Role of LncRNA MAGI2-AS3 in Lipopolysaccharide-induced Nucleus Pulposus Cells Injury by Regulating MiR-374b-5p/interleukin-10 Axis

Overview

Journal Immun Inflamm Dis

Specialties Allergy & Immunology
Infectious Diseases

Date 2023 Apr 27

PMID 37102649

Authors

Jiang Yu

Chengjin Li

Affiliations

Soon will be listed here.

Abstract

Background: Intervertebral disc degeneration (IDD) is a pathological process that occurs during the natural aging of intervertebral discs. Accumulating evidence suggests that noncoding RNAs (ncRNAs), including microRNAs and long ncRNAs (lncRNAs), participate in the pathogenesis and development of IDD. Herein, we examined the role of lncRNA MAGI2-AS3 in the pathogenic mechanism of IDD.

Material And Methods: To develop an IDD in vitro model, we treated human nucleus pulposus (NP) cells with lipopolysaccharide (LPS). Aberrant levels of lncRNA MAGI2-AS3, miR-374b-5p, interleukin (IL)-10 and extracellular matrix (ECM)-related proteins in NP cells were examined using reverse transcription-quantitative PCR and western blot analysis. LPS-induced NP cell injury and inflammatory response were confirmed using the MTT assay, flow cytometry, Caspase3 activity, and enzyme-linked immunosorbent assay. Dual-luciferase reporter assay and rescue experiments were performed to confirm targets between lncRNA MAGI2-AS3 and miR-374b-5p or miR-374b-5p and IL-10.

Results: LPS-induced NP cells exhibited low levels of lncRNA MAGI2-AS3 and IL-10 expression, along with high miR-374b-5p expression. miR-374b-5p was a target of lncRNA MAGI2-AS3 and IL-10. LncRNA MAGI2-AS3 ameliorated injury, inflammatory response, and ECM degradation in LPS-treated NP cells by downregulating miR-374b-5p to upregulate IL-10 expression.

Conclusions: LncRNA MAGI2-AS3 increased IL-10 expression levels by sponging miR-374b-5p, which, in turn, alleviated LPS-triggered decreased NP cell proliferation and increased apoptosis, inflammatory response, and ECM degradation. Therefore, lncRNA MAGI2-AS3 may be a potential therapeutic target for IDD.

Citing Articles

Downregulation of circTLK1 improves the impairments in learning and memory induced by anesthetics via regulating miR-374b-5p expression and reducing neuroinflammation.

Zhu X Toxicol Res (Camb). 2024; 13(6):tfae220.

PMID: 39712639 PMC: 11659641. DOI: 10.1093/toxres/tfae220.

Research progress on long non‑coding RNAs in non‑infectious spinal diseases (Review).

Ma Z, Liu X, Zhang X, Li S, An J, Luo Z Mol Med Rep. 2024; 30(3).

PMID: 38994759 PMC: 11267249. DOI: 10.3892/mmr.2024.13288.

LncRNA MAGI2-AS3 promotes fracture healing through downregulation of miR-223-3p.

Dong Z, Hu B, Wang S, Wang M, Sun S, Liu X J Orthop Surg Res. 2024; 19(1):370.

PMID: 38907263 PMC: 11193218. DOI: 10.1186/s13018-024-04850-5.

Role of lncRNA MAGI2-AS3 in lipopolysaccharide-induced nucleus pulposus cells injury by regulating miR-374b-5p/interleukin-10 axis.

Yu J, Li C Immun Inflamm Dis. 2023; 11(4):e772.

PMID: 37102649 PMC: 10108685. DOI: 10.1002/iid3.772.

References

Zhang Q, Hu S, Hu A, Zhang T, Jiang L, Li X . Autophagy-activated nucleus pulposus cells deliver exosomal miR-27a to prevent extracellular matrix degradation by targeting MMP-13. J Orthop Res. 2020; 39(9):1921-1932. DOI: 10.1002/jor.24880. View

Akbaba T, Akkaya-Ulum Y, Tavukcuoglu Z, Bilginer Y, Ozen S, Balci-Peynircioglu B . Inflammation-related differentially expressed common miRNAs in systemic autoinflammatory disorders patients can regulate the clinical course. Clin Exp Rheumatol. 2021; 39 Suppl 132(5):109-117. DOI: 10.55563/clinexprheumatol/t67tvc. View

Kaji R, Kiyoshima-Shibata J, Tsujibe S, Nanno M, Shida K . Short communication: Probiotic induction of interleukin-10 and interleukin-12 production by macrophages is modulated by co-stimulation with microbial components. J Dairy Sci. 2018; 101(4):2838-2841. DOI: 10.3168/jds.2017-13868. View

Li H, Liang J, Qin F, Zhai Y . MiR-374b-5p-FOXP1 feedback loop regulates cell migration, epithelial-mesenchymal transition and chemosensitivity in ovarian cancer. Biochem Biophys Res Commun. 2018; 505(2):554-560. DOI: 10.1016/j.bbrc.2018.09.161. View

Xu Y, Zhang S, Fu D, Lu D . Circulating miR-374b-5p negatively regulates osteoblast differentiation in the progression of osteoporosis via targeting Wnt3 AND Runx2. J Biol Regul Homeost Agents. 2020; 34(2):345-355. DOI: 10.23812/19-507-A-9. View

Cheng X, Zhang L, Zhang K, Zhang G, Hu Y, Sun X . Circular RNA VMA21 protects against intervertebral disc degeneration through targeting miR-200c and X linked inhibitor-of-apoptosis protein. Ann Rheum Dis. 2018; 77(5):770-779. PMC: 5909753. DOI: 10.1136/annrheumdis-2017-212056. View

Chen X, Li Z, Xu D, Li S . LINC01121 induced intervertebral disc degeneration via modulating miR-150-5p/MMP16 axis. J Gene Med. 2020; 22(10):e3231. DOI: 10.1002/jgm.3231. View

Zhao B, Lu M, Wang D, Li H, He X . Genome-Wide Identification of Long Noncoding RNAs in Human Intervertebral Disc Degeneration by RNA Sequencing. Biomed Res Int. 2017; 2016:3684875. PMC: 5206422. DOI: 10.1155/2016/3684875. View

Shi C, Wu L, Lin W, Cai Y, Zhang Y, Hu B . MiR-202-3p regulates interleukin-1β-induced expression of matrix metalloproteinase 1 in human nucleus pulposus. Gene. 2018; 687:156-165. DOI: 10.1016/j.gene.2018.11.056. View

10.

Pfander P, Eiers A, Burret U, Vettorazzi S . Deletion of in Macrophages Ameliorates Anti-Inflammatory Response during Endotoxemia through Induction of C-Maf and Il-10. Int J Mol Sci. 2021; 22(17). PMC: 8431799. DOI: 10.3390/ijms22179648. View

11.

Aurilia C, Donati S, Palmini G, Miglietta F, Iantomasi T, Brandi M . The Involvement of Long Non-Coding RNAs in Bone. Int J Mol Sci. 2021; 22(8). PMC: 8069547. DOI: 10.3390/ijms22083909. View

12.

Cui S, Liu Z, Tang B, Wang Z, Li B . LncRNA MAGI2-AS3 is down-regulated in intervertebral disc degeneration and participates in the regulation of FasL expression in nucleus pulposus cells. BMC Musculoskelet Disord. 2020; 21(1):149. PMC: 7059357. DOI: 10.1186/s12891-020-3086-y. View

13.

Li D, Du X, Zhu M, Yang S, Zhao W . MiR-374b-5p Regulates T Cell Differentiation and Is Associated with rEg.P29 Immunity. Biomed Res Int. 2020; 2020:8024763. PMC: 7463394. DOI: 10.1155/2020/8024763. View

14.

Alpantaki K, Kampouroglou A, Koutserimpas C, Effraimidis G, Hadjipavlou A . Diabetes mellitus as a risk factor for intervertebral disc degeneration: a critical review. Eur Spine J. 2019; 28(9):2129-2144. DOI: 10.1007/s00586-019-06029-7. View

15.

Fei Q, Yu Y, Liu L, Zhang Y, Baldrich P, Dai Q . Biogenesis of a 22-nt microRNA in Phaseoleae species by precursor-programmed uridylation. Proc Natl Acad Sci U S A. 2018; 115(31):8037-8042. PMC: 6077734. DOI: 10.1073/pnas.1807403115. View

16.

Ge J, Yan Q, Wang Y, Cheng X, Song D, Wu C . IL-10 delays the degeneration of intervertebral discs by suppressing the p38 MAPK signaling pathway. Free Radic Biol Med. 2019; 147:262-270. DOI: 10.1016/j.freeradbiomed.2019.12.040. View

17.

Li Z, Sun Y, He M, Liu J . Differentially-expressed mRNAs, microRNAs and long noncoding RNAs in intervertebral disc degeneration identified by RNA-sequencing. Bioengineered. 2021; 12(1):1026-1039. PMC: 8806213. DOI: 10.1080/21655979.2021.1899533. View

18.

Chen Y, Wu Y, Chen R, Xu C, Chen Q . LncRNA LINC00324 is upregulated in intervertebral disk degeneration and upregulates FasL in nucleus pulposus cells. Mol Cell Biochem. 2021; 476(5):1995-2000. DOI: 10.1007/s11010-021-04058-9. View

19.

Li W, Liu T, Wu L, Chen C, Jia Z, Bai X . Blocking the function of inflammatory cytokines and mediators by using IL-10 and TGF-β: a potential biological immunotherapy for intervertebral disc degeneration in a beagle model. Int J Mol Sci. 2014; 15(10):17270-83. PMC: 4227161. DOI: 10.3390/ijms151017270. View

20.

Teraguchi M, Yoshimura N, Hashizume H, Yamada H, Oka H, Minamide A . Progression, incidence, and risk factors for intervertebral disc degeneration in a longitudinal population-based cohort: the Wakayama Spine Study. Osteoarthritis Cartilage. 2017; 25(7):1122-1131. DOI: 10.1016/j.joca.2017.01.001. View