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2. Evaluating Eosinophilic Colitis as a Unique Disease Using Colonic Molecular Profiles: A Multi-Site Study

Author

Tetsuo Shoda, Margaret H. Collins, Mark Rochman, Ting Wen, Julie M. Caldwell, Lydia E. Mack, Garrett A. Osswald, John A. Besse, Yael Haberman, Seema S. Aceves, Nicoleta C. Arva, Kelley E. Capocelli, Mirna Chehade, Carla M. Davis, Evan S. Dellon, Gary W. Falk, Nirmala Gonsalves, Sandeep K. Gupta, Ikuo Hirano, Paneez Khoury, Amy Klion, Calies Menard-Katcher, John Leung, Vincent A. Mukkada, Philip E. Putnam, Jonathan M. Spergel, Joshua B. Wechsler, Guang-Yu Yang, Glenn T. Furuta, Lee A. Denson, Marc E. Rothenberg, J. Pablo Abonia, Seema Aceves, Samuel Almonte, Rachel Andrews, Sara Anvari, Ashley Arrington, Nicoleta Arva, Fred Atkins, Dominique Bailey, Alexis Berry, Bridget Besl, Scott Bolton, Peter Bonis, Wendy Book, Kimberly Bray, Teresa Brown, Cassandra Burger, Deirdre Burke, Jonathon Cahoon, Kelley Capocelli, Eric Chiou, Margaret Collins, Carla Davis, Evan Dellon, Maureen DeMarshall, Lauren DiTommaso, Ranjan Dohil, Michael Eby, Gary Falk, David Fleischer, Heather Foote, Kelci Foss, Joel Friedlander, Patricia Fulkerson, Glenn Furuta, Debra Geno, Thomas Greuter, Sandeep Gupta, Frank Hamilton, Kirk Harris, Jennifer Harris, Girish Hiremath, Nicole Holland-Thomas, Lea Jacinto, Amir Kagalwalla, Timothy Kaseta, David Katzka, Kaitlin Keeley, Emad Khosh-Hemmat, Eileen King, Kara Kliewer, Jennifer Knowles, Kendra Kocher, Ellyn Kodroff, Jeffrey Krischer, Shay Kyle, Meredith Levy, Chris Liacouras, Denise Mack, Lisa Martin, Ellen Martin, Talaya McCright-Gill, Paul Menard-Katcher, Gabriela Mendoza, Melissa Mingler, Mike Minnicozzi, Amanda Muir, Vincent Mukkada, Cristin Murray-Petzold, Robert Newbury, Quan Nhu, Anthony Olive, Oghenekpaobor (Joel) Oyibo, Allisa Paliana, Zhaoxing Pan, Robbie Pesek, Kathryn Peterson, Heidi Poppendeck, Philip Putnam, Fabian Rivera, Marc Rothenberg, Amanda Rudman Spergel, Kathleen Sable, Alain Schoepfer, Melissa Scott, Rachel Sheridan, Selma Sinanovic, Jonathan Spergel, Mary Jo Strobel, Kiki Sun, Amy Tasco, Crystal Tholen, Katherine Thompson, Tiffany Tomkinson, Daisy Tran, Alexandra Tylicki, Tiina Urv, Mei-Lun Wang, Joshua Wechsler, Barry Wershil, Lisa Wheatley, Leah Wilkey, Angelika Zalewski, and Amy Zicarelli

Subjects
Colitis, Microscopic, Hepatology, Gastritis, Eosinophilia, Gastroenterology, Humans, Colitis, Inflammatory Bowel Diseases, Article, Enteritis
Abstract

BACKGROUND AND AIMS: Colonic eosinophilia, an enigmatic finding often referred to as eosinophilic colitis (EoC), is a poorly understood condition. Whether EoC is a distinct disease or a colonic manifestation of eosinophilic gastrointestinal diseases (EGIDs) or inflammatory bowel disease (IBD) is undetermined. METHODS: Subjects with EoC (n=27) and controls (normal [NL, n=20], Crohn disease [CD, n=14]) were enrolled across sites associated with the Consortium of Eosinophilic Gastrointestinal Disease Researchers (CEGIR). EoC was diagnosed as colonic eosinophilia (ascending ≥100, descending ≥85, sigmoid ≥65 eosinophils/high-power field) with related symptoms. Colon biopsies were subjected to RNA sequencing. Associations between gene expression and histologic features were analyzed with Spearman correlation; operational pathways and cellular constituents were computationally derived. RESULTS: We identified 987 differentially expressed genes (EoC transcriptome) between EoC and NL (>1.5-fold change, P < .05). Colonic eosinophil count correlated with 31% of EoC transcriptome, most notably with CCL11 and CLC (r=0.78 and 0.77, P < .001). Among EoC and other EGIDs, there was minimal transcriptomic overlap; and minimal evidence of a strong allergic type 2 immune response compared with other EGIDs. Decreased cell-cycle and increased apoptosis in EoC compared with NL were identified by functional enrichment analysis and immunostaining using Ki-67 and cleaved caspase-3. Pericryptal circumferential eosinophil collars were associated with the EoC transcriptome (P < .001). EoC transcriptome-based scores were reversible with disease remission and differentiated EoC from IBD, even after controlling for colonic eosinophil levels (P < .0001). CONCLUSION: We established EoC transcriptomic profiles, identified mechanistic pathways, and integrated findings with parallel IBD and EGID data. These findings establish EoC as a distinct disease compared with other EGIDs and IBD, thereby providing a basis for improving diagnosis and treatment.

Published
2022
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3. Loss of Endothelial TSPAN12 Promotes Fibrostenotic Eosinophilic Esophagitis via Endothelial Cell–Fibroblast Crosstalk

Author

Tetsuo Shoda, Ting Wen, Julie M. Caldwell, Netali Ben-Baruch Morgenstern, Garrett A. Osswald, Mark Rochman, Lydia E. Mack, Jennifer M. Felton, J. Pablo Abonia, Nicoleta C. Arva, Dan Atkins, Peter A. Bonis, Kelley E. Capocelli, Margaret H. Collins, Evan S. Dellon, Gary W. Falk, Nirmala Gonsalves, Sandeep K. Gupta, Ikuo Hirano, John Leung, Paul A. Menard-Katcher, Vincent A. Mukkada, Philip E. Putnam, Amanda K. Rudman Spergel, Jonathan M. Spergel, Joshua B. Wechsler, Guang-Yu Yang, Seema S. Aceves, Glenn T. Furuta, Marc E. Rothenberg, Seema Aceves, Samuel Almonte, Rachel Andrews, Ashley Arrington, Nicoleta Arva, Fred Atkins, Dominique Bailey, Alexis Berry, Bridget Besl, Scott Bolton, Peter Bonis, Wendy Book, Kimberly Bray, Teresa Brown, Cassandra Burger, Deirdre Burke, Jonathon Cahoon, Kelley Capocelli, Mirna Chehade, Margaret Collins, Carla Davis, Evan Dellon, Maureen DeMarshall, Lauren DiTommaso, Ranjan Dohil, Michael Eby, Gary Falk, David Fleischer, Heather Foote, Kelci Foss, Joel Friedlander, Patricia Fulkerson, Glenn Furuta, Debra Geno, Thomas Greuter, Sandeep Gupta, Frank Hamilton, Kirk Harris, Jennifer Harris, Girish Hiremath, Nicole Holland-Thomas, Lea Jacinto, Amir Kagalwalla, Timothy Kaseta, David Katzka, Kaitlin Keeley, Emad Khosh-Hemmat, Paneez Khoury, Eileen King, Kara Kliewer, Amy Klion, Jennifer Knowles, Kendra Kocher, Ellyn Kodroff, Jeffrey Krischer, Shay Kyle, Meredith Levy, Chris Liacouras, Denise Mack, Lisa Martin, Ellen Martin, Talaya McCright-Gill, Paul Menard-Katcher, Calies Menard-Katcher, Gabriela Mendoza, Melissa Mingler, Mike Minnicozzi, Amanda Muir, Vincent Mukkada, Cristin MurrayPetzold, Robert Newbury, Quan Nhu, Oghenekpaobor (Joel) Oyibo, Allisa Paliana, Zhaoxing Pan, Robbie Pesek, Kathryn Peterson, Heidi Poppendeck, Philip Putnam, Fabian Rivera, Marc Rothenberg, Amanda Rudman Spergel, Kathleen Sable, Alain Schoepfer, Melissa Scott, Rachel Sheridan, Selma Sinanovic, Jonathan Spergel, MaryJo Strobel, Kiki Sun, Amy Tasco, Crystal Tholen, Katherine Thompson, Tiffany Tomkinson, Daisy Tran, Alexandra Tylicki, Tiina Urv, Mei-Lun Wang, Joshua Wechsler, Barry Wershil, Lisa Wheatley, Leah Wilkey, Angelika Zalewski, and Amy Zicarelli

Subjects
Adult, Male, Pathology, medicine.medical_specialty, Thymic stromal lymphopoietin, Adolescent, Endothelium, Tetraspanins, medicine.drug_class, Proton-pump inhibitor, Young Adult, Esophagus, Fibrosis, Eosinophilic, medicine, Humans, Gene Silencing, RNA, Small Interfering, Child, Eosinophilic esophagitis, Interleukin-13, Hepatology, business.industry, Gastroenterology, Endothelial Cells, Eosinophilic Esophagitis, Fibroblasts, Middle Aged, Eosinophil, medicine.disease, medicine.anatomical_structure, Gene Expression Regulation, Gastrointestinal disease, Child, Preschool, Esophageal Stenosis, Female, business
Abstract

Eosinophilic esophagitis (EoE) can progress to fibrostenosis by unclear mechanisms. Herein, we investigated gene dysregulation in fibrostenotic EoE, its association with clinical parameters and specific pathways, and the functional consequences.Esophageal biopsies from subjects with EoE were collected across 11 Consortium of Eosinophilic Gastrointestinal Disease Researchers sites (n = 311) and 2 independent replication cohorts (n = 83). Inclusion criteria for fibrostenotic EoE were endoscopic rings, stricture, and/or a history of dilation. Endoscopic, histologic, and molecular features were assessed by the EoE Endoscopic Reference Score, EoE Histology Scoring System, EoE Diagnostic Panel, and RNA sequencing. Esophageal endothelial TSPAN12 expression and functional effects on barrier integrity and gene expression were analyzed in vitro.TSPAN12 was the gene most correlated with fibrostenosis (r = -0.40, P.001). TSPAN12 was lower in fibrostenotic EoE and correlated with EoE Endoscopic Reference Score, EoE Diagnostic Panel, and EoE Histology Scoring System (r = 0.34-0.47, P.001). Lower TSPAN12 associated with smaller esophageal diameter (r = 0.44, P = .03), increased lamina propria fibrosis (r = -0.41, P.001), and genes enriched in cell cycle-related pathways. Interleukin (IL)-13 reduced TSPAN12 expression in endothelial cells. Conversely, anti-IL-13 therapy increased TSPAN12 expression. TSPAN12 gene silencing increased endothelial cell permeability and dysregulated genes associated with extracellular matrix pathways. Endothelial cell-fibroblast crosstalk induced extracellular matrix changes relevant to esophageal remodeling.Patients with fibrostenotic EoE express decreased levels of endothelial TSPAN12. We propose that IL-13 decreases TSPAN12, likely contributing to the chronicity of EoE by promoting tissue remodeling through fibroblast-endothelial cell crosstalk.

Published
2022
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4. Advancing patient care through the Consortium of Eosinophilic Gastrointestinal Disease Researchers (CEGIR)

Author

Seema Aceves, Margaret H. Collins, Marc E. Rothenberg, Glenn T. Furuta, Nirmala Gonsalves, J. Pablo Abonia, Samuel Almonte, Rachel Andrews, Ashley Arrington, Nicoleta Arva, Fred Atkins, Dominique Bailey, Alexis Berry, Bridget Besl, Scott Bolton, Peter Bonis, Wendy Book, Kimberly Bray, Teresa Brown, Cassandra Burger, Deirdre Burke, Jonathon Cahoon, Kelley Capocelli, Mirna Chehade, Margaret Collins, Carla Davis, Evan Dellon, Maureen DeMarshall, Lauren DiTommaso, Ranjan Dohil, Michael Eby, Gary Falk, David Fleischer, Heather Foote, Kelci Foss, Joel Friedlander, Patricia Fulkerson, Glenn Furuta, Debra Geno, Thomas Greuter, Sandeep Gupta, Frank Hamilton, Kirk Harris, Jennifer Harris, Ikuo Hirano, Girish Hiremath, Nicole Holland-Thomas, Lea Jacinto, Amir Kagalwalla, Timothy Kaseta, David Katzka, Kaitlin Keeley, Emad Khosh-Hemmat, Paneez Khoury, Eileen King, Kara Kliewer, Amy Klion, Jennifer Knowles, Kendra Kocher, Ellyn Kodroff, Jeffrey Krischer, Shay Kyle, John Leung, Meredith Levy, Chris Liacouras, Denise Mack, Lisa Martin, Ellen Martin, Talaya McCright-Gill, Paul Menard-Katcher, Calies Menard-Katcher, Gabriela Mendoza, Melissa Mingler, Mike Minnicozzi, Amanda Muir, Vincent Mukkada, Cristin MurrayPetzold, Robert Newbury, Quan Nhu, Oghenekpaobor (Joel) Oyibo, Allisa Paliana, Zhaoxing Pan, Robbie Pesek, Kathryn Peterson, Heidi Poppendeck, Philip Putnam, Fabian Rivera, Marc Rothenberg, Amanda Rudman-Spergel, Kathleen Sable, Alain Schoepfer, Melissa Scott, Rachel Sheridan, Selma Sinanovic, Jonathan Spergel, MaryJo Strobel, Kiki Sun, Amy Tasco, Crystal Tholen, Katherine Thompson, Tiffany Tomkinson, Daisy Tran, Alexandra Tylicki, Tiina Urv, Mei-Lun Wang, Joshua Wechsler, Barry Wershil, Lisa Wheatley, Leah Wilkey, Guang-Yu Yang, Angelika Zalewski, and Amy Zicarelli

Subjects
Clinical Trials as Topic, Medical education, Biomedical Research, Eosinophilic gastritis, business.industry, Immunology, Eosinophilic Esophagitis, Patient advocacy, Enteritis, United States, Article, Patient care, Clinical trial, Natural history, National Institutes of Health (U.S.), Multidisciplinary approach, Gastritis, Eosinophilia, Eosinophilic, Immunology and Allergy, Medicine, Patient-reported outcome, business
Abstract

Recent advances in rare disease research are accelerated by the work of consortia that have been supported by the National Institutes of Health. Development of such consortia rely on multidisciplinary relationships and engagement with patient advocacy groups, as well as the National Institutes of Health and industry and academic partners. In this rostrum we present the development of such a process that focuses on eosinophilic gastrointestinal diseases. Principal investigators, patient advocacy groups, research assistants, and trainees work together to perform natural history studies that promote clinical trial readiness tools, conduct clinical trials, train a new generation of investigators, and perform innovative pilot studies.

Published
2020
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