IL-5Rα marks nasal polyp IgG4- and IgE-expressing cells in aspirin-exacerbated respiratory disease
The cause of severe nasal polyposis in aspirin-exacerbated respiratory disease (AERD) is unknown. Elevated antibody levels have been associated with disease severity in nasal polyps, but upstream drivers of local antibody production in nasal polyps are undetermined. We sought to identify upstream dr...
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| Published in | Journal of allergy and clinical immunology Vol. 145; no. 6; pp. 1574 - 1584 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.06.2020
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 1097-6825 |
| DOI | 10.1016/j.jaci.2020.02.035 |
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| Abstract | The cause of severe nasal polyposis in aspirin-exacerbated respiratory disease (AERD) is unknown. Elevated antibody levels have been associated with disease severity in nasal polyps, but upstream drivers of local antibody production in nasal polyps are undetermined.
We sought to identify upstream drivers and phenotypic properties of local antibody-expressing cells in nasal polyps from subjects with AERD.
Sinus tissue was obtained from subjects with AERD, chronic rhinosinusitis (CRS) with nasal polyps (CRSwNP), CRS without nasal polyps, and controls without CRS. Tissue antibody levels were quantified via ELISA and immunohistochemistry and were correlated with disease severity. Antibody-expressing cells were profiled with single-cell RNA sequencing, flow cytometry, and immunofluorescence, with IL-5Rα function determined through IL-5 stimulation and subsequent RNA sequencing and quantitative PCR.
Tissue IgE and IgG4 levels were elevated in AERD compared with in controls (P < .01 for IgE and P < .001 for IgG4 vs CRSwNP). Subjects with AERD whose nasal polyps recurred rapidly had higher IgE levels than did subjects with AERD, with slower regrowth (P = .005). Single-cell RNA sequencing revealed increased IL5RA, IGHG4, and IGHE in antibody-expressing cells from patients with AERD compared with antibody-expressing cells from patients with CRSwNP. There were more IL-5Rα+ plasma cells in the polyp tissue from those with AERD than in polyp tissue from those with CRSwNP (P = .026). IL-5 stimulation of plasma cells in vitro induced changes in a distinct set of transcripts.
Our study identifies an increase in antibody-expressing cells in AERD defined by transcript enrichment of IL5RA and IGHG4 or IGHE, with confirmed surface expression of IL-5Rα and functional IL-5 signaling. Tissue IgE and IgG4 levels are elevated in AERD, and higher IgE levels are associated with faster nasal polyp regrowth. Our findings suggest a role for IL-5Rα+ antibody-expressing cells in facilitating local antibody production and severe nasal polyps in AERD. |
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| AbstractList | Our study identified a plasma cell population enriched in the nasal polyps of patients with aspirin-exacerbated respiratory disease, defined by transcript enrichment of
IL5RA, IGHG4
and
IGHE
, surface expression of IL-5Rα, and a functional IL-5 signaling pathway. The cause of severe nasal polyposis in aspirin-exacerbated respiratory disease (AERD) is unknown. Elevated antibody levels have been associated with disease severity in nasal polyps, but upstream drivers of local antibody production in nasal polyps are undetermined. We sought to identify upstream drivers and phenotypic properties of local antibody-expressing cells in nasal polyps from subjects with AERD. Sinus tissue was obtained from subjects with AERD, chronic rhinosinusitis (CRS) with nasal polyps (CRSwNP), CRS without nasal polyps, and controls without CRS. Tissue antibody levels were quantified via ELISA and immunohistochemistry and were correlated with disease severity. Antibody-expressing cells were profiled with single-cell RNA sequencing, flow cytometry, and immunofluorescence, with IL-5Rα function determined through IL-5 stimulation and subsequent RNA sequencing and quantitative PCR. Tissue IgE and IgG4 levels were elevated in AERD compared with in controls (P < .01 for IgE and P < .001 for IgG4 vs CRSwNP). Subjects with AERD whose nasal polyps recurred rapidly had higher IgE levels than did subjects with AERD, with slower regrowth (P = .005). Single-cell RNA sequencing revealed increased IL5RA, IGHG4, and IGHE in antibody-expressing cells from patients with AERD compared with antibody-expressing cells from patients with CRSwNP. There were more IL-5Rα plasma cells in the polyp tissue from those with AERD than in polyp tissue from those with CRSwNP (P = .026). IL-5 stimulation of plasma cells in vitro induced changes in a distinct set of transcripts. Our study identifies an increase in antibody-expressing cells in AERD defined by transcript enrichment of IL5RA and IGHG4 or IGHE, with confirmed surface expression of IL-5Rα and functional IL-5 signaling. Tissue IgE and IgG4 levels are elevated in AERD, and higher IgE levels are associated with faster nasal polyp regrowth. Our findings suggest a role for IL-5Rα antibody-expressing cells in facilitating local antibody production and severe nasal polyps in AERD. The cause of severe nasal polyposis in aspirin-exacerbated respiratory disease (AERD) is unknown. Elevated antibody levels have been associated with disease severity in nasal polyps, but upstream drivers of local antibody production in nasal polyps are undetermined. We sought to identify upstream drivers and phenotypic properties of local antibody-expressing cells in nasal polyps from subjects with AERD. Sinus tissue was obtained from subjects with AERD, chronic rhinosinusitis (CRS) with nasal polyps (CRSwNP), CRS without nasal polyps, and controls without CRS. Tissue antibody levels were quantified via ELISA and immunohistochemistry and were correlated with disease severity. Antibody-expressing cells were profiled with single-cell RNA sequencing, flow cytometry, and immunofluorescence, with IL-5Rα function determined through IL-5 stimulation and subsequent RNA sequencing and quantitative PCR. Tissue IgE and IgG4 levels were elevated in AERD compared with in controls (P < .01 for IgE and P < .001 for IgG4 vs CRSwNP). Subjects with AERD whose nasal polyps recurred rapidly had higher IgE levels than did subjects with AERD, with slower regrowth (P = .005). Single-cell RNA sequencing revealed increased IL5RA, IGHG4, and IGHE in antibody-expressing cells from patients with AERD compared with antibody-expressing cells from patients with CRSwNP. There were more IL-5Rα+ plasma cells in the polyp tissue from those with AERD than in polyp tissue from those with CRSwNP (P = .026). IL-5 stimulation of plasma cells in vitro induced changes in a distinct set of transcripts. Our study identifies an increase in antibody-expressing cells in AERD defined by transcript enrichment of IL5RA and IGHG4 or IGHE, with confirmed surface expression of IL-5Rα and functional IL-5 signaling. Tissue IgE and IgG4 levels are elevated in AERD, and higher IgE levels are associated with faster nasal polyp regrowth. Our findings suggest a role for IL-5Rα+ antibody-expressing cells in facilitating local antibody production and severe nasal polyps in AERD. The cause of severe nasal polyposis in aspirin-exacerbated respiratory disease (AERD) is unknown. Elevated antibody levels have been associated with disease severity in nasal polyps, but upstream drivers of local antibody production in nasal polyps are undetermined.BACKGROUNDThe cause of severe nasal polyposis in aspirin-exacerbated respiratory disease (AERD) is unknown. Elevated antibody levels have been associated with disease severity in nasal polyps, but upstream drivers of local antibody production in nasal polyps are undetermined.We sought to identify upstream drivers and phenotypic properties of local antibody-expressing cells in nasal polyps from subjects with AERD.OBJECTIVEWe sought to identify upstream drivers and phenotypic properties of local antibody-expressing cells in nasal polyps from subjects with AERD.Sinus tissue was obtained from subjects with AERD, chronic rhinosinusitis (CRS) with nasal polyps (CRSwNP), CRS without nasal polyps, and controls without CRS. Tissue antibody levels were quantified via ELISA and immunohistochemistry and were correlated with disease severity. Antibody-expressing cells were profiled with single-cell RNA sequencing, flow cytometry, and immunofluorescence, with IL-5Rα function determined through IL-5 stimulation and subsequent RNA sequencing and quantitative PCR.METHODSSinus tissue was obtained from subjects with AERD, chronic rhinosinusitis (CRS) with nasal polyps (CRSwNP), CRS without nasal polyps, and controls without CRS. Tissue antibody levels were quantified via ELISA and immunohistochemistry and were correlated with disease severity. Antibody-expressing cells were profiled with single-cell RNA sequencing, flow cytometry, and immunofluorescence, with IL-5Rα function determined through IL-5 stimulation and subsequent RNA sequencing and quantitative PCR.Tissue IgE and IgG4 levels were elevated in AERD compared with in controls (P < .01 for IgE and P < .001 for IgG4 vs CRSwNP). Subjects with AERD whose nasal polyps recurred rapidly had higher IgE levels than did subjects with AERD, with slower regrowth (P = .005). Single-cell RNA sequencing revealed increased IL5RA, IGHG4, and IGHE in antibody-expressing cells from patients with AERD compared with antibody-expressing cells from patients with CRSwNP. There were more IL-5Rα+ plasma cells in the polyp tissue from those with AERD than in polyp tissue from those with CRSwNP (P = .026). IL-5 stimulation of plasma cells in vitro induced changes in a distinct set of transcripts.RESULTSTissue IgE and IgG4 levels were elevated in AERD compared with in controls (P < .01 for IgE and P < .001 for IgG4 vs CRSwNP). Subjects with AERD whose nasal polyps recurred rapidly had higher IgE levels than did subjects with AERD, with slower regrowth (P = .005). Single-cell RNA sequencing revealed increased IL5RA, IGHG4, and IGHE in antibody-expressing cells from patients with AERD compared with antibody-expressing cells from patients with CRSwNP. There were more IL-5Rα+ plasma cells in the polyp tissue from those with AERD than in polyp tissue from those with CRSwNP (P = .026). IL-5 stimulation of plasma cells in vitro induced changes in a distinct set of transcripts.Our study identifies an increase in antibody-expressing cells in AERD defined by transcript enrichment of IL5RA and IGHG4 or IGHE, with confirmed surface expression of IL-5Rα and functional IL-5 signaling. Tissue IgE and IgG4 levels are elevated in AERD, and higher IgE levels are associated with faster nasal polyp regrowth. Our findings suggest a role for IL-5Rα+ antibody-expressing cells in facilitating local antibody production and severe nasal polyps in AERD.CONCLUSIONSOur study identifies an increase in antibody-expressing cells in AERD defined by transcript enrichment of IL5RA and IGHG4 or IGHE, with confirmed surface expression of IL-5Rα and functional IL-5 signaling. Tissue IgE and IgG4 levels are elevated in AERD, and higher IgE levels are associated with faster nasal polyp regrowth. Our findings suggest a role for IL-5Rα+ antibody-expressing cells in facilitating local antibody production and severe nasal polyps in AERD. |
| Author | Buchheit, Kathleen M. Lewis, Erin Ordovas-Montanes, Jose Vukovic, Marko Barrett, Nora A. Lai, Juying Laidlaw, Tanya M. Bankova, Lora G. Dwyer, Daniel F. Boyce, Joshua A. Shalek, Alex K. Bhattacharyya, Neil Katz, Howard R. |
| AuthorAffiliation | 5 Institute for Medical Engineering and Science (IMES), Department of Chemistry, and Koch Institute for Integrative Cancer Research, MIT, Cambridge, MA, USA 9 Harvard-MIT Division of Health Sciences & Technology, Cambridge, MA, USA 6 Broad Institute of MIT and Harvard, Cambridge, MA, USA 7 Ragon Institute of MGH, MIT and Harvard, Cambridge, MA, USA 2 Department of Surgery, Harvard Medical School, Boston, MA 8 Division of Gastroenterology, Boston Children’s Hospital, Boston, MA, USA 1 Department of Medicine, Harvard Medical School, Boston, MA 3 Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, MA 4 Department of Otolaryngology, Massachusetts Eye and Ear Infirmary, Boston, MA |
| AuthorAffiliation_xml | – name: 6 Broad Institute of MIT and Harvard, Cambridge, MA, USA – name: 1 Department of Medicine, Harvard Medical School, Boston, MA – name: 4 Department of Otolaryngology, Massachusetts Eye and Ear Infirmary, Boston, MA – name: 5 Institute for Medical Engineering and Science (IMES), Department of Chemistry, and Koch Institute for Integrative Cancer Research, MIT, Cambridge, MA, USA – name: 3 Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, MA – name: 8 Division of Gastroenterology, Boston Children’s Hospital, Boston, MA, USA – name: 2 Department of Surgery, Harvard Medical School, Boston, MA – name: 7 Ragon Institute of MGH, MIT and Harvard, Cambridge, MA, USA – name: 9 Harvard-MIT Division of Health Sciences & Technology, Cambridge, MA, USA |
| Author_xml | – sequence: 1 givenname: Kathleen M. surname: Buchheit fullname: Buchheit, Kathleen M. organization: Department of Medicine, Harvard Medical School, Boston, Mass – sequence: 2 givenname: Daniel F. surname: Dwyer fullname: Dwyer, Daniel F. organization: Department of Medicine, Harvard Medical School, Boston, Mass – sequence: 3 givenname: Jose surname: Ordovas-Montanes fullname: Ordovas-Montanes, Jose organization: Institute for Medical Engineering and Science, Department of Chemistry, and Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, Mass – sequence: 4 givenname: Howard R. surname: Katz fullname: Katz, Howard R. organization: Department of Medicine, Harvard Medical School, Boston, Mass – sequence: 5 givenname: Erin surname: Lewis fullname: Lewis, Erin organization: Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass – sequence: 6 givenname: Marko surname: Vukovic fullname: Vukovic, Marko organization: Institute for Medical Engineering and Science, Department of Chemistry, and Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, Mass – sequence: 7 givenname: Juying surname: Lai fullname: Lai, Juying organization: Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass – sequence: 8 givenname: Lora G. surname: Bankova fullname: Bankova, Lora G. organization: Department of Medicine, Harvard Medical School, Boston, Mass – sequence: 9 givenname: Neil surname: Bhattacharyya fullname: Bhattacharyya, Neil organization: Department of Surgery, Harvard Medical School, Boston, Mass – sequence: 10 givenname: Alex K. surname: Shalek fullname: Shalek, Alex K. organization: Institute for Medical Engineering and Science, Department of Chemistry, and Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, Mass – sequence: 11 givenname: Nora A. surname: Barrett fullname: Barrett, Nora A. organization: Department of Medicine, Harvard Medical School, Boston, Mass – sequence: 12 givenname: Joshua A. surname: Boyce fullname: Boyce, Joshua A. organization: Department of Medicine, Harvard Medical School, Boston, Mass – sequence: 13 givenname: Tanya M. surname: Laidlaw fullname: Laidlaw, Tanya M. email: tlaidlaw@bwh.harvard.edu organization: Department of Medicine, Harvard Medical School, Boston, Mass |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32199912$$D View this record in MEDLINE/PubMed |
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| Copyright | 2020 American Academy of Allergy, Asthma & Immunology Copyright © 2020 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. |
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| Keywords | UMAP CRS Aspirin-exacerbated respiratory disease IgE AERD IgG4 CRSwNP nasal polyposis CRSsNP interleukin-5 scRNA-seq SPRI PC F(ab')2 chronic rhinosinusitis qPCR IL-5Rα plasma cell |
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| Snippet | The cause of severe nasal polyposis in aspirin-exacerbated respiratory disease (AERD) is unknown. Elevated antibody levels have been associated with disease... Our study identified a plasma cell population enriched in the nasal polyps of patients with aspirin-exacerbated respiratory disease, defined by transcript... |
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| SubjectTerms | Adult Aged Antibodies - metabolism Aspirin - adverse effects Aspirin-exacerbated respiratory disease chronic rhinosinusitis Female Humans IgE IgG4 IL-5Rα Immunoglobulin E - metabolism Immunoglobulin G - metabolism interleukin-5 Interleukin-5 - metabolism Interleukin-5 Receptor alpha Subunit - metabolism Male Middle Aged nasal polyposis Nasal Polyps - chemically induced Nasal Polyps - metabolism plasma cell Plasma Cells - drug effects Plasma Cells - metabolism Sequence Analysis, RNA - methods Sinusitis - chemically induced Sinusitis - metabolism Young Adult |
| Title | IL-5Rα marks nasal polyp IgG4- and IgE-expressing cells in aspirin-exacerbated respiratory disease |
| URI | https://www.clinicalkey.com/#!/content/1-s2.0-S0091674920303456 https://dx.doi.org/10.1016/j.jaci.2020.02.035 https://www.ncbi.nlm.nih.gov/pubmed/32199912 https://www.proquest.com/docview/2381848995 https://pubmed.ncbi.nlm.nih.gov/PMC7282948 |
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