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Elling, Roland; Robinson, Elektra K.; Shapleigh, Barbara; Liapis, Stephen C.; Covarrubias, Sergio; Katzman, Sol; Groff, Abigail F.; Jiang, Zhaozhao; Agarwal, Shiuli; Motwani, Mona; Chan, Jennie; Sharma, Shruti; Hennessy, Elizabeth J.; FitzGerald, Garret A.; McManus, Michael T.; Rinn, John L.; Fitzgerald, Katherine A.; Carpenter, Susan
Cell reports (Cambridge), 11/2018, Letnik: 25, Številka: 6Journal Article
An inducible gene expression program is a hallmark of the host inflammatory response. Recently, long intergenic non-coding RNAs (lincRNAs) have been shown to regulate the magnitude, duration, and resolution of these responses. Among these is lincRNA-Cox2, a dynamically regulated gene that broadly controls immune gene expression. To evaluate the in vivo functions of this lincRNA, we characterized multiple models of lincRNA-Cox2-deficient mice. LincRNA-Cox2-deficient macrophages and murine tissues had altered expression of inflammatory genes. Transcriptomic studies from various tissues revealed that deletion of the lincRNA-Cox2 locus also strongly impaired the basal and inducible expression of the neighboring gene prostaglandin-endoperoxide synthase (Ptgs2), encoding cyclooxygenase-2, a key enzyme in the prostaglandin biosynthesis pathway. By utilizing different genetic manipulations in vitro and in vivo, we found that lincRNA-Cox2 functions through an enhancer RNA mechanism to regulate Ptgs2. More importantly, lincRNA-Cox2 also functions in trans, independently of Ptgs2, to regulate critical innate immune genes in vivo. Display omitted •Study of lincRNA-Cox2 in vivo using recently generated KO and splicing mutant mice•lincRNA-Cox2 functions through an enhancer RNA mechanism to regulate Ptgs2 levels•lincRNA-Cox2 has a trans regulatory role controlling many innate immune genes•The lincRNA locus simultaneously regulates the expression of local and distant genes Elling et al. utilize a number of lincRNA-Cox2 genetic models to show that lincRNA-Cox2 can regulate its neighboring gene Ptgs2 (Cox2) through an enhancer RNA mechanism. They generate a lincRNA-Cox2 splicing-deficient mouse and confirm that lincRNA-Cox2 functions in trans to regulate immune genes following LPS-induced endotoxic shock.
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