Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease

<h3>Background & Aims</h3><p dir="ltr">The gastrointestinal epithelium plays a crucial role in maintaining homeostasis with the gut microbiome. Mucins are essential for intestinal barrier function and serve as a scaffold for antimicrobial factors. Mucin 2 (MUC2) is th...

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التفاصيل البيبلوغرافية
المؤلف الرئيسي: Ahmad A. Al-Shaibi (18552234) (author)
مؤلفون آخرون: Ussama M. Abdel-Motal (138406) (author), Satanay Z. Hubrack (18552236) (author), Alex N. Bullock (18552237) (author), Amna A. Al-Marri (18552239) (author), Nourhen Agrebi (14151222) (author), Abdulrahman A. Al-Subaiey (18552242) (author), Nazira A. Ibrahim (18552247) (author), Adrian K. Charles (112557) (author), Mamoun Elawad (438979) (author), Holm H. Uhlig (564856) (author), Bernice Lo (3441317) (author)
منشور في: 2021
الموضوعات:
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author Ahmad A. Al-Shaibi (18552234)
author2 Ussama M. Abdel-Motal (138406)
Satanay Z. Hubrack (18552236)
Alex N. Bullock (18552237)
Amna A. Al-Marri (18552239)
Nourhen Agrebi (14151222)
Abdulrahman A. Al-Subaiey (18552242)
Nazira A. Ibrahim (18552247)
Adrian K. Charles (112557)
Mamoun Elawad (438979)
Holm H. Uhlig (564856)
Bernice Lo (3441317)
author2_role author
author
author
author
author
author
author
author
author
author
author
author_facet Ahmad A. Al-Shaibi (18552234)
Ussama M. Abdel-Motal (138406)
Satanay Z. Hubrack (18552236)
Alex N. Bullock (18552237)
Amna A. Al-Marri (18552239)
Nourhen Agrebi (14151222)
Abdulrahman A. Al-Subaiey (18552242)
Nazira A. Ibrahim (18552247)
Adrian K. Charles (112557)
Mamoun Elawad (438979)
Holm H. Uhlig (564856)
Bernice Lo (3441317)
author_role author
dc.creator.none.fl_str_mv Ahmad A. Al-Shaibi (18552234)
Ussama M. Abdel-Motal (138406)
Satanay Z. Hubrack (18552236)
Alex N. Bullock (18552237)
Amna A. Al-Marri (18552239)
Nourhen Agrebi (14151222)
Abdulrahman A. Al-Subaiey (18552242)
Nazira A. Ibrahim (18552247)
Adrian K. Charles (112557)
Mamoun Elawad (438979)
Holm H. Uhlig (564856)
Bernice Lo (3441317)
dc.date.none.fl_str_mv 2021-01-01T06:00:00Z
dc.identifier.none.fl_str_mv 10.1016/j.jcmgh.2021.07.001
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Human_AGR2_Deficiency_Causes_Mucus_Barrier_Dysfunction_and_Infantile_Inflammatory_Bowel_Disease/25816675
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Genetics
Biomedical and clinical sciences
Clinical sciences
AGR2
MUC2
ER Stress
Intestinal Metaplasia
Goblet Cells
dc.title.none.fl_str_mv Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <h3>Background & Aims</h3><p dir="ltr">The gastrointestinal epithelium plays a crucial role in maintaining homeostasis with the gut microbiome. Mucins are essential for intestinal barrier function and serve as a scaffold for antimicrobial factors. Mucin 2 (MUC2) is the major intestinal gel-forming mucin produced predominantly by goblet cells. Goblet cells express anterior gradient 2 (AGR2), a protein disulfide isomerase that is crucial for proper processing of gel-forming mucins. Here, we investigated 2 siblings who presented with severe infantile-onset inflammatory bowel disease.</p><h3>Methods</h3><p dir="ltr">We performed whole-genome sequencing to identify candidate variants. We quantified goblet cell numbers using H&E histology and investigated the expression of gel-forming mucins, stress markers, and goblet cell markers using immunohistochemistry. AGR2-MUC2 binding was evaluated using co-immunoprecipitation. Endoplasmic reticulum (ER) stress regulatory function of mutant AGR2 was examined by expression studies in Human Embryonic Kidney 293T (HEK293T) using tunicamycin to induce ER stress.</p><h3>Results</h3><p dir="ltr">Both affected siblings were homozygous for a missense variant in <i>AGR2</i> . Patient biopsy specimens showed reduced goblet cells; depletion of MUC2, MUC5AC, and MUC6; up-regulation of AGR2; and increased ER stress. The mutant AGR2 showed reduced capacity to bind MUC2 and alleviate tunicamycin-induced ER stress.</p><h3>Conclusions</h3><p dir="ltr">Phenotype–genotype segregation, functional experiments, and the striking similarity of the human phenotype to <i>AGR2</i> <sup><em>-/-</em></sup><sup><em> </em></sup>mouse models suggest that the AGR2 missense variant is pathogenic. The Mendelian deficiency of AGR2, termed “Enteropathy caused by AGR2 deficiency, Goblet cell Loss, and ER Stress” (EAGLES), results in a mucus barrier defect, the inability to mitigate ER stress, and causes infantile-onset inflammatory bowel disease.</p><h2>Other Information</h2><p dir="ltr">Published in: Circulation: Cellular and Molecular Gastroenterology and Hepatology<br>License: <a href="https://creativecommons.org/licenses/by/4.0/" target="_blank">https://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://doi.org/10.1016/j.jcmgh.2021.07.001" target="_blank">https://doi.org/10.1016/j.jcmgh.2021.07.001</a></p>
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network_acronym_str Manara2
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oai_identifier_str oai:figshare.com:article/25816675
publishDate 2021
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rights_invalid_str_mv CC BY 4.0
spelling Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel DiseaseAhmad A. Al-Shaibi (18552234)Ussama M. Abdel-Motal (138406)Satanay Z. Hubrack (18552236)Alex N. Bullock (18552237)Amna A. Al-Marri (18552239)Nourhen Agrebi (14151222)Abdulrahman A. Al-Subaiey (18552242)Nazira A. Ibrahim (18552247)Adrian K. Charles (112557)Mamoun Elawad (438979)Holm H. Uhlig (564856)Bernice Lo (3441317)Biological sciencesBiochemistry and cell biologyGeneticsBiomedical and clinical sciencesClinical sciencesAGR2MUC2ER StressIntestinal MetaplasiaGoblet Cells<h3>Background & Aims</h3><p dir="ltr">The gastrointestinal epithelium plays a crucial role in maintaining homeostasis with the gut microbiome. Mucins are essential for intestinal barrier function and serve as a scaffold for antimicrobial factors. Mucin 2 (MUC2) is the major intestinal gel-forming mucin produced predominantly by goblet cells. Goblet cells express anterior gradient 2 (AGR2), a protein disulfide isomerase that is crucial for proper processing of gel-forming mucins. Here, we investigated 2 siblings who presented with severe infantile-onset inflammatory bowel disease.</p><h3>Methods</h3><p dir="ltr">We performed whole-genome sequencing to identify candidate variants. We quantified goblet cell numbers using H&E histology and investigated the expression of gel-forming mucins, stress markers, and goblet cell markers using immunohistochemistry. AGR2-MUC2 binding was evaluated using co-immunoprecipitation. Endoplasmic reticulum (ER) stress regulatory function of mutant AGR2 was examined by expression studies in Human Embryonic Kidney 293T (HEK293T) using tunicamycin to induce ER stress.</p><h3>Results</h3><p dir="ltr">Both affected siblings were homozygous for a missense variant in <i>AGR2</i> . Patient biopsy specimens showed reduced goblet cells; depletion of MUC2, MUC5AC, and MUC6; up-regulation of AGR2; and increased ER stress. The mutant AGR2 showed reduced capacity to bind MUC2 and alleviate tunicamycin-induced ER stress.</p><h3>Conclusions</h3><p dir="ltr">Phenotype–genotype segregation, functional experiments, and the striking similarity of the human phenotype to <i>AGR2</i> <sup><em>-/-</em></sup><sup><em> </em></sup>mouse models suggest that the AGR2 missense variant is pathogenic. The Mendelian deficiency of AGR2, termed “Enteropathy caused by AGR2 deficiency, Goblet cell Loss, and ER Stress” (EAGLES), results in a mucus barrier defect, the inability to mitigate ER stress, and causes infantile-onset inflammatory bowel disease.</p><h2>Other Information</h2><p dir="ltr">Published in: Circulation: Cellular and Molecular Gastroenterology and Hepatology<br>License: <a href="https://creativecommons.org/licenses/by/4.0/" target="_blank">https://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://doi.org/10.1016/j.jcmgh.2021.07.001" target="_blank">https://doi.org/10.1016/j.jcmgh.2021.07.001</a></p>2021-01-01T06:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1016/j.jcmgh.2021.07.001https://figshare.com/articles/journal_contribution/Human_AGR2_Deficiency_Causes_Mucus_Barrier_Dysfunction_and_Infantile_Inflammatory_Bowel_Disease/25816675CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/258166752021-01-01T06:00:00Z
spellingShingle Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease
Ahmad A. Al-Shaibi (18552234)
Biological sciences
Biochemistry and cell biology
Genetics
Biomedical and clinical sciences
Clinical sciences
AGR2
MUC2
ER Stress
Intestinal Metaplasia
Goblet Cells
status_str publishedVersion
title Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease
title_full Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease
title_fullStr Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease
title_full_unstemmed Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease
title_short Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease
title_sort Human AGR2 Deficiency Causes Mucus Barrier Dysfunction and Infantile Inflammatory Bowel Disease
topic Biological sciences
Biochemistry and cell biology
Genetics
Biomedical and clinical sciences
Clinical sciences
AGR2
MUC2
ER Stress
Intestinal Metaplasia
Goblet Cells