Abstract
The zeste(1) (z(1)) mutation of Drosophila melanogaster produces a mutant yellow eye color instead of the wild-type red. Genetic and molecular data suggest that z(1) achieves this change by altering expression of the wild-type white gene in a manner that exhibits transvection effects. There exist suppressor and enhancer mutations that modify the z(1) eye color, and this paper summarizes our studies of those belonging to the Suppressor 2 of zeste complex [Su(z)2-C]. The Su(z)2-C consists of at least three subregions called Psc (Posterior sex combs), Su(z)2 and Su(z)2D (Distal). The products of these subregions are proposed to act at the level of chromatin. Complementation analyses predict that the products are functionally similar and interacting. The alleles of Psc define two overlapping phenotypic classes, the hopeful and hapless. The distinctions between these two classes and the intragenic complementation seen among some of the Psc alleles are consistent with a multidomain structure for the product of Psc. Psc is a member of the homeotic Polycomb group of genes. A general discussion of the Polycomb and trithorax group of genes, position-effect variegation, transvection, chromosome pairing and chromatin structure is presented.
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- Adler P. N., Charlton J., Brunk B. Genetic interactions of the suppressor 2 of zeste region genes. Dev Genet. 1989;10(3):249–260. doi: 10.1002/dvg.1020100314. [DOI] [PubMed] [Google Scholar]
- Baker B. S., Carpenter A. T., Ripoll P. The Utilization during Mitotic Cell Division of Loci Controlling Meiotic Recombination and Disjunction in DROSOPHILA MELANOGASTER. Genetics. 1978 Nov;90(3):531–578. doi: 10.1093/genetics/90.3.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baker N. E., Mlodzik M., Rubin G. M. Spacing differentiation in the developing Drosophila eye: a fibrinogen-related lateral inhibitor encoded by scabrous. Science. 1990 Dec 7;250(4986):1370–1377. doi: 10.1126/science.2175046. [DOI] [PubMed] [Google Scholar]
- Baksa K., Morawietz H., Dombrádi V., Axton M., Taubert H., Szabó G., Török I., Udvardy A., Gyurkovics H., Ször B. Mutations in the protein phosphatase 1 gene at 87B can differentially affect suppression of position-effect variegation and mitosis in Drosophila melanogaster. Genetics. 1993 Sep;135(1):117–125. doi: 10.1093/genetics/135.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Bingham P. M., Zachar Z. Evidence that two mutations, wDZL and z1, affecting synapsis-dependent genetic behavior of white are transcriptional regulatory mutations. Cell. 1985 Apr;40(4):819–825. doi: 10.1016/0092-8674(85)90341-1. [DOI] [PubMed] [Google Scholar]
- Bone J. R., Lavender J., Richman R., Palmer M. J., Turner B. M., Kuroda M. I. Acetylated histone H4 on the male X chromosome is associated with dosage compensation in Drosophila. Genes Dev. 1994 Jan;8(1):96–104. doi: 10.1101/gad.8.1.96. [DOI] [PubMed] [Google Scholar]
- Breen T. R., Duncan I. M. Maternal expression of genes that regulate the bithorax complex of Drosophila melanogaster. Dev Biol. 1986 Dec;118(2):442–456. doi: 10.1016/0012-1606(86)90015-1. [DOI] [PubMed] [Google Scholar]
- Brizuela B. J., Elfring L., Ballard J., Tamkun J. W., Kennison J. A. Genetic analysis of the brahma gene of Drosophila melanogaster and polytene chromosome subdivisions 72AB. Genetics. 1994 Jul;137(3):803–813. doi: 10.1093/genetics/137.3.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brunk B. P., Adler P. N. Aristapedioid: a gain of function, homeotic mutation in Drosophila melanogaster. Genetics. 1990 Jan;124(1):145–156. doi: 10.1093/genetics/124.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brunk B. P., Adler P. N. The sequence of the Drosophila regulatory gene Suppressor two of zeste. Nucleic Acids Res. 1991 Jun 11;19(11):3149–3149. doi: 10.1093/nar/19.11.3149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brunk B. P., Martin E. C., Adler P. N. Drosophila genes Posterior Sex Combs and Suppressor two of zeste encode proteins with homology to the murine bmi-1 oncogene. Nature. 1991 Sep 26;353(6342):351–353. doi: 10.1038/353351a0. [DOI] [PubMed] [Google Scholar]
- Brunk B. P., Martin E. C., Adler P. N. Molecular genetics of the Posterior sex combs/Suppressor 2 of zeste region of Drosophila: aberrant expression of the Suppressor 2 of zeste gene results in abnormal bristle development. Genetics. 1991 May;128(1):119–132. doi: 10.1093/genetics/128.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Cairns B. R., Kim Y. J., Sayre M. H., Laurent B. C., Kornberg R. D. A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1950–1954. doi: 10.1073/pnas.91.5.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Casanova J., Sánchez-Herrero E., Morata G. Contrabithorax and the control of spatial expression of the bithorax complex genes of Drosophila. J Embryol Exp Morphol. 1985 Dec;90:179–196. [PubMed] [Google Scholar]
- 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]
- Chen J. D., Chan C. S., Pirrotta V. Conserved DNA binding and self-association domains of the Drosophila zeste protein. Mol Cell Biol. 1992 Feb;12(2):598–608. doi: 10.1128/mcb.12.2.598. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen J. D., Pirrotta V. Stepwise assembly of hyperaggregated forms of Drosophila zeste mutant protein suppresses white gene expression in vivo. EMBO J. 1993 May;12(5):2061–2073. doi: 10.1002/j.1460-2075.1993.tb05855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chung J. H., Whiteley M., Felsenfeld G. A 5' element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell. 1993 Aug 13;74(3):505–514. doi: 10.1016/0092-8674(93)80052-g. [DOI] [PubMed] [Google Scholar]
- Coen D. P element regulatory products enhance zeste repression of a P[white duplicated] transgene in Drosophila melanogaster. Genetics. 1990 Dec;126(4):949–960. doi: 10.1093/genetics/126.4.949. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Condie J. M., Brower D. L. Allelic interactions at the engrailed locus of Drosophila: engrailed protein expression in imaginal discs. Dev Biol. 1989 Sep;135(1):31–42. doi: 10.1016/0012-1606(89)90155-3. [DOI] [PubMed] [Google Scholar]
- Csink A. K., Linsk R., Birchler J. A. Mosaic suppressor, a gene in Drosophila that modifies retrotransposon expression and interacts with zeste. Genetics. 1994 Feb;136(2):573–583. doi: 10.1093/genetics/136.2.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Dorer D. R., Henikoff S. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell. 1994 Jul 1;77(7):993–1002. doi: 10.1016/0092-8674(94)90439-1. [DOI] [PubMed] [Google Scholar]
- Dreesen T. D., Henikoff S., Loughney K. A pairing-sensitive element that mediates trans-inactivation is associated with the Drosophila brown gene. Genes Dev. 1991 Mar;5(3):331–340. doi: 10.1101/gad.5.3.331. [DOI] [PubMed] [Google Scholar]
- Dura J. M., Brock H. W., Santamaria P. Polyhomeotic: a gene of Drosophila melanogaster required for correct expression of segmental identity. Mol Gen Genet. 1985;198(2):213–220. doi: 10.1007/BF00382998. [DOI] [PubMed] [Google Scholar]
- Eissenberg J. C., Elgin S. C. Boundary functions in the control of gene expression. Trends Genet. 1991 Oct;7(10):335–340. doi: 10.1016/0168-9525(91)90424-o. [DOI] [PubMed] [Google Scholar]
- Eissenberg J. C., James T. C., Foster-Hartnett D. M., Hartnett T., Ngan V., Elgin S. C. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9923–9927. doi: 10.1073/pnas.87.24.9923. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eissenberg J. C., Morris G. D., Reuter G., Hartnett T. The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation. Genetics. 1992 Jun;131(2):345–352. doi: 10.1093/genetics/131.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eissenberg J. C. Position effect variegation in Drosophila: towards a genetics of chromatin assembly. Bioessays. 1989 Jul;11(1):14–17. doi: 10.1002/bies.950110105. [DOI] [PubMed] [Google Scholar]
- Ephrussi B., Sutton E. A Reconsideration of the Mechanism of Position Effect. Proc Natl Acad Sci U S A. 1944 Aug 15;30(8):183–197. doi: 10.1073/pnas.30.8.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Freemont P. S., Hanson I. M., Trowsdale J. A novel cysteine-rich sequence motif. Cell. 1991 Feb 8;64(3):483–484. doi: 10.1016/0092-8674(91)90229-r. [DOI] [PubMed] [Google Scholar]
- Fuller M. T., Regan C. L., Green L. L., Robertson B., Deuring R., Hays T. S. Interacting genes identify interacting proteins involved in microtubule function in Drosophila. Cell Motil Cytoskeleton. 1989;14(1):128–135. doi: 10.1002/cm.970140122. [DOI] [PubMed] [Google Scholar]
- Furia M., D'Avino P. P., Crispi S., Artiaco D., Polito L. C. Dense cluster of genes is located at the ecdysone-regulated 3C puff of Drosophila melanogaster. J Mol Biol. 1993 May 20;231(2):531–538. doi: 10.1006/jmbi.1993.1304. [DOI] [PubMed] [Google Scholar]
- Gatti M., Baker B. S. Genes controlling essential cell-cycle functions in Drosophila melanogaster. Genes Dev. 1989 Apr;3(4):438–453. doi: 10.1101/gad.3.4.438. [DOI] [PubMed] [Google Scholar]
- Gaunt S. J., Singh P. B. Homeogene expression patterns and chromosomal imprinting. Trends Genet. 1990 Jul;6(7):208–212. [PubMed] [Google Scholar]
- Gelbart W. M., Wu C. T. Interactions of zeste mutations with loci exhibiting transvection effects in Drosophila melanogaster. Genetics. 1982 Oct;102(2):179–189. doi: 10.1093/genetics/102.2.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Geyer P. K., Green M. M., Corces V. G. Tissue-specific transcriptional enhancers may act in trans on the gene located in the homologous chromosome: the molecular basis of transvection in Drosophila. EMBO J. 1990 Jul;9(7):2247–2256. doi: 10.1002/j.1460-2075.1990.tb07395.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glover D. M. Mitosis in the Drosophila embryo--in and out of control. Trends Genet. 1991 Apr;7(4):125–132. doi: 10.1016/0168-9525(91)90457-2. [DOI] [PubMed] [Google Scholar]
- Goldberg M. L., Colvin R. A., Mellin A. F. The Drosophila zeste locus is nonessential. Genetics. 1989 Sep;123(1):145–155. doi: 10.1093/genetics/123.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman M., Kuroda M. I., Baker B. S. Regulation of the sex-specific binding of the maleless dosage compensation protein to the male X chromosome in Drosophila. Cell. 1993 Jan 15;72(1):39–49. doi: 10.1016/0092-8674(93)90048-u. [DOI] [PubMed] [Google Scholar]
- Gubb D., Ashburner M., Roote J., Davis T. A novel transvection phenomenon affecting the white gene of Drosophila melanogaster. Genetics. 1990 Sep;126(1):167–176. doi: 10.1093/genetics/126.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hama C., Ali Z., Kornberg T. B. Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev. 1990 Jul;4(7):1079–1093. doi: 10.1101/gad.4.7.1079. [DOI] [PubMed] [Google Scholar]
- Hanscombe O., Whyatt D., Fraser P., Yannoutsos N., Greaves D., Dillon N., Grosveld F. Importance of globin gene order for correct developmental expression. Genes Dev. 1991 Aug;5(8):1387–1394. doi: 10.1101/gad.5.8.1387. [DOI] [PubMed] [Google Scholar]
- Hays T. S., Deuring R., Robertson B., Prout M., Fuller M. T. Interacting proteins identified by genetic interactions: a missense mutation in alpha-tubulin fails to complement alleles of the testis-specific beta-tubulin gene of Drosophila melanogaster. Mol Cell Biol. 1989 Mar;9(3):875–884. doi: 10.1128/mcb.9.3.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hazelrigg T., Petersen S. An unusual genomic position effect on Drosophila white gene expression: pairing dependence, interactions with zeste, and molecular analysis of revertants. Genetics. 1992 Jan;130(1):125–138. doi: 10.1093/genetics/130.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henikoff S. A reconsideration of the mechanism of position effect. Genetics. 1994 Sep;138(1):1–5. doi: 10.1093/genetics/138.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henikoff S. Position effect and related phenomena. Curr Opin Genet Dev. 1992 Dec;2(6):907–912. doi: 10.1016/s0959-437x(05)80114-5. [DOI] [PubMed] [Google Scholar]
- Henikoff S. Position-effect variegation after 60 years. Trends Genet. 1990 Dec;6(12):422–426. doi: 10.1016/0168-9525(90)90304-o. [DOI] [PubMed] [Google Scholar]
- Izpisúa-Belmonte J. C., Falkenstein H., Dollé P., Renucci A., Duboule D. Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 1991 Aug;10(8):2279–2289. doi: 10.1002/j.1460-2075.1991.tb07764.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- JUDD B. H. Formation of duplication-deficiency products by asymmetrical exchange within a complex locus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1961 Apr 15;47:545–550. doi: 10.1073/pnas.47.4.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jack J. W., Judd B. H. Allelic pairing and gene regulation: A model for the zeste-white interaction in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1368–1372. doi: 10.1073/pnas.76.3.1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
- James T. C., Eissenberg J. C., Craig C., Dietrich V., Hobson A., Elgin S. C. Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur J Cell Biol. 1989 Oct;50(1):170–180. [PubMed] [Google Scholar]
- Jones R. S., Gelbart W. M. Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics. 1990 Sep;126(1):185–199. doi: 10.1093/genetics/126.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Judd B. H. Transvection: allelic cross talk. Cell. 1988 Jun 17;53(6):841–843. doi: 10.1016/s0092-8674(88)90209-7. [DOI] [PubMed] [Google Scholar]
- Kassis J. A., Noll E., VanSickle E. P., Odenwald W. F., Perrimon N. Altering the insertional specificity of a Drosophila transposable element. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1919–1923. doi: 10.1073/pnas.89.5.1919. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kassis J. A. Unusual properties of regulatory DNA from the Drosophila engrailed gene: three "pairing-sensitive" sites within a 1.6-kb region. Genetics. 1994 Mar;136(3):1025–1038. doi: 10.1093/genetics/136.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kassis J. A., VanSickle E. P., Sensabaugh S. M. A fragment of engrailed regulatory DNA can mediate transvection of the white gene in Drosophila. Genetics. 1991 Aug;128(4):751–761. doi: 10.1093/genetics/128.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaufman T. C., Tasaka S. E., Suzuki D. T. The interaction of two complex loci, zeste and bithorax in Drosophila melanogaster. Genetics. 1973 Oct;75(2):299–321. doi: 10.1093/genetics/75.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kellum R., Schedl P. A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol Cell Biol. 1992 May;12(5):2424–2431. doi: 10.1128/mcb.12.5.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Kennison J. A., Tamkun J. W. Trans-regulation of homeotic genes in Drosophila. New Biol. 1992 Feb;4(2):91–96. [PubMed] [Google Scholar]
- 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]
- Kopczynski C. C., Muskavitch M. A. Introns excised from the Delta primary transcript are localized near sites of Delta transcription. J Cell Biol. 1992 Nov;119(3):503–512. doi: 10.1083/jcb.119.3.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Lasko P. F., Pardue M. L. Studies of the genetic organization of the vestigial microregion of Drosophila melanogaster. Genetics. 1988 Oct;120(2):495–502. doi: 10.1093/genetics/120.2.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lemaitre B., Coen D. P regulatory products repress in vivo the P promoter activity in P-lacZ fusion genes. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4419–4423. doi: 10.1073/pnas.88.10.4419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lemaitre B., Ronsseray S., Coen D. Maternal repression of the P element promoter in the germline of Drosophila melanogaster: a model for the P cytotype. Genetics. 1993 Sep;135(1):149–160. doi: 10.1093/genetics/135.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Locke J., Tartof K. D. Molecular analysis of cubitus interruptus (ci) mutations suggests an explanation for the unusual ci position effects. Mol Gen Genet. 1994 Apr;243(2):234–243. doi: 10.1007/BF00280321. [DOI] [PubMed] [Google Scholar]
- Lovering R., Hanson I. M., Borden K. L., Martin S., O'Reilly N. J., Evan G. I., Rahman D., Pappin D. J., Trowsdale J., Freemont P. S. Identification and preliminary characterization of a protein motif related to the zinc finger. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2112–2116. doi: 10.1073/pnas.90.6.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mansukhani A., Crickmore A., Sherwood P. W., Goldberg M. L. DNA-binding properties of the Drosophila melanogaster zeste gene product. Mol Cell Biol. 1988 Feb;8(2):615–623. doi: 10.1128/mcb.8.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mansukhani A., Gunaratne P. H., Sherwood P. W., Sneath B. J., Goldberg M. L. Nucleotide sequence and structural analysis of the zeste locus of Drosophila melanogaster. Mol Gen Genet. 1988 Jan;211(1):121–128. doi: 10.1007/BF00338402. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Micol J. L., García-Bellido A. Genetic analysis of "transvection" effects involving contrabithorax mutations in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1146–1150. doi: 10.1073/pnas.85.4.1146. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mlodzik M., Baker N. E., Rubin G. M. Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. Genes Dev. 1990 Nov;4(11):1848–1861. doi: 10.1101/gad.4.11.1848. [DOI] [PubMed] [Google Scholar]
- 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]
- Palmer M. J., Mergner V. A., Richman R., Manning J. E., Kuroda M. I., Lucchesi J. C. The male-specific lethal-one (msl-1) gene of Drosophila melanogaster encodes a novel protein that associates with the X chromosome in males. Genetics. 1993 Jun;134(2):545–557. doi: 10.1093/genetics/134.2.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Palmer M. J., Richman R., Richter L., Kuroda M. I. Sex-specific regulation of the male-specific lethal-1 dosage compensation gene in Drosophila. Genes Dev. 1994 Mar 15;8(6):698–706. doi: 10.1101/gad.8.6.698. [DOI] [PubMed] [Google Scholar]
- Pan D. J., Huang J. D., Courey A. J. Functional analysis of the Drosophila twist promoter reveals a dorsal-binding ventral activator region. Genes Dev. 1991 Oct;5(10):1892–1901. doi: 10.1101/gad.5.10.1892. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Persson K. Modification of the eye colour mutant zeste by suppressor, enhancer and minute genes in Drosophila melanogaster. Hereditas. 1976;82(1):111–119. doi: 10.1111/j.1601-5223.1976.tb01544.x. [DOI] [PubMed] [Google Scholar]
- Peterson K. M., Davis P. S., Judd B. H. The determined state of white expression in the Drosophila eye is modified by zeste1 in the wzm family of mutants. Mol Gen Genet. 1994 Mar;242(6):717–726. doi: 10.1007/BF00283427. [DOI] [PubMed] [Google Scholar]
- Peterson K. R., Stamatoyannopoulos G. Role of gene order in developmental control of human gamma- and beta-globin gene expression. Mol Cell Biol. 1993 Aug;13(8):4836–4843. doi: 10.1128/mcb.13.8.4836. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Phillips M. D., Shearn A. Mutations in polycombeotic, a Drosophila polycomb-group gene, cause a wide range of maternal and zygotic phenotypes. Genetics. 1990 May;125(1):91–101. doi: 10.1093/genetics/125.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pirrotta V., Bickel S., Mariani C. Developmental expression of the Drosophila zeste gene and localization of zeste protein on polytene chromosomes. Genes Dev. 1988 Dec;2(12B):1839–1850. doi: 10.1101/gad.2.12b.1839. [DOI] [PubMed] [Google Scholar]
- Pirrotta V., Rastelli L. White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila. Bioessays. 1994 Aug;16(8):549–556. doi: 10.1002/bies.950160808. [DOI] [PubMed] [Google Scholar]
- Pirrotta V. The genetics and molecular biology of zeste in Drosophila melanogaster. Adv Genet. 1991;29:301–348. doi: 10.1016/s0065-2660(08)60110-8. [DOI] [PubMed] [Google Scholar]
- Pirrotta V. Transvection and long-distance gene regulation. Bioessays. 1990 Sep;12(9):409–414. doi: 10.1002/bies.950120903. [DOI] [PubMed] [Google Scholar]
- Powers J. A., Eissenberg J. C. Overlapping domains of the heterochromatin-associated protein HP1 mediate nuclear localization and heterochromatin binding. J Cell Biol. 1993 Jan;120(2):291–299. doi: 10.1083/jcb.120.2.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Regan C. L., Fuller M. T. Interacting genes that affect microtubule function: the nc2 allele of the haywire locus fails to complement mutations in the testis-specific beta-tubulin gene of Drosophila. Genes Dev. 1988 Jan;2(1):82–92. doi: 10.1101/gad.2.1.82. [DOI] [PubMed] [Google Scholar]
- 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]
- Roseman R. R., Pirrotta V., Geyer P. K. The su(Hw) protein insulates expression of the Drosophila melanogaster white gene from chromosomal position-effects. EMBO J. 1993 Feb;12(2):435–442. doi: 10.1002/j.1460-2075.1993.tb05675.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sandmeyer S. B., Hansen L. J., Chalker D. L. Integration specificity of retrotransposons and retroviruses. Annu Rev Genet. 1990;24:491–518. doi: 10.1146/annurev.ge.24.120190.002423. [DOI] [PubMed] [Google Scholar]
- Santamaria P. Evolution and aggregulates: role of the Polycomb-group genes of Drosophila. C R Acad Sci III. 1993 Oct;316(10):1200–1206. [PubMed] [Google Scholar]
- 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]
- Schlossherr J., Eggert H., Paro R., Cremer S., Jack R. S. Gene inactivation in Drosophila mediated by the Polycomb gene product or by position-effect variegation does not involve major changes in the accessibility of the chromatin fibre. Mol Gen Genet. 1994 May 25;243(4):453–462. doi: 10.1007/BF00280476. [DOI] [PubMed] [Google Scholar]
- Shaffer C. D., Wallrath L. L., Elgin S. C. Regulating genes by packaging domains: bits of heterochromatin in euchromatin? Trends Genet. 1993 Feb;9(2):35–37. doi: 10.1016/0168-9525(93)90171-D. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Simon J., Chiang A., Bender W. Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development. 1992 Feb;114(2):493–505. doi: 10.1242/dev.114.2.493. [DOI] [PubMed] [Google Scholar]
- Snyder P. B., Galanopoulos V. K., Kafatos F. C. Trans-acting amplification mutants and other eggshell mutants of the third chromosome in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1986 May;83(10):3341–3345. doi: 10.1073/pnas.83.10.3341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spradling A. C., Karpen G. H. Sixty years of mystery. Genetics. 1990 Dec;126(4):779–784. doi: 10.1093/genetics/126.4.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Talbert P. B., LeCiel C. D., Henikoff S. Modification of the Drosophila heterochromatic mutation brownDominant by linkage alterations. Genetics. 1994 Feb;136(2):559–571. doi: 10.1093/genetics/136.2.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Tartof K. D., Henikoff S. Trans-sensing effects from Drosophila to humans. Cell. 1991 Apr 19;65(2):201–203. doi: 10.1016/0092-8674(91)90153-p. [DOI] [PubMed] [Google Scholar]
- TenHarmsel A., Austin R. J., Savenelli N., Biggin M. D. Cooperative binding at a distance by even-skipped protein correlates with repression and suggests a mechanism of silencing. Mol Cell Biol. 1993 May;13(5):2742–2752. doi: 10.1128/mcb.13.5.2742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Tripoulas N. A., Hersperger E., La Jeunesse D., Shearn A. Molecular genetic analysis of the Drosophila melanogaster gene absent, small or homeotic discs1 (ash1). Genetics. 1994 Aug;137(4):1027–1038. doi: 10.1093/genetics/137.4.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Williams J. A., Bell J. B., Carroll S. B. Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev. 1991 Dec;5(12B):2481–2495. doi: 10.1101/gad.5.12b.2481. [DOI] [PubMed] [Google Scholar]
- Williams J. A., Bell J. B. Molecular organization of the vestigial region in Drosophila melanogaster. EMBO J. 1988 May;7(5):1355–1363. doi: 10.1002/j.1460-2075.1988.tb02951.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Winston F., Carlson M. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 1992 Nov;8(11):387–391. doi: 10.1016/0168-9525(92)90300-s. [DOI] [PubMed] [Google Scholar]
- Wolffe A. P. Gene regulation. Insulating chromatin. Curr Biol. 1994 Jan 1;4(1):85–87. doi: 10.1016/s0960-9822(00)00022-1. [DOI] [PubMed] [Google Scholar]
- Wu C. T., Budding M., Griffin M. S., Croop J. M. Isolation and characterization of Drosophila multidrug resistance gene homologs. Mol Cell Biol. 1991 Aug;11(8):3940–3948. doi: 10.1128/mcb.11.8.3940. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wu C. T., Goldberg M. L. The Drosophila zeste gene and transvection. Trends Genet. 1989 Jun;5(6):189–194. doi: 10.1016/0168-9525(89)90074-7. [DOI] [PubMed] [Google Scholar]
- Wu C. T., Jones R. S., Lasko P. F., Gelbart W. M. Homeosis and the interaction of zeste and white in Drosophila. Mol Gen Genet. 1989 Sep;218(3):559–564. doi: 10.1007/BF00332424. [DOI] [PubMed] [Google Scholar]
- Wu C. T. Transvection, nuclear structure, and chromatin proteins. J Cell Biol. 1993 Feb;120(3):587–590. doi: 10.1083/jcb.120.3.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zabin I., Villarejo M. R. Protein complementation. Annu Rev Biochem. 1975;44:295–313. doi: 10.1146/annurev.bi.44.070175.001455. [DOI] [PubMed] [Google Scholar]
- Zachar Z., Bingham P. M. Regulation of white locus expression: the structure of mutant alleles at the white locus of Drosophila melanogaster. Cell. 1982 Sep;30(2):529–541. doi: 10.1016/0092-8674(82)90250-1. [DOI] [PubMed] [Google Scholar]
- 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]
- van Lohuizen M., Frasch M., Wientjens E., Berns A. Sequence similarity between the mammalian bmi-1 proto-oncogene and the Drosophila regulatory genes Psc and Su(z)2. Nature. 1991 Sep 26;353(6342):353–355. doi: 10.1038/353353a0. [DOI] [PubMed] [Google Scholar]
