Requirement of male-specific dosage compensation in Drosophila females-implications of early X chromosome gene expression

PLoS Genetics

Volumn 6, Issue 7, 2010, Pages 1-10

  Gladstein, Natalie ^a   McKeon, Meghan N ^a   Horabin, Jamila I ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; MALE SPECIFIC LETHAL PROTEIN 1; MALE SPECIFIC LETHAL PROTEIN 3; MALE SPECIFIC LETHALS PROTEIN; SEX LETHAL PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; RNA BINDING PROTEIN; SXL PROTEIN, DROSOPHILA;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; FEMALE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE FUNCTION; HOMOZYGOSITY; INSECT GENETICS; MALE; NONHUMAN; NULL ALLELE; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SEX CHROMOSOME; SEX DETERMINATION; SEX TRANSFORMATION; TRANSCRIPTION REGULATION; UPREGULATION; X CHROMOSOME; ANIMAL; GENE EXPRESSION; GENETICS; PHYSIOLOGY; X CHROMOSOMAL INHERITANCE;

ANIMALS; DOSAGE COMPENSATION, GENETIC; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES, X-LINKED; MALE; RNA-BINDING PROTEINS; X CHROMOSOME;

EID: 77957360463     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001041     Document Type: Article

References (46)

1. Lucchesi JC, Kelly WG, Panning B (2005) Chromatin remodeling in dosage compensation. Annual Review of Genetics 39: 615-51.
2. Fukunaga A, Tanaka A, Oishi K (1975) Maleless, a recessive autosomal mutant of Drosophila melanogaster that specifically kills male zygotes. Genetics 81: 135-141.
3. Belote J, Lucchesi JC (1980) Male-specific lethal mutations of Drosophila melanogaster. Genetics 96: 165-186.
4. Uchida S, Uenoyama T, Oishi K (1981) Studies on the sex-specific lethal of Drosophila melanogaster III. A third chromosome male-specific lethal mutant. Jpn J Genet 56: 523-527.
5. Hilficker A, Hilfiker-Kleiner D, Pannuti A, Lucchesi JC (1997) mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila. EMBO J 16: 2054-2060.
6. Kelley RL (2004) Path to equality strewn with roX. Dev Biol 269: 18-25.
7. Gelbart ME, Kuroda MI (2009) Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136: 1399-1410.
8. Franke A, Baker BS (1999) The roX1 and roX2 RNAs Are Essential Components of the Compensasome, which Mediates Dosage Compensation in Drosophila. Mol Cell 4: 117-122.
9. Meller VH (2003) Initiation of dosage compensation in Drosophila embryos depends on expression of the roX RNAs. Mech Dev 120: 759-67.
10. Jin Y, Wang Y, Walker DL, Dong H, Conley C, et al. (1999) JIL-1: A Novel Chromosomal Tandem Kinase Implicated in Transcriptional Regulation in Drosophila. Mol Cell 4: 129-135.
11. Skripsky T, Lucchesi JC (1980) Females with sex-combs. Genetics 94: s98-s99.
12. Uenoyama T, Fukunaga A, Oishi K (1982) Studies on the sex-specific lethals of Drosophila melanogaster V. sex transformation caused by interactions between a female-specific lethal, Sxlf#1, and the male-specific lethals mle(3)132, ms1-227, and mle. Genetics 102: 233-243.
13. Bashaw GJ, Baker BS (1995) The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex specifically regulated by Sex-lethal. Development 121: 3245-58.
14. Bashaw GJ, Baker BS (1997) The regulation of the Drosophila msl-2 gene reveals a function for Sex-lethal in translational control. Cell 89: 789-798.
15. Kelley RL, Solovyeva I, Lyman LM, Richman R, Solovyev V, 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.
16. Kelley RL, Wang J, Bell L, Kuroda MI (1997) Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 387: 195-199.
17. Zhou S, Yang Y, Scott MJ, Pannuti A, Fehr KC, et al. (1999) Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cysteine cluster. EMBO J 14: 2884-2895.
18. Keyes LN, Cline TW, Schedl P (1992) The Primary Sex Determination Signal of Drosophila Acts at the Level of Transcription. Cell 68: 933-943.
19. Schutt C, Nothiger R (2000) Structure, function and evolution of sexdetermining systems in Dipteran insects. Development 127: 667-677.
20. Bell L, Horabin J, Schedl P, Cline T (1991) Positive autoregulation of Sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 65: 229-239.
21. Kind J, Akhtar A (2007) Cotranscriptional recruitment of the dosage compensation complex to X-linked target genes. Genes Dev 21: 2030-2040.
22. Bai X, Alekseyenko AA, Kuroda MI (2004) Sequence-specific targeting of MSL complex regulates transcription of the roX RNA genes. EMBO J 23: 2853-61.
23. Avila FW, Erickson JW (2007) Drosophila JAK/STAT pathway reveals distinct initiation and reinforcement steps in early transcription of Sxl. Curr Biol 17: 643-648.
24. Li F, Schiemann AH, Scott MJ (2008) Incorporation of the noncoding roX RNAs alters the chromatin-binding specificity of the Drosophila MSL1/MSL2 complex. Mol Cell Biol 28: 1252-64.
25. Erickson JW, Cline TW (1993) A bZIP protein, sisterless-a, collaborates with bHLH transcription factors early in Drosophila development to determine sex. Genes Dev 7: 1688-1702.
26. ten Bosch JR, Benavides JA, Cline TW (2006) The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development 133: 1967-1977.
27. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF (2007) Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 5: e117. doi:10.1371/journal.pbio.0050117. Erratum in: PLoS Biol 8:e213.doi:10.1371/journal.pbio.0050213.
28. Rastelli L, Richman R, Kuroda MI (1995) The dosage compensation regulators MLE, MSL-1 and MSL-2 are interdependent since early embryogenesis in Drosophila. Mech Dev 53: 223-33.
29. Franke A, Dernburg A, Bashaw GJ, Baker BS (1996) Evidence that MSLmediated dosage compensation in Drosophila begins at blastoderm. Development 122: 2751-60.
30. McDowell KA, Hilfiker A, Lucchesi JC (1996) Dosage compensation in Drosophila: the X chromosome binding of MSL-1 and MSL-2 in female embryos is prevented by the early expression of the Sxl gene. Mech Dev 57: 113-9.
31. Alekseyenko AA, Larschan E, Lai WR, Park PJ, Kuroda MI (2006) Highresolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome. Genes Dev 20: 848-857.
32. Cline T (1984) Autoregulatory functioning of a Drosophila gene product that establishes and maintains the sexually determined state. Genetics 107: 231-277.
33. Gergen JP (1987) Dosage Compensation in Drosophila: Evidence That daughterless and Sex-lethal Control X Chromosome Activity at the Blastoderm Stage of Embryogenesis. Genetics 117: 477-485.
34. Smith ER, Allis CD, Lucchesi JC (2001) Linking global histone acetylation to the transcription enhancement of X-chromosomal genes in Drosophila males. J Biol Chem 276: 31483-31486.
35. Alekseyenko AA, Peng S, Larschan E, Gorchakov AA, Lee O, et al. (2008) A Sequence Motif within Chromatin Entry Sites Directs MSL Establishment on the Drosophila X Chromosome. Cell 134: 599-609.
36. Straub T, Grimaud C, Gilfillan GD, Mitterweger A, Becker PB (2008) The Chromosomal High-Affinity Binding Sites for the Drosophila Dosage Compensation Complex. PLoS Genetics 4: e1000302. doi:10.1371/journal. pgen.1000302.
37. Younger-Shepherd S, Vaessin H, Bier E, Jan LY, Jan YN (1992) deadpan, an essential pan-neural gene encoding an HLH protein, acts as a denominator in Drosophila sex determination. Cell 70: 911-922.
38. Barbash DA, Cline TW (1995) Genetic and molecular analysis of the autosomal component of the primary sex determination signal of Drosophila melanogaster. Genetics 141: 1451-71.
39. Aronson BD, Fisher AL, Blechman K, Caudy M, Gergen JP (1997) Grouchodependent and -independent repression activities of Runt domain proteins. Mol Cell Biol 17: 5581-7.
40. Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, et al. (2003) A protein interaction map of Drosophila melanogaster. Science 302: 1727-36.
41. Kramer SG, Jinks TM, Schedl P, Gergen JP (1999) Direct activation of Sexlethal transcription by the Drosophila runt protein. Development 126: 191-200.
42. Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, et al. (2006) Global analysis of X-chromosome dosage compensation. J Biol 5: 3.
43. Nguyen DK, Disteche CM (2006) Dosage compensation of the active X chromosome in mammals. Nat.Genet 38: 47-53.
44. Lin H, Gupta V, Vermilyea MD, Falciani F, Lee JT, et al. (2007) Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biol 5: e326. doi:10.1371/journal.pbio.0050326.
45. Walthall SL, Moses M, Horabin JI (2007) A large complex containing both Patched and Smoothened initiates Hedgehog signaling in Drosophila. J Cell Science 120: 826-837.
46. Mendjan S, Taipale M, Kind J, Holz H, Gebhardt P, et al. (2006) Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol Cell 21: 811-23.