Methyl p‑hydroxycinnamate exerts anti‑inflammatory effects in mouse models of lipopolysaccharide‑induced ARDS

Kim,Seong-Man; Min,Jae-Hong; Kim,Jung Hee; Choi,Jinseon; Park,Jin-Mi; Lee,Juhyun; Goo,Soo Hyeon; Oh,Jae Hoon; Kim,Seung-Ho; Chun,Wanjoo; Ahn,Kyung-Seop; Kang,Sukmo; Lee,Jae-Won

doi:10.3892/mmr.2021.12553

Methyl p‑hydroxycinnamate exerts anti‑inflammatory effects in mouse models of lipopolysaccharide‑induced ARDS

Authors:
- Seong-Man Kim
- Jae-Hong Min
- Jung Hee Kim
- Jinseon Choi
- Jin-Mi Park
- Juhyun Lee
- Soo Hyeon Goo
- Jae Hoon Oh
- Seung-Ho Kim
- Wanjoo Chun
- Kyung-Seop Ahn
- Sukmo Kang
- Jae-Won Lee
View Affiliations

Affiliations: Natural Medicine Research Center, Korea Research Institute of Bioscience and Biotechnology, Ochang, Cheongju, Chungcheongbuk‑do 28116, Republic of Korea, Department of Pharmacology, College of Medicine, Kangwon National University, Chuncheon 24341, Republic of Korea, Biotoxtech Co., Ltd., Ochang, Cheongju, Chungcheongbuk‑do 28115, Republic of Korea
Published online on: December 2, 2021 https://doi.org/10.3892/mmr.2021.12553
Article Number: 37
Copyright: © Kim 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

Methyl p‑hydroxycinnamate (MH), an esterified derivative of p‑Coumaric acid exerts anti‑inflammatory effects on lipopolysaccharide (LPS)‑stimulated RAW264.7 macrophages. Based on these effects, the present study investigated the protective role of MH in a mouse model of LPS‑induced acute respiratory distress syndrome (ARDS). The results demonstrated that administration of LPS (5 mg/kg intranasally) markedly increased the neutrophil/macrophage numbers and levels of inflammatory molecules (TNF‑α, IL‑6, IL‑1β and reactive oxygen species) in the bronchoalveolar lavage ﬂuid (BALF) of mice. On histological examination, the presence of inflammatory cells was observed in the lungs of mice administered LPS. LPS also notably upregulated the secretion of monocyte chemoattractant protein‑1 and protein content in BALF as well as expression of inducible nitric oxide synthase in the lungs of mice; it also caused activation of p38 mitogen‑activated protein kinase (MAPK) and NF‑κB signaling. However, MH treatment significantly suppressed LPS‑induced upregulation of inflammatory cell recruitment, inflammatory molecule levels and p38MAPK/NF‑κB activation, and also led to upregulation of heme oxygenase‑1 (HO‑1) expression in the lungs of mice. In addition, the ability of MH to induce HO‑1 expression was confirmed in RAW264.7 macrophages. Taken together, the findings of the present study indicated that MH may exert protective effects against airway inflammation in ARDS mice by inhibiting inflammatory cell recruitment and the production of inflammatory molecules.

View Figures

View References

1	Spadaro S, Park M, Turrini C, Tunstall T, Thwaites R, Mauri T, Ragazzi R, Ruggeri P, Hansel TT, Caramori G and Volta CA: Biomarkers for Acute Respiratory Distress syndrome and prospects for personalised medicine. J Inflamm (Lond). 16:12019. View Article : Google Scholar : PubMed/NCBI
2	Bhargava M and Wendt CH: Biomarkers in acute lung injury. Transl Res. 159:205–217. 2012. View Article : Google Scholar : PubMed/NCBI
3	Barnett N and Ware LB: Biomarkers in acute lung injury-marking forward progress. Crit Care Clin. 27:661–683. 2011. View Article : Google Scholar : PubMed/NCBI
4	Kellner M, Noonepalle S, Lu Q, Srivastava A, Zemskov E and Black SM: ROS signaling in the pathogenesis of acute lung Injury (ALI) and acute respiratory distress syndrome (ARDS). Adv Exp Med Biol. 967:105–137. 2017. View Article : Google Scholar : PubMed/NCBI
5	Lee JW, Chun W, Lee HJ, Min JH, Kim SM, Seo JY, Ahn KS and Oh SR: The role of macrophages in the development of acute and chronic inflammatory lung diseases. Cells. 10:8972021. View Article : Google Scholar : PubMed/NCBI
6	Lee JW, Chun W, Kwon OK, Park HA, Lim Y, Lee JH, Kim DY, Kim JH, Lee HK, Ryu HW, et al: 3,4,5-Trihydroxycinnamic acid attenuates lipopolysaccharide (LPS)-induced acute lung injury via downregulating inflammatory molecules and upregulating HO-1/AMPK activation. Int Immunopharmacol. 64:123–130. 2018. View Article : Google Scholar : PubMed/NCBI
7	Lee JW, Park HA, Kwon OK, Park JW, Lee G, Lee HJ, Lee SJ, Oh SR and Ahn KS: NPS 2143, a selective calcium-sensing receptor antagonist inhibits lipopolysaccharide-induced pulmonary inflammation. Mol Immunol. 90:150–157. 2017. View Article : Google Scholar : PubMed/NCBI
8	Liu B, Cheng Y, Wu Y, Zheng X, Li X, Yang G, He T, Li S and Shen F: Emodin improves alveolar hypercoagulation and inhibits pulmonary inflammation in LPS-provoked ARDS in mice via NF-κB inactivation. Int Immunopharmacol. 88:1070202020. View Article : Google Scholar : PubMed/NCBI
9	Frank JA, Pittet JF, Lee H, Godzich M and Matthay MA: High tidal volume ventilation induces NOS2 and impairs cAMP- dependent air space fluid clearance. Am J Physiol Lung Cell Mol Physiol. 284:L791–L798. 2003. View Article : Google Scholar : PubMed/NCBI
10	Xiao Q, Cui Y, Zhao Y, Liu L, Wang H and Yang L: Orientin relieves lipopolysaccharide-induced acute lung injury in mice: The involvement of its anti-inflammatory and anti-oxidant properties. Int Immunopharmacol. 90:1071892021. View Article : Google Scholar : PubMed/NCBI
11	Lee SA, Lee SH, Kim JY and Lee WS: Effects of glycyrrhizin on lipopolysaccharide-induced acute lung injury in a mouse model. J Thorac Dis. 11:1287–1302. 2019. View Article : Google Scholar : PubMed/NCBI
12	Moine P, McIntyre R, Schwartz MD, Kaneko D, Shenkar R, Le Tulzo Y, Moore EE and Abraham E: NF-kappaB regulatory mechanisms in alveolar macrophages from patients with acute respiratory distress syndrome. Shock. 13:85–91. 2000. View Article : Google Scholar : PubMed/NCBI
13	Zhong WT, Wu YC, Xie XX, Zhou X, Wei MM, Soromou LW, Ci XX and Wang DC: Phillyrin attenuates LPS-induced pulmonary inflammation via suppression of MAPK and NF-κB activation in acute lung injury mice. Fitoterapia. 90:132–139. 2013. View Article : Google Scholar : PubMed/NCBI
14	Guo S, Jiang K, Wu H, Yang C, Yang Y, Yang J, Zhao G and Deng G: Magnoflorine ameliorates lipopolysaccharide-induced acute lung injury via suppressing NF-κB and MAPK activation. Front Pharmacol. 9:9822018. View Article : Google Scholar : PubMed/NCBI
15	Lei J, Wei Y, Song P, Li Y, Zhang T, Feng Q and Xu G: Cordycepin inhibits LPS-induced acute lung injury by inhibiting inflammation and oxidative stress. Eur J Pharmacol. 818:110–114. 2018. View Article : Google Scholar : PubMed/NCBI
16	Pooladanda V, Thatikonda S, Bale S, Pattnaik B, Sigalapalli DK, Bathini NB, Singh SB and Godugu C: Nimbolide protects against endotoxin-induced acute respiratory distress syndrome by inhibiting TNF-α mediated NF-κB and HDAC-3 nuclear translocation. Cell Death Dis. 10:812019. View Article : Google Scholar : PubMed/NCBI
17	Kwon YS and Kim CM: Antioxidant constituents from the stem of Sorghum bicolor. Arch Pharm Res. 26:535–539. 2003. View Article : Google Scholar : PubMed/NCBI
18	Vo VA, Lee JW, Shin SY, Kwon JH, Lee HJ, Kim SS, Kwon YS and Chun W: Methyl p-Hydroxycinnamate suppresses lipopolysaccharide-induced inflammatory responses through akt phosphorylation in RAW264.7 cells. Biomol Ther (Seoul). 22:10–16. 2014. View Article : Google Scholar : PubMed/NCBI
19	Park JW, Ryu HW, Ahn HI, Min JH, Kim SM, Kim MG, Kwon OK, Hwang D, Kim SY, Choi S, et al: The anti-inflammatory effect of trichilia martiana C. DC. in the lipopolysaccharide-stimulated inflammatory response in macrophages and airway epithelial cells and in LPS-challenged mice. J Microbiol Biotechnol. 30:1614–1625. 2020. View Article : Google Scholar : PubMed/NCBI
20	Lee JW, Ryu HW, Lee SU, Kim MG, Kwon OK, Kim MO, Oh TK, Lee JK, Kim TY, Lee SW, et al: Pistacia weinmannifolia ameliorates cigarette smoke and lipopolysaccharide-induced pulmonary inflammation by inhibiting interleukin8 production and NF-κB activation. Int J Mol Med. 44:949–959. 2019.PubMed/NCBI
21	Tian M, Peng S, Wang S, Li X, Li H and Shen L: Pristimerin reduces dextran sulfate sodium-induced colitis in mice by inhibiting microRNA-155. Int Immunopharmacol. 94:1074912021. View Article : Google Scholar : PubMed/NCBI
22	Bhatia M and Moochhala S: Role of inflammatory mediators in the pathophysiology of acute respiratory distress syndrome. J Pathol. 202:145–156. 2004. View Article : Google Scholar : PubMed/NCBI
23	Parsons PE, Eisner MD, Thompson BT, Matthay MA, Ancukiewicz M, Bernard GR and Wheeler AP; NHLBI Acute Respiratory Distress Syndrome Clinical Trials Network, : Lower tidal volume ventilation and plasma cytokine markers of inflammation in patients with acute lung injury. Crit Care Med. 33:1–6; discussion 230-2. 2005. View Article : Google Scholar : PubMed/NCBI
24	Dong Z and Yuan Y: Accelerated inflammation and oxidative stress induced by LPS in acute lung injury: Inhibition by ST1926. Int J Mol Med. 41:3405–3421. 2018.PubMed/NCBI
25	Guimarães LMF, Rossini CVT and Lameu C: Implications of SARS-Cov-2 infection on eNOS and iNOS activity: Consequences for the respiratory and vascular systems. Nitric Oxide. 111-112:64–71. 2021. View Article : Google Scholar : PubMed/NCBI
26	Chen JR, Tang Y, Wang YL, Cui Q, Inam M, Kong LC and Ma HX: Serine protease inhibitor MDSPI16 ameliorates LPS-induced acute lung injury through its anti-inflammatory activity. Int Immunopharmacol. 88:1070152020. View Article : Google Scholar : PubMed/NCBI
27	Wu YX, Zeng S, Wan BB, Wang YY, Sun HX, Liu G, Gao ZQ, Chen D, Chen YQ, Lu MD and Pang QF: Sophoricoside attenuates lipopolysaccharide-induced acute lung injury by activating the AMPK/Nrf2 signaling axis. Int Immunopharmacol. 90:1071872021. View Article : Google Scholar : PubMed/NCBI
28	Sun WH, Liu F, Chen Y and Zhu YC: Hydrogen sulfide decreases the levels of ROS by inhibiting mitochondrial complex IV and increasing SOD activities in cardiomyocytes under ischemia/reperfusion. Biochem Biophys Res Commun. 421:164–169. 2012. View Article : Google Scholar : PubMed/NCBI
29	Lan A, Liao X, Mo L, Yang C, Yang Z, Wang X, Hu F, Chen P, Feng J, Zheng D and Xiao L: Hydrogen sulfide protects against chemical hypoxia-induced injury by inhibiting ROS-activated ERK1/2 and p38MAPK signaling pathways in PC12 cells. PLoS One. 6:e259212011. View Article : Google Scholar : PubMed/NCBI
30	Fang W, Cai SX, Wang CL, Sun XX, Li K, Yan XW, Sun YB, Sun XZ, Gu CK, Dai MY, et al: Modulation of mitogen-activated protein kinase attenuates sepsis-induced acute lung injury in acute respiratory distress syndrome rats. Mol Med Rep. 16:9652–9658. 2017. View Article : Google Scholar : PubMed/NCBI
31	Wu H, Zhao G, Jiang K, Chen X, Zhu Z, Qiu C, Li C and Deng G: Plantamajoside ameliorates lipopolysaccharide-induced acute lung injury via suppressing NF-κB and MAPK activation. Int Immunopharmacol. 35:315–322. 2016. View Article : Google Scholar : PubMed/NCBI
32	Jha P and Das H: KLF2 in Regulation of NF-κB-Mediated immune cell function and inflammation. Int J Mol Sci. 18:23832017. View Article : Google Scholar : PubMed/NCBI
33	Meng L, Li L, Lu S, Li K, Su Z, Wang Y, Fan X, Li X and Zhao G: The protective effect of dexmedetomidine on LPS-induced acute lung injury through the HMGB1-mediated TLR4/NF-κB and PI3K/Akt/mTOR pathways. Mol Immunol. 94:7–17. 2018. View Article : Google Scholar : PubMed/NCBI
34	Tang J, Xu L, Zeng Y and Gong F: Effect of gut microbiota on LPS-induced acute lung injury by regulating the TLR4/NF-kB signaling pathway. Int Immunopharmacol. 91:1072722021. View Article : Google Scholar : PubMed/NCBI
35	Zhang WB, Yang F, Wang Y, Jiao FZ, Zhang HY, Wang LW and Gong ZJ: Inhibition of HDAC6 attenuates LPS-induced inflammation in macrophages by regulating oxidative stress and suppressing the TLR4-MAPK/NF-κB pathways. Biomed Pharmacother. 117:1091662019. View Article : Google Scholar : PubMed/NCBI
36	Dong Q, Li Y, Chen J and Wang N: Azilsartan Suppressed LPS-Induced Inflammation in U937 Macrophages through Suppressing Oxidative Stress and Inhibiting the TLR2/MyD88 Signal Pathway. ACS Omega. 6:113–118. 2020. View Article : Google Scholar : PubMed/NCBI
37	Liu Q, Ci X, Wen Z and Peng L: Diosmetin Alleviates Lipopolysaccharide-Induced acute lung injury through activating the Nrf2 Pathway and inhibiting the NLRP3 Inflammasome. Biomol Ther (Seoul). 26:157–166. 2018. View Article : Google Scholar : PubMed/NCBI
38	Liu Y, Song M, Zhu G, Xi X, Li K, Wu C and Huang L: Corynoline attenuates LPS-induced acute lung injury in mice by activating Nrf2. Int Immunopharmacol. 48:96–101. 2017. View Article : Google Scholar : PubMed/NCBI