Cooperative and antagonistic contributions of two heterochromatin proteins to transcriptional regulation of the drosophila sex determination decision

PLoS Genetics

Volumn 7, Issue 6, 2011, Pages

  Li, Hui ^a   Rodriguez, Janel ^b   Yoo, Youngdong ^a   Shareef, Momin Mohammed ^a   Badugu, RamaKrishna ^a   Horabin, Jamila I ^b   Kellum, Rebecca ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1 ORIGIN RECOGNITION COMPLEX ASSOCIATED PROTEIN; NUCLEAR PROTEIN; RNA POLYMERASE II; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HETEROCHROMATIN PROTEIN 1, DROSOPHILA; HP1 ORC ASSOCIATED PROTEIN, DROSOPHILA; HP1 ORC-ASSOCIATED PROTEIN, DROSOPHILA; NONHISTONE PROTEIN; RNA BINDING PROTEIN; SXL PROTEIN, DROSOPHILA;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; FEMALE; GENE; GENE ACTIVATION; GENE SEQUENCE; MALE; MUTANT; NONHUMAN; PROMOTER REGION; PROTEIN FUNCTION; RNA SPLICING; SEX DETERMINATION PROCESS; SXL GENE; TRANSCRIPTION REGULATION; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HETEROCHROMATIN; METABOLISM; PHYSIOLOGY;

EUKARYOTA;

ANIMALS; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL PROTEINS, NON-HISTONE; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HETEROCHROMATIN; MALE; RNA-BINDING PROTEINS; SEX DETERMINATION PROCESSES; TRANSCRIPTION, GENETIC;

EID: 79959855171     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002122     Document Type: Article

References (63)

1. Heitz E, (1928) Das Heterochromatin der Moose. Jahrb Wissensch Bot 69: 762-818.
2. James TC, Elgin SC, (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6: 3862-3872.
3. Wreggett KA, Hill F, James PS, Hutchings A, Butcher GW, et al. (1994) A mammalian homologue of Drosophila heterochromatin protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet Cell Genet 66: 99-103.
4. Allshire RC, Nimmo ER, Ekwall K, Javerzat JP, Cranston G, (1995) Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes Dev 9: 218-233.
5. Nielsen SJ, Schneider R, Bauer UM, Bannister AJ, Morrison A, et al. (2001) Rb targets histone H3 methylation and HP1 to promoters. Nature 412: 561-565.
6. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T, (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120.
7. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, et al. (2002) Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. Embo J 21: 1121-1131.
8. Nielsen AL, Oulad-Abdelghani M, Ortiz JA, Remboutsika E, Chambon P, et al. (2001) Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. Mol Cell 7: 729-739.
9. Ekwall K, Ruusala T, (1994) Mutations in rik1, clr2, clr3 and clr4 genes asymmetrically derepress the silent mating-type loci in fission yeast. Genetics 136: 53-64.
10. Hwang KK, Eissenberg JC, Worman HJ, (2001) Transcriptional repression of euchromatic genes by Drosophila heterochromatin protein 1 and histone modifiers. Proc Natl Acad Sci U S A 98: 11423-11427.
11. Cryderman DE, Grade SK, Li Y, Fanti L, Pimpinelli S, et al. (2005) Role of Drosophila HP1 in euchromatic gene expression. Dev Dyn 232: 767-774.
12. Fanti L, Berloco M, Piacentini L, Pimpinelli S, (2003) Chromosomal distribution of heterochromatin protein 1 (HP1) in Drosophila: a cytological map of euchromatic HP1 binding sites. Genetica 117: 135-147.
13. Vakoc CR, Mandat SA, Olenchock BA, Blobel GA, (2005) Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell 19: 381-391.
14. Pak DT, Pflumm M, Chesnokov I, Huang DW, Kellum R, et al. (1997) Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91: 311-323.
15. Huang DW, Fanti L, Pak DT, Botchan MR, Pimpinelli S, et al. (1998) Distinct cytoplasmic and nuclear fractions of Drosophila heterochromatin protein 1: their phosphorylation levels and associations with origin recognition complex proteins. J Cell Biol 142: 307-318.
16. Shareef MM, King C, Damaj M, Badagu R, Huang DW, et al. (2001) Drosophila heterochromatin protein 1 (HP1)/origin recognition complex (ORC) protein is associated with HP1 and ORC and functions in heterochromatin-induced silencing. Mol Biol Cell 12: 1671-1685.
17. Reinhart BJ, Bartel DP, (2002) Small RNAs correspond to centromere heterochromatic repeats. Science 297: 1831.
18. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, et al. (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837.
19. Haynes KA, Caudy AA, Collins L, Elgin SC, (2006) Element 1360 and RNAi components contribute to HP1-dependent silencing of a pericentric reporter. Curr Biol 16: 2222-2227.
20. Riddle NC, Leung W, Haynes KA, Granok H, Wuller J, et al. (2008) An investigation of heterochromatin domains on the fourth chromosome of Drosophila melanogaster. Genetics 178: 1177-1191.
21. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, et al. (2002) Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237.
22. Ryan RF, Schultz DC, Ayyanathan K, Singh PB, Friedman JR, et al. (1999) KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Kruppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol Cell Biol 19: 4366-4378.
23. Aguilar-Arnal L, Marsellach FX, Azorin F, (2008) The fission yeast homologue of CENP-B, Abp1, regulates directionality of mating-type switching. Embo J 27: 1029-1038.
24. Nakagawa H, Lee JK, Hurwitz J, Allshire RC, Nakayama J, et al. (2002) Fission yeast CENP-B homologs nucleate centromeric heterochromatin by promoting heterochromatin-specific histone tail modifications. Genes Dev 16: 1766-1778.
25. Petrie VJ, Wuitschick JD, Givens CD, Kosinski AM, Partridge JF, (2005) RNA interference (RNAi)-dependent and RNAi-independent association of the Chp1 chromodomain protein with distinct heterochromatic loci in fission yeast. Mol Cell Biol 25: 2331-2346.
26. Peng H, Ivanov AV, Oh HJ, Lau YF, Rauscher FJ 3rd, (2009) Epigenetic gene silencing by the SRY protein is mediated by a KRAB-O protein that recruits the KAP1 co-repressor machinery. J Biol Chem 284: 35670-35680.
27. Cenci G, Siriaco G, Raffa GD, Kellum R, Gatti M, (2003) The Drosophila HOAP protein is required for telomere capping. Nat Cell Biol 5: 82-84.
28. Bi X, Srikanta D, Fanti L, Pimpinelli S, Badugu R, et al. (2005) Drosophila ATM and ATR checkpoint kinases control partially redundant pathways for telomere maintenance. Proc Natl Acad Sci U S A 102: 15167-15172.
29. Gao G, Walser JC, Beaucher ML, Morciano P, Wesolowska N, et al. (2010) HipHop interacts with HOAP and HP1 to protect Drosophila telomeres in a sequence-independent manner. Embo J 29: 819-829.
30. Badugu R, Shareef MM, Kellum R, (2003) Novel Drosophila heterochromatin protein 1 (HP1)/origin recognition complex-associated protein (HOAP) repeat motif in HP1/HOAP interactions and chromocenter associations. J Biol Chem 278: 34491-34498.
31. Cline TW, (1986) A female-specific lethal lesion in an X-linked positive regulator of the Drosophila sex determination gene, Sex-lethal. Genetics 113: 641-663.
32. Keyes LN, Cline TW, Schedl P, (1992) The primary sex determination signal of Drosophila acts at the level of transcription. Cell 68: 933-943.
33. Estes PA, Keyes LN, Schedl P, (1995) Multiple response elements in the Sex-lethal early promoter ensure its female-specific expression pattern. Mol Cell Biol 15: 904-917.
34. Salz HK, Erickson JW, (2010) Sex determination in Drosophila: The view from the top. Fly (Austin) pp. 4.
35. Andrews J, Bouffard GG, Cheadle C, Lu J, Becker KG, et al. (2000) Gene discovery using computational and microarray analysis of transcription in the Drosophila melanogaster testis. Genome Res 10: 2030-2043.
36. Stapleton M, Carlson J, Brokstein P, Yu C, Champe M, et al. (2002) A Drosophila full-length cDNA resource. Genome Biol 3: RESEARCH0080.
37. Stapleton M, Liao G, Brokstein P, Hong L, Carninci P, et al. (2002) The Drosophila gene collection: identification of putative full-length cDNAs for 70% of D. melanogaster genes. Genome Res 12: 1294-1300.
38. Chintapalli VR, Wang J, Dow JA, (2007) Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39: 715-720.
39. Parisi M, Nuttall R, Edwards P, Minor J, Naiman D, et al. (2004) A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol 5: R40.
40. Boutanaev AM, Kalmykova AI, Shevelyov YY, Nurminsky DI, (2002) Large clusters of co-expressed genes in the Drosophila genome. Nature 420: 666-669.
41. Liu LP, Ni JQ, Shi YD, Oakeley EJ, Sun FL, (2005) Sex-specific role of Drosophila melanogaster HP1 in regulating chromatin structure and gene transcription. Nat Genet 37: 1361-1366.
42. Dimitri P, Pisano C, (1989) Position effect variegation in Drosophila melanogaster: relationship between suppression effect and the amount of Y chromosome. Genetics 122: 793-800.
43. Spofford JB, eds. (1976) Position-effect variegation in Drosophila London Academic Press pp. 955-1018.
44. Lucchesi JC, Kelly WG, Panning B, (2005) Chromatin remodeling in dosage compensation. Annu Rev Genet 39: 615-651.
45. Lyon MF, (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190: 372-373.
46. Lucchesi JC, (2009) The structure-function link of compensated chromatin in Drosophila. Curr Opin Genet Dev 19: 550-556.
47. Spierer A, Begeot F, Spierer P, Delattre M, (2008) SU(VAR)3-7 links heterochromatin and dosage compensation in Drosophila. PLoS Genet 4: e1000066 doi:10.1371/journal.pgen.1000066.
48. Demakova OV, Kotlikova IV, Gordadze PR, Alekseyenko AA, Kuroda MI, et al. (2003) The MSL complex levels are critical for its correct targeting to the chromosomes in Drosophila melanogaster. Chromosoma 112: 103-115.
49. Lu H, Kozhina E, Mahadevaraju S, Yang D, Avila FW, et al. (2008) Maternal Groucho and bHLH repressors amplify the dose-sensitive X chromosome signal in Drosophila sex determination. Dev Biol 323: 248-260.
50. Badugu R, Yoo Y, Singh PB, Kellum R, (2005) Mutations in the heterochromatin protein 1 (HP1) hinge domain affect HP1 protein interactions and chromosomal distribution. Chromosoma 113: 370-384.
51. Shimada A, Dohke K, Sadaie M, Shinmyozu K, Nakayama J, et al. (2009) Phosphorylation of Swi6/HP1 regulates transcriptional gene silencing at heterochromatin. Genes Dev 23: 18-23.
52. Lin CH, Li B, Swanson S, Zhang Y, Florens L, et al. (2008) Heterochromatin protein 1a stimulates histone H3 lysine 36 demethylation by the Drosophila KDM4A demethylase. Mol Cell 32: 696-706.
53. Piacentini L, Fanti L, Negri R, Del Vescovo V, Fatica A, et al. (2009) Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila. PLoS Genet 5: e1000670 doi:10.1371/journal.pgen.1000670.
54. Zofall M, Grewal SI, (2006) Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol Cell 22: 681-692.
55. Zeitlinger J, Stark A, Kellis M, Hong JW, Nechaev S, et al. (2007) RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 39: 1512-1516.
56. Kornblihtt AR, (2006) Chromatin, transcript elongation and alternative splicing. Nat Struct Mol Biol 13: 5-7.
57. Deshpande G, Calhoun G, Jinks TM, Polydorides AD, Schedl P, (2005) Nanos downregulates transcription and modulates CTD phosphorylation in the soma of early Drosophila embryos. Mech Dev 122: 645-657.
58. Sprinthall RC, (2003) Basic Statistical Analysis, Seventh Edition: Pearson Education Group.
59. 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.
60. Alekseyenko AA, Larschan E, Lai WR, Park PJ, Kuroda MI, (2006) High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome. Genes Dev 20: 848-857.
61. Shareef MM, Badugu R, Kellum R, (2003) HP1/ORC complex and heterochromatin assembly. Genetica 117: 127-134.
62. Gladstein N, McKeon MN, Horabin JI, (2010) Requirement of male-specific dosage compensation in Drosophila females-implications of early X chromosome gene expression. PLoS Genet 6: e1001041 doi:10.1371/journal.pgen.1001041.
63. Jinks TM, Calhoun G, Schedl P, (2003) Functional conservation of the sex-lethal sex determining promoter, Sxl-Pe, in Drosophila virilis. Dev Genes Evol 213: 155-165.