Non-genic transcription at the Drosophila bithorax complex - Functional activity of the dark matter of the genome

International Journal of Developmental Biology

Volumn 53, Issue 4, 2009, Pages 459-468

  Ho, Margaret C W ^a   Schiller, Benjamin J ^a   Goetz, Sara E ^a   Drewell, Robert A ^a  

^a HARVEY MUDD COLLEGE   (United States)

Author keywords

Bithorax; Chromatin; cis regulation; RNA; Transcription

Indexed keywords

DROSOPHILA PROTEIN; HOX PROTEIN; POLYCOMB GROUP PROTEIN; POLYCOMB PROTEIN, DROSOPHILA;

CHROMATIN STRUCTURE; DNA SEQUENCE; DROSOPHILA; EMBRYO PATTERN FORMATION; GENE EXPRESSION; GENE FUNCTION; GENE SEQUENCE; GENE SILENCING; GENETIC REGULATION; GENETIC TRANSCRIPTION; INSECT DEVELOPMENT; INSECT GENOME; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; ANIMAL; CHROMATIN; GENE EXPRESSION REGULATION; GENETICS; GENOME; HUMAN; METABOLISM;

DROSOPHILA MELANOGASTER;

ANIMALS; CHROMATIN; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HUMANS; TRANSCRIPTION, GENETIC;

EID: 68849129191     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.082647mh     Document Type: Review

References (87)

1. ADYHA, S. and GOTTESMAN, M. (1982). Promoter occlusion: transcription through a promoter may inhibit its activity. Cell 29: 939-944.
2. AKBARI, O.S., BAE, E., JOHNSEN, H., VILLALUZ, A., WONG, D. and DREWELL, R.A. (2008). A novel promoter-tethering element regulates enhancer-driven gene expression at the bithorax complex in the Drosophila embryo. Development 135: 123-131.
3. AKBARI, O.S., BOUSUM, A., BAE, E. and DREWELL, R.A. (2006). Unraveling cis-regulatory mechanisms at the abdominal-A and Abdominal-B genes in the Drosophila bithorax complex. Dev. Biol. 293: 294-304.
4. AKBARI, O.S., SCHILLER, B.J., GOETZ, S.G., HO, M.C.W., BAE, E. and DREWELL, R.A. (2007). The Abdominal-B promoter tethering element mediates promoter-enhancer specificity at the Drosophila bithorax complex. Fly 1: 337-339.
5. ARAVIN, A.A., KLENOV, M.S., VAGIN, V.V., BANTIGNIES, F., CAVALLI, G. and GVOZDEV, V.A. (2004). Dissection of a natural RNA silencing process in the Drosophila melanogaster germ line. Mol. Cell. Biol. 24: 6742-6750.
6. ARAVIN, A.A., LAGOS-QUINTANA, M., YALCIN, A., ZAVOLAN, M., MARKS, D., SNYDER, B., GAASTERLAND, T., MEYER, J. and TUSCHL, T. (2003). The Small RNA Profile during Drosophila melanogaster Development. Developmental Cell 5: 337-350.
7. BAE, E., CALHOUN, V.C., LEVINE, M., LEWIS, E.B. and DREWELL, R.A. (2002). Characterization of the intergenic RNA profile at abdominal-A and Abdominal-B in the Drosophila bithorax complex. Proc. Natl. Acad. Sci. USA 99: 16847-16852.
8. BANTIGNIES, F. and CAVALLI, G. (2006). Cellular memory and dynamic regulation of polycomb group proteins. Curr Opin Cell Biol. 18: 275-283.
9. BANTIGNIES, F., GRIMAUD, C., LAVROV, S., GABUT, M. and CAVALLI, G. (2003). Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev. 17: 2406-2420.
10. BENDER, W. (2008). MicroRNAs in the Drosophila bithorax complex. Genes Dev. 22: 14-19.
11. BENDER, W. and FITZGERALD, D.P. (2002). Transcription activates repressed domains in the Drosophila bithorax complex. Development 129: 4923-4930.
12. BERNSTEIN, E., CAUDY, A.A., HAMMOND, S.M. and HANNON, G.J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366.
13. BEUCHLE, D., STRUHL, G. and MULLER, J. (2001). Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development 128: 993-1004.
14. BLASTYÁK, A., MISHRA, R.K., KARCH, F. and GYURKOVICS, H. (2006). Efficient and specific targeting of Polycomb group proteins requires cooperative interaction between Grainyhead and Pleiohomeotic. Mol. Cell. Biol. 26: 1344-1344.
15. BREILING, A., O'NEILL, L.P., D'ELISEO, D., TURNER, B.M. and ORLANDO, V. (2004). Epigenome changes in active and inactive polycomb-group-controlled regions. EMBO Reports 5: 976-982.
16. BRENNECKE, J., ARAVIN, A.A., STARK, A., DUS, M., KELLIS, M., SACHIDANANDAM, R. and HANNON, G.J. (2007). Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
17. BROWN, J.L., MUCCI, D., WHITELEY, M., DIRKSEN, M.L. and KASSIS, J.A. (1998). The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1. Mol. Cell. 1: 1057-1064.
18. BUSTURIA, A. and BIENZ, M. (1993). Silencers in abdominal-B, a homeotic Drosophila gene. The EMBO J. 12: 1415-1425.
19. BUSTURIA, A. and MORATA, G. (1988). Ectopic expression of homeotic genes caused by the elimination of the Polycomb gene in Drosophila imaginal epidermis. Development 104: 713-720.
20. CALLEN, B.P., SHEARWIN, K.E. and EGAN, J.B. (2004). Transcriptional interference between convergent promoters caused by elongation over the promoter. Mol. Cell 14: 647-656.
21. CAO, R. and ZHANG, Y. (2004). The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 14: 155-164.
22. CARMELL, M.A., XUAN, Z., ZHANG, M.Q. and HANNON, G.J. (2002). The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16: 2733-2742.
23. CASARES, F. and SANCHEZ-HERRERO, E. (1995). Regulation of the infraabdominal regions of the bithorax complex of Drosophila by gap genes. Development 121: 1855-1866.
24. CELNIKER, S. and DREWELL, R.A. (2007). Chromatin looping mediates boundary element promoter interactions. BioEssays 29: 7-10.
25. CLEARD, F., MOSHKIN, Y., KARCH, F. and MAEDA, R.K. (2006). Probing long-distance regulatory interactions in the Drosophila melanogaster bithorax complex using Dam identification. Nature Genetics 38: 931-935.
26. COOK, P.R. (2003). Nongenic transcription, gene regulation and action at a distance. J Cell Sci 116: 4483-4491.
27. CUMBERLEDGE, S., ZARATZIAN, A. and SAKONJU, S. (1990). Characterization of two RNAs transcribed from the cis-regulatory region of the abd-A domain within the Drosophila bithorax complex. Proc. Natl. Acad. Sci. USA 87: 3259-3263.
28. CZERMIN, B., MELFI, R., MCCABE, D., SEITZ, V., IMHOF, A. and PIRROTTA, V. (2002). Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196.
29. DREWELL, R.A., BAE, E., BURR, J. and LEWIS, E.B. (2002). Transcription defines the embryonic domains of cis-regulatory activity at the Drosophila bithorax complex. Proc. Natl. Acad. Sci. USA 99: 16853-16858.
30. FRITSCH, C., BROWN, J.L., KASSIS, J.A. and MÜLLER, J. (1999). The DNA-binding polycomb group protein pleiohomeotic mediates silencing of a Drosophila homeotic gene. Development 126: 3905-3913.
31. GRIMAUD, C., BANTIGNIES, F., PAL-BHADRA, M., GHANA, P., BHADRA, U. and CAVALLI, G. (2006). RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 10: 957-971.
32. GUNAWARDANE, L.S., SAITO, K., NISHIDA, K.M., MIYOSHI, K., KAWAMURA, Y., NAGAMI, T., SIOMI, H. and SIOMI, M.C. (2007). A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 315: 1587-1590.
33. HAMMOND, S.M. (2005). Dicing and slicing: the core machinery of the RNA interference pathway. FEBS Lett 579: 5822-5829.
34. HAMMOND, S.M., BERNSTEIN, E., BEACH, D. and HANNON, G.J. (2000). An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404: 293-296.
35. HARRIS, A.N. and MACDONALD, P.M. (2001). Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128: 2823-2832.
36. HARTIG, J.V., TOMARI, Y. and FORSTEMANN, K. (2007). piRNAs the ancient hunters of genome invaders. Genes Dev. 21: 1707-1713.
37. HOGNESS, D.S., LIPSHITZ, H.D., BEACHY, P.A., PEATTIE, D.A., SAINT, R.B., GOLDSCHMIDT-CLERMONT, M., HARTE, P.J., GAVIS, E.R. and HELFAND, S.L. (1985). Regulation and products of the Ubx domain of the bithorax complex. CSH Symp Quant. Biol. 50: 181-194.
38. HUTVAGNER, G., MCLACHLAN, J., PASQUINELLI, A.E., BALINT, E., TUSCHL, T. and ZAMORE, P.D. (2001). A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293: 834-838.
39. HUTVAGNER, G. and SIMARD, M.J. (2008). Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol. 9: 22-32.
40. JACKSON, R.J. and STANDART, N. (2007). How do microRNAs regulate gene expression? Sci STKE 367: re1.
41. KARCH, F., WEIFFENBACH, B., PEIFER, M., BENDER, W., DUNCAN, I., CELNIKER, S., CROSBY, M. and LEWIS, E.B. (1985). The abdominal region of the bithorax complex. Cell 43: 81-96.
42. KIM, V.N. (2005). MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol. 6: 376-385.
43. KLYMENKO, T. and MULLER, J. (2004). The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins. EMBO Reports 5: 373-377.
44. KUZMICHEV, A., NISHIOKA, K., ERDJUMENT-BROMAGE, H., TEMPST, P. and REINBERG, D. (2002). Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16: 2893-2905.
45. LANZUOLO, C., ROURE, V., DEKKER, J., BANTIGNIES, F. and ORLANDO, V. (2007). Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Natute Cell Biology 9: 1167-1174.
46. LEE, Y.S., AHN, C., HAN, J., CHOI, H., KIM, J., YIM, J., LEE, J., PROVOST, P., RADMARK, O., KIM, S. et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425: 415-419.
47. LEE, Y.S., NAKAHARA, K., PHAM, J.W., KIM, K., HE, Z., SONTHEIMER, E.J. and CARTHEW, R.W. (2004). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117: 69-81.
48. LEI, E.P. and CORCES, V.G. (2006). A long-distance relationship between RNAi and Polycomb. Cell 124: 886-888.
49. LEI, E.P. and CORCES, V.G. (2006). RNA interference machinery influences the nuclear organization of a chromatin insulator. Nature Genetics 38: 936-941.
50. LEMONS, D. and MCGINNIS, W. (2006). Genomic evolution of Hox gene clusters. Science 313: 1918-1922.
51. LEMPRADL, A. and RINGROSE, L. (2008). How does noncoding transcription regulate Hox genes? BioEssays 30: 110-121.
52. LEVINE, S.S., KING, I.F. and KINGSTON, R.E. (2004). Division of labor in polycomb group repression. Trends Biochem. Sci. 29: 478-485.
53. LEWIS, E.B. (1954). The Theory and Application of a New Method of Detecting Chromosomal Rearrangements in Drosophila melanogaster. American Naturalist 88: 225-239.
54. LEWIS, E.B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
55. LEWIS, E.B., PFEIFFER, B.D., MATHOG, D.R. and CELNIKER, S.E. (2003). Evolution of the homeobox complex in the Diptera. Curr. Biol. 13: R587-R588.
56. LIPSHITZ, H.D., PEATTIE, D.A. and HOGNESS, D.S. (1987). Novel transcripts from the Ultrabithorax domain of the bithorax complex. Genes Dev. 1: 307-322.
57. LIU, Q., RAND, T.A., KALIDAS, S., DU, F., KIM, H.E., SMITH, D.P. and WANG, X. (2003). R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301: 1921-1925.
58. MAEDA, R.K. and KARCH, F. (2006). The ABC of the BX-C: the bithorax complex explained. Development 133: 1413-1422.
59. MARTIN, C.H., MAYEDA, C.A., DAVIS, C.A., ERICSSON, C.L., KNAFELS, J.D., MATHOG, D.R., CELNIKER, S.E., LEWIS, E.B. and PALAZZOLO, M.J. (1995). Complete sequence of the bithorax complex of Drosophila. Proc. Natl. Acad. Sci. USA 92: 8398-8402.
60. MAZO, A., HODGSON, J.W., PETRUK, S., SEDKOV, Y. and BROCK, H.W. (2007). Transcriptional interference: an unexpected layer of complexity in gene regulation. J. Cell Sci. 120: 2755-2761.
61. MOHD-SARIP, A., CLEARD, F., MISHRA, R.K., KARCH, F. and VERRIJZER, C.P. (2005). Synergistic recognition of an epigenetic DNA element by Pleiohomeotic and a Polycomb core complex. Genes Dev. 19: 1755-1760.
62. MULLER, J. and BIENZ, M. (1991). Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo. EMBO J. 10: 3147-3155.
63. MULLER, J. and BIENZ, M. (1992). Sharp anterior boundary of homeotic gene expression conferred by the fushi tarazu protein. EMBO J 11: 3653-3661.
64. MULLER, J., HART, C.M., FRANCIS, N.J., VARGAS, M.L., SENGUPTA, A., WILD, B., MILLER, E.L., O'CONNOR, M.B., KINGSTON, R.E. and SIMON, J.A. (2002). Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208.
65. PAL-BHADRA, M., LEIBOVITCH, B.A., GANDHI, S.G., RAO, M., BHADRA, U., BIRCHLER, J.A. and ELGIN, S.C. (2004). Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303: 669-672.
66. PETRUK, S., SEDKOV, Y., RILEY, K.M., HODGSON, J., SCHWEISGUTH, F., HIROSE, S., JAYNES, J.B., BROCK, H.W. and MAZO, A. (2006). Transcription of bxd noncoding RNAs promoted by trithorax represses Ubx in cis by transcriptional interference. Cell 127: 1209-1221.
67. PHAM, J.W., PELLINO, J.L., LEE, Y.S., CARTHEW, R.W. and SONTHEIMER, E.J. (2004). A Dicer-2-dependent 80s complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 117: 1-3.
68. PIRROTTA, V. (1995). Chromatin complexes regulating gene expression in Drosophila. Curr Opin Genet Develop 5: 466-472.
69. QIAN, S., CAPOVILLA, M. and PIRROTTA, V. (1991). The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes. EMBO J 10: 1415-1425.
70. RINGROSE, L. and PARO, R. (2007). Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134: 223-232.
71. RONSHAUGEN, M., BIEMAR, F., PIEL, J., LEVINE, M. and LAI, E.C. (2005). The Drosophila microRNA iab-4 causes a dominant homeotic transformation of halteres to wings. Genes Dev. 19: 2947-2952.
72. RUBY, J.G., STARK, A., JOHNSTON, W.K., KELLIS, M., BARTEL, D.P. and LAI, E.C. (2007). Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res. 17: 1850-1864.
73. SAITO, K., NISHIDA, K.M., MORI, T., KAWAMURA, Y., MIYOSHI, K., NAGAMI, T., SIOMI, H. and SIOMI, M.C. (2006). Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev. 20: 2214-2222.
74. SANCHEZ-ELSNER, T., GOU, D., KREMMER, E. and SAUER, F. (2006). Noncoding RNAs of trithorax response elements recruit Drosophila Ash1 to Ultrabithorax. Science 311: 1118-1123.
75. SANCHEZ-HERRERO, E. and AKAM, M. (1989). Spatially ordered transcription of regulatory DNA in the bithorax complex of Drosophila. Development 107: 321-329.
76. SANCHEZ-HERRERO, E., VERNOS, I., MARCO, R. and MORATA, G. (1985). Genetic organization of Drosophila bithorax complex. Nature 313: 108-113.
77. SAROT, E., PAYEN-GROSCHENE, G., BUCHETON, A. and PELISSON, A. (2004). Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166: 1313-1321.
78. SHAO, Z., RAIBLE, F., MOLLAAGHABABA, R., GUYON, J.R., WU, C.T., BENDER, W. and KINGSTON, R.E. (1999). Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98: 37-46.
79. SHIMELL, M.J., SIMON, J., BENDER, W. and O-CONNOR, M.B. (1994). Enhancer point mutation results in a homeotic transformation in Drosophila. Science 264: 968-971.
80. SIMON, J., PEIFER, M., BENDER, W. and O'CONNOR, M. (1990). Regulatory elements of the bithorax complex that control expression along the anterior-posterior axis. EMBO J. 9: 3945-3956.
81. STARK, A., BUSHATI, N., JAN, C.H., KHERADPOUR, P., HODGES, E., BRENNECKE, J., BARTEL, D.P., COHEN, S.M. and KELLIS, M. (2008). A single Hox locus in Drosophila produces functional microRNAs from opposite DNA strands. Genes Dev. 22: 8-13.
82. STARK, A., KHERADPOUR, P., PARTS, L., BRENNECKE, J., HODGES, E., HANNON, G.J. and KELLIS, M. (2007). Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes. Genome Res. 17: 1865-1879.
83. TYLER, D.M., OKAMURA, K., CHUNG, W.-J., HAGEN, J.W., BEREZIKOV, E., HANNON, G.J. and LAI, E.C. (2008). Functionally distinct regulatory RNAs generated by bidirectional transcription and processing of microRNA loci. Genes Dev. 22: 26-36.
84. VAGIN, V.V., SIGOVA, A., LI, C., SEITZ, H., GVOZDEV, V. and ZAMORE, P.D. (2006). A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313: 320-324.
85. WANG, L., BROWN, J.L., CAO, R., ZHANG, Y., KASSIS, J.A. and JONES, R.S. (2004). Hierarchical recruitment of polycomb group silencing complexes. Molecular Cell 14: 637-646.
86. ZAMORE, P.D., TUSCHL, T., SHARP, P.A. and BARTEL, D.P. (2000). RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101: 25-33.
87. ZINK, D. and PARO, R. (1995). Drosophila Polycomb-group regulated chromatin inhibits the accessibility of a trans-activator to its target DNA. EMBO J 14: 5660-5671.