Sequence conservation and combinatorial complexity of Drosophila neural precursor cell enhancers

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Brody, Thomas ^a   Rasband, Wayne ^b   Baler, Kevin ^b   Kuzin, Alexander ^a   Kundu, Mukta ^a   Odenwald, Ward F ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; DROSOPHILA PROTEIN; NERVY PROTEIN, DROSOPHILA; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; ENHANCER REGION; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC CONSERVATION; IN VIVO STUDY; NERVE GROWTH; NEURAL STEM CELL; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PHYLOGENY; PROTEIN FOOTPRINTING; PROTEIN FUNCTION; SEQUENCE ALIGNMENT; ANIMAL; BIOLOGY; COMPARATIVE STUDY; COMPUTER PROGRAM; GENE; GENE LIBRARY; GENETICS; NERVE CELL; NUCLEOTIDE SEQUENCE; STEM CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; DROSOPHILA; DROSOPHILA PROTEINS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; GENES, INSECT; NEURONS; SEQUENCE ALIGNMENT; SOFTWARE; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 51249103417     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-371     Document Type: Article

References (64)

1. Davidson EH The regulatory genome; Gene regulatory networks in development and evolution Burlington MA, Academic Press (Elsevier) 2006
2. Levine M Davidson EH Gene regulatory networks for development Proc Natl Acad Sci USA 2005, 102:4936-42. 555974 15788537 10.1073/pnas.0408031102
3. Castro B Barolo S Bailey AM Posakony JW Lateral inhibition in proneural clusters: Cis-regulatory logic and default repression by Suppressor of Hairless Development 2005, 132:3333-44. 10.1242/dev.01920 15975935
4. Cave JW Loh F Surpris JW Xia L Caudy MA A DNA transcription code for cell-specific gene activation by notch signaling Curr Biol 2005, 15:94-104. 10.1016/j.cub.2004.12.070 15668164
5. Kiefer JC Jarman A Johnson J Pro-neural factors and neurogenesis Dev Dyn 2005 234 808 13 10.1002/dvdy.20522 16059914
6. Zhao G Wheeler SR Skeath JB Genetic control of dorsoventral patterning and neuroblast specification in the Drosophila central nervous system Int J Dev Biol 2007, 51:107-15. 10.1387/ijdb.062188gz 17294361
7. Campos-Ortega JA Genetic mechanisms of early neurogenesis in Drosophila melanogaster Mol Neurobiol 1995, 10:75-89. 10.1007/BF02740668 7576311
8. Cornell RA Ohlen TV Vnd/nkx, ind/gsh, and msh/msx: Conserved regulators of dorsoventral neural patterning? Curr Opin Neurobiol 2000, 10:63-71. 10.1016/S0959-4388(99)00049-5 10679430
9. Berman BP Pfeiffer BD Laverty TR Salzberg SL Rubin GM Eisen MB Celniker SE Computational identification of developmental enhancers: Conservation and function of TFbinding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura Genome Biol 2004, 5:R61. 522868 15345045 10.1186/gb-2004-5-9-r61
10. Odenwald WF Rasband W Kuzin A Brody T EVOPRINTER, a multigenomic comparative tool for rapid identification of functionally important DNA Proc Natl Acad Sci USA 2005, 102:14700-5. 1239946 16203978 10.1073/ pnas.0506915102
11. Brody T Rasband W Baler K Kuzin A Kundu M Odenwald WF cis-Decoder discovers constellations of conserved DNA sequences shared among tissue-specific enhancers Genome Biol 2007, 8:R75. 1929141 17490485 10.1186/gb-2007-8-5-r75
12. Hoch M Schröder C Seifert E Jäckle H cis-acting control elements for Krüppel expression in the Drosophila embryo EMBO J 1990, 9:2587-2595. 552291 2114978
13. Hoch M Seifert E Jäckle H Gene expression mediated by cis-acting sequences of the Kruppel gene in response to the Drosophila morphogens bicoid and hunchback EMBO J 1991, 10:2267-78. 452917 2065664
14. Hoch M Gerwin N Taubert H Jäckle H Competition for overlapping sites in the regulatory region of the Drosophila gene Kruppel Science 1992, 256:94-7. 10.1126/science.1348871 1348871
15. Emery JF Bier E Specificity of CNS and PNS regulatory subelements comprising pan-neural enhancers of the deadpan and scratch genes is achieved by repression Development 1995, 121:3549-3560. 8582269
16. Schröder C Tautz D Seifert E Jäckle H Differential regulation of the two transcripts from the Drosophila gap segmentation gene hunchback EMBO J 1998, 7(9):2881-2887. 2846287 457082
17. Ashraf SI Ganguly A Roote J Ip YT Worniu, a snail family zinc-finger protein, is required for brain development in Drosophila Dev Dynamics 2004, 231:379-386. 10.1002/dvdy.20130
18. Ip YT Levine M Bier E Neurogenic expression of snail is controlled by separable CNS and PNS promoter elements Development 1994, 120:199-207. 8119127
19. García-García MJ Ramain P Simpson P Modolell J Different contributions of pannier and wingless to the patterning of the dorsal mesothorax of Drosophila Development 1999, 126:3523-3532. 10409499
20. Holohan EE zur Lage PI Jarman AP Multiple enhancers contribute to spatial but not temporal complexity in the expression of the proneural gene, amos BMC Dev Biol 2006, 6:53. 1657009 17094800 10.1186/ 1471-213X-6-53
21. Sun Y Jan LY Jan YN Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system Development 1998, 125:3731-40. 9716538
22. Singson A Leviten MW Bang AG Hua XH Posakony JW Direct downstream targets of proneural activators in the imaginal disc include genes involved in lateral inhibitory signaling Genes Dev 1994, 8:2058-71. 10.1101/gad.8.17.2058 7958878
23. Reeves N Posakony JW Genetic programs activated by proneural proteins in the developing Drosophila PNS Dev Cell 2005, 8:413-425. 10.1016/ j.devcel.2005.01.020 15737936
24. Culi J Modolell J Proneural gene self-stimulation in neural precursors: an essential mechanism for sense organ development that is regulated by Notch signaling Genes Dev 1998, 12:2036-47. 316959 9649507 10.1101/ gad.12.13.2036
25. Nellesen DT Lai EC Posakony JW Discrete enhancer elements mediate selective responsiveness of enhancer of split complex genes to common transcriptional activators Dev Biol 1999, 213:33-53. 10.1006/ dbio.1999.9324 10452845
26. Lai EC Bodner R Posakony JW The Enhancer of split complex of Drosophila includes four Notch-regulated members of the bearded gene family Development 2000, 127:3441-55. 10903170
27. Bailey AM Posakony JW Suppressor of Hairless directly activates transcription of Enhancer of split complex genes in response to Notch receptor activity Genes Dev 1995, 9:2609-2622. 10.1101/gad.9.21.2609 7590239
28. Lecourtois M Schweisguth F The neurogenic Suppressor of Hairless DNA-binding protein mediates the transcriptional activation of the Enhancer of split complex genes triggered by Notch signaling Genes Dev 1995, 9:2598-2608. 10.1101/gad.9.21.2598 7590238
29. Akin ZN Nazarali AJ Hox genes and their candidate downstream targets in the developing central nervous system Cell Mol Neurobiol 2005, 25:697-741. 10.1007/s10571-005-3971-9 16075387
30. Sagerstrom CG PbX marks the spot Dev Cell 2004, 6:737-8. 10.1016/ j.devcel.2004.05.015 15177017
31. Bertrand N Castro DS Guillemot F Proneural genes and the specification of neural cell types Nat Rev Neurosci 2002, 3:517-30. 10.1038/nrn874 12094208
32. Powell LM zur Lage PI Prentice DR Senthinathan B Jarman AP The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites Mol Cell Biol 2004, 24:9517-26. 522279 15485919 10.1128/MCB.24.21.9517-9526.2004
33. Jennings BH Tyler DM Bray SJ Target specificities of Drosophila Enhancer of split basic helix-loop-helix proteins Mol Cell Biol 1999, 19:4600-4610. 84258 10373509
34. Morgenstern B Atchley WR Evolution of bHLH TFs: Modular evolution by domain shuffling? Mol Biol Evol 1999, 16:1654-63. 10605108
35. Hughes CL Kaufman TC Hox genes and the evolution of the arthropod body plan Evol Dev 2002, 4:459-99. 10.1046/j.1525-142X.2002.02034.x 12492146
36. Prokop A Bray S Harrison E Technau GM Homeotic regulation of segment- specific differences in neuroblast numbers and proliferation in the Drosophila central nervous system Mech Dev 1998, 74:99-110. 10.1016/ S0925-4773(98)00068-9 9651493
37. Cenci C Gould AP Drosophila Grainyhead specifies late programmes of neural proliferation by regulating the mitotic activity and Hox-dependent apoptosis of neuroblasts Development 2005, 132:3835-45. 10.1242/dev.01932 16049114
38. Berger C Pallavi SK Prasad M Shashidhara LS Technau GM A critical role for cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster Nat Cell Biol 2005, 7:56-62. 10.1038/ncb1203 15580266
39. Bello B Holbro N Reichert H Polycomb group genes are required for neural stem cell survival in postembryonic neurogenesis of Drosophila Development 2007, 134:1091-9. 10.1242/dev.02793 17287254
40. Gehring WJ Qian YQ Billeter M Furukubo-Tokunaga K Schier AF Resendez-Perez D Affolter M Otting G Wüthrich K Homeodomain-DNA recognition Cell 1994, 78:211-23. 10.1016/0092-8674(94)90292-5 8044836
41. Van Dijk MA Voorhoeve PM Murre C Pbx1 is converted into a transcriptional activator upon acquiring the N-terminal region of E2A in pre-B-cell acute lymphoblastoid leukemia Proc Natl Acad Sci USA 1992 90 6061 5 10.1073/pnas.90.13.6061
42. Lu Q Wright DD Kamps MP Fusion with E2A converts the Pbx1 homeodomain protein into a constitutive transcriptional activator in human leukemias carrying the t(1;19) translocation Mol Cell Biol 1994, 14:3938-48. 358760 7910944
43. Moens CB Selleri L Hox cofactors in vertebrate development Dev Biol 2006, 291:193-206. 10.1016/j.ydbio.2005.10.032 16515781
44. Knoepfler PS Lu Q Kamps MP Pbx-1 Hox heterodimers bind DNA on inseparable half-sites that permit intrinsic DNA binding specificity of the Hox partner at nucleotides 3′ to a TAAT motif Nucleic Acids Res 1996, 24:2288-94. 145957 8710498 10.1093/nar/24.12.2288
45. Bray S Furriols M Notch pathway: Making sense of suppressor of hairless Curr Biol 2001, 11:R217-21. 10.1016/S0960-9822(01)00109-9 11301266
46. Nam Y Sliz P Pear WS Aster JC Blacklow SC Cooperative assembly of higher-order Notch complexes functions as a switch to induce transcription Proc Natl Acad Sci USA 2007, 104:2103-8. 1892977 17284587 10.1073/pnas.0611092104
47. Maeder ML Polansky BJ Robson BE Eastman DA Phylogenetic footprinting analysis in the upstream regulatory regions of the Drosophila Enhancer of split genes Genetics 2007, 177:1377-94. 2147979 18039873 10.1534/ genetics.107.070425
48. Klämbt C Knust E Tietze K Campos-Ortega JA Closely related transcripts encoded by the neurogenic gene complex enhancer of split of Drosophila melanogaster EMBO J 1989, 8:203-10. 400790 2540957
49. Tietze K Oellers N Knust E Enhancer of split D. A dominant mutation of Drosophila, and its use in the study of functional domains of a helix-loop-helix protein Proc Natl Acad Sci USA 1992, 89:6152-6156. 402140 1631102 10.1073/pnas.89.13.6152
50. Fairall L Schwabe JW Chapman L Finch JT Rhodes D The crystal structure of a two zinc-finger peptide reveals an extension to the rules for zinc-finger/DNA recognition Nature 1993, 366:483-7. 10.1038/366483a0 8247159
51. Guo M Bier E Jan LY Jan YN tramtrack acts downstream of numb to specify distinct daughter cell fates during asymmetric cell divisions in the Drosophila PNS Neuron 1995, 14:913-925. 10.1016/0896-6273(95)90330-5 7748559
52. Giesen K Hummel T Stollewerk A Harrison S Travers A Klambt C Glial development in the Drosophila CNS requires concomitant activation of glial and repression of neuronal differentiation genes Development 1997, 124:2307-2316. 9199357
53. Badenhorst P Finch JT Travers AA Tramtrack co-operates to prevent inappropriate neural development in Drosophila Mech Dev 2002, 117:87-101. 10.1016/S0925-4773(02)00183-1 12204250
54. Breslin MB Zhu M Notkins AL Lan MS Neuroendocrine differentiation factor, IA-1, is a transcriptional repressor and contains a specific DNA- binding domain: Identification of consensus IA-1 binding sequence Nucleic Acid Res 2002, 30:1038-1045. 100352 11842116 10.1093/nar/ 30.4.1038
55. Markstein M Markstein P Markstein V Levine MS Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo Proc Natl Acad Sci USA 2002, 99:763-8. 117379 11752406 10.1073/pnas.012591199
56. Feinstein PG Kornfeld K Hogness DS Mann RS Identification of homeotic target genes in Drosophila melanogaster including nervy, a proto-oncogene homologue Genetics 1995, 140:573-86. 1206636 7498738
57. Terman JR Kolodkin AL Nervy links protein kinase a to plexin-mediated semaphorin repulsion Science 2004, 303:1204-7. 10.1126/science.1092121 14976319
58. Wildonger J Mann RS Evidence that nervy, the Drosophila homolog of ETO/ MTG8, promotes mechanosensory organ development by enhancing Notch signaling Dev Biol 2005, 286:507-20. 10.1016/j.ydbio.2005.08.026 16168983
59. Brewster R Bodmer R Origin and specification of type II sensory neurons in Drosophila Development 1995, 121:2923-36. 7555719
60. Down TA Bergman CM Su J Hubbard TJ Large-scale discovery of promoter motifs in Drosophila melanogaster PLoS Comput Biol 2007, 3:e7. 1779301 17238282 10.1371/journal.pcbi.0030007
61. Yavatkar A Lin Y Ross J Fann Y Brody T Odenwald WF Rapid detection and curation of conserved DNA via enhanced-BLAT and EvoPrinterHD analysis BMC Genomics 2008, 9:106. 2268679 18307801 10.1186/1471-2164-9-106
62. Shannon P Markiel A Ozier O Baliga NS Wang JT Ramage D Amin N Schwikowski B Ideker T Cytoscape: A software environment for integrated models of biomolecular interaction networks Genome Res 2003, 13:2498-504. 403769 14597658 10.1101/gr.1239303
63. Barolo S Castro B Posakony JW New Drosophila transgenic reporters: insulated P-element vectors expressing fast-maturing RFP Biotechniques 2004, 36:436 40, 442 15038159
64. Kuzin A Kundu M Brody T Odenwald WF The Drosophila nerfin-1 mRNA requires multiple microRNAs to regulate its spatial and temporal translation dynamics in the developing nervous system Dev Biol 2007, 310:35-43. 2064069 17714701 10.1016/j.ydbio.2007.07.012