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The Effect of Phenotype and Genotype on the Plasma Proteome in Patients with Inflammatory Bowel Disease

  • Arno R. Bourgonje
  • , Shixian Hu
  • , Lieke M. Spekhorst
  • , Daria V. Zhernakova
  • , Arnau Vich Vila
  • , Yanni Li
  • , Michiel D. Voskuil
  • , Lisette A. van Berkel
  • , Brenda Bley Folly
  • , Mohammed Charrout
  • , Ahmed Mahfouz
  • , Marcel J. T. Reinders
  • , Julia I. P. van Heck
  • , Leo A. B. Joosten
  • , Marijn C. Visschedijk
  • , Hendrik M. van Dullemen
  • , Klaas Nico Faber
  • , Janneke N. Samsom
  • , Eleonora A. M. Festen
  • , Gerard Dijkstra
  • Rinse K. Weersma*
*Corresponding author for this work
  • University of Groningen
  • St. Petersburg National Research University of Information Technologies, Mechanics and Optics (ITMO)
  • Erasmus University Rotterdam
  • Delft University of Technology
  • Leiden University
  • Radboud University Nijmegen

Research output: Contribution to journalArticleAcademicpeer-review

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Abstract

Background and Aims: Protein profiling in patients with inflammatory bowel diseases [IBD] for diagnostic and therapeutic purposes is underexplored. This study analysed the association between phenotype, genotype, and the plasma proteome in IBD. Methods: A total of 92 inflammation-related proteins were quantified in plasma of 1028 patients with IBD (567 Crohn's disease [CD]; 461 ulcerative colitis [UC]) and 148 healthy individuals to assess protein-phenotype associations. Corresponding whole-exome sequencing and global screening array data of 919 patients with IBD were included to analyse the effect of genetics on protein levels (protein quantitative trait loci [pQTL] analysis). Intestinal mucosal RNA sequencing and faecal metagenomic data were used for complementary analyses. Results: Thirty-two proteins were differentially abundant between IBD and healthy individuals, of which 22 proteins were independent of active inflammation; 69 proteins were associated with 15 demographic and clinical factors. Fibroblast growth factor-19 levels were decreased in CD patients with ileal disease or a history of ileocecal resection. Thirteen novel cis-pQTLs were identified and 10 replicated from previous studies. One trans-pQTL of the fucosyltransferase 2 [FUT2] gene [rs602662] and two independent cis-pQTLs of C-C motif chemokine 25 [CCL25] affected plasma CCL25 levels. Intestinal gene expression data revealed an overlapping cis-expression [e]QTL-variant [rs3745387] of the CCL25 gene. The FUT2 rs602662 trans-pQTL was associated with reduced abundances of faecal butyrate-producing bacteria. Conclusions: This study shows that genotype and multiple disease phenotypes strongly associate with the plasma inflammatory proteome in IBD, and identifies disease-associated pathways that may help to improve disease management in the future.
Original languageEnglish
Pages (from-to)414-429
Number of pages16
JournalJournal of Crohn's and Colitis
Volume16
Issue number3
DOIs
Publication statusPublished - 1 Mar 2022
Externally publishedYes

Keywords

  • Inflammatory bowel disease
  • genetics
  • proteomics

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