Chromatin reader L(3)mbt requires the Myb-MuvB/DREAM transcriptional regulatory complex for chromosomal recruitment

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 40, 2014, Pages E4234-E4243

  Blanchard, Daniel P ^a   Georlette, Daphne ^a,c   Antoszewski, Lisa ^b   Botchan, Michael R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CANISIUS COLLEGE   (United States)

^c Meso Scale Discovery   (United States)

Author keywords

Bar coding; Epigenetics; Tumorigenesis

Indexed keywords

CALSENILIN; CORE PROTEIN; DNA; MIP130 PROTEIN; PROTEIN MUVB; PROTEIN MYB; REGULATOR PROTEIN; TRANSCRIPTION FACTOR E2F2; UNCLASSIFIED DRUG; CARRIER PROTEIN; CASPASE; CELL CYCLE PROTEIN; CHROMATIN; DREAM PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; E2F2 PROTEIN, DROSOPHILA; HISTONE; L(3)MBT PROTEIN, DROSOPHILA; MIP120 PROTEIN, DROSOPHILA; MIP130 PROTEIN, DROSOPHILA; MULTIPROTEIN COMPLEX; MYB PROTEIN, DROSOPHILA; PHOTOPROTEIN; PROTEIN C MYB; TRANSCRIPTION FACTOR;

BRAIN; CELLULAR DISTRIBUTION; CHROMATIN; CONFERENCE PAPER; CONTROLLED STUDY; DNA BINDING; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; HISTONE MODIFICATION; LARVA; NONHUMAN; POLYTENE CHROMOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATOR GENE; SALIVARY GLAND; TRANSPOSON; ANIMAL; CELL LINE; CONFOCAL MICROSCOPY; CYTOLOGY; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; INSECT CHROMOSOME; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARRIER PROTEINS; CASPASES; CELL CYCLE PROTEINS; CELL LINE; CHROMATIN; CHROMOSOMES, INSECT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; E2F2 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; HISTONES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MULTIPROTEIN COMPLEXES; PROTO-ONCOGENE PROTEINS C-MYB; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALIVARY GLANDS; TRANSCRIPTION FACTORS;

EID: 84949024074     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416321111     Document Type: Article

References (48)

1. Gateff E, Löffler T, Wismar J. (1993) A temperature-sensitive brain tumor suppressor mutation of Drosophila melanogaster: Developmental studies and molecular localization of the gene. Mech Dev 41(1):15-31.
2. Wismar J, et al (1995) The Drosophila melanogaster tumor suppressor gene lethal(3) malignant brain tumor encodes a proline-rich protein with a novel zinc finger. Mech Dev 53(1):141-154.
3. MacGrogan D, et al (2004) Structural integrity and expression of the L3MBTL gene in normal and malignant hematopoietic cells. Genes Chromosomes Cancer 41(3):203-213.
4. Gurvich N, et al (2010) L3MBTL1 polycomb protein, a candidate tumor suppressor in del(20q12) myeloid disorders, is essential for genome stability. Proc Natl Acad Sci USA 107(52):22552-22557.
5. Feichtinger J, Larcombe L, McFarlane R.J. (2014) Meta-analysis of expression of 1(3)mbt tumor-associated germline genes supports the model that a soma-to-germline transition is a hallmark of human cancers. Int J Cancer 134(10):2359-65.
6. Bonasio R, Lecona E, Reinberg D. (2010) MBT domain proteins in development and disease. Semin Cell Dev Biol 21(2):221-230.
7. Bornemann D, Miller E, Simon J. (1996) The Drosophila Polycomb group gene Sex comb on midleg (Scm) encodes a zinc finger protein with similarity to polyhomeotic protein. Development 122(5):1621-1630.
8. Klymenko T, et al (2006) A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev 20(9): 1110-1122.
9. Peterson AJ, et al (1997) A domain shared by the Polycomb group proteins Scm and ph mediates heterotypic and homotypic interactions. Mol Cell Biol 17(11):6683-6692.
10. Georlette D, et al (2007) Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. Genes Dev 21(22):2880-2896.
11. Janic A, Mendizabal L, Llamazares S., Rossell D, Gonzalez C. (2010) Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila. Science 330 (6012):1824-1827.
12. Meier K, et al (2012) LINT, a novel dL(3)mbt-containing complex, represses malignant brain tumour signature genes. PLoS Genet 8(5):e1002676.
13. Lewis PW, et al (2004) Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev 18(23):2929-2940.
14. Trojer P, et al (2007) L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129(5):915-928.
15. Li H, et al (2007) Structural basis for lower lysine methylation state-specific readout by MBT repeats of L3MBTL1 and an engineered PHD finger. Mol Cell 28(4):677-691.
16. Min J, et al (2007) L3MBTL1 recognition of mono- and dimethylated histones. Nat Struct Mol Biol 14(12):1229-1230.
17. Kalakonda N, et al (2008) Histone H4 lysine 20 monomethylation promotes transcriptional repression by L3MBTL1. Oncogene 27(31):4293-4304.
18. Maurer-Stroh S., et al (2003) The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem Sci 28(2):69-74.
19. Adams-Cioaba M.A., Min J. (2009) Structure and function of histone methylation binding proteins. Biochem Cell Biol 87(1):93-105.
20. Kim J, et al (2006) Tudor, MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep 7(4):397-403.
21. Grimm C, et al (2007) Structural and functional analyses of methyl-lysine binding by the malignant brain tumour repeat protein Sex comb on midleg. EMBO Rep 8(11): 1031-1037.
22. Wang WK, et al (2003) Malignant brain tumor repeats: A three-leaved propeller architecture with ligand/peptide binding pockets. Structure 11(7):775-789.
23. Richter C, Oktaba K, Steinmann J., Müller J, Knoblich J.A. (2011) The tumour suppressor L(3)mbt inhibits neuroepithelial proliferation and acts on insulator elements. Nat Cell Biol 13(9):1029-1039.
24. Sakaguchi A, Joyce E, Aoki T., Schedl P, Steward R. (2012) The histone H4 lysine 20 monomethyl mark, set by PR-Set7 and stabilized by L(3)mbt, is necessary for proper interphase chromatin organization. PLoS ONE 7(9):e45321.
25. Beall EL, et al (2002) Role for a Drosophila Myb-containing protein complex in sitespecific DNA replication. Nature 420 (6917):833-837.
26. Korenjak M, et al (2004) Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 119(2): 181-193.
27. Dimova DK, Stevaux O, Frolov M.V., Dyson N.J. (2003) Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway. Genes Dev 17(18):2308-2320.
28. Schmit F, et al (2007) LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6(15):1903-1913.
29. Harrison MM, Ceol CJ, Lu X, Horvitz H.R. (2006) Some C. elegans class B synthetic multivulva proteins encode a conserved LIN-35 Rb-containing complex distinct from a NuRD-like complex. Proc Natl Acad Sci USA 103(45):16782-16787.
30. Litovchick L, et al (2007) Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol Cell 26(4):539-551.
31. Roy S, et al; modENCODE Consortium (2010) Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330 (6012):1787-1797.
32. Yohn CB, Pusateri L, Barbosa V., Lehmann R. (2003) 1(3)malignant brain tumor and three novel genes are required for Drosophila germ-cell formation. Genetics 165(4): 1889-1900.
33. Nishioka K, et al (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell 9(6): 1201-1213.
34. Zhimulev IF (1999) Genetic organization of polytene chromosomes. Adv Genet 39: 1-589.
35. Rizzo MA, Springer GH, Granada B, Piston D.W. (2004) An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 22(4):445-449.
36. Shaner NC, et al (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22(12): 1567-1572.
37. Dyson N (1998) The regulation of E2F by pRB-family proteins. Genes Dev 12(15): 2245-2262.
38. Wen H, Andrejka L, Ashton J., Karess R, Lipsick J.S. (2008) Epigenetic regulation of gene expression by Drosophila Myb and E2F2-RBF via the Myb-MuvB/dREAM complex. Genes Dev 22(5):601-614.
39. Fisher WW, et al (2012) DNA regions bound at low occupancy by transcription factors do not drive patterned reporter gene expression in Drosophila. Proc Natl Acad Sci USA 109(52):21330-21335.
40. Schmit F, Cremer S, Gaubatz S. (2009) LIN54 is an essential core subunit of the DREAM/ LINC complex that binds to the cdc2 promoter in a sequence-specific manner. FEBS J 276(19):5703-5716.
41. Beall EL, et al (2007) Discovery of tMAC: A Drosophila testis-specific meiotic arrest complex paralogous to Myb-Muv B. Genes Dev 21(8):904-919.
42. Casso D, Ramírez-Weber FA, Kornberg TB (1999) GFP-tagged balancer chromosomes for Drosophila melanogaster. Mech Dev 88(2):229-232.
43. Le Thomas A., et al (2013) Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 27(4):390-399.
44. Beall EL, Bell M, Georlette D., Botchan M.R. (2004) Dm-myb mutant lethality in Drosophila is dependent upon mip130: Positive and negative regulation of DNA replication. Genes Dev 18(14):1667-1680.
45. Cox DN, Chao A, Lin H. (2000) piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127(3): 503-514.
46. Saito K, et al (2010) Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev 24(22):2493-2498.
47. Brandt T, Corces V.G. (2008) The Lawc protein is required for proper transcription by RNA polymerase II in Drosophila. Mol Genet Genomics 280(5):385-396.
48. Kharchenko PV, et al (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471 (7339):480-485.