Neuropeptide CGRP Limits Group 2 Innate Lymphoid Cell Responses and Constrains Type 2 Inflammation

Innate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling helminth infection. While the molecular understanding of ILC2 responses has advanced, the complexity of microenvironmental factors impacting ILC2s...

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Bibliographic Details
Published inImmunity (Cambridge, Mass.) Vol. 51; no. 4; pp. 682 - 695.e6
Main Authors Nagashima, Hiroyuki, Mahlakõiv, Tanel, Shih, Han-Yu, Davis, Fred P., Meylan, Francoise, Huang, Yuefeng, Harrison, Oliver J., Yao, Chen, Mikami, Yohei, Urban, Joseph F., Caron, Kathleen M., Belkaid, Yasmine, Kanno, Yuka, Artis, David, O’Shea, John J.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 15.10.2019
Elsevier Limited
Subjects
Animals
Calcitonin
Calcitonin gene-related peptide
Cells, Cultured
CGRP
Cytokines
Cytokines - metabolism
Data points
Expulsion
Flow cytometry
Gene expression
Homeostasis
host defense
IL-33
Immune response
Immunity, Innate
immunoregulation
Infections
Inflammation
Inflammation - immunology
Inflammatory bowel disease
Innate immunity
innate lymphoid cells
Interleukin 13
Interleukin 5
Interleukin-33 - metabolism
Lymphocytes
Lymphocytes - immunology
Lymphoid cells
Mice
Mice, Inbred C57BL
Mice, Knockout
Mucosa
Neuromedin
Neuropeptides
Neuropeptides - metabolism
Nippostrongylus - physiology
Nippostrongylus brasiliensis
NMU
Receptors, Calcitonin Gene-Related Peptide - genetics
Receptors, Calcitonin Gene-Related Peptide - metabolism
Scholarships & fellowships
Single-Cell Analysis
single-cell RNA-seq
Strongylida Infections - immunology
Th2 Cells - immunology
Transplantation Chimera
host defense
NMU
immunoregulation
neuropeptides
single-cell RNA-seq
cytokines
innate lymphoid cells
CGRP
IL-33
Nippostrongylus brasiliensis
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Abstract Innate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling helminth infection. While the molecular understanding of ILC2 responses has advanced, the complexity of microenvironmental factors impacting ILC2s is becoming increasingly apparent. Herein, we used single-cell analysis to explore the diversity of gene expression among lung lymphocytes during helminth infection. Following infection, we identified a subset of ILC2s that preferentially expressed Il5-encoding interleukin (IL)-5, together with Calca-encoding calcitonin gene-related peptide (CGRP) and its cognate receptor components. CGRP in concert with IL-33 and neuromedin U (NMU) supported IL-5 but constrained IL-13 expression and ILC2 proliferation. Without CGRP signaling, ILC2 responses and worm expulsion were enhanced. Collectively, these data point to CGRP as a context-dependent negative regulatory factor that shapes innate lymphocyte responses to alarmins and neuropeptides during type 2 innate immune responses. [Display omitted] •Single-cell analysis reveals heterogeneity of ILC2 responses to N. brasiliensis•Il5hiILC2s express CGRP and its receptor following helminth infection•CGRP modulates type 2 cytokine production by ILC2s induced by alarmin and NMU•CGRP constrains the magnitude of innate type 2 responses following helminth infection Neuronal and immune systems coordinately orchestrate responses at mucosal barriers. Nagashima et al. applied scRNA-seq technology to track type 2 immune responses in worm infection, identifying neuropeptide CGRP as a factor that modulates inflammation. The study suggests that CGRP may be a useful target in type 2 inflammation.
AbstractList Innate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling helminth infection. While the molecular understanding of ILC2 responses has advanced, the complexity of microenvironmental factors impacting ILC2s is becoming increasingly apparent. Herein, we used single-cell analysis to explore the diversity of gene expression among lung lymphocytes during helminth infection. Following infection, we identified a subset of ILC2s that preferentially expressed Il5-encoding interleukin (IL)-5, together with Calca-encoding calcitonin gene-related peptide (CGRP) and its cognate receptor components. CGRP in concert with IL-33 and neuromedin U (NMU) supported IL-5 but constrained IL-13 expression and ILC2 proliferation. Without CGRP signaling, ILC2 responses and worm expulsion were enhanced. Collectively, these data point to CGRP as a context-dependent negative regulatory factor that shapes innate lymphocyte responses to alarmins and neuropeptides during type 2 innate immune responses.Innate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling helminth infection. While the molecular understanding of ILC2 responses has advanced, the complexity of microenvironmental factors impacting ILC2s is becoming increasingly apparent. Herein, we used single-cell analysis to explore the diversity of gene expression among lung lymphocytes during helminth infection. Following infection, we identified a subset of ILC2s that preferentially expressed Il5-encoding interleukin (IL)-5, together with Calca-encoding calcitonin gene-related peptide (CGRP) and its cognate receptor components. CGRP in concert with IL-33 and neuromedin U (NMU) supported IL-5 but constrained IL-13 expression and ILC2 proliferation. Without CGRP signaling, ILC2 responses and worm expulsion were enhanced. Collectively, these data point to CGRP as a context-dependent negative regulatory factor that shapes innate lymphocyte responses to alarmins and neuropeptides during type 2 innate immune responses.
Innate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling helminth infection. While the molecular understanding of ILC2 responses has advanced, the complexity of microenvironmental factors impacting ILC2s is becoming increasingly apparent. Herein, we used single-cell analysis to explore the diversity of gene expression among lung lymphocytes during helminth infection. Following infection, we identified a subset of ILC2s that preferentially expressed Il5-encoding interleukin (IL)-5, together with Calca-encoding calcitonin gene-related peptide (CGRP) and its cognate receptor components. CGRP in concert with IL-33 and neuromedin U (NMU) supported IL-5 but constrained IL-13 expression and ILC2 proliferation. Without CGRP signaling, ILC2 responses and worm expulsion were enhanced. Collectively, these data point to CGRP as a context-dependent negative regulatory factor that shapes innate lymphocyte responses to alarmins and neuropeptides during type 2 innate immune responses.
SummaryInnate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling helminth infection. While the molecular understanding of ILC2 responses has advanced, the complexity of microenvironmental factors impacting ILC2s is becoming increasingly apparent. Herein, we used single-cell analysis to explore the diversity of gene expression among lung lymphocytes during helminth infection. Following infection, we identified a subset of ILC2s that preferentially expressed Il5-encoding interleukin (IL)-5, together with Calca-encoding calcitonin gene-related peptide (CGRP) and its cognate receptor components. CGRP in concert with IL-33 and neuromedin U (NMU) supported IL-5 but constrained IL-13 expression and ILC2 proliferation. Without CGRP signaling, ILC2 responses and worm expulsion were enhanced. Collectively, these data point to CGRP as a context-dependent negative regulatory factor that shapes innate lymphocyte responses to alarmins and neuropeptides during type 2 innate immune responses.
Innate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling helminth infection. While the molecular understanding of ILC2 responses has advanced, the complexity of microenvironmental factors impacting ILC2s is becoming increasingly apparent. Herein, we used single cell analysis to explore the diversity of gene expression among lung lymphocytes during helminth infection. Following infection, we identified a subset of ILC2s that preferentially expressed Il5 encoding interleukin (IL)-5, together with Calca encoding calcitonin gene related peptide (CGRP) and its cognate receptor components. CGRP in concert with IL-33 and neuromedin-U (NMU) supported IL-5 but constrained IL-13 expression and ILC2 proliferation. Without CGRP signaling, ILC2 responses and worm expulsion were enhanced. Collectively, these data point to CGRP as a context dependent negative regulatory factor that shapes innate lymphocyte responses to alarmins and neuropeptides during type 2 innate immune responses. Neuronal and immune systems coordinately orchestrate responses at mucosal barriers. Nagashima et al applied scRNA-seq technology to track type 2 immune responses in worm infection, identifying neuropeptide CGRP as a factor that modulates inflammation. The study suggests that CGRP may be a useful target in type 2 inflammation.
Innate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling helminth infection. While the molecular understanding of ILC2 responses has advanced, the complexity of microenvironmental factors impacting ILC2s is becoming increasingly apparent. Herein, we used single-cell analysis to explore the diversity of gene expression among lung lymphocytes during helminth infection. Following infection, we identified a subset of ILC2s that preferentially expressed Il5-encoding interleukin (IL)-5, together with Calca-encoding calcitonin gene-related peptide (CGRP) and its cognate receptor components. CGRP in concert with IL-33 and neuromedin U (NMU) supported IL-5 but constrained IL-13 expression and ILC2 proliferation. Without CGRP signaling, ILC2 responses and worm expulsion were enhanced. Collectively, these data point to CGRP as a context-dependent negative regulatory factor that shapes innate lymphocyte responses to alarmins and neuropeptides during type 2 innate immune responses. [Display omitted] •Single-cell analysis reveals heterogeneity of ILC2 responses to N. brasiliensis•Il5hiILC2s express CGRP and its receptor following helminth infection•CGRP modulates type 2 cytokine production by ILC2s induced by alarmin and NMU•CGRP constrains the magnitude of innate type 2 responses following helminth infection Neuronal and immune systems coordinately orchestrate responses at mucosal barriers. Nagashima et al. applied scRNA-seq technology to track type 2 immune responses in worm infection, identifying neuropeptide CGRP as a factor that modulates inflammation. The study suggests that CGRP may be a useful target in type 2 inflammation.
Author Yao, Chen
Davis, Fred P.
Mikami, Yohei
Nagashima, Hiroyuki
Kanno, Yuka
Harrison, Oliver J.
Shih, Han-Yu
Caron, Kathleen M.
Artis, David
O’Shea, John J.
Meylan, Francoise
Huang, Yuefeng
Mahlakõiv, Tanel
Urban, Joseph F.
Belkaid, Yasmine
AuthorAffiliation 2 Jill Roberts Institute for Research in Inflammatory Bowel Disease, Joan and Sanford I. Weill Department of Medicine, Department of Microbiology and Immunology, Weill Cornell Medicine, Cornell University, New York, NY 10021, USA
4 Metaorganism Immunity Section, Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA
6 Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
9 Lead contact
3 Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA
7 Present address: Department of Microbiology and Immunology, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
5 U.S. Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, Diet, Genomics, and Immunology Laboratory, Beltsville, MD 20705-2350, USA
1 Lympho
AuthorAffiliation_xml – name: 3 Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA
– name: 4 Metaorganism Immunity Section, Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA
– name: 1 Lymphocyte Cell Biology Section, Molecular Immunology and Inflammation Branch, National Institute of Arthritis, Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD 20892, USA
– name: 9 Lead contact
– name: 2 Jill Roberts Institute for Research in Inflammatory Bowel Disease, Joan and Sanford I. Weill Department of Medicine, Department of Microbiology and Immunology, Weill Cornell Medicine, Cornell University, New York, NY 10021, USA
– name: 5 U.S. Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, Diet, Genomics, and Immunology Laboratory, Beltsville, MD 20705-2350, USA
– name: 6 Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
– name: 7 Present address: Department of Microbiology and Immunology, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
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  surname: Nagashima
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  organization: Lymphocyte Cell Biology Section, Molecular Immunology and Inflammation Branch, National Institute of Arthritis, Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892, USA
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  fullname: Mahlakõiv, Tanel
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  givenname: Han-Yu
  surname: Shih
  fullname: Shih, Han-Yu
  organization: Lymphocyte Cell Biology Section, Molecular Immunology and Inflammation Branch, National Institute of Arthritis, Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892, USA
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  givenname: Fred P.
  surname: Davis
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  surname: Mikami
  fullname: Mikami, Yohei
  organization: Lymphocyte Cell Biology Section, Molecular Immunology and Inflammation Branch, National Institute of Arthritis, Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892, USA
– sequence: 10
  givenname: Joseph F.
  surname: Urban
  fullname: Urban, Joseph F.
  organization: US Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, Diet, Genomics, and Immunology Laboratory, Beltsville, MD 20705-2350, USA
– sequence: 11
  givenname: Kathleen M.
  surname: Caron
  fullname: Caron, Kathleen M.
  organization: Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
– sequence: 12
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  surname: Belkaid
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  organization: Metaorganism Immunity Section, Laboratory of Immune System Biology, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA
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  givenname: Yuka
  surname: Kanno
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  surname: O’Shea
  fullname: O’Shea, John J.
  email: john.oshea@nih.gov
  organization: Lymphocyte Cell Biology Section, Molecular Immunology and Inflammation Branch, National Institute of Arthritis, Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31353223$$D View this record in MEDLINE/PubMed
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Keywords host defense
NMU
immunoregulation
neuropeptides
single-cell RNA-seq
cytokines
innate lymphoid cells
CGRP
IL-33
Nippostrongylus brasiliensis
Language English
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AUTHOR CONTRIBUTIONS
H.N. and T.M. designed the project, performed and analyzed experiments with assistance and advice from H-Y.S., F.P.D., F.M., Y.H., O.J.H., C.Y and YM. . H-Y.S. performed and analyzed ATAC-seq. F.P.D. performed computational analysis. J.F.U. and K.M.C. contributed to analytical tools and input regarding experimental design. K.M.C., Y.B., D.A., Y.K., and JO’S. planned and supervised this project. H.N., T.M., D.A., Y.K. and JO’S wrote the manuscript with input, advice and revisions from all authors.
These authors contributed equally
OpenAccessLink http://www.cell.com/article/S1074761319302791/pdf
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Snippet Innate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and controlling...
SummaryInnate lymphocytes maintain tissue homeostasis at mucosal barriers, with group 2 innate lymphoid cells (ILC2s) producing type 2 cytokines and...
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SubjectTerms Animals
Calcitonin
Calcitonin gene-related peptide
Cells, Cultured
CGRP
Cytokines
Cytokines - metabolism
Data points
Expulsion
Flow cytometry
Gene expression
Homeostasis
host defense
IL-33
Immune response
Immunity, Innate
immunoregulation
Infections
Inflammation
Inflammation - immunology
Inflammatory bowel disease
Innate immunity
innate lymphoid cells
Interleukin 13
Interleukin 5
Interleukin-33 - metabolism
Lymphocytes
Lymphocytes - immunology
Lymphoid cells
Mice
Mice, Inbred C57BL
Mice, Knockout
Mucosa
Neuromedin
Neuropeptides
Neuropeptides - metabolism
Nippostrongylus - physiology
Nippostrongylus brasiliensis
NMU
Receptors, Calcitonin Gene-Related Peptide - genetics
Receptors, Calcitonin Gene-Related Peptide - metabolism
Scholarships & fellowships
Single-Cell Analysis
single-cell RNA-seq
Strongylida Infections - immunology
Th2 Cells - immunology
Transplantation Chimera
Title Neuropeptide CGRP Limits Group 2 Innate Lymphoid Cell Responses and Constrains Type 2 Inflammation
URI https://dx.doi.org/10.1016/j.immuni.2019.06.009
https://www.ncbi.nlm.nih.gov/pubmed/31353223
https://www.proquest.com/docview/2305761513
https://www.proquest.com/docview/2266334127
https://pubmed.ncbi.nlm.nih.gov/PMC6801073
Volume 51
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