Evidence against a Role for the JIL-1 Kinase in H3S28 Phosphorylation and 14-3-3 Recruitment to Active Genes in Drosophila

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Wang, Chao ^a   Yao, Changfu ^a   Li, Yeran ^a   Cai, Weili ^a   Bao, Xiaomin ^a   Girton, Jack ^a   Johansen, Jørgen ^a   Johansen, Kristen M ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ENZYME; JIL 1 KINASE; PROTEIN 14 3 3; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HISTONE; JIL-1 PROTEIN, DROSOPHILA; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CELL NUCLEUS MATRIX; CELLULAR DISTRIBUTION; CHROMOSOMAL LOCALIZATION; CHROMOSOME ARM; CONTROLLED STUDY; CROSS REACTION; DROSOPHILA; ENZYME ACTIVITY; HISTONE PHOSPHORYLATION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MUTANT; NEUROBLAST; NONHUMAN; PROTEIN BINDING; PROTEIN LOCALIZATION; SALIVARY GLAND; UPREGULATION; WILD TYPE; X CHROMOSOME; ANIMAL; GENE; GENE DELETION; GENETICS; METABOLISM; PHOSPHORYLATION; POLYTENE CHROMOSOME;

14-3-3 PROTEINS; ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; GENE DELETION; GENES, INSECT; HISTONES; PHOSPHORYLATION; POLYTENE CHROMOSOMES; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; UP-REGULATION;

EID: 84876957818     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062484     Document Type: Article

References (35)

1. Jin Y, Wang Y, Walker DL, Dong H, Conley C, et al. (1999) JIL-1: a novel chromosomal kinase implicated in transcriptional regulation in Drosophila. Mol Cell 4: 129-135.
2. Wang Y, Zhang W, Jin Y, Johansen J, Johansen KM, (2001) The JIL-1 tandem kinase mediates histone H3 phosphorylation and is required for maintenance of chromatin structure in Drosophila. Cell 105: 433-443.
3. Cai W, Wang C, Shen L, Li Y, Liu S, et al. (2011) Genome wide analysis of of the binding sites of the JIL-1 H3S10 kinase and its contribution to modulation of gene expression. Mol Biol Cell 22: 1097 doi: 10.1091/mbc.E11-10-0886.
4. Wang C, Cai W, Li Y, Girton J, Johansen J, et al. (2012) H3S10 phosphorylation by the JIL-1 kinase regulates H3K9 dimethylation and gene expression at the white locus in Drosophila. Fly 6: 1-5.
5. Ebert A, Schotta G, Lein S, Kubicek S, Krauss V, et al. (2004) Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev 18: 2973-2983.
6. Zhang W, Deng H, Bao X, Lerach S, Girton J, et al. (2006) The JIL-1 histone H3S10 kinase regulates dimethyl H3K9 modifications and heterochromatic spreading in Drosophila. Development 133: 229-235.
7. Deng H, Cai W, Wang C, Lerach S, Delattre M, et al. (2010) JIL-1 and Su(var)3-7 interact genetically and counterbalance each others' effect on position effect variegation in Drosophila. Genetics 185: 1183-1192.
8. Wang C, Cai W, Li Y, Deng H, Bao X, et al. (2011) The epigenetic H3S10 phosphorylation mark is required for counteracting heterochromatic spreading and gene silencing in Drosophila melanogaster. J Cell Sci 124: 4309-4317.
9. Ivaldi MS, Karam CS, Corces VG, (2007) Phosphorylation of histone H3 at Ser10 facilitates RNA polymerase II release from promoter-proximal pausing in Drosophila. Genes Dev 21: 2818-2831.
10. Karam CS, Kellner WA, Takenada N, Clemmons AW, Corces VG, (2010) 14-3-3 mediates histone cross-talk during transcription elongation in Drosophila. PLoS Genetics 6: e1000975 doi: 10.1371/journal.pgen.1000975.
11. Kellner WA, Ramos E, Bortle KV, Takenada N, Corces VG, (2012) Genome-wide phosphoacetylation of histone H3 at Drosophila enhancers and promoters. Genome Res 22: 1081-1088.
12. Cai W, Bao X, Deng H, Jin Y, Girton J, et al. (2008) RNA polymerase II-mediated transcription at active loci does not require histone H3S10 phosphorylation in Drosophila. Development 135: 2917-2925.
13. Roberts DB. (1998) Drosophila: A Practical Approach, 2nd ed, IRL Press, Oxford, UK.
14. Zhang W, Jin Y, Ji Y, Girton J, Johansen J, et al. (2003) Genetic and phenotypic analysis of alleles of the Drosophila chromosomal JIL-1 kinase reveals a functional requirement at multiple developmental stages. Genetics 165: 1341-1354.
15. Deng H, Zhang W, Bao X, Martin JN, Girton J, et al. (2005) The JIL-1 kinase regulates the structure of Drosophila polytene chromosomes. Chromosoma 114: 173-182.
16. Yao C, Rath U, Maiato H, Sharp D, Girton J, et al. (2012) A nuclear-derived proteinaceous matrix embeds the microtubule spindle apparatus during mitosis. Mol Biol Cell 23: 3532-3541.
17. Deng H, Bao X, Cai W, Blacketer MJ, Belmont AS, et al. (2008) Ectopic histone H3S10 phosphorylation causes chromatin structure remodeling in Drosophila. Development 135: 699-705.
18. Li Y, Danzer JR, Alvarez P, Belmont A, Wallrath LL, (2003) Effects of tethering HP1 to euchromatic regions of the Drosophila genome. Development 130: 1817-1824.
19. Nowak SJ, Pai C-Y, Corces VG, (2003) Protein phosphatase 2A activity affects histone H3 phosphorylation and transcription in Drosophila melanogaster. Mol Cell Biol 23: 6129-6138.
20. Cai W, Jin Y, Girton J, Johansen J, Johansen KM (2010) Preparation of polytene chromosome squashes for antibody labeling. J Vis Exp http://www.jove.com/index/Details.stp?ID=1748. doi: 10.3791/1748.
21. Bonaccorsi S, Giansanti MG, Gatti M, (2000) Spindle assembly in Drosophila neuroblasts and ganglion mother cells. Nat Cell Biol 2: 54-6.
22. Ding Y, Yao C, Lince-Faria M, Rath U, Cai W, et al. (2009) Chromator is required for proper microtubule spindle formation and mitosis in Drosophila. Dev Biol 334: 253-263.
23. Qi H, Yao C, Cai W, Girton J, Johansen KM, et al. (2009) Asator, a tau-tubulin kinase homolog in Drosophila localizes to the mitotic spindle. Dev Dynamics 238: 3248-3256.
24. Jin Y, Wang Y, Johansen J, Johansen KM, (2000) JIL-1, a chromosomal kinase implicated in regulation of chromatin structure, associates with the MSL dosage compensation complex. J Cell Biol 149: 1005-1010.
25. Yao C, Ding Y, Cai W, Wang C, Girton J, et al. (2012) The chromodomain-containing NH2-terminus of Chromator interacts with histone H1 and is required for correct targeting to chromatin. Chromosoma 121: 209-220.
26. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, NY.
27. Bao X, Cai W, Deng H, Zhang W, Krencik R, et al. (2008) The COOH-terminal domain of the JIL-1 histone H3S10 kinase interacts with histone H3 and is required for correct targeting to chromatin. J Biol Chem 283: 32741-32750.
28. Perez-Cadahia B, Drobic B, Davie JR, (2009) H3 phosphorylation: dual role in mitosis and interphase. Biochem Cell Biol 87: 695-709.
29. Giet R, Glover DM, (2001) Drosophila Aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152: 669-681.
30. Morrison DK, (2008) The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol 19: 16-23.
31. Su TT, Parry DH, Donahoe B, Chien C-T, O'Farrell PH, et al. (2001) Cell cycle roles for two 14-3-3 proteins during Drosophila development. J Cell Sci 114: 3445-3462.
32. Yano M, Nakamuta S, Wu X, Okumura Y, Kido H, (2006) A novel function of 14-3-3 protein: 14-3-3ζ is a heat-shock-related molecular chaperone that dissolves thermal-aggregated proteins. Mol Biol Cell 17: 4769-4779.
33. Qi H, Rath U, Wang D, Xu Y-Z, Ding Y, et al. (2004) Megator, an essential coiled-coil protein localizes to the putative spindle matrix during mitosis. Mol Biol Cell 15: 4854-4865.
34. Qi H, Rath U, Ding Y, Ji Y, Blacketer MJ, et al. (2005) EAST interacts with Megator and localizes to the putative spindle matrix during mitosis in Drosophila. J Cell Biochem 95: 1284-1291.
35. Regnard C, Straub T, Mitterweger A, Dahlsveen IK, Fabian V, et al. (2011) Global analysis of the relationship between JIL-1 kinase and transcription. PLoS Genetics 7: e1001327 doi: 10.1371/journal.pgen.1001327.