The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons

Development

Volumn 126, Issue 7, 1999, Pages 1547-1562

  Hubert, Oliver ^a,b   Tessmar, Kristin ^a   Ruvkun, Gary ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

Axogenesis; Caenorhabditis elegans; GABA; LIM homeobox; Uterus

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE DECARBOXYLASE;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; DEVELOPMENTAL GENETICS; EMBRYO; EYE DEVELOPMENT; HOMEOBOX; INTERNEURON; KIDNEY DEVELOPMENT; LIMB DEVELOPMENT; MOTONEURON; MUSCLE CONTRACTION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, HELMINTH; GENES, HOMEOBOX; GENES, REPORTER; GLUTAMATE DECARBOXYLASE; HOMEODOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NERVOUS SYSTEM; NEURITES; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; CAENORHABDITIS ELEGANS; INVERTEBRATA; MAMMALIA; NEMATODA;

EID: 0032913942     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (74)

1. Avery, L. and Thomas, J. H. (1997). Feeding and defecation. In C. elegans II, (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), pp. 679-716. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
2. Bargmann, C. I. and Horvitz, H. R. (1991). Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7, 729-742.
3. Bargmann, C. I. and Kaplan, J. M. (1998). Signal transduction in the Caenorhabditis elegans nervous system. Ann. Rev. Neurosci. 21, 279-308.
4. Basson, M. and Horvitz, H. R. (1996). The Caenorhabditis elegans gene sem-4 controls neuronal and mesodermal cell development and encodes a zinc finger protein. Genes Dev. 10, 1953-1965.
5. Benveniste, R. J., Thor, S., Thomas, J. B. and Taghert, P. H. (1998). Cell type-specific regulation of the Drosophila FMRF-NH2 neuropeptide gene by Apterous, a LIM homeodomain transcription factor. Development 125, 4757-4765.
6. Bredt, D. S. (1998). Sorting out genes that regulate epithelial and neuronal polarity. Cell 94, 691-4.
7. Chalfie, M., Sulston, J. E., White, J. G., Southgate, E., Thomson, J. N. and Brenner, S. (1985). The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5, 956-964.
8. Chamberlin, H. M., Palmer, R. E., Newman, A. P., Sternberg, P. W., Baillie, D. L. and Thomas, J. H. (1997). The PAX gene egl-38 mediates developmental patterning in Caenorhabditis elegans. Development 124, 3919-3928.
9. Chen, H., Lun, Y., Ovchinnikov, D., Kokubo, H., Oberg, K. C., Pepicelli, C. V., Gan, L., Lee, B. and Johnson, R. L. (1998). Limb and kidney detects in Lmxlb mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nut. Genet. 19, 51-55.
10. Chen, H., Ovchinnikov, D., Pressman, C. L., Aulehla, A., Lun, Y. and Johnson, R. L. (1998). Multiple calvarial defects in Imx1b mutant mice. Dev. Genet. 22, 314-320.
11. Coburn, C. M. and Bargmann, C. I. (1996). A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17, 695-706.
12. Coburn, C. M., Mori, I., Ohshima, Y. and Bargmann, C. I. (1998). A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure. Development 125, 249-258.
13. Dahm, L. M. and Landmesser, L. T. (1988). The regulation of intramuscular nerve branching during normal development and following activity blockade. Dev. Biol. 130, 621-644.
14. Dahm, L. M. and Landmesser, L. T. (1991). The regulation of synaptogenesis during normal development and following activity blockade. J. Neurosci. 11, 238-255.
15. Dawid, I. B., Breen, J. J. and Toyama, R. (1998). LIM domains: multiple roles as adapters and functional modifiers in protein interactions. Trends Genet. 14, 156-162.
16. Dreyer, S. D., Zhou, G., Baldini, A., Winterpacht, A., Zabel, B., Cole, W., Johnson, R. L. and Lee, B. (1998). Mutations in LMX1B cause abnormal skeletal patterning and renal dysplasia in nail patella syndrome. Nat. Genet. 19, 47-50.
17. Duret, L., Guex, N., Peitsch, M. C. and Bairoch, A. (1998). New insulin-like proteins with atypical disulfide bond pattern characterized in Caenorhabditis elegans by comparative sequence analysis and homology modeling. Genome Res. 8, 348-353.
18. Freyd, G. (1991). Molecular analysis of the Caenorhabditis elegans cell lineage gene lin-11. Cambridge, MA: Massachusetts Institute of Technology.
19. 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, 876-9.
20. German, M. S., Wang, J., Chadwick, R. B. and Rutter, W. J. (1992). Synergistic activation of the insulin gene by a LIM-homeo domain protein and a basic helix-loop-helix protein: building a functional insulin minienhancer complex. Genes Dev. 6, 2165-2176.
21. Granato, M., Schnabel, H. and Schnabel, R. (1994). pha- 1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res. 22, 1762-3.
22. Grider, J. R. and Makhlouf, G. M. (1992). Enteric GABA: mode of action and role in the regulation of the peristaltic reflex. Am. J. Physiol. 262, G690-694.
23. Gu, X. H., Kurose, T., Kato, S., Masuda, K., Tsuda, K., Ishida, H. and Seino, Y. (1993). Suppressive effect of GABA on insulin secretion from the pancreatic beta-cells in the rat. Life Sci. 52, 687-694.
24. Hart, A. C., Sims, S. and Kaplan, J. M. (1995). Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378, 82-85.
25. Hedgecock, E. M., Culotti, J. G., Hall, D. H. and Stern, B. D. (1987). Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100, 365-382.
26. Hobert, 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, 2084-2096.
27. Hobert, O., Mori, I., Yamashita, Y., Honda, H., Ohshima, Y., Liu, Y. and Ruvkun, G. (1997). Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19, 3453-3457.
28. Iannotti, C. A., Inoue, H., Bernai, E., Aoki, M., Liu, L., Donis-Keller, H., German, M. S. and Permutt, M. A. (1997). Identification of a human LMX1 (LMX1.1)-related gene, LMX1.2: tissue- specific expression and linkage mapping on chromosome 9. Genomics 46, 520-524.
29. Jansen, G., Hazendonk, E., Thijssen, K. L. and Plasterk, R. H. (1997). Reverse genetics by chemical mutagenesis in Caenorhabditis elegans. Nat. Genet. 17, 119-121.
30. Jessen, K. R., Hills, J. M. and Saffrey, M. J. (1986). Immunohistochemical demonstration of GABAergic neurons in the enteric nervous system. J. Neurosci. 6, 1628-1634.
31. Jin, Y., Hoskins, R. and Horvitz, H. R. (1994). Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature 372, 780-783.
32. Jin, Y., Jorgensen, E., Hartwieg, E. and Horvitz, H. R. (1999). The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J. Neurosci. 19, in press.
33. Kimura, K. D., Tissenbaum, H. A., Liu, Y. and Ruvkun, G. (1997). daf- 2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans [see comments]. Science 277, 942-946.
34. Liu, D. W. and Thomas, J. H. (1994). Regulation of a periodic motor program in C. elegans. J. Neurosci. 14, 1953-1962.
35. 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.
36. Manak, J. R., and Scott, M. P. (1994). A class act: conservation of homeodomain protein functions. Development Supplement 61-77.
37. Matise, M. P., and Joyner, A. L. (1997). Expression patterns of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveal early diversity in developing interneurons. J. Neurosci. 17, 7805-7816.
38. McIntire, S.L., Garriga, G., White, J., Jacobson, D. and Horvitz, H.R. (1992). Genes necessary for directed axonal elongation or fasciculation in C.elegans. Neuron 8, 307-322.
39. McIntire, S. L., Jorgensen, E. and Horvitz, H. R. (1993a). Genes required for GABA function in Caenorhabditis elegans [see comments]. Nature 364, 334-337.
40. McIntire, S. L., Jorgensen, E., Kaplan, J. and Horvitz, H. R. (1993b). The GABAergic nervous system of Caenorhabditis elegans [see comments]. Nature 364, 337-341.
41. McIntire, S. L., Reimer, R. J., Schuske, K., Edwards, R. H. and Jorgensen, E. M. (1997). Identification and characterization of the vesicular GABA transporter. Nature 389, 870-876.
42. Miller, C. and Sassoon, D. A. (1998). Wnt-7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract. Development 125, 3201-32311.
43. Miller, D. M., Shen, M. M., Shamu, C. E., Burglin, T. R., Ruvkun, G., Dubois, M. L., Ghee, M. and Wilson, L. (1992). C. elegans unc-4 gene encodes a homeodomain protein that determines the pattern of synaptic input to specific motor neurons. Nature 355, 841-845.
44. Mori, I. and Ohshima, Y. (1995). Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376, 344-348.
45. Nelson, F. K., Albert, P. S. and Riddle, D. L. (1983). Fine structure of the Caenorhabditis elegans secretory-excretory system. J. Ultrastruct. Res. 82, 156-171.
46. Nelson, F. K. and Riddle, D. L. (1984). Functional study of the Caenorhabditis elegans secretory-excretory system using laser microsurgery. J. Exp. Zool. 231, 45-56.
47. Newman, A. P., White, J. G. and Sternberg, P. W. (1996). Morphogenesis of the C. elegans hermaphrodite uterus. Development 122, 3617-3626.
48. Ogg, S., Paradis, S., Gottlieb, S., Patterson, G. I., Lee, L., Tissenbaum, H. A. and Ruvkun, G. (1997). The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994-999.
49. Pfaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T. and Jessell, T. M. (1996). Requirement for LIM homeobox gene Is11 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320.
50. Porter, F. D., Drago, J., Xu, Y., Cheema, S. S., Wassif, C., Huang, S. P., Lee, E., Grinberg, 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.
51. Ren, P., Lim, C. S., Johnsen, R., Albert, P. S., Pilgrim, D. and Riddle, D. L. (1996). Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274, 1389-1391.
52. Riddle, D. L. and Albert, P. S. (1997). Genetic and Environmental Regulation of Dauer Larva Development. In C.elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), pp. 739-768. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
53. Riddle, R. D., Ensini, M., Nelson, C., Tsuchida, T., Jessell, T. M. and Tabin, C. (1995). Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 83, 631-640.
54. Rongo, C., Whitfield, C. W., Rodal, A., Kim, S. K. and Kaplan, J. M. (1998). LIN-10 is a shared component of the polarized protein localization pathways in neurons and epithelia. Cell 94, 751-759.
55. Ruvkun, G. and Hobert, O. (1998). The Taxonomy of Developmental Control in Caenorhabditis elegans. Science 282, 2033-2041.
56. Sanders, K. M. (1996). A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111, 492-515.
57. Sawa, H., Lobel, L. and Horvitz, H. R. (1996). The Caenorhabditis elegans gene lin-17, which is required for certain asymmetric cell divisions, encodes a putative seven-transmembrane protein similar to the Drosophila frizzled protein. Genes Dev. 10, 2189-2197.
58. Schinkmann, K. and Li, C. (1992). Localization of FMRFamide-like peptides in Caenorhabditis elegans. J. Comp. Neurol. 316, 251-260.
59. Sharma, K., Sheng, H. Z., Lettieri, K., Li, H., Karavanov, A., Potter, S., Westphal, H. and Pfaff, S. L. (1998). LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95, 817-828.
60. Shatz, C. J. and Stryker, M. P. (1988). Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242, 87-89.
61. Sorenson, R. L., Garry, D. G. and Brelje, T. C. (1991). Structural and functional considerations of GABA in islets of Langerhans, beta-cells and nerves. Diabetes 40, 1365-1374.
62. Sulston, J. E. (1983). Neuronal cell lineages in the nematode Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 48, 443-452.
63. Thomas, J. H. (1990). Genetic analysis of defecation in Caenorhabditis elegans. Genetics 124, 855-872.
64. Thor, S. and Thomas, J. B. (1997). The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 18, 397-409.
65. Thor, S., Andersson, S.G.E., Tomlinson, A. and Thomas, J.B. (1999). A LIM-homeodomain combinatorial code for motor neuron pathway selection. Nature 397, 76-80.
66. 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 [see comments]. Cell 79, 957-970.
67. Vogel, A., Rodriguez, C., Warnken, W. and Izpisua Belmonte, J. C. (1995). Dorsal cell fate specified by chick Lmx1 during vertebrate limb development [published erratum appears in Nature 1996 Feb 29;379(6568):848]. Nature 378, 716-720.
68. Wadsworth, W. G., Bhatt, H. and Hedgecock, E. M. (1996). Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16, 35-46.
69. Way, J. C. and Chalfie, M. (1989). The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev. 3, 1823-33.
70. Way, J. C., and Chalfie, M. (1988). mec- 3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54, 5-16.
71. White, J. G., Southgate, E., and Thomson, J. N. (1992). Mutations in the Caenorhabditis elegans unc-4 gene alter the synaptic input to ventral cord motor neurons. Nature 355, 838-41.
72. White, J. G., Southgate, E., Thomson, J. N., and Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. Royal Soc. London B. 314, 1-340.
73. Yu, S., Avery, L., Baude, E., and Garbers, D. L. (1997). Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc. Natl. Acad. Sci. USA 94, 3384-7.
74. Zhou, H. M., and Walthall, W. W. (1998). UNC-55, an orphan nuclear hormone receptor, orchestrates synaptic specificity among two classes of motor neurons in Caenorhabditis elegans. J. Neurosci. 18, 10438-10444.