Multiple levels of transcriptional and post-transcriptional regulation are required to define the domain of Hoxb4 expression

Development

Volumn 130, Issue 12, 2003, Pages 2717-2728

  Brend, Tim ^a,b   Gilthorpe, Jonathan ^b,c   Summerbell, Dennis ^a,b   Rigby, Peter W J ^a,b  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Anterior boundary; Hoxb4; Maintenance; Mouse; Paraxial mesoderm; RNA stability; Transcription; Translation

Indexed keywords

HOX PROTEIN; HOMEODOMAIN PROTEIN; HOXB4 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENHANCER REGION; GENE EXPRESSION; GENE SEQUENCE; HOX GENE; INTRON; MESODERM; MOUSE; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; RNA TRANSLATION; SOMITE; TRANSCRIPTION REGULATION; TRANSGENE; ANIMAL; ARTICLE; BIOSYNTHESIS; CENTRAL NERVOUS SYSTEM; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROMOTER REGION; REPORTER GENE; TRANSGENIC MOUSE;

ANIMALIA; MAMMALIA;

ANIMALS; CENTRAL NERVOUS SYSTEM; DOWN-REGULATION; EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HOMEODOMAIN PROTEINS; MICE; MICE, TRANSGENIC; PROMOTER REGIONS (GENETICS); SOMITES; TRANSCRIPTION FACTORS; TRANSGENES;

EID: 0042913184     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00471     Document Type: Review

References (50)

1. Akasaka, T., van Lohuizen, M., van der Lugt, N., Mizutani-Koseki, Y., Kanno, M., Taniguchi, M., Vidal, M., Alkema, M., Berns, A. and Koseki, H. (2001). Mice doubly deficient for the Polycomb Group genes Mel18 and Bmi1 reveal synergy and requirement for maintenance but not activation of Hox gene expression. Development 128, 1587-1597.
2. Amores, A., Force, A., Yan, Y.-L., Joly, L., Amemiya, C., Fritz, A., Ho, R. K., Langeland, J., Prince, V., Wang, Y.-L. et al. (1998). Zebrafish Hox clusters and vertebrate genome evolution. Science 282, 1711-1714.
3. Aparicio, S., Morrison, A., Gould, A., Gilthorpe, J., Chaudhuri, C., Rigby, P., Krumlauf, R. and Brenner, S. (1995). Detecting conserved regulatory elements with the model genome of the Japanese puffer fish, Fugu rubripes. Proc. Natl. Acad. Sci. USA 92, 1684-1688.
4. Awgulewitsch, A. and Jacobs, D. (1990). Differential expression of Hox 3.1 protein in subregions of the embryonic and adult spinal cord. Development 108, 411-420.
5. Behringer, R. R., Crotty, D. A., Tennyson, V. M., Brinster, R. L., Palmiter, R. D. and Wolgemuth, D. J. (1993). Sequences 5′ of the homeobox of the Hox-1.4 gene direct tissue-specific expression of lacZ during mouse development. Development 117, 823-833.
6. Bel-Vialar, S., Coré, N., Terranova, R., Goudot, V., Boned, A. and Djabali, M. (2000). Altered retinoic acid sensitivity and temporal expression of Hox genes in Polycomb-M33-deficient mice. Dev. Biol. 224, 238-249.
7. Belting, H.-G., Shashikant, C. S. and Ruddle, F. H. (1998). Multiple phases of expression and regulation of mouse Hoxc8 during early embryology. J. Exp. Zool. 282, 196-222.
8. Bradshaw, M. S., Shashikant, C. S., Belting, H.-G., Bollekens, J. A. and Ruddle, F. H. (1996). A long-range regulatory element of Hoxc8 identified by using the pClasper vector. Proc. Natl. Acad. Sci. USA 93, 2426-2430.
9. Burke, A. C., Nelson, C. E., Morgan, B. A. and Tabin, C. (1995). Hox genes and the evolution of vertebrate axial morphology. Development 121, 333-346.
10. Butler, J. E. and Kadonaga, J. T. (2001). Enhancer-promoter specificity mediated by DPE or TATA core promoter motifs. Genes Dev. 15, 2515-2519.
11. Conlon, R. A. and Rossant, J. (1992). Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116, 357-368.
12. de Rosa, R., Grenier, J. K., Andreeva, T., Cook, C. E., Adoutte, A., Akam, M., Carroll, S. B. and Balavoine, G. (1999). Hox genes in brachiopods and priapulids and protostome evolution. Nature 399, 772-776.
13. Dubrelle, J., McGrew, M. J. and Pourquié, O. (2001). FGF signalling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106, 219-232.
14. Ferrier, D. E. K. and Holland, P. W. H. (2001). Ancient origin of the Hox gene cluster. Nat. Rev. Genet. 2, 33-37.
15. Gilthorpe, J. D. and Rigby, P. W. J. (1999). Reporter genes for the study of transcriptional regulation in transgenic mouse embryos. Methods Mol. Biol. 97, 159-182.
16. Gilthorpe, J., Vandromme, M., Brend, T., Gutman, A., Summerbell, D., Totty, N. and Rigby, P. W. J. (2002). Spatially specific expression of Hoxb4 is dependent on the ubiquitous transcription factor NFY. Development 129, 3887-3899.
17. Gould, A. (1997). Functions of mammalian Polycomb group and trithorax group related genes. Curr. Opin. Genet. Dev. 7, 488-494.
18. Gould, A., Morrison, A., Sproat, G., White, R. A. H. and Krumlauf, R. (1997). Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 11, 900-913.
19. Gould, A., Itsaki, N. and Krumlauf, R. (1998). Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 21, 39-51.
20. Gutman, A., Gilthorpe, J. and Rigby, P. W. J. (1994). Multiple positive and negative regulatory elements in the promoter of the mouse homeobox gene Hoxb-4. Mol. Cell. Biol. 14, 8143-8154.
21. Izpisùa-Belmonte, J. C., Dollé, P., Renucci, A., Zappavigna, V., Falkenstein, H. and Duboule, D. (1990). Primary structure and embryonic expression pattern of the mouse Hox-4.3 homeobox gene. Development 110, 733-745.
22. Jack, T. and McGinnis, W. (1990). Establishment of the Deformed expression stripe requires the combinatorial action of coordinate, gap and pair-rule proteins. EMBO J. 9, 1187-1198.
23. Keegan, L. P., Haerry, T. E., Crotty, D. A., Packer, A. I., Wolgemuth, D. J. and Gehring, W. J. (1997). A sequence conserved in vertebrate Hox gene introns functions as an enhancer regulated by posterior homeotic genes in Drosophila imaginal discs. Mech. Dev. 63, 145-157.
24. Kennison, J. A. (1995). The Polycomb and Trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu. Rev. Genet. 29, 289-303.
25. Kondo, T. and Duboule, D. (1999). Breaking colinearity in the mouse HoxD complex. Cell 97, 407-417.
26. Maconochie, M. K., Nonchev, S., Studer, M., Chan, S.-K., Pöpperl, H., Sham, M. H., Mann, R. S. and Krumlauf, R. (1997). Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhombomere 4 is regulated by Hoxb1. Genes Dev. 11, 1885-1895.
27. Manzanares, M., Bel-Vialar, S., Ariza-McNaughton, L., Ferretti, E., Marshall, H., Maconochie, M., Blasi, F. and Krumlauf, R. (2001). Independent regulation of initiation and maintenance phases of Hoxa3 expression in the vertebrate hindbrain involve auto- and cross-regulatory mechanisms. Development 128, 3595-3607.
28. Marshall, H., Studer, M., Pöpperl, H., Aparicio, S., Kuroiwa, A., Brenner, S. and Krumlauf, R. (1994). A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature 370, 567-571.
29. Miller, D. F. B., Rogers, B. T., Kalkbrenner, A., Hamilton, B., Holtzman, S. L. and Kaufman, T. (2001). Cross-regulation of Hox genes in the Drosophila melanogaster embryo. Mech. Dev. 102, 3-16.
30. Morrison, A., Chaudhuri, C., Ariza-McNaughton, L., Muchamore, I., Kuroiwa, A. and Krumlauf, R. (1995). Comparative analysis of chicken Hoxb-4 regulation in transgenic mice. Mech. Dev. 53, 47-59.
31. Morrison, A., Ariza-McNaughton, L., Gould, A., Featherstone, M. and Krumlauf, R. (1997). HOXD4 and regulation of the group 4 paralog genes. Development 124, 3135-3146.
32. Niessing, D., Driever, W., Sprenger, F., Taubert, H., Jäckle, H. and Rivera-Pomar, R. (2000). Homeodomain position 54 specifies transcriptional versus translational control by Bicoid. Mol. Cell 5, 395-401.
33. Niessing, D., Blanke, S. and Jäckle, H. (2002). Bicoid associates with the 5′-cap bound complex of caudal mRNA and represses translation. Genes Dev. 16, 2576-2582.
34. Ohtsuki, S., Levine, M. and Cai, H. N. (1998). Different core promoters possess distinct regulatory activities in the Drosophila embryo. Genes Dev. 12, 547-556.
35. Oosterveen, T., Niederreither, K., Dollé, P., Chambon, P., Meijlink, F. and Deschamps, J. (2003). Retinoids regulate the anterior expression boundaries of 5′ Hoxb genes in posterior hindbrain. EMBO J. 22, 262-269.
36. Petruk, S., Sedkov, Y., Smith, S., Tillib, S., Kraevski, V., Nakamura, T., Canaani, E., Croce, C. M. and Mazo, A. (2001). Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene. Science 294, 1331-1334.
37. Pöpperl, H., Bienz, M., Studer, M., Chan, S.-K., Aparicio, S., Brenner, S., Mann, R. S. and Krumlauf, R. (1995). Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81, 1031-1042.
38. Sharpe, J., Nonchev, S., Gould, A., Whiting, J. and Krumlauf, R. (1998). Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO J. 17, 1788-1798.
39. Smale, S. T. (2001). Core promoters: active contributors to combinatorial gene regulation. Genes Dev. 15, 2503-2508.
40. Spörle, R. and Schughart, K. (1997). System to identify individual somites and their derivatives in the developing mouse embryo. Dev. Dyn. 210, 216-226.
41. Stauber, M., Jäckle, H. and Schmidt-Ott, U. (1999). The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc. Natl. Acad. Sci. USA 96, 3786-3789.
42. Studer, M., Gavalas, A., Marshall, H., Ariza-McNaughton, L., Rijli, F. M., Chambon, P. and Krumlauf, R. (1998). Genetic interactions between Hoxal and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125, 1025-1036.
43. Summerbell, D., Ashby, P. R., Coutelle, O., Cox, D., Yee, S.-P. and Rigby, P. W. J. (2000). The expression of Myf5 in the developing mouse embryo is controlled by discrete and dispersed enhancers specific for particular populations of skeletal muscle precursors. Development 127, 3745-3757.
44. Teboul, L., Hadchouel, J., Daubas, P., Summerbell, D., Buckingham, M. and Rigby, P. W. J. (2002). The early epaxial enhancer is essential for the initial expression of the skeletal muscle determination gene Myf5 but not for subsequent, multiple phases of somitic myogenesis. Development 129, 4571-4580.
45. Tie, F., Furuyama, T., Prasad-Sinha, J., Jane, E. and Harte, P. J. (2001). The Drosophila Polycomb Group proteins ESC and E(Z) are present in a complex containing the histone-binding protein p55 and the histone deactylase RPD3. Development 128, 275-286.
46. Wall, N. A., Jones, M. C., Hogan, B. L. M. and Wright, C. V. E. (1992). Expression and modification of Hox 2.1 protein in mouse embryos. Mech. Dev. 37, 111-120.
47. Whiting, J., Marshall, H., Cook, M., Krumlauf, R., Rigby, P. W. J., Stott, D. and Allemann, R. K. (1991). Multiple spatially specific enhancers are required to reconstruct the pattern of Hox-2.6 gene expression. Genes Dev. 5, 2048-2059.
48. Yu, B. D., Hanson, R. D., Hess, J. L., Horning, S. E. and Korsmeyer, S. J. (1998). MLL, a mammalian trithorax-group gene, functions as a transcriptional maintenance factor in morphogenesis. Proc. Natl. Acad. Sci. USA 95, 10632-10636.
49. Zákány, J., Kmita, M., Alarcon, P., de la Pompa, J.-L. and Duboule, D. (2001). Localized and transient transcription of Hox genes suggests a link between patterning and the segmentation clock. Cell 106, 207-217.
50. Zhang, F., Popperl, H., Morrison, A., Kovacs, E. N., Prideaux, V., Schwarz, L., Krumlauf, R., Rossant, J. and Featherstone, M. S. (1997). Elements both 5′ and 3′ to the murine Hoxd4 gene establish anterior borders of expression in mesoderm and neuroectoderm. Mech. Dev. 67, 49-58.