Identification of the AFD neuron as the site of action of the CREB protein in <i>Caenorhabditis elegans</i> thermotaxis

Nishida, Yukuo; Sugi, Takuma; Nonomura, Mayu; Mori, Ikue

doi:10.1038/embor.2011.120

Cited by 52 publications

(54 citation statements)

References 26 publications

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“…CREB activity in the reversal interneurons AVA and AVD is required for habituation, a nonassociative tap withdrawal behavior (Timbers and Rankin, 2011), and in the AFD neuron for thermotaxis (Nishida et al, 2011). Our microarray data suggest that CREB activity in neurons is sufficient to rescue LTAM and the transcriptional program specific to memory.…”

Section: Resultsmentioning

confidence: 99%

Genome-wide Functional Analysis of CREB/Long-Term Memory-Dependent Transcription Reveals Distinct Basal and Memory Gene Expression Programs

Lakhina

Arey

Kaletsky

et al. 2015

Neuron

131

138

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SUMMARY Induced CREB activity is a hallmark of long-term memory, but the full repertoire of CREB transcriptional targets required specifically for memory is not known in any system. To obtain a more complete picture of the mechanisms involved in memory, we combined memory training with genome-wide transcriptional analysis of C. elegans CREB mutants. This approach identified 757 significant CREB/memory-induced targets and confirmed the involvement of known memory genes from other organisms, but also suggested new mechanisms and novel components that may be conserved through mammals. CREB mediates distinct basal and memory transcriptional programs at least partially through spatial restriction of CREB activity: basal targets are regulated primarily in nonneuronal tissues, while memory targets are enriched for neuronal expression, emanating from CREB activity in AIM neurons. This suite of novel memory-associated genes will provide a platform for the discovery of orthologous mammalian long-term memory components.

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Section: Resultsmentioning

confidence: 99%

Genome-wide Functional Analysis of CREB/Long-Term Memory-Dependent Transcription Reveals Distinct Basal and Memory Gene Expression Programs

Lakhina

Arey

Kaletsky

et al. 2015

Neuron

131

138

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“…CaMK proteins regulate activity-dependent changes in gene expression in part via phosphorylation of transcription factors such as CREB and HSF1 (Eto et al, 1999; Holmberg et al, 2001; Sheng et al, 1991; Wayman et al, 2008), and crh-1 CREB mutants have been reported to exhibit thermotaxis defects and altered thermotransduction in AFD (Nishida et al, 2011). crh-1 mutants did not exhibit significant defects in either thermotaxis behaviors or temperature-regulated intracellular calcium dynamics in AFD under our assay conditions (Figure S4A-C).…”

Section: Resultsmentioning

confidence: 99%

CaMKI-Dependent Regulation of Sensory Gene Expression Mediates Experience-Dependent Plasticity in the Operating Range of a Thermosensory Neuron

Bell

Glauser

et al. 2014

Neuron

132

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SUMMARY Sensory adaptation represents a form of experience-dependent plasticity that allows neurons to retain high sensitivity over a broad dynamic range. The mechanisms by which sensory neuron responses are altered on different timescales during adaptation are unclear. The threshold for temperature-evoked activity in the AFD thermosensory neurons (T*AFD) in C. elegans is set by the cultivation temperature (Tc), and regulated by intracellular cGMP levels. We find that T*AFD adapts on both short and long timescales upon exposure to temperatures warmer than Tc, and that prolonged exposure to warmer temperatures alters expression of AFD-specific receptor guanylyl cyclase genes. These temperature-regulated changes in gene expression are mediated by the CMK-1 CaMKI enzyme which exhibits Tc-dependent nucleocytoplasmic shuttling in AFD. Our results indicate that CaMKI-mediated changes in sensory gene expression contribute to long-term adaptation of T*AFD, and suggest that similar temporally and mechanistically distinct phases may regulate the operating ranges of other sensory neurons.

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“…Behavioral geneticists have frequently used a visible selection marker, such as GFP, for germ-line transformation of a transgene of interest (17,19,20). To simultaneously illuminate four Petri plates by a GFP excitation beam, we constructed an optical device in which the beam from a high-power (200 mW) 488-nm excitation laser was quadruply multiplexed by half-mirrors, and these split beams were then guided to each Petri plate (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Using the developed system, we tried to address which neurons within the mechanosensory neural circuit are involved in memory formation. We focused on the C. elegans CREB homolog CRH-1, because CREB phosphorylation is a key factor in determining which neurons are recruited to a given memory trace (5,17,19,23,24). Previous studies have revealed that worms carrying a loss-of-function mutation in crh-1 exhibit a defect in mechanosensory habituation (8,17).…”

Section: Crh-1/creb Phosphorylation During Mechanosensory Habituationmentioning

confidence: 99%

“…Therefore, we performed cell-specific inhibitions of CRH-1 phosphorylation for behavioral analysis. We constructed a cDNA encoding full-length CRH-1 harboring a missense mutation in Ser29, which is known to abolish the transcriptional activity of mammalian CREB (19,25,29), and initially created two transgenic strains expressing the dominantnegative form of CRH-1 (CRH-1DN) under the control of either the mec-4 promoter that induces transgene expressions in mechanosensory neurons (ALM, AVM, PLM, and PVM), or the magi-1 promoter, both of which were used in the previous study (17) (Figs. S7 and S8).…”

Section: Crh-1/creb Phosphorylation During Mechanosensory Habituationmentioning

confidence: 99%

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High-throughput optical quantification of mechanosensory habituation reveals neurons encoding memory in Caenorhabditis elegans

Sugi

Ohtani

Kumiya

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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A major goal of neuroscience studies is to identify the neurons and molecules responsible for memory. Mechanosensory habituation in Caenorhabditis elegans is a simple form of learning and memory, in which a circuit of several sensory neurons and interneurons governs behavior. However, despite the usefulness of this paradigm, there are hardly any systems for rapid and accurate behavioral genetic analysis. Here, we developed a multiplexed optical system to genetically analyze C. elegans mechanosensory habituation, and identified two interneurons involved in memory formation. The system automatically trains large populations of animals and simultaneously quantifies the behaviors of various strains by optically discriminating between transgenic and nontransgenic animals. Biochemical and cell-specific behavioral analyses indicated that phosphorylation of cyclic AMP response element-binding protein (CREB), a factor known to regulate memory allocation, was facilitated during training and this phosphorylation in AVA and AVD interneurons was required for habituation. These interneurons are a potential target for cell-specific exploration of the molecular substrates of memory.Caenorhabditis elegans | mechanosensory habituation | memory | optical quantification | neural circuit I dentification of the physical substrates of memory in the brain, namely neurons and molecules encoding memory, is a major challenge in neuroscience. Recent studies have revealed that the transcription factor cAMP response element-binding protein (CREB) (1) is crucial for determining which neurons in the lateral amygdala participate in encoding an auditory fear memory, and that neurons with higher CREB activity are preferentially allocated into a unique memory trace (memory engram) (2-6). Thus, it has been generally thought through the accumulated weight of evidence that memory is represented by a specific population of neurons in the brain that forms memory engrams: only a portion of eligible neurons are recruited into a specific memory. Although this CREB-dependent memory allocation model is established (5), the identification of specific neurons supporting a given memory remains a long-standing challenge. Moreover, the extreme complexity of nervous systems in model animals still hampers cell-specific genetic analyses; therefore, even if neurons encoding memory could be identified, it would be difficult to address the subsequent question of how these neurons store memory at the molecular level in situ.The nematode Caenorhabditis elegans is a genetically tractable model organism with a neural circuit composed of only 302 neurons. Moreover, the wiring of this nervous system has been completely determined. These unique features of the C. elegans nervous system have proven to be advantageous for various behavioral experiments, such as genetic rescue experiments, ectopic expression analysis, overexpression analysis, and RNA interference-mediated gene disruption, because all of these transgenic studies can be conducted in situ in a cell-specific manner...

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Identification of the AFD neuron as the site of action of the CREB protein in Caenorhabditis elegans thermotaxis

Cited by 52 publications

References 26 publications

Genome-wide Functional Analysis of CREB/Long-Term Memory-Dependent Transcription Reveals Distinct Basal and Memory Gene Expression Programs

Genome-wide Functional Analysis of CREB/Long-Term Memory-Dependent Transcription Reveals Distinct Basal and Memory Gene Expression Programs

CaMKI-Dependent Regulation of Sensory Gene Expression Mediates Experience-Dependent Plasticity in the Operating Range of a Thermosensory Neuron

High-throughput optical quantification of mechanosensory habituation reveals neurons encoding memory in Caenorhabditis elegans

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