The correlation between micro-RNA 146a and IL-17 in the serum of Iraqi patients with cystic echinococcosis

Authors

  • Nisreen shaker Mahmoud Department of Biology, College of Science for Women, University of Baghdad, Baghdad, Iraq. https://orcid.org/0000-0002-9658-8448
  • Ekhlas M. Idan Department of Biology, College of Science for Women, University of Baghdad, Baghdad, Iraq.
  • Muhanned K Ali Department of Thoracic and Vascular Surgery, Ghazi AL-Hariri Subspecialty Surgical Hospital, Baghdad, Iraq.

DOI:

https://doi.org/10.21123/bsj.2024.9515

Keywords:

Cystic echinococcosis, cytokine, hydatid cyst, IL-17, miRNA-146a, microRNA

Abstract

Cystic echinococcosis (CE) is an endemic disease that causes serious disease and economic loss in the majority of countries around the world. MiRNAs are an epigenetic factor that is essential to the regulation of the immune response by interfering with cytokine expression; one such miRNA is microRNA-146a. The aim of the present study was to assess if we could use microRNA 146a as a biomarker for the detection of CE and to determine the relationship between microRNA 146a gene expression and IL-17 in patients with CE. The study included 50 CE patients who were admitted to the hospital in Baghdad, Iraq, for CE removal surgery and 50 healthy controls. The serum was collected from September 2022 to June 2023. The sample’s age range was 20–55 years. Rural patients were infected at a higher rate than urban patients (74.00% and 42.00%, respectively), The lung was the most affected organ (74%), followed by the liver (18%), then the liver and lung together (8%). CE patients had significantly higher miRNA-146a fold expression than control group members (4.33 ± 1.01 and 1.00 ± 0.23, respectively). The serum level of IL-17 was significantly higher in the control group, at 129.15 ± 4.73ng/L, than in patients, at 105.99 ± 5.81ng/L. According to our findings, miRNA-146a is upregulated in the sera of CE patients, which leads to the development of novel biomarkers for echinococcosis and it is associated negatively with IL-17 levels. This may interfere with their immune system's inflammatory response and contribute to the pathogenesis of CE.

References

Pakala T, Molina M, Wu GY. Hepatic Echinococcal Cysts: A Review. J Clin Transl Hepatol. 2016 Mar 28; 4(1): 39-46. https://doi.org/10.14218/JCTH.2015.00036

Zhang W, Zhang Z, Wu W, Shi B, Li J, Zhou X, et al. Epidemiology and control of echinococcosis in central Asia, with particular reference to the People's Republic of China. Acta Trop. 2015 Jan; 141(Pt B): 235-43. https://doi.org/10.1016/j.actatropica.2014.03.014

Abdul Rasool YA, AL-Taie LH, Husain HA. Serovalue of hydatid disease in Baghdad. J Fac Med Baghdad. 2012 Apr. 1; 54(1): 47-50. https://doi.org/10.32007/jfacmedbagdad.541770

Al-Kuraishi AH. Histopathological Changes of Experimental Hydatidosis in Liver and Spleen of Albino Mice: Age and Sex Effect. J Fac Med Baghdad. 2010. 51(4): 423-8. https://doi.org/10.32007/jfacmedbagdad.5141099

AL-Asadi SAM, Hansh WJ, Awad A-HH. Employing NADH Dehydrogenase Subunit 1 in the Determination of Echinococcus granulosus Strain in Sheep, Cattle and Human in Thi-Qar Province, Iraq. Baghdad Sci J. 2021 Jun. 1; 18(2): 238-246. https://doi.org/10.21123/bsj.2021.18.2.0238

Al-Tikrity IAA, Al-Janabi ZA, Al-jubory AHA. Comparative study of hydatid cysts isolated from livers of different hosts. Baghdad Sci J. 2014 Jun. 1; 11(2): 928-33. doi: https://doi.org/10.21123/bsj.2014.11.2.928-933

Edan EM, Ardalan NM. Estimation of humural immune response on the rabbits that immunizing with Hydatid cyst antigens by using IHAT and ElISA. J Fac Med Baghdad. 2009. 1; 51(3): 332-5. doi: https://doi.org/10.32007/jfacmedbagdad.5131145

AL-Shanawi FA, Baker NN, Ibrahim AQ. Study the effect of the mixture aquatic extract of Peganum harmala seeds and Pericarp of Punica granutum on viability of protoscolices of Echinococcus granulosus in vitro and in vivo. Baghdad Sci 2012 Jun. 3;9(2):200-6. https://doi.org/10.21123/bsj.2012.9.2.200-206

Budke CM, Deplazes P, Torgerson PR. Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis. 2006 Feb; 12(2): 296-303. https://doi.org/10.3201/eid1202.050499

Zhang W, Li J, McManus DP. Concepts in immunology and diagnosis of hydatid disease. Clin Microbiol Rev. 2003 Jan; 16(1): 18-36. https://doi.org/10.1128/CMR.16.1.18-36.2003

Torcal J, Navarro-Zorraquino M, Lozano R, Larrad L, Salinas JC, Ferrer J, et al. Immune response and in vivo production of cytokines in patients with liver hydatidosis. Clin Exp Immunol. 1996 Nov; 106(2): 317-22. https://doi.org/10.1046/j.1365-2249.1996.d01-843.x

Siracusano A, Margutti P, Delunardo F, Profumo E, Riganò R, Buttari B, et al. Molecular cross-talk in host-parasite relationships: the intriguing immunomodulatory role of Echinococcus antigen B in cystic echinococcosis. Int J Parasitol. 2008 Oct; 38(12): 1371-6. https://doi.org/10.1016/j.ijpara.2008.06.003

Chandrasekhar S, Parija SC. Serum antibody & Th2 cytokine profiles in patients with cystic echinococcosis. Indian J Med Res. 2009 Dec; 130(6): 731-5.

Van der Zande HJP, Zawistowska-Deniziak A, Guigas B. Immune regulation of metabolic homeostasis by helminths and their molecules. Trends Parasitol. 2019; 35: 795–808. https://doi.org/10.1016/j.pt.2019.07.014

Baz A, Ettlin GM, Dematteis S. Complexity and function of cytokine responses in experimental infection by Echinococcus granulosus. Immunobiology. 2006; 211: 3–9. https://doi.org/10.1016/j.imbio.2005.09.001

Siracusano A, Delunardo F, Teggi A, Ortona E. Cystic echinococcosis: aspects of immune response, immunopathogenesis and immune evasion from the human host. Endocr Metab Immune Disord Drug Targets. 2012 Mar; 12(1): 16-23. https://doi.org/10.2174/187153012799279117 PMID: 22214328.

Hammond SM. An overview of microRNAs. Adv Drug Deliv Rev. 2015 Jun 29; 87: 3-14. https://doi.org/10.1016/j.addr.2015.05.001

He Z, Yan T, Yuan Y, Yang D, Yang G. miRNAs and lncRNAs in Echinococcus and Echinococcosis. Int J Mol Sci. 2020 Jan 22; 21(3): 730. https://doi.org/10.3390/ijms21030730

Al-Mashhadani MS, Mahood WS, Al-Abassi HM. Measuring The Level of MIR-148A in Iraqi Women Diagnosed with Breast Cancer. Pak J Med Health Sci. 2022; 16(6): 560-563. https://doi.org/10.53350/pjmhs22166560

Perry MM, Moschos SA, Williams AE, Shepherd NJ, Larner-Svensson HM, Lindsay MA. Rapid changes in microRNA-146a expression negatively regulate the IL-1beta-induced inflammatory response in human lung alveolar epithelial cells. J Immunol. 2008 Apr 15; 180(8): 5689-98. https://doi.org/10.4049/jimmunol.180.8.5689

Zhao JL, Rao DS, Boldin MP, Taganov KD, O'Connell RM, Baltimore D. NF-kappaB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc Natl Acad Sci U S A. 2011 May 31; 108(22): 9184-9. https://doi.org/10.1073/pnas.1105398108

Chiricozzi A, Guttman-Yassky E, Suárez-Fariñas M, Nograles KE, Tian S, Cardinale I, et al. Integrative responses to IL-17 and TNF-α in human keratinocytes account for key inflammatory pathogenic circuits in psoriasis. J Invest Dermatol. 2011 Mar; 131(3): 677-87. https://doi.org/10.1038/jid.2010.340

Mariconti M, Vola A, Manciulli T, Genco F, Lissandrin R, Meroni V, et al. Role of microRNAs in host defense against Echinococcus granulosus infection: a preliminary assessment. Immunol Res. 2019 Feb;67(1):93-97. https://doi.org/10.1007/s12026-018-9041-4

Wang WM, Liu JC. Effect and molecular mechanism of mir-146a on proliferation of lung cancer cells by targeting and regulating MIF gene. Asian Pac J Trop Med. 2016 Aug; 9(8): 806-11. https://doi.org/10.1016/j.apjtm.2016.06.001

Su S, Zhao Q, Dan L, Lin Y, Li X, Zhang Y, et al .Inhibition of miR-146a-5p and miR-8114 in Insulin-Secreting Cells Contributes to the Protection of Melatonin against Stearic Acid-Induced Cellular Senescence by Targeting Mafa. Endocrinol Metab (Seoul). 2022; 37(6): 901-917. https://doi.org/10.3803/EnM.2022.1565

Tavakolian S, Goudarzi H, Faghihloo E. Evaluating the expression level of miR-9-5p and miR-192-5p in gastrointestinal cancer: introducing novel screening biomarkers for patients. BMC Res Notes. 2020 Apr 19; 13(1): 226. https://doi.org/10.1186/s13104-020-05071-9

Mousavi SM, Afgar A, Mohammadi MA, Mortezaei S, Faridi A, Sadeghi B, et al. Biological and morphological consequences of dsRNA-induced suppression of tetraspanin mRNA in developmental stages of Echinococcus granulosus. Parasit Vectors. 2020 Apr 10; 13(1): 190. https://doi.org/10.1186/s13071-020-04052-y

Wang N, Zhu H, Zhan J, Guo C, Shen N, Gu X, et al. Cloning, expression, characterization, and immunological properties of citrate synthase from Echinococcus granulosus. Parasitol Res. 2019 Jun; 118(6): 1811-1820. https://doi.org/10.1007/s00436-019-06334-6

Dorosti Z, Tolouei S, Khanahmad H, Jafari R, Jafaee F, Sharafi SM, et al. IL-4 gene expression in adventitial layer (fibrous layer) of hepatic ovine and bovine hydatid cysts. J Parasit Dis. 2016 Sep; 40(3): 855-9. https://doi.org/10.1007/s12639-014-0593-5

Siracusano A, Delunardo F, Teggi A, Ortona E. Host-parasite relationship in cystic echinococcosis: an evolving story. Clin Dev Immunol. 2012; 2012: 639362. https://doi.org/10.1155/2012/639362

Ahmed ZA, Idan EM, Ardalan NM. Role of IL-37 and Dectin-1 during Toxoplasmosis. Baghdad Sci J. 2023; 20(3): 0746. https://doi.org/10.21123/bsj.2022.7618

Bi, Y., Liu, G. and Yang, R., 2009. MicroRNAs: novel regulators during the immune response. J Cell Physiol. 2009. 218(3): 467-72. https://doi.org/10.1002/jcp.21639 . PMID: 19034913.

Al-Heety RA, Al-Hadithi HS. Association of Circulating MicroRNA-142-3p with Graves Disease. Baghdad Sci.J. 2021 Dec. 1; 18(4): 1133. https://doi.org/10.21123/bsj.2021.18.4.1133

Mahami-Oskouei M, Norouzi B, Ahmadpour E, Kazemi T, Spotin A, Alizadeh Z, et al. Expression analysis of circulating miR-146a and miR-155 as novel biomarkers related to effective immune responses in human cystic echinococcosis. Microb Pathog. 2021 Aug; 157: 104962. https://doi.org/10.1016/j.micpath.2021.104962

Guo X, Zheng Y. Expression profiling of circulating miRNAs in mouse serum in response to Echinococcus multilocularis infection. Parasitology. 2017 Jul; 144(8): 1079-1087. https://doi.org/10.1017/S0031182017000300

Pan W, Hao WT, Shen YJ, Li XY, Wang YJ, Sun FF, et al. The excretory-secretory products of Echinococcus granulosus protoscoleces directly regulate the differentiation of B10, B17 and Th17 cells. Parasit Vectors. 2017 Jul 21; 10(1): 348. https://doi.org/10.1186/s13071-017-2263-9

Zhao S, Cheng Y, Kim JG. microRNA-146a downregulates IL-17 and IL-35 and inhibits proliferation of human periodontal ligament stem cells. J Cell Biochem. 2019 Aug; 120(8): 13861-13866. https://doi.org/10.1002/jcb.28659

Hong Y, Fu Z, Cao X, Lin J. Changes in microRNA expression in response to Schistosoma japonicum infection. Parasite Immunol. 2017 Feb; 39(2). https://doi.org/10.1111/pim.12416

Okoye IS, Czieso S, Ktistaki E, Roderick K, Coomes SM, Pelly VS, et al. Transcriptomics identified a critical role for Th2 cell-intrinsic miR-155 in mediating allergy and antihelminth immunity. Proc Natl Acad Sci U S A. 2014 Jul 29; 111(30): E3081-90. https://doi.org/10.1073/pnas.1406322111

van Loon W, Gai PP, Hamann L, Bedu-Addo G, Mockenhaupt FP. MiRNA-146a polymorphism increases the odds of malaria in pregnancy. Malar J. 2019 Jan 14; 18(1): 7. https://doi.org/10.1186/s12936-019-2643-z

Boldin MP, Taganov KD, Rao DS, Yang L, Zhao JL, Kalwani M, et al. miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J Exp Med. 2011 Jun 6; 208(6): 1189-201. https://doi.org/10.1084/jem.20101823 . Epub 2011 May 9.

Zhao JL, Rao DS, Boldin MP, Taganov KD, O'Connell RM, Baltimore D. NF-kappaB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc Natl Acad Sci U S A. 2011 May 31; 108(22): 9184-9. https://doi.org/10.1073/pnas.1105398108

Tan W, Liao Y, Qiu Y, Liu H, Tan D, Wu T, et al. miRNA 146a promotes chemotherapy resistance in lung cancer cells by targeting DNA damage inducible transcript 3 (CHOP). Cancer Lett. 2018 Aug 1; 428: 55-68. https://doi.org/10.1016/j.canlet.2018.04.028

Li D, Duan M, Feng Y, Geng L, Li X, Zhang W. MiR-146a modulates macrophage polarization in systemic juvenile idiopathic arthritis by targeting INHBA. Mol Immunol. 2016 Sep; 77: 205-12. https://doi.org/10.1016/j.molimm.2016.08.007

Wu ZW, Liu YF, Wang S, Li B. miRNA-146a induces vascular smooth muscle cell apoptosis in a rat model of coronary heart disease via NF-κB pathway. Genet Mol Res. 2015 Dec 29; 14(4): 18703-12. https://doi.org/10.4238/2015.December.28.19

Zhang B, Wang LL, Ren RJ, Dammer EB, Zhang YF, Huang Y, Chen SD, Wang G, et al. MicroRNA-146a represses LRP2 translation and leads to cell apoptosis in Alzheimer's disease. FEBS Lett. 2016 Jul; 590(14): 2190-200. https://doi.org/10.1002/1873-3468.12229

Mao H, Xu G. Protective effect and mechanism of microRNA-146a on ankle fracture. Exp Ther Med. 2020 Nov; 20(5): 3. https://doi.org/10.3892/etm.2020.9131

Downloads

Issue

Section

article

How to Cite

1.
The correlation between micro-RNA 146a and IL-17 in the serum of Iraqi patients with cystic echinococcosis. Baghdad Sci.J [Internet]. [cited 2024 Dec. 30];22(2). Available from: https://bsj.uobaghdad.edu.iq/index.php/BSJ/article/view/9515