The Balance between Cytoplasmic and Nuclear CaM Kinase-1 Signaling Controls the Operating Range of Noxious Heat Avoidance

Schild, Lisa C.; Zbinden, Laurie; Bell, Harold W.; Yu, Yanxun V.; Sengupta, Piali; Goodman, Miriam B.; Glauser, Dominique A.

doi:10.1016/j.neuron.2014.10.039

Cited by 45 publications

(90 citation statements)

References 51 publications

(68 reference statements)

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“…Together, these observations suggest that CKK-1-mediated phosphorylation regulates temperature-dependent nuclear translocation, but not activity, of CMK-1 in AFD, and support the idea that nuclear localization of CMK-1 upregulates gcy gene expression and T* AFD at warmer temperatures. CKK-1 similarly regulates nuclear localization of CMK-1 in response to noxious heat in the FLP nociceptor neurons in C. elegans (Schild et al, 2014). …”

Section: Resultsmentioning

confidence: 99%

“…However, upon prolonged exposure to warmer temperatures, adaptation of T* AFD to the correct value requires CKK-1-mediated regulation of CMK-1 nuclear localization, and CMK-1-mediated changes in gcy and other gene expression to increase intracellular cGMP levels (Figure 4F). Similarly, CMK-1 activity in the cytoplasm or nucleus of the nociceptive FLP neurons also increases or decreases the behavioral threshold, respectively, for heat nociception in C. elegans (Schild et al, 2014). In the absence of CMK-1 function, T* AFD adapts at the same rate but to lower values due to reduced levels of GCY proteins, thereby narrowing the effective dynamic range of AFD.…”

Section: Discussionmentioning

confidence: 99%

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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

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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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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

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

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132

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“…For expression in the gentle touch receptor neurons (TRNs), we used the mec-4 promoter. For expression in the FLP nociceptor neurons, we used the Q-system based on three transgenes, as previously described (Schild et al 2014).…”

Section: Chrimson and Cochr Gene Synthesis And Expression Plasmid Conmentioning

confidence: 99%

“…Since no specific promoter is available for FLP neurons, we used a Q-system-based strategy combining several promoters (Wei et al 2012;Schild et al 2014). FLP::CoChR animals grown with ATR produced robust blue light-induced backing behaviors (see File S1 and Figure S1B), but no response to red light ( Figure S1A).…”

Section: Cochr-mediated Activation Of the Polymodal Nociceptor Flp Trmentioning

confidence: 99%

Dual Color Neural Activation and Behavior Control with Chrimson and CoChR in Caenorhabditis elegans

Schild

Glauser

2015

Genetics

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By enabling a tight control of cell excitation, optogenetics is a powerful approach to study the function of neurons and neural circuits. With its transparent body, a fully mapped nervous system, easily quantifiable behaviors and many available genetic tools, Caenorhabditis elegans is an extremely well-suited model to decipher the functioning logic of the nervous system with optogenetics. Our goal was to establish an efficient dual color optogenetic system for the independent excitation of different neurons in C. elegans. We combined two recently discovered channelrhodopsins: the red-light sensitive Chrimson from Chlamydomonas noctigama and the bluelight sensitive CoChR from Chloromonas oogama. Codon-optimized versions of Chrimson and CoChR were designed for C. elegans and expressed in different mechanosensory neurons. Freely moving animals produced robust behavioral responses to light stimuli of specific wavelengths. Since CoChR was five times more sensitive to blue light than the commonly used ChR2, we were able to use low blue light intensities producing no cross-activation of Chrimson. Thanks to these optogenetics tools, we revealed asymmetric cross-habituation effects between the gentle and harsh touch sensory motor pathways. Collectively, our results establish the Chrimson/CoChR pair as a potent tool for bimodal neural excitation in C. elegans and equip this genetic model organism for the next generation of in vivo optogenetic analyses.

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“…On December 3, 2014, two research articles [59,60] were published in Neuron on the subject of C. elegans ’ ability to alter thermotaxis based on past experience. These studies built on years of work showing that CaM Kinase cascade signals to CREB and other transcription factors in the nematode [61,62].…”

Section: Introductionmentioning

confidence: 99%

Evolutionary and functional perspectives on signaling from neuronal surface to nucleus

Cohen

Tsien

et al. 2015

Biochemical and Biophysical Research Communications

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Reliance on Ca2+ signaling has been well-preserved through the course of evolution. While the complexity of Ca2+ signaling pathways has increased, activation of transcription factors including CREB by Ca2+/CaM-dependent kinases (CaMKs) has remained critical for long-term plasticity. In C. elegans, the CaMK family is made up of only three members, and CREB phosphorylation is mediated by CMK-1, the homologue of CaMKI. CMK-1 nuclear translocation directly regulates adaptation of thermotaxis behavior in response to changes in the environment. In mammals, the CaMK family has been expanded from three to ten members, enabling specialization of individual elements of a signal transduction pathway and increased reliance on the CaMKII subfamily. This increased complexity enables private line communication between Ca2+ sources at the cell surface and specific cellular targets. Using both new and previously published data, we review the mechanism of a γCaMKII-CaM nuclear translocation. This intricate pathway depends on a specific role for multiple Ca2+/CaM-dependent kinases and phosphatases: α/βCaMKII phosphorylates γCaMKII to trap CaM; CaN dephosphorylates γCaMKII to dispatch it to the nucleus; and PP2A induces CaM release from γCaMKII so that CaMKK and CaMKIV can trigger CREB phosphorylation. Thus, while certain basic elements have been conserved from C. elegans, evolutionary modifications offer opportunities for targeted communication, regulation of key nodes and checkpoints, and greater specificity and flexibility in signaling.

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The Balance between Cytoplasmic and Nuclear CaM Kinase-1 Signaling Controls the Operating Range of Noxious Heat Avoidance

Cited by 45 publications

References 51 publications

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

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

Dual Color Neural Activation and Behavior Control with Chrimson and CoChR in Caenorhabditis elegans

Evolutionary and functional perspectives on signaling from neuronal surface to nucleus

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