Mechanism of IL‑8‑induced acute lung injury through pulmonary surfactant proteins A and B

Yang,Yinong; Li,Qing; Tan,Feng; Zhang,Jun; Zhu,Wu

doi:10.3892/etm.2019.8192

Mechanism of IL‑8‑induced acute lung injury through pulmonary surfactant proteins A and B

Authors:
- Yinong Yang
- Qing Li
- Feng Tan
- Jun Zhang
- Wu Zhu
View Affiliations

Affiliations: Medical School, Hunan University of Medicine, Huaihua, Hunan 418000, P.R. China, Nursing School, Hunan University of Medicine, Huaihua, Hunan 418000, P.R. China, School of Stomatology, Hunan University of Medicine, Huaihua, Hunan 418000, P.R. China
Published online on: November 13, 2019 https://doi.org/10.3892/etm.2019.8192
Pages: 287-293
Copyright: © Yang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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

This study explored how interleukin‑8 (IL‑8) causes acute lung injury (ALI) through pulmonary surfactant protein A (SP‑A) and surfactant protein B (SP‑B). Serum was collected from 53 ALI patients and further 56 healthy subjects who underwent physical examination. The IL‑8, SP‑A, and SP‑B levels were determined using enzyme‑linked immunosorbent assay (ELISA). An ALI model was constructed using lipopolysaccharide (LSP)‑induced normal A549 cells. siRNA was employed to interfere with the expression of IL‑8, SP‑A and SP‑B. Western blot analysis was carried out to determine the protein levels, and MTT assay to determine the cell activity. In addition, co‑immunoprecipitation (Co‑IP) assay was used to verify the interaction between IL‑8, SP‑A and SP‑B. ALI patients showed high expression of serum IL‑8, and low expression of SP‑A and SP‑B, and IL‑8 was negatively correlated with SP‑A and SP‑B, respectively. LSP‑induced normal A549 cells showed increased expression of IL‑8 and decreased expression of SP‑A and SP‑B. Silencing IL‑8 led to increased expression levels of SP‑A, SP‑B and Bcl2, decreased expression levels of caspase‑9, caspase‑3, Bax, TNF‑α, IL‑17 and IL‑1β, reduced cell apoptosis rate, and enhanced cell viability. Silencing SP‑A and SP‑B resulted in increased expression of IL‑8, caspase‑9, caspase‑3, Bax, TNF‑α, IL‑17 and IL‑1β, and decreased expression of Bcl2. Co‑IP assay revealed that IL‑8 could interact with SP‑A and SP‑B, respectively. IL‑8 induces apoptosis by inhibiting SP‑A and SP‑B, and intensifies cellular inflammatory reaction, leading eventually to ALI.

View Figures

View References

1	Lumb AB: Acute lung injuryNunn's Applied Respiratory Physiology. 8th. Elsevier; pp. 439–449. 2017, View Article : Google Scholar
2	Butt Y, Kurdowska A and Allen TC: Acute lung injury: A clinical and molecular review. Arch Pathol Lab Med. 140:345–350. 2016. View Article : Google Scholar : PubMed/NCBI
3	Fanelli V and Ranieri VM: Mechanisms and clinical consequences of acute lung injury. Ann Am Thorac Soc. 12 (Suppl 1):S3–S8. 2015. View Article : Google Scholar : PubMed/NCBI
4	Terasaki Y, Suzuki T, Tonaki K, Terasaki M, Kuwahara N, Ohsiro J, Iketani M, Takahashi M, Hamanoue M, Kajimoto Y, et al: Molecular hydrogen attenuates gefitinib-induced exacerbation of naphthalene-evoked acute lung injury through a reduction in oxidative stress and inflammation. Lab Invest. 99:793–806. 2019. View Article : Google Scholar : PubMed/NCBI
5	Kapur R, Kim M, Aslam R, McVey MJ, Tabuchi A, Luo A, Liu J, Li Y, Shanmugabhavananthan S, Speck ER, et al: T regulatory cells and dendritic cells protect against transfusion-related acute lung injury via IL-10. Blood. 129:2557–2569. 2017. View Article : Google Scholar : PubMed/NCBI
6	Martin TR, Nakamura M and Matute-Bello G: The role of apoptosis in acute lung injury. Crit Care Med. 31 (Suppl):S184–S188. 2003. View Article : Google Scholar : PubMed/NCBI
7	Oppenheim JJ, Zachariae COC, Mukaida N and Matsushima K: Properties of the novel proinflammatory supergene ‘intercrine’ cytokine family. Annu Rev Immunol. 9:617–648. 1991. View Article : Google Scholar : PubMed/NCBI
8	Krupa A, Kato H, Matthay MA and Kurdowska AK: Proinflammatory activity of anti-IL-8 autoantibody: IL-8 complexes in alveolar edema fluid from patients with acute lung injury. Am J Physiol Lung Cell Mol Physiol. 286:L1105–L1113. 2004. View Article : Google Scholar : PubMed/NCBI
9	Liu XW, Ma T, Cai Q, Wang L, Song HW and Liu Z: Elevation of serum PARK7 and IL-8 levels is associated with acute lung injury in patients with severe sepsis/septic shock. J Intensive Care Med. 34:662–668. 2019. View Article : Google Scholar : PubMed/NCBI
10	Selman M, Lin HM, Montaño M, Jenkins AL, Estrada A, Lin Z, Wang G, DiAngelo SL, Guo X, Umstead TM, et al: Surfactant protein A and B genetic variants predispose to idiopathic pulmonary fibrosis. Hum Genet. 113:542–550. 2003. View Article : Google Scholar : PubMed/NCBI
11	Goto H, Ledford JG, Mukherjee S, Noble PW, Williams KL and Wright JR: The role of surfactant protein A in bleomycin-induced acute lung injury. Am J Respir Crit Care Med. 181:1336–1344. 2010. View Article : Google Scholar : PubMed/NCBI
12	Cheng G, Ueda T, Nakajima H, Nakajima A, Arima M, Kinjyo S and Fukuda T: Surfactant protein A exhibits inhibitory effect on eosinophils IL-8 production. Biochem Biophys Res Commun. 270:831–835. 2000. View Article : Google Scholar : PubMed/NCBI
13	Schagat TL, Wofford JA and Wright JR: Surfactant protein A enhances alveolar macrophage phagocytosis of apoptotic neutrophils. J Immunol. 166:2727–2733. 2001. View Article : Google Scholar : PubMed/NCBI
14	Ingenito EP, Mora R, Cullivan M, Marzan Y, Haley K, Mark L and Sonna LA: Decreased surfactant protein-B expression and surfactant dysfunction in a murine model of acute lung injury. Am J Respir Cell Mol Biol. 25:35–44. 2001. View Article : Google Scholar : PubMed/NCBI
15	Martínez-Calle M, Olmeda B, Dietl P, Frick M and Pérez-Gil J: Pulmonary surfactant protein SP-B promotes exocytosis of lamellar bodies in alveolar type II cells. FASEB J. 32:4600–4611. 2018. View Article : Google Scholar : PubMed/NCBI
16	Ramana CV: Insights into the signal transduction pathways of mouse lung type II cells revealed by transcription factor profiling in the transcriptome. Genomics Inform. 17:e82019. View Article : Google Scholar : PubMed/NCBI
17	Han B, Lodyga M and Liu M: Ventilator-induced lung injury: Role of protein-protein interaction in mechanosensation. Proc Am Thorac Soc. 2:181–187. 2005. View Article : Google Scholar : PubMed/NCBI
18	Decuypere JP, Parys JB and Bultynck G: Regulation of the autophagic bcl-2/beclin 1 interaction. Cells. 1:284–312. 2012. View Article : Google Scholar : PubMed/NCBI
19	Zhao X, Yu Z, Lv Z, Meng L, Xu J, Yuan S and Fu Z: Activation of alpha-7 nicotinic acetylcholine receptors (α7nAchR) promotes the protective autophagy in LPS-induced acute lung injury (ALI) in vitro and in vivo. Inflammation. Sep 14–2019.(Epub ahead of print). View Article : Google Scholar
20	Hough RF, Islam MN, Gusarova GA, Jin G, Das S and Bhattacharya J: Endothelial mitochondria determine rapid barrier failure in chemical lung injury. JCI Insight. 4:42019. View Article : Google Scholar
21	Zhang NN, Zhang Y, Wang L, Xia JG, Liang ST, Wang Y, Wang ZZ, Huang X, Li M, Zeng H, et al: Expression profiling analysis of long noncoding RNAs in a mouse model of ventilator-induced lung injury indicating potential roles in inflammation. J Cell Biochem. 120:11660–11679. 2019. View Article : Google Scholar
22	Li T, Zhao B, Wang C, Wang H, Liu Z, Li W, Jin H, Tang C and Du J: Regulatory effects of hydrogen sulfide on IL-6, IL-8 and IL-10 levels in the plasma and pulmonary tissue of rats with acute lung injury. Exp Biol Med (Maywood). 233:1081–1087. 2008. View Article : Google Scholar : PubMed/NCBI
23	Harrod KS, Trapnell BC, Otake K, Korfhagen TR and Whitsett JA: SP-A enhances viral clearance and inhibits inflammation after pulmonary adenoviral infection. Am J Physiol. 277:L580–L588. 1999.PubMed/NCBI
24	Arias-Diaz J, Garcia-Verdugo I, Casals C, Sanchez-Rico N, Vara E and Balibrea JL: Effect of surfactant protein A (SP-A) on the production of cytokines by human pulmonary macrophages. Shock. 14:300–306. 2000. View Article : Google Scholar : PubMed/NCBI
25	Epaud R, Ikegami M, Whitsett JA, Jobe AH, Weaver TE and Akinbi HT: Surfactant protein B inhibits endotoxin-induced lung inflammation. Am J Respir Cell Mol Biol. 28:373–378. 2003. View Article : Google Scholar : PubMed/NCBI