C. elegans G Protein Regulator RGS-3 Controls Sensitivity to Sensory Stimuli

Neuron

Volumn 53, Issue 1, 2007, Pages 39-52

  Ferkey, Denise M ^a,b   Hyde, Rhonda ^a,b   Haspel, Gal ^a,b   Dionne, Heather M ^a,b   Hess, Heather A ^c   Suzuki, Hiroshi ^d   Schafer, William R ^d   Koelle, Michael R ^e   Hart, Anne C ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e YALE UNIVERSITY   (United States)

Author keywords

CELLBIO; MOLNEURO; SIGNALING

Indexed keywords

CALCIUM BINDING PROTEIN; DOPAMINE; G PROTEIN COUPLED RECEPTOR;

ANIMAL CELL; ARTICLE; BEHAVIOR DISORDER; CAENORHABDITIS ELEGANS; CALCIUM BLOOD LEVEL; CALCIUM SIGNALING; DOWN REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SENSORY ANALYSIS; SENSORY NERVE CELL; SENSORY STIMULATION; SIGNAL TRANSDUCTION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; CALCIUM SIGNALING; GLUTAMIC ACID; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; MUTATION; NERVOUS SYSTEM; RECEPTORS, G-PROTEIN-COUPLED; RGS PROTEINS; SENSATION; SIGNAL TRANSDUCTION; SMELL; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33845713709     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.11.015     Document Type: Article

References (70)

1. Avery L., and Horvitz H.R. Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J. Exp. Zool. 253 (1990) 263-270
2. Bargmann C.I. Neurobiology of the Caenorhabditis elegans genome. Science 282 (1998) 2028-2033
3. Bargmann C.I., Thomas J.H., and Horvitz H.R. Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 55 (1990) 529-538
4. Bargmann C.I., Hartwieg E., and Horvitz H.R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74 (1993) 515-527
5. Bellocchio E.E., Reimer R.J., Fremeau Jr. R.T., and Edwards R.H. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289 (2000) 957-960
6. Berger A.J., Hart A.C., and Kaplan J.M. Gαs-induced neurodegeneration in Caenorhabditis elegans. J. Neurosci. 18 (1998) 2871-2880
7. Birnby D.A., Link E.M., Vowels J.J., Tian H., Colacurcio P.L., and Thomas J.H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155 (2000) 85-104
8. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
9. Brockie P.J., Madsen D.M., Zheng Y., Mellem J., and Maricq A.V. Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J. Neurosci. 21 (2001) 1510-1522
10. Chao M.Y., Komatsu H., Fukuto H.S., Dionne H.M., and Hart A.C. Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit. Proc. Natl. Acad. Sci. USA 101 (2004) 15512-15517
11. Chase D.L., Pepper J.S., and Koelle M.R. Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat. Neurosci. 7 (2004) 1096-1103
12. Chen C.K., Burns M.E., He W., Wensel T.G., Baylor D.A., and Simon M.I. Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature 403 (2000) 557-560
13. Coburn C.M., and Bargmann C.I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17 (1996) 695-706
14. Colbert H.A., Smith T.L., and Bargmann C.I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J. Neurosci. 17 (1997) 8259-8269
15. Cuppen E., van der Linden A.M., Jansen G., and Plasterk R.H. Proteins interacting with Caenorhabditis elegans Gα subunits. Comp. Funct. Genomics 4 (2003) 479-491
16. Dong M.Q., Chase D., Patikoglou G.A., and Koelle M.R. Multiple RGS proteins alter neural G protein signaling to allow C. elegans to rapidly change behavior when fed. Genes Dev. 14 (2000) 2003-2014
17. Fukuto H.S., Ferkey D.M., Apicella A.J., Lans H., Sharmeen T., Chen W., Lefkowitz R.J., Jansen G., Schafer W.R., and Hart A.C. G protein-coupled receptor kinase function is essential for chemosensation in C. elegans. Neuron 42 (2004) 581-593
18. Guerrero G., Reiff D.F., Agarwal G., Ball R.W., Borst A., Goodman C.S., and Isacoff E.Y. Heterogeneity in synaptic transmission along a Drosophila larval motor axon. Nat. Neurosci. 8 (2005) 1188-1196
19. Hart A.C., Sims S., and Kaplan J.M. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378 (1995) 82-85
20. Hart A.C., Kass J., Shapiro J.E., and Kaplan J.M. Distinct signaling pathways mediate touch and osmosensory responses in a polymodal sensory neuron. J. Neurosci. 19 (1999) 1952-1958
21. Hess H.A., Roper J.C., Grill S.W., and Koelle M.R. RGS-7 completes a receptor-independent heterotrimeric G protein cycle to asymmetrically regulate mitotic spindle positioning in C. elegans. Cell 119 (2004) 209-218
22. Hilliard M.A., Bergamasco C., Arbucci S., Plasterk R.H., and Bazzicalupo P. Worms taste bitter: ASH neurons, QUI-1, GPA-3 and ODR-3 mediate quinine avoidance in Caenorhabditis elegans. EMBO J. 23 (2004) 1101-1111
23. Hilliard M.A., Apicella A.J., Kerr R., Suzuki H., Bazzicalupo P., and Schafer W.R. In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. EMBO J. 24 (2005) 63-72
24. Hills T., Brockie P.J., and Maricq A.V. Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J. Neurosci. 24 (2004) 1217-1225
25. Hollinger S., and Hepler J.R. Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol. Rev. 54 (2002) 527-559
26. Horvitz H.R., Chalfie M., Trent C., Sulston J.E., and Evans P.D. Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216 (1982) 1012-1014
27. Jansen G., Thijssen K.L., Werner P., van der Horst M., Hazendonk E., and Plasterk R.H. The complete family of genes encoding G proteins of Caenorhabditis elegans. Nat. Genet. 21 (1999) 414-419
28. Kahn-Kirby A.H., Dantzker J.L., Apicella A.J., Schafer W.R., Browse J., Bargmann C.I., and Watts J.L. Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell 119 (2004) 889-900
29. Kaplan J.M., and Horvitz H.R. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 90 (1993) 2227-2231
30. Kass J., Jacob T.C., Kim P., and Kaplan J.M. The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. J. Neurosci. 21 (2001) 9265-9272
31. Komatsu H., Mori I., Rhee J.S., Akaike N., and Ohshima Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17 (1996) 707-718
32. Kuhara A., Inada H., Katsura I., and Mori I. Negative regulation and gain control of sensory neurons by the C. elegans calcineurin TAX-6. Neuron 33 (2002) 751-763
33. Kunitomo H., Uesugi H., Kohara Y., and Iino Y. Identification of ciliated sensory neuron-expressed genes in Caenorhabditis elegans using targeted pull-down of poly(A) tails. Genome Biol. 6 (2005) R17
34. Lans H., Rademakers S., and Jansen G. A network of stimulatory and inhibitory Gα-subunits regulates olfaction in Caenorhabditis elegans. Genetics 167 (2004) 1677-1687
35. Lee R.Y., Sawin E.R., Chalfie M., Horvitz H.R., and Avery L. EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans. J. Neurosci. 19 (1999) 159-167
36. L'Etoile N.D., and Bargmann C.I. Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. Neuron 25 (2000) 575-586
37. Lints R., and Emmons S.W. Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFbeta family signaling pathway and a Hox gene. Development 126 (1999) 5819-5831
38. Luo X., Popov S., Bera A.K., Wilkie T.M., and Muallem S. RGS proteins provide biochemical control of agonist-evoked [Ca2+]i oscillations. Mol. Cell 7 (2001) 651-660
39. Maricq A.V., Peckol E., Driscoll M., and Bargmann C.I. Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378 (1995) 78-81
40. Mellem J.E., Brockie P.J., Zheng Y., Madsen D.M., and Maricq A.V. Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans. Neuron 36 (2002) 933-944
41. 2+ based on green fluorescent proteins and calmodulin. Nature 388 (1997) 882-887
42. Miyawaki A., Griesbeck O., Heim R., and Tsien R.Y. Dynamic and quantitative Ca2+ measurements using improved cameleons. Proc. Natl. Acad. Sci. USA 96 (1999) 2135-2140
43. Neer E.J. Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80 (1995) 249-257
44. 2+ entry at the gate. Pflugers Arch. 451 (2005) 181-192
45. Nishiguchi K.M., Sandberg M.A., Kooijman A.C., Martemyanov K.A., Pott J.W., Hagstrom S.A., Arshavsky V.Y., Berson E.L., and Dryja T.P. Defects in RGS9 or its anchor protein R9AP in patients with slow photoreceptor deactivation. Nature 427 (2004) 75-78
46. Nuttley W.M., Harbinder S., and van der Kooy D. Regulation of distinct attractive and aversive mechanisms mediating benzaldehyde chemotaxis in Caenorhabditis elegans. Learn. Mem. 8 (2001) 170-181
47. 2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem. Biol. 13 (2006) 521-530
48. Prasad B.C., and Reed R.R. Chemosensation: molecular mechanisms in worms and mammals. Trends Genet. 15 (1999) 150-153
49. Rios M., Habecker B., Sasaoka T., Eisenhofer G., Tian H., Landis S., Chikaraishi D., and Roffler-Tarlov S. Catecholamine synthesis is mediated by tyrosinase in the absence of tyrosine hydroxylase. J. Neurosci. 19 (1999) 3519-3526
50. Roayaie K., Crump J.G., Sagasti A., and Bargmann C.I. The Gα protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron 20 (1998) 55-67
51. Ross E.M., and Wilkie T.M. GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu. Rev. Biochem. 69 (2000) 795-827
52. Saitoh O., Kubo Y., Miyatani Y., Asano T., and Nakata H. RGS8 accelerates G-protein-mediated modulation of K+ currents. Nature 390 (1997) 525-529
53. Sanyal S., Wintle R.F., Kindt K.S., Nuttley W.M., Arvan R., Fitzmaurice P., Bigras E., Merz D.C., Hebert T.E., van der Kooy D., et al. Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. EMBO J. 23 (2004) 473-482
54. Sawin E.R., Ranganathan R., and Horvitz H.R. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26 (2000) 619-631
55. Schafer W.R., and Kenyon C.J. A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375 (1995) 73-78
56. Ségalat L., Elkes D.A., and Kaplan J.M. Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science 267 (1995) 1648-1651
57. Siderovski D.P., and Willard F.S. The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int. J. Biol. Sci. 1 (2005) 51-66
58. Sinnarajah S., Dessauer C.W., Srikumar D., Chen J., Yuen J., Yilma S., Dennis J.C., Morrison E.E., Vodyanoy V., and Kehrl J.H. RGS2 regulates signal transduction in olfactory neurons by attenuating activation of adenylyl cyclase III. Nature 409 (2001) 1051-1055
59. Stringham E.G., Dixon D.K., Jones D., and Candido E.P. Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol. Biol. Cell 3 (1992) 221-233
60. Suzuki H., Kerr R., Bianchi L., Frokjaer-Jensen C., Slone D., Xue J., Gerstbrein B., Driscoll M., and Schafer W.R. In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 39 (2003) 1005-1017
61. Takamori S., Rhee J.S., Rosenmund C., and Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407 (2000) 189-194
62. 2+. Cell Calcium 32 (2002) 321-334
63. Tobin D., Madsen D., Kahn-Kirby A., Peckol E., Moulder G., Barstead R., Maricq A., and Bargmann C. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35 (2002) 307-318
64. Troemel E.R. Chemosensory signaling in C. elegans. Bioessays 21 (1999) 1011-1020
65. Troemel E.R., Chou J.H., Dwyer N.D., Colbert H.A., and Bargmann C.I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83 (1995) 207-218
66. Vazquez G., Wedel B.J., Aziz O., Trebak M., and Putney Jr. J.W. The mammalian TRPC cation channels. Biochim. Biophys. Acta 1742 (2004) 21-36
67. Weinshenker D., Garriga G., and Thomas J.H. Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans. J. Neurosci. 15 (1995) 6975-6985
68. White J.G., Southgate E., Thomson J.N., and Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314 (1986) 1-340
69. 2+-binding proteins in the functional regulation of TRP channels. Pflugers Arch. 451 (2005) 105-115
70. Zwaal R.R., Mendel J.E., Sternberg P.W., and Plasterk R.H. Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans Dauer-inducing pheromone. Genetics 145 (1997) 715-727