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Long noncoding RNA PARAL1 regulates myeloid dendritic cell differentiation and TLR signaling

Genes & Immunity volume 26, pages 151–165 (2025)Cite this article

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Abstract

Dendritic cells (DCs) are professional antigen presentation cells (APCs) that bridge innate and adaptive immune functions to contain pathogenic threats. Long noncoding RNAs (lncRNAs) are implicated in regulating biological processes, including inflammation and immunity. However, the knowledge of myeloid DC-expressed lncRNA repertoire and their regulatory functions is limited. Here we profiled lncRNA expression kinetics during monocyte-to-DC (moDC) differentiation and characterized their functional roles. Our RNA-seq data identified a repertoire of differentially expressed lncRNAs associated with moDC differentiation and a large subset of these lncRNAs are distinct from M1 or M2 macrophages. We selected two DC-enriched lncRNAs and observed that PARAL1 silencing, or overexpression modulates DC surface markers expression. Importantly, PARAL1 RNAi significantly reduced, while its overexpression upregulated the levels of multiple TLRs. Upon treatment with TLR agonists PARAL1 knockdown cells exhibit reduced NF-κB, IRF3 and IRF7 phosphorylation substantiating its role in potentiating TLR signaling. Mechanistically, PARAL1 silencing showed significant downregulation of multiple NF-κB-induced genes and time-dependent inhibition of proinflammatory cytokine secretion upon challenge with TLR agonists. Finally, PARAL1 RNAi in DCs significantly impaired antigen processing and presentation to T cells. Overall, this study characterized novel functions of PARAL1 in regulating DC differentiation, TLR-dependent innate immunity and activation of adaptive immune response.

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Fig. 1: LncRNA expression dynamics during monocyte-to-DC differentiation.
Fig. 2: LncRNA PARAL1 regulates monocyte-to-DC differentiation.
Fig. 3: LncRNA PARAL1 regulates TLR expression during monocyte-to-DC differentiation.
Fig. 4: LncRNA PARAL1 knockdown impairs proinflammatory cytokine secretion by DCs upon TLR stimulation.
Fig. 5: LncRNA PARAL1 regulates TLR signaling-dependent phosphorylation.
Fig. 6: PARAL1 knockdown affects TLR-directed NF-κB-dependent gene expression.
Fig. 7: LncRNA PARAL1 regulates DC antigen processing and presentation to T cells.

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Data availability

The raw RNA sequencing data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database under the accession number GSE285316 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE285316). All study data are included in the article and Supplementary files.

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Funding

This study was supported by NIH/NIDCR contract grant numbers R03DE027147, R01DE027980, R21DE026259 (ARN) and NIH/NEI contract grant number 1R01EY033622 (DS and ARN). We acknowledge Flow cytometry core, UIC for assisting in flow cytometry analyses.

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Authors and Affiliations

  1. Department of Periodontics, College of Dentistry, University of Illinois Chicago, Chicago, IL, 60612, USA

    Raza Ali Naqvi, Araceli Valverde & Afsar Naqvi

  2. Department of Microbiology and Immunology, College of Medicine, University of Illinois Chicago, Chicago, IL, 60612, USA

    Deepak Shukla & Afsar Naqvi

  3. Department of Ophthalmology and Visual Sciences, University of Illinois Medical Center, Chicago, IL, 60612, USA

    Deepak Shukla

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  1. Raza Ali Naqvi
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RAN (Investigation, Methodology, Validation, Formal analysis, Resources, Original draft preparation, Reviewing and Editing); AV (Investigation, Methodology, Validation, Formal analysis, Resources); DS (Methodology, Resources, Writing- Original draft preparation, Reviewing and Editing); AN (Conceptualization, Investigation, Resources, Writing- Original draft preparation, Reviewing and Editing).

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Correspondence to Afsar Naqvi.

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Naqvi, R.A., Valverde, A., Shukla, D. et al. Long noncoding RNA PARAL1 regulates myeloid dendritic cell differentiation and TLR signaling. Genes Immun 26, 151–165 (2025). https://doi.org/10.1038/s41435-025-00323-9

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