TBX2/TBX3 Transcriptional Factor Homologue Controls Olfactory Adaptation in Caenorhabditis elegans

Journal of Neurobiology

Volumn 58, Issue 3, 2004, Pages 392-402

  Miyahara, Kohji ^a,b   Suzuki, Norio ^a,c,d   Ishihara, Takeshi ^a,c   Tsuchiya, Eiko ^b   Katsura, Isao ^a,c  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^d RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Adaptation; C. elegans; Odorant; T box; Transcriptional factor

Indexed keywords

T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX2; TRANSCRIPTION FACTOR TBX3; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; CAENORHABDITIS ELEGANS; CHEMOTAXIS; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENE EXPRESSION; MISSENSE MUTATION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PHARYNX; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SMELLING;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; CYTOPLASM; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NERVOUS SYSTEM; NEURONAL PLASTICITY; OLFACTORY RECEPTOR NEURONS; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SMELL; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS;

EID: 1042278119     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10299     Document Type: Article

References (55)

1. Agulnik SI, Bollag RJ, Silver LM. 1995. Conservation of the T-box gene family from Mus musculus to Caenorhabditis elegans. Genomics 25:214-219.
2. Anholt RRH. 1993. Molecular neurobiology of olfaction, Crit Rev Neurobiol 7:1-22.
3. Avery L, Bargmann CI, Horvitz HR. 1993. The Caenorhabditis elegans unc-31 gene affects multiple nervous system-controlled functions. Genetics 134:455-464.
4. Avery L, Horvitz HR. 1989. Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 3:473-485.
5. Bamshad M, Lin RC, Law DJ, Watkins WC, Krakowiak PA, Moore ME, Franceschini P, Lala R, Holmes LB, Gebuhr TC, et al. 1997. Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome. Nat Genet 16:311-315.
6. Bargmann CI, Hartwieg E, Horvitz HR. 1993. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515-527.
7. Boekhoff I, Inglese J, Schleicher S, Koch WJ, Lefkowitz RJ, Breer H. 1994. Olfactory desensitization requires membrane targeting of receptor kinase mediated by beta gamma-subunits of heterotrimeric G proteins. J Biol Chem 269:37-40.
8. Bollag RJ, Siegfried Z, Cebra-Thomas JA, Garvey N, Davison EM, Silver LM. 1994. An ancient family of embryonically expressed mouse genes sharing a conserved protein motif with the T locus. Nat Genet 7:383-389.
9. Bradley J, Reuter D, Frings S. 2001. Facilitation of calmodulin-mediated odor adaptation by cAMP-gated channel subunits. Science 294:2176-2178.
10. Carlson H, Ota S, Campbell CE, Hurlin PJ. 2001. A dominant repression domain in Tbx3 mediates transcriptional repression and cell immortalization: relevance to mutations in Tbx3 that cause ulnar-mammary syndrome. Hum Mol Genet 10:2403-2413.
11. Carreira S, Dexter TJ, Yavuzer U, Easty DJ, Goding CR. 1998. Brachyury-related transcription factor Tbx2 and repression of the melanocyte-specific TRP-1 promoter. Mol Cell Biol 18:5099-5108.
12. Casey ES, O'Reilly MA, Conlon FL, Smith JC. 1998. The T-box transcription factor Brachyury regulates expression of eFGF through binding to a non-palindromic response element. Development 125:3887-3894.
13. Chen Z, Yuhanna IS, Galcheva-Gargova Z, Karas RH, Mendelsohn ME, Shaul PW. 1999. Estrogen receptor alpha mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J Clin Invest 103:401-406.
14. Chess A, Simon I, Cedar H, Axel R. 1994. Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823-834.
15. Colbert HA, Bargmann CI. 1995. Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14:803-812.
16. Colbert HA, Smith TL, Bargmann CI. 1997. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17:8259-8269.
17. Dalton P, 2000. Psychophysical and behavioral characteristics of olfactory adaptation. Chem Senses 25:487-492.
18. Daniels SA, Ailion M, Thomas JH, Sengupta P. 2000. eg1-4 acts through a transforming growth factor-β/SMAD pathway in Caenorhabditis elegans to regulate multiple neuronal circuits in response to sensory cues. Genetics 156:123-141.
19. Fujiwara M, Sengupta P, McIntire SL. 2002. Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36:1091-1102.
20. Greenberg AE. 2001. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 98:11024-11031.
21. Heisenberg M, Wonneberger R, Wolf R. 1978. Optomotor-blind H31 - a Drosophila mutant of the lobula plate giant neurons. J Comp Physiol 124:287-296.
22. Kispert A, Herrmann BG. 1993. The Brachyury gene encodes a novel DNA binding protein. EMBO J 12:3211-3220.
23. Kohara Y. 2001. NEXTDB (The Nematode Expression Pattern Data Base) Ver. 3.0 beta, July 07 2001. http://nematode.lab.nig.ac.jp/db/index.html
24. Komatsu H, Jin YH, L'Etoile N, Mori I, Bargmann CI, Akaike N, Ohshima T. 1999. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res 821:160-168.
25. Komeili A, O'Shea EK. 2000. Nuclear transport and transcription. Curr Opin Cell Biol 12:355-360.
26. Kurahashi T, Menini A. 1997. Mechanism of odorant adaptation in the olfactory receptor cell. Nature 385:677-679.
27. 2+-dependent adaptive properties in the solitary olfactory receptor cell of the newt. Brain Res 515:261-268.
28. Law DJ, Gebuhr T, Garvey N, Agulnik SI, Silver LM. 1995. Identification, characterization, and localization to chromember of a conserved developmental gene family. Mamm Genome 6:793-797.
29. Leinders-Zufall T, Shepherd GM, Zufall F. 1996. Modulation by cyclic GMP of the odour sensitivity of vertebrate olfactory receptor cells. Proc R Soc Lond B Biol Sci 263:803-811.
30. L'Etoile ND, Bargmann CI. 2000. Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. Neuron 25:575-586.
31. L'Etoile ND, Coburn CM, Eastham J, Kistler A, Gallegos G, Bargmann CI. 2002. The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 36:1079-1089.
32. Lonze BE, Ginty DD. 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623.
33. Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, Rand JB. 1996. A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci USA 93:12593-12598.
34. Muller CW, Herrmann BG. 1997. Crystallographic structure of the T domain-DNA complex of the Brachyury transcription factor. Nature 389:884-888.
35. 2+-calmodulin-dependent odor adaptation. Science 294:2172-2175.
36. Papaioannou VE. 2001. T-box genes in development: from hydra to humans. Int Rev Cytol 207:1-70.
37. Papaioannou VE, Silver LM. 1998. The T-box gene family. Bioessays 20:9-19.
38. Pflugfelder GO, Roth H, Poeck B, Kerscher S, Schwarz H, Jonschker B, Heisenberg M. 1992. The lethal(1) optomotor-blind gene of Drosophila melanogaster is a major organizer of optic lobe development: isolation and characterization of the gene. Proc Natl Acad Sci USA 89:1199-1203.
39. Prasad BC, Ye B, Zackhary R, Schrader K, Seydoux G, Reed RR. 1998. unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors. Development 125:1561-1568.
40. Rankin ML, Alvania RS, Gleason EL, Bruch RC. 1999. Internalization of G protein-coupled receptors in single olfactory receptor neurons. J Neurochem 72:541-548.
41. Riddle DL, Albert PS. 1997. Genetic and environmental regulation of dauer larva development. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Press, p 739-768.
42. Sagasti A, Hisamoto N, Hyodo J, Tanaka-Hino M, Matsumoto K, Bargmann CI. 2001. The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 105:221-232.
43. Schackwitz WS, Inoue T, Thomas JH. 1996. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17:719-728.
44. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK. 2000. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538-541.
45. Smith J. 1999. T-box genes: what they do and how they do it. Trends Genet 15:154-158.
46. Starich TA, Herman RK, Kari CK, Yeh WH, Schackwitz WS, Schuyler MW, Collet J, Thomas JH, Riddle DL. 1995. Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics 139:171-188.
47. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI. 1995. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83:207-218.
48. Troemel ER, Kimmel BE, Bargmann CI. 1997. Reprogramming chemotaxis responses: Sensory neurons define olfactory preferences in C. elegans. Cell 91:161-169.
49. Troemel ER, Sagasti A, Bargmann CI. 1999. Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell 99:387-398.
50. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
51. Watt WC, Storm DR. 2001. Odorants stimulate the ERK/ mitogen-activated protein kinase pathway and activate cAMP-response element-mediated transcription in olfactory sensory neurons. J Biol Chem 276:2047-2052.
52. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode C. elegans. Phil Trans R Soc Lond B314:1-340.
53. Yu S, Avery L, Baude E, Garbers DL. 1997. Guanylyl cyclase expression in specific sensory neurons: A new family of chemosensory receptors. Proc Natl Acad Sci USA 94:3384-3387.
54. Zufall F, Leinders-Zufall T. 2000. The cellular and molecular basis of odor adaptation. Chem Senses 25:473-481.
55. Zwaal RR, Mendel JE, Sternberg PW, Plasterk RHA. 1997. Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans dauer-inducing pheromone. Genetics 145:715-727.