Protective effects of fucoidan against hyperoxic lung injury via the ERK signaling pathway

Nie,Minghao; Wang,Yan; Lu,Yanhong; Yuan,Ying; Liu,Yingying; Li,Xiurong

doi:10.3892/mmr.2017.8022

Protective effects of fucoidan against hyperoxic lung injury via the ERK signaling pathway

Authors:
- Minghao Nie
- Yan Wang
- Yanhong Lu
- Ying Yuan
- Yingying Liu
- Xiurong Li
View Affiliations

Affiliations: Department of Pathology, Heilongjiang Provincial Hospital, Harbin, Heilongjiang 150036, P.R. China
Published online on: November 10, 2017 https://doi.org/10.3892/mmr.2017.8022
Pages: 1813-1818

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

High oxygen mechanical ventilation is widely used to treat various lung diseases; however, it may result in hyperoxia, which induces inflammation and lung injury. Fucoidan is an extract of the seaweed Fucus vesiculosus, which has previously been reported to exert effects against diabetic nephropathy. The present study is the first, to the best of our knowledge, to investigate the protective effects of fucoidan against hyperoxic lung injury. Balb/c mice were ventilated with 100% oxygen, with or without the atomization inhalation of fucoidan, for 36 h. Hyperoxia reduced the body weight and increased the relative lung weight of the mice. In addition, cell quantity and differentiation were determined using a hemocytometer, hyperoxia increased the total number of cells, and the number of macrophages, neutrophils and lymphocytes in the bronchoalveolar lavage fluid. Reverse transcription‑quantitative polymerase chain reaction (RT‑qPCR) demonstrated that hyperoxia also increased the mRNA expression levels of cluster of differentiation (CD)68, F4/80, CD64 and CD19 in lung tissue, and induced lung morphological alterations. Furthermore, western blotting assay demonstrated that hyperoxia increased the expression levels of interleukin (IL)‑1, IL‑6 and tumor necrosis factor (TNF)‑α, and the phosphorylation of extracellular signal‑regulated kinase (ERK)1/2. Conversely, hyperoxia‑induced inflammation and morphological alterations were significantly attenuated in the mice treated with fucoidan. Atomization inhalation of fucoidan also reduced the hyperoxia‑induced expression of IL‑1, IL‑6 and TNF‑α, and the phosphorylation of ERK1/2. These findings suggested that fucoidan may attenuate hyperoxic lung injury via the ERK1/2 signaling pathway.

View Figures

View References

1	Xu Y, Tian Z and Xie P: Targeting complement anaphylatoxin C5a receptor in hyperoxic lung injury in mice. Mol Med Rep. 10:1786–1792. 2014. View Article : Google Scholar :
2	Vitacca M, Bianchi L, Bazza A and Clini EM: Advanced COPD patients under home mechanical ventilation and/or long term oxygen therapy: Italian healthcare costs. Monaldi Arch Chest Dis. 75:207–214. 2011.
3	Panikkanvalappil SR, James M, Hira SM, Mobley J, Jilling T, Ambalavanan N and El-Sayed MA: Hyperoxia induces intracellular acidification in neonatal mouse lung fibroblasts: Real-time investigation using plasmonically enhanced Raman spectroscopy. J Am Chem Soc. 138:3779–3788. 2016. View Article : Google Scholar
4	Vosdoganes P, Lim R, Koulaeva E, Chan ST, Acharya R, Moss TJ and Wallace EM: Human amnion epithelial cells modulate hyperoxia-induced neonatal lung injury in mice. Cytotherapy. 15:1021–1029. 2013. View Article : Google Scholar
5	George CL, Fantuzzi G, Bursten S, Leer L and Abraham E: Effects of lisofylline on hyperoxia-induced lung injury. Am J Physiol. 276:L776–L785. 1999.
6	Kallet RH and Matthay MA: Hyperoxic acute lung injury. Respir Care. 58:123–141. 2013. View Article : Google Scholar :
7	Johnson-Varghese L, Brodsky N and Bhandari V: Effect of antioxidants on apoptosis and cytokine release in fetal rat Type II pneumocytes exposed to hyperoxia and nitric oxide. Cytokine. 28:10–16. 2004. View Article : Google Scholar
8	Fukuhara K, Nakashima T, Abe M, Masuda T, Hamada H, Iwamoto H, Fujitaka K, Kohno N and Hattori N: Suplatast tosilate protects the lung against hyperoxic lung injury by scavenging hydroxyl radicals. Free Radic Biol Med. 106:1–9. 2017. View Article : Google Scholar
9	Xie P, Fujii I, Zhao J, Shinohara M and Matsukura M: A novel polysaccharide compound derived from algae extracts protects retinal pigment epithelial cells from high glucose-induced oxidative damage in vitro. Biol Pharm Bull. 35:1447–1453. 2012. View Article : Google Scholar
10	Kasai A, Arafuka S, Koshiba N, Takahashi D and Toshima K: Systematic synthesis of low-molecular weight fucoidan derivatives and their effect on cancer cells. Org Biomol Chem. 13:10556–10568. 2015. View Article : Google Scholar
11	Fukahori S, Yano H, Akiba J, Ogasawara S, Momosaki S, Sanada S, Kuratomi K, Ishizaki Y, Moriya F, Yagi M and Kojiro M: Fucoidan, a major component of brown seaweed, prohibits the growth of human cancer cell lines in vitro. Mol Med Rep. 1:537–542. 2008.
12	Li X, Zhao H, Wang Q, Liang H and Jiang X: Fucoidan protects ARPE-19 cells from oxidative stress via normalization of reactive oxygen species generation through the Ca²+-dependent ERK signaling pathway. Mol Med Rep. 11:3746–3752. 2015. View Article : Google Scholar
13	Wang Y, Nie M, Lu Y, Wang R, Li J, Yang B, Xia M, Zhang H and Li X: Fucoidan exerts protective effects against diabetic nephropathy related to spontaneous diabetes through the NF-κB signaling pathway in vivo and in vitro. Int J Mol Med. 35:1067–1073. 2015. View Article : Google Scholar
14	Glotin AL, Calipel A, Brossas JY, Faussat AM, Tréton J and Mascarelli F: Sustained versus transient ERK1/2 signaling underlies the anti- and proapoptotic effects of oxidative stress in human RPE cells. Invest Ophthalmol Vis Sci. 47:4614–4623. 2006. View Article : Google Scholar
15	Pushparaj PN, Tay HK, Wang CC, Hong W and Melendez AJ: VAMP8 is essential in anaphylatoxin-induced degranulation, TNF-alpha secretion, peritonitis, and systemic inflammation. J Immunol. 183:1413–1418. 2009. View Article : Google Scholar
16	Davies J, Karmouty-Quintana H, Le TT, Chen NY, Weng T, Luo F, Molina J, Moorthy B and Blackburn MR: Adenosine promotes vascular barrier function in hyperoxic lung injury. Physiol Rep. 2:pii: e12155. 2014. View Article : Google Scholar :
17	Mikawa K, Nishina K, Maekawa N and Obara H: Attenuation of hyperoxic lung injury in rabbits with superoxide dismutase: Effects on inflammatory mediators. Acta Anaesthesiol Scand. 39:317–322. 1995. View Article : Google Scholar
18	Takao Y, Mikawa K, Nishina K, Maekawa N and Obara H: Lidocaine attenuates hyperoxic lung injury in rabbits. Acta Anaesthesiol Scand. 40:318–325. 1996. View Article : Google Scholar
19	Dolinay T, Wu W, Kaminski N, Ifedigbo E, Kaynar AM, Szilasi M, Watkins SC, Ryter SW, Hoetzel A and Choi AM: Mitogen-activated protein kinases regulate susceptibility to ventilator-induced lung injury. PLoS One. 3:e16012008. View Article : Google Scholar :
20	Camacho Villarreal JL, Torres Mendoza E, Cadena C, Prieto J, Varela Prieto LL and DA Torregroza Villanueva: The use of factorial design, image analysis, and an efficiency calculation for multiplex PCR optimization. J Clin Lab Anal. 27:249–252. 2013. View Article : Google Scholar
21	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
22	Jiang X, Ma Y, Yu J, Li H and Xie F: Protective effect of C4a against hyperoxic lung injury via a macrophage-dependent but not a neutrophil/lymphocyte-dependent signaling pathway. Mol Med Rep. 13:1250–1256. 2016. View Article : Google Scholar
23	Runzi M, Raptopoulos V, Saluja AK, Kaiser AM, Nishino H, Gerdes D and Steer ML: Evaluation of necrotizing pancreatitis in the opossum by dynamic contrast-enhanced computed tomography: Correlation between radiographic and morphologic changes. J Am Coll Surg. 180:673–682. 1995.
24	Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680–685. 1970. View Article : Google Scholar
25	Tsuruta T, Yamamoto T, Matsubara S, Nagasawa S, Tanase S, Tanaka J, Takagi K and Kambara T: Novel function of C4a anaphylatoxin. Release from monocytes of protein which inhibits monocyte chemotaxis. Am J Pathol. 142:1848–1857. 1993.
26	Matsubara S, Yamamoto T, Tsuruta T, Takagi K and Kambara T: Complement C4-derived monocyte-directed chemotaxis inhibitory factor. A molecular mechanism to cause polymorphonuclear leukocyte-predominant infiltration in rheumatoid arthritis synovial cavities. Am J Pathol. 138:1279–1291. 1991.
27	Janssen WJ, Barthel L, Muldrow A, Oberley-Deegan RE, Kearns MT, Jakubzick C and Henson PM: Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am J Respir Crit Care Med. 184:547–560. 2011. View Article : Google Scholar :
28	Zhao Y, Xu H, Yu W and Xie BD: Complement anaphylatoxin C4a inhibits C5a-induced neointima formation following arterial injury. Mol Med Rep. 10:45–52. 2014. View Article : Google Scholar :
29	Jones SA: Directing transition from innate to acquired immunity: Defining a role for IL-6. J Immunol. 175:3463–3468. 2005. View Article : Google Scholar
30	Bao JP, Jiang LF, Li J, Chen WP, Hu PF and Wu LD: Visceral adipose tissue-derived serine protease inhibitor inhibits interleukin-1β-induced catabolic and inflammatory responses in murine chondrocytes. Mol Med Rep. 10:2191–2197. 2014. View Article : Google Scholar
31	Wolters PJ, Wray C, Sutherland RE, Kim SS, Koff J, Mao Y and Frank JA: Neutrophil-derived IL-6 limits alveolar barrier disruption in experimental ventilator-induced lung injury. J Immunol. 182:8056–8062. 2009. View Article : Google Scholar :
32	Frank JA, Parsons PE and Matthay MA: Pathogenetic significance of biological markers of ventilator-associated lung injury in experimental and clinical studies. Chest. 130:1906–1914. 2006. View Article : Google Scholar :
33	Piguet PF, Collart MA, Grau GE, Sappino AP and Vassalli P: Requirement of tumour necrosis factor for development of silica-induced pulmonary fibrosis. Nature. 344:245–247. 1990. View Article : Google Scholar
34	Guillonneau X, Régnier-Ricard F, Dupuis C, Courtois Y and Mascarelli F: Paracrine effects of phosphorylated and excreted FGF1 by retinal pigmented epithelial cells. Growth Factors. 15:95–112. 1998. View Article : Google Scholar