The JIL-1 kinase regulates the structure of Drosophila polytene chromosomes

Abstract

The JIL-1 kinase localizes to interband regions of Drosophila polytene chromosomes and phosphorylates histone H3 Ser10. Analysis of JIL-1 hypomorphic alleles demonstrated that reduced levels of JIL-1 protein lead to global changes in polytene chromatin structure. Here we have performed a detailed ultrastructural and cytological analysis of the defects in JIL-1 mutant chromosomes. We show that all autosomes and the female X chromosome are similarly affected, whereas the defects in the male X chromosome are qualitatively different. In polytene autosomes, loss of JIL-1 leads to misalignment of interband chromatin fibrils and to increased ectopic contacts between nonhomologous regions. Furthermore, there is an abnormal coiling of the chromosomes with an intermixing of euchromatic regions and the compacted chromatin characteristic of banded regions. In contrast, coiling of the male X polytene chromosome was not observed. Instead, the shortening of the male X chromosome appeared to be caused by increased dispersal of the chromatin into a diffuse network without any discernable banded regions. To account for the observed phenotypes we propose a model in which JIL-1 functions to establish or maintain the parallel alignment of interband chromosome fibrils as well as to repress the formation of contacts and intermingling of nonhomologous chromatid regions.

The JIL-1 histone H3S10 kinase regulates dimethyl H3K9 modifications and heterochromatic spreading inDrosophila

“…The GFP-lacI transgenic stock 128.1, and the lac operator repeats transgenic stock 4D5 were the generous gifts of Dr L. Wallrath (University of Iowa, Iowa City). The application of the GFP-lacI and lac operator repeat stocks for X chromosome identification in JIL-1 mutant backgrounds is described by Deng et al (Deng et al, 2005).…”

“…The GFP-lacI transgenic stock 128.1, and the lac operator repeats transgenic stock 4D5 were the generous gifts of Dr L. Wallrath (University of Iowa, Iowa City). The application of the GFP-lacI and lac operator repeat stocks for X chromosome identification in JIL-1 mutant backgrounds is described by Deng et al (Deng et al, 2005)./TM3 Sb Ser stocks were obtained from the Bloomington Stock Center, whereas the Su(var)3-9 1 and Su(var)3-9 2 stocks were from the Umeå Stock Center. The molecular lesion of Su(var)3-1 3 was determined by PCR mapping and sequencing, as described by Zhang et al (Zhang et al, 2003).…”

A Balance Between Euchromatic (JIL-1) and Heterochromatic [SU(VAR)2-5 and SU(VAR)3-9] Factors Regulates Position-Effect Variegation inDrosophila

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ABSTRACT In this study, we show that the haplo-enhancer effect of JIL-1 has the ability to counterbalance the haplo-suppressor effect of both Su(var)3-9 and Su(var)2-5 on position-effect variegation, providing evidence that a finely tuned balance between the levels of JIL-1 and the major heterochromatin components contributes to the regulation of gene expression.T HE essential JIL-1 histone H3S10 kinase (Jin et al 1999;Wang et al 2001) is a major regulator of chromatin structure (Deng et al 2005(Deng et al , 2008) that functions to maintain euchromatic domains while counteracting heterochromatization and gene silencing (Ebert et al 2004;Lerach et al 2006;Zhang et al 2006;Bao et al 2007). In the absence of the JIL-1 kinase, the major heterochromatin markers H3K9me2, HP1a [Su(var)2-5], and Su(var)3-7 spread to ectopic locations on the chromosome arms Deng et al 2007Deng et al , 2010.

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Loss-of-Function Alleles of the JIL-1 Histone H3S10 Kinase Enhance Position-Effect Variegation at Pericentric Sites in Drosophila Heterochromatin

“…Transgenes inserted into centromeric regions of chromosomes in Drosophila can exhibit position-effect variegation (PEV), a mosaic silencing of transcription of euchromatic genes as a result of their placement in or near heterochromatin (reviewed by Wallrath 1998;Henikoff 2000;Schotta et al 2003;Girton and Johansen 2007). It has recently been demonstrated that alleles of the JIL-1 locus are important regulators of chromatin structure and gene expression (Wang et al 2001;Ebert et al 2004;Deng et al 2005;Lerach et al 2005Lerach et al , 2006. The JIL-1 histone H3S10 tandem kinase localizes specifically to euchromatic interband regions of polytene chromosomes in Drosophila ( Jin et al 1999) and analysis of a JIL-1 null allele, JIL-1 z2 , has shown that JIL-1 is essential for viability (Wang et al 2001;Zhang et al 2003).…”