egl-4 Acts Through a Transforming Growth Factor-β/SMAD Pathway in Caenorhabditis elegans to Regulate Multiple Neuronal Circuits in Response to Sensory Cues

Genetics - Tập 156 Số 1 - Trang 123-141 - 2000
Susan A. Daniels1, Michael Ailion2, James H. Thomas3,2, Piali Sengupta1
1Department of Biology and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454
2Molecular and Cellular Biology Program of the University of Washington and Fred Hutchinson Cancer Research Center
3Department of Genetics, University of Washington, Seattle, Washington, 98195

Tóm tắt

Abstract

Sensory cues regulate several aspects of behavior and development in Caenorhabditis elegans, including entry into and exit from an alternative developmental stage called the dauer larva. Three parallel pathways, including a TGF-β-like pathway, regulate dauer formation. The mechanisms by which the activities of these pathways are regulated by sensory signals are largely unknown. The gene egl-4 was initially identified based on its egg-laying defects. We show here that egl-4 has many pleiotropies, including defects in chemosensory behavior, body size, synaptic transmission, and dauer formation. Our results are consistent with a role for egl-4 in relaying sensory cues to multiple behavioral and developmental circuits in C. elegans. By epistasis analysis, we also place egl-4 in the TGF-β-like branch and show that a SMAD gene functions downstream of egl-4 in multiple egl-4-regulated pathways, including chemosensation.

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Tài liệu tham khảo

Ailion, 2000, Dauer formation induced by high temperatures in Caenorhabditis elegans, Genetics, 156

Ailion, 1999, Neurosecretory control of aging in Caenorhabditis elegans, Proc. Natl. Acad. Sci. USA, 96, 7394, 10.1073/pnas.96.13.7394

Albert, 1981, Sensory control of dauer larva formation in Caenorhabditis elegans, J. Comp. Neurol., 198, 435, 10.1002/cne.901980305

Alfonso, 1993, The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter, Science, 261, 617, 10.1126/science.8342028

Alfonso, 1994, Cloning and characterization of the choline acetyltransferase structural gene (cha-1) from C. elegans, J. Neurosci., 14, 2290, 10.1523/JNEUROSCI.14-04-02290.1994

Ann, 1997, Novel Ca2+-binding protein (CAPS) related to UNC-31 required for Ca2+-activated exocytosis, J. Biol. Chem., 272, 19637, 10.1074/jbc.272.32.19637

Antebi, 1998, daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans, Development, 125, 1191, 10.1242/dev.125.7.1191

Apfeld, 1999, Regulation of lifespan by sensory perception in Caenorhabditis elegans, Nature, 402, 804, 10.1038/45544

Avery, 1990, Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans, J. Exp. Zool., 253, 263, 10.1002/jez.1402530305

Avery, 1993, The Caenorhabditis elegans unc-31 gene affects multiple nervous system-controlled functions, Genetics, 134, 455, 10.1093/genetics/134.2.455

Bargmann, 1991, Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans, Neuron, 7, 729, 10.1016/0896-6273(91)90276-6

Bargmann, 1991, Control of larval development by chemosensory neurons in Caenorhabditis elegans, Science, 251, 1243, 10.1126/science.2006412

Bargmann, 1990, Chemosensory cell function in the behavior and development of Caenorhabditis elegans, Cold Spring Harbor Symp. Quant. Biol., LV, 529, 10.1101/SQB.1990.055.01.051

Bargmann, 1993, Odorant-selective genes and neurons mediate olfaction in C. elegans, Cell, 74, 515, 10.1016/0092-8674(93)80053-H

Birnby, 2000, A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in C. elegans, Genetics, 155, 85, 10.1093/genetics/155.1.85

Brenner, 1974, The genetics of Caenorhabditis elegans, Genetics, 77, 71, 10.1093/genetics/77.1.71

Chalfie, 1985, The neural circuit for touch sensitivity in Caenorhabditis elegans, J. Neurosci., 5, 956, 10.1523/JNEUROSCI.05-04-00956.1985

Coburn, 1996, A putative cyclic nucleotidegated channel is required for sensory development and function in C. elegans, Neuron, 17, 695, 10.1016/S0896-6273(00)80201-9

Coburn, 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, 10.1242/dev.125.2.249

Colbert, 1995, Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans, Neuron, 14, 803, 10.1016/0896-6273(95)90224-4

Colbert, 1997, OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans, J. Neurosci., 17, 8259, 10.1523/JNEUROSCI.17-21-08259.1997

Desai, 1988, A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons, Nature, 336, 638, 10.1038/336638a0

Driscoll, 1997, Mechanotransduction, C. elegans II, 645

Duerr, 1999, The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors, J. Neurosci., 19, 72, 10.1523/JNEUROSCI.19-01-00072.1999

Dusenbery, 1974, Analysis of chemotaxis in the nematode Caenorhabditis elegans by countercurrent separation, J. Exp. Zool., 188, 41, 10.1002/jez.1401880105

Estevez, 1993, The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development, Nature, 365, 644, 10.1038/365644a0

Fleming, 1997, Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits, J. Neurosci., 17, 5843, 10.1523/JNEUROSCI.17-15-05843.1997

Georgi, 1990, daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase, Cell, 61, 635, 10.1016/0092-8674(90)90475-T

Gil, 1999, Regulation of the insulin-like developmental pathway of Caenorhabditis elegans by a homolog of the PTEN tumor suppressor gene, Proc. Natl. Acad. Sci. USA, 96, 2925, 10.1073/pnas.96.6.2925

Golden, 1982, A pheromone influences larval development in the nematode Caenorhabditis elegans, Science, 218, 578, 10.1126/science.6896933

Golden, 1984, The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature, Dev. Biol., 102, 368, 10.1016/0012-1606(84)90201-X

Golden, 1984, A pheromone-induced developmental switch in Caenorhabditis elegans: temperature-sensitive mutants reveal a wild-type temperature-dependent process, Proc. Natl. Acad. Sci. USA, 81, 819, 10.1073/pnas.81.3.819

Golden, 1985, A gene affecting production of the Caenorhabditis elegans dauer-inducing pheromone, Mol. Gen. Genet., 198, 534, 10.1007/BF00332953

Gottlieb, 1994, daf-2, daf-16 and daf-23: genetically interacting genes controlling dauer formation in Caenorhabditis elegans, Genetics, 137, 107, 10.1093/genetics/137.1.107

Hart, 1995, Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor, Nature, 378, 82, 10.1038/378082a0

Herman, 1990, Limitation of the size of the vulval primordium of Caenorhabditis elegans by lin-15 expression in surrounding hypodermis, Nature, 348, 169, 10.1038/348169a0

Horvitz, 1982, Serotonin and octopamine in the nematode Caenorhabditis elegans, Science, 216, 1012, 10.1126/science.6805073

Inoue, 2000, Targets of TGF-β signaling in Caenorhabditis elegans dauer formation, Dev. Biol., 217, 192, 10.1006/dbio.1999.9545

Jansen, 1999, The complete family of genes encoding G proteins of Caenorhabditis elegans, Nat. Genet., 21, 414, 10.1038/7753

Kaplan, 1993, A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans, Proc. Natl. Acad. Sci. USA, 90, 2227, 10.1073/pnas.90.6.2227

Kenyon, 1993, A C. elegans mutant that lives twice as long as wild type, Nature, 366, 461, 10.1038/366461a0

Kimura, 1997, daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans, Science, 277, 942, 10.1126/science.277.5328.942

Koga, 1999, Control of DAF-7 TGF-β expression and neuronal process development by a receptor tyrosine kinase KIN-8 in Caenorhabditis elegans, Development, 126, 5387, 10.1242/dev.126.23.5387

Komatsu, 1996, Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans, Neuron, 17, 707, 10.1016/S0896-6273(00)80202-0

Lackner, 1999, Facilitation of synaptic transmission by EGL-30 Gqα and EGL-8 PLCβ: DAG binding to UNC-13 is required to stimulate acetylcholine release, Neuron, 24, 335, 10.1016/S0896-6273(00)80848-X

Larsen, 1995, Genes that regulate both development and longevity in Caenorhabditis elegans, Genetics, 139, 1567, 10.1093/genetics/139.4.1567

Lewis, 1977, Specific neuroanatomical changes in chemosensory mutants of the nematode Caenorhabditis elegans, J. Comp. Neurol., 172, 489, 10.1002/cne.901720306

Lewis, 1980, The genetics of levamisole resistance in the nematode Caenorhabditis elegans, Genetics, 95, 905, 10.1093/genetics/95.4.905

Lewis, 1980, Levamisole-resistant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors, Neuroscience, 5, 967, 10.1016/0306-4522(80)90180-3

Lin, 1997, daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans, Science, 278, 1319, 10.1126/science.278.5341.1319

Liu, 1994, Regulation of a periodic motor program in C. elegans, J. Neurosci., 14, 1953, 10.1523/JNEUROSCI.14-04-01953.1994

Livingstone D , 1991  Studies on the unc-31 gene of Caenorhabditis elegans. Ph.D. Dissertation, University of Cambridge.

Loer, 1993, Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans, J. Neurosci., 13, 5407, 10.1523/JNEUROSCI.13-12-05407.1993

Maricq, 1995, Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor, Nature, 378, 78, 10.1038/378078a0

Miller, 1996, A genetic selection for Caenorhabditis elegans synaptic transmission mutants, Proc. Natl. Acad. Sci. USA, 93, 12593, 10.1073/pnas.93.22.12593

Miller, 1999, Goα and diacylglycerol kinase negatively regulate the Gqα pathway in C. elegans, Neuron, 24, 323, 10.1016/S0896-6273(00)80847-8

Mori, 1995, Neural regulation of thermotaxis in Caenorhabditis elegans, Nature, 376, 344, 10.1038/376344a0

Morris, 1996, A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans, Nature, 382, 536, 10.1038/382536a0

Nguyen, 1995, Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase, Genetics, 140, 527, 10.1093/genetics/140.2.527

Nurrish, 1999, Serotonin inhibition of synaptic transmission: Gα(0) decreases the abundance of UNC-13 at release sites, Neuron, 24, 231, 10.1016/S0896-6273(00)80835-1

Ogawa, 1998, Functional properties of the unc-64 gene encoding a Caenorhabditis elegans syntaxin, J. Biol. Chem., 273, 2192, 10.1074/jbc.273.4.2192

Ogg, 1998, The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway, Mol. Cell, 2, 887, 10.1016/S1097-2765(00)80303-2

Ogg, 1997, The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans, Nature, 389, 994, 10.1038/40194

Padgett, 1998, TGF-β signaling, Smads, and tumor suppressors, Bioessays, 20, 382, 10.1002/(SICI)1521-1878(199805)20:5<382::AID-BIES5>3.0.CO;2-Q

Paradis, 1999, A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans, Genes Dev., 13, 1438, 10.1101/gad.13.11.1438

Patterson, 2000, TGF β-related pathways. Roles in Caenorhabditis elegans development, Trends Genet., 16, 27, 10.1016/S0168-9525(99)01916-2

Patterson, 1997, The DAF-3 Smad protein antagonizes TGF-β-related receptor signaling in the Caenorhabditis elegans dauer pathway, Genes Dev., 11, 2679, 10.1101/gad.11.20.2679

Perkins, 1986, Mutant sensory cilia in the nematode Caenorhabditis elegans, Dev. Biol., 117, 456, 10.1016/0012-1606(86)90314-3

Prasad, 1998, unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors, Development, 125, 1561, 10.1242/dev.125.8.1561

Ren, 1996, Control of C. elegans larval development by neuronal expression of a TGF-β homolog, Science, 274, 1389, 10.1126/science.274.5291.1389

Riddle, 1997, Genetic and environmental regulation of dauer larva development, C. elegans II, 739

Riddle, 1981, Interacting genes in nematode dauer larva formation, Nature, 290, 668, 10.1038/290668a0

Roayaie, 1998, The Gα protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons, Neuron, 20, 55, 10.1016/S0896-6273(00)80434-1

Rouault, 1999, Regulation of dauer larva development in Caenorhabditis elegans by daf-18, a homologue of the tumour suppressor PTEN, Curr. Biol., 9, 329, 10.1016/S0960-9822(99)80143-2

Saifee, 1998, The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin, Mol. Biol. Cell, 9, 1235, 10.1091/mbc.9.6.1235

Savage, 1996, Caenorhabditis elegans genes sma-2, sma-3, and sma-4 define a conserved family of transforming growth factor beta pathway components, Proc. Natl. Acad. Sci. USA, 93, 790, 10.1073/pnas.93.2.790

Schackwitz, 1996, Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans, Neuron, 17, 719, 10.1016/S0896-6273(00)80203-2

Schinkmann, 1992, Localization of FMRFamide-like peptides in Caenorhabditis elegans, J. Comp. Neurol., 316, 251, 10.1002/cne.903160209

Sengupta, 1994, The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily, Cell, 79, 971, 10.1016/0092-8674(94)90028-0

Sengupta, 1996, odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl, Cell, 84, 899, 10.1016/S0092-8674(00)81068-5

Starich, 1995, Mutations affecting the chemosensory neurons of Caenorhabditis elegans, Genetics, 139, 171, 10.1093/genetics/139.1.171

Suzuki, 1999, A BMP homolog acts as a dose-dependent regulator of body size and male tail patterning in Caenorhabditis elegans, Development, 126, 241, 10.1242/dev.126.2.241

Sze, 2000, Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant, Nature, 403, 560, 10.1038/35000609

Thatcher, 1999, The DAF-3 Smad binds DNA and represses gene expression in the Caenorhabditis elegans pharynx, Development, 126, 97, 10.1242/dev.126.1.97

Thomas, 1990, Genetic analysis of defecation in Caenorhabditis elegans, Genetics, 124, 855, 10.1093/genetics/124.4.855

Thomas, 1993, Chemosensory regulation of development in C. elegans, Bioessays, 15, 791, 10.1002/bies.950151204

Thomas, 1993, Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans, Genetics, 134, 1105, 10.1093/genetics/134.4.1105

Tissenbaum, 2000, A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum, Proc. Natl. Acad. Sci. USA, 97, 460, 10.1073/pnas.97.1.460

Trent, 1983, Egg-laying defective mutants of the nematode Caenorhabditis elegans, Genetics, 104, 619, 10.1093/genetics/104.4.619

Troemel, 1999, Chemosensory signaling in C. elegans, Bioessays, 21, 1011, 10.1002/(SICI)1521-1878(199912)22:1<1011::AID-BIES5>3.0.CO;2-V

Troemel, 1995, Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans, Cell, 83, 207, 10.1016/0092-8674(95)90162-0

Troemel, 1997, Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans, Cell, 91, 161, 10.1016/S0092-8674(00)80399-2

Troemel, 1999, Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans, Cell, 99, 387, 10.1016/S0092-8674(00)81525-1

Vowels, 1992, Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans, Genetics, 130, 105, 10.1093/genetics/130.1.105

Vowels, 1994, Multiple chemosensory defects in daf-11 and daf-21 mutants of Caenorhabditis elegans, Genetics, 138, 303, 10.1093/genetics/138.2.303

Waggoner, 1998, Control of alternative behavioral states by serotonin in Caenorhabditis elegans, Neuron, 21, 203, 10.1016/S0896-6273(00)80527-9

Waggoner, 2000, Effect of a neuropeptide gene on behavioral states in Caenorhabditis elegans egg-laying, Genetics, 154, 1181, 10.1093/genetics/154.3.1181

Ward, 1973, Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants, Proc. Natl. Acad. Sci. USA, 70, 817, 10.1073/pnas.70.3.817

Weinshenker, 1995, Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans, J. Neurosci., 15, 6975, 10.1523/JNEUROSCI.15-10-06975.1995

White, 1986, The structure of the nervous system of the nematode Caenorhabditis elegans, Philos. Trans. R. Soc. Lond. Ser. B, 314, 1, 10.1098/rstb.1986.0056

Zwaal, 1997, Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans dauer-inducing pheromone, Genetics, 145, 715, 10.1093/genetics/145.3.715