Lipoteichoic acid upregulates NF-κB and proinflammatory cytokines by modulating β-catenin in bronchial epithelial cells

Jang,Jaewoong; Kim,Wonyong; Kim,Kijeong; Chung,Sang-In; Shim,Yae  Jie; Kim,Seok-Min; Yoon,Yoosik

doi:10.3892/mmr.2015.3965

Lipoteichoic acid upregulates NF-κB and proinflammatory cytokines by modulating β-catenin in bronchial epithelial cells

Authors:
- Jaewoong Jang
- Wonyong Kim
- Kijeong Kim
- Sang-In Chung
- Yae Jie Shim
- Seok-Min Kim
- Yoosik Yoon
View Affiliations

Affiliations: Department of Microbiology, Chung-Ang University College of Medicine, Seoul 156-756, Republic of Korea, College of General Studies, Sangmyung University, Seoul 110-743, Republic of Korea, School of Mechanical Engineering, Chung-Ang University, Seoul 156-756, Republic of Korea
Published online on: June 19, 2015 https://doi.org/10.3892/mmr.2015.3965
Pages: 4720-4726

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

Lipoteichoic acid (LTA) is a major cell wall component and virulence factor of gram-positive bacteria. The present study investigated the LTA‑induced inflammatory response of BEAS‑2B human bronchial epithelial cells, and detected the expression levels of proinflammatory cytokines interleukin (IL)‑6, IL‑8, IL‑1β, tumour necrosis factor‑α and monocyte chemotactic protein‑1, the upregulation of NF‑κB, and the phosphorylation and degradation of I‑κB. During the LTA‑induced inflammatory response of the BEAS‑2B human bronchial epithelial cells, the activity levels of the β‑catenin‑dependent promoter, and the protein expression levels of β‑catenin were significantly upregulated, whereas β‑catenin phosphorylation and the expression levels of AXIN were significantly downregulated. Following knockdown of β‑catenin by small interfering (si)RNA transfection, both the LTA-induced protein expression levels of NF‑κB and the LTA-induced activity levels of the NF‑κB‑dependent promoter were significantly reduced. Similarly, a marked reduction in I‑κB phosphorylation and degradation was observed following β‑catenin knockdown. The expression levels of the LTA‑induced proinflammatory cytokines were also significantly reduced following β‑catenin siRNA. These results suggest that β‑catenin has a significant role in the regulation of NF‑κB activity and proinflammatory cytokine expression during the LTA-induced inflammatory response of bronchial epithelial cells.

View Figures

View References

1	Schneewind O and Missiakas D: Lipoteichoic acids, phosphate-containing polymers in the envelope of gram-positive bacteria. J Bacteriol. 196:1133–1142. 2014. View Article : Google Scholar : PubMed/NCBI
2	Ginsburg I: Role of lipoteichoic acid in infection and inflammation. Lancet Infect Dis. 2:171–179. 2002. View Article : Google Scholar : PubMed/NCBI
3	Opal SM and Cohen J: Clinical gram-positive sepsis: Does it fundamentally differ from gram-negative bacterial sepsis? Crit Care Med. 27:1608–1616. 1999. View Article : Google Scholar : PubMed/NCBI
4	Sriskandan S and Cohen J: Gram-positive sepsis. Mechanisms and differences from gram-negative sepsis. Infect Dis Clin North Am. 13:397–412. 1999. View Article : Google Scholar : PubMed/NCBI
5	Schmeck B, Huber S, Moog K, Zahlten J, Hocke AC, Opitz B, Hammerschmidt S, Mitchell TJ, Kracht M, Rosseau S, et al: Pneumococci induced TLR- and Rac1-dependent NF-kappaB-recruitment to the IL-8 promoter in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol. 290:L730–L737. 2006. View Article : Google Scholar
6	Kawai T and Akira S: Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 34:637–650. 2011. View Article : Google Scholar : PubMed/NCBI
7	Lee IT, Lee CW, Tung WH, Wang SW, Lin CC, Shu JC and Yang CM: Cooperation of TLR2 with MyD88, PI3K, and Rac1 in lipoteichoic acid-induced cPLA2/COX-2-dependent airway inflammatory responses. Am J Pathol. 176:1671–1684. 2010. View Article : Google Scholar : PubMed/NCBI
8	Bradding P, Roberts JA, Britten KM, Montefort S, Djukanovic R, Mueller R, Heusser CH, Howarth PH and Holgate ST: Interleukin-4, -5, and -6 and tumor necrosis factor-alpha in normal and asthmatic airways: Evidence for the human mast cell as a source of these cytokines. Am J Respir Cell Mol Biol. 10:471–480. 1994. View Article : Google Scholar : PubMed/NCBI
9	Moon RT, Bowerman B, Boutros M and Perrimon N: The promise and perils of Wnt signaling through beta-catenin. Science. 296:1644–1646. 2002. View Article : Google Scholar : PubMed/NCBI
10	Jang J, Ha JH, Chung SI and Yoon Y: B-catenin regulates NF-κB activity and inflammatory cytokine expression in bronchial epithelial cells treated with lipopolysaccharide. Int J Mol Med. 34:632–638. 2014.PubMed/NCBI
11	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25:402–408. 2001. View Article : Google Scholar
12	Cadigan KM and Liu YI: Wnt signaling: Complexity at the surface. J Cell Sci. 119:395–402. 2006. View Article : Google Scholar : PubMed/NCBI
13	Willert K and Nusse R: Beta-catenin: A key mediator of Wnt signaling. Curr Opin Genet Dev. 8:95–102. 1998. View Article : Google Scholar : PubMed/NCBI
14	Profita M, Bonanno A, Montalbano AM, Ferraro M, Siena L, Bruno A, Girbino S, Albano GD, Casarosa P, Pieper MP and Gjamarkaj M: Cigarette smoke extract activates human bronchial epithelial cells affecting non-neuronal cholinergic system signalling in vitro. Life Sci. 89:36–43. 2011. View Article : Google Scholar : PubMed/NCBI
15	Tal TL, Simmons SO, Silbajoris R, Dailey L, Cho SH, Ramabhadran R, Linak W, Reed W, Bromberg PA and Samet JM: Differential transcriptional regulation of IL-8 expression by human airway epithelial cells exposed to diesel exhaust particles. Toxicol Appl Pharmacol. 243:46–54. 2010. View Article : Google Scholar
16	Pylkkänen L, Stockmann-Juvala H, Alenius H, Husgafvel-Pursiainen K and Savolainen K: Wood dusts induce the production of reactive oxygen species and caspase-3 activity in human bronchial epithelial cells. Toxicology. 262:265–270. 2009. View Article : Google Scholar : PubMed/NCBI
17	Bossios A, Gourgiotis D, Skevaki CL, Saxoni-Papageorgiou P, Lötvall J, Psarras S, Karpathios T, Constandopoulos AG, Johnston SL and Papadopoulos NG: Rhinovirus infection and house dust mite exposure synergize in inducing bronchial epithelial cell interleukin-8 release. Clin Exp Allergy. 38:1615–1626. 2008. View Article : Google Scholar : PubMed/NCBI
18	Ishibashi Y and Nishikawa A: Role of nuclear factor-kappa B in the regulation of intercellular adhesion molecule 1 after infection of human bronchial epithelial cells by Bordetella pertussis. Microb Pathog. 35:169–177. 2003. View Article : Google Scholar : PubMed/NCBI
19	Thomas LH, Friedland JS, Sharland M and Becker S: Respiratory syncytial virus-induced RANTES production from human bronchial epithelial cells is dependent on nuclear factor-kappa B nuclear binding and is inhibited by adenovirus-mediated expression of inhibitor of kappa B alpha. J Immunol. 161:1007–1016. 1998.PubMed/NCBI
20	Kim JS, Yeo S, Shin DG, Bae YS, Lee JJ, Chin BR, Lee CH and Baek SH: Glycogen synthase kinase 3beta and beta-catenin pathway is involved in toll-like receptor 4-mediated NADPH oxidase 1 expression in macrophages. FEBS J. 277:2830–2837. 2010. View Article : Google Scholar : PubMed/NCBI
21	Jang J, Ha JH, Kim SM, Kim W, Kim K, Chung SI and Yoon Y: β-catenin mediates the inflammatory cytokine expression induced by the Der p 1 house dust mite allergen. Mol Med Rep. 9:633–638. 2014.