Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1995 Dec;15(12):6601–6612. doi: 10.1128/mcb.15.12.6601

Functional reconstruction of trans regulation of the Ultrabithorax promoter by the products of two antagonistic genes, trithorax and Polycomb.

Y L Chang 1, B O King 1, M O'Connor 1, A Mazo 1, D H Huang 1
PMCID: PMC230913  PMID: 8524225

Abstract

Maintenance of the "on-off" state of Drosophila homeotic genes in Antennapedia and bithorax complexes requires activities of the trithorax and Polycomb groups of genes. To identify cis-acting sequences for functional reconstruction of regulation by both trithorax and Polycomb, we examined the expression patterns of several Ubx-lacZ transgenes that carry upstream fragments corresponding to a region of approximately 50 kb. A 14.5-kb fragment from the postbithorax/bithoraxoid region of Ultrabithorax exhibited proper regulation by both trithorax and Polycomb in the embryonic central nervous system. Using a Drosophila haploid cell line for transient expression, we found that trithorax or Polycomb can function independently through this upstream fragment to activate or repress the Ultrabithorax promoter, respectively. Studies of deletion mutants of trithorax and Polycomb demonstrated that trithorax-dependent activation requires the central zinc-binding domain, while Polycomb-dependent repression requires the intact chromodomain. In addition, trithorax-dependent activity can be abrogated by increasing the amount of Polycomb, suggesting a competitive interaction between the products of trithorax and Polycomb. Deletion analysis of this fragment demonstrated that a 440-bp fragment contains response elements for both trithorax and Polycomb. Furthermore, we showed that the integrity of the proximal promoter region is essential for trithorax-dependent activation, implicating a long-range interaction for promoter activation.

Full Text

The Full Text of this article is available as a PDF (1.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beachy P. A., Helfand S. L., Hogness D. S. Segmental distribution of bithorax complex proteins during Drosophila development. Nature. 1985 Feb 14;313(6003):545–551. doi: 10.1038/313545a0. [DOI] [PubMed] [Google Scholar]
  2. Bender W., Akam M., Karch F., Beachy P. A., Peifer M., Spierer P., Lewis E. B., Hogness D. S. Molecular Genetics of the Bithorax Complex in Drosophila melanogaster. Science. 1983 Jul 1;221(4605):23–29. doi: 10.1126/science.221.4605.23. [DOI] [PubMed] [Google Scholar]
  3. Bender W., Weiffenbach B., Karch F., Peifer M. Domains of cis-interaction in the bithorax complex. Cold Spring Harb Symp Quant Biol. 1985;50:173–180. doi: 10.1101/sqb.1985.050.01.023. [DOI] [PubMed] [Google Scholar]
  4. Benson M., Pirrotta V. The Drosophila zeste protein binds cooperatively to sites in many gene regulatory regions: implications for transvection and gene regulation. EMBO J. 1988 Dec 1;7(12):3907–3915. doi: 10.1002/j.1460-2075.1988.tb03277.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bienz M. Molecular mechanisms of determination in Drosophila. Curr Opin Cell Biol. 1992 Dec;4(6):955–961. doi: 10.1016/0955-0674(92)90124-u. [DOI] [PubMed] [Google Scholar]
  6. Biggin M. D., Bickel S., Benson M., Pirrotta V., Tjian R. Zeste encodes a sequence-specific transcription factor that activates the Ultrabithorax promoter in vitro. Cell. 1988 Jun 3;53(5):713–722. doi: 10.1016/0092-8674(88)90089-x. [DOI] [PubMed] [Google Scholar]
  7. Biggin M. D., Tjian R. Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell. 1988 Jun 3;53(5):699–711. doi: 10.1016/0092-8674(88)90088-8. [DOI] [PubMed] [Google Scholar]
  8. Breen T. R., Harte P. J. Molecular characterization of the trithorax gene, a positive regulator of homeotic gene expression in Drosophila. Mech Dev. 1991 Sep;35(2):113–127. doi: 10.1016/0925-4773(91)90062-b. [DOI] [PubMed] [Google Scholar]
  9. Breen T. R., Harte P. J. Trithorax regulates multiple homeotic genes in the bithorax and Antennapedia complexes and exerts different tissue-specific, parasegment-specific and promoter-specific effects on each. Development. 1993 Jan;117(1):119–134. doi: 10.1242/dev.117.1.119. [DOI] [PubMed] [Google Scholar]
  10. Bunker C. A., Kingston R. E. Transcriptional repression by Drosophila and mammalian Polycomb group proteins in transfected mammalian cells. Mol Cell Biol. 1994 Mar;14(3):1721–1732. doi: 10.1128/mcb.14.3.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Castelli-Gair J. E., García-Bellido A. Interactions of Polycomb and trithorax with cis regulatory regions of Ultrabithorax during the development of Drosophila melanogaster. EMBO J. 1990 Dec;9(13):4267–4275. doi: 10.1002/j.1460-2075.1990.tb07875.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chan C. S., Rastelli L., Pirrotta V. A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J. 1994 Jun 1;13(11):2553–2564. doi: 10.1002/j.1460-2075.1994.tb06545.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chinwalla V., Jane E. P., Harte P. J. The Drosophila trithorax protein binds to specific chromosomal sites and is co-localized with Polycomb at many sites. EMBO J. 1995 May 1;14(9):2056–2065. doi: 10.1002/j.1460-2075.1995.tb07197.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. DeCamillis M., Cheng N. S., Pierre D., Brock H. W. The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb. Genes Dev. 1992 Feb;6(2):223–232. doi: 10.1101/gad.6.2.223. [DOI] [PubMed] [Google Scholar]
  15. Debec A., Courgeon A. M., Maingourd M., Maisonhaute C. The response of the centrosome to heat shock and related stresses in a Drosophila cell line. J Cell Sci. 1990 Jul;96(Pt 3):403–412. doi: 10.1242/jcs.96.3.403. [DOI] [PubMed] [Google Scholar]
  16. Denell R. E., Frederick R. D. Homoeosis in Drosophila: a description of the Polycomb lethal syndrome. Dev Biol. 1983 May;97(1):34–47. doi: 10.1016/0012-1606(83)90061-1. [DOI] [PubMed] [Google Scholar]
  17. Di Nocera P. P., Dawid I. B. Transient expression of genes introduced into cultured cells of Drosophila. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7095–7098. doi: 10.1073/pnas.80.23.7095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Digan M. E., Haynes S. R., Mozer B. A., Dawid I. B., Forquignon F., Gans M. Genetic and molecular analysis of fs(1)h, a maternal effect homeotic gene in Drosophila. Dev Biol. 1986 Mar;114(1):161–169. doi: 10.1016/0012-1606(86)90392-1. [DOI] [PubMed] [Google Scholar]
  19. Duncan I. The bithorax complex. Annu Rev Genet. 1987;21:285–319. doi: 10.1146/annurev.ge.21.120187.001441. [DOI] [PubMed] [Google Scholar]
  20. Farkas G., Gausz J., Galloni M., Reuter G., Gyurkovics H., Karch F. The Trithorax-like gene encodes the Drosophila GAGA factor. Nature. 1994 Oct 27;371(6500):806–808. doi: 10.1038/371806a0. [DOI] [PubMed] [Google Scholar]
  21. Franke A., DeCamillis M., Zink D., Cheng N., Brock H. W., Paro R. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J. 1992 Aug;11(8):2941–2950. doi: 10.1002/j.1460-2075.1992.tb05364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gehring W. J., Qian Y. Q., Billeter M., Furukubo-Tokunaga K., Schier A. F., Resendez-Perez D., Affolter M., Otting G., Wüthrich K. Homeodomain-DNA recognition. Cell. 1994 Jul 29;78(2):211–223. doi: 10.1016/0092-8674(94)90292-5. [DOI] [PubMed] [Google Scholar]
  23. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gu Y., Nakamura T., Alder H., Prasad R., Canaani O., Cimino G., Croce C. M., Canaani E. The t(4;11) chromosome translocation of human acute leukemias fuses the ALL-1 gene, related to Drosophila trithorax, to the AF-4 gene. Cell. 1992 Nov 13;71(4):701–708. doi: 10.1016/0092-8674(92)90603-a. [DOI] [PubMed] [Google Scholar]
  25. Han K., Levine M. S., Manley J. L. Synergistic activation and repression of transcription by Drosophila homeobox proteins. Cell. 1989 Feb 24;56(4):573–583. doi: 10.1016/0092-8674(89)90580-1. [DOI] [PubMed] [Google Scholar]
  26. Harding K., Levine M. Gap genes define the limits of antennapedia and bithorax gene expression during early development in Drosophila. EMBO J. 1988 Jan;7(1):205–214. doi: 10.1002/j.1460-2075.1988.tb02801.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hayashi S., Scott M. P. What determines the specificity of action of Drosophila homeodomain proteins? Cell. 1990 Nov 30;63(5):883–894. doi: 10.1016/0092-8674(90)90492-w. [DOI] [PubMed] [Google Scholar]
  28. Ingham P. W. Genetic control of the spatial pattern of selector gene expression in Drosophila. Cold Spring Harb Symp Quant Biol. 1985;50:201–208. doi: 10.1101/sqb.1985.050.01.026. [DOI] [PubMed] [Google Scholar]
  29. Ingham P. W., Martinez-Arias A. The correct activation of Antennapedia and bithorax complex genes requires the fushi tarazu gene. Nature. 1986 Dec 11;324(6097):592–597. doi: 10.1038/324592a0. [DOI] [PubMed] [Google Scholar]
  30. Irish V. F., Martinez-Arias A., Akam M. Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. EMBO J. 1989 May;8(5):1527–1537. doi: 10.1002/j.1460-2075.1989.tb03537.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Irvine K. D., Helfand S. L., Hogness D. S. The large upstream control region of the Drosophila homeotic gene Ultrabithorax. Development. 1991 Feb;111(2):407–424. doi: 10.1242/dev.111.2.407. [DOI] [PubMed] [Google Scholar]
  32. Jones R. S., Gelbart W. M. The Drosophila Polycomb-group gene Enhancer of zeste contains a region with sequence similarity to trithorax. Mol Cell Biol. 1993 Oct;13(10):6357–6366. doi: 10.1128/mcb.13.10.6357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kaufman T. C., Seeger M. A., Olsen G. Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster. Adv Genet. 1990;27:309–362. doi: 10.1016/s0065-2660(08)60029-2. [DOI] [PubMed] [Google Scholar]
  34. Kennison J. A., Tamkun J. W. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136–8140. doi: 10.1073/pnas.85.21.8136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kennison J. A. Transcriptional activation of Drosophila homeotic genes from distant regulatory elements. Trends Genet. 1993 Mar;9(3):75–79. doi: 10.1016/0168-9525(93)90227-9. [DOI] [PubMed] [Google Scholar]
  36. Krasnow M. A., Saffman E. E., Kornfeld K., Hogness D. S. Transcriptional activation and repression by Ultrabithorax proteins in cultured Drosophila cells. Cell. 1989 Jun 16;57(6):1031–1043. doi: 10.1016/0092-8674(89)90341-3. [DOI] [PubMed] [Google Scholar]
  37. Kuzin B., Tillib S., Sedkov Y., Mizrokhi L., Mazo A. The Drosophila trithorax gene encodes a chromosomal protein and directly regulates the region-specific homeotic gene fork head. Genes Dev. 1994 Oct 15;8(20):2478–2490. doi: 10.1101/gad.8.20.2478. [DOI] [PubMed] [Google Scholar]
  38. Laney J. D., Biggin M. D. zeste, a nonessential gene, potently activates Ultrabithorax transcription in the Drosophila embryo. Genes Dev. 1992 Aug;6(8):1531–1541. doi: 10.1101/gad.6.8.1531. [DOI] [PubMed] [Google Scholar]
  39. Lawrence P. A., Morata G. Homeobox genes: their function in Drosophila segmentation and pattern formation. Cell. 1994 Jul 29;78(2):181–189. doi: 10.1016/0092-8674(94)90289-5. [DOI] [PubMed] [Google Scholar]
  40. Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
  41. Locke J., Kotarski M. A., Tartof K. D. Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect. Genetics. 1988 Sep;120(1):181–198. doi: 10.1093/genetics/120.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lonie A., D'Andrea R., Paro R., Saint R. Molecular characterisation of the Polycomblike gene of Drosophila melanogaster, a trans-acting negative regulator of homeotic gene expression. Development. 1994 Sep;120(9):2629–2636. doi: 10.1242/dev.120.9.2629. [DOI] [PubMed] [Google Scholar]
  43. Martin E. C., Adler P. N. The Polycomb group gene Posterior Sex Combs encodes a chromosomal protein. Development. 1993 Feb;117(2):641–655. doi: 10.1242/dev.117.2.641. [DOI] [PubMed] [Google Scholar]
  44. Martínez-Laborda A., González-Reyes A., Morata G. Trans regulation in the Ultrabithorax gene of Drosophila: alterations in the promoter enhance transvection. EMBO J. 1992 Oct;11(10):3645–3652. doi: 10.1002/j.1460-2075.1992.tb05449.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Mazo A. M., Huang D. H., Mozer B. A., Dawid I. B. The trithorax gene, a trans-acting regulator of the bithorax complex in Drosophila, encodes a protein with zinc-binding domains. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2112–2116. doi: 10.1073/pnas.87.6.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell. 1992 Jan 24;68(2):283–302. doi: 10.1016/0092-8674(92)90471-n. [DOI] [PubMed] [Google Scholar]
  47. Messmer S., Franke A., Paro R. Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev. 1992 Jul;6(7):1241–1254. doi: 10.1101/gad.6.7.1241. [DOI] [PubMed] [Google Scholar]
  48. Milner C. M., Campbell R. D. The G9a gene in the human major histocompatibility complex encodes a novel protein containing ankyrin-like repeats. Biochem J. 1993 Mar 15;290(Pt 3):811–818. doi: 10.1042/bj2900811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Müller J., Bienz M. Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo. EMBO J. 1991 Nov;10(11):3147–3155. doi: 10.1002/j.1460-2075.1991.tb04876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Müller J., Bienz M. Sharp anterior boundary of homeotic gene expression conferred by the fushi tarazu protein. EMBO J. 1992 Oct;11(10):3653–3661. doi: 10.1002/j.1460-2075.1992.tb05450.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Müller J. Transcriptional silencing by the Polycomb protein in Drosophila embryos. EMBO J. 1995 Mar 15;14(6):1209–1220. doi: 10.1002/j.1460-2075.1995.tb07104.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Orlando V., Paro R. Mapping Polycomb-repressed domains in the bithorax complex using in vivo formaldehyde cross-linked chromatin. Cell. 1993 Dec 17;75(6):1187–1198. doi: 10.1016/0092-8674(93)90328-n. [DOI] [PubMed] [Google Scholar]
  53. Paro R., Hogness D. S. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):263–267. doi: 10.1073/pnas.88.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Paro R. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 1990 Dec;6(12):416–421. doi: 10.1016/0168-9525(90)90303-n. [DOI] [PubMed] [Google Scholar]
  55. Paro R. Mechanisms of heritable gene repression during development of Drosophila. Curr Opin Cell Biol. 1993 Dec;5(6):999–1005. doi: 10.1016/0955-0674(93)90084-4. [DOI] [PubMed] [Google Scholar]
  56. Parry P., Djabali M., Bower M., Khristich J., Waterman M., Gibbons B., Young B. D., Evans G. Structure and expression of the human trithorax-like gene 1 involved in acute leukemias. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4738–4742. doi: 10.1073/pnas.90.10.4738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pearce J. J., Singh P. B., Gaunt S. J. The mouse has a Polycomb-like chromobox gene. Development. 1992 Apr;114(4):921–929. doi: 10.1242/dev.114.4.921. [DOI] [PubMed] [Google Scholar]
  58. Peifer M., Bender W. The anterobithorax and bithorax mutations of the bithorax complex. EMBO J. 1986 Sep;5(9):2293–2303. doi: 10.1002/j.1460-2075.1986.tb04497.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Qian S., Capovilla M., Pirrotta V. The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J. 1991 Jun;10(6):1415–1425. doi: 10.1002/j.1460-2075.1991.tb07662.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Rastelli L., Chan C. S., Pirrotta V. Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. EMBO J. 1993 Apr;12(4):1513–1522. doi: 10.1002/j.1460-2075.1993.tb05795.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sato T., Denell R. E. Homoeosis in Drosophila: The Lethal Syndrome of the Regulator of bithorax (or trithorax) Locus and Its Interaction with Other Homoeotic Loci. Genetics. 1987 Jul;116(3):389–398. doi: 10.1093/genetics/116.3.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Sedkov Y., Tillib S., Mizrokhi L., Mazo A. The bithorax complex is regulated by trithorax earlier during Drosophila embryogenesis than is the Antennapedia complex, correlating with a bithorax-like expression pattern of distinct early trithorax transcripts. Development. 1994 Jul;120(7):1907–1917. doi: 10.1242/dev.120.7.1907. [DOI] [PubMed] [Google Scholar]
  63. Shearn A. The ash-1, ash-2 and trithorax genes of Drosophila melanogaster are functionally related. Genetics. 1989 Mar;121(3):517–525. doi: 10.1093/genetics/121.3.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Shimell M. J., Simon J., Bender W., O'Connor M. B. Enhancer point mutation results in a homeotic transformation in Drosophila. Science. 1994 May 13;264(5161):968–971. doi: 10.1126/science.7909957. [DOI] [PubMed] [Google Scholar]
  65. Simon J., Chiang A., Bender W., Shimell M. J., O'Connor M. Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev Biol. 1993 Jul;158(1):131–144. doi: 10.1006/dbio.1993.1174. [DOI] [PubMed] [Google Scholar]
  66. Simon J., Peifer M., Bender W., O'Connor M. Regulatory elements of the bithorax complex that control expression along the anterior-posterior axis. EMBO J. 1990 Dec;9(12):3945–3956. doi: 10.1002/j.1460-2075.1990.tb07615.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Singh P. B. Molecular mechanisms of cellular determination: their relation to chromatin structure and parental imprinting. J Cell Sci. 1994 Oct;107(Pt 10):2653–2668. doi: 10.1242/jcs.107.10.2653. [DOI] [PubMed] [Google Scholar]
  68. Soeller W. C., Oh C. E., Kornberg T. B. Isolation of cDNAs encoding the Drosophila GAGA transcription factor. Mol Cell Biol. 1993 Dec;13(12):7961–7970. doi: 10.1128/mcb.13.12.7961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tamkun J. W., Deuring R., Scott M. P., Kissinger M., Pattatucci A. M., Kaufman T. C., Kennison J. A. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell. 1992 Feb 7;68(3):561–572. doi: 10.1016/0092-8674(92)90191-e. [DOI] [PubMed] [Google Scholar]
  70. Thummel C. S., Boulet A. M., Lipshitz H. D. Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene. 1988 Dec 30;74(2):445–456. doi: 10.1016/0378-1119(88)90177-1. [DOI] [PubMed] [Google Scholar]
  71. Tkachuk D. C., Kohler S., Cleary M. L. Involvement of a homolog of Drosophila trithorax by 11q23 chromosomal translocations in acute leukemias. Cell. 1992 Nov 13;71(4):691–700. doi: 10.1016/0092-8674(92)90602-9. [DOI] [PubMed] [Google Scholar]
  72. Tschiersch B., Hofmann A., Krauss V., Dorn R., Korge G., Reuter G. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 1994 Aug 15;13(16):3822–3831. doi: 10.1002/j.1460-2075.1994.tb06693.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Tsukiyama T., Becker P. B., Wu C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature. 1994 Feb 10;367(6463):525–532. doi: 10.1038/367525a0. [DOI] [PubMed] [Google Scholar]
  74. Wedeen C., Harding K., Levine M. Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell. 1986 Mar 14;44(5):739–748. doi: 10.1016/0092-8674(86)90840-8. [DOI] [PubMed] [Google Scholar]
  75. White R. A., Lehmann R. A gap gene, hunchback, regulates the spatial expression of Ultrabithorax. Cell. 1986 Oct 24;47(2):311–321. doi: 10.1016/0092-8674(86)90453-8. [DOI] [PubMed] [Google Scholar]
  76. White R. A., Wilcox M. Distribution of Ultrabithorax proteins in Drosophila. EMBO J. 1985 Aug;4(8):2035–2043. doi: 10.1002/j.1460-2075.1985.tb03889.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. White R. A., Wilcox M. Protein products of the bithorax complex in Drosophila. Cell. 1984 Nov;39(1):163–171. doi: 10.1016/0092-8674(84)90202-2. [DOI] [PubMed] [Google Scholar]
  78. Zhang C. C., Müller J., Hoch M., Jäckle H., Bienz M. Target sequences for hunchback in a control region conferring Ultrabithorax expression boundaries. Development. 1991 Dec;113(4):1171–1179. doi: 10.1242/dev.113.4.1171. [DOI] [PubMed] [Google Scholar]
  79. Zink B., Paro R. In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster. Nature. 1989 Feb 2;337(6206):468–471. doi: 10.1038/337468a0. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES