Pulmonary surfactant-associated protein B regulates prostaglandin-endoperoxide synthase-2 and inflammation in chronic obstructive pulmonary disease.
chronic obstructive pulmonary disease
inflammation
prostaglandin-endoperoxide synthase-2
pulmonary surfactant-associated protein B
Journal
Experimental physiology
ISSN: 1469-445X
Titre abrégé: Exp Physiol
Pays: England
ID NLM: 9002940
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
received:
09
11
2020
accepted:
10
03
2021
pubmed:
18
3
2021
medline:
1
4
2022
entrez:
17
3
2021
Statut:
ppublish
Résumé
What is the central question of this study? It is reported that polymorphism of the gene for pulmonary surfactant-associated protein B (SFTPB) is associated with chronic obstructive pulmonary disease (COPD): what are the function and mechanism of action of SFTPB in COPD? What is the main finding and its importance? Under stimulation of the risk factors of COPD, SFTPB expression is decreased, which may be involved in the formation of COPD. The progress of COPD induces an inflammatory response and reduces SFTPB expression. Levels of prostaglandin-endoperoxide synthase-2 (PTGS2) and inflammatory responses are changed by SFTPB, which indicates that SFTPB promotes the progression of COPD by PTGS2 and inflammation. Pulmonary surfactant-associated protein B (SFTPB) is a critical protein for lung homeostasis, and polymorphism of its gene is associated with chronic obstructive pulmonary disease (COPD). However, few studies have so far confirmed the functional involvement of SFTPB in COPD. Serum SFTPB and inflammatory cytokine levels were measured in 54 patients with acute exacerbation of COPD and 29 healthy controls. A549 cells were induced using 10% cigarette smoke extract (CSE) and treated with dexamethasone to investigate the effect of inflammation on SFTPB expression, and the effect of SFTPB overexpression and silencing on inflammatory cytokines was measured using real-time PCR and enzyme-linked immunosorbent assay. SFTPB expression was assessed in mouse lung tissues using immunofluorescence. Serum levels of SFTPB were significantly lower in COPD patients than in controls (P = 0.009). Conversely, levels of interleukin (IL)-6 and prostaglandin-endoperoxide synthase-2 (PTGS2) were increased in COPD patients (IL-6: P = 0.006; PTGS2: P = 0.043). After CSE treatment, SFTPB mRNA and protein levels were significantly decreased compared to controls (mRNA: P = 0.002; protein: P = 0.011), while IL-6, IL-8 and PTGS2 were elevated. Dexamethasone treatment increased SFTPB levels. Following overexpression of SFTPB in A549 cells, mRNA and protein levels of IL-6, IL-8 and PTGS2 were significantly reduced, while gene silencing induced the opposite effect. SFTPB levels were significantly reduced in the lung tissue of a mouse model of COPD compared to controls. Reduced SFTPB levels may induce PTGS2 and inflammatory responses in COPD and SFTPB could be a key protein for evaluation of COPD progression.
Substances chimiques
Protein Precursors
0
Pulmonary Surfactant-Associated Protein B
0
Pulmonary Surfactant-Associated Proteins
0
SFTPB protein, human
0
Cyclooxygenase 2
EC 1.14.99.1
PTGS2 protein, human
EC 1.14.99.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1303-1311Informations de copyright
© 2021 The Authors. Experimental Physiology © 2021 The Physiological Society.
Références
Amin, R. S., Wert, S. E., Baughman, R. P., Tomashefski, J. F. Jr., Nogee, L. M., Brody, A. S., Hull, W. M. & Whitsett, J. A. (2001). Surfactant protein deficiency in familial interstitial lung disease. Journal of Pediatrics, 139, 85-92.
Barnes, P. J. (2017). Cellular and molecular mechanisms of asthma and COPD. Clinical Science, 131, 1541-1558.
Baskoro, H., Sato, T., Karasutani, K., Suzuki, Y., Mitsui, A., Arano, N., Nurwidya, F., Kato, M., Takahashi, F., Kodama, Y., Seyama, K., & Takahashi, K. (2018). Regional heterogeneity in response of airway epithelial cells to cigarette smoke. BMC Pulmonary Medicine, 18, 148.
Choi, S., Lim, J. W., & Kim, H. (2018). Effect of thiol antioxidants on lipopolysaccharide-induced cyclooxygenase-2 expression in pulmonary epithelial cells. Journal of Physiology and Pharmacology, 69, https://doi.org/10.26402/jpp.2018.4.04.
de Valliere, C., Cosin-Roger, J., Simmen, S., Atrott, K., Melhem, H., Zeitz, J., Madanchi, M., Tcymbarevich, I., Fried, M., Kullak-Ublick, G. A., Vavricka, S. R., Misselwitz, B., Seuwen, K., Wagner, C. A., Eloranta, J. J., Rogler, G., & Ruiz, P. A. (2016). Hypoxia positively regulates the expression of pH-sensing G-protein-coupled receptor OGR1 (GPR68). Cellular and Molecular Gastroenterology and Hepatology, 2, 796-810.
Gandhi, C. K., Chen, C., Wu, R., Yang, L., Thorenoor, N., Thomas, N. J., DiAngelo, S. L., Spear, D., Keim, G., Yehya, N., & Floros, J. (2020). Association of SNP-SNP interactions of surfactant protein genes with pediatric acute respiratory failure. Journal of Clinical Medicine, 9, 1183.
Guida, F., Sun, N., Bantis, L. E., Muller, D. C., Li, P., Taguchi, A., Dhillon, D., Kundnani, D. L., Patel, N. J., Yan, Q., Byrnes, G., Moons, K. G. M., Tjønneland, A., Panico, S., Agnoli, C., Vineis, P., Palli, D., Bueno-de-Mesquita, B., Peeters, P. H., … Hanash S. M. (2018). Assessment of lung cancer risk on the basis of a biomarker panel of circulating proteins. JAMA Oncology, 4, e182078.
He, Y., Jiang, Z., Tong, F., Li, M., Yin, X., Hu, S., & Wang, L. (2017). Experimental study of peripheral-blood pro-surfactant protein B for screening non-small cell lung cancer. Acta Cirurgica Brasileira 32, 568-575.
Ikegami, M., Whitsett, J. A., Martis, P. C., & Weaver, T. E. (2005). Reversibility of lung inflammation caused by SP-B deficiency. American Journal of Physiology. Lung Cellular and Molecular Physiology, 289, L962-L970.
Kandemir, Y., Doğan, N., Yaka, E., Pekdemir, M., & Yılmaz, S. (2021). Clinical characteristics of neutrophilic, eosinophilic and mixed-type exacerbation phenotypes of COPD. American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2020.08.044.
Kang, M. H., van Lieshout, L. P., Xu, L., Domm, J. M., Vadivel, A., Renesme, L., Mühlfeld, C., Hurskainen, M., Mižíková, I., Pei, Y., van Vloten, J. P., Thomas, S. P., Milazzo, C., Cyr-Depauw, C., Whitsett, J. A., Nogee, L. M., Wootton, S. K., & Thébaud, B. (2020). A lung tropic AAV vector improves survival in a mouse model of surfactant B deficiency. Nature Communications, 11, 3929.
Lee, J. H., & Rawlins, E. L. (2018). Developmental mechanisms and adult stem cells for therapeutic lung regeneration. Developmental Biology, 433, 166-176.
Leung, J. M., Mayo, J., Tan, W., Tammemagi, C. M., Liu, G., Peacock, S., Shepherd, F. A., Goffin, J., Goss, G., Nicholas, G., Tremblay, A., Johnston, M., Martel, S., Laberge, F., Bhatia, R., Roberts, H., Burrowes, P., Manos, D., Stewart, L., … Sin, D. D. (2015). Plasma pro-surfactant protein B and lung function decline in smokers. European Respiratory Journal, 45, 1037-1045.
Li, D., Wang, J., Sun, D., Gong, X., Jiang, H., Shu, J., Wang, Z., Long, Z., Chen, Y., Zhang, Z., Yuan, L., Guan, R., Liang, X., Li, Z., Yao, H., Zhong, N., & Lu, W. (2018). Tanshinone IIA sulfonate protects against cigarette smoke-induced COPD and down-regulation of CFTR in mice. Scientific Reports, 8, 376.
Magnani, J. E., & Donn, S. M. (2020). Persistent respiratory distress in the term neonate: Genetic surfactant deficiency diseases. Current Pediatric Reviews, 16, 17-25.
Milara, J., Díaz-Platas, L., Contreras, S., Ribera, P., Roger, I., Ballester, B., Montero, P., Cogolludo, Á., Morcillo, E., & Cortijo, J. (2018). MUC1 deficiency mediates corticosteroid resistance in chronic obstructive pulmonary disease. Respiratory Research, 19, 226.
Molino, A., Terlizzi, M., Colarusso, C., Rossi, A., Somma, P., Saglia, A., Pinto, A., & Sorrentino, R. (2019). AIM2/IL-1α/TGF-β axis in PBMCs from exacerbated chronic obstructive pulmonary disease (COPD) patients is not related to COX-2-dependent inflammatory pathway. Frontiers in Physiology, 10, 1235.
Moll, M., Sakornsakolpat, P., Shrine, N., Hobbs, B. D., DeMeo, D. L., John, C., Guyatt, A. L., McGeachie, M. J., Gharib, S. A., Obeidat, M., Lahousse, L., Wijnant, S. R. A., Brusselle, G., Meyers, D. A., Bleecker, E. R., Li, X., Tal-Singer, R., Manichaikul, A., Rich, S. S., … Cho, M. H. (2020). Chronic obstructive pulmonary disease and related phenotypes: Polygenic risk scores in population-based and case-control cohorts. The Lancet. Respiratory Medicine, 8, 696-708.
Mourad, B. H. (2020). Prediction of lung cancer risk using circulating pro-surfactant protein B and high-sensitivity C-reactive protein among Egyptian workers in the rubber industry. Toxicology and Industrial Health, 36, 237-249.
Pan, J., Zhan, C., Yuan, T., Wang, W., Shen, Y., Sun, Y., Wu, T., Gu, W., Chen, L., & Yu, H. (2018). Effects and molecular mechanisms of intrauterine infection/inflammation on lung development. Respiratory Research, 19, 93.
Papaioannou, A. I., Konstantelou, E., Papaporfyriou, A., Bartziokas, K., Spathis, A., Bakakos, P., Loukides, S., Koulouris, N., Papiris, S., & Kostikas, K. (2018). Serum surfactant protein levels in patients admitted to the hospital with acute COPD exacerbation. Lung, 196, 201-205.
Pires-Neto, R. C., Morales, M. M., Lancas, T., Inforsato, N., Duarte, M. I., Amato, M. B., de Carvalho, C. R., da Silva, L. F., Mauad, T., & Dolhnikoff, M. (2013). Expression of acute-phase cytokines, surfactant proteins, and epithelial apoptosis in small airways of human acute respiratory distress syndrome. Journal of Critical Care, 28, 111.e119-e115.
Qian, G. Q. (2020). Advances in genome-wide association study of chronic obstructive pulmonary disease. Yi Chuan, 42, 832-846.
Seeger, W., Günther, A., & Thede, C. (1992). Differential sensitivity to fibrinogen inhibition of SP-C- vs. SP-B-based surfactants. American Journal of Physiology, 262, L286-L291.
Singh, S., Verma, S. K., Kumar, S., Ahmad, M. K., Nischal, A., Singh, S. K., & Dixit, R. K. (2018). Correlation of severity of chronic obstructive pulmonary disease with potential biomarkers. Immunology Letters, 196, 1-10.
Um, S. J., Lam, S., Coxson, H., Man, S. F., & Sin, D. D. (2013). Budesonide/formoterol enhances the expression of pro Surfactant Protein-B in lungs of COPD patients. PLoS One, 8, e83881.
Vestbo, J., Hurd, S. S., Agustí, A. G., Jones, P. W., Vogelmeier, C., Anzueto, A., Barnes, P. J., Fabbri, L. M., Martinez, F. J., Nishimura, M., Stockley, R. A., Sin, D. D., & Rodriguez-Roisin, R. (2013). Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. American Journal of Respiratory and Critical Care Medicine, 187, 347-365.
Wang, C., Xu, J., Yang, L., Xu, Y., Zhang, X., Bai, C., Kang, J., Ran, P., Shen, H., Wen, F., Huang, K., Yao, W., Sun, T., Shan, G., Yang, T., Lin, Y., Wu, S., Zhu, J., Wang, R., … He, J. (2018). Prevalence and risk factors of chronic obstructive pulmonary disease in China (the China Pulmonary Health [CPH] study): A national cross-sectional study. Lancet, 391, 1706-1717.
Wang, D., Zhang, S., Liu, B., Wang, B., He, S., & Zhang, R. (2020a). Anti-inflammatory effects of adiponectin in cigarette smoke-activated alveolar macrophage through the COX-2/PGE2 and TLRs signaling pathway. Cytokine, 133, 155148.
Wang, K., Huang, Q., Zhao, G., Yang, J., Yang, K., & Huang, Y. (2019). Gene polymorphisms of SFTPB rs7316, rs9752 and PAOX rs1046175 affect the diagnostic value of plasma Pro-SFTPB and DAS in Chinese Han non-small-cell lung cancer patients. Journal of Cellular Biochemistry, 120, 14804-14812.
Wang, P., Tan, Z. X., Fu, L., Fan, Y. J., Luo, B., Zhang, Z. H., Xu, S., Chen, Y. H., Zhao, H., & Xu, D. X. (2020b). Gestational vitamin D deficiency impairs fetal lung development through suppressing type II pneumocyte differentiation. Reproductive Toxicology, 94, 40-47.
Wu, H., Miao, Y., Shang, L. Q., Chen, R. L., & Yang, S. M. (2020). MiR-31 aggravates inflammation and apoptosis in COPD rats via activating the NF-κB signaling pathway. European Review for Medical and Pharmacological Sciences, 24, 9626-9632.
Yang, J., Wang, B., Zhou, H. X., Liang, B. M., Chen, H., Ma, C. L., Xiao, J., Deng, J., Yan, L., Chen, Y. P., Chen, C. L., Chen, F., Ou, X. M., & Feng, Y. L. (2014). Association of surfactant protein B gene with chronic obstructive pulmonary disease susceptibility. International Journal of Tuberculosis and Lung Disease, 18, 1378-1384.
Zhang, D., Cao, L., Wang, Z., Feng, H., Cai, X., Xu, M., Li, M., Yu, N., Yin, Y., Wang, W., & Kang, J. (2019). Salidroside mitigates skeletal muscle atrophy in rats with cigarette smoke-induced COPD by up-regulating myogenin and down-regulating myostatin expression. Bioscience Reports, 39, BSR20190440.
Zhou, L., Liu, Y., Chen, X., Wang, S., Liu, H., Zhang, T., Zhang, Y., Xu, Q., Han, X., Zhao, Y., Song, X., & Ye, L. (2018). Over-expression of nuclear factor-κB family genes and inflammatory molecules is related to chronic obstructive pulmonary disease. International Journal of Chronic Obstructive Pulmonary Disease, 13, 2131-2138.