Reduced LHFPL3-AS2 lncRNA expression is linked to altered epithelial polarity and proliferation, and to ileal ulceration in Crohn disease

Katya E. Sosnovski, Tzipi Braun, Amnon Amir, Marina BenShoshan, Haya Abbas-Egbariya, Rakefet Ben-Yishay, Liat Anafi, Camilla Avivi, Iris Barshack, Lee A. Denson, Yael Haberman*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Disruption of intestinal epithelial functions is linked to Crohn disease (CD) pathogenesis. We identified a widespread reduction in the expression of long non-coding RNAs (lncRNAs) including LHFPL3-AS2 in the treatment-naïve CD ileum of the RISK pediatric cohort. We validated the reduction of LHFPL3-AS2 in adult CD and noted a further reduction in patients with more severe CD from the RISK cohort. LHFPL3-AS2 knockdown in Caco-2 cells robustly affected epithelial monolayer morphogenesis with markedly reduced confluency and spreading, showing atypical rounding, and clumping. mRNA-seq analysis of LHFPL3-AS2 knockdown cells highlighted the reduction of genes and pathways linked with apical polarity, actin bundles, morphogenesis, and the b-catenin-TCF4 complex. LHFPL3-AS2 knockdown significantly reduced the ability of cells to form an internal lumen within the 3-dimensional (3D) cyst model, with mislocalization of actin and adherent and tight junction proteins, affecting epithelial polarity. LHFPL3-AS2 knockdown also resulted in defective mitotic spindle formation and consequent reduction in epithelial proliferation. Altogether, we show that LHFPL3-AS2 reduction affects epithelial morphogenesis, polarity, mitotic spindle formation, and proliferation, which are key processes in maintaining epithelial homeostasis in CD. Reduced expression of LHFPL3-AS2 in CD patients and its further reduction with ileal ulceration outcome, emphasizes its significance in this context.

Original languageEnglish
Article number20513
JournalScientific Reports
Volume13
Issue number1
DOIs
StatePublished - Dec 2023

Funding

FundersFunder number
Leona M. and Harry B. Helmsley Charitable TrustP30 DK078392
Leona M. and Harry B. Helmsley Charitable Trust
European Research Council758313
European Research Council
Israel Science Foundation908/15, 785/22
Israel Science Foundation
Israeli Centers for Research Excellence41/11
Israeli Centers for Research Excellence

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