دورية أكاديمية
أعرض في EDS

The kainate receptor GluK2 mediates cold sensing in mice.

التفاصيل البيبلوغرافية
العنوان: The kainate receptor GluK2 mediates cold sensing in mice.
المؤلفون: Cai W; Life Sciences Institute, University of Michigan, Ann Arbor, MI, USA.; Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, USA., Zhang W; Life Sciences Institute, University of Michigan, Ann Arbor, MI, USA.; Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, USA., Zheng Q; Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.; The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD, USA., Hor CC; Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, USA., Pan T; Life Sciences Institute, University of Michigan, Ann Arbor, MI, USA.; Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, USA., Fatima M; Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, USA., Dong X; The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD, USA.; Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, MD, USA., Duan B; Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, USA. bduan@umich.edu., Xu XZS; Life Sciences Institute, University of Michigan, Ann Arbor, MI, USA. shawnxu@umich.edu.; Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, MI, USA. shawnxu@umich.edu.
المصدر: Nature neuroscience [Nat Neurosci] 2024 Apr; Vol. 27 (4), pp. 679-688. Date of Electronic Publication: 2024 Mar 11.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: United States NLM ID: 9809671 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1546-1726 (Electronic) Linking ISSN: 10976256 NLM ISO Abbreviation: Nat Neurosci Subsets: MEDLINE
أسماء مطبوعة: Publication: <2002->: New York, NY : Nature Publishing Group
Original Publication: New York, NY : Nature America Inc., c1998-
مواضيع طبية MeSH: GluK2 Kainate Receptor*/metabolism , Receptors, Kainic Acid*/genetics , Receptors, Kainic Acid*/metabolism, Animals ; Mice ; Caenorhabditis elegans/metabolism ; Cold Temperature ; Glutamic Acid ; Mammals/metabolism ; Neurons/metabolism ; Synaptic Transmission
مستخلص: Thermosensors expressed in peripheral somatosensory neurons sense a wide range of environmental temperatures. While thermosensors detecting cool, warm and hot temperatures have all been extensively characterized, little is known about those sensing cold temperatures. Though several candidate cold sensors have been proposed, none has been demonstrated to mediate cold sensing in somatosensory neurons in vivo, leaving a knowledge gap in thermosensation. Here we characterized mice lacking the kainate-type glutamate receptor GluK2, a mammalian homolog of the Caenorhabditis elegans cold sensor GLR-3. While GluK2 knockout mice respond normally to heat and mechanical stimuli, they exhibit a specific deficit in sensing cold but not cool temperatures. Further analysis supports a key role for GluK2 in sensing cold temperatures in somatosensory DRG neurons in the periphery. Our results reveal that GluK2-a glutamate-sensing chemoreceptor mediating synaptic transmission in the central nervous system-is co-opted as a cold-sensing thermoreceptor in the periphery.
(© 2024. The Author(s), under exclusive licence to Springer Nature America, Inc.)
References: Xiao, R. & Xu, X. Z. S. Temperature sensation: from molecular thermosensors to neural circuits and coding principles. Annu. Rev. Physiol. 83, 205–230 (2021). (PMID: 3308592710.1146/annurev-physiol-031220-095215)
Palkar, R., Lippoldt, E. K. & McKemy, D. D. The molecular and cellular basis of thermosensation in mammals. Curr. Opin. Neurobiol. 34, 14–19 (2015). (PMID: 25622298451293410.1016/j.conb.2015.01.010)
Vandewauw, I. et al. A TRP channel trio mediates acute noxious heat sensing. Nature 555, 662–666 (2018). (PMID: 2953964210.1038/nature26137)
Tan, C. H. & McNaughton, P. A. The TRPM2 ion channel is required for sensitivity to warmth. Nature 536, 460–463 (2016). (PMID: 27533035572034410.1038/nature19074)
Song, K. et al. The TRPM2 channel is a hypothalamic heat sensor that limits fever and can drive hypothermia. Science 353, 1393–1398 (2016). (PMID: 27562954761227610.1126/science.aaf7537)
Bautista, D. M. et al. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448, 204–208 (2007). (PMID: 1753862210.1038/nature05910)
Dhaka, A. et al. TRPM8 is required for cold sensation in mice. Neuron 54, 371–378 (2007). (PMID: 1748139110.1016/j.neuron.2007.02.024)
Buijs, T. J. & McNaughton, P. A. The role of cold-sensitive ion channels in peripheral thermosensation. Front. Cell. Neurosci. 14, 262 (2020). (PMID: 32973456746844910.3389/fncel.2020.00262)
Traynelis, S. F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharm. Rev. 62, 405–496 (2010). (PMID: 20716669296490310.1124/pr.109.002451)
Gong, J. et al. A cold-sensing receptor encoded by a glutamate receptor gene. Cell 178, 1375–1386 e1311 (2019). (PMID: 31474366674397910.1016/j.cell.2019.07.034)
Fujita, F., Uchida, K., Takaishi, M., Sokabe, T. & Tominaga, M. Ambient temperature affects the temperature threshold for TRPM8 activation through interaction of phosphatidylinositol 4,5-bisphosphate. J. Neurosci. 33, 6154–6159 (2013). (PMID: 23554496661893710.1523/JNEUROSCI.5672-12.2013)
McKemy, D. D., Neuhausser, W. M. & Julius, D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416, 52–58 (2002). (PMID: 1188288810.1038/nature719)
Peier, A. M. et al. A TRP channel that senses cold stimuli and menthol. Cell 108, 705–715 (2002). (PMID: 1189334010.1016/S0092-8674(02)00652-9)
Bandell, M., Macpherson, L. J. & Patapoutian, A. From chills to chilis: mechanisms for thermosensation and chemesthesis via thermoTRPs. Curr. Opin. Neurobiol. 17, 490–497 (2007). (PMID: 17706410208061710.1016/j.conb.2007.07.014)
Usoskin, D. et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci. 18, 145–153 (2015). (PMID: 2542006810.1038/nn.3881)
Sharma, N. et al. The emergence of transcriptional identity in somatosensory neurons. Nature 577, 392–398 (2020). (PMID: 31915380730742210.1038/s41586-019-1900-1)
Duan, B. et al. Identification of spinal circuits transmitting and gating mechanical pain. Cell 159, 1417–1432 (2014). (PMID: 25467445425851110.1016/j.cell.2014.11.003)
Ma, Q. A functional subdivision within the somatosensory system and its implications for pain research. Neuron 110, 749–769 (2022). (PMID: 35016037889727510.1016/j.neuron.2021.12.015)
Knowlton, W. M. et al. A sensory-labeled line for cold: TRPM8-expressing sensory neurons define the cellular basis for cold, cold pain, and cooling-mediated analgesia. J. Neurosci. 33, 2837–2848 (2013). (PMID: 23407943371139010.1523/JNEUROSCI.1943-12.2013)
Mulle, C. et al. Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392, 601–605 (1998). (PMID: 958026010.1038/33408)
Zhou, X. et al. Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway. Proc. Natl Acad. Sci. USA 107, 9424–9429 (2010). (PMID: 20439739288905410.1073/pnas.0914725107)
Han, L. et al. Mrgprs on vagal sensory neurons contribute to bronchoconstriction and airway hyper-responsiveness. Nat. Neurosci. 21, 324–328 (2018). (PMID: 29403029585722210.1038/s41593-018-0074-8)
Sarria, I., Ling, J., Xu, G. Y. & Gu, J. G. Sensory discrimination between innocuous and noxious cold by TRPM8-expressing DRG neurons of rats. Mol. Pain 8, 79 (2012). (PMID: 23092296349567510.1186/1744-8069-8-79)
Kim, Y. S. et al. Coupled activation of primary sensory neurons contributes to chronic pain. Neuron 91, 1085–1096 (2016). (PMID: 27568517501792010.1016/j.neuron.2016.07.044)
Emery, E. C. et al. In vivo characterization of distinct modality-specific subsets of somatosensory neurons using GCaMP. Sci. Adv. 2, e1600990 (2016). (PMID: 27847865510620110.1126/sciadv.1600990)
Wang, F. et al. Sensory afferents use different coding strategies for heat and cold. Cell Rep. 23, 2001–2013 (2018). (PMID: 2976820010.1016/j.celrep.2018.04.065)
Story, G. M. et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112, 819–829 (2003). (PMID: 1265424810.1016/S0092-8674(03)00158-2)
Buijs, T. J., Vilar, B., Tan, C. H. & McNaughton, P. A. STIM1 and ORAI1 form a novel cold transduction mechanism in sensory and sympathetic neurons. EMBO J. 42, e111348 (2022). (PMID: 36524441989023210.15252/embj.2022111348)
Zimmermann, K. et al. Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. Proc. Natl Acad. Sci. USA 108, 18114–18119 (2011). (PMID: 22025699320766710.1073/pnas.1115387108)
MacDonald, D. I., Wood, J. N. & Emery, E. C. Molecular mechanisms of cold pain. Neurobiol. Pain 7, 100044 (2020). (PMID: 32090187702528810.1016/j.ynpai.2020.100044)
Foulkes, T. & Wood, J. N. Mechanisms of cold pain. Channels (Austin) 1, 154–160 (2007). (PMID: 1869003310.4161/chan.4692)
Rodriguez-Moreno, A. & Lerma, J. Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 20, 1211–1218 (1998). (PMID: 965550810.1016/S0896-6273(00)80501-2)
Valbuena, S. & Lerma, J. Non-canonical signaling, the hidden life of ligand-gated ion channels. Neuron 92, 316–329 (2016). (PMID: 2776466510.1016/j.neuron.2016.10.016)
Lerma, J. Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 4, 481–495 (2003). (PMID: 1277812010.1038/nrn1118)
Venkatachalam, K. & Montell, C. TRP channels. Annu. Rev. Biochem. 76, 387–417 (2007). (PMID: 17579562419687510.1146/annurev.biochem.75.103004.142819)
Xiao, R. & Xu, X. Z. C. elegans TRP channels. Adv. Exp. Med. Biol. 704, 323–339 (2011). (PMID: 2129030410.1007/978-94-007-0265-3_18)
Viswanath, V. et al. Opposite thermosensor in fruitfly and mouse. Nature 423, 822–823 (2003). (PMID: 1281541810.1038/423822a)
Gracheva, E. O. et al. Molecular basis of infrared detection by snakes. Nature 464, 1006–1011 (2010). (PMID: 20228791285540010.1038/nature08943)
Xiao, R. et al. A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152, 806–817 (2013). (PMID: 23415228359409710.1016/j.cell.2013.01.020)
Zhang, B. et al. Environmental temperature differentially modulates C. elegans longevity through a thermosensitive TRP channel. Cell Rep. 11, 1414–1424 (2015). (PMID: 26027928475883610.1016/j.celrep.2015.04.066)
Zhang, B. et al. Brain-gut communications via distinct neuroendocrine signals bidirectionally regulate longevity in C. elegans. Genes Dev. 32, 258–270 (2018). (PMID: 29491136585996710.1101/gad.309625.117)
Marshall, J. J., Xu, J. & Contractor, A. Kainate receptors inhibit glutamate release via mobilization of endocannabinoids in striatal direct pathway spiny projection neurons. J. Neurosci. 38, 3901–3910 (2018). (PMID: 29540547590705310.1523/JNEUROSCI.1788-17.2018)
Kim, A. Y. et al. Pirt, a phosphoinositide-binding protein, functions as a regulatory subunit of TRPV1. Cell 133, 475–485 (2008). (PMID: 18455988260597010.1016/j.cell.2008.02.053)
Pan, H. et al. Identification of a spinal circuit for mechanical and persistent spontaneous itch. Neuron 103, 1135–1149 e1136 (2019). (PMID: 31324538676339010.1016/j.neuron.2019.06.016)
Chaplan, S. R., Bach, F. W., Pogrel, J. W., Chung, J. M. & Yaksh, T. L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53, 55–63 (1994). (PMID: 799051310.1016/0165-0270(94)90144-9)
Ran, C., Hoon, M. A. & Chen, X. The coding of cutaneous temperature in the spinal cord. Nat. Neurosci. 19, 1201–1209 (2016). (PMID: 27455110559912510.1038/nn.4350)
Ouyang, J. F., Kamaraj, U. S., Cao, E. Y. & Rackham, O. J. L. ShinyCell: simple and sharable visualization of single-cell gene expression data. Bioinformatics 37, 3374–3376 (2021). (PMID: 3377465910.1093/bioinformatics/btab209)
Michki, N. S. et al. The molecular landscape of neural differentiation in the developing Drosophila brain revealed by targeted scRNA-seq and multi-informatic analysis. Cell Rep. 35, 109039 (2021). (PMID: 33909998813928710.1016/j.celrep.2021.109039)
المشرفين على المادة: 0 (GluK2 Kainate Receptor)
3KX376GY7L (Glutamic Acid)
0 (Receptors, Kainic Acid)
تواريخ الأحداث: Date Created: 20240312 Date Completed: 20240410 Latest Revision: 20240415
رمز التحديث: 20240415
DOI: 10.1038/s41593-024-01585-8
PMID: 38467901
قاعدة البيانات: MEDLINE
الوصف
تدمد:1546-1726
DOI:10.1038/s41593-024-01585-8