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Up-regulated lncRNA-PVT1 expression in peripheral blood mononuclear cells of patients with coronary artery disease is correlated with decreased interleukin-10 production

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Abstract

Objectives

Plasmacytoma variant translocation 1 (PVT1) is a newly discovered long non-coding RNA, which has not been previously studied in the inflammatory responses of the peripheral blood mononuclear cells (PBMCs) of patients with coronary artery disease (CAD).

Materials and methods

This cross-sectional study was conducted on 15 CAD patients and 15 non-CAD (NCAD) individuals. The PVT1 expression was assessed in the PBMCs of the participants using a real-time polymerase chain reaction. Interleukin (IL)-10, IL-22, and matrix metalloproteinase-9 (MMP-9) were measured in the plasma and supernatant of cultured PBMCs in the presence or absence of lipopolysaccharide (LPS) using flow cytometry and enzyme-linked immunosorbent assay.

Results

An increased expression of PVT1 was observed in the untreated PBMCs of CAD patients, compared to the NCAD group. The PVT1 was significantly up-regulated after LPS treatment in the PBMCs of both groups. Plasma MMP-9 levels were found to be higher in CAD patients than in the control individuals. The level of IL-10 and IL-22 production by the non-treated PBMCs of CAD cases was significantly lower than the NCAD group. Overall, in the examined population, PVT1 expression was negatively correlated with IL-10 secretion. Moreover, the results showed a significant negative correlation between PVT1 expression and IL-10 production by untreated cells.

Conclusions

The PVT1 expression augmented in the PBMCs of CAD patients, which could be associated with the decreased IL-10 generation by the PBMCs of these patients.

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Data availability

All data will available from corresponding author, with reasonable request. A preprint of this study has already been published (https://doi.org/10.21203/rs.3.rs-50028/v2).

References

  1. Zhang L, Lou D, He D, Wang Y, Wu Y, Cao X et al (2021) Dysregulated circulating apoptosis- and autophagy-related lncRNAs as diagnostic markers in coronary artery disease. Biomed Res Int 2021:5517786

    PubMed  PubMed Central  Google Scholar 

  2. Silvestre-Roig C, de Winther MP, Weber C, Daemen MJ, Lutgens E, Soehnlein O (2014) Atherosclerotic plaque destabilization: mechanisms, models, and therapeutic strategies. Circ Res 114(1):214–226

    Article  CAS  PubMed  Google Scholar 

  3. Nguyen MT, Fernando S, Schwarz N, Tan J, Bursill CA, Psaltis PJ (2019) Inflammation as a therapeutic target in atherosclerosis. J Clin Med 8(8):1109

    Article  CAS  PubMed Central  Google Scholar 

  4. Akbari H, Asadikaram G, Jafari A, Nazari-Robati M, Ebrahimi G, Ebrahimi N et al (2018) Atorvastatin, losartan and captopril may upregulate IL-22 in hypertension and coronary artery disease; the role of gene polymorphism. Life Sci 207:525–531

    Article  CAS  PubMed  Google Scholar 

  5. Poznyak AV, Bharadwaj D, Prasad G, Grechko AV, Sazonova MA, Orekhov AN (2021) Anti-inflammatory therapy for atherosclerosis: focusing on cytokines. Int J Mol Sci. https://doi.org/10.3390/ijms22137061

    Article  PubMed  PubMed Central  Google Scholar 

  6. Munjal A, Khandia R (2020) Atherosclerosis: orchestrating cells and biomolecules involved in its activation and inhibition. Adv Protein Chem Struct Biol 120:85–122

    Article  CAS  PubMed  Google Scholar 

  7. Wang X, Ota N, Manzanillo P, Kates L, Zavala-Solorio J, Eidenschenk C et al (2014) Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature 514(7521):237–241

    Article  CAS  PubMed  Google Scholar 

  8. Tokuhara CK, Santesso MR, de Oliveira GSN, da Silva Ventura TM, Doyama JT, Zambuzzi WF et al (2019) Updating the role of matrix metalloproteinases in mineralized tissue and related diseases. J Appl Oral Sci. https://doi.org/10.1590/1678-7757-2018-0596

    Article  PubMed  Google Scholar 

  9. Santos JCD, Cruz MS, Bortolin RH, Oliveira KM, Araújo JNG, Duarte VHR et al (2018) Relationship between circulating VCAM-1, ICAM-1, E-selectin and MMP9 and the extent of coronary lesions. Clinics (Sao Paulo) 73:e203

    Article  Google Scholar 

  10. Chen X, Tang FR, Arfuso F, Cai WQ, Ma Z, Yang J et al (2019) The Emerging role of long non-coding RNAs in the metastasis of hepatocellular carcinoma. Biomolecules. https://doi.org/10.3390/biom10010066

    Article  PubMed  PubMed Central  Google Scholar 

  11. Wang W, Zhou R, Wu Y, Liu Y, Su W, Xiong W et al (2019) PVT1 promotes cancer progression via microRNAs. Front Oncol. https://doi.org/10.3389/fonc.2019.00609

    Article  PubMed  PubMed Central  Google Scholar 

  12. Wu Z-y, Trenner M, Boon RA, Spin JM, Maegdefessel L (2019) Long noncoding RNAs in key cellular processes involved in aortic aneurysms. Atherosclerosis. https://doi.org/10.1016/j.atherosclerosis.2019.11.013

    Article  PubMed  PubMed Central  Google Scholar 

  13. Zhao, Y., Zhao, J., Guo, X., She, J. & Liu, Y (2018) Long non-coding RNA PVT1, a molecular sponge for miR-149, contributes aberrant metabolic dysfunction and inflammation in IL-1β-simulated osteoarthritic chondrocytes, Biosci Rep, https://doi.org/10.1042/BSR20180576

  14. Lu X, Yu Y, Yin F, Yang C, Li B, Lin J et al (2020) Knockdown of PVT1 inhibits IL-1β-induced injury in chondrocytes by regulating miR-27b-3p/TRAF3 axis. Int Immunopharmacol 79:106052

    Article  CAS  PubMed  Google Scholar 

  15. Zhao T, Ding Y, Li M, Zhou C, Lin W (2019) Silencing lncRNA PVT1 inhibits activation of astrocytes and increases BDNF expression in hippocampus tissues of rats with epilepsy by downregulating the Wnt signaling pathway. J Cell Physiol 234(9):16054–16067

    Article  CAS  Google Scholar 

  16. Zhang Z, Zou G, Chen X, Lu W, Liu J, Zhai S et al (2019) Knockdown of lncRNA PVT1 inhibits vascular smooth muscle cell apoptosis and extracellular matrix disruption in a murine abdominal aortic aneurysm model. Mol Cells 42(3):218

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Huang W, Lan X, Li X, Wang D, Sun Y, Wang Q et al (2017) Long non-coding RNA PVT1 promote LPS-induced septic acute kidney injury by regulating TNFα and JNK/NF-κB pathways in HK-2 cells. Int Immunopharmacol 47:134–140

    Article  CAS  PubMed  Google Scholar 

  18. Feng F, Qi Y, Dong C, Yang C (2018) PVT1 regulates inflammation and cardiac function via the MAPK/NF-κB pathway in a sepsis model. Exp Ther Med 16(6):4471–4478

    CAS  PubMed  PubMed Central  Google Scholar 

  19. World Medical Association (2013) World Medical Association declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310(20):2191–2194

    Article  Google Scholar 

  20. Cheng Y, Hu Q, Zhou J (2021) Silencing of lncRNA PVT1 ameliorates streptozotocin-induced pancreatic β cell injury and enhances insulin secretory capacity by regulating miR-181a-5p. Can J Physiol Pharmacol 99(3):303–312

    Article  CAS  PubMed  Google Scholar 

  21. Chang Y, Liu C, Wang J, Feng J, Chen Y, Qi M et al (2021) Downregulation of lncRNA-PVT1 participates in the development of progressive chronic kidney disease among patients with congestive heart failure. J Inflamm (London) 18(1):27

    Article  CAS  Google Scholar 

  22. Ma C, Nie XG, Wang YL, Wu DP, Liang QD (2018) Meta-analysis of the prognostic value of long non-coding RNA PVT1 for cancer patients. Medicine 97(49):e13548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Cao F, Li Z, Ding WM, Yan L, Zhao QY (2019) LncRNA PVT1 regulates atrial fibrosis via miR-128-3p-SP1-TGF-β1-Smad axis in atrial fibrillation. Mol Med (Cambridge) 25(1):7

    Article  Google Scholar 

  24. Quan W, Hu PF, Zhao X, Lianhua CG, Batu BR (2020) Expression level of lncRNA PVT1 in serum of patients with coronary atherosclerosis disease and its clinical significance. Eur Rev Med Pharmacol Sci 24(11):6333–6337

    CAS  PubMed  Google Scholar 

  25. Jackowska P, Chałubiński M, Łuczak E, Wojdan K, Gorzelak-Pabis P, Olszewska-Banaszczyk M et al (2019) The influence of statin monotherapy and statin-ezetimibe combined therapy on FoxP3 and IL 10 mRNA expression in patients with coronary artery disease. Adv Clin Exp Med 28(9):1243–1248

    Article  PubMed  Google Scholar 

  26. Liu HT, Fang L, Cheng YX, Sun Q (2016) LncRNA PVT1 regulates prostate cancer cell growth by inducing the methylation of miR-146a. Cancer Med 5(12):3512–3519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wang Y, Lyu X, Wu X, Yu L, Hu K (2020) Long non-coding RNA PVT1, a novel biomarker for chronic obstructive pulmonary disease progression surveillance and acute exacerbation prediction potentially through interaction with microRNA-146a. J Clin Lab Anal. https://doi.org/10.1002/jcla.23346

    Article  PubMed  PubMed Central  Google Scholar 

  28. Tang H, Lai Y, Zheng J, Chen K, Jiang H, Xu G (2020) MiR-146a promotes tolerogenic properties of dendritic cells and through targeting Notch1 signaling. Immunol Invest 49(5):555–570

    Article  CAS  PubMed  Google Scholar 

  29. Gong F, Wu J, Zhou P, Zhang M, Liu J, Liu Y et al (2016) Interleukin-22 Might act as a double-edged sword in type 2 diabetes and coronary artery disease. Mediators Inflamm 2016:8254797

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We greatly appreciate all participants in the study. We also thank the assistance provided by the staff of the Al-Zahra Heart Hospital of Shiraz, Iran.

Funding

This study was funded by Fasa University of Medical Sciences, Grant No. 97093. Dr. Behnoosh Miladpour is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

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Authors and Affiliations

  1. Department of Biochemistry, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

    Peyman Nowrouzi-Sohrabi & Atefeh Seghatoleslam

  2. Research Center Traditional Medicine and History of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

    Peyman Nowrouzi-Sohrabi

  3. Professor Alborzi Clinical Microbiology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

    Atefeh Seghatoleslam

  4. Student Research Committee, Shiraz University of Medical Sciences, Shiraz, Iran

    Mehdi Kalani

  5. Department of Biochemistry, School of Medicine, Hormozgan University of Medical Sciences, Hormozgan, Iran

    Mehran Erfani

  6. Department of Clinical Biochemistry, Fasa University of Medical Sciences, Fasa, Fars, Iran

    Alireza Hosseini Abgir, Shekoufeh Hatami, Mahdi Namdar, Mohammadjavad Tahmasebi & Behnoosh Miladpour

Authors
  1. Peyman Nowrouzi-Sohrabi
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  2. Atefeh Seghatoleslam
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  9. Behnoosh Miladpour
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Correspondence to Behnoosh Miladpour.

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No potential conflicts of interest relevant to this article were reported.

Ethical approval

This study approved with the ethic code of IR.FUMS.REC.1397.144.

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All research procedures were completely explained to the participants and they signed the consent forms.

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Nowrouzi-Sohrabi, P., Seghatoleslam, A., Kalani, M. et al. Up-regulated lncRNA-PVT1 expression in peripheral blood mononuclear cells of patients with coronary artery disease is correlated with decreased interleukin-10 production. Mol Biol Rep 49, 3453–3459 (2022). https://doi.org/10.1007/s11033-022-07181-y

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  • DOI: https://doi.org/10.1007/s11033-022-07181-y

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