In Vivo Analysis of Scaffold-associated Regions in Drosophila: a Synthetic High-affinity SAR Binding Protein Suppresses Position Effect Variegation

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1998 Jun 6

PMID 9524129

Citations 23

Authors

F Girard

B Bello

U K Laemmli

W J Gehring

Affiliations

Soon will be listed here.

Abstract

Scaffold-associated regions (SARs) were studied in Drosophila melanogaster by expressing a synthetic, high-affinity SAR-binding protein called MATH (multi-AT-hook), which consists of reiterated AT-hook peptide motifs; each motif is known to recognize a wide variety of short AT-rich sequences. MATH proteins were expressed specifically in the larval eye imaginal discs by means of the tetracycline-regulated transactivation system and tested for their effect on position effect variegation (PEV). MATH20, a highly potent SAR ligand consisting of 20 AT-hooks, was found to suppress whitemottled 4 variegation. This suppression required MATH20 expression at an early larval developmental stage. Our data suggest an involvement of the high AT-rich SARs in higher order chromatin structure and gene expression.

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References

Reeves R, Nissen M . The A.T-DNA-binding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure. J Biol Chem. 1990; 265(15):8573-82. View

Locke J, Kotarski M, Tartof K . Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect. Genetics. 1988; 120(1):181-98. PMC: 1203489. DOI: 10.1093/genetics/120.1.181. View

Kas E, Laemmli U . In vivo topoisomerase II cleavage of the Drosophila histone and satellite III repeats: DNA sequence and structural characteristics. EMBO J. 1992; 11(2):705-16. PMC: 556503. DOI: 10.1002/j.1460-2075.1992.tb05103.x. View

Bode J, Kohwi Y, Dickinson L, Joh T, Klehr D, Mielke C . Biological significance of unwinding capability of nuclear matrix-associating DNAs. Science. 1992; 255(5041):195-7. DOI: 10.1126/science.1553545. View

Gossen M, Bujard H . Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci U S A. 1992; 89(12):5547-51. PMC: 49329. DOI: 10.1073/pnas.89.12.5547. View

Laemmli U, Kas E, Poljak L, Adachi Y . Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr Opin Genet Dev. 1992; 2(2):275-85. DOI: 10.1016/s0959-437x(05)80285-0. View

Patton J, Gomes X, Geyer P . Position-independent germline transformation in Drosophila using a cuticle pigmentation gene as a selectable marker. Nucleic Acids Res. 1992; 20(21):5859-60. PMC: 334443. DOI: 10.1093/nar/20.21.5859. View

Kas E, Poljak L, Adachi Y, Laemmli U . A model for chromatin opening: stimulation of topoisomerase II and restriction enzyme cleavage of chromatin by distamycin. EMBO J. 1993; 12(1):115-26. PMC: 413181. DOI: 10.1002/j.1460-2075.1993.tb05637.x. View

Zhao K, Kas E, Gonzalez E, Laemmli U . SAR-dependent mobilization of histone H1 by HMG-I/Y in vitro: HMG-I/Y is enriched in H1-depleted chromatin. EMBO J. 1993; 12(8):3237-47. PMC: 413591. DOI: 10.1002/j.1460-2075.1993.tb05993.x. View

10.

Karpen G . Position-effect variegation and the new biology of heterochromatin. Curr Opin Genet Dev. 1994; 4(2):281-91. DOI: 10.1016/s0959-437x(05)80055-3. View

11.

Quiring R, Walldorf U, Kloter U, Gehring W . Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science. 1994; 265(5173):785-9. DOI: 10.1126/science.7914031. View

12.

Poljak L, Seum C, Mattioni T, Laemmli U . SARs stimulate but do not confer position independent gene expression. Nucleic Acids Res. 1994; 22(21):4386-94. PMC: 308471. DOI: 10.1093/nar/22.21.4386. View

13.

Strick R, Laemmli U . SARs are cis DNA elements of chromosome dynamics: synthesis of a SAR repressor protein. Cell. 1995; 83(7):1137-48. DOI: 10.1016/0092-8674(95)90140-x. View

14.

Dernburg A, Broman K, Fung J, Marshall W, Philips J, Agard D . Perturbation of nuclear architecture by long-distance chromosome interactions. Cell. 1996; 85(5):745-59. DOI: 10.1016/s0092-8674(00)81240-4. View

15.

Elgin S . Heterochromatin and gene regulation in Drosophila. Curr Opin Genet Dev. 1996; 6(2):193-202. DOI: 10.1016/s0959-437x(96)80050-5. View

16.

Kirillov A, Kistler B, Mostoslavsky R, Cedar H, Wirth T, Bergman Y . A role for nuclear NF-kappaB in B-cell-specific demethylation of the Igkappa locus. Nat Genet. 1996; 13(4):435-41. DOI: 10.1038/ng0895-435. View

17.

Rattner J, Hendzel M, Furbee C, Muller M, Bazett-Jones D . Topoisomerase II alpha is associated with the mammalian centromere in a cell cycle- and species-specific manner and is required for proper centromere/kinetochore structure. J Cell Biol. 1996; 134(5):1097-107. PMC: 2120978. DOI: 10.1083/jcb.134.5.1097. View

18.

Jenuwein T, Forrester W, Laible G, Dull M, Grosschedl R . Extension of chromatin accessibility by nuclear matrix attachment regions. Nature. 1997; 385(6613):269-72. DOI: 10.1038/385269a0. View

19.

Hsieh T, Brutlag D . Sequence and sequence variation within the 1.688 g/cm3 satellite DNA of Drosophila melanogaster. J Mol Biol. 1979; 135(2):465-81. DOI: 10.1016/0022-2836(79)90447-9. View

20.

Spradling A, Rubin G . Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982; 218(4570):341-7. DOI: 10.1126/science.6289435. View