A sequence conserved in vertebrate Hox gene introns functions as an enhancer regulated by posterior homeotic genes in Drosophila imaginal discs

Mechanisms of Development

Volumn 63, Issue 2, 1997, Pages 145-157

  Keegan, Liam P ^a   Haerry, Theodor E ^a   Crotty, David A ^b   Packer, Alan I ^b   Wolgemuth, Debra J ^b   Gehring, Walter J ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b Columbia University ^*  (United States)

Author keywords

DNA binding proteins; Drosophila; Homeotic response element; Hoxa 4; Leg development; Mouse

Indexed keywords

ARTICLE; DROSOPHILA; EMBRYO DEVELOPMENT; ENHANCER REGION; GENE SEQUENCE; HOMEOBOX; IMAGINAL DISC; INTRON; NONHUMAN; PRIORITY JOURNAL; VERTEBRATE;

DROSOPHILA MELANOGASTER; MELANOGASTER; VERTEBRATA;

EID: 0030982227     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0925-4773(97)00038-5     Document Type: Article

References (58)

1. 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.
2. Bachiller, D., Macias, A., Duboule, D. and Morata, G. (1994) Conservation of a functional hierarchy between mammalian and insect Hox/HOM genes. EMBO J. 13, 1930-1941.
3. 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.
4. Capovilla, M., Brandt, M. and Botas, J. (1994) Direct regulation of decapentaplegic by Ultrabithorax and its role in Drosophila midgut morphogenesis. Proc. Natl. Acad. Sci. USA 76, 4464-4468.
5. Cianetti, L., Di Cristofaro, A., Zappavigna, V., Bottero, L., Boccoli, G., Testa, U., Russo, G., Boncinelli, E. and Peschle, C. (1990) Molecular mechanisms underlying the expression of the human HOX-5.1 gene. Nucleic Acids Res. 18, 4361-4368.
6. Cohen, S.M. (1993) Imaginai disc development. In Bate, M. and Martinez Arias, A. (eds.), The Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 747-843.
7. Cribbs, D.L., Benassayag, C., Randozzo, F.R. and Kaufman, T. (1995) Levels of homeotic protein function can determine developmental identity: evidence from low level expression of the Drosophila homeotic gene proboscipedia under Hsp70 control. EMBO J. 14, 767-778.
8. Devereux, J., Haeberli, P. and Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12, 387-395.
9. Diaz-Benjumea, F.J., Cohen, B. and Cohen, S.M. (1994) Cell interactions between compartments establishes the proximo-distal axis of Drosophila legs. Nature 372, 175-179.
10. Duboule, D.E. (1994). Guidebook to the Homeobox Genes. Oxford University Press, Oxford.
11. Furukubo-Tokunaga, K., Flister, S. and Gehring, W.J. (1993) Functional specificity of the Antennapedia homeodomain. Proc. Natl. Acad. Sci. USA 90, 6360-6364.
12. Gehring, W.J., Affolter, M. and Bürglin, T. (1994a) Homeodomain proteins. Annu. Rev. Biochem. 63, 487-526.
13. Gehring, W.J., Qian, Y.Q., Billeter, M., Furukubo-Tokunaga, K., Schier, A.F., Resendez-Perez, D., Affolter, M., Otting, O. and Wüthrich, K. (1994b) Homeodomain-DNA recognition. Cell 78, 211-223.
14. Gibson, G. and Gehring, W.J. (1991) P-element-mediated enhancer detection in imaginai discs and third instar larval brain of Drosophila melanogaster. Drosophila Inf. Serv. 70, 78-83.
15. Gibson, G., Schier, A., LeMotte, P. and Gehring, W.J. (1990) The specificities of Sex combs reduced and Antennapedia are defined by a distinct portion of each protein that includes the homeodomain. Cell 62, 1087-1103.
16. Gonzales-Crespo, S. and Morata, G. (1995) Control of Drosophila adult pattern by extradenticle. Development 121, 2117-2125.
17. Gonzales-Rey, A., Urquia, N., Gehring, W.J., Struhl, G. and Morata, G. (1990) Are cross-regulatory interactions between homeotic genes functionally significant? Nature 344, 78-80.
18. Haerry, T. (1994) Are cis-regulatory elements of vertebrate homeobox genes recognized by homeotic proteins in Drosophila? PhD Thesis, University of Basel, Basel.
19. Haerry, T.E. and Gehring, W.J. (1996) The intron of the mouse Hoxa-7 gene contains conserved homeodomain binding sites which can function as an enhancer element in Drosophila. Proc. Natl. Acad. Sci. USA 93, 13884-13889.
20. Haerry, T.E. and Gehring, W.J. (1997) A conserved cluster of homeodomain binding sites in the mouse Hoxa-4 intron functions in Drosophila embryos as an enhancer that is directly regulated by Ultrabithorax. Dev. Biol., in press.
21. Heuer, J.G. and Kaufman, T.C. (1992) Homeotic genes have specific functional roles in the establishment of the Drosophila embryonic peripheral nervous system. Development 115, 35-47.
22. Hiromi, Y., Kuroiwa, A. and Gehring, W.J. (1985) Control elements of the Drosophila segmentation gene fushi tarazu. Cell 43, 603-613.
23. Keegan, L., Gill, G. and Ptashne, M. (1986) Separation of DNA-binding from the transcription-activating function of a eukaryotic regulatory protein. Science 231, 699-704.
24. Kessel, M., Schulze, F., Fibi, M. and Gruss, P. (1987) Primary structure and nuclear localization of a murine homeodomain protein. Proc. Natl. Acad. Sci. USA 84, 5306-5310.
25. Krumlauf, R. (1994) Hox genes in vertebrate development. Cell 78, 191-201.
26. Kuziora, M.A. and McGinnis, W. (1988) Autoregulation of a Drosophila homeotic selector gene. Cell 55, 477-485.
27. 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.
28. LeMotte, P., Kuroiwa, A., Fessier, L.I. and Gehring, W.J. (1989) The homeotic gene Sex combs reduced of Drosophila: gene structure and embryonic expression. EMBO J. 8, 219-227.
29. Mahon, K.A., Westphal, H. and Gruss, P. (1988) Expression of homeobox gene Hox1.1 during mouse embryogenesis. Development 104 (Suppl.), 187-195.
30. Malicki, J., Schughart, K. and McGinnis, W. (1990) Mouse Hox 2.2 specifies thoracic segmental identity in Drosophila embryos and larvae. Cell 63, 961-967.
31. Manak, J.R., Mathies, L.D. and Scott, M.P. (1994) Regulation of a decapentaplegic midgut enhancer by homeotic proteins. Development 120, 3605-3619.
32. Mangelsdorf, D.J. and Evans, R.W. (1995) The RXR heterodimers and orphan receptors. Cell 83, 841-850.
33. Maniatis, T., Fritsch, E.F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Mann, R.S. (1995) The specificity of homeotic gene function. BioEssays 17, 855-863.
35. Mann, R.S. and Chan, S.-K. (1996) Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet. 12, 258-262.
36. Mann, R.S. and Hogness, D.S. (1990) Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell 60, 597-610.
37. Marmorstein, R. and Harrison, S. (1994) Crystal structure of a PPR1-DNA complex: DNA recognition by proteins containing a Zn2Cys2 binuclear cluster. Genes Dev. 8, 2504-2512.
38. Marmorstein, R., Carey, M., Ptashne, M. and Harrison, S. (1992) DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356, 408-414.
39. McGinnis, W. and Krumlauf, R. (1992) Homeobox genes and axial patterning. Cell 68, 283-302.
40. Meyer, B. and Gruss, P. (1993) Mouse Cdx1 expression during gastrulation. Development 117, 191-203.
41. Mlodzik, M., Gibson, G. and Gehring, W.J. (1990) Effects of ectopic expression of caudal during Drosophila development. Development 109, 271-277.
42. 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.
43. Müller, J., Thüringer, F., Biggin, M., Züst, B. and Bienz, M. (1989) Coordinate action of a proximal homeoprotein binding site and a distal sequence confers the Ultrabithorax expression pattern in the visceral mesoderm. EMBO J. 8, 4143-4151.
44. Popperl, 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 on exd/ pbx. Cell 81, 1031-1042.
45. Robertson, A.M., Preston, C.R., Phillis, D., Johnson-Schlitz, D., Genz, W.K. and Engels, W.R. (1988) A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461-470.
46. Sanchez-Herrero, E., Guerrero, I., Sampedro, J. and Gonzalez-Reyes, A. (1994) Developmental consequences of unrestricted expression of the abd-A gene of Drosophila. Mech. Dev. 46, 153-167.
47. Schneuwly, S. and Gehring, W.J. (1985) Homeotic transformation of thorax into head: developmental analysis of a new Antennapedia allele in Drosophila melanogaster. Dev. Biol. 108, 377-386.
48. Schneuwly, S., Klemenz, R. and Gehring, W.J. (1987) Redesigning the body plan of Drosophila by ectopic expression of the homeotic gene Antennapedia. Nature 325, 816-818.
49. Scott, M.P. (1992) Vertebrate homeobox gene nomenclature. Cell 71, 551-553.
50. Subramanian, V., Meyer, B.I. and Gruss, P. (1995) Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell 83, 641-653.
51. Viviano, C.M., Galliot, B. and Wolgemuth, D.J. (1993) Multiple levels of regulation exist for expression of the Hoxa-4 (Hox-1-4) gene in mouse testis. Cell. Mol. Biol. Res. 39, 483-495.
52. Wagner-Bernholz, J.T., Wilson, C., Gibson, G., Schuh, R. and Gehring, W.J. (1991) Identification of target genes of the homeotic gene Antennapedia by enhancer detection. Genes Dev. 5, 2467-2480.
53. Walldorf, U. and Gehring, W.J. (1992) Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J. 11, 2247-2259.
54. Wilde, C.D. and Akam, M. (1987) Conserved sequence elements in the 5′ region of the Ultrabithorax transcription unit. EMBO J. 6, 1393-1401.
55. Wolgemuth, D.J., Behringer, R., Mosteller, M.P., Brinster, R.L. and Palmiter, R.D. (1989) Transgenic mice overexpressing the mouse homeobox-containing gene Hox-1.4 exhibit abnormal gut development. Nature 337, 464-467.
56. Zappavigna, V., Renucci, A., Izpisua-Belmonte, J.-C., Urier, G., Peschle, C. and Duboule, D. (1991) HOX4 gene encode transcription factors with potential auto- and cross-regulatory capacities. EMBO J. 10, 4177-4187.
57. Zeng, W., Andrew, D.J., Mathies, L.D., Horner, M.A. and Scott, M.P. (1993) Ectopic expression and function of the Antp and Scr homeotic genes: the N terminus of the homeodomain is critical to functional specificity. Development 118, 339-352.
58. Zhao, J.J., Lazzarini, R.A. and Pick, L. (1993) The mouse Hox-1.3 gene is functionally equivalent to the Drosophila Sex combs reduced gene. Genes Dev. 7, 343-354.