TBX2/TBX3 transcriptional factor homologue controls olfactory adaptation in Caenorhabditis elegans

Abstract

Although transcriptional factors are known to play important roles in synaptic plasticity, their role in olfactory adaptation has not been studied well. Here we report that Ce-TBX-2, the TBX2/TBX3 transcriptional factor homologue of the nematode Caenorhabditis elegans, is involved in olfactory adaptation. Two missense hypomorphic mutations in this gene confer abnormality in adaptation, but not chemotaxis, to all the odorants sensed by AWC olfactory neurons. The Ce-tbx-2 gene is expressed in AWB, AWC, ASJ, and many pharyngeal neurons, but expression in AWC neurons is sufficient for normal adaptation. Unexpectedly, the protein product is localized mostly in cytoplasm. The AWC neurons in the mutants retain their characteristic morphology and many marker gene expressions, suggesting that the mutants are abnormal in neural functions rather than neuronal differentiation. The results of this study imply that some of the mammalian T-box family proteins, which play central roles in embryonic development, may also control functions like neural plasticity in differentiated neurons.

G o α regulates olfactory adaptation by antagonizing G q α-DAG signaling in Caenorhabditis elegans

“…These studies have revealed that multiple proteins, most of which are likely to act cell-autonomously in AWC chemosensory neurons, are involved in olfactory adaptation (7,(9)(10)(11)(12)(13). Our results on the G o -G q signaling pathway strongly suggest that non-cell-autonomous mechanisms act to control olfactory adaptation in C. elegans.…”

“…By contrast, animals with mutated tax-6, which encodes calcineurin, exhibited hyperadaptation (11), suggesting that Ca 2ϩ and cGMP signaling cascades participate in olfactory adaptation. Moreover, ARR-1 arrestin (12), TBX-2 T-box transcription factor (13), and the Ras-MAPK pathway (14) are also known to act in olfactory adaptation, illustrating that olfactory adaptation in C. elegans is modulated by complicated mechanisms consisting of multiple signaling cascades and control of gene expression.…”

Generation and modulation of chemosensory behaviors in C. elegans

“…3a). Cytoplasmic activity of the TBX-2 transcription factor also affects early adaptation steps via as yet unknown mechanisms [156] (Fig. 3a).…”

“…a Molecules acting in the AWC neurons to modulate AWC neuron plasticity are shown in red. ARR-1 encodes an arrestin possibly playing a role in receptor desensitization [154]; overexpression of the ODR-1 receptor guanylyl cyclase alters adaptation to a subset of AWC-sensed odorants [142]; the TBX-2 transcription factor acts cytoplasmically to regulate olfactory adaptation via as yet unknown mechanisms [156]; the EGL-4 cGMP-dependent protein kinase phosphorylates the TAX-2 channel, and also translocates to the nucleus to regulate early and late steps in olfactory adaptation, respectively [145]; Ca 2+ entry through the OSM-9 TRPV channel is required for olfactory adaptation to a subset of AWC-sensed chemicals [146]; the TAX-6 Ca 2+ -dependent calcineurin phosphatase negatively regulates adaptation [155]. b Simplified summary of intercellular mechanisms proposed to mediate chemosensory behavioral plasticity.…”

Nuclear entry of a cGMP-dependent kinase converts transient into long-lasting olfactory adaptation

“…Genetic analysis has produced a list of factors required for adaptation (4,6,16,17,(20)(21)(22)(23)(24); however, the process by which these factors promote adaptation is unknown. To understand how adaptation proceeds in the AWC neuron, we complemented genetic methods with cell biological techniques.…”