The ABC of the BX-C: The bithorax complex explained

Development

Volumn 133, Issue 8, 2006, Pages 1413-1422

  Maeda, Robert K ^a   Karch, François ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; HOX PROTEIN;

ABDOMEN; ANIMAL TISSUE; ARTICLE; CHROMATIN; CONTROLLED STUDY; DISSECTION; DROSOPHILA; EMBRYO; EMBRYO SEGMENTATION; EVOLUTION; FLY; GENE; GENE EXPRESSION; HOMEOBOX; NONHUMAN; PRIORITY JOURNAL; THORAX;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; MULTIGENE FAMILY; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 33646690307     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02323     Document Type: Article

References (112)

1. Barges, S., Mihaly, J., Galloni, M., Hagstrom, K., Müller, M., Shanower, G., Schedl, R, Gyurkovics, H. and Karch, F. (2000). The Fab-8 boundary defines the distal limit of the bithorax complex iab-7 domain and insulates iab-7 from initiation elements and a PRE in the adjacent iab-8 domain. Development 127, 779-790.
2. Bateson, W. (1894). Materials for the Study of Variation. London: Macmillan.
3. Beachy, P. A., Helfand, S. L. and Hogness, D. S. (1985). Segmental distribution of bithorax complex proteins during Drosophila development. Nature 313, 545-551.
4. Bender, W. and Hudson, A. (2000). P element homing to the Drosophila bithorax complex. Development 127, 3981-3992.
5. Bender, W. and Fitzgerald, D. P. (2002). Transcription activates repressed domains in the Drosophila bithorax complex. Development 129, 4923-4930.
6. Bender, W., Spierer, P. and Hogness, D. S. (1983a). Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J. Mol. Biol. 168, 17-33.
7. Bender, W., Akam, M., Karch, F., Beachy, P. A., Peifer, M., Spierer, P., Lewis, E. B. and Hogness, D. S. (1983b). Molecular genetics of the bithorax complex in Drosophila melanogaster. Science 221, 23-29.
8. Boivin, A. and Dura, J. M. (1998). In vivo chromatin accessibility correlates with gene silencing in Drosophila. Genetics 150, 1539-1549.
9. Boulet, A., Lloyd, A. and Sakonju, S. (1991). Molecular definition of the morphogenetic and regulatory functions and the cis-regulatory elements of the Drosophila Abd-B homeotic gene. Development 111, 393-405.
10. Brock, H. W. and van Lohuizen, M. (2001). The Polycomb group - no longer an exclusive club? Curr. Opin. Genet. Dev. 11, 175-181.
11. Busturia, A. and Bienz, M. (1993). Silencers in abdominal-B, a homeotic Drosophila gene. EMBO J. 12, 1415-1425.
12. Busturia, A., Lloyd, A., Bejarano, F., Zavortink, M., Xin, H. and Sakonju, S. (2001). The MCP silencer of the Drosophila Abd-B gene requires both Pleiohomeotic and GAGA factor for the maintenance of repression. Development 128, 2163-2173.
13. Cai, H. N. and Shen, P. (2001). Effects of cis arrangement of chromatin insulators on enhancer-blocking activity. Science 291, 493-495.
14. Casanova, J., Sanchez-Herrero, E. and Morata, G. (1986). Identification and characterization of a parasegment specific regulatory element of the abdominal-B gene of Drosophila. Cell 47, 627-636.
15. Casanova, J., Sanchez-Herrero, E., Busturia, A. and Morata, G. (1987). Double and triple mutant combinations of the bithorax complex of Drosophila. EMBO J. 6, 3103-3109.
16. 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.
17. Castelli-Gair, J. and Akam, M. (1995). How the Hox gene Ultrabithorax specifies two different segments: the significance of spatial and temporal regulation within metameres. Development 121, 2973-2982.
18. Celniker, S. E., Keelan, D. J. and Lewis, E. B. (1989). The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain. Genes Dev 3, 1424-1436.
19. Celniker, S. E., Sharma, S., Keelan, D. J. and Lewis, E. B. (1990). The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J. 9, 4277-4286.
20. Chan, C. S., Rastelli, L. and Pirrotta, V. (1994). A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J. 13, 2553-2564.
21. Chen, Q., Lin, L., Smith, S., Lin, Q. and Zhou, J. (2005). Multiple promoter targeting sequences exist in Abdominal-B to regulate long-range gene activation. Dev. Biol. 286, 629-636.
22. Chiang, A., O'Connor, M. B., Paro, R., Simon, J. and Bender, W. (1995). Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex. Development 121, 1681-1689.
23. 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.
24. 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.
25. Delorenzi, M. and Bienz, M. (1990). Expression of Abdominal-B homeoproteins in Drosophila embryos. Development 108, 323-329.
26. DiNardo, S., Heemskerk, J., Dougan, S. and O'Farrell, P. H. (1994). The making of a maggot: patterning the Drosophila embryonic epidermis. Curr. Opin. Genet. Dev. 4, 529-534.
27. 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.
28. Duboule, D. (1992). The vertebrate limb: a model system to study the Hox/ HOM gene network during development and evolution. BioEssays 14, 375-384.
29. Duncan, I. M. (1982). Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene complexes of Drosophila melanogaster. Genetics 102, 49-70.
30. Duncan, I. (1987). The bithorax complex. Annu. Rev. Genet. 21, 285-319.
31. Estrada, B., Casares, F., Busturia, A. and Sanchez-Herrero, E. (2002). Genetic and molecular characterization of a novel iab-8 regulatory domain in the Abdominal-B gene of Drosophila melanogaster. Development 129, 5195-5204.
32. Fitzgerald, D. P. and Bender, W. (2001). Polycomb group repression reduces DNA accessibility. Mol. Cell. Biol. 21, 6585-6597.
33. Francis, N. J., Saurin, A. J., Shao, Z. and Kingston, R. E. (2001). Reconstitution of a functional core polycomb repressive complex. Mol. Cell 8, 545-556.
34. Fritsch, C., Brown, J. L., Kassis, J. A. and Muller, J. (1999). The DNA-binding Polycomb group protein Pleiohomeotic mediates silencing of a Drosophila homeotic gene. Development 126, 3905-3913.
35. Galloni, M., Gyurkovics, H., Schedl, P. and Karch, F. (1993). The bluetail transposon: evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex. EMBO J. 12, 1087-1097.
36. Garber, R. L., Kuroiwa, A. and Gehring, W. J. (1983). Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J. 2, 2027-2036.
37. Geyer, P. K. and Corces, V. G. (1992). DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev 6, 1865-1873.
38. Gruzdeva, N., Kyrchanova, O., Parshikov, A., Kullyev, A. and Georgiev, P. (2005). The Mcp element from the bithorax complex contains an insulator that is capable of pairwise interactions and can facilitate enhancer-promoter communication. Mol. Cell. Biol. 25, 3682-3689.
39. Gyurkovics, H., Gausz, J., Kummer, J. and Karch, F. (1990). A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation. EMBO J. 9, 2579-2585.
40. Hagstrom, K., Muller, M. and Schedl, P. (1996). Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex. Genes Dev. 10, 3202-3215.
41. Hartenstein, V. (1993). Altas of Drosophila Development. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
42. Hoch, M. and Jackle, H. (1993). Transcriptional regulation and spatial patterning in Drosophila. Curr. Opin. Genet. Dev. 3, 566-573.
43. Hogga, I. and Karch, F. (2002). Transcription through the iab-7 cis-regulatory domain of the bithorax complex interferes with maintenance of Polycomb-mediated silencing. Development 129, 4915-4922.
44. Hogga, I., Mihaly, J., Barges, S. and Karch, F. (2001). Replacement of Fab-7 by the gypsy or scs insulator disrupts long-distance regulatory interactions in the Abd-B gene of the bithorax complex. Mol. Cell 8, 1145-1151.
45. Ingham, P. W. (1988). The molecular genetics of embryonic pattern formation in Drosophila. Nature 335, 25-34.
46. Irish, V. F., Martinez-Arias, A. and Akam, M. (1989). Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. EMBO J. 8, 1527-1537.
47. Jürgens, G. (1985). A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature 316, 153-155.
48. 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.
49. Karch, F., Bender, W. and Weiffenbach, B. (1990). abdA expression in Drosophila embryos. Genes Dev 4, 1573-1587.
50. Karch, F., Galloni, M., Sipos, L., Gausz, J., Gyurkovics, H. and Schedl, P. (1994). Mcp and Fab-7: molecular analysis of putative boundaries of cis-regulatory domains in the bithorax complex of Drosophila melanogaster. Nucleic Acids Res. 22, 3138-3146.
51. Kaufman, T. C., Seeger, M. A. and Olsen, G. (1990). Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster. Adv. Genet. 27, 309-362.
52. Kellum, R. and Schedl, P. (1991). A position-effect assay for boundaries of higher order chromosomal domains. Cell 64, 941-950.
53. Kennison, J. A. (1993). Transcriptional activation of Drosophila homeotic genes from distant regulatory elements. Trends Genet. 9, 75-78.
54. Kennison, J. A. and Tamkun, J. W. (1988). Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc. Natl. Acad. Sci. USA 85, 8136-8140.
55. Kornberg, T. B. and Tabata, T. (1993). Segmentation of the Drosophila embryo. Curr. Opin. Genet. Dev. 3, 585-594.
56. Kuziora, M. A. and McGinnis, W. (1988), Different transcripts of the Drosophila Abd-B gene correlate with distinct genetic sub-functions. EMBO J. 7, 3233-3244.
57. Le Calvez, J. (1948). In (3R) SSAr: Mutation Aristapedia, hétérozygote dominante, homozygote lethal chez Drosophila melanogaster. Bull. Biol. Fr. Belg. 82, 97-113.
58. Lewis, E. B. (1951). Pseudoallelism and gene evolution. Cold Spring Harbor Symp. Quant. Biol. 16, 159-174.
59. Lewis, E. B. (1954). The theory and application of a new method of detecting chromosomal rearrangements in Drosophila melanogaster. Am. Nat. 88, 225-239.
60. Lewis, E. B. (1963). Genes and developmental pathways. Am. Zool. 3, 33-56.
61. Lewis, E. B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565-570.
62. 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.
63. 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.
64. Lis, J. T., Simon, J. A. and Sutton, C. A. (1983). New heat shock puffs and beta-galactosidase activity resulting from transformation of Drosophila with an hsp70-lacZ hybrid gene. Cell 35, 403-410.
65. Little, J. W., Byrd, C. A. and Brower, D. L. (1990). Effect of abx, bx and pbx mutations on expression of homeotic genes in Drosophila larvae. Genetics 124, 899-908.
66. Macias, A., Casanova, J. and Morata, G. (1990). Expression and regulation of the abd-A gene of Drosophila. Development 110, 1197-1207.
67. 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.
68. Martinez-Arias, A. and Lawrence, P. (1985). Parasegments and compartments in the Drosophila embryo. Nature 313, 639-642.
69. McCall, K. and Bender, W. (1996). Probes of chromatin accessibility in the Drosophila bithorax complex respond differently to Polycomb-mediated repression. EMBO J. 15, 569-580.
70. McCall, K., O'Connor, M. B. and Bender, W. (1994). Enhancer traps in the Drosophila bithorax complex mark parasegmental domains. Genetics 138, 387-399.
71. McGinnis, W. and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell 68, 283-302.
72. McGinnis, W., Levine, M. S., Hafen, E., Kuroiwa, A. and Gehring, W. J. (1984). A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308, 428-433.
73. Mihaly, J., Hogga, I., Gausz, J., Gyurkovics, H. and Karch, F. (1997). In situ dissection of the Fab-7 region of the bithorax complex into a chromatin domain boundary and a Polycomb-response element. Development 124, 1809-1820.
74. Mihaly, J., Hogga, I., Barges, S., Galloni, M., Mishra, R. K., Hagstrom, K., Muller, M., Schedl, P., Sipos, L., Gausz, J. et al. (1998). Chromatin domain boundaries in the Bithorax complex. Cell. Mol. Life Sci. 54, 60-70.
75. Muller, J. and Bienz, M. (1991). Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo. EMBO J. 10, 3147-3155.
76. Muller, J. and Bienz, M. (1992). Sharp anterior boundary of homeotic gene expression conferred by the fushi tarazu protein. EMBO J. 11, 3653-3661.
77. 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.
78. Muravyova, E., Golovnin, A., Gracheva, E., Parshikov, A., Belenkaya, T., Pirrotta, V. V. and Georgiev, P. (2001). Loss of insulator activity by paired Su(Hw) chromatin insulators. Science 291, 495-498.
79. Ng, J., Hart, C. M., Morgan, K. and Simon, J. A. (2000). A Drosophila ESC-E(Z) protein complex is distinct from other polycomb group complexes and contains covalently modified ESC. Mol. Cell. Biol. 20, 3069-3078.
80. O'Kane, C. J. and Gehring, W. J. (1987). Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl. Acad. Sci. USA 84, 9123-9127.
81. Paro, R. (1990). Imprinting a determined state into the chromatin of Drosophila. Trends Genet 6, 416-421.
82. Peifer, M., Karch, F. and Bender, W. (1987). The bithorax complex: control of segmental identity. Genes Dev. 1, 891-898.
83. Pirrotta, V. (1997). Chromatin-silencing mechanisms in Drosophila maintain patterns of gene expression. Trends Genet 13, 314-318.
84. Pirrotta, V., Chan, C. S., McCabe, D. and Qian, S. (1995). Distinct parasegmental and imaginal enhancers and the establishment of the expression pattern of the Ubx gene. Genetics 141, 1439-1450.
85. 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.
86. Rank, G., Prestel, M. and Paro, R. (2002). Transcription through intergenic chromosomal memory elements of the Drosophila bithorax complex correlates with an epigenetic switch. Mol. Cell. Biol. 22, 8026-8034.
87. Sanchez-Elsner, T., Gou, D., Kremmer, E. and Sauer, F. (2006). Non coding RNAs of Trithorax response elements recruit Drorophila Ash1 to Ultrabithorax. Science 311, 1118-1123.
88. Sanchez-Herrero, E. (1991). Control of the expression of the bithorax complex genes abdominal-A and abdominal-B by cis-regulatory regions in Drosophila embryos. Development 111, 437-449.
89. Sanchez-Herrero, E. and Crosby, M. A. (1988). The Abdominal-B gene of Drosophila melanogaster: overlapping transcripts exhibit two different spatial distributions. EMBO J. 7, 2163-2173.
90. Sanchez-Herrero, E. and Akam, M. (1989). Spatially ordered transcription of regulatory DNA in the bithorax complex of Drosophila. Development 107, 321-329.
91. Sanchez-Herrero, E., Vernos, I., Marco, R. and Morata, G. (1985). Genetic organization of Drosophila bithorax complex. Nature 313, 108-113.
92. Schmitt, S., Prestel, M. and Paro, R. (2005). Intergenic transcription through a polycomb group response element counteracts silencing. Genes Dev 19, 697-708.
93. Scott, M. P. and Weiner, A. J. (1984). Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc. Natl. Acad. Sci. USA 81, 4115-4119.
94. Scott, M. P., Weiner, A. J., Hazelrigg, T. I., Polisky, B. A., Pirrotta, V., Scalenghe, F. and Kaufman, T. C. (1983). The molecular organization of the Antennapedia locus of Drosophila. Cell 35, 763-776.
95. Shearn, A. (1989). The ash-1, ash-2 and trithorax genes of Drosophila melanogaster are functionally related. Genetics 121, 517-525.
96. 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.
97. Shimell, M. J., Peterson, A. J., Burr, J., Simon, J. A. and O'Connor, M. B. (2000). Functional analysis of repressor binding sites in the iab-2 regulatory region of the abdominal-A homeotic gene. Dev. Biol. 218, 38-52.
98. Simon, J. (1995). Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr. Opin. Cell Biol. 7, 376-385.
99. Simon, J. A. and Tamkun, J. W. (2002). Programming off and on states in chromatin: mechanisms of Polycomb and trithorax group complexes. Curr. Opin. Genet. Dev. 12, 210-218.
100. 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.
101. Simon, J., Chiang, A., Bender, W., Shimell, M. J. and O'Connor, M. (1993). Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev. Biol. 158, 131-144.
102. Struhl, G. and Akam, M. (1985). Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 4, 3259-3264.
103. Tie, F., Furuyama, T., Prasad-Sinha, J., Jane, E. and Harte, P. J. (2001). The Drosophila Polycomb Group proteins ESC and E(Z) are present in a complex containing the histone-binding protein p55 and the histone deacetylase RPD3. Development 128, 275-286.
104. Tiong, S., Bone, L. M. and Whittle, J. R. (1985). Recessive lethal mutations within the bithorax-complex in Drosophila. Mol. Gen. Genet. 200, 335-342.
105. Von Allmen, G., Hogga, I., Spierer, A., Karch, F., Bender, W., Gyurkovics, H. and Lewis, E. (1996). Splits in fruitfly Hox gene complexes. Nature 380, 116.
106. White, R. A. H. and Wilcox, M. (1985). Regulation of the distribution of Ultrabithorax proteins in Drosophila. Nature 318, 563-567.
107. White, R. A. and Lehmann, R. (1986). A gap gene, hunchback, regulates the spatial expression of Ultrabithorax. Cell 47, 311-321.
108. Zavortink, M. and Sakonju, S. (1989). The morphogenetic and regulatory functions of the Drosophila Abdominal-B gene are encoded in overlapping RNAs transcribed from separate promoters. Genes Dev 3, 1969-1981.
109. Zhang, C. C., Muller, J., Hoch, M., Jackle, H. and Bienz, M. (1991). Target sequences for hunchback in a control region conferring Ultrabithorax expression boundaries. Development 113, 1171-1179.
110. Zhou, J. and Levine, M. (1999). A novel cis-regulatory element, the PTS, mediates an anti-insulator activity in the Drosophila embryo. Cell 99, 567-575.
111. Zhou, J., Barolo, S., Szymanski, P. and Levine, M. (1996). The Fab-7 element of the bithorax complex attenuates enhancer-promoter interactions in the Drosophila embryo. Genes Dev. 10, 3195-3201.
112. Zhou, J., Ashe, H., Burks, C. and Levine, M. (1999). Characterization of the transvection mediating region of the abdominal-B locus in Drosophila. Development 126, 3057-3065.