Long-range regulation by shared retinoic acid response elements modulates dynamic expression of posterior Hoxb genes in CNS development

Developmental Biology

Volumn 388, Issue 1, 2014, Pages 134-144

  Ahn, Youngwook ^a   Mullan, Hillary E ^a,c   Krumlauf, Robb ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c OBERLIN COLLEGE   (United States)

Author keywords

Central nervous system; Enhancer sharing; Enhancers; Gene regulation; Hox genes; Long range regulation; Retinoids; Transgenic reporters

Indexed keywords

RETINOIC ACID;

5' UNTRANSLATED REGION; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL EXPANSION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; HOXB GENE; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; ANIMAL EXPERIMENT; BACTERIAL ARTIFICIAL CHROMOSOME; DNA STRUCTURE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE INSERTION; GENETIC REGULATION; HOXB5 GENE; HOXB9 GENE; NERVE ELONGATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; REGULATORY MECHANISM; REPORTER GENE; RETINOIC ACID RESPONSIVE ELEMENT;

CENTRAL NERVOUS SYSTEM; ENHANCER SHARING; ENHANCERS; GENE REGULATION; HOX GENES; LONG-RANGE REGULATION; RETINOIDS; TRANSGENIC REPORTERS;

ANIMALS; BASE SEQUENCE; CHROMOSOMES, ARTIFICIAL, BACTERIAL; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HOMEODOMAIN PROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MUTATION; NEURONS; PLASMIDS; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINATION, GENETIC; RESPONSE ELEMENTS; RETINOIDS; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIGNAL TRANSDUCTION; TRANSGENES; TRETINOIN;

EID: 84895427966     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.01.027     Document Type: Article

References (54)

1. Akin Z.N., Nazarali A.J. Hox genes and their candidate downstream targets in the developing central nervous system. Cell. Mol. Neurobiol 2005, 25:697-741.
2. Alexander T., Nolte C., Krumlauf R. Hox genes and segmentation of the hindbrain and axial skeleton. Annu. Rev. Cell. Dev. Biol. 2009, 25:431-456.
3. Andrey G., Montavon T., Mascrez B., Gonzalez F., Noordermeer D., Leleu M., Trono D., Spitz F., Duboule D. A switch between topological domains underlies HoxD genes collinearity in mouse limbs. Science 2013, 340:1234167.
4. 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. 2011, 353:266-274.
5. Branda C.S., Dymecki S.M. Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 2004, 6:7-28.
6. Charite J., de Graaf W., Vogels R., Meijlink F., Deschamps J. Regulation of the Hoxb8 gene: synergism between multimerised cis-acting elements increases responsiveness to positional information. Dev. Biol. 1995, 171:294-305.
7. Conlon R.A., Rossant J. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 1992, 116:357-368.
8. Copeland N.G., Jenkins N.A., Court D.L. Recombineering: a powerful new tool for mouse functional genomics. Nat. Rev. Genet. 2001, 2:769-779.
9. de Vries W.N., Binns L.T., Fancher K.S., Dean J., Moore R., Kemler R., Knowles B.B. Expression of Cre recombinase in mouse oocytes: a means to study maternal effect genes. Genesis 2000, 26:110-112.
10. Deschamps J., van Nes J. Developmental regulation of the Hox genes during axial morphogenesis in the mouse. Development 2005, 132:2931-2942.
11. Duboule D. The rise and fall of Hox gene clusters. Development 2007, 134:2549-2560.
12. Duester G. Retinoic acid synthesis and signaling during early organogenesis. Cell 2008, 134:921-931.
13. Dupé V., Davenne M., Brocard J., Dollé P., Mark M., Dierich A., Chambon P., Rijli F. In vivo functional analysis of the Hoxa1 3' retinoid response element (3' RARE). Development 1997, 124:399-410.
14. Gould A., Itasaki N., Krumlauf R. Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 1998, 21:39-51.
15. Gould A., Morrison A., Sproat G., White R.A., Krumlauf R. Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 1997, 11:900-913.
16. 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 2007, 134:177-187.
17. Kashyap V., Gudas L.J., Brenet F., Funk P., Viale A., Scandura J.M. Epigenomic reorganization of the clustered Hox genes in embryonic stem cells induced by retinoic acid. J. Biol. Chem. 2011, 286:3250-3260.
18. Kessel M. Respecification of vertebral identities by retinoic acid. Development 1992, 115:487-501.
19. Kmita M., Duboule D. Organizing axes in time and space; 25 years of colinear tinkering. Science 2003, 301:331-333.
20. Krumlauf R. Hox genes in vertebrate development. Cell 1994, 78:191-201.
21. Kwan C.T., Tsang S.L., Krumlauf R., Sham M.H. Regulatory analysis of the mouse Hoxb3 gene: multiple elements work in concert to direct temporal and spatial patterns of expression. Dev. Biol. 2001, 232:176-190.
22. Lee E.C., Yu D., Martinez de Velasco J., Tessarollo L., Swing D.A., Court D.L., Jenkins N.A., Copeland N.G. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 2001, 73:56-65.
23. Lee G., Saito I. Role of nucleotide sequences of loxP spacer region in Cre-mediated recombination. Gene 1998, 216:55-65.
24. Linville A., Gumusaneli E., Chandraratna R.A., Schilling T.F. Independent roles for retinoic acid in segmentation and neuronal differentiation in the zebrafish hindbrain. Dev. Biol. 2004, 270:186-199.
25. Maconochie M., Krishnamurthy R., Nonchev S., Meier P., Manzanares M., Mitchell P.J., Krumlauf R. Regulation of Hoxa2 in cranial neural crest cells involves members of the AP-2 family. Development 1999, 126:1483-1494.
26. Mainguy G., In der Rieden P.M., Berezikov E., Woltering J.M., Plasterk R.H., Durston A.J. A position-dependent organisation of retinoid response elements is conserved in the vertebrate Hox clusters. Trends Genet. 2003, 19:476-479.
27. Mallo M., Wellik D.M., Deschamps J. Hox genes and regional patterning of the vertebrate body plan. Dev. Biol. 2010, 344:7-15.
28. Marshall H., Nonchev S., Sham M.H., Muchamore I., Lumsden A., Krumlauf R. Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 1992, 360:737-741.
29. Mazzoni E.O., Mahony S., Peljto M., Patel T., Thornton S.R., McCuine S., Reeder C., Boyer L.A., Young R.A., Gifford D.K., Wichterle H. Saltatory remodeling of Hox chromatin in response to rostrocaudal patterning signals. Nat. Neurosci. 2013, 16:1191-1198.
30. Meyer A. Hox gene variation and evolution. Nature 1998, 391(225):227-228.
31. Muyrers J.P., Zhang Y., Benes V., Testa G., Ansorge W., Stewart A.F. Point mutation of bacterial artificial chromosomes by ET recombination. EMBO Rep 2000, 1:239-243.
32. Nolte C., Amores A., Nagy Kovacs E., Postlethwait J., Featherstone M. The role of a retinoic acid response element in establishing the anterior neural expression border of Hoxd4 transgenes. Mech. Dev. 2003, 120:325-335.
33. 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. 2013, 383:158-173.
34. Nolte C., Rastegar M., Amores A., Bouchard M., Grote D., Maas R., Kovacs E.N., Postlethwait J., Rambaldi I., Rowan S., Yan Y.L., Zhang F., Featherstone M. Stereospecificity and PAX6 function direct Hoxd4 neural enhancer activity along the antero-posterior axis. Dev. Biol. 2006, 299:582-593.
35. Oosterveen T., Meijlink F., Deschamps J. Expression of retinaldehyde dehydrogenase II and sequential activation of 5' Hoxb genes in the mouse caudal hindbrain. Gene. Expr. Patterns 2004, 4:243-247.
36. Oosterveen T., Niederreither K., Dolle P., Chambon P., Meijlink F., Deschamps J. Retinoids regulate the anterior expression boundaries of 5' Hoxb genes in posterior hindbrain. EMBO J. 2003, 22:262-269.
37. 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 2003, 278:24103-24107.
38. Parrish M., Unruh J., Krumlauf R. BAC modification through serial or simultaneous use of CRE/Lox technology. J. Biomed. Biotechnol. 2011, 2011:924068.
39. Pikaart M.J., Recillas-Targa F., Felsenfeld G. Loss of transcriptional activity of a transgene is accompanied by DNA methylation and histone deacetylation and is prevented by insulators. Genes Dev. 1998, 12:2852-2862.
40. Ramirez-Solis R., Liu P., Bradley A. Chromosome engineering in mice. Nature 1995, 378:720-724.
41. Rhinn M., Dolle P. Retinoic acid signalling during development. Development 2012, 139:843-858.
42. Sharpe J., Nonchev S., Gould A., Whiting J., Krumlauf R. Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO J. 1998, 17:1788-1798.
43. Sirbu I.O., Gresh L., Barra J., Duester G. Shifting boundaries of retinoic acid activity control hindbrain segmental gene expression. Development 2005, 132:2611-2622.
44. Soshnikova N., Dewaele R., Janvier P., Krumlauf R., Duboule D. Duplications of hox gene clusters and the emergence of vertebrates. Dev. Biol. 2013, 378:194-199.
45. Spitz F., Gonzalez F., Duboule D. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 2003, 113:405-417.
46. Studer M., Gavalas A., Marshall H., Ariza-McNaughton L., Rijli F.M., Chambon P., Krumlauf R. Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 1998, 125:1025-1036.
47. 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 1994, 265:1728-1732.
48. Tschopp P., Duboule D. A genetic approach to the transcriptional regulation of Hox gene clusters. Annu. Rev. Genet. 2011, 45:145-166.
49. Tümpel S., Wiedemann L.M., Krumlauf R. Hox genes and segmentation of the vertebrate hindbrain. HOX Genes 2009, 103-137. Academic Press, Burlington. O. Pourquié (Ed.).
50. Valarche I., de Graaff W., Deschamps J. A 3' remote control region is a candidate to modulate Hoxb-8 expression boundaries. Int. J. Dev. Biol. 1997, 41:705-714.
51. Valarché I., De Graff W., Deschamps J. A 3' remote control region is a candidate to modulate Hoxb8 expression boundaries. Int. J. Dev. Biol. 1997, 41:705-714.
52. van der Hoeven F., Zakany J., Duboule D. Gene transpositions in the HoxD complex reveal a hierarchy of regulatory controls. Cell 1996, 85:1025-1035.
53. Vogels R., Charite J., de Graaff W., Deschamps J. Proximal cis-acting elements co-operate to set Hox-b7 (Hox-2.3) expression boundaries in transgenic mice. Development 1993, 117:71-82.
54. 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., Beck F., Mallo M., Deschamps J. Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Dev. Cell 2009, 17:516-526.