Microglia Are Indispensable for Synaptic Plasticity in the Spinal Dorsal Horn and Chronic Pain
Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, a causal link between spinal LTP and chronic pain is still lacking. Here, we report that high-frequency stimulation (HFS; 100 Hz, 10 V) of the mouse sciatic nerve reliably induces spinal LTP wi...
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| Published in | Cell reports (Cambridge) Vol. 27; no. 13; pp. 3844 - 3859.e6 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
25.06.2019
Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, a causal link between spinal LTP and chronic pain is still lacking. Here, we report that high-frequency stimulation (HFS; 100 Hz, 10 V) of the mouse sciatic nerve reliably induces spinal LTP without causing nerve injury. LTP-inducible stimulation triggers chronic pain lasting for more than 35 days and increases the number of calcitonin gene-related peptide (CGRP) terminals in the spinal dorsal horn. The behavioral and morphological changes can be prevented by blocking NMDA receptors, ablating spinal microglia, or conditionally deleting microglial brain-derived neurotrophic factor (BDNF). HFS-induced spinal LTP, microglial activation, and upregulation of BDNF are inhibited by antibodies against colony-stimulating factor 1 (CSF-1). Together, our results show that microglial CSF1 and BDNF signaling are indispensable for spinal LTP and chronic pain. The microglia-dependent transition of synaptic potentiation to structural alterations in pain pathways may underlie pain chronicity.
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•HFS triggers synaptic plasticity of CGRP afferents and chronic pain•LTP-inducible HFS activates spinal microglia through CSF1 signaling•Microglial BDNF is essential for HFS-induced spinal LTP and chronic pain
Zhou et al. characterize chronic pain behaviors triggered by LTP-inducible HFS without nerve injury. They identify that HFS-induced LTP is accompanied by an increase in CGRP terminals in the spinal dorsal horn. Activation of neuronal CSF1-microglial BDNF signaling is indispensable for the synaptic and structural plasticity underlying HFS-induced chronic pain. |
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| AbstractList | Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, a causal link between spinal LTP and chronic pain is still lacking. Here, we report that high-frequency stimulation (HFS; 100 Hz, 10 V) of the mouse sciatic nerve reliably induces spinal LTP without causing nerve injury. LTP-inducible stimulation triggers chronic pain lasting for more than 35 days and increases the number of calcitonin gene-related peptide (CGRP) terminals in the spinal dorsal horn. The behavioral and morphological changes can be prevented by blocking NMDA receptors, ablating spinal microglia, or conditionally deleting microglial brain-derived neurotrophic factor (BDNF). HFS-induced spinal LTP, microglial activation, and upregulation of BDNF are inhibited by antibodies against colony-stimulating factor 1 (CSF-1). Together, our results show that microglial CSF1 and BDNF signaling are indispensable for spinal LTP and chronic pain. The microglia-dependent transition of synaptic potentiation to structural alterations in pain pathways may underlie pain chronicity. : Zhou et al. characterize chronic pain behaviors triggered by LTP-inducible HFS without nerve injury. They identify that HFS-induced LTP is accompanied by an increase in CGRP terminals in the spinal dorsal horn. Activation of neuronal CSF1-microglial BDNF signaling is indispensable for the synaptic and structural plasticity underlying HFS-induced chronic pain. Keywords: long-term potentiation, chronic pain, calcitonin gene-related peptide, microglia, high-frequency stimulation, colony-stimulating factor 1, brain-derived neurotrophic factor Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, a causal link between spinal LTP and chronic pain is still lacking. Here, we report that high-frequency stimulation (HFS; 100 Hz, 10 V) of the mouse sciatic nerve reliably induces spinal LTP without causing nerve injury. LTP-inducible stimulation triggers chronic pain lasting for more than 35 days and increases the number of calcitonin gene-related peptide (CGRP) terminals in the spinal dorsal horn. The behavioral and morphological changes can be prevented by blocking NMDA receptors, ablating spinal microglia, or conditionally deleting microglial brain-derived neurotrophic factor (BDNF). HFS-induced spinal LTP, microglial activation, and upregulation of BDNF are inhibited by antibodies against colony-stimulating factor 1 (CSF-1). Together, our results show that microglial CSF1 and BDNF signaling are indispensable for spinal LTP and chronic pain. The microglia-dependent transition of synaptic potentiation to structural alterations in pain pathways may underlie pain chronicity. [Display omitted] •HFS triggers synaptic plasticity of CGRP afferents and chronic pain•LTP-inducible HFS activates spinal microglia through CSF1 signaling•Microglial BDNF is essential for HFS-induced spinal LTP and chronic pain Zhou et al. characterize chronic pain behaviors triggered by LTP-inducible HFS without nerve injury. They identify that HFS-induced LTP is accompanied by an increase in CGRP terminals in the spinal dorsal horn. Activation of neuronal CSF1-microglial BDNF signaling is indispensable for the synaptic and structural plasticity underlying HFS-induced chronic pain. Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, a causal link between spinal LTP and chronic pain is still lacking. Here, we report that high-frequency stimulation (HFS; 100 Hz, 10 V) of the mouse sciatic nerve reliably induces spinal LTP without causing nerve injury. LTP-inducible stimulation triggers chronic pain lasting for more than 35 days and increases the number of calcitonin gene-related peptide (CGRP) terminals in the spinal dorsal horn. The behavioral and morphological changes can be prevented by blocking NMDA receptors, ablating spinal microglia, or conditionally deleting microglial brain-derived neurotrophic factor (BDNF). HFS-induced spinal LTP, microglial activation, and upregulation of BDNF are inhibited by antibodies against colony-stimulating factor 1 (CSF-1). Together, our results show that microglial CSF1 and BDNF signaling are indispensable for spinal LTP and chronic pain. The microglia-dependent transition of synaptic potentiation to structural alterations in pain pathways may underlie pain chronicity.Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, a causal link between spinal LTP and chronic pain is still lacking. Here, we report that high-frequency stimulation (HFS; 100 Hz, 10 V) of the mouse sciatic nerve reliably induces spinal LTP without causing nerve injury. LTP-inducible stimulation triggers chronic pain lasting for more than 35 days and increases the number of calcitonin gene-related peptide (CGRP) terminals in the spinal dorsal horn. The behavioral and morphological changes can be prevented by blocking NMDA receptors, ablating spinal microglia, or conditionally deleting microglial brain-derived neurotrophic factor (BDNF). HFS-induced spinal LTP, microglial activation, and upregulation of BDNF are inhibited by antibodies against colony-stimulating factor 1 (CSF-1). Together, our results show that microglial CSF1 and BDNF signaling are indispensable for spinal LTP and chronic pain. The microglia-dependent transition of synaptic potentiation to structural alterations in pain pathways may underlie pain chronicity. Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, a causal link between spinal LTP and chronic pain is still lacking. Here, we report that high-frequency stimulation (HFS; 100 Hz, 10 V) of the mouse sciatic nerve reliably induces spinal LTP without causing nerve injury. LTP-inducible stimulation triggers chronic pain lasting for more than 35 days and increases the number of calcitonin gene-related peptide (CGRP) terminals in the spinal dorsal horn. The behavioral and morphological changes can be prevented by blocking NMDA receptors, ablating spinal microglia, or conditionally deleting microglial brain-derived neurotrophic factor (BDNF). HFS-induced spinal LTP, microglial activation, and upregulation of BDNF are inhibited by antibodies against colony-stimulating factor 1 (CSF-1). Together, our results show that microglial CSF1 and BDNF signaling are indispensable for spinal LTP and chronic pain. The microglia-dependent transition of synaptic potentiation to structural alterations in pain pathways may underlie pain chronicity. Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, the causal link between spinal LTP and chronic pain is still lacking. Here we report that high frequency stimulation (HFS, 100 Hz, 10 V) of the mouse sciatic nerve reliably induces spinal LTP without causing nerve injury. LTP-inducible stimulation triggers chronic pain lasting for > 35 d and increases the number of calcitonin gene related peptide (CGRP) terminals in spinal dorsal horn. The behavioral and morphological changes can be prevented by blocking NMDA receptors, ablating spinal microglia, or conditionally deleting microglial BDNF. HFS-induced spinal LTP, microglial activation, and upregulation of BDNF are inhibited by antibodies against colony stimulating factor 1 (CSF-1). Together, our results show that microglial CSF1 and BDNF signaling is indispensable for spinal LTP and chronic pain. The microglia dependent transition of synaptic potentiation to structural alterations in pain pathways may underlie pain chronicity. |
| Author | Murugan, Madhuvika Li, Mingtao Wang, Hui Wei, Xiao Richardson, Jason R. Zeng, Wei-Jie Chen, Tao Xu, Ya-Nan Liu, Xian-Guo Wu, Long-Jun Peng, Jiyun Lin, Zhen-Jia Xin, Wen-Jun Tan, Zhi Liu, Yong Umpierre, Anthony D. Zhang, Jun Zhou, Li-Jun Mai, Chun-Lin Eyo, Ukpong B. |
| AuthorAffiliation | 1 Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China 10 Department of Immunology, Mayo Clinic, Rochester, MN 55905, USA 5 Department of Anatomy, Histology and Embryology and K.K. Leung Brain Research, Center, the Fourth Military Medical University, Xi’an 710032, China 4 Department of Neurology, Mayo Clinic, Rochester, MN 55905, USA 2 Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ, 08854, USA 7 Department of Pharmacology, School of Pharmacy, Nantong University, Nantong 22600, China 9 Department of Neuroscience, Mayo Clinic, Jacksonville, FL 32224, USA 3 Guangdong Province Key Laboratory of Brain Function and Disease, Guangzhou, 510080, China 8 Departments of Environmental Health Sciences, Florida International University, Miami, FL 33199 6 Department of Neuroscience and Cell Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA |
| AuthorAffiliation_xml | – name: 6 Department of Neuroscience and Cell Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA – name: 7 Department of Pharmacology, School of Pharmacy, Nantong University, Nantong 22600, China – name: 9 Department of Neuroscience, Mayo Clinic, Jacksonville, FL 32224, USA – name: 2 Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ, 08854, USA – name: 3 Guangdong Province Key Laboratory of Brain Function and Disease, Guangzhou, 510080, China – name: 4 Department of Neurology, Mayo Clinic, Rochester, MN 55905, USA – name: 10 Department of Immunology, Mayo Clinic, Rochester, MN 55905, USA – name: 8 Departments of Environmental Health Sciences, Florida International University, Miami, FL 33199 – name: 1 Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – name: 5 Department of Anatomy, Histology and Embryology and K.K. Leung Brain Research, Center, the Fourth Military Medical University, Xi’an 710032, China |
| Author_xml | – sequence: 1 givenname: Li-Jun surname: Zhou fullname: Zhou, Li-Jun organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 2 givenname: Jiyun surname: Peng fullname: Peng, Jiyun organization: Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ 08854, USA – sequence: 3 givenname: Ya-Nan surname: Xu fullname: Xu, Ya-Nan organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 4 givenname: Wei-Jie surname: Zeng fullname: Zeng, Wei-Jie organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 5 givenname: Jun surname: Zhang fullname: Zhang, Jun organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 6 givenname: Xiao surname: Wei fullname: Wei, Xiao organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 7 givenname: Chun-Lin surname: Mai fullname: Mai, Chun-Lin organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 8 givenname: Zhen-Jia surname: Lin fullname: Lin, Zhen-Jia organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 9 givenname: Yong surname: Liu fullname: Liu, Yong organization: Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ 08854, USA – sequence: 10 givenname: Madhuvika surname: Murugan fullname: Murugan, Madhuvika organization: Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ 08854, USA – sequence: 11 givenname: Ukpong B. surname: Eyo fullname: Eyo, Ukpong B. organization: Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ 08854, USA – sequence: 12 givenname: Anthony D. surname: Umpierre fullname: Umpierre, Anthony D. organization: Department of Neurology, Mayo Clinic, Rochester, MN 55905, USA – sequence: 13 givenname: Wen-Jun surname: Xin fullname: Xin, Wen-Jun organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 14 givenname: Tao surname: Chen fullname: Chen, Tao organization: Department of Anatomy, Histology and Embryology and K.K. Leung Brain Research Center, the Fourth Military Medical University, Xi’an 710032, China – sequence: 15 givenname: Mingtao surname: Li fullname: Li, Mingtao organization: Guangdong Province Key Laboratory of Brain Function and Disease, Guangzhou 510080, China – sequence: 16 givenname: Hui surname: Wang fullname: Wang, Hui organization: Department of Neuroscience and Cell Biology, Rutgers-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA – sequence: 17 givenname: Jason R. surname: Richardson fullname: Richardson, Jason R. organization: Departments of Environmental Health Sciences, Florida International University, Miami, FL 33199, USA – sequence: 18 givenname: Zhi surname: Tan fullname: Tan, Zhi email: tanzhi@mail.sysu.edu.cn organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 19 givenname: Xian-Guo surname: Liu fullname: Liu, Xian-Guo email: liuxg@mail.sysu.edu.cn organization: Department of Physiology and Pain Research Center, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China – sequence: 20 givenname: Long-Jun surname: Wu fullname: Wu, Long-Jun email: wu.longjun@mayo.edu organization: Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ 08854, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31242418$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2019 The Author(s) Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved. |
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| Keywords | chronic pain colony-stimulating factor 1 calcitonin gene-related peptide brain-derived neurotrophic factor microglia high-frequency stimulation long-term potentiation |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work. AUTHOR CONTRIBUTIONS Lead Contact: Long-Jun Wu (wu.longjun@mayo.edu) L.J.Z., J.R.R., Z.T., X.G.L. and L.J.W. conceived the study, designed the experiments and wrote the manuscript. L.J.Z. performed most of the experiments. J.Y.P. and Y.N.X. performed the intrathecal injection of drugs and performed all blind pain behavior tests. L.J.Z. Y.N.X., J. Z., and W.J.Z. finished the spinal culture, DRG neuron culture and qRT-PCR experiments. W.J.Z., Z.T. and T.C. performed the IEM experiments and data analysis. X.W. performed the experiment in rats. L.J.Z. C.L.M, Z.J.L., M.M., Y.L., U.B.E., A.D.U, W.J.X., M.T.L., and H.W. assisted with experiments. |
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| Snippet | Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, a causal link between spinal LTP and chronic pain is... Spinal long-term potentiation (LTP) at C-fiber synapses is hypothesized to underlie chronic pain. However, the causal link between spinal LTP and chronic pain... |
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| SubjectTerms | Animals brain-derived neurotrophic factor calcitonin gene-related peptide Calcitonin Gene-Related Peptide - genetics Calcitonin Gene-Related Peptide - metabolism chronic pain Chronic Pain - genetics Chronic Pain - metabolism Chronic Pain - pathology colony-stimulating factor 1 high-frequency stimulation Long-Term Potentiation Mice Mice, Transgenic microglia Microglia - metabolism Microglia - pathology Neuronal Plasticity Rats Rats, Sprague-Dawley Receptors, N-Methyl-D-Aspartate - genetics Receptors, N-Methyl-D-Aspartate - metabolism Spinal Cord Dorsal Horn - metabolism Spinal Cord Dorsal Horn - pathology |
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| Title | Microglia Are Indispensable for Synaptic Plasticity in the Spinal Dorsal Horn and Chronic Pain |
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