Coordinated regulation of heterochromatic genes in Drosophila melanogaster males

Genetics

Volumn 182, Issue 2, 2009, Pages 481-491

  Deng, Xinxian ^a,c   Koya, S Kiran ^a   Kong, Ying ^a   Meller, Victoria H ^a,b  

^a WAYNE STATE UNIVERSITY   (United States)

^b KARMANOS CANCER INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOPROTEIN; UNTRANSLATED RNA; DROSOPHILA PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL NUCLEUS; CHROMATIN; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EVOLUTION; FEMALE; GENE CONTROL; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC TRANSCRIPTION; HETEROCHROMATIN; MALE; NONHUMAN; POSITION EFFECT VARIEGATION; PRIORITY JOURNAL; REGULATORY MECHANISM; X CHROMOSOME; Y CHROMOSOME; ANIMAL; GENE; GENETICS; LARVA; METABOLISM; SEXUAL DEVELOPMENT;

DROSOPHILA MELANOGASTER;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; GENES, INSECT; HETEROCHROMATIN; LARVA; MALE; RNA, UNTRANSLATED; SEX CHARACTERISTICS; TRANSCRIPTION FACTORS; X CHROMOSOME;

EID: 68949219467     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.102087     Document Type: Article

References (65)

1. AKHTAR, A., and P. B. BECKER, 2000 Activation of transcription through histone H4acetylation byMOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol. Cell 5: 367-375.
2. ALEKSEYENKO, A. A., S. PENG, E. LARSCHAN, A. A. GORCHAKOV, O.-K. LEE et al., 2008 A sequence motif within chromatin entry sites directs MSL establishment on the Drosophila X chromosome. Cell 134: 599-609.
3. BAKER, B. S., M. GORMAN and I. MARIN, 1994 Dosage compensation in Drosophila. Annu. Rev. Genet. 28: 491-521.
4. BONALDI, T., T. STRAUB, J. COX, C. KUMAR, P. B. BECKER et al., 2008 Combined use of RNAi and quantitative proteomics to study gene function in Drosophila. Mol. Cell 31: 762-772.
5. CARVALHO, A. B., 2002 Origin and evolution of the Drosophila Y chromosome. Curr. Opin. Genet. Dev. 12: 664-668.
6. CHARLESWORTH, B., 1991 The evolution of sex chromosomes. Science 251: 1030-1033.
7. COPPS, K., R. RICHMAN, L. M. LYMAN, K. A. CHANG, J. RAMPERSAD-AMMONS et al., 1998 Complex formation by the Drosophila MSL proteins: role of the MSL2 RING finger in protein complex assembly. EMBO J. 17: 5409-5417.
8. CORONA, D. F., C. R. CLAPIER, P. B. BECKER and J. W. TAMKUN, 2002 Modulation of ISWI function by site-specific histone acetylation. EMBO Rep. 3: 242-247. (Pubitemid 34269517)
9. DE WIT, E., F. GREIL and B. VAN STEENSEL, 2005 Genome-wide HP1 binding in Drosophila: developmental plasticity and genomic targeting signals. Genome Res. 15: 1265-1273.
10. DENG, X., and V. H. MELLER, 2006 roX RNAs are required for increased expression of X-linked genes in Drosophila melanogaster males. Genetics 174: 1859-1866.
11. DENG, X., B. P. RATTNER, S. SOUTER and V. H. MELLER, 2005 The severity of roX1 mutations are predicted by MSL localization on the X chromosome. Mech. Dev. 122: 1094-1105.
12. EBERT, A., G. SCHOTTA, S. LEIN, S. KUBICEK, V. KRAUSS et al., 2004 Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev. 18: 2973-2983.
13. GAUTIER, L., L. COPE, B.M. BOLSTAD and R. A. IRIZARRY, 2004 affy: Analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
14. GUPTA, V., M. PARISI, D. STURGILL, R. NUTTALL, M. DOCTOLERO et al., 2006 Global analysis of X Chromosome compensation. J. Biol. 5: 3.
15. HAMADA, F. N., P. J. PARK, P. R. GORDADZE and M. I. KURODA, 2005 Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster. Genes Dev. 19: 2289-2294. (Pubitemid 41396905)
16. HAYNES, K. A., E. GRACHEVA and S. C. R. ELGIN, 2007 A distinct type of heterochromatin within Drosophila melanogaster chromosome 4. Genetics 175: 1539-1542.
17. HOSKINS, R. A., J. W. CARLSON, C. KENNEDY, D. ACEVEDO, M. EVANS-HOLM et al., 2007 Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 316: 1625-1628. (Pubitemid 46982037)
18. IRIZARRY, R. A., B. HOBBS, F. COLLIN, Y. D. BEAZER-BARCLAY, K. J. ANTONELLIS et al., 2003 Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
19. JOHANSSON, A.-M., P. STENBERG, C. BERNHARDSSON AND J. LARSSON, 2007 Painting of fourth and chromosome-wide regulation of the 4th chromosome in Drosophila melanogaster. EMBO J. 26: 2307-2316.
20. KELLEY, R. L., V. H. MELLER, P. R. GORDADZE, G. ROMAN, R. L. DAVIS et al., 1999 Epigenetic spreading of the Drosophila dosage compensation complex from roX RNA genes into flanking chromatin. Cell 98: 513-522.
21. KELLEY, R. L., I. SOLOVYEVA, L. M. LYMAN, R. RICHMAN, V. SOLOVYEV et al., 1995 Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila. Cell 81: 867-877.
22. KIND, J., and A. AKHTAR, 2007 Cotranscriptional recruitment of the dosage compensation complex to X-linked target genes. Genes Dev. 21: 2030-2040. (Pubitemid 47267289)
23. KIND, J., J. M. VAQUERIZAS, P. GEBHARDT, M. GENTZEL, N. M. LUSCOMBE et al., 2008 Genome-wide analysis reveals MOF as a key regulator of dosage compensation and gene expression in Drosophila. Cell 133: 813-828.
24. KOTLIKOVA, I. V., O. V. DEMAKOVA, V. F. SEMESHIN, V. V. SHLOMA, L. V. BOLDYREVA et al., 2006 The Drosophila dosage compensation complex binds to polytene chromosomes independently of developmental changes in transcription. Genetics 172: 963-974.
25. LARSCHAN, E., A. A. ALEKSEYENKO, A. A. GORTCHAKOV, S. PENG, B. LI et al., 2007 MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism. Mol. Cell 28: 121-133.
26. LARSSON, J., J. D. CHEN, V. RASHEVA, A. RASMUSON-LESTANDER and V. PIRROTTA, 2001 Painting of fourth, a chromosome-specific protein in Drosophila. Proc. Natl. Acad. Sci. USA 98: 6273-6278.
27. LARSSON, J., AND V. H. MELLER, 2006 Dosage compensation, the origin and afterlife of sex chromosomes. Chromosome Res. 14: 417-431.
28. LARSSON, J., M. J. SVENSSON, P. STENBERG and M. MAKITALO, 2004 Painting of fourth in genus Drosophila suggests autosome-specific gene regulation. Proc. Natl. Acad. Sci. USA 101: 9728-9733.
29. m4 allele in Drosophila. Genetics 173: 2403-2406.
30. LERACH, S., W. ZHANG, H. DENG, X. BAO, J. GIRTON et al., 2005 JIL-1 kinase, a member of the Male-specific lethal (MSL) complex, is necessary for proper dosage compensation of eye pigmentation in Drosophila. Genesis 43: 213-215.
31. LI, F., D. A. PARRY and M. J. SCOTT, 2005 The amino-terminal region of Drosphila MSL1 contains basic, glycine-rich and leucine zipper-like motifs that promote X chromosome binding, self-association and MSL2 binding, respectively. Mol. Cell. Biol. 25: 8913-8924.
32. LINDSLEY, D. L., and G. G. ZIMM, 1992 The Genome of Drosophila melanogaster. Academic Press, San Diego.
33. LIU, L.-P., J.-Q. NI, Y.-D. SHI, E. J. OAKELEY and F.-L. SUN, 2005 Sexspecific roleofDrosophilamelanogasterHP1 in regulatingchromatin structure and gene transcription. Nat. Genet. 37: 1361-1366.
34. LIU, T.-Y., C. W. LIN, S. FALCON, J. ZHANG and J. W. MACDONALD, 2007 drosophila2: Affymetrix Drosophila Genome 2.0 Array Annotation Data (drosophila2). R packager version 2.2.0.
35. LU, B. Y., J. MA and J. C. EISSENBERG, 1998 Developmental regulation of heterochromatin-mediated gene silencing in Drosophila. Development 125: 2223-2234. (Pubitemid 28336384)
36. LUCCHESI, J. C., W. G. KELLY and B. PANNING, 2005 Chromatin remodeling in dosage compensation. Annu. Rev. Genet. 39: 615-651.
37. MAGGERT, K. A., and K. G. GOLIC, 2002 The Y chromosome of Drosophila melanogaster exhibits chromosome-wide imprinting. Genetics 162: 1245-1258. (Pubitemid 35417516)
38. MELLER, V. H., 2003 Initiation of dosage compensation in Drosophila embryos depends on expression of the roX RNAs. Mech. Dev. 120: 759-767.
39. MELLER, V. H., and B. P. RATTNER, 2002 The roX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex. EMBO J. 21: 1084-1091.
40. MELLER, V. H., K. H. WU, G. ROMAN, M. I. KURODA and R. L. DAVIS, 1997 roX1 RNA paints the X chromosome of male Drosophila and is regulated by the dosage compensation system. Cell 88: 445-457.
41. NGUYEN, D. K., and C. M. DISTECHE, 2006 Dosage compensation of the active X chromosome in mammals. Nat. Genet. 38: 47-53.
42. PALMER, M. J., R. RICHMAN, L. RICHTER and M. I. KURODA, 1994 Sex-specific regulation of the male-specific lethal-1 dosage compensation gene in Drosophila. Genes Dev. 8: 698-706.
43. PARISI, M., R. NUTTALL, D. NAIMAN, G. BOUFFARD, J. MALLEY et al., 2003 Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299: 697-700.
44. PFAFFL, M. W., 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
45. RASTELLI, L., and M. I. KURODA, 1998 An analysis of maleless and histone H4 acetylation in Drosophila melanogaster spermatogenesis. Mech. Dev. 71: 107-117.
46. RASTELLI, L., R. RICHMAN and M. I. KURODA, 1995 The dosage compensation regulators MLE, MSL-1 and MSL-2 are interdependent since early embryogenesis in Drosophila. Mech. Dev. 53: 223-233.
47. RATTNER, B. P., and V. H. MELLER, 2004 Drosophila Male Specific Lethal 2 protein controls male-specific expression of the roX genes. Genetics 166: 1825-1832.
48. RICE, W. R., 1996 Evolution of the Y sex chromosome in animals. Bioscience 46: 331-343.
49. RIDDLE, N. C., and S. C. R. ELGIN, 2006 The dot chromosome of Drosophila: insights into chromatin states and their change over evolutionary time. Chromosome Res. 14: 405-416.
50. RIDDLE, N. C., W. LEUNG, K. A. HAYNES, H. GRANOK, J. WULLER et al., 2008 An investigation of heterochromatin domains on the fourth chromosome of Drosophila melanogaster. Genetics 178: 1177-1191.
51. SEUM, C., E. REO, H. PENG, F. J. RAUSCHER, P. SPIERER et al., 2007 Drosophila SETDB1 is required for chromosome 4 silencing. PLoS Genet. 3: e76.
52. SMITH, C. D., S. SHU, C. J. MUNGALL and G. H. KARPEN, 2007 The release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 316: 1586-1591. (Pubitemid 46982025)
53. SMYTH, G. K., 2005 Limma: linear models for microarray data, pp. 397-420 in Bioinformatics and Computational Biology Solutions Using R and 'Bioconductor,' edited by R. GENTLEMAN, V. CAREY, S. DUDOIT, R. IRIZARRY and W. HUBER. Springer, New York.
54. SPIERER, A., F. BEGOT, P. SPIERER and M. DELATTRE, 2008 Su(var)3-7 links heterochromatin and dosage compensation in Drosophila. PLoS Genet. 4: e1000066.
55. SPIERER, A., C. SEUM, M. DELATTRE and P. SPIERER, 2005 Loss of the modifiers of variegation Su(var)3-7 or HP1 impacts male X polytene chromosome morphology and dosage compensation. J. Cell Sci. 118: 5047-5057.
56. SUN, F. L., M. H. CUAYCONG, C. A. CRAIG, L. L. WALLRATH, J. LOCKE et al., 2000 The fourth chromosome of Drosophila melanogaster: interspersed euchromatic and heterochromatic domains. Proc. Natl. Acad. Sci. USA 97: 5340-5345.
57. TSAI, C. J., D. G. METS, M. R. ALBRECHT, P. NIX, A. CHAN et al., 2008 Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev. 22: 194-211.
58. TZENG, T.-Y., C.-H. LEE, L.-W. CHAN and J. SHEN, 2007 Epigenetic regulation of the Drosophila chromosome 4 by the histone H3K9 methyltransferase dSETDB1. Proc. Natl. Acad. Sci. USA 104: 12691-12696.
59. VLASSOVA, I. E., A. S. GRAPHODATSKY, E. S. BELYAEVA and I. F. ZHIMULEV, 1991 Constitutive heterochromatin in early embryogenesis of Drosophila melanogaster. Mol. Gen. Genet. 229: 316-318.
60. WALLRATH, L. L., and S. C. R. ELGIN, 1995 Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev. 9: 1263-1277.
61. WEILER, K. S., and B. T. WAKIMOTO, 1995 Heterochromatin and gene expression in Drosophila. Annu. Rev. Genet. 29: 577-605.
62. YAN, C. M., K. W. DOBIE, H. D. Le, A. Y. KONEV and G. H. KARPEN, 2002 Efficient recovery of centric heterochromatin P-element insertions in Drosophila melanogaster. Genetics 161: 217-229.
63. YASUHARA, J. C., and B. T. WAKIMOTO, 2006 Oxymoron no more: the expanding world of heterochromatic genes. Trends Genet. 22: 330-338.
64. YASUHARA, J. C., and B. T. WAKIMOTO, 2008 Molecular landscape of modified histones in Drosophila heterochromatic genes and euchromatin-heterochromatin transition zones. PLoS Genet. 4: 159-172.
65. ZHANG, W., H. DENG, X. BAO, S. LERACH, J. GIRTON et al., 2006 The JIL-1 histone H3S10 kinase regulates dimethyl H3K9 modifications and heterochromatic spreading in Drosophila. Development 133: 229-235.