schulman, I. G., Juguilon, H., Montminy, M. and Evans, R. M. (1996). Role of CBP/P300 in nuclear receptor signalling. Nature 383, 99-103.
16. Chamorro-Garci{dotless}a, R., Kirchner, S., Li, X., Janesick, A., Casey, S. C., Chow, C. and Blumberg, B. (2012). Bisphenol A diglycidyl ether induces adipogenic differentiation of multipotent stromal stem cells through a peroxisome proliferatoractivated receptor gamma-independent mechanism. Environ. Health Perspect. 120, 984-989.
17. Chen, J. D. and Evans, R. M. (1995). A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature 377, 454-457.
18. Chen, J. D., Umesono, K. and Evans, R. M. (1996). SMRT isoforms mediate repression and anti-repression of nuclear receptor heterodimers. Proc. Natl. Acad. Sci. U.S.A. 93, 7567-7571.
19. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
20. Davis, R. L. and Kirschner, M.W. (2000). The fate of cells in the tailbud of Xenopus laevis. Development 127, 255-267.
21. de Roos, K., Sonneveld, E., Compaan, B., ten Berge, D., Durston, A. J. and van der Saag, P. T. (1999). Expression of retinoic acid 4-hydroxylase (CYP26) during mouse and Xenopus laevis embryogenesis. Mech. Dev. 82, 205-211.
22. Dequéant, M.-L. and Pourquié, O. (2008). Segmental patterning of the vertebrate embryonic axis. Nat. Rev. Genet. 9, 370-382.
23. Dubrulle, J., McGrew, M. J. and Pourquié, O. (2001). FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106, 219-232.
24. Escriva, H., Bertrand, S., Germain, P., Robinson-Rechavi, M., Umbhauer, M., Cartry, J., Duffraisse, M., Holland, L., Gronemeyer, H. and Laudet, V. (2006). Neofunctionalization in vertebrates: the example of retinoic acid receptors. PLoS Genet. 2, e102.
25. Fior, R., Maxwell, A. A., Ma, T. P., Vezzaro, A., Moens, C. B., Amacher, S. L., Lewis, J. and Saude, L. (2012). The differentiation and movement of presomitic mesoderm progenitor cells are controlled by Mesogenin 1. Development 139, 4656-4665.
26. Fujii, H., Sato, T., Kaneko, S., Gotoh, O., Fujii-Kuriyama, Y., Osawa, K., Kato, S. and Hamada, H. (1997). Metabolic inactivation of retinoic acid by a novel P450 differentially expressed in developing mouse embryos. EMBO J. 16, 4163-4173.
27. Gabellini, D., Colaluca, I. N., Vodermaier, H. C., Biamonti, G., Giacca, M., Falaschi, A., Riva, S. and Peverali, F. A. (2003). Early mitotic degradation of the homeoprotein HOXC10 is potentially linked to cell cycle progression. EMBO J. 22, 3715-3724.
28. Glinka, A., Delius, H., Blumenstock, C. and Niehrs, C. (1996). Combinatorial signalling by Xwnt-11 and Xnr3 in the organizer epithelium. Mech. Dev. 60, 221-231.
29. Gomez, C. and Pourquié, O. (2009). Developmental control of segment numbers in vertebrates. J. Exp. Zool. B Mol. Dev. Evol. 312B, 533-544.
30. Hitachi, K., Kondow, A., Danno, H., Inui, M., Uchiyama, H. and Asashima, M. (2008). Tbx6, Thylacine1, and E47 synergistically activate bowline expression in Xenopus somitogenesis. Dev. Biol. 313, 816-828.
31. Hollemann, T., Chen, Y., Grunz, H. and Pieler, T. (1998). Regionalized metabolic activity establishes boundaries of retinoic acid signalling. EMBO J. 17, 7361-7372.
32. Hopwood, N. D., Pluck, A. and Gurdon, J. B. (1989). MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. EMBO J. 8, 3409-3417.
33. Iimura, T., Denans, N. and Pourquié, O. (2009). Establishment of Hox vertebral identities in the embryonic spine precursors. Curr. Top. Dev. Biol. 88, 201-234.
34. Janesick, A., Shiotsugu, J., Taketani, M. and Blumberg, B. (2012). RIPPLY3 is a retinoic acid-inducible repressor required for setting the borders of the preplacodal ectoderm. Development 139, 1213-1224.
35. Janesick, A., Abbey, R., Chung, C., Liu, S., Taketani, M. and Blumberg, B. (2013). ERF and ETV3L are retinoic acid-inducible repressors required for primary neurogenesis. Development 140, 3095-3106.
36. Kanno, J., Aisaki, K.-i., Igarashi, K., Nakatsu, N., Ono, A., Kodama, Y. and Nagao, T. (2006). "Per cell" normalization method for mRNA measurement by quantitative PCR and microarrays. BMC Genomics 7, 64.
37. Kayala, M. A. and Baldi, P. (2012). Cyber-T web server: differential analysis of highthroughput data. Nucleic Acids Res. 40, W553-W559.
38. Klein, E. S., Pino, M. E., Johnson, A. T., Davies, P. J.A., Nagpal, S., Thacher, S. M., Krasinski, G. and Chandraratna, R. A. S. (1996). Identification and functional separation of retinoic acid receptor neutral antagonists and inverse agonists. J. Biol. Chem. 271, 22692-22696.
39. Klein, S. L., Strausberg, R. L., Wagner, L., Pontius, J., Clifton, S. W. and Richardson, P. (2002). Genetic and genomic tools for Xenopus research: the NIH Xenopus initiative. Dev. Dyn. 225, 384-391.
40. Koide, T., Downes, M., Chandraratna, R. A. S., Blumberg, B. and Umesono, K. (2001). Active repression of RAR signaling is required for head formation. Genes Dev. 15, 2111-2121.
41. Lamka, M. L., Boulet, A. M. and Sakonju, S. (1992). Ectopic expression of UBX and ABD-B proteins during Drosophila embryogenesis: competition, not a functional hierarchy, explains phenotypic suppression. Development 116, 841-854.
42. Leroy, P., Nakshatri, H. and Chambon, P. (1991). 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, 10138-10142.
43. Lombardo, A. and Slack, J. M. (2001). Abdominal B-type Hox gene expression in Xenopus laevis. Mech. Dev. 106, 191-195.
44. Malartre, M., Short, S. and Sharpe, C. (2004). Alternative splicing generates multiple SMRT transcripts encoding conserved repressor domains linked to variable transcription factor interaction domains. Nucleic Acids Res. 32, 4676-4686.
45. McGrew, M. J., Sherman, A., Lillico, S. G., Ellard, F. M., Radcliffe, P. A., Gilhooley, H. J., Mitrophanous, K. A., Cambray, N., Wilson, V. and Sang, H. (2008). Localised axial progenitor cell populations in the avian tail bud are not committed to a posterior Hox identity. Development 135, 2289-2299.
46. Mollard, R., Viville, S., Ward, S. J., Décimo, D., Chambon, P. and Dollé, P. (2000). Tissue-specific expression of retinoic acid receptor isoform transcripts in the mouse embryo. Mech. Dev. 94, 223-232.
47. Moreno, T. A. and Kintner, C. (2004). Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis. Dev. Cell 6, 205-218.
48. Nakaya, Y., Kuroda, S., Katagiri, Y. T., Kaibuchi, K. and Takahashi, Y. (2004). Mesenchymal-epithelial transition during somitic segmentation is regulated by differential roles of Cdc42 and Rac1. Dev. Cell 7, 425-438.
49. Nowotschin, S., Ferrer-Vaquer, A., Concepcion, D., Papaioannou, V. E. and Hadjantonakis, A.-K. (2012). Interaction of Wnt3a, Msgn1 and Tbx6 in neural versus paraxial mesoderm lineage commitment and paraxial mesoderm differentiation in the mouse embryo. Dev. Biol. 367, 1-14.
50. Olivera-Martinez, I., Harada, H., Halley, P. A. and Storey, K. G. (2012). Loss of FGF-dependent mesoderm identity and rise of endogenous retinoid signalling determine cessation of body axis elongation. PLoS Biol. 10, e1001415.
51. Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
52. Pfeffer, P. L. and De Robertis, E. M. (1994). Regional specificity of RAR gamma isoforms in Xenopus development. Mech. Dev. 45, 147-153.
53. Pourquié, O. and Tam, P. P. L. (2001). A nomenclature for prospective somites and phases of cyclic gene expression in the presomitic mesoderm. Dev. Cell 1, 619-620.
54. Rhinn, M. and Dolle, P. (2012). Retinoic acid signalling during development. Development 139, 843-858.
55. Sakai, Y., Meno, C., Fujii, H., Nishino, J., Shiratori, H., Saijoh, Y., Rossant, J. and Hamada, H. (2001). 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, 213-225.
56. Shimono, K., Tung, W.-e., Macolino, C., Chi, A. H.-T., Didizian, J. H., Mundy, C., Chandraratna, R. A., Mishina, Y., Enomoto-Iwamoto, M., Pacifici, M. et al. (2011). Potent inhibition of heterotopic ossification by nuclear retinoic acid receptor-gamma agonists. Nat. Med. 17, 454-460.
57. Shum, A. S. W., Poon, L. L. M., Tang, W. W. T., Koide, T., Chan, B. W. H., Leung, Y.-C. G., Shiroishi, T. and Copp, A. J. (1999). Retinoic acid induces down-regulation of Wnt-3a, apoptosis and diversion of tail bud cells to a neural fate in the mouse embryo. Mech. Dev. 84, 17-30.
58. Sive, H. L., Draper, B. W., Harland, R. M. and Weintraub, H. (1990). Identification of a retinoic acid-sensitive period during primary axis formation in Xenopus laevis. Genes Dev. 4, 932-942.
59. Sucov, H. M., Murakami, K. K. and Evans, R. M. (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.
60. Takemoto, T., Uchikawa, M., Yoshida, M., Bell, D. M., Lovell-Badge, R., Papaioannou, V. E. and Kondoh, H. (2011). Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 470, 394-398.
61. Tam, P. P. L., Goldman, D., Camus, A. and Schoenwolf, G. C. (2000). 1 Early events of somitogenesis in higher vertebrates: allocation of precursor cells during gastrulation and the organization of a meristic pattern in the paraxial mesoderm. Curr. Top. Dev. Biol. 47, 1-32.
62. Thacher, S. M., Vasudevan, J. and Chandraratna, R. A. S. (2000). Therapeutic applications for ligands of retinoid receptors. Curr. Pharm. Des. 6, 25-58.
63. Tsang, K. Y., Sinha, S., Liu, X., Bhat, S. and Chandraratna, R., A. (2003). Disubstituted Chalcone Oximes Having Rar(Gamma)-Retinoid Receptor Antagonist Activity. European Patent Office.
64. Uchiyama, H., Kobayashi, T., Yamashita, A., Ohno, S. and Yabe, S. (2001). Cloning and characterization of the T-box gene Tbx6 in Xenopus laevis. Dev. Growth Differ. 43, 657-669.
65. von Dassow, G., Schmidt, J. E. and Kimelman, D. (1993). Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activinregulated homeo box gene. Genes Dev. 7, 355-366.
66. Wellik, D. M. (2007). Hox patterning of the vertebrate axial skeleton. Dev. Dyn. 236, 2454-2463.
67. Weston, A. D., Blumberg, B. and Underhill, T. M. (2003). Active repression by unliganded retinoid receptors in development: less is sometimes more. J. Cell Biol. 161, 223-228.
68. Wong, C. W. and Privalsky, M. L. (1998). Transcriptional silencing is defined by isoform-and heterodimer-specific interactions between nuclear hormone receptors and corepressors. Mol. Cell. Biol. 18, 5724-5733.
69. Yabe, T. and Takada, S. (2012). Mesogenin causes embryonic mesoderm progenitors to differentiate during development of zebrafish tail somites. Dev. Biol. 370, 213-222.
70. Yoon, J. K. and Wold, B. (2000). The bHLH regulator pMesogenin1 is required for maturation and segmentation of paraxial mesoderm. Genes Dev. 14, 3204-3214.
71. Yoon, J. K., Moon, R. T. andWold, B. (2000). The bHLH class protein pMesogenin1 can specify paraxial mesoderm phenotypes. Dev. Biol. 222, 376-391.
72. Young, T., Rowland, J. E., van de Ven, C., Bialecka, M., Novoa, A., Carapuco, M., van Nes, J., de Graaff, W., Duluc, I., Freund, J.-N. et al. (2009). Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Dev. Cell 17, 516-526.