Analysis of the IL-10 mRNA level in the peripheral blood of patients with cancer and benign prostatic hyperplasia
https://doi.org/10.17650/1726-9784-2023-22-4-35-42
Abstract
Background. Interleukin-10 (IL-10) is a pleiotropic cytokine with immunomodulatory properties and may inhibit tumor development and progression or stimulate tumor growth.
Aim. Analysis of the changes of the IL-10 mRNA level in the peripheral blood (PB) of patients with prostate cancer (PC) and benign prostatic hyperplasia (BPH) in comparison with clinical and laboratory data.
Materials and methods. 63 patients with histologically confirmed PC and 52 patients with histologically confirmed BPH were under observation. The control group consisted of 30 practically healthy persons comparable in age. Determination of the relative level of IL-10 mRNA in PB samples was performed by real-time reverse transcription polymerase chain reaction.
Results. Both in patients with PC and in patients with BPH, a statistically significant decrease in the level of IL-10 mRNA in the PB of patients was observed in comparison with the control. In PC, the lowest levels were found in patients with a prostate-specific antigen (PSA) concentration above 10 ng / l and with a prostate volume of more than 50 cm3. Differences in the level of IL-10 mRNA at T2 and T3 stages and at different testosterone concentrations were not statistically significant, although there was a pronounced downward trend in prognostically unfavorable cases. Patients with BPH had a relative level of IL-10 mRNA, which was statistically significantly higher than in patients with PC. At PSA concentrations above 10 ng / mL, the level of IL-10 mRNA was also lower than at its lower concentrations.
Conclusion. In patients with cancer and BPH, a reduced level of IL-10 mRNA was found in the PB. The decrease is more pronounced in the unfavorable course of diseases and, apparently, is a consequence of the instability of IL-10 mRNA at the post-transcriptional level.
About the Authors
O. A. KorovinRussian Federation
54 Lenin Ave., Nizhny Novgorod 603032
10 / 1 Minin and Pozharsky pl., Nizhny Novgorod 603005
A. V. Alyasova
Russian Federation
10 / 1 Minin and Pozharsky pl., Nizhny Novgorod 603005
Kh. M. Arioua
Russian Federation
23 Gagarin Ave., Nizhny Novgorod 603022
D. V. Novikov
Russian Federation
71 Malaya Yamskaya St., Nizhny Novgorod 603950
N. V. Krasnogorova
Russian Federation
54 Lenin Ave., Nizhny Novgorod 603032
23 Gagarin Ave., Nizhny Novgorod 603022
V. V. Novikov
Russian Federation
23 Gagarin Ave., Nizhny Novgorod 603022
71 Malaya Yamskaya St., Nizhny Novgorod 603950
References
1. Mannino H., Ziwen Z., Xiao H. et al. The paradoxical role of IL-10 in immunity and cancer. Cancer Letters 2015;367(2):103–7. DOI: 10.1016/j.canlet.2015.07.009
2. Xuan L., Zhang N., Wang X. et al. IL-10 family cytokines in chronic rhinosinusitis with nasal polyps: From experiments to the clinic. Front Immunol 2022;13:947983. DOI: 10.3389/fimmu.2022.947983
3. Rasquinha M.T., Sur M., Lasrado N. et al. IL-10 as a Th2 cytokine: differences between mice and humans. J Immunol 2021;207(9):2205–15. DOI: 10.4049/jimmunol.2100565
4. Al-Nasralla A.S.H., Hussian S.S., Tektook N.K. Immunological analysis of Interleukin-10 (IL-10), tumor necrosis factor-a (TNF-a), and Prostate-specific antigen (PSA) in benign and malignant prostate cancer. Hum Antibodies 2023. DOI: 10.3233/HAB-220018
5. Palano M.T., Gallazzi M., Cucchiara M. et al. The tumor innate immune microenvironment in prostate cancer: an overview of soluble factors and cellular effectors. Explor Target Antitumor Ther 2022;3(5):694–718. DOI: 10.37349/etat.2022.00108
6. Katongole P., Sande O.J., Nabweyambo S. et al. IL-6 and IL-8 cytokines are associated with elevated prostate-specific antigen levels among patients with adenocarcinoma of the prostate at the Uganda Cancer Institute. Future Oncol 2022;18(6):661–7. DOI: 10.2217/fon-2021-0683
7. Garrido M.M., Ribeiro R.M., Krüger K. et al. Are proinflam ma- tory cytokines relevant for the diagnosis of prostate cancer? Anti- cancer Res 2021:41(6):3067–73. DOI: 10.21873/anticanres.15090
8. Roya N., Fatemeh T., Faramarz M.-A. et al. Frequency of IL-10+CD19+ B cells in patients with prostate cancer compared to patients with benign prostatic hyperplasia. Afr Health Sci 2020;20(3):1264–72. DOI: 10.4314/ahs.v20i3.31
9. Novikov D.V., Krasnogorova N.V., Gorshkova E.N. et al. Serum protein corona abolishes changes in the expression of proinflammatory genes induced by quantum dots in human blood mononuclear cell. Bull Exp Biol Med 2020;169(1):95–9. DOI: 10.1007/s10517-020-04832-7
10. Adeola F. Normalization of gene expression by quantitative RT-PCR in human cell line: Comparison of 12 endogenous reference genes. Ethiop J Health Sci 2018;28(6):741–8. DOI: 10.4314/ejhs.v28i6.9
11. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 2001;25(4):402–8. DOI: 10.1006/meth.2001.1262
12. Brown C.Y., Lagnado C.A., Vadas M.A. et al. Differential regulation of the stability of cytokine mRNAs in lipopolysaccharide-activated blood monocytes in response to interleukin-10. J Biol Chem 1996;271(33):20108–12. DOI: 10.1074/jbc.271.33.20108
13. Zhu Z.-Y., Liu J.-B., Liu X., Qian L.-X. Association of interleukin 10 rs1800896 polymorphism with susceptibility to breast cancer: a meta-analysis. J Int Med Res 2020;48(4):0300 060520904863. DOI: 10.1177/0300060520904863
14. Yadav U., Kumar P., Rai V. Interleukin-10 (IL-10) gene polymorphisms and prostate cancer susceptibility: Evidence from a meta-analysis. Gene Reports 2021;25:101377. DOI: 10.1101/2020.11.09.20228825
15. Elyseeva I.A., Kim E.R., Gurianov S.G. et al. Y-box-binding pro- tein 1 (YB-1) and its functions. Uspekhi biologicheskoy khimii = Advances in biological chemistry 2011;51:65–132. (In Russ.)
16. Powell M.J., Thompson S.A., Tone Y. et al. Posttranscriptional regulation of IL-10 gene expression through sequences in the 3’-untranslated region. J Immunol 2000;165(1):292–6. DOI: 10.4049/jimmunol.165.1.292
17. Sharma A., Kumar M., Aich J. et al. Posttranscriptional regulation of interleukin-10 expression by hsa-miR-106a. Proc Natl AcadSci USA 2009;106(14):5761–6. DOI: 10.1073/pnas.0808743106
18. Huang Q.-R., Pan X.B. Prognostic lncRNAs, miRNAs, and mRNAs form a competing endogenous RNA network in colon cancer. Front Oncol 2019;9:712. DOI: 10.3389/fonc.2019.00712
19. Sullivan K.M., Jiang X., Guha P. et al. Blockade of interleukin 10 potentiates antitumour immune function in human colorectal cancer liver metastases. Gut 2023;72(2):325–37. DOI: 10.1136/gutjnl-2021-325808
20. Townsend M.H., Felsted A.M., Piccolo S.R. et al. Metastatic colon adenocarcinoma has a significantly elevated expression of IL-10 compared with primary colon adenocarcinoma tumors. Cancer Biol Ther 2018;19(10):913–20. DOI: 10.1080/15384047.2017.1360453
21. Borowczak J., Szczerbowski K., Maniewski M. et al. The role of inflammatory cytokines in the pathogenesis of colorectal carcinoma-recent findings and review. Biomedicines 2022;10(7):1670. DOI: 10.3390/biomedicines10071670
22. Li Y., Yu H., Jiao S., Yang J. Prognostic value of IL-10 expression in tumor tissues of breast cancer patients. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 2014;30:517–20. (In Chinese) PMID: 24796749
23. Zhou L., Tang C., Li X. et al. IL-6/IL-10 mRNA expression ratio in tumor tissues predicts prognosis in gastric cancer patients without distant metastasis. Sci Rep 2022;12:19427. DOI: 10.1038/s41598-022-24189-3
24. Abtahi S., Davani F., Mojtahedi Z. et al. Dual association of serum interleukin-10 levels with colorectal cancer. J Cancer Res Ther 2017;13(2):252–6. DOI: 10.4103/0973-1482.199448
25. Krause P., Morris V., Greenbaum J.A. et al. IL-10-producing intestinal macrophages prevent excessive antibacterial innate immunity by limiting IL-23. Synthesis Nat Commun 2015;6:7055. DOI: 10.1038/ncomms8055
26. Thomas C.E., Bauer D.C., Yuan J.-M. et al. Circulating IL-10 is associated with reduced risk of prostate cancer in a prospective cohort of elderly men: the MrOS Study. Cancer Causes Control 2023;34(1):59–68. DOI: 10.1007/s10552-022-01639-x
Review
For citations:
Korovin O.A., Alyasova A.V., Arioua Kh.M., Novikov D.V., Krasnogorova N.V., Novikov V.V. Analysis of the IL-10 mRNA level in the peripheral blood of patients with cancer and benign prostatic hyperplasia. Russian Journal of Biotherapy. 2023;22(4):35-42. (In Russ.) https://doi.org/10.17650/1726-9784-2023-22-4-35-42