Multi-omics empowered deep phenotyping of ulcerative colitis identifies biomarker signatures reporting functional remission states

Author(s)
Lukas Janker, Dina Schuster, Patricia Bortel, Gerhard Hagn, Samuel M Meier-Menches, Thomas Mohr, Johanna C Mader, Astrid Slany, Andrea Bileck, Julia Brunmair, Christian Madl, Lukas Unger, Barbara Hennlich, Barbara Weitmayr, Giorgia Del Favero, Dietmar Pils, Tobias Pukrop, Nikolaus Pfisterer, Thomas Feichtenschlager, Christopher Gerner
Abstract

Introduction: Ulcerative colitis [UC] is a chronic disease with rising incidence and unclear aetiology. Deep molecular phenotyping by multiomics analyses may provide novel insights into disease processes and characteristic features of remission states. Methods: UC pathomechanisms were assessed by proteome profiling of human tissue specimens, obtained from five distinct colon locations for each of the 12 patients included in the study. Systemic disease-associated alterations were evaluated thanks to a cross-sectional setting of mass spectrometry-based multiomics analyses comprising proteins, metabolites, and eicosanoids of plasma obtained from UC patients during acute episodes and upon remission, in comparison with healthy controls. Results: Tissue proteome profiling indicated colitis-associated activation of neutrophils, macrophages, B and T cells, fibroblasts, endothelial cells and platelets, and hypoxic stress, and suggested a general downregulation of mitochondrial proteins accompanying the establishment of apparent wound healing-promoting activities including scar formation. Whereas pro-inflammatory proteins were apparently upregulated by immune cells, the colitis-associated epithelial cells, fibroblasts, endothelial cells, and platelets seemed to predominantly contribute anti-inflammatory and wound healing-promoting proteins. Blood plasma proteomics indicated chronic inflammation and platelet activation, whereas plasma metabolomics identified disease-associated deregulations of gut and gut microbiome-derived metabolites. Upon remission several, but not all, molecular candidate biomarker levels recovered back to normal. Conclusion:. The findings may indicate that microvascular damage and platelet deregulation hardly resolve upon remission, but apparently persist as disease-associated molecular signatures. This study presents local and systemic molecular alterations integrated in a model for UC pathomechanisms, potentially supporting the assessment of disease and remission states in UC patients.

Organisation(s)
Department of Analytical Chemistry, Joint Metabolome Facility, Department of Inorganic Chemistry, Core Facility Multimodal Imaging, Department of Food Chemistry and Toxicology, Mass Spectrometry Centre
External organisation(s)
Medizinische Universität Wien, Krankenanstalt Rudolfstiftung, University Hospital Regensburg
Journal
Journal of Crohn's & colitis
Volume
17
Pages
1514-1527
No. of pages
14
ISSN
1873-9946
DOI
https://doi.org/10.1093/ecco-jcc/jjad052
Publication date
09-2023
Peer reviewed
Yes
Austrian Fields of Science 2012
302016 Gastroenterology, 106037 Proteomics, 301303 Medical biochemistry
Keywords
ASJC Scopus subject areas
General Medicine
Sustainable Development Goals
SDG 3 - Good Health and Well-being
Portal url
https://ucrisportal.univie.ac.at/en/publications/64cfa9b2-eed8-46cf-bd1e-0ddeeb271b63