MicroRNA-181b stimulates inflammation via the nuclear factor-κB signaling pathway in vitro

Wang,Yazhen; Mao,Genxiang; Lv,Yuandong; Huang,Qingdong; Wang,Guofu

doi:10.3892/etm.2015.2702

MicroRNA-181b stimulates inflammation via the nuclear factor-κB signaling pathway in vitro

Authors:
- Yazhen Wang
- Genxiang Mao
- Yuandong Lv
- Qingdong Huang
- Guofu Wang
View Affiliations

Affiliations: Zhejiang Provincial Key Laboratory of Geriatrics and Geriatrics Institute of Zhejiang, Zhejiang Hospital, Hangzhou, Zhejiang 310013, P.R. China
Published online on: August 24, 2015 https://doi.org/10.3892/etm.2015.2702
Pages: 1584-1590

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Acute lung injury (ALI) is characterized by severe lung edema and an increase in the inflammatory reaction. Considerable evidence has indicated that microRNAs (miRNAs or miRs) are involved in various human diseases; however, the expression profile and function of miRNAs in ALI have been rarely reported. The present study used miRNA microarray and reverse transcription‑quantitative polymerase chain reaction to demonstrate that miR‑181b is the one of the most significantly upregulated miRNA after lipopolysaccharide (LPS) stimulation in human bronchial epithelial cells, BEAS‑2B. To elaborate the role of miR‑181b in ALI, an assay was performed to investigate the overexpression of miR‑181b in BEAS‑2B cells, and the expression of inflammatory factors was then analyzed. The overexpression of miR‑181b resulted in the induction of an increment in interleukin (IL)‑6 levels. p65 was identified to be a primary component of NF‑κB, since it was upregulated in the miR‑181b overexpression in the BEAS‑2B cells, while pyrrolidine dithiocarbamate, a specific inhibitor of NF‑κB, was found to be able to abrogate the upregulation of the expression of p65. In conclusion, the findings of the present study suggested that miR‑181b may be involved in the process of LPS‑induced inflammation in BEAS‑2B cells by activating the NF‑κB signaling pathway, which implies that it may serve as a potential therapeutic target for ALI.

View Figures

View References

1	Avecillas JF, Freire AX and Arroliga AC: Clinical epidemiology of acute lung injury and acute respiratory distress syndrome: Incidence, diagnosis and outcomes. Clin Chest Med. 27:549–557. 2006. View Article : Google Scholar : PubMed/NCBI
2	Ware LB and Matthay MA: The acute respiratory distress syndrome. N Engl J Med. 342:1334–1349. 2000. View Article : Google Scholar : PubMed/NCBI
3	Crosby LM and Waters CM: Epithelial repair mechanisms in the lung. Am J Physiol Lung Cell Mol Physiol. 298:L715–L731. 2010. View Article : Google Scholar : PubMed/NCBI
4	Papi A and Johnston SL: Rhinovirus infection induces expression of its own receptor intercellular adhesion molecule 1 (ICAM-1) via increased NF-kappaB-mediated transcription. J Biol Chem. 274:9707–9720. 1999. View Article : Google Scholar : PubMed/NCBI
5	Hoare GS, Chester AH, Yacoub MH and Marczin N: Regulation of NF-kappaB and ICAM-1 expression in human airway epithelial cells. Int J Mol Med. 9:35–44. 2002.PubMed/NCBI
6	Li Z, Zhang de K, Yi WQ, Ouyang Q, Chen YQ and Gan HT: NF-kappaB p65 antisense oligonucleotides may serve as a novel molecular approach for the treatment of patients with ulcerative colitis. Arch Med Res. 39:729–734. 2008. View Article : Google Scholar : PubMed/NCBI
7	Bartel DP: MicroRNAs: Target recognition and regulatory functions. Cell. 136:215–233. 2009. View Article : Google Scholar : PubMed/NCBI
8	Guo H, Ingolia NT, Weissman JS and Bartel DP: Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 466:835–840. 2010. View Article : Google Scholar : PubMed/NCBI
9	Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI
10	Latronico MV and Condorelli G: MicroRNAs and cardiac pathology. Nat Rev Cardiol. 6:419–429. 2009. View Article : Google Scholar : PubMed/NCBI
11	Port JD and Sucharov C: Role of microRNAs in cardiovascular disease: Therapeutic challenges and potentials. J Cardiovasc Pharmacol. 56:444–453. 2010. View Article : Google Scholar : PubMed/NCBI
12	Buechner J, Henriksen JR, Haug BH, Tømte E, Flaegstad T and Einvik C: Inhibition of mir-21, which is upregulated during MYCN knockdown-mediated differentiation, does not prevent differentiation of neuroblastoma cells. Differentiation. 81:25–34. 2011. View Article : Google Scholar : PubMed/NCBI
13	Li X, Zhang Y, Shi Y, Dong G, Liang J, Han Y, Wang X, Zhao Q, Ding J, Wu K, et al: MicroRNA-107, an oncogene microRNA that regulates tumour invasion and metastasis by targeting DICER1 in gastric cancer. J Cell Mol Med. 15:1887–1895. 2011. View Article : Google Scholar : PubMed/NCBI
14	O'Connell RM, Rao DS, Chaudhuri AA and Baltimore D: Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol. 10:111–122. 2010. View Article : Google Scholar : PubMed/NCBI
15	Oglesby IK, McElvaney NG and Greene CM: MicroRNAs in inflammatory lung disease-master regulators or target practice? Respir Res. 11:1482010. View Article : Google Scholar : PubMed/NCBI
16	Roggli E, Britan A, Gattesco S, Lin-Marq N, Abderrahmani A, Meda P and Regazzi R: Involvement of microRNAs in the cytotoxic effects exerted by proinflammatory cytokines on pancreatic beta-cells. Diabetes. 59:978–986. 2010. View Article : Google Scholar : PubMed/NCBI
17	Angulo M, Lecuona E and Sznajder JI: Role of MicroRNAs in lung disease. Arch Bronconeumol. 48:325–330. 2012.(In English, Spanish). View Article : Google Scholar : PubMed/NCBI
18	Cai ZG, Zhang SM, Zhang Y, Zhou YY, Wu HB and Xu XP: MicroRNAs are dynamically regulated and play an important role in LPS-induced lung injury. Can J Physiol Pharmacol. 90:37–43. 2012. View Article : Google Scholar : PubMed/NCBI
19	Xie T, Liang J, Liu N, Wang Q, Li Y, Noble PW and Jiang D: MicroRNA-127 inhibits lung inflammation by targeting IgG Fcγ receptor I. J Immunol. 188:2437–2444. 2012. View Article : Google Scholar : PubMed/NCBI
20	Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML and Struhl K: STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell. 39:493–506. 2010. View Article : Google Scholar : PubMed/NCBI
21	Wang YZ, Mao GX, Lv YD, Huang QD and Wang GF: MicroRNA-181b stimulates inflammation via the NF-kappa B signaling pathway in vitro. J Am Geriatr Soc. 62:S394. 2014.
22	Schulz C, Farkas L, Wolf K, Kratzel K, Eissner G and Pfeifer M: Differences in LPS-induced activation of bronchial epithelial cells (BEAS-2B) and type II-like pneumocytes (A-549). Scand J Immunol. 56:294–302. 2002. View Article : Google Scholar : PubMed/NCBI
23	Pencheva N, Tran H, Buss C, Huh D, Dorbnjak M, Busam K and Tavazoie SF: Concergent multi-miRNA targeting of ApoE drives LRP1/LRP8-dependent melanoma metastasis and angiogenesis. Cell. 151:1068–1082. 2012. View Article : Google Scholar : PubMed/NCBI
24	Ma Y, Zhang P, Wang F, Zhang H, Yang J, Peng J, Liu W and Qin H: miR-150 as a potential biomarker associated with prognosis and therapeutic outcome in colorectal cancer. Gut. 61:1447–1453. 2012. View Article : Google Scholar : PubMed/NCBI
25	Elder ACP, Gelein R, Finkelstein JN, Cox C and Oberdorster G: Endotoxin priming affects the lung response to ultrafine particles and ozone in young and old rats. Inhalation Toxicology. 12:(Suppl 1). 85–98. 2000. View Article : Google Scholar
26	Meduri GU, Headley S, Kohler G, Stentz F, Tolley E, Umberger R and Leeper K: Persistent elevation of inflammatory cytokines predicts a poor outcome in ARDS. Plasma IL-1 beta and IL-6 levels are consistent and efficient predictors of outcome over time. Chest. 107:1062–1073. 1995. View Article : Google Scholar : PubMed/NCBI
27	Dave RS and Khalili K: Morphine treatment of human monocyte-derived macrophages induces differential miRNA and protein expression: Impact on inflammation and oxidative stress in the central nervous system. J Cell Biochem. 110:834–845. 2010. View Article : Google Scholar : PubMed/NCBI
28	Ma X, Becker Buscaglia LE, Barker JR and Li Y: MicroRNAs in NF-kappaB signaling. J Mol Cell Biol. 3:159–166. 2011. View Article : Google Scholar : PubMed/NCBI
29	Nelson S and Martin TR: Cytokines in Pulmonary Disease: Infection and Inflammation (Lung Biology in Health and Disease). Martin T: 141:(1st). Marcel Dekker. (New York, NY). 2000.PubMed/NCBI
30	Pedersen I and David M: MicroRNAs in the immune response. Cytokine. 43:391–394. 2008. View Article : Google Scholar : PubMed/NCBI
31	Sun X, Icli B, Wara AK, Belkin N, He S, Kobzik L, Hunninghake GM, Vera MP, MICU Registry, Blackwell TS, et al: MicroRNA-181b regulates NF-κB-mediated vascular inflammation. J Clin Invest. 122:1973–1990. 2012.PubMed/NCBI
32	Koyama S, Sato E, Nomura H, Kubo K, Miura M, Yamashita T, Nagai S and Izumi T: The potential of various lipopolysaccharides to release monocyte chemotactic activity from lung epithelial cells and fibroblasts. Eur Respir J. 14:545–552. 1999. View Article : Google Scholar : PubMed/NCBI
33	Reddel RR, Ke Y, Gerwin BI, McMenamin MG, Lechner JF, Su RT, Brash DE, Park JB, Rhim JS and Harris CC: Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Res. 48:1904–1909. 1988.PubMed/NCBI
34	Boots AW, Gerloff K, Bartholomé R, van Berlo D, Ledermann K, Haenen GR, Bast A, van Schooten FJ, Albrecht C and Schins RP: Neutrophils augment LPS-mediated pro-inflammatory signaling in human lung epithelial cells. Biochim Biophys Acta. 1823:1151–1162. 2012. View Article : Google Scholar : PubMed/NCBI
35	Yeh CH, Cho W, So EC, Chu CC, Lin MC, Wang JJ and Hsing CH: Propofol inhibits lipopolysaccharide-induced lung epithelial cell injury by reducing hypoxia-inducible factor-1alpha expression. Br J Anaesth. 106:590–599. 2011. View Article : Google Scholar : PubMed/NCBI
36	Fortis S, Spieth PM, Lu WY, Parotto M, Haitsma JJ, Slutsky AS, Zhong N, Mazer CD and Zhang H: Effects of anesthetic regimes on inflammatory responses in a rat model of acute lung injury. Intensive Care Med. 38:1548–1555. 2012. View Article : Google Scholar : PubMed/NCBI
37	Mittal N and Sanyal SN: In vivo effect of surfactant on inflammatory cytokines during endotoxin-induced lung injury in rodents. J Immunotoxicol. 8:274–283. 2011. View Article : Google Scholar : PubMed/NCBI
38	Cheng DS, Han W, Chen SM, Sherrill TP, Chont M, Park GY, Sheller JR, Polosukhin VV, Christman JW, Yull FE, et al: Airway epithelium controls lung inflammation and injury through the NF-kappa B pathway. J Immunol. 178:6504–6513. 2007. View Article : Google Scholar : PubMed/NCBI
39	Tang PS, Mura M, Seth R and Liu M: Acute lung injury and cell death: How many ways can cells die? Am J Physiol Lung Cell Mol Physiol. 294:L632–L641. 2008. View Article : Google Scholar : PubMed/NCBI
40	Veranth JM, Reilly CA, Veranth MM, Moss TA, Langelier CR, Lanza DL and Yost GS: Inflammatory cytokines and cell death in BEAS-2B lung cells treated with soil dust, lipopolysaccharide and surface-modified particles. Toxicol Sci. 82:88–96. 2004. View Article : Google Scholar : PubMed/NCBI
41	Stern JB, Jaffré S, Dehoux M and Crestani B: Keratinocyte growth factor and Hepatocyte growth factor: Their roles in alveolar epithelial repair. Rev Mal Respir. 20:896–903. 2003.PubMed/NCBI
42	Hoke TS, Douglas IS, Klein CL, He Z, Fang W, Thurman JM, Tao Y, Dursun B, Voelkel NF, Edelstein CL, et al: Acute renal failure after bilateral nephrectomy is associated with cytokine-mediated pulmonary injury. J Am Soc Nephrol. 18:155–164. 2007. View Article : Google Scholar : PubMed/NCBI
43	Hayden MS and Ghosh S: Shared principles in NF-kappaB signaling. 132:344–362. 2008.
44	Kawai M, Nishikomori R, Jung EY, Tai G, Yamanaka C, Mayumi M and Heike T: Pyrrolidine dithiocarbamate inhibits intercellular adhesion molecule-1 biosynthesis induced by cytokines in human fibroblasts. J Immunol. 154:2333–2341. 1995.PubMed/NCBI
45	Schreck R, Meier B, Männel DN, Dröge W and Baeuerle PA: Dithiocarbamates as potent inhibitors of nuclear factor kappa B activation in intact cells. J Exp Med. 175:1181–1194. 1992. View Article : Google Scholar : PubMed/NCBI
46	Zhang M, Zhou SH, Li XP, Shen XQ, Fang ZF, Liu QM, Qiu SF and Zhao SP: Atorvastatin downregulates BMP-2 expression induced by oxidized low-density lipoprotein in human umbilical vein endothelial cells. Circ J. 72:807–812. 2008. View Article : Google Scholar : PubMed/NCBI
47	Griffiths-Jones S: The microRNA Registry. Nucleic Acids Res. 32:D109–D111. 2004. View Article : Google Scholar : PubMed/NCBI
48	Fang Y, Shi C, Manduchi E, Civelek M and Davies PF: MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc Natl Acad Sci USA. 107:13450–13455. 2010. View Article : Google Scholar : PubMed/NCBI
49	Suárez Y, Wang C, Manes TD and Pober JS: Cutting edge: TNF-induced microRNAs regulate TNF-induced expression of E-selectin and intercellular adhesion molecule-1 on human endothelial cells: Feedback control of inflammation. J Immunol. 184:21–25. 2010. View Article : Google Scholar : PubMed/NCBI
50	Pugin J, Ricou B, Steinberg KP, Suter PM and Martin TR: Proinflammatory activity in bronchoalveolar lavage fluids from patients with ARDS, a prominent role for interleukin-1. Am J Respir Crit Care Med. 153:1850–1856. 1996. View Article : Google Scholar : PubMed/NCBI