Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation

Sensory and behavioral plasticity are essential for animals to thrive in changing environments. As key effectors of intracellular calcium signaling, Ca2+/calmodulin-dependent protein kinases (CaMKs) can bridge neural activation with the many regulatory processes needed to orchestrate sensory adaptat...

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Autores principales:	Domenica Ippolito, Saurabh Thapliyal, Dominique A Glauser
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	behavioral plasticity calcium signaling thermosensation protein subcellular localization Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/d1dd524f974a42f5a53dce6dbff66114
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spelling	oai:doaj.org-article:d1dd524f974a42f5a53dce6dbff661142021-12-01T15:06:10ZCa2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation10.7554/eLife.714432050-084Xe71443https://doaj.org/article/d1dd524f974a42f5a53dce6dbff661142021-11-01T00:00:00Zhttps://elifesciences.org/articles/71443https://doaj.org/toc/2050-084XSensory and behavioral plasticity are essential for animals to thrive in changing environments. As key effectors of intracellular calcium signaling, Ca2+/calmodulin-dependent protein kinases (CaMKs) can bridge neural activation with the many regulatory processes needed to orchestrate sensory adaptation, including by relaying signals to the nucleus. Here, we elucidate the molecular mechanism controlling the cell activation-dependent nuclear translocation of CMK-1, the Caenorhabditis elegans ortholog of mammalian CaMKI/IV, in thermosensory neurons in vivo. We show that an intracellular Ca2+ concentration elevation is necessary and sufficient to favor CMK-1 nuclear import. The binding of Ca2+/CaM to CMK-1 increases its affinity for IMA-3 importin, causing a redistribution with a relatively slow kinetics, matching the timescale of sensory adaptation. Furthermore, we show that this mechanism enables the encoding of opposite nuclear signals in neuron types with opposite calcium-responses and that it is essential for experience-dependent behavioral plasticity and gene transcription control in vivo. Since CaMKI/IV are conserved regulators of adaptable behaviors, similar mechanisms could exist in other organisms and for other sensory modalities.Domenica IppolitoSaurabh ThapliyalDominique A GlausereLife Sciences Publications Ltdarticlebehavioral plasticitycalcium signalingthermosensationprotein subcellular localizationMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	behavioral plasticity calcium signaling thermosensation protein subcellular localization Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	behavioral plasticity calcium signaling thermosensation protein subcellular localization Medicine R Science Q Biology (General) QH301-705.5 Domenica Ippolito Saurabh Thapliyal Dominique A Glauser Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation
description	Sensory and behavioral plasticity are essential for animals to thrive in changing environments. As key effectors of intracellular calcium signaling, Ca2+/calmodulin-dependent protein kinases (CaMKs) can bridge neural activation with the many regulatory processes needed to orchestrate sensory adaptation, including by relaying signals to the nucleus. Here, we elucidate the molecular mechanism controlling the cell activation-dependent nuclear translocation of CMK-1, the Caenorhabditis elegans ortholog of mammalian CaMKI/IV, in thermosensory neurons in vivo. We show that an intracellular Ca2+ concentration elevation is necessary and sufficient to favor CMK-1 nuclear import. The binding of Ca2+/CaM to CMK-1 increases its affinity for IMA-3 importin, causing a redistribution with a relatively slow kinetics, matching the timescale of sensory adaptation. Furthermore, we show that this mechanism enables the encoding of opposite nuclear signals in neuron types with opposite calcium-responses and that it is essential for experience-dependent behavioral plasticity and gene transcription control in vivo. Since CaMKI/IV are conserved regulators of adaptable behaviors, similar mechanisms could exist in other organisms and for other sensory modalities.
format	article
author	Domenica Ippolito Saurabh Thapliyal Dominique A Glauser
author_facet	Domenica Ippolito Saurabh Thapliyal Dominique A Glauser
author_sort	Domenica Ippolito
title	Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation
title_short	Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation
title_full	Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation
title_fullStr	Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation
title_full_unstemmed	Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation
title_sort	ca2+/cam binding to camki promotes ima-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/d1dd524f974a42f5a53dce6dbff66114
work_keys_str_mv	AT domenicaippolito ca2cambindingtocamkipromotesima3importinbindingandnucleartranslocationinsensoryneuronstocontrolbehavioraladaptation AT saurabhthapliyal ca2cambindingtocamkipromotesima3importinbindingandnucleartranslocationinsensoryneuronstocontrolbehavioraladaptation AT dominiqueaglauser ca2cambindingtocamkipromotesima3importinbindingandnucleartranslocationinsensoryneuronstocontrolbehavioraladaptation
_version_	1718404898443231232

Ca2+/CaM binding to CaMKI promotes IMA-3 importin binding and nuclear translocation in sensory neurons to control behavioral adaptation

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