Mepolizumab targets multiple immune cells in aspirin-exacerbated respiratory disease
Eosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to provide therapeutic benefit. However, IL-5Rα is expressed on many cells in addition to eosinophils, and the mechanisms by which IL-5 inhibition leads to clin...
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| Published in | Journal of allergy and clinical immunology Vol. 148; no. 2; pp. 574 - 584 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.08.2021
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Eosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to provide therapeutic benefit. However, IL-5Rα is expressed on many cells in addition to eosinophils, and the mechanisms by which IL-5 inhibition leads to clinical benefit in eosinophilic asthma and nasal polyposis are unlikely to be due exclusively to antieosinophil effects.
We sought to identify the mechanisms by which anti–IL-5 treatment with mepolizumab improves respiratory inflammation in AERD.
The clinical characteristics, circulating granulocytes, nasal scraping transcripts, eosinophilic cationic protein, tryptase, and antibody levels, and urinary and nasal eicosanoid levels were measured for 18 subjects with AERD who were taking mepolizumab and compared with those of 18 matched subjects with AERD who were not taking mepolizumab.
Subjects taking mepolizumab had significantly fewer peripheral blood eosinophils and basophils, and those cells that remained had higher surface CRTH2 expression than did the cells from subjects not taking mepolizumab. Nasal prostaglandin F2α, prostaglandin D2 metabolites, leukotriene B4, and thromboxane levels were lower in subjects taking mepolizumab, as were urinary levels of tetranor–prostaglandin D2 and leukotriene E4. The nasal epithelial cell transcripts that were overexpressed among subjects with AERD who were taking mepolizumab were enriched for genes involved in tight junction formation and cilium organization. Nasal and urinary prostaglandin E2, tryptase, and antibody levels were not different between the 2 groups.
IL-5 inhibition in AERD decreases production of inflammatory eicosanoids and upregulates tight junction–associated nasal epithelial cell transcripts, likely due to decreased IL-5 signaling on tissue mast cells, eosinophils, and epithelial cells. These direct effects on multiple relevant immune cells contribute to the mechanism of benefit afforded by mepolizumab.
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| AbstractList | Subjects with aspirin-exacerbated respiratory disease (AERD) treated with mepolizumab had decreased inflammatory eicosanoids and upregulation of nasal epithelial cell transcripts involved in tight junction pathways when compared to matched subjects with AERD not treated with mepolizumab. Eosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to provide therapeutic benefit. However, IL-5Rα is expressed on many cells in addition to eosinophils, and the mechanisms by which IL-5 inhibition leads to clinical benefit in eosinophilic asthma and nasal polyposis are unlikely to be due exclusively to antieosinophil effects. We sought to identify the mechanisms by which anti–IL-5 treatment with mepolizumab improves respiratory inflammation in AERD. The clinical characteristics, circulating granulocytes, nasal scraping transcripts, eosinophilic cationic protein, tryptase, and antibody levels, and urinary and nasal eicosanoid levels were measured for 18 subjects with AERD who were taking mepolizumab and compared with those of 18 matched subjects with AERD who were not taking mepolizumab. Subjects taking mepolizumab had significantly fewer peripheral blood eosinophils and basophils, and those cells that remained had higher surface CRTH2 expression than did the cells from subjects not taking mepolizumab. Nasal prostaglandin F2α, prostaglandin D2 metabolites, leukotriene B4, and thromboxane levels were lower in subjects taking mepolizumab, as were urinary levels of tetranor–prostaglandin D2 and leukotriene E4. The nasal epithelial cell transcripts that were overexpressed among subjects with AERD who were taking mepolizumab were enriched for genes involved in tight junction formation and cilium organization. Nasal and urinary prostaglandin E2, tryptase, and antibody levels were not different between the 2 groups. IL-5 inhibition in AERD decreases production of inflammatory eicosanoids and upregulates tight junction–associated nasal epithelial cell transcripts, likely due to decreased IL-5 signaling on tissue mast cells, eosinophils, and epithelial cells. These direct effects on multiple relevant immune cells contribute to the mechanism of benefit afforded by mepolizumab. [Display omitted] Eosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to provide therapeutic benefit. However, IL-5Rα is expressed on many cells in addition to eosinophils, and the mechanisms by which IL-5 inhibition leads to clinical benefit in eosinophilic asthma and nasal polyposis are unlikely to be due exclusively to antieosinophil effects. We sought to identify the mechanisms by which anti-IL-5 treatment with mepolizumab improves respiratory inflammation in AERD. The clinical characteristics, circulating granulocytes, nasal scraping transcripts, eosinophilic cationic protein, tryptase, and antibody levels, and urinary and nasal eicosanoid levels were measured for 18 subjects with AERD who were taking mepolizumab and compared with those of 18 matched subjects with AERD who were not taking mepolizumab. Subjects taking mepolizumab had significantly fewer peripheral blood eosinophils and basophils, and those cells that remained had higher surface CRTH2 expression than did the cells from subjects not taking mepolizumab. Nasal prostaglandin F , prostaglandin D metabolites, leukotriene B , and thromboxane levels were lower in subjects taking mepolizumab, as were urinary levels of tetranor-prostaglandin D and leukotriene E . The nasal epithelial cell transcripts that were overexpressed among subjects with AERD who were taking mepolizumab were enriched for genes involved in tight junction formation and cilium organization. Nasal and urinary prostaglandin E , tryptase, and antibody levels were not different between the 2 groups. IL-5 inhibition in AERD decreases production of inflammatory eicosanoids and upregulates tight junction-associated nasal epithelial cell transcripts, likely due to decreased IL-5 signaling on tissue mast cells, eosinophils, and epithelial cells. These direct effects on multiple relevant immune cells contribute to the mechanism of benefit afforded by mepolizumab. Eosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to provide therapeutic benefit. However, IL-5Rα is expressed on many cells in addition to eosinophils, and the mechanisms by which IL-5 inhibition leads to clinical benefit in eosinophilic asthma and nasal polyposis are unlikely to be due exclusively to antieosinophil effects.BACKGROUNDEosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to provide therapeutic benefit. However, IL-5Rα is expressed on many cells in addition to eosinophils, and the mechanisms by which IL-5 inhibition leads to clinical benefit in eosinophilic asthma and nasal polyposis are unlikely to be due exclusively to antieosinophil effects.We sought to identify the mechanisms by which anti-IL-5 treatment with mepolizumab improves respiratory inflammation in AERD.OBJECTIVEWe sought to identify the mechanisms by which anti-IL-5 treatment with mepolizumab improves respiratory inflammation in AERD.The clinical characteristics, circulating granulocytes, nasal scraping transcripts, eosinophilic cationic protein, tryptase, and antibody levels, and urinary and nasal eicosanoid levels were measured for 18 subjects with AERD who were taking mepolizumab and compared with those of 18 matched subjects with AERD who were not taking mepolizumab.METHODSThe clinical characteristics, circulating granulocytes, nasal scraping transcripts, eosinophilic cationic protein, tryptase, and antibody levels, and urinary and nasal eicosanoid levels were measured for 18 subjects with AERD who were taking mepolizumab and compared with those of 18 matched subjects with AERD who were not taking mepolizumab.Subjects taking mepolizumab had significantly fewer peripheral blood eosinophils and basophils, and those cells that remained had higher surface CRTH2 expression than did the cells from subjects not taking mepolizumab. Nasal prostaglandin F2α, prostaglandin D2 metabolites, leukotriene B4, and thromboxane levels were lower in subjects taking mepolizumab, as were urinary levels of tetranor-prostaglandin D2 and leukotriene E4. The nasal epithelial cell transcripts that were overexpressed among subjects with AERD who were taking mepolizumab were enriched for genes involved in tight junction formation and cilium organization. Nasal and urinary prostaglandin E2, tryptase, and antibody levels were not different between the 2 groups.RESULTSSubjects taking mepolizumab had significantly fewer peripheral blood eosinophils and basophils, and those cells that remained had higher surface CRTH2 expression than did the cells from subjects not taking mepolizumab. Nasal prostaglandin F2α, prostaglandin D2 metabolites, leukotriene B4, and thromboxane levels were lower in subjects taking mepolizumab, as were urinary levels of tetranor-prostaglandin D2 and leukotriene E4. The nasal epithelial cell transcripts that were overexpressed among subjects with AERD who were taking mepolizumab were enriched for genes involved in tight junction formation and cilium organization. Nasal and urinary prostaglandin E2, tryptase, and antibody levels were not different between the 2 groups.IL-5 inhibition in AERD decreases production of inflammatory eicosanoids and upregulates tight junction-associated nasal epithelial cell transcripts, likely due to decreased IL-5 signaling on tissue mast cells, eosinophils, and epithelial cells. These direct effects on multiple relevant immune cells contribute to the mechanism of benefit afforded by mepolizumab.CONCLUSIONIL-5 inhibition in AERD decreases production of inflammatory eicosanoids and upregulates tight junction-associated nasal epithelial cell transcripts, likely due to decreased IL-5 signaling on tissue mast cells, eosinophils, and epithelial cells. These direct effects on multiple relevant immune cells contribute to the mechanism of benefit afforded by mepolizumab. BackgroundEosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to provide therapeutic benefit. However, IL-5Rα is expressed on many cells in addition to eosinophils, and the mechanisms by which IL-5 inhibition leads to clinical benefit in eosinophilic asthma and nasal polyposis are unlikely to be due exclusively to antieosinophil effects.ObjectiveWe sought to identify the mechanisms by which anti–IL-5 treatment with mepolizumab improves respiratory inflammation in AERD.MethodsThe clinical characteristics, circulating granulocytes, nasal scraping transcripts, eosinophilic cationic protein, tryptase, and antibody levels, and urinary and nasal eicosanoid levels were measured for 18 subjects with AERD who were taking mepolizumab and compared with those of 18 matched subjects with AERD who were not taking mepolizumab.ResultsSubjects taking mepolizumab had significantly fewer peripheral blood eosinophils and basophils, and those cells that remained had higher surface CRTH2 expression than did the cells from subjects not taking mepolizumab. Nasal prostaglandin F2α, prostaglandin D2 metabolites, leukotriene B4, and thromboxane levels were lower in subjects taking mepolizumab, as were urinary levels of tetranor–prostaglandin D2 and leukotriene E4. The nasal epithelial cell transcripts that were overexpressed among subjects with AERD who were taking mepolizumab were enriched for genes involved in tight junction formation and cilium organization. Nasal and urinary prostaglandin E2, tryptase, and antibody levels were not different between the 2 groups.ConclusionIL-5 inhibition in AERD decreases production of inflammatory eicosanoids and upregulates tight junction–associated nasal epithelial cell transcripts, likely due to decreased IL-5 signaling on tissue mast cells, eosinophils, and epithelial cells. These direct effects on multiple relevant immune cells contribute to the mechanism of benefit afforded by mepolizumab. |
| Author | Buchheit, Kathleen M. Lewis, Erin Hacker, Jonathan Taliaferro, Faith Ordovas-Montanes, Jose Sohail, Aaqib Vukovic, Marko Berreondo Giron, Evans Laidlaw, Tanya M. Dwyer, Daniel F. Gakpo, Deborah Bensko, Jillian C. Shalek, Alex K. Asare, Chelsea |
| AuthorAffiliation | 3 Division of Gastroenterology, Boston Children’s Hospital, Boston, Massachusetts 7 Ragon Institute of MGH, MIT and Harvard, Cambridge, Massachusetts 9 Harvard-MIT Division of Health Sciences & Technology, Cambridge, Massachusetts 4 Broad Institute of MIT and Harvard, Cambridge, Massachusetts 1 Department of Medicine, Harvard Medical School, the Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Massachusetts 6 Harvard Stem Cell Institute, Cambridge, Massachusetts 5 Program in Immunology, Harvard Medical School, Boston, Massachusetts 2 Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Massachusetts 8 Institute for Medical Engineering and Science (IMES), Department of Chemistry, and Koch Institute for Integrative Cancer Research, MIT, Cambridge, Massachusetts |
| AuthorAffiliation_xml | – name: 5 Program in Immunology, Harvard Medical School, Boston, Massachusetts – name: 1 Department of Medicine, Harvard Medical School, the Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Massachusetts – name: 2 Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Massachusetts – name: 8 Institute for Medical Engineering and Science (IMES), Department of Chemistry, and Koch Institute for Integrative Cancer Research, MIT, Cambridge, Massachusetts – name: 4 Broad Institute of MIT and Harvard, Cambridge, Massachusetts – name: 6 Harvard Stem Cell Institute, Cambridge, Massachusetts – name: 3 Division of Gastroenterology, Boston Children’s Hospital, Boston, Massachusetts – name: 9 Harvard-MIT Division of Health Sciences & Technology, Cambridge, Massachusetts – name: 7 Ragon Institute of MGH, MIT and Harvard, Cambridge, Massachusetts |
| Author_xml | – sequence: 1 givenname: Kathleen M. surname: Buchheit fullname: Buchheit, Kathleen M. organization: Department of Medicine, Harvard Medical School, the Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Mass – sequence: 2 givenname: Erin surname: Lewis fullname: Lewis, Erin organization: Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Mass – sequence: 3 givenname: Deborah surname: Gakpo fullname: Gakpo, Deborah organization: Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Mass – sequence: 4 givenname: Jonathan surname: Hacker fullname: Hacker, Jonathan organization: Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Mass – sequence: 5 givenname: Aaqib surname: Sohail fullname: Sohail, Aaqib organization: Department of Medicine, Harvard Medical School, the Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Mass – sequence: 6 givenname: Faith surname: Taliaferro fullname: Taliaferro, Faith organization: Division of Gastroenterology, Boston Children’s Hospital, Boston, Mass – sequence: 7 givenname: Evans surname: Berreondo Giron fullname: Berreondo Giron, Evans organization: Division of Gastroenterology, Boston Children’s Hospital, Boston, Mass – sequence: 8 givenname: Chelsea surname: Asare fullname: Asare, Chelsea organization: Division of Gastroenterology, Boston Children’s Hospital, Boston, Mass – sequence: 9 givenname: Marko surname: Vukovic fullname: Vukovic, Marko organization: Broad Institute of MIT and Harvard, Cambridge, Mass – sequence: 10 givenname: Jillian C. surname: Bensko fullname: Bensko, Jillian C. organization: Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Mass – sequence: 11 givenname: Daniel F. surname: Dwyer fullname: Dwyer, Daniel F. organization: Department of Medicine, Harvard Medical School, the Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Mass – sequence: 12 givenname: Alex K. surname: Shalek fullname: Shalek, Alex K. organization: Broad Institute of MIT and Harvard, Cambridge, Mass – sequence: 13 givenname: Jose surname: Ordovas-Montanes fullname: Ordovas-Montanes, Jose organization: Division of Gastroenterology, Boston Children’s Hospital, Boston, Mass – sequence: 14 givenname: Tanya M. surname: Laidlaw fullname: Laidlaw, Tanya M. email: tlaidlaw@bwh.harvard.edu organization: Department of Medicine, Harvard Medical School, the Division of Allergy and Clinical Immunology, Brigham and Women’s Hospital, Boston, Mass |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34144111$$D View this record in MEDLINE/PubMed |
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| Keywords | PGD2 Aspirin-exacerbated respiratory disease leukotriene PGF2α prostaglandin F2α AERD GO IL-5 CRSwNP nasal polyp ILC2 ECP TXB2 LTE4 prostaglandin D2 mepolizumab chronic rhinosinusitis CRTH2 LTB4 prostaglandin D prostaglandin F(2α) |
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| Snippet | Eosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to provide... BackgroundEosinophilic asthma and nasal polyposis are hallmarks of aspirin-exacerbated respiratory disease (AERD), and IL-5 inhibition has been shown to... Subjects with aspirin-exacerbated respiratory disease (AERD) treated with mepolizumab had decreased inflammatory eicosanoids and upregulation of nasal... |
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| SubjectTerms | Adolescent Adult Aged Antibodies, Monoclonal, Humanized - administration & dosage Aspirin Aspirin-exacerbated respiratory disease Asthma Asthma, Aspirin-Induced - drug therapy Asthma, Aspirin-Induced - immunology Asthma, Aspirin-Induced - urine Basophils - immunology Basophils - pathology chronic rhinosinusitis CRTH2 Eicosanoids Eicosanoids - immunology Eicosanoids - urine Eosinophils - immunology Eosinophils - pathology Epithelial cells FDA approval Female Granulocytes Humans IL-5 Inflammation Interleukin 5 Interleukin-5 - immunology Interleukin-5 Receptor alpha Subunit - immunology Leukocytes (basophilic) Leukocytes (eosinophilic) Leukocytes (granulocytic) leukotriene Leukotriene B4 Male Mast cells mepolizumab Middle Aged Monoclonal antibodies nasal polyp Nasal Polyps - drug therapy Nasal Polyps - immunology Nasal Polyps - urine Patients Peripheral blood Polyposis Polyps Prostaglandin D2 Prostaglandin E2 prostaglandin F2α Respiratory diseases Rhinitis Sinusitis Tryptase |
| Title | Mepolizumab targets multiple immune cells in aspirin-exacerbated respiratory disease |
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