Histone H4 acetylated at lysine 16 and proteins of the Drosophila dosage compensation pathway co-localize on the male X chromosome through mitosis
Received: 01 April 1994 Revised: 26 April 1994 Accepted: 26 April 1994 DOI:
Cite this article as: Lavender, J.S., Birley, A.J., Palmer, M.J. et al. Chromosome Res (1994) 2: 398. doi:10.1007/BF01552799 Abstract
In the fruit fly
Drosophila, dosage compensation involves several proteins acting in concert to double the transcriptional activity of genes on the single male X chromosome. Three of these proteins, MLE, MSL-1 and histone H4 acetylated at lysine 16 (H4Ac16), have recently been shown to be located almost exclusively on the male X chromosome in interphase (polytene) cells. We show here that in neuroblasts from third instar Drosophila larvae antisera to H4Ac16, MLE and MSL-1 uniquely label the distal, euchromatic region of the male X chromosome through mitosis. The centromere-proximal, heterochromatic region of the male X is not labelled with these antisera, nor are male autosomes or any chromosomes in female cells. That the association of H4Ac16 with the male X chromosome persists, even when the chromosome is maximally compacted and transcriptionally quiescent, argues that this modified histone is an integral component of the dosage compensation pathway. In the nuclei of interphase neuroblasts from male (but never female) larvae, antibodies to H4Ac16 revealed a small, brightly labelled patch against a background of generally weak nuclear staining. In double-labelling experiments, this patch was also labelled, albeit comparatively weakly, with antibodies to MSL-1. These results strongly suggest that the distal, euchromatic region of the X chromosome in male cells occupies a limited and relatively compact nuclear domain. Key words dosage compensation Drosophila histone acetylation nuclear domains References
Ashburner M (1989)
Drosophila: A Laboratory Handbook. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
Barigozzi C, Dolfini S, Fraccaro M, Raimondi GR, Tiepolo L (1966) In vitro study of the DNA replication patterns of somatic chromosomes of
Exp Cell Res
Bone JR, Lavender JS, Richman R, Palmer MJ, Turner BM, Kuroda MI (1994) Acetylated histone H4 on the male X chromosome is associated with dosage compensation in
Cooper KW (1959) Cytogenetic analysis of major heterochromatic elements (especially Xh and Y) in
and the theory of ‘heterochromatin’.
Gatti M, Pimpinelli S, Santini G (1976) Characterization of
heterochromatin. I. Staining and decondensation with Hoechst 33258 and quinacrine.
Gorman M, Kuroda MI, Baker BS (1993) Regulation of the sex specific binding of the maleless dosage compensation protein to the male X chromosome in
Grunstein M (1990) Histone function in transcription.
Annu Rev Cell Biol
Holmquist G (1975) Hoechst 33258 fluorescent staining of
Hsu TC (1971) Heterochromatin pattern in metaphase chromosomes of
Jeppesen P, Turner BM (1993) The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression.
Jeppesen P, Mitchell A, Turner B, Perry P (1992) Antibodies to defined histone epitopes reveal variations in chromatin conformation and underacetylation of centric heterochromatin in human metaphase chromosomes.
Johnson LS, Kayne PS, Kahn ES, Grunstein M (1990) Genetic evidence for an interaction between SIR3 and histone H4 in the repression of the silent mating loci in
Proc Natl Acad Sci USA
Kuroda MI, Kernan MJ, Kreber R, Ganetzky B, Baker BS (1991) The
protein associates with the X chromosome to regulate dosage compensation in
Kuroda MI, Palmer MJ, Lucchesi JC (1993) X chromosome dosage compensation in
Drosophila. Sem Devel Biol
Lewin B (1980)
Gene Expression, Vol. 2 Eucaryotic Chromosomes. New York: John Wiley & Sons, pp 649–652.
Lucchesi JC, Manning JE (1987) Gene dosage compensation in
Palmer MJ, Mergner VA, Richman, Manning JE, Kuroda MI, Lucchesi JC (1993) The
male specific lethal-one
-1) gene of
encodes a novel protein that associates with the male X chromosome.
Prescott DM, Bender MA (1962) Synthesis of RNA and protein during mitosis in mammalian tissue culture cells.
Exp Cell Res
Robert M (1975) Isolation and manipulation of salivary gland nuclei and chromosomes.
Methods Cell Biol
Roth SY, Shimizu M, Johnson L. Grunstein M, Simpson RT (1992) Stable nucleosome positioning and complete repression by the yeast α2 repressor are disrupted by amino terminal mutations in histone H4.
Turner BM (1993) Decoding the nucleosome.
Turner BM, Fellows G (1989) Specific antibodies reveal ordered and cell cycle-related use of histone H4 acetylation sites in mammalian cells.
Eur J Biochem
Turner BM, O'Neill LP, Allan IM (1989) Histone H4 acetylation in human cells. Frequency of acetylation at different sites defined by immunolabelling with site-specific antibodies.
Turner BM, Franchi L, Wallace H (1990) Islands of acetylated histone H4 in polytene chromosomes and their relationship to chromatin packaging and transcriptional activity.
J Cell Sci
Turner BM, Birley AJ, Lavender JS (1992) Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in
PubMed Copyright information
© Rapid Communications of Oxford Ltd 1994