Single-cell RNA sequencing reveals time- and sex-specific responses of mouse spinal cord microglia to peripheral nerve injury and links ApoE to chronic pain

Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it remains unclear whether distinct microglia subpopulations or states contribute to different stages of pain development and maintenance. Usin...

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Published in:	Nature communications Vol. 13; no. 1; pp. 843 - 16
Main Authors:	Tansley, Shannon, Uttam, Sonali, Ureña Guzmán, Alba, Yaqubi, Moein, Pacis, Alain, Parisien, Marc, Deamond, Haley, Wong, Calvin, Rabau, Oded, Brown, Nicole, Haglund, Lisbet, Ouellet, Jean, Santaguida, Carlo, Ribeiro-da-Silva, Alfredo, Tahmasebi, Soroush, Prager-Khoutorsky, Masha, Ragoussis, Jiannis, Zhang, Ji, Salter, Michael W., Diatchenko, Luda, Healy, Luke M., Mogil, Jeffrey S., Khoutorsky, Arkady
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 11.02.2022 Nature Publishing Group Nature Portfolio
Subjects:	14 14/19 38 45 631/378/2596/1953 692/699/375/1692 Animals Apolipoprotein E Apolipoproteins E - genetics Cell Proliferation Chronic pain Chronic Pain - genetics Developmental stages Female Gene Expression Gene sequencing Humanities and Social Sciences Hypersensitivity Inflammation Injuries Male Males Mice Mice, Inbred C57BL Microglia multidisciplinary Pain Peripheral Nerve Injuries Peripheral nerves Peripheral neuropathy Polymorphism, Genetic Ribonucleic acid RNA Science Science (multidisciplinary) Sequence analysis Sequence Analysis, RNA Sex Spinal Cord Spinal cord injuries Subpopulations Transcription
ISSN:	2041-1723, 2041-1723
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Abstract	Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it remains unclear whether distinct microglia subpopulations or states contribute to different stages of pain development and maintenance. Using single-cell RNA-sequencing, we show that peripheral nerve injury induces the generation of a male-specific inflammatory microglia subtype, and demonstrate increased proliferation of microglia in male as compared to female mice. We also show time- and sex-specific transcriptional changes in different microglial subpopulations following peripheral nerve injury. Apolipoprotein E ( Apoe ) is the top upregulated gene in spinal cord microglia at chronic time points after peripheral nerve injury in mice. Furthermore, polymorphisms in the APOE gene in humans are associated with chronic pain. Single-cell RNA sequencing analysis of human spinal cord microglia reveals a subpopulation with a disease-related transcriptional signature. Our data provide a detailed analysis of transcriptional states of mouse and human spinal cord microglia, and identify a link between ApoE and chronic pain in humans. Microglia subpopulations may differentially contribute to pain. Here, the authors show that peripheral nerve injury induces time- and sex-specific transcriptional changes in mouse spinal cord microglia subpopulations and that ApoE is linked to neuropathic pain hypersensitivity in mice and humans.
AbstractList	Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it remains unclear whether distinct microglia subpopulations or states contribute to different stages of pain development and maintenance. Using single-cell RNA-sequencing, we show that peripheral nerve injury induces the generation of a male-specific inflammatory microglia subtype, and demonstrate increased proliferation of microglia in male as compared to female mice. We also show time- and sex-specific transcriptional changes in different microglial subpopulations following peripheral nerve injury. Apolipoprotein E ( Apoe ) is the top upregulated gene in spinal cord microglia at chronic time points after peripheral nerve injury in mice. Furthermore, polymorphisms in the APOE gene in humans are associated with chronic pain. Single-cell RNA sequencing analysis of human spinal cord microglia reveals a subpopulation with a disease-related transcriptional signature. Our data provide a detailed analysis of transcriptional states of mouse and human spinal cord microglia, and identify a link between ApoE and chronic pain in humans. Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it remains unclear whether distinct microglia subpopulations or states contribute to different stages of pain development and maintenance. Using single-cell RNA-sequencing, we show that peripheral nerve injury induces the generation of a male-specific inflammatory microglia subtype, and demonstrate increased proliferation of microglia in male as compared to female mice. We also show time- and sex-specific transcriptional changes in different microglial subpopulations following peripheral nerve injury. Apolipoprotein E ( Apoe ) is the top upregulated gene in spinal cord microglia at chronic time points after peripheral nerve injury in mice. Furthermore, polymorphisms in the APOE gene in humans are associated with chronic pain. Single-cell RNA sequencing analysis of human spinal cord microglia reveals a subpopulation with a disease-related transcriptional signature. Our data provide a detailed analysis of transcriptional states of mouse and human spinal cord microglia, and identify a link between ApoE and chronic pain in humans. Microglia subpopulations may differentially contribute to pain. Here, the authors show that peripheral nerve injury induces time- and sex-specific transcriptional changes in mouse spinal cord microglia subpopulations and that ApoE is linked to neuropathic pain hypersensitivity in mice and humans. Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it remains unclear whether distinct microglia subpopulations or states contribute to different stages of pain development and maintenance. Using single-cell RNA-sequencing, we show that peripheral nerve injury induces the generation of a male-specific inflammatory microglia subtype, and demonstrate increased proliferation of microglia in male as compared to female mice. We also show time- and sex-specific transcriptional changes in different microglial subpopulations following peripheral nerve injury. Apolipoprotein E (Apoe) is the top upregulated gene in spinal cord microglia at chronic time points after peripheral nerve injury in mice. Furthermore, polymorphisms in the APOE gene in humans are associated with chronic pain. Single-cell RNA sequencing analysis of human spinal cord microglia reveals a subpopulation with a disease-related transcriptional signature. Our data provide a detailed analysis of transcriptional states of mouse and human spinal cord microglia, and identify a link between ApoE and chronic pain in humans. Microglia subpopulations may differentially contribute to pain. Here, the authors show that peripheral nerve injury induces time- and sex-specific transcriptional changes in mouse spinal cord microglia subpopulations and that ApoE is linked to neuropathic pain hypersensitivity in mice and humans. Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it remains unclear whether distinct microglia subpopulations or states contribute to different stages of pain development and maintenance. Using single-cell RNA-sequencing, we show that peripheral nerve injury induces the generation of a male-specific inflammatory microglia subtype, and demonstrate increased proliferation of microglia in male as compared to female mice. We also show time- and sex-specific transcriptional changes in different microglial subpopulations following peripheral nerve injury. Apolipoprotein E (Apoe) is the top upregulated gene in spinal cord microglia at chronic time points after peripheral nerve injury in mice. Furthermore, polymorphisms in the APOE gene in humans are associated with chronic pain. Single-cell RNA sequencing analysis of human spinal cord microglia reveals a subpopulation with a disease-related transcriptional signature. Our data provide a detailed analysis of transcriptional states of mouse and human spinal cord microglia, and identify a link between ApoE and chronic pain in humans. Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it remains unclear whether distinct microglia subpopulations or states contribute to different stages of pain development and maintenance. Using single-cell RNA-sequencing, we show that peripheral nerve injury induces the generation of a male-specific inflammatory microglia subtype, and demonstrate increased proliferation of microglia in male as compared to female mice. We also show time- and sex-specific transcriptional changes in different microglial subpopulations following peripheral nerve injury. Apolipoprotein E (Apoe) is the top upregulated gene in spinal cord microglia at chronic time points after peripheral nerve injury in mice. Furthermore, polymorphisms in the APOE gene in humans are associated with chronic pain. Single-cell RNA sequencing analysis of human spinal cord microglia reveals a subpopulation with a disease-related transcriptional signature. Our data provide a detailed analysis of transcriptional states of mouse and human spinal cord microglia, and identify a link between ApoE and chronic pain in humans.Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it remains unclear whether distinct microglia subpopulations or states contribute to different stages of pain development and maintenance. Using single-cell RNA-sequencing, we show that peripheral nerve injury induces the generation of a male-specific inflammatory microglia subtype, and demonstrate increased proliferation of microglia in male as compared to female mice. We also show time- and sex-specific transcriptional changes in different microglial subpopulations following peripheral nerve injury. Apolipoprotein E (Apoe) is the top upregulated gene in spinal cord microglia at chronic time points after peripheral nerve injury in mice. Furthermore, polymorphisms in the APOE gene in humans are associated with chronic pain. Single-cell RNA sequencing analysis of human spinal cord microglia reveals a subpopulation with a disease-related transcriptional signature. Our data provide a detailed analysis of transcriptional states of mouse and human spinal cord microglia, and identify a link between ApoE and chronic pain in humans. Microglia subpopulations may differentially contribute to pain. Here, the authors show that peripheral nerve injury induces time- and sex-specific transcriptional changes in mouse spinal cord microglia subpopulations and that ApoE is linked to neuropathic pain hypersensitivity in mice and humans.
ArticleNumber	843
Author	Ureña Guzmán, Alba Ribeiro-da-Silva, Alfredo Santaguida, Carlo Uttam, Sonali Salter, Michael W. Zhang, Ji Brown, Nicole Deamond, Haley Wong, Calvin Khoutorsky, Arkady Yaqubi, Moein Parisien, Marc Tansley, Shannon Ouellet, Jean Diatchenko, Luda Pacis, Alain Mogil, Jeffrey S. Tahmasebi, Soroush Prager-Khoutorsky, Masha Healy, Luke M. Ragoussis, Jiannis Haglund, Lisbet Rabau, Oded
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Diatchenko, Luda organization: Department of Anesthesia and Faculty of Dental Medicine and Oral Health Sciences, McGill University, Alan Edwards Centre for Research on Pain, McGill University – sequence: 21 givenname: Luke M. surname: Healy fullname: Healy, Luke M. email: luke.healy@mcgill.ca organization: Neuroimmunology Unit, Montreal Neurological Institute, McGill University – sequence: 22 givenname: Jeffrey S. orcidid: 0000-0003-1359-5720 surname: Mogil fullname: Mogil, Jeffrey S. email: jeffrey.mogil@mcgill.ca organization: Department of Anesthesia and Faculty of Dental Medicine and Oral Health Sciences, McGill University, Department of Psychology, McGill University, Alan Edwards Centre for Research on Pain, McGill University – sequence: 23 givenname: Arkady orcidid: 0000-0003-3846-8728 surname: Khoutorsky fullname: Khoutorsky, Arkady email: arkady.khoutorsky@mcgill.ca organization: Department of Anesthesia and Faculty of Dental Medicine and Oral Health Sciences, McGill University, Alan Edwards Centre for Research on Pain, McGill University
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/35149686$$D View this record in MEDLINE/PubMed
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Snippet	Activation of microglia in the spinal cord following peripheral nerve injury is critical for the development of long-lasting pain hypersensitivity. However, it... Microglia subpopulations may differentially contribute to pain. Here, the authors show that peripheral nerve injury induces time- and sex-specific...
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SubjectTerms	14 14/19 38 45 631/378/2596/1953 692/699/375/1692 Animals Apolipoprotein E Apolipoproteins E - genetics Cell Proliferation Chronic pain Chronic Pain - genetics Developmental stages Female Gene Expression Gene sequencing Humanities and Social Sciences Hypersensitivity Inflammation Injuries Male Males Mice Mice, Inbred C57BL Microglia multidisciplinary Pain Peripheral Nerve Injuries Peripheral nerves Peripheral neuropathy Polymorphism, Genetic Ribonucleic acid RNA Science Science (multidisciplinary) Sequence analysis Sequence Analysis, RNA Sex Spinal Cord Spinal cord injuries Subpopulations Transcription
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Title	Single-cell RNA sequencing reveals time- and sex-specific responses of mouse spinal cord microglia to peripheral nerve injury and links ApoE to chronic pain
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