Immunomolecular and reactivity landscapes of gut IgA subclasses in homeostasis and inflammatory bowel disease
The human gut includes plasma cells (PCs) expressing immunoglobulin A1 (IgA1) or IgA2, two structurally distinct IgA subclasses with elusive regulation, function, and reactivity. We show here that intestinal IgA1+ and IgA2+ PCs co-emerged early in life, comparably accumulated somatic mutations, and...
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| Published in | The Journal of experimental medicine Vol. 221; no. 12 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Rockefeller University Press
02.12.2024
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| Online Access | Get full text |
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| Abstract | The human gut includes plasma cells (PCs) expressing immunoglobulin A1 (IgA1) or IgA2, two structurally distinct IgA subclasses with elusive regulation, function, and reactivity. We show here that intestinal IgA1+ and IgA2+ PCs co-emerged early in life, comparably accumulated somatic mutations, and were enriched within short-lived CD19+ and long-lived CD19− PC subsets, respectively. IgA2+ PCs were extensively clonally related to IgA1+ PCs and a subset of them presumably emerged from IgA1+ precursors. Of note, secretory IgA1 (SIgA1) and SIgA2 dually coated a large fraction of mucus-embedded bacteria, including Akkermansia muciniphila. Disruption of homeostasis by inflammatory bowel disease (IBD) was associated with an increase in actively proliferating IgA1+ plasmablasts, a depletion in long-lived IgA2+ PCs, and increased SIgA1+SIgA2+ gut microbiota. Such increase featured enhanced IgA1 reactivity to pathobionts, including Escherichia coli, combined with depletion of beneficial A. muciniphila. Thus, gut IgA1 and IgA2 emerge from clonally related PCs and show unique changes in both frequency and reactivity in IBD. |
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| AbstractList | Tejedor Vaquero et al. show that gut IgA1 and IgA2 subclasses co-emerge early in life, largely derive from clonally related and somatically mutated plasma cells in adults, and show unique changes of both frequency and reactivity in inflammatory bowel disease.
The human gut includes plasma cells (PCs) expressing immunoglobulin A1 (IgA1) or IgA2, two structurally distinct IgA subclasses with elusive regulation, function, and reactivity. We show here that intestinal IgA1
+
and IgA2
+
PCs co-emerged early in life, comparably accumulated somatic mutations, and were enriched within short-lived CD19
+
and long-lived CD19
−
PC subsets, respectively. IgA2
+
PCs were extensively clonally related to IgA1
+
PCs and a subset of them presumably emerged from IgA1
+
precursors. Of note, secretory IgA1 (SIgA1) and SIgA2 dually coated a large fraction of mucus-embedded bacteria, including
Akkermansia muciniphila
. Disruption of homeostasis by inflammatory bowel disease (IBD) was associated with an increase in actively proliferating IgA1
+
plasmablasts, a depletion in long-lived IgA2
+
PCs, and increased SIgA1
+
SIgA2
+
gut microbiota. Such increase featured enhanced IgA1 reactivity to pathobionts, including
Escherichia coli
, combined with depletion of beneficial
A. muciniphila.
Thus, gut IgA1 and IgA2 emerge from clonally related PCs and show unique changes in both frequency and reactivity in IBD. The human gut includes plasma cells (PCs) expressing immunoglobulin A1 (IgA1) or IgA2, two structurally distinct IgA subclasses with elusive regulation, function, and reactivity. We show here that intestinal IgA1+ and IgA2+ PCs co-emerged early in life, comparably accumulated somatic mutations, and were enriched within short-lived CD19+ and long-lived CD19- PC subsets, respectively. IgA2+ PCs were extensively clonally related to IgA1+ PCs and a subset of them presumably emerged from IgA1+ precursors. Of note, secretory IgA1 (SIgA1) and SIgA2 dually coated a large fraction of mucus-embedded bacteria, including Akkermansia muciniphila. Disruption of homeostasis by inflammatory bowel disease (IBD) was associated with an increase in actively proliferating IgA1+ plasmablasts, a depletion in long-lived IgA2+ PCs, and increased SIgA1+SIgA2+ gut microbiota. Such increase featured enhanced IgA1 reactivity to pathobionts, including Escherichia coli, combined with depletion of beneficial A. muciniphila. Thus, gut IgA1 and IgA2 emerge from clonally related PCs and show unique changes in both frequency and reactivity in IBD.The human gut includes plasma cells (PCs) expressing immunoglobulin A1 (IgA1) or IgA2, two structurally distinct IgA subclasses with elusive regulation, function, and reactivity. We show here that intestinal IgA1+ and IgA2+ PCs co-emerged early in life, comparably accumulated somatic mutations, and were enriched within short-lived CD19+ and long-lived CD19- PC subsets, respectively. IgA2+ PCs were extensively clonally related to IgA1+ PCs and a subset of them presumably emerged from IgA1+ precursors. Of note, secretory IgA1 (SIgA1) and SIgA2 dually coated a large fraction of mucus-embedded bacteria, including Akkermansia muciniphila. Disruption of homeostasis by inflammatory bowel disease (IBD) was associated with an increase in actively proliferating IgA1+ plasmablasts, a depletion in long-lived IgA2+ PCs, and increased SIgA1+SIgA2+ gut microbiota. Such increase featured enhanced IgA1 reactivity to pathobionts, including Escherichia coli, combined with depletion of beneficial A. muciniphila. Thus, gut IgA1 and IgA2 emerge from clonally related PCs and show unique changes in both frequency and reactivity in IBD. The human gut includes plasma cells (PCs) expressing immunoglobulin A1 (IgA1) or IgA2, two structurally distinct IgA subclasses with elusive regulation, function, and reactivity. We show here that intestinal IgA1+ and IgA2+ PCs co-emerged early in life, comparably accumulated somatic mutations, and were enriched within short-lived CD19+ and long-lived CD19− PC subsets, respectively. IgA2+ PCs were extensively clonally related to IgA1+ PCs and a subset of them presumably emerged from IgA1+ precursors. Of note, secretory IgA1 (SIgA1) and SIgA2 dually coated a large fraction of mucus-embedded bacteria, including Akkermansia muciniphila. Disruption of homeostasis by inflammatory bowel disease (IBD) was associated with an increase in actively proliferating IgA1+ plasmablasts, a depletion in long-lived IgA2+ PCs, and increased SIgA1+SIgA2+ gut microbiota. Such increase featured enhanced IgA1 reactivity to pathobionts, including Escherichia coli, combined with depletion of beneficial A. muciniphila. Thus, gut IgA1 and IgA2 emerge from clonally related PCs and show unique changes in both frequency and reactivity in IBD. The human gut includes plasma cells (PCs) expressing immunoglobulin A1 (IgA1) or IgA2, two structurally distinct IgA subclasses with elusive regulation, function, and reactivity. We show here that intestinal IgA1+ and IgA2+ PCs co-emerged early in life, comparably accumulated somatic mutations, and were enriched within short-lived CD19+ and long-lived CD19- PC subsets, respectively. IgA2+ PCs were extensively clonally related to IgA1+ PCs and a subset of them presumably emerged from IgA1+ precursors. Of note, secretory IgA1 (SIgA1) and SIgA2 dually coated a large fraction of mucus-embedded bacteria, including Akkermansia muciniphila. Disruption of homeostasis by inflammatory bowel disease (IBD) was associated with an increase in actively proliferating IgA1+ plasmablasts, a depletion in long-lived IgA2+ PCs, and increased SIgA1+SIgA2+ gut microbiota. Such increase featured enhanced IgA1 reactivity to pathobionts, including Escherichia coli, combined with depletion of beneficial A. muciniphila. Thus, gut IgA1 and IgA2 emerge from clonally related PCs and show unique changes in both frequency and reactivity in IBD. |
| Author | Neuman, Hadas Grassi, Fabio Magri, Giuliana Santiago-Diaz, Pablo Guerra, Joana Gonzalez Farré, Monica Mehr, Ramit Uzzan, Mathieu Corral-Vazquez, Celia Martin-Nalda, Andrea Segura-Garzón, Daniel Lop, Joan Márquez-Mosquera, Lucia Marcos-Fa, Xavi Tachó-Piñot, Roser Varela, Encarna Grasset, Emilie K. Pybus, Marc Martinez Gallo, Monica Perruzza, Lisa Rosenstein, Adam Sintes, Jordi Guarner, Francisco Larrubia-Loring, Monica Iglesias, Mar Tejedor Vaquero, Sonia Berenguer-Molins, Pau Comerma, Laura Garrido-Pontnou, Marta Perera-Bel, Júlia Mehandru, Saurabh Cerutti, Andrea Patriaca-Amiano, Maria Evangelina |
| AuthorAffiliation | 3 Department of Medicine, https://ror.org/04a9tmd77 Icahn School of Medicine at Mount Sinai, Immunology Institute , New York, NY, USA 6 Immunology Division, Vall d’Hebron University Hospital and Translational Immunology Research Group, Vall d’Hebron Research Institute (VHIR), Department of Cell Biology, Physiology and Immunology, Autonomous University of Barcelona (UAB), Barcelona, Spain 1 https://ror.org/03a8gac78 Translational Clinical Research Program, Hospital del Mar Research Institute , Barcelona, Spain 12 Catalan Institute for Research and Advanced Studies , Barcelona, Spain 11 Department of Gastroenterology, https://ror.org/03a8gac78 Hospital del Mar Medical Research Institute Barcelona , Barcelona, Spain 5 Pathology Department, https://ror.org/03a8gac78 Hospital del Mar , Barcelona, Spain 10 Pathology Department, https://ror.org/03ba28x55 Hospital Universitari Vall d’Hebron , Barcelona, Spain 9 Biomedical Research Networking Center in Hepatic and Digestive Diseases, Instituto Carlos |
| AuthorAffiliation_xml | – name: 6 Immunology Division, Vall d’Hebron University Hospital and Translational Immunology Research Group, Vall d’Hebron Research Institute (VHIR), Department of Cell Biology, Physiology and Immunology, Autonomous University of Barcelona (UAB), Barcelona, Spain – name: 9 Biomedical Research Networking Center in Hepatic and Digestive Diseases, Instituto Carlos III , Madrid, Spain – name: 4 Institute for Research in Biomedicine, Faculty of Biomedical Sciences, Università della Svizzera Italiana , Bellinzona, Switzerland – name: 2 Computational Immunology Laboratory, The Mina and Everard Goodman Faculty of Life Sciences, https://ror.org/03kgsv495 Bar-Ilan University , Ramat-Gan, Israel – name: 8 Department of Gastroenterology, Vall d’Hebron Research Institute , Barcelona, Spain – name: 10 Pathology Department, https://ror.org/03ba28x55 Hospital Universitari Vall d’Hebron , Barcelona, Spain – name: 5 Pathology Department, https://ror.org/03a8gac78 Hospital del Mar , Barcelona, Spain – name: 3 Department of Medicine, https://ror.org/04a9tmd77 Icahn School of Medicine at Mount Sinai, Immunology Institute , New York, NY, USA – name: 11 Department of Gastroenterology, https://ror.org/03a8gac78 Hospital del Mar Medical Research Institute Barcelona , Barcelona, Spain – name: 7 Pediatric Infectious Diseases and Immunodeficiencies Unit, https://ror.org/03ba28x55 Vall d’Hebron University Hospital, Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiencies , Barcelona, Spain – name: 12 Catalan Institute for Research and Advanced Studies , Barcelona, Spain – name: 1 https://ror.org/03a8gac78 Translational Clinical Research Program, Hospital del Mar Research Institute , Barcelona, Spain |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Disclosures: L. Comerma reported personal fees from Roche, MSD, AstraZeneca, and Diaceutics and non-financial support from Roche, MSD, AstraZeneca, and Phillips outside the submitted work. M. Iglesias reported personal fees from Bristol Myers Squibb, Merck Sharp & Dohme, Roche, Astellas, Merck, Agilent, and Seagen outside the submitted work. No other disclosures were reported. R. Mehr, A. Cerutti, and G. Magri contributed equally to this paper. G. Magri’s current affiliation is Immunology Unit, Department of Biomedical Sciences, Faculty of Medicine and Health Sciences, University of Barcelona, Barcelona, Spain. M. Uzzan’s current affiliation is Department of gastroenterology, Hospital Henri Mondor, APHP, Creteil France; INSERM U955, IMRB, Creteil, France. E.K. Grasset’s current affiliation is Department of Pediatrics, Gale and Ira Drukier Institute for Children's Health, Weill Cornell Medicine, New York, NY, USA. S. Tejedor Vaquero and H. Neuman contributed equally to this paper. |
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Immunol. doi: 10.1093/intimm/3.11.1099 |
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| Snippet | The human gut includes plasma cells (PCs) expressing immunoglobulin A1 (IgA1) or IgA2, two structurally distinct IgA subclasses with elusive regulation,... Tejedor Vaquero et al. show that gut IgA1 and IgA2 subclasses co-emerge early in life, largely derive from clonally related and somatically mutated plasma... |
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| SubjectTerms | Adult Akkermansia - immunology Female Gastrointestinal Microbiome - immunology Homeostasis - immunology Humans Immunoglobulin A - immunology Immunoglobulin A - metabolism Immunoglobulin A, Secretory - immunology Immunoglobulin A, Secretory - metabolism Inflammatory Bowel Diseases - immunology Intestinal Mucosa - immunology Intestinal Mucosa - metabolism Leukemia & Lymphoma Lymphocyte Biology Male Plasma Cells - immunology Plasma Cells - metabolism |
| Title | Immunomolecular and reactivity landscapes of gut IgA subclasses in homeostasis and inflammatory bowel disease |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/39560666 https://www.proquest.com/docview/3130210919 https://pubmed.ncbi.nlm.nih.gov/PMC11577441 |
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