Function and specificity of LIM domains in Drosophila nervous system and wing development

Development

Volumn 125, Issue 19, 1998, Pages 3915-3923

  O'Keefe, David D ^a   Thor, Stefan ^b   Thomas, John B ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Development; Drosophila melanogaster; Homeodomain; LIM domain; Nervous system

Indexed keywords

HOMEODOMAIN PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; FORELIMB; LIMB DEVELOPMENT; MUTANT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION;

ALLELES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; GENES, INSECT; HOMEODOMAIN PROTEINS; INSECT PROTEINS; MALE; MUTATION; NERVOUS SYSTEM; PHENOTYPE; TRANSCRIPTION FACTORS; WING;

ANIMALIA; DROSOPHILA MELANOGASTER; HEXAPODA; MELANOGASTER;

EID: 0031767937     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Agulnick, A. D., Taira, M., Breen, J. J., Tanaka, T., Dawid, I. B. and Westphal, H. (1996). Interactions of the LIM-domain-binding factor Lbd1 with LIM homeodomain proteins. Nature 384, 270-272.
2. Altartz, M., Applebaum, S. W., Richard, D. S., Gilbert, L. I. and Segal, D. (1991). Regulation of juvenile hormone synthesis in wild-type and ap mutant Drosophila. Mol. Cell. Endocrinol 81, 205-216.
3. Appel, B., Korzh, V., Glasgow, E., Thor, S., Edlund, T., Dawid, I. B. and Eisen, J. S. (1995). Motorneuron fate specification revealed by patterned LIM honieobox gene expression in embryonic zebrafish. Development 121, 4117-4125.
4. Arber, S. and Caroni, P. (1996). Specificity of single LIM motifs in targeting and LIM/LIM interactions in situ. Genes Dev. 10, 289-300.
5. Archer, V. E. V., Breton, J., Sanchez-Garcia, I., Osada, H., Forster, A., Thomson, A. J. and Rabbitts. T. H. (1994). Cysteine-rich LIM domains of LIM-homeodomain and LIM-only proteins contain zinc but not iron. Proc. Natl. Acad. Sci. USA 91, 316-320.
6. Bach, I., Carriere, C., Ostendorff, H. P., Andersen, B. and Rosenfeld, M. G. (1997). A family of LIM domain-associated cofactors confer transcriptional synergism betwwn LIM and Otx homeodomain proteins. Genes Dev. 11, 1370-1380.
7. Bach, I., Rhodes, S. J., Pearse, R. V. I., Heinzel, T., Gloss, B., Scully, K. M., Sawchenko, P. E. and Rosenfeld, M. G. (1995). P-Lim. a LIM homeodomain factor, is expressed during pituitary organ and cell commitment and synergizes with Pit-1. Proc. Natl. Acad. Sci. USA 92, 2720-2724.
8. Blair, S. S., Brower, D. L., Thomas, J. B. and Zavortink, M. (1994). The role of apterous in the control of doroventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120, 1805-1815.
9. Bourgouin, C., Lundgren, S. E. and Thomas, J. B. (1992). apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9, 549-561.
10. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
11. Butterworth, F. M. and King, R. C. (1965). The developmental genetics of ap mutants of Drosophila melanogaster. Genetics 52, 1153-1174.
12. Callahan, C. A., Bonkovsky, J. L., Scully, A. L. and Thomas, J. B. (1996). derailed is required for muscle attachment site selection in Drosophila, Development 122, 2761-2767.
13. Callahan, C. A. and Thomas, J. B. (1994). Tau-β-gulactosidase. an axontargeted fusion protein. Proc. Natl. Acad. Sci. USA 91, 5972-5976.
14. Calleja, M., Moreno, E., Pelaz, S. and Morata, G. (1996). Visualization of Gene Expression in Living Adult Drosophila. Science 274, 252-255.
15. Cohen, B., McGuffin, M. E., Pfeifle, C., Segal, D. and Cohen, S. M. (1992). apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genex Dev. 6, 715-729.
16. Copeland, J. W. R., Nasiadka, A., Dietrich, B. H. and Krause, H. M. (1996). Patterning of the Drosophila embryo by a homeodomain-deleted Ftz polypeptide. Nature 379, 162-165.
17. Curtiss, J. and Heilig, J. S. (1997). Arrowhead Encodes a LIM Homeodomain Protein That Distinguishes Subsets of Drosophila Imaginal Cells. Dev. Biol. 190, 129-141.
18. Diaz-Benjumea, F. J. and Cohen, S. M. (1993). Interaction between dorsal and ventral cells in the imaginai disc directs wing development in Drosophila. Cell 75, 741-752.
19. Ericson, J., Thor, S., Edlund, T., Jessell, T. M. and Yamada, T. (1992). Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-60.
20. Freyd, G., Kim, S. K. and Horvitz, H. R. (1990). Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11 Nature 344, 876-879.
21. German, M. S., Wang, J., Chadwick, R. B. and Rutter, W. J. (1992). Synergistic activation of the insulin gene by a LIM-homeo protein and a basic helix-loop-helix protein: building a functional insulin minienhancer complex. Genes Dev. 6, 2165-2176.
22. Guichet, A., Copeland, J. W. R., Erdelyl, M., Hlousek, D., Zavorszky, P., Ho, J., Brown, S., Percival-Smith, A., Krause, H. M. and Ephrussi, A. (1997). The nuclear receptor homologue Ftz-F1 and the homeodomain protein Ftz are mutually dependent cotactors. Nature 385, 548-552.
23. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. and Pease, L. R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
24. Hubert, O., D'Alberti, T., Liu, Y. and Ruvkun, G. (1998). Control of neural development and function in a thermoregulatory network by the LIM homeobox gene lin-11. J. Neurosci 18, 2084-96.
25. Hobert, O., Mori, I., Yamashita, Y., Honda, H., Ohshima, Y., Lui, Y. and Ruvkun, G. (1997). Regulation of Interneuron Function in the c. elegans Thermoregulatory Pathway by the ttx-3 LIM Homeobox Gene. Neuron 19, 345-357.
26. Hoey, T. and Levine, M. (1988). Divergent homeo box proteins recognize similar DNA sequences in Drosophila. Nature 332, 858-861.
27. Johnson, J. D., Zhang, W., Rudnick, A., Rutter, W. J. and German, M. S. (1997). Transcriptional Synergy between LIM-Homeodomain Proteins and Basic Helix-Loop-Helix Proteins: the LIM2 Domain Determines Specificity. Mol. Cell. Biol. 17, 3488-3496.
28. Jurata, L. W. and Gill, G. N. (1997). Functional analysis of the nuclear LIM domain interactor NLI. Mol. Cell. Biol. 17, 5688-5698.
29. Jurata, L. W. and Gill, G. N. (1998). Structure and Function of LIM Domains. Curr. Top. Microbiol. Immunol. 228, 75-113.
30. Jurata, L. W., Kenny, D. A. and Gill, G. N. (1996). Nuclear LIM Interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. Proc. Natl. Acad. Sci. USA 93, 11693-11698.
31. Jurata, L. W., Pfaff, S. L. and Gill, G. N. (1998). The nuclear LIM domain interactor NLI mediates homo- and heterodimerization of LIM domain transcription factors. J. Biol. Chem. 273, 3152-7.
32. Kalionis, B. and O'Farrell, P. H. (1993). A universal target sequence is bound in vitro by diverse homeodomains. Mech. Dev. 43, 57-70.
33. Karlsson, O., Thor, S., Norberg, T., Ohlsson, H. and Edlund, T. (1990). Insulin gene binding protein Is1-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature 344, 879-882.
34. Kikuchi, Y., Segawa, H., Tokumoto, M., Tsubokawa, T., Hotta, Y., Uyemura, K. and Okamoto, H. (1997). Ocular and Cerebellar Defects in Zebratish Induced by Overexpression of the LIM Domains of the Islet-3 LIM/Homeodomain Protein. Neuron 18, 369-382.
35. Klämbt, C., Jacobs, J. R. and Goodman, C. S. (1991). The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64, 801-815.
36. Lin, D. M., Auld, V.J. and Goodman, C. S. (1995). Targeted neuronal ablation in the Drosophila embryo: pathfinding by follower growth cones in the absence of pioneers. Neuron 14, 707-715.
37. Lundgren, S. E., Callahan, C. A., Thor, S. and Thomas, J. B. (1995). Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development 121, 1769-1773.
38. Marchuk, D., Drumm, M., Saulino, A. and Collins, F. S. (1990). Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nuc. Acids Res. 19, 1154.
39. Matsumoto, K., Tanaka, T., Furuyama, T., Kashihara, Y., Ishii, N., Tohyama, M., Kitanaka, J., Takemura, M., Mori, T. and Wanaka, A. (1996). Differential expression of LIM-homeodomain genes in the embryonic murine brain. Neurosci Lett. 211, 147-150.
40. Michelsen, J. W., Schmeichel, K. L., Beckerle, M. C. and Winge, D. R. (1993). The LIM motif defines a specific zinc-binding protein domain. Proc. Natl. Acad. Sci. USA 90, 4404-4408.
41. Morcillo, P., Rosen, C., Baylies, M. K. and Dorsett, D. (1997). Chip, a widely expressed chromosomal protein required for segmentation and activity of a remote wing margin enhancer in Drosophila. Genes Dev. 11, 2729-2740.
42. Pfaff, S. L., Mendelsohn, C. L., Stewart, C. L., Edlund, T. and Jessell, T. M. (1996). Requirement for LIM Homeobox Gene lsl-1 in Motor Neuron Generation Reveals a Motor Neuron-Dependent Step in Interneuron Differentiation. Cell 84, 309-320.
43. Porter, F. D., Drago, J., Xu, Y., Cheema, S. S., Wassif, C., Huang, S., Lee, E., Grin berg, A., Massalas, J. S., Bodine, D., Alt, F. and Westphal, H. (1997). Lhx2, a LIM homeobox gene, is required for eye, forebrain, and definitive erythrocyte development. Development 124, 2935-2944.
44. Rubin, G. M. and Spradling, A. C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
45. Sanchez-Garcia, I., Osada, H., Forster, A. and Rabbitts, T. H. (1993). The cysteine-rich LIM domains inhibit DNA binding by the associated homeodomain in Isl-1. EMBO J. 12, 4243-4250.
46. Schmeichel, K. L. and Beckerle, M. C. (1994). The LIM Domain Is a Modular Protein-Binding Interface. Cell 79, 211-219.
47. Shawlot, W. and Behringer, R. R. (1995). Requirement for Lim I in headorganizer function. Nature 374, 425-430.
48. Sheng, H. Z., Moriyama, K., Yamashita, T., Li, H., Potter, S. S., Mahon, K. A. and Westphal, H. (1997). Multistep control of pituitary organogenesis. Science 278, 1809-1812.
49. Sheng, H. Z., Zhadanov, A. B., Mosinger, B. J., Fuji, T., Bertuzzi, S., Grinberg, A., Lee, E. J., Huang, S., Mahon, K. A. and Westphal, H. (1996). Specification of pituitary cell lineages by the LIM homeobox gene Lhx3. Science 272, 1004-1007.
50. Staehling-Hampton, K., Hoffmann, F. M., Baylies, M. K., Rushton, E. and Bate, M. (1994). dpp induces mesodermal gene expression in Drosophila. Nature 372, 783-786.
51. Taira, M., Otani, H., Saint-Jeannet, J. and Dawid, I. B. (1994). Role of the LIM class homeodomain protein Xlim-1 in neural and muscle induction by the Spemann organizer in Xenopus. Nature 372, 677-679.
52. Taira, M., Saint-Jeannet, J. and Dawid, I. (1997). Role of the Xlim-1 and Xbra genes in anteroposterior patterning of neural tissue by the head and trunk organizer. Proc. Natl. Acad. Sci. USA 94, 895-900.
53. Thor, S. and Thomas, J. B. (1997). The Drosophila islet gene governs axon pathfinding and neurostrunsmitter identity. Neuron 18, 1-20.
54. Toyama, R., Kobayashi, M., Tomita, T. and Dawid, I. B. (1998). Expression of LIM-domain binding proteins (ldb) genes during zebrafish embryogenesis, Mech. Dev. 71, 197-200.
55. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
56. Varela-Echavarria, A., Pfaff, S. L. and Guthrie, S. (1996). Differential Expression of LIM Homeobox Genes among Motor Neuron Surpopulations in the Developing Chick Brain Stem. Mol. Cell. Neurosci. 8, 242-257.
57. Vogel, A., Rodriguez, C., Warnken, W. and Belmonte, J. C. I. (1995). Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature 378, 716-720.
58. Way, J. C. and Chalfie, M. (1988). mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegant. Cell 54, 5-16.
59. Way, J. C. and Chalfie, M. (1989). The mec-3 hene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev. 3, 1823-1833.
60. Wilson, T. G. (1981). Expression of phenotypes in a temperature-sensitive allele of the apterous mutation in Drosophila melanogaster. Dev. Biol. 85, 425-433.
61. Xue, D., Tu, Y. and Chalfie, M. (1993). Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science 261, 1324-1328.
62. Yu, Y., Li, W., Su, K., Yussa, M., Han, W., Perrimon, N. and Pick, L. (1997). The nuclear hormone receptor Ftz-F1 is a cofactor for the Drosophila homeodomain protein Ftz. Nature 385, 552-555.
63. Zelzer, E., Wappner P. and Shilo, B. (1997). The PAS domain confers target gene specificity of Drosophila bHLH-PAS proteins. Cenex Dev. 11, 2079-2089.