Functional tests of enhancer conservation between distantly related species

Development

Volumn 130, Issue 21, 2003, Pages 5133-5142

  Ruvinsky, Ilya ^a   Ruvkun, Gary ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

C. briggsae; C. elegans; Co evolution; D. melanogaster; Enhancer; Evolution

Indexed keywords

CIS ACTING ELEMENT; GREEN FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR;

ARTHROPOD; ARTICLE; BINDING SITE; CAENORHABDITIS; CAENORHABDITIS BRIGGSAE; CAENORHABDITIS ELEGANS; CELL TYPE; CONTROLLED STUDY; DEVELOPMENT; DROSOPHILA MELANOGASTER; ENHANCER REGION; EVOLUTIONARY HOMOLOGY; FUNCTIONAL ASSESSMENT; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE FUSION; GENE SEQUENCE; GENE STRUCTURE; GENETIC CONSERVATION; GENETIC DISTANCE; GENETIC MODEL; GENETIC VARIABILITY; HYPOTHESIS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MOLECULAR RECOGNITION; MUSCLE; NEMATODE; NERVE CELL; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; SPECIES DIFFERENCE; TIME; TISSUE TYPES;

ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; ENHANCER ELEMENTS (GENETICS); EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS;

ARTHROPODA; CAENORHABDITIS; CAENORHABDITIS BRIGGSAE; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; MELANOGASTER; NEMATODA;

EID: 0242467199     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00711     Document Type: Article

References (68)

1. Aurelio, O., Hall, D. H. and Hobert, O. (2002). Immunoglobulin-domain proteins required for maintenance of ventral nerve cord organization. Science 295, 686-690.
2. Benveniste, R. J. and Taghert, P. H. (1999). Cell type-specific regulatory sequences control expression of the Drosophila FMRF-NH2 neuropeptide gene. J. Neurobiol. 38, 507-520.
3. Brenner, S., Venkatesh, B., Yap, W. H., Chou, C. F., Tay, A., Ponniah, S., Wang, Y. and Tan, Y. H. (2002). Conserved regulation of the lymphocyte-specific expression of lck in the Fugu and mammals. Proc. Natl. Acad. Sci. USA 99, 2936-2941.
4. Burr, A. H. (1985). The photomovement of Caenorhabditis elegans, a nematode which lacks ocelli. Proof that the response is to light not radiant heating. Photochem. Photobiol. 41, 577-582.
5. Carroll, S. B., Grenier, J. K. and Weatherbee, S. D. (2001). From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. Malden, MA: Blackwell Scientific.
6. Chung, Y. D., Zhu, J., Han, Y. and Kernan, M. J. (2001). nompA encodes a PNS-specific, ZP domain protein required to connect mechanosensory dendrites to sensory structures. Neuron 29, 415-428.
7. Coghlan, A. and Wolfe, K. H. (2002). Fourfold faster rate of genome rearrangement in nematodes than in Drosophila. Genome Res. 12, 857-867.
8. Combes, D., Fedon, Y., Toutant, J. P. and Arpagaus, M. (2001). Acetyleholinesterase genes in the nematode Caenorhabditis elegans. Int. Rev. Cytol. 209, 207-239.
9. Conlon, E. L., Fairclough, L., Price, B. M., Casey, E. S. and Smith, J. C. (2001). Determinants of T box protein specificity. Development 128, 3749-3758.
10. Cripps, R. M., Zhao, B. and Olson, E. N. (1999). Transcription of the myogenic regulatory gene Mef2 in cardiac, somatic, and visceral muscle cell lineages is regulated by a Tinman-dependent core enhancer. Dev. Biol. 215, 420-430.
11. Davidson, E. H. (2001). Genomic Regulatory Systems: Development and Evolution. San Diego, CA: Academic Press.
12. Eastman, C., Horvitz, H. R. and Jin, Y. (1999). Coordinated transcriptional regulation of the unc-25 glutamic acid decarboxylase and the unc-47 GABA vesicular transporter by the Caenorhabditis elegans UNC-30 homeodomain protein. J. Neurosci. 19, 6225-6234.
13. Fishman, M. C. and Olson, E. N. (1997). Parsing the heart: genetic modules for organ assembly. Cell 91, 153-156.
14. Fitch, D. H. A. and Thomas, W. K. (1997). Evolution. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), pp. 815-850. Plainview, NY. Cold Spring Harbor Laboratory Press.
15. Frasch, M., Chen, X. and Lufkin, T. (1995). Evolutionary-conserved enhancers direct region-specific expression of the murine Hoxa-1 and Hoxa-2 loci in both mice and Drosophila. Development 121, 957-974.
16. Galant, R. and Carroll, S. B. (2002). Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415, 910-913.
17. Gao, Q., Yuan, B. and Chess, A. (2000). Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci. 3, 780-785.
18. Granato, M., Schnabel, H. and Schnabel, R. (1994). pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res. 22, 1762-1763.
19. Grens, A., Mason, E., Marsh, J. L. and Bode, H. R. (1995). Evolutionary conservation of a cell fate specification gene: the Hydra achaete-scute homolog has proneural activity in Drosophila. Development 121, 4027-4035.
20. Guastella, J., Johnson, C. D. and Stretton, A. O. (1991). GABA-immunoreactive neurons in the nematode Ascaris. J. Comp. Neurol. 307, 584-597.
21. Halfon, M. S., Carmena, A., Gisselbrecht, S., Sackerson, C. M., Jimenez, F., Baylies, M. K. and Michelson, A. M. (2000). Ras pathway specificity is determined by the integration of multiple signal- activated and tissue-restricted transcription factors. Cell 103, 63-74.
22. Hauck, B., Gehring, W. J. and Walldorf, U. (1999). Functional analysis of an eye specific enhancer of the eyeless gene in Drosophila. Proc. Natl. Acad. Sci. USA 96, 564-569.
23. Haun, C., Alexander, J., Stainier, D. Y. and Okkema, P. G. (1998). Rescue of Caenorhabditis elegans pharyngeal development by a vertebrate heart specification gene. Proc. Natl. Acad. Sci. USA 95, 5072-5075.
24. Hobert, O., Tessmar, K. and Ruvkun, G. (1999). The Caenorhabditis elegans lim-6 LIM homeobox gone regulates neurite outgrowth and function of particular GABAergic neurons. Development 126, 1547-1562.
25. Hoffmann, F., Fournier, D. and Spierer, P. (1992). Minigene rescues acetylcholinesterase lethal mutations in Drosophila melanogaster. J. Mol. Biol. 223, 17-22.
26. Hsia, C. C. and McGinnis, W. (2003). Evolution of transcription factor function. Curr. Opin. Genet. Dev. 13, 199-206.
27. Johnson, W. A., McCormick, C. A., Bray, S. J. and Hirsh, J. (1989). A neuron-specific enhancer of the Drosophila dopa decarboxylase gene. Genes Dev. 3, 676-686.
28. Jones, B. K., Levorse, J. and Tilghman, S. M. (2002). A human H19 transgene exhibits impaired paternal-specific imprint acquisition and maintenance in mice. Hum. Mol. Genet. 11, 411-418.
29. King, M.-C. and Wilson, A. C. (1975). Evolution at two levels in humans and chimpanzees. Science 188, 107-116.
30. Kitamoto, T., Ikeda, K. and Salvaterra, P. M. (1992). Analysis of cis-regulatory elements in the 5′ flanking region of the Drosophila melanogaster choline acetyltransferase gene. J. Neurosci. 12, 1628-1639.
31. Locascio, A., Aniello, F., Amoroso, A., Manzanares, M., Krumlauf, R. and Branno, M. (1999). Patterning the ascidian nervous system: structure, expression and transgenic analysis of the CiHox3 gene. Development 126, 4737-4748.
32. Ludwig, M. Z., Patel, N. H. and Kreitman, M. (1998). Functional analysis of eve stripe 2 enhancer evolution in Drosophila: rules governing conservation and change. Development 125, 949-958.
33. Ludwig, M. Z., Bergman. C., Patel, N. H. and Kreitman, M. (2000). Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403, 564-567.
34. Maduro, M. F., Gordon, M., Jacobs, R. and Pilgrim, D. B. (2000). The UNC-119 family of neural proteins is functionally conserved between humans, Drosophila and C. elegans. J. Neurogenet. 13, 191-212.
35. Maduro, M. and Pilgrim, D. (1995). Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141, 977-988.
36. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
37. McCormick, A., Core, N., Kerridge, S. and Scott, M. P. (1995). Homeotic response elements are tightly linked to tissue-specific elements in a transcriptional enhancer of the teashirt gene. Development 121, 2799-2812.
38. McIntire, S. L., Jorgensen, E., Kaplan, J. and Horvitz, H. R. (1993). The GABAergic nervous system of Caenorhabditis elegans. Nature 364, 337-341.
39. Molin, L., Mounsey, A., Aslam, S., Bauer, P., Young, J., James, M., Sharma-Oates, A. and Hope, I. A. (2000). Evolutionary conservation of redundancy between a diverged pair of forkhead transcription factor homologues. Development 127, 4825-4835.
40. Morris, S. C. (2000). Evolution: bringing molecules into the fold. Cell 100, 1-11.
41. Okkema, P. G., Ha, E., Haun, C., Chen, W. and Fire, A. (1997). The Caenorhabditis elegans NK-2 homeobox gene ceh-22 activates pharyngeal muscle gene expression in combination with pha-1 and is required for normal pharyngeal development. Development 124, 3965-3973.
42. Pilon, M., Peng, X. R., Spence, A. M., Plasterk, R. H. and Dosch, H. M. (2000). The diabetes autoantigen ICA69 and its Caenorhabditis elegans homologue, ric-19, are conserved regulators of neuroendocrine secretion. Mol. Biol. Cell 11, 3277-3288.
43. Pöpperl, H., Bienz, M., Studer, M., Chan, S. K., Aparicio, S., Brenner, S., Mann, R. S. and Krumlauf, R. (1995). Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81, 1031-1042.
44. Rand, J. B. and Nonet, M. L. (1997). Synaptic transmission. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), pp. 611-643. Plainview, NY: Cold Spring Harbor Laboratory Press.
45. Romano, L. A. and Wray, G. A. (2003). Conservation of Endo16 expression in sea urchins despite evolutionary divergence in both cis and trans-acting components of transcriptional regulation. Development 130, 4187-4199.
46. Ronshaugen, M., McGinnis, N. and McGinnis, W. (2002). Hox protein mutation and macroevolution of the insect body plan. Nature 415, 914-917.
47. Satterlee, J. S., Sasakura, H., Kuhara, A., Berkeley, M., Mori, I. and Sengupta, P. (2001). Specification of thermosensory neuron fate in C. elegans requires ttx-1, a homolog of otd/Otx. Neuron 31, 943-956.
48. Scott, K., Brady, R. Jr, Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C. and Axel, R. (2001). A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673.
49. Shaw, P. J., Wratten, N. S., McGregor, A. P. and Dover, G. A. (2002). Coevolution in bicoid-dependent promoters and the inception of regulatory incompatibilities among species of higher Diptera. Evol. Dev. 4, 265-277.
50. Skaer, N. and Simpson, P. (2000). Genetic analysis of bristle loss in hybrids between Drosophila melanogaster and D. simulans provides evidence for divergence of cis-regulatory sequences in the achaete-scute gene complex. Dev. Biol. 221, 148-167.
51. Stone, J. R. and Wray, G. A. (2001). Rapid evolution of cis-regulatory sequences via local point mutations. Mol. Biol. Evol. 18, 1764-1770.
52. Streit, A., Kohler, R., Marty, T., Belfiore, M., Takacs-Vellai, K., Vigano, M. A., Schnabel, R., Affolter, M. and Muller, F. (2002). Conserved regulation of the Caenorhabditis elegans labial/Hox1 gene ceh-13. Dev. Biol. 242, 96-108.
53. Sucena, E. and Stern, D. L. (2000). Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc. Natl. Acad. Sci. USA 97, 4530-4534.
54. Svendsen, P. C. and McGhee, J. D. (1995). The C. elegans neuronally expressed homeobox gene ceh-10 is closely related to genes expressed in the vertebrate eye. Development 121, 1253-1262.
55. Takahashi, H., Mitani, Y., Satoh, G. and Satoh, N. (1999). Evolutionary alterations of the minimal promoter for notochord-specific Brachyury expression in ascidian embryos. Development 126, 3725-3734.
56. Tjian, R. and Maniatis, T. (1994). Transcriptional activation: a complex puzzle with few easy pieces. Cell 77, 5-8.
57. True, J. R. and Haag, E. S. (2001). Developmental system drift and flexibility in evolutionary trajectories. Evol. Dev. 3, 109-119.
58. Vorbruggen, G., Constien, R., Zilian, O., Wimmer, E. A., Dowe, G., Taubert, H., Noll, M. and Jackle, H. (1997). Embryonic expression and characterization of a Ptx1 homolog in Drosophila. Mech. Dev. 68, 139-147.
59. Vosshall, L. B., Wong, A. M. and Axel, R. (2000). An olfactory sensory map in the fly brain. Cell 102, 147-159.
60. Walker, R. G., Willingham, A. T. and Zuker, C. S. (2000). A Drosophila mechanosensory transduction channel. Science 287, 2229-2234.
61. Webb, C. T., Shabalina, S. A., Ogurtsov, A. Y. and Kondrashov, A. S. (2002). Analysis of similarity within 142 pairs of orthologous intergenic regions of Caenorhabditis elegans and Caenorhabditis briggsae. Nucleic Acids Res. 30, 1233-1239.
62. Westmoreland, J. J., McEwen, J., Moore, B. A., Jin, Y. and Condie, B. G. (2001). Conserved function of Caenorhabditis elegans UNC-30 and mouse Pitx2 in controlling GABAergic neuron differentiation. J Neurosci. 21, 6810-6819.
63. White, J. G., Southgate, E., Thomson, J. N. and Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314, 1-340.
64. Wilson, A. C., Maxson, L. R. and Sarich, V. M. (1974). Two types of molecular evolution. Evidence from studies of interspecific hybridization. Proc. Natl. Acad. Sci. USA 71, 2843-2847.
65. Xu, P. X., Zhang, X., Heaney, S., Yoon, A., Michelson, A. M. and Maas, R. L. (1999). Regulation of Pax6 expression is conserved between mice and flies. Development 126, 383-395.
66. Yin, Z., Xu, X. L. and Frasch, M. (1997). Regulation of the twist target gene tinman by modular cis-regulatory elements during early mesoderm development. Development 124, 4971-4982.
67. Zhao, H. and Nonet, M. L. (2001). A conserved mechanism of synaptogyrin localization. Mol. Biol. Cell 12, 2275-2289.
68. Zimmerman, J. E., Bui, Q. T., Liu, H. and Bonini, N. M. (2000). Molecular genetic analysis of Drosophila eyes absent mutants reveals an eye enhancer element. Genetics 154, 237-246.