Genetically Derepressed Nucleoplasmic Stellate Protein in Spermatocytes of D. melanogaster Interacts with the Catalytic Subunit of Protein Kinase 2 and Carries Histone-Like Lysine-Methylated Mark

Journal of Molecular Biology

Volumn 389, Issue 5, 2009, Pages 895-906

  Egorova, Ksenia S ^a   Olenkina, Oxana M ^a   Kibanov, Mikhail V ^a   Kalmykova, Alla I ^a   Gvozdev, Vladimir A ^a   Olenina, Ludmila V ^a  

^a INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

Author keywords

lysine trimethylation; protein kinase CK2; spermatogenesis; Stellate; testes

Indexed keywords

CASEIN KINASE II; CASEIN KINASE IIALPHA; CELL PROTEIN; HISTONE H3; STELLATE PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA MELANOGASTER; EPIGENETICS; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SPERMATOGENESIS; STELLATE CELL;

DROSOPHILA MELANOGASTER;

EID: 67349150000     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.04.064     Document Type: Article

References (45)

1. Hardy R.W., Lindsley D.L., Livak K.J., Lewis B., Siversten A.V., Joslyn G.L., et al. Cytogenetic analysis of a segment of the Y chromosome of Drosophila melanogaster. Genetics 107 (1984) 591-610
2. Livak K.J. Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics 107 (1984) 611-634
3. Palumbo G., Bonaccorsi S., Robbins L., and Pimpinelli S. Genetic analysis of Stellate elements of Drosophila melanogaster. Genetics 138 (1994) 1181-1197
4. Aravin A.A., Naumova N.M., Tulin A.V., Vagin V.V., Rozovsky Y.M., and Gvozdev V.A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol. 11 (2001) 1017-1027
5. Aravin A.A., Klenov M.S., Vagin V.V., Bantignies F., Cavalli G., and Gvozdev V.A. Dissection of a natural RNA silencing process in the Drosophila melanogaster germ line. Mol. Cell. Biol. 24 (2004) 6742-6750
6. Vagin V.V., Sigova A., Li C., Seitz H., Gvozdev V., and Zamore P.D. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313 (2006) 320-324
7. Livak K.J. Detailed structure of the Drosophila melanogaster Stellate genes and their transcripts. Genetics 124 (1990) 303-316
8. Bozzetti M.P., Massari S., Finelli P., Meggio F., Pinna L.A., Boldyreff B., et al. The Ste locus, a component of the parasitic cry-Ste system of Drosophila melanogaster, encodes a protein that forms crystals in primary spermatocytes and mimics properties of the β-subunit of casein kinase 2. Proc. Natl Acad. Sci. USA 92 (1995) 6067-6071
9. Bibby A.C., and Litchfield D.W. The multiple personalities of the regulatory subunit of protein kinase CK2: CK2 dependent and CK2 independent roles reveal a secret identity for CK2β. Int. J. Biol. Sci. 1 (2005) 67-79
10. Zhao T., and Eissenberg J.C. Phosphorylation of heterochromatin protein 1 by casein kinase II is required for efficient heterochromatin binding in Drosophila. J. Biol. Chem. 274 (1999) 15095-15100
11. Ackerman P., Glover C.V., and Osheroff N. Phosphorylation of DNA topoisomerase II by casein kinase II: modulation of eukaryotic topoisomerase II activity in vitro. Proc. Natl Acad. Sci. USA 82 (1985) 3164-3168
12. Takemoto A., Kimura K., Yanagisawa J., Yokoyama S., and Hanaoka F. Negative regulation of condensin I by CK2-mediated phosphorylation. EMBO J. 25 (2006) 5339-5348
13. Cenci G., Bonaccorsi S., Pisano C., Verni F., and Gatti M. Chromatin and microtubule organization during premeiotic, meiotic and early postmeiotic stages of Drosophila melanogaster spermatogenesis. J. Cell Sci. 107 (1994) 3521-3534
14. Vazquez J., Belmont A.S., and Sedat J.W. The dynamics of homologous chromosome pairing during male Drosophila meiosis. Curr. Biol. 12 (2002) 1473-1483
15. Mendez J., and Stillman B. Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20 (2000) 8602-8612
16. DePamphilis M.L. Cell cycle dependent regulation of the origin recognition complex. Cell Cycle 4 (2005) 70-79
17. Bidwai A.P., Saxena A., Zhao W., McCann R.O., and Glover C.V. Multiple, closely spaced alternative 5′ exons in the DmCKIIβ gene of Drosophila melanogaster. Mol. Cell. Biol. Res. Commun. 3 (2000) 283-291
18. Kalmykova A.I., Shevelyov Y.Y., Polesskaya O.O., Dobritsa A.A., Evstafieva A.G., Boldyreff B., et al. CK2βtes gene encodes a testis-specific isoform of the regulatory subunit of casein kinase 2 in Drosophila melanogaster. Eur. J. Biochem. 269 (2002) 1418-1427
19. Jauch E., Melzig J., Brkulj M., and Raabe T. In vivo functional analysis of Drosophila protein kinase casein kinase 2 (CK2) β-subunit. Gene 298 (2002) 29-39
20. Karandikar U., Anderson S., Mason N., Trott R.L., Bishop C.P., and Bidwai A.P. The Drosophila SSL gene is expressed in larvae, pupae, and adults, exhibits sexual dimorphism, and mimics properties of the β subunit of casein kinase II. Biochem. Biophys. Res. Commun. 301 (2003) 941-947
21. Waggener J.M., and DiMario P.J. Two splice variants of Nopp140 in Drosophila melanogaster. Mol. Biol. Cell. 13 (2002) 362-381
22. Karandikar U.C., Shaffer J., Bishop C.P., and Bidwai A.P. Drosophila CK2 phosphorylates Deadpan, a member of the HES family of basic-helix-loop-helix (bHLH) repressors. Mol. Cell. Biochem. 274 (2005) 133-139
23. Kahali B., Trott R., Paroush Z., Allada R., Bishop C.P., and Bidwai A.P. Drosophila CK2 phosphorylates Hairy and regulates its activity in vivo. Biochem. Biophys. Res. Commun. 373 (2008) 637-642
24. Bonet C., Fernandez I., Aran X., Bernues J., Giralt E., and Azorin F. The GAGA protein of Drosophila is phosphorylated by CK2. J. Mol. Biol. 351 (2005) 562-572
25. Lin J.M., Schroeder A., and Allada R. In vivo circadian function of casein kinase 2 phosphorylation sites in Drosophila PERIOD. J. Neurosci. 25 (2005) 11175-11183
26. Bouazoune K., and Brehm A. dMi-2 chromatin binding and remodeling activities are regulated by dCK2 phosphorylation. J. Biol. Chem. 280 (2005) 41912-44120
27. Kellum R., and Alberts B.M. Heterochromatin protein 1 is required for correct chromosome segregation in Drosophila embryos. J. Cell Sci. 108 (1995) 1419-1431
28. Bettencourt-Dias M., Giet R., Sinka R., Mazumdar A., Lock W.G., Balloux F., et al. Genome-wide survey of protein kinases required for cell cycle progression. Nature 432 (2004) 980-987
29. Martin C., and Zhang Y. The diverse function of histone lysine methylation. Nat. Rev. Mol. Cell. Biol. 6 (2005) 838-849
30. Chuikov S., Kurash J.K., Wilson J.R., Xiao B., Justin N., Ivanov G.S., et al. Regulation of p53 activity through lysine methylation. Nature 432 (2004) 353-360
31. Kouskouti A., Scheer E., Staub A., Tora L., and Talianidis I. Gene-specific modulation of TAF10 function by SET9-mediated methylation. Mol. Cell 14 (2004) 175-182
32. Rathert P., Dhayalan A., Murakami M., Zhang X., Tamas R., Jurkowska R., et al. Protein lysine methyltransferase G9a acts on non-histone targets. Nat. Chem. Biol. 4 (2008) 344-346
33. Sampath S.C., Marazzi I., Yap K.L., Sampath S.C., Krutchinsky A.N., Mecklenbrauker I., et al. Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly. Mol. Cell 27 (2007) 596-608
34. Chin H.G., Esteve P.-O., Pradhan M., Benner J., Patnaik D., Carey M.F., and Pradhan S. Automethylation of G9a and its implication in wider substrate specificity and HP1 binding. Nucleic Acids Res. 35 (2007) 7313-7323
35. Lachner M., O'Carroll D., Rea S., Mechtler K., and Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410 (2001) 116-120
36. Cheng X., and Zhang X. Structural dynamics of protein lysine methylation and demethylation. Mutat. Res. 618 (2007) 102-115
37. Schotta G., Ebert A., Krauss V., Fischer A., Hoffmann J., Rea S., et al. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 21 (2002) 1121-1131
38. Stabell M., Eskeland R., Bjørkmo M., Larsson J., Aalen R., Imhof A., and Lambertsson A. The Drosophila G9a gene encodes a multi-catalytic histone methyltransferase required for normal development. Nucleic Acids Res. 34 (2006) 4609-4621
39. Seum C., Reo E., Peng H., Rauscher III F.J., Spierer P., and Bontron S. Drosophila SETDB1 is required for chromosome 4 silencing. PLoS Genet. 3 (2007) 0709-0719
40. Yoon J., Lee K.-S., Park J.S., Yu K., Paik S.-G., and Kang Y.K. dSETDB1 and SU(VAR)3-9 sequentially function during germline-stem cell differentiation in Drosophila melanogaster. PLoS ONE 3 (2008) 1-11
41. Tulin A.V., Naumova N.M., Aravin A.A., and Gvozdev V.A. Repeated, protein-encoding heterochromatic genes cause inactivation of a juxtaposed euchromatic gene. FEBS Lett. 425 (1998) 513-516
42. Hinton R.H., and Mullock B.M. Isolation of subcellular fractions. In: Graham J.M., and Rickwood D. (Eds). Subcellular fractionation: A Practical Approach (1997), Oxford University Press, New York 31-69
43. Wessel D., and Fluegge U.I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138 (1984) 141-143
44. Vann L.R., Wooding F.B., Irvine R.F., and Divecha N. Metabolism and possible compartmentalization of inositol lipids in isolated rat-liver nuclei. Biochem J. 327 (1997) 569-576
45. Shevchenko A., Tomas H., Havlis J., Olsen J.V., and Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1 (2006) 2856-2860