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-beta-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-beta-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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- Ailion M., Inoue T., Weaver C. I., Holdcraft R. W., Thomas J. H. Neurosecretory control of aging in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7394–7397. doi: 10.1073/pnas.96.13.7394. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Albert P. S., Brown S. J., Riddle D. L. Sensory control of dauer larva formation in Caenorhabditis elegans. J Comp Neurol. 1981 May 20;198(3):435–451. doi: 10.1002/cne.901980305. [DOI] [PubMed] [Google Scholar]
- Alfonso A., Grundahl K., Duerr J. S., Han H. P., Rand J. B. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science. 1993 Jul 30;261(5121):617–619. doi: 10.1126/science.8342028. [DOI] [PubMed] [Google Scholar]
- Alfonso A., Grundahl K., McManus J. R., Rand J. B. Cloning and characterization of the choline acetyltransferase structural gene (cha-1) from C. elegans. J Neurosci. 1994 Apr;14(4):2290–2300. doi: 10.1523/JNEUROSCI.14-04-02290.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ann K., Kowalchyk J. A., Loyet K. M., Martin T. F. Novel Ca2+-binding protein (CAPS) related to UNC-31 required for Ca2+-activated exocytosis. J Biol Chem. 1997 Aug 8;272(32):19637–19640. doi: 10.1074/jbc.272.32.19637. [DOI] [PubMed] [Google Scholar]
- Antebi A., Culotti J. G., Hedgecock E. M. daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans. Development. 1998 Apr;125(7):1191–1205. doi: 10.1242/dev.125.7.1191. [DOI] [PubMed] [Google Scholar]
- Apfeld J., Kenyon C. Regulation of lifespan by sensory perception in Caenorhabditis elegans. Nature. 1999 Dec 16;402(6763):804–809. doi: 10.1038/45544. [DOI] [PubMed] [Google Scholar]
- Avery L., Bargmann C. I., Horvitz H. R. The Caenorhabditis elegans unc-31 gene affects multiple nervous system-controlled functions. Genetics. 1993 Jun;134(2):455–464. doi: 10.1093/genetics/134.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Avery L., Horvitz H. R. Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J Exp Zool. 1990 Mar;253(3):263–270. doi: 10.1002/jez.1402530305. [DOI] [PubMed] [Google Scholar]
- Bargmann C. I., Hartwieg E., Horvitz H. R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell. 1993 Aug 13;74(3):515–527. doi: 10.1016/0092-8674(93)80053-h. [DOI] [PubMed] [Google Scholar]
- Bargmann C. I., Horvitz H. R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron. 1991 Nov;7(5):729–742. doi: 10.1016/0896-6273(91)90276-6. [DOI] [PubMed] [Google Scholar]
- Bargmann C. I., Horvitz H. R. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science. 1991 Mar 8;251(4998):1243–1246. doi: 10.1126/science.2006412. [DOI] [PubMed] [Google Scholar]
- Bargmann C. I., Thomas J. H., Horvitz H. R. Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol. 1990;55:529–538. doi: 10.1101/sqb.1990.055.01.051. [DOI] [PubMed] [Google Scholar]
- Birnby D. A., Link E. M., Vowels J. J., Tian H., Colacurcio P. L., Thomas J. H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in caenorhabditis elegans. Genetics. 2000 May;155(1):85–104. doi: 10.1093/genetics/155.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chalfie M., Sulston J. E., White J. G., Southgate E., Thomson J. N., Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci. 1985 Apr;5(4):956–964. doi: 10.1523/JNEUROSCI.05-04-00956.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coburn C. M., Bargmann C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron. 1996 Oct;17(4):695–706. doi: 10.1016/s0896-6273(00)80201-9. [DOI] [PubMed] [Google Scholar]
- Coburn C. M., Mori I., Ohshima Y., Bargmann C. I. 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. 1998 Jan;125(2):249–258. doi: 10.1242/dev.125.2.249. [DOI] [PubMed] [Google Scholar]
- Colbert H. A., Bargmann C. I. Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron. 1995 Apr;14(4):803–812. doi: 10.1016/0896-6273(95)90224-4. [DOI] [PubMed] [Google Scholar]
- Desai C., Garriga G., McIntire S. L., Horvitz H. R. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature. 1988 Dec 15;336(6200):638–646. doi: 10.1038/336638a0. [DOI] [PubMed] [Google Scholar]
- Duerr J. S., Frisby D. L., Gaskin J., Duke A., Asermely K., Huddleston D., Eiden L. E., Rand J. B. The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J Neurosci. 1999 Jan 1;19(1):72–84. doi: 10.1523/JNEUROSCI.19-01-00072.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dusenbery D. B. Analysis of chemotaxis in the nematode Caenorhabditis elegans by countercurrent separation. J Exp Zool. 1974 Apr;188(1):41–47. doi: 10.1002/jez.1401880105. [DOI] [PubMed] [Google Scholar]
- Estevez M., Attisano L., Wrana J. L., Albert P. S., Massagué J., Riddle D. L. The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development. Nature. 1993 Oct 14;365(6447):644–649. doi: 10.1038/365644a0. [DOI] [PubMed] [Google Scholar]
- Fleming J. T., Squire M. D., Barnes T. M., Tornoe C., Matsuda K., Ahnn J., Fire A., Sulston J. E., Barnard E. A., Sattelle D. B. Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J Neurosci. 1997 Aug 1;17(15):5843–5857. doi: 10.1523/JNEUROSCI.17-15-05843.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Georgi L. L., Albert P. S., Riddle D. L. daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell. 1990 May 18;61(4):635–645. doi: 10.1016/0092-8674(90)90475-t. [DOI] [PubMed] [Google Scholar]
- Gil E. B., Malone Link E., Liu L. X., Johnson C. D., Lees J. A. Regulation of the insulin-like developmental pathway of Caenorhabditis elegans by a homolog of the PTEN tumor suppressor gene. Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2925–2930. doi: 10.1073/pnas.96.6.2925. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Golden J. W., Riddle D. L. A pheromone influences larval development in the nematode Caenorhabditis elegans. Science. 1982 Nov 5;218(4572):578–580. doi: 10.1126/science.6896933. [DOI] [PubMed] [Google Scholar]
- Golden J. W., Riddle D. L. A pheromone-induced developmental switch in Caenorhabditis elegans: Temperature-sensitive mutants reveal a wild-type temperature-dependent process. Proc Natl Acad Sci U S A. 1984 Feb;81(3):819–823. doi: 10.1073/pnas.81.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Golden J. W., Riddle D. L. The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev Biol. 1984 Apr;102(2):368–378. doi: 10.1016/0012-1606(84)90201-x. [DOI] [PubMed] [Google Scholar]
- Gottlieb S., Ruvkun G. daf-2, daf-16 and daf-23: genetically interacting genes controlling Dauer formation in Caenorhabditis elegans. Genetics. 1994 May;137(1):107–120. doi: 10.1093/genetics/137.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herman R. K., Hedgecock E. M. Limitation of the size of the vulval primordium of Caenorhabditis elegans by lin-15 expression in surrounding hypodermis. Nature. 1990 Nov 8;348(6297):169–171. doi: 10.1038/348169a0. [DOI] [PubMed] [Google Scholar]
- Horvitz H. R., Chalfie M., Trent C., Sulston J. E., Evans P. D. Serotonin and octopamine in the nematode Caenorhabditis elegans. Science. 1982 May 28;216(4549):1012–1014. doi: 10.1126/science.6805073. [DOI] [PubMed] [Google Scholar]
- Jansen G., Thijssen K. L., Werner P., van der Horst M., Hazendonk E., Plasterk R. H. The complete family of genes encoding G proteins of Caenorhabditis elegans. Nat Genet. 1999 Apr;21(4):414–419. doi: 10.1038/7753. [DOI] [PubMed] [Google Scholar]
- Kaplan J. M., Horvitz H. R. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2227–2231. doi: 10.1073/pnas.90.6.2227. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kenyon C., Chang J., Gensch E., Rudner A., Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature. 1993 Dec 2;366(6454):461–464. doi: 10.1038/366461a0. [DOI] [PubMed] [Google Scholar]
- Kimura K. D., Tissenbaum H. A., Liu Y., Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science. 1997 Aug 15;277(5328):942–946. doi: 10.1126/science.277.5328.942. [DOI] [PubMed] [Google Scholar]
- Koga M., Take-uchi M., Tameishi T., Ohshima Y. Control of DAF-7 TGF-(alpha) expression and neuronal process development by a receptor tyrosine kinase KIN-8 in Caenorhabditis elegans. Development. 1999 Dec;126(23):5387–5398. doi: 10.1242/dev.126.23.5387. [DOI] [PubMed] [Google Scholar]
- Komatsu H., Mori I., Rhee J. S., Akaike N., Ohshima Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron. 1996 Oct;17(4):707–718. doi: 10.1016/s0896-6273(00)80202-0. [DOI] [PubMed] [Google Scholar]
- Lackner M. R., Nurrish S. J., Kaplan J. M. Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron. 1999 Oct;24(2):335–346. doi: 10.1016/s0896-6273(00)80848-x. [DOI] [PubMed] [Google Scholar]
- Larsen P. L., Albert P. S., Riddle D. L. Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics. 1995 Apr;139(4):1567–1583. doi: 10.1093/genetics/139.4.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewis J. A., Hodgkin J. A. Specific neuroanatomical changes in chemosensory mutants of the nematode Caenorhabditis elegans. J Comp Neurol. 1977 Apr 1;172(3):489–510. doi: 10.1002/cne.901720306. [DOI] [PubMed] [Google Scholar]
- Lewis J. A., Wu C. H., Berg H., Levine J. H. The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics. 1980 Aug;95(4):905–928. doi: 10.1093/genetics/95.4.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewis J. A., Wu C. H., Levine J. H., Berg H. Levamisole-resistant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors. Neuroscience. 1980;5(6):967–989. doi: 10.1016/0306-4522(80)90180-3. [DOI] [PubMed] [Google Scholar]
- Lin K., Dorman J. B., Rodan A., Kenyon C. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science. 1997 Nov 14;278(5341):1319–1322. doi: 10.1126/science.278.5341.1319. [DOI] [PubMed] [Google Scholar]
- Liu D. W., Thomas J. H. Regulation of a periodic motor program in C. elegans. J Neurosci. 1994 Apr;14(4):1953–1962. doi: 10.1523/JNEUROSCI.14-04-01953.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loer C. M., Kenyon C. J. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J Neurosci. 1993 Dec;13(12):5407–5417. doi: 10.1523/JNEUROSCI.13-12-05407.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maricq A. V., Peckol E., Driscoll M., Bargmann C. I. Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature. 1995 Nov 2;378(6552):78–81. doi: 10.1038/378078a0. [DOI] [PubMed] [Google Scholar]
- Miller K. G., Alfonso A., Nguyen M., Crowell J. A., Johnson C. D., Rand J. B. A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12593–12598. doi: 10.1073/pnas.93.22.12593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller K. G., Emerson M. D., Rand J. B. Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron. 1999 Oct;24(2):323–333. doi: 10.1016/s0896-6273(00)80847-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mori I., Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature. 1995 Jul 27;376(6538):344–348. doi: 10.1038/376344a0. [DOI] [PubMed] [Google Scholar]
- Morris J. Z., Tissenbaum H. A., Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature. 1996 Aug 8;382(6591):536–539. doi: 10.1038/382536a0. [DOI] [PubMed] [Google Scholar]
- Nurrish S., Ségalat L., Kaplan J. M. Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron. 1999 Sep;24(1):231–242. doi: 10.1016/s0896-6273(00)80835-1. [DOI] [PubMed] [Google Scholar]
- Ogawa H., Harada S., Sassa T., Yamamoto H., Hosono R. Functional properties of the unc-64 gene encoding a Caenorhabditis elegans syntaxin. J Biol Chem. 1998 Jan 23;273(4):2192–2198. doi: 10.1074/jbc.273.4.2192. [DOI] [PubMed] [Google Scholar]
- Ogg S., Paradis S., Gottlieb S., Patterson G. I., Lee L., Tissenbaum H. A., Ruvkun G. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature. 1997 Oct 30;389(6654):994–999. doi: 10.1038/40194. [DOI] [PubMed] [Google Scholar]
- Ogg S., Ruvkun G. The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Mol Cell. 1998 Dec;2(6):887–893. doi: 10.1016/s1097-2765(00)80303-2. [DOI] [PubMed] [Google Scholar]
- Padgett R. W., Das P., Krishna S. TGF-beta signaling, Smads, and tumor suppressors. Bioessays. 1998 May;20(5):382–390. doi: 10.1002/(SICI)1521-1878(199805)20:5<382::AID-BIES5>3.0.CO;2-Q. [DOI] [PubMed] [Google Scholar]
- Paradis S., Ailion M., Toker A., Thomas J. H., Ruvkun G. A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev. 1999 Jun 1;13(11):1438–1452. doi: 10.1101/gad.13.11.1438. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patterson G. I., Koweek A., Wong A., Liu Y., Ruvkun G. The DAF-3 Smad protein antagonizes TGF-beta-related receptor signaling in the Caenorhabditis elegans dauer pathway. Genes Dev. 1997 Oct 15;11(20):2679–2690. doi: 10.1101/gad.11.20.2679. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patterson G. I., Padgett R. W. TGF beta-related pathways. Roles in Caenorhabditis elegans development. Trends Genet. 2000 Jan;16(1):27–33. doi: 10.1016/s0168-9525(99)01916-2. [DOI] [PubMed] [Google Scholar]
- Perkins L. A., Hedgecock E. M., Thomson J. N., Culotti J. G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol. 1986 Oct;117(2):456–487. doi: 10.1016/0012-1606(86)90314-3. [DOI] [PubMed] [Google Scholar]
- Prasad B. C., Ye B., Zackhary R., Schrader K., Seydoux G., Reed R. R. unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors. Development. 1998 Apr;125(8):1561–1568. doi: 10.1242/dev.125.8.1561. [DOI] [PubMed] [Google Scholar]
- Ren P., Lim C. S., Johnsen R., Albert P. S., Pilgrim D., Riddle D. L. Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science. 1996 Nov 22;274(5291):1389–1391. doi: 10.1126/science.274.5291.1389. [DOI] [PubMed] [Google Scholar]
- Riddle D. L., Swanson M. M., Albert P. S. Interacting genes in nematode dauer larva formation. Nature. 1981 Apr 23;290(5808):668–671. doi: 10.1038/290668a0. [DOI] [PubMed] [Google Scholar]
- Roayaie K., Crump J. G., Sagasti A., Bargmann C. I. The G alpha protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron. 1998 Jan;20(1):55–67. doi: 10.1016/s0896-6273(00)80434-1. [DOI] [PubMed] [Google Scholar]
- Rouault J. P., Kuwabara P. E., Sinilnikova O. M., Duret L., Thierry-Mieg D., Billaud M. Regulation of dauer larva development in Caenorhabditis elegans by daf-18, a homologue of the tumour suppressor PTEN. Curr Biol. 1999 Mar 25;9(6):329–332. doi: 10.1016/s0960-9822(99)80143-2. [DOI] [PubMed] [Google Scholar]
- Saifee O., Wei L., Nonet M. L. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol Biol Cell. 1998 Jun;9(6):1235–1252. doi: 10.1091/mbc.9.6.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Savage C., Das P., Finelli A. L., Townsend S. R., Sun C. Y., Baird S. E., Padgett R. W. 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 U S A. 1996 Jan 23;93(2):790–794. doi: 10.1073/pnas.93.2.790. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schackwitz W. S., Inoue T., Thomas J. H. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron. 1996 Oct;17(4):719–728. doi: 10.1016/s0896-6273(00)80203-2. [DOI] [PubMed] [Google Scholar]
- Schinkmann K., Li C. Localization of FMRFamide-like peptides in Caenorhabditis elegans. J Comp Neurol. 1992 Feb 8;316(2):251–260. doi: 10.1002/cne.903160209. [DOI] [PubMed] [Google Scholar]
- Sengupta P., Chou J. H., Bargmann C. I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell. 1996 Mar 22;84(6):899–909. doi: 10.1016/s0092-8674(00)81068-5. [DOI] [PubMed] [Google Scholar]
- Smyth R. L., Fletcher J. N., Thomas H. M., Hart C. A., Openshaw P. J. Respiratory syncytial virus and wheeze. Lancet. 1999 Dec 4;354(9194):1997–1998. doi: 10.1016/s0140-6736(05)76769-6. [DOI] [PubMed] [Google Scholar]
- Starich T. A., Herman R. K., Kari C. K., Yeh W. H., Schackwitz W. S., Schuyler M. W., Collet J., Thomas J. H., Riddle D. L. Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics. 1995 Jan;139(1):171–188. doi: 10.1093/genetics/139.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Suzuki Y., Yandell M. D., Roy P. J., Krishna S., Savage-Dunn C., Ross R. M., Padgett R. W., Wood W. B. A BMP homolog acts as a dose-dependent regulator of body size and male tail patterning in Caenorhabditis elegans. Development. 1999 Jan;126(2):241–250. doi: 10.1242/dev.126.2.241. [DOI] [PubMed] [Google Scholar]
- Sze J. Y., Victor M., Loer C., Shi Y., Ruvkun G. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature. 2000 Feb 3;403(6769):560–564. doi: 10.1038/35000609. [DOI] [PubMed] [Google Scholar]
- Thatcher J. D., Haun C., Okkema P. G. The DAF-3 Smad binds DNA and represses gene expression in the Caenorhabditis elegans pharynx. Development. 1999 Jan;126(1):97–107. doi: 10.1242/dev.126.1.97. [DOI] [PubMed] [Google Scholar]
- Thomas J. H., Birnby D. A., Vowels J. J. Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans. Genetics. 1993 Aug;134(4):1105–1117. doi: 10.1093/genetics/134.4.1105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas J. H. Genetic analysis of defecation in Caenorhabditis elegans. Genetics. 1990 Apr;124(4):855–872. doi: 10.1093/genetics/124.4.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tissenbaum H. A., Hawdon J., Perregaux M., Hotez P., Guarente L., Ruvkun G. A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):460–465. doi: 10.1073/pnas.97.1.460. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Troemel E. R., Chou J. H., Dwyer N. D., Colbert H. A., Bargmann C. I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell. 1995 Oct 20;83(2):207–218. doi: 10.1016/0092-8674(95)90162-0. [DOI] [PubMed] [Google Scholar]
- Troemel E. R., Kimmel B. E., Bargmann C. I. Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell. 1997 Oct 17;91(2):161–169. doi: 10.1016/s0092-8674(00)80399-2. [DOI] [PubMed] [Google Scholar]
- Troemel E. R., Sagasti A., Bargmann C. I. Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell. 1999 Nov 12;99(4):387–398. doi: 10.1016/s0092-8674(00)81525-1. [DOI] [PubMed] [Google Scholar]
- Vowels J. J., Thomas J. H. Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics. 1992 Jan;130(1):105–123. doi: 10.1093/genetics/130.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vowels J. J., Thomas J. H. Multiple chemosensory defects in daf-11 and daf-21 mutants of Caenorhabditis elegans. Genetics. 1994 Oct;138(2):303–316. doi: 10.1093/genetics/138.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weinshenker D., Garriga G., Thomas J. H. Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J Neurosci. 1995 Oct;15(10):6975–6985. doi: 10.1523/JNEUROSCI.15-10-06975.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zwaal R. R., Mendel J. E., Sternberg P. W., Plasterk R. H. Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans Dauer-inducing pheromone. Genetics. 1997 Mar;145(3):715–727. doi: 10.1093/genetics/145.3.715. [DOI] [PMC free article] [PubMed] [Google Scholar]