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. 1997 Oct 15;25(20):3963–3968. doi: 10.1093/nar/25.20.3963

Dynamics of potentiation and activation: GAGA factor and its role in heat shock gene regulation.

R C Wilkins 1, J T Lis 1
PMCID: PMC147008  PMID: 9321643

Abstract

GAGA factor (GAF) binds to specific DNA sequences and participates in a complex spectrum of chromosomal activities.Products of the Trithorax-like locus (Trl), which encodes multiple GAF isoforms, are required for homeotic gene expression and are essential for Drosophila development. While homozygous null mutations in Trl are lethal, heterozygotes display enhanced position effect variegation (PEV) indicative of the broad role of GAF in chromatin architecture and its positive role in gene expression.The distribution of GAF on chromosomes is complex, as it is associated with hundreds of chromosomal loci in euchromatin of salivary gland polytene chromosomes, however, it also displays a strong association with pericentric heterochromatin in diploid cells, where it appears to have roles in chromosome condensation and segregation. At higher resolution GAF binding sites have been identified in the regulatory regions of many genes. In some cases, the positive role of GAF in gene expression has been examined in detail using a variety of genetic, biochemical, and cytological approaches. Here we review what is currently known of GAF and, in the context of the heat shock genes of Drosophila, we examine the effects of GAF on multiple steps in gene expression.

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Selected References

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  1. Bardwell V. J., Treisman R. The POZ domain: a conserved protein-protein interaction motif. Genes Dev. 1994 Jul 15;8(14):1664–1677. doi: 10.1101/gad.8.14.1664. [DOI] [PubMed] [Google Scholar]
  2. Benyajati C., Ewel A., McKeon J., Chovav M., Juan E. Characterization and purification of Adh distal promoter factor 2, Adf-2, a cell-specific and promoter-specific repressor in Drosophila. Nucleic Acids Res. 1992 Sep 11;20(17):4481–4489. doi: 10.1093/nar/20.17.4481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benyajati C., Mueller L., Xu N., Pappano M., Gao J., Mosammaparast M., Conklin D., Granok H., Craig C., Elgin S. Multiple isoforms of GAGA factor, a critical component of chromatin structure. Nucleic Acids Res. 1997 Aug 15;25(16):3345–3353. doi: 10.1093/nar/25.16.3345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bhadra U., Birchler J. A. Characterization of a sex-influenced modifier of gene expression and suppressor of position-effect variegation in Drosophila. Mol Gen Genet. 1996 Mar 20;250(5):601–613. doi: 10.1007/BF02174448. [DOI] [PubMed] [Google Scholar]
  5. Bhat K. M., Farkas G., Karch F., Gyurkovics H., Gausz J., Schedl P. The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division. Development. 1996 Apr;122(4):1113–1124. doi: 10.1242/dev.122.4.1113. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Burns L. G., Peterson C. L. Protein complexes for remodeling chromatin. Biochim Biophys Acta. 1997 Feb 7;1350(2):159–168. doi: 10.1016/s0167-4781(96)00162-5. [DOI] [PubMed] [Google Scholar]
  8. Chen W., Zollman S., Couderc J. L., Laski F. A. The BTB domain of bric à brac mediates dimerization in vitro. Mol Cell Biol. 1995 Jun;15(6):3424–3429. doi: 10.1128/mcb.15.6.3424. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]
  9. Chung Y. T., Keller E. B. Regulatory elements mediating transcription from the Drosophila melanogaster actin 5C proximal promoter. Mol Cell Biol. 1990 Jan;10(1):206–216. doi: 10.1128/mcb.10.1.206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Courey A. J., Tjian R. Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell. 1988 Dec 2;55(5):887–898. doi: 10.1016/0092-8674(88)90144-4. [DOI] [PubMed] [Google Scholar]
  11. Croston G. E., Kerrigan L. A., Lira L. M., Marshak D. R., Kadonaga J. T. Sequence-specific antirepression of histone H1-mediated inhibition of basal RNA polymerase II transcription. Science. 1991 Feb 8;251(4994):643–649. doi: 10.1126/science.1899487. [DOI] [PubMed] [Google Scholar]
  12. De Rubertis F., Kadosh D., Henchoz S., Pauli D., Reuter G., Struhl K., Spierer P. The histone deacetylase RPD3 counteracts genomic silencing in Drosophila and yeast. Nature. 1996 Dec 12;384(6609):589–591. doi: 10.1038/384589a0. [DOI] [PubMed] [Google Scholar]
  13. Dorn R., Krauss V., Reuter G., Saumweber H. The enhancer of position-effect variegation of Drosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11376–11380. doi: 10.1073/pnas.90.23.11376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eissenberg J. C., Cartwright I. L., Thomas G. H., Elgin S. C. Selected topics in chromatin structure. Annu Rev Genet. 1985;19:485–536. doi: 10.1146/annurev.ge.19.120185.002413. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Fischer J. A., Giniger E., Maniatis T., Ptashne M. GAL4 activates transcription in Drosophila. Nature. 1988 Apr 28;332(6167):853–856. doi: 10.1038/332853a0. [DOI] [PubMed] [Google Scholar]
  17. Garabedian M. J., Shepherd B. M., Wensink P. C. A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell. 1986 Jun 20;45(6):859–867. doi: 10.1016/0092-8674(86)90560-x. [DOI] [PubMed] [Google Scholar]
  18. Gerasimova T. I., Gdula D. A., Gerasimov D. V., Simonova O., Corces V. G. A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation. Cell. 1995 Aug 25;82(4):587–597. doi: 10.1016/0092-8674(95)90031-4. [DOI] [PubMed] [Google Scholar]
  19. Giardina C., Lis J. T. Polymerase processivity and termination on Drosophila heat shock genes. J Biol Chem. 1993 Nov 15;268(32):23806–23811. [PubMed] [Google Scholar]
  20. Gill G., Pascal E., Tseng Z. H., Tjian R. A glutamine-rich hydrophobic patch in transcription factor Sp1 contacts the dTAFII110 component of the Drosophila TFIID complex and mediates transcriptional activation. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):192–196. doi: 10.1073/pnas.91.1.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gilmour D. S., Lis J. T. In vivo interactions of RNA polymerase II with genes of Drosophila melanogaster. Mol Cell Biol. 1985 Aug;5(8):2009–2018. doi: 10.1128/mcb.5.8.2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gilmour D. S., Thomas G. H., Elgin S. C. Drosophila nuclear proteins bind to regions of alternating C and T residues in gene promoters. Science. 1989 Sep 29;245(4925):1487–1490. doi: 10.1126/science.2781290. [DOI] [PubMed] [Google Scholar]
  23. Glaser R. L., Lis J. T. Multiple, compensatory regulatory elements specify spermatocyte-specific expression of the Drosophila melanogaster hsp26 gene. Mol Cell Biol. 1990 Jan;10(1):131–137. doi: 10.1128/mcb.10.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Glaser R. L., Thomas G. H., Siegfried E., Elgin S. C., Lis J. T. Optimal heat-induced expression of the Drosophila hsp26 gene requires a promoter sequence containing (CT)n.(GA)n repeats. J Mol Biol. 1990 Feb 20;211(4):751–761. doi: 10.1016/0022-2836(90)90075-W. [DOI] [PubMed] [Google Scholar]
  25. Granok H., Leibovitch B. A., Shaffer C. D., Elgin S. C. Chromatin. Ga-ga over GAGA factor. Curr Biol. 1995 Mar 1;5(3):238–241. doi: 10.1016/s0960-9822(95)00048-0. [DOI] [PubMed] [Google Scholar]
  26. Greisman H. A., Pabo C. O. A general strategy for selecting high-affinity zinc finger proteins for diverse DNA target sites. Science. 1997 Jan 31;275(5300):657–661. doi: 10.1126/science.275.5300.657. [DOI] [PubMed] [Google Scholar]
  27. Henchoz S., De Rubertis F., Pauli D., Spierer P. The dose of a putative ubiquitin-specific protease affects position-effect variegation in Drosophila melanogaster. Mol Cell Biol. 1996 Oct;16(10):5717–5725. doi: 10.1128/mcb.16.10.5717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ito T., Bulger M., Pazin M. J., Kobayashi R., Kadonaga J. T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell. 1997 Jul 11;90(1):145–155. doi: 10.1016/s0092-8674(00)80321-9. [DOI] [PubMed] [Google Scholar]
  29. Judd B. H. Mutations of zeste that mediate transvection are recessive enhancers of position-effect variegation in Drosophila melanogaster. Genetics. 1995 Sep;141(1):245–253. doi: 10.1093/genetics/141.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kao S. Y., Calman A. F., Luciw P. A., Peterlin B. M. Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature. 1987 Dec 3;330(6147):489–493. doi: 10.1038/330489a0. [DOI] [PubMed] [Google Scholar]
  31. Kerrigan L. A., Croston G. E., Lira L. M., Kadonaga J. T. Sequence-specific transcriptional antirepression of the Drosophila Krüppel gene by the GAGA factor. J Biol Chem. 1991 Jan 5;266(1):574–582. [PubMed] [Google Scholar]
  32. Krumm A., Hickey L. B., Groudine M. Promoter-proximal pausing of RNA polymerase II defines a general rate-limiting step after transcription initiation. Genes Dev. 1995 Mar 1;9(5):559–572. doi: 10.1101/gad.9.5.559. [DOI] [PubMed] [Google Scholar]
  33. Krumm A., Meulia T., Brunvand M., Groudine M. The block to transcriptional elongation within the human c-myc gene is determined in the promoter-proximal region. Genes Dev. 1992 Nov;6(11):2201–2213. doi: 10.1101/gad.6.11.2201. [DOI] [PubMed] [Google Scholar]
  34. Larsson J., Zhang J., Rasmuson-Lestander A. Mutations in the Drosophila melanogaster gene encoding S-adenosylmethionine synthetase [corrected] suppress position-effect variegation. Genetics. 1996 Jun;143(2):887–896. doi: 10.1093/genetics/143.2.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lee H., Kraus K. W., Wolfner M. F., Lis J. T. DNA sequence requirements for generating paused polymerase at the start of hsp70. Genes Dev. 1992 Feb;6(2):284–295. doi: 10.1101/gad.6.2.284. [DOI] [PubMed] [Google Scholar]
  36. Lis J., Wu C. Protein traffic on the heat shock promoter: parking, stalling, and trucking along. Cell. 1993 Jul 16;74(1):1–4. doi: 10.1016/0092-8674(93)90286-y. [DOI] [PubMed] [Google Scholar]
  37. Lu Q., Wallrath L. L., Allan B. D., Glaser R. L., Lis J. T., Elgin S. C. Promoter sequence containing (CT)n.(GA)n repeats is critical for the formation of the DNase I hypersensitive sites in the Drosophila hsp26 gene. J Mol Biol. 1992 Jun 20;225(4):985–998. doi: 10.1016/0022-2836(92)90099-6. [DOI] [PubMed] [Google Scholar]
  38. Lu Q., Wallrath L. L., Granok H., Elgin S. C. (CT)n (GA)n repeats and heat shock elements have distinct roles in chromatin structure and transcriptional activation of the Drosophila hsp26 gene. Mol Cell Biol. 1993 May;13(5):2802–2814. doi: 10.1128/mcb.13.5.2802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Martin M., Giangrande A., Ruiz C., Richards G. Induction and repression of the Drosophila Sgs-3 glue gene are mediated by distinct sequences in the proximal promoter. EMBO J. 1989 Feb;8(2):561–568. doi: 10.1002/j.1460-2075.1989.tb03410.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. McKnight S. L. Transcription revisited: a commentary on the 1995 Cold Spring Harbor Laboratory meeting, "Mechanisms of Eukaryotic Transcription". Genes Dev. 1996 Feb 15;10(4):367–381. doi: 10.1101/gad.10.4.367. [DOI] [PubMed] [Google Scholar]
  41. Miller J., McLachlan A. D., Klug A. Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 1985 Jun;4(6):1609–1614. doi: 10.1002/j.1460-2075.1985.tb03825.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Mirkovitch J., Darnell J. E., Jr Mapping of RNA polymerase on mammalian genes in cells and nuclei. Mol Biol Cell. 1992 Oct;3(10):1085–1094. doi: 10.1091/mbc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Nardelli J., Gibson T. J., Vesque C., Charnay P. Base sequence discrimination by zinc-finger DNA-binding domains. Nature. 1991 Jan 10;349(6305):175–178. doi: 10.1038/349175a0. [DOI] [PubMed] [Google Scholar]
  44. O'Brien T., Hardin S., Greenleaf A., Lis J. T. Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature. 1994 Jul 7;370(6484):75–77. doi: 10.1038/370075a0. [DOI] [PubMed] [Google Scholar]
  45. O'Brien T., Lis J. T. RNA polymerase II pauses at the 5' end of the transcriptionally induced Drosophila hsp70 gene. Mol Cell Biol. 1991 Oct;11(10):5285–5290. doi: 10.1128/mcb.11.10.5285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. O'Brien T., Lis J. T. Rapid changes in Drosophila transcription after an instantaneous heat shock. Mol Cell Biol. 1993 Jun;13(6):3456–3463. doi: 10.1128/mcb.13.6.3456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. O'Brien T., Wilkins R. C., Giardina C., Lis J. T. Distribution of GAGA protein on Drosophila genes in vivo. Genes Dev. 1995 May 1;9(9):1098–1110. doi: 10.1101/gad.9.9.1098. [DOI] [PubMed] [Google Scholar]
  48. O'Donnell K. H., Wensink P. C. GAGA factor and TBF1 bind DNA elements that direct ubiquitous transcription of the Drosophila alpha 1-tubulin gene. Nucleic Acids Res. 1994 Nov 11;22(22):4712–4718. doi: 10.1093/nar/22.22.4712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Omichinski J. G., Pedone P. V., Felsenfeld G., Gronenborn A. M., Clore G. M. The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode. Nat Struct Biol. 1997 Feb;4(2):122–132. doi: 10.1038/nsb0297-122. [DOI] [PubMed] [Google Scholar]
  50. Pascal E., Tjian R. Different activation domains of Sp1 govern formation of multimers and mediate transcriptional synergism. Genes Dev. 1991 Sep;5(9):1646–1656. doi: 10.1101/gad.5.9.1646. [DOI] [PubMed] [Google Scholar]
  51. Pedone P. V., Ghirlando R., Clore G. M., Gronenborn A. M., Felsenfeld G., Omichinski J. G. The single Cys2-His2 zinc finger domain of the GAGA protein flanked by basic residues is sufficient for high-affinity specific DNA binding. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2822–2826. doi: 10.1073/pnas.93.7.2822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Perutz M. Polar zippers: their role in human disease. Protein Sci. 1994 Oct;3(10):1629–1637. doi: 10.1002/pro.5560031002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Raff J. W., Kellum R., Alberts B. The Drosophila GAGA transcription factor is associated with specific regions of heterochromatin throughout the cell cycle. EMBO J. 1994 Dec 15;13(24):5977–5983. doi: 10.1002/j.1460-2075.1994.tb06943.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rasmussen E. B., Lis J. T. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7923–7927. doi: 10.1073/pnas.90.17.7923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Read D., Nishigaki T., Manley J. L. The Drosophila even-skipped promoter is transcribed in a stage-specific manner in vitro and contains multiple, overlapping factor-binding sites. Mol Cell Biol. 1990 Aug;10(8):4334–4344. doi: 10.1128/mcb.10.8.4334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Reuter G., Spierer P. Position effect variegation and chromatin proteins. Bioessays. 1992 Sep;14(9):605–612. doi: 10.1002/bies.950140907. [DOI] [PubMed] [Google Scholar]
  57. Rougvie A. E., Lis J. T. Postinitiation transcriptional control in Drosophila melanogaster. Mol Cell Biol. 1990 Nov;10(11):6041–6045. doi: 10.1128/mcb.10.11.6041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Seum C., Spierer A., Pauli D., Szidonya J., Reuter G., Spierer P. Position-effect variegation in Drosophila depends on dose of the gene encoding the E2F transcriptional activator and cell cycle regulator. Development. 1996 Jun;122(6):1949–1956. doi: 10.1242/dev.122.6.1949. [DOI] [PubMed] [Google Scholar]
  59. Shopland L. S., Hirayoshi K., Fernandes M., Lis J. T. HSF access to heat shock elements in vivo depends critically on promoter architecture defined by GAGA factor, TFIID, and RNA polymerase II binding sites. Genes Dev. 1995 Nov 15;9(22):2756–2769. doi: 10.1101/gad.9.22.2756. [DOI] [PubMed] [Google Scholar]
  60. Shopland L. S., Lis J. T. HSF recruitment and loss at most Drosophila heat shock loci is coordinated and depends on proximal promoter sequences. Chromosoma. 1996 Sep;105(3):158–171. doi: 10.1007/BF02509497. [DOI] [PubMed] [Google Scholar]
  61. 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]
  62. Soeller W. C., Poole S. J., Kornberg T. In vitro transcription of the Drosophila engrailed gene. Genes Dev. 1988 Jan;2(1):68–81. doi: 10.1101/gad.2.1.68. [DOI] [PubMed] [Google Scholar]
  63. Stott K., Blackburn J. M., Butler P. J., Perutz M. Incorporation of glutamine repeats makes protein oligomerize: implications for neurodegenerative diseases. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6509–6513. doi: 10.1073/pnas.92.14.6509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Thummel C. S. The Drosophila E74 promoter contains essential sequences downstream from the start site of transcription. Genes Dev. 1989 Jun;3(6):782–792. doi: 10.1101/gad.3.6.782. [DOI] [PubMed] [Google Scholar]
  65. Topol J., Dearolf C. R., Prakash K., Parker C. S. Synthetic oligonucleotides recreate Drosophila fushi tarazu zebra-stripe expression. Genes Dev. 1991 May;5(5):855–867. doi: 10.1101/gad.5.5.855. [DOI] [PubMed] [Google Scholar]
  66. 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]
  67. 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]
  68. Tsukiyama T., Wu C. Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell. 1995 Dec 15;83(6):1011–1020. doi: 10.1016/0092-8674(95)90216-3. [DOI] [PubMed] [Google Scholar]
  69. Wall G., Varga-Weisz P. D., Sandaltzopoulos R., Becker P. B. Chromatin remodeling by GAGA factor and heat shock factor at the hypersensitive Drosophila hsp26 promoter in vitro. EMBO J. 1995 Apr 18;14(8):1727–1736. doi: 10.1002/j.1460-2075.1995.tb07162.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Walter J., Dever C. A., Biggin M. D. Two homeo domain proteins bind with similar specificity to a wide range of DNA sites in Drosophila embryos. Genes Dev. 1994 Jul 15;8(14):1678–1692. doi: 10.1101/gad.8.14.1678. [DOI] [PubMed] [Google Scholar]
  71. Weber J. A., Taxman D. J., Lu Q., Gilmour D. S. Molecular architecture of the hsp70 promoter after deletion of the TATA box or the upstream regulation region. Mol Cell Biol. 1997 Jul;17(7):3799–3808. doi: 10.1128/mcb.17.7.3799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Weiler K. S., Wakimoto B. T. Heterochromatin and gene expression in Drosophila. Annu Rev Genet. 1995;29:577–605. doi: 10.1146/annurev.ge.29.120195.003045. [DOI] [PubMed] [Google Scholar]
  73. Zimarino V., Wu C. Induction of sequence-specific binding of Drosophila heat shock activator protein without protein synthesis. 1987 Jun 25-Jul 1Nature. 327(6124):727–730. doi: 10.1038/327727a0. [DOI] [PubMed] [Google Scholar]
  74. Zollman S., Godt D., Privé G. G., Couderc J. L., Laski F. A. The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10717–10721. doi: 10.1073/pnas.91.22.10717. [DOI] [PMC free article] [PubMed] [Google Scholar]

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