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Food Microbiology and Biotechnology(FMB)  |  Bioactive compounds and Physiological properties

Protective Effects of the Ethanol Extract of Viola tianshanica Maxim against Acute Lung Injury Induced by Lipopolysaccharides in Mice

Xue Wang 1, Qiao-Li Yang 1, Yu-Zhu Shi 1, Bi-Yu Hou 2, Sheng-Qian Yang 2, Hua Huang 1, Li Zhang 2 and Guan-Hua Du 2*

1Xinjiang Key Laboratory for Uighur Medicine, Xinjiang Institute of Materia Medica, Urumqi 830004, P.R. China, 2Beijing Key Laboratory of Drug Target Identification and Drug Screening, Institute of Materia Medica, Chinese Academy of Medical Sciences, Beijing 100050, P.R. China

Received: January 26, 2017; Accepted: July 28, 2017

J. Microbiol. Biotechnol. 2017; 27(9): 1628-1638

Published September 28, 2017 https://doi.org/10.4014/jmb.1701.01067

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Viola tianshanica Maxim, belonging to the Violaceae plant family, is traditionally used in Uighur medicine for treating pneumonia, headache, and fever. There is, however, a lack of basic understanding of its pharmacological activities. This study was designed to observe the effects of the ethanol extract (TSM) from Viola tianshanica Maxim on the inflammation response in acute lung injury (ALI) induced by LPS and the possible underlying mechanisms. We found that TSM (200 and 500 mg/kg) significantly decreased inflammatory cytokine production and the number of inflammatory cells, including macrophages and neutrophils, in bronchoalveolar lavage fluid. TSM also markedly inhibited the lung wet-to-dry ratio and alleviated pathological changes in lung tissues. In vitro, after TSM (12.5-100 μg/ml) treatment to RAW 264.7 cells for 1 h, LPS (1 μg/ml) was added and the cells were further incubated for 24 h. TSM dose-dependently inhibited the levels of proinflammatory cytokines, such as NO, PGE2, TNF-α, IL-6, and IL-1β, and remarkably decreased the protein and mRNA expression of TNF-α and IL-6 in LPS-stimulated RAW 264.7 cells. TSM also suppressed protein expression of p-IκBa and p-ERK1/2 and blocked nuclear translocation of NF-κB p65. The results indicate that TSM exerts anti-inflammatory effects related with inhibition on NF-κB and MAPK (p-ERK1/2) signaling pathways. In conclusion, our data demonstrate that TSM might be a potential agent for the treatment of ALI.

Keywords

Viola tianshanica Maxim, acute lung injury, anti-inflammation effect

References

  1. Yang J, Qu JM, Summah H, Zhang J, Zhu YG, Jiang HN. 2010. Protective effects of imipramine in murine endotoxin induced acute lung injury. Eur. J. Pharmacol. 638: 128-133.
    Pubmed CrossRef
  2. Bhatia M, Moochhala S. 2004. Role of inflammatory mediators in the pathophysiology of acute respiratory distress syndrome. J. Pathol. 202: 145-156.
    Pubmed CrossRef
  3. Ware LB, Matthay MA. 2000. The acute respiratory distress syndrome. N. Engl. J. Med. 342: 1334-1349.
    Pubmed CrossRef
  4. Chu X, Song K, Xu K, Zhang X, Song Y, Wang D, et al. 2010. Ceftiofur attenuates lipopolysaccharide-induced acute lung injury. Int. Immunopharmacol. 10: 600-604.
    Pubmed CrossRef
  5. Chen H , Bai C, Wang X. 2010. The value o f the lipopolysaccharide-induced acute lung injury model in respiratory medicine. Expert Rev Respir. Med. 4: 773-783.
    Pubmed CrossRef
  6. Wang G, Huang X, Li Y, Guo K, Ning P, Zhang Y. 2013. PARP-1 inhibitor, DPQ, attenuates LPS-induced acute lung injury through inhibiting NF-κB-mediated inflammatory response. PLoS One 8: e79757.
    Pubmed PMC CrossRef
  7. Liu YM. 1999. Pharmacography of Uighur, Part 1, pp. 35-37. Xinjiang Science & Technology & Hygiene Publishing House, Urumuqi, China.
  8. Chinese Pharmacopoeia Commission of Sanitary Ministry of People’s Republic of China. 2010. Chinese Pharmacopoeia, Part 1. Chemical Industry Publishing House, Beijing, China.
  9. Kim YW, Zhao RJ, Park SJ, Lee JR, Cho IJ, Yang CH, et al. 2008. Anti-inflammatory effects of liquiritigenin as a consequence of the inhibition of NF-κB-dependent iNOS and proinflammatory cytokines production. Br. J. Pharmacol. 154: 165-173.
    Pubmed PMC CrossRef
  10. Xie C, Kang J, Li Z, Schauss AG, Badger TM, Nagarajan S, et al. 2012. The acai flavonoid velutin is a potent antiinflammatory agent: blockade of LPS-mediated TNF-α and IL-6 production through inhibiting NF-κB activation and MAPK pathway. J. Nutr. Biochem. 23: 1184-1191.
    Pubmed CrossRef
  11. Kim KS, Cui X, Lee DS, Ko W, Sohn JH, Yim JH, et al. 2014. Inhibitory effects of benzaldehyde derivatives from the marine fungus Eurotium sp. SF-5989 on inflammatory mediators via the induction of heme oxygenase-1 in lipopolysaccharide-stimulated RAW264.7 macrophages. Int. J. Mol. Sci. 15: 23749-23765.
    Pubmed PMC CrossRef
  12. Kim KH, Kim DH, Jeong N, Kim KI, Kim YH, Lee M, et al. 2013. Therapeutic effect of Chung-Pae, an experimental herbal formula, on acute lung inflammation is associated with suppression of NF-κB and activation of Nrf2. Evid. Based Complement. Alternat. Med. 2013: 1-11.
    CrossRef
  13. von Bismarck P, Klemm K, Garcia Wistadt CF, Winoto MS, Schutze S, Krause MF. 2009. Selective NF-κB inhibition, but not dexamethasone, decreases acute lung injury in a newborn piglet airway inflammation model. Pulm. Pharmacol. Ther. 22: 297-304.
    Pubmed CrossRef
  14. Meduri GU, Tolley EA, Chrousos GP, Stentz F. 2002. Prolonged methylprednisolone treatment suppresses systemic inflammation in patients with unresolving acute respiratory distress syndrome: evidence for inadequate endogenous glucocorticoid secretion and inflammation-induced immune cell resistance to glucocorticoids. Am. J. Respir. Crit. Care Med. 165: 983-991.
    Pubmed CrossRef
  15. San Z, Fu Y, Li W, Zhou E, Li Y, Song X, et al. 2014. Protective effect of taraxasterol on acute lung injury induced by lipopolysaccharide in mice. Int. Immunopharmacol. 19: 342-350.
    Pubmed CrossRef
  16. Kalyan KG, Dhamotharan R, Kulkarni NM, Mahat MY, Gunasekaran J, Ashfaque M. 2011. Embelin reduces cutaneous TNF-α level and ameliorates skin edema in acute and chronic model of skin inflammation in mice. Eur. J. Pharmacol. 662: 63-69.
    Pubmed CrossRef
  17. Tureyen K, Bowen K, Liang J, Dempsey RJ, Vemuganti R. 2011. Exacerbated brain damage, edema and inflammation in type-2 diabetic mice subjected to focal ischemia. J. Neurochem. 116: 499-507.
    Pubmed PMC CrossRef
  18. Aderem A, Ulevitch RJ. 2000. Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
    Pubmed CrossRef
  19. Nantel F, Denis D, Gordon R, Northey A, Cirino M, Metters KM, Chan CC. 1999. Distribution and regulation of cyclooxygenase-2 in carrageenan-induced inflammation. Br. J. Pharmacol. 128: 853-859.
    Pubmed PMC CrossRef
  20. Moynagh PN. 2005. The NF-κB pathway. J. Cell Sci. 118: 4589-4592.
    Pubmed CrossRef
  21. Goodman RB, Pugin J, Lee JS, Matthay MA. 2003. Cytokinemediated inflammation in acute lung injury. Cytokine Growth Factor Rev. 14: 523-535.
    CrossRef
  22. Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E. 2004. Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-κB. J. Immunol. 172: 2522-2529.
    Pubmed CrossRef
  23. Chen X, Zhang S, Xuan Z, Ge D, Chen X, Zhang J, et al. 2017. The phenolic fraction of Mentha haplocalyx and its constituent linarin ameliorate inflammatory response through inactivation of NF-κB and MAPKs in lipopolysaccharideinduced RAW264.7 cells. Molecules 22: 811.
    Pubmed CrossRef
  24. Guan F, Wang H, Shan Y, Chen Y, Wang M, Wang Q, et al. 2014. Inhibition o f COX-2 a nd P GE2 in LPS-stimulated RAW264.7 cells by lonimacranthoide VI, achlorogenic acid ester saponin. Biomed. Rep. 2: 760-764.
    Pubmed PMC CrossRef
  25. Bose S, Kar N, Maitra R, DiDonato JA, Banerjee AK. 2003. Temporal activation of NF-κB regulates an interferon independent innate antiviral response against cytoplasmic RNA viruses. Proc. Natl. Acad. Sci. USA 100: 10890-10895.
    Pubmed PMC CrossRef
  26. Chen F, Kuhn DC, Sun SC, Gaydos LJ, Demers LM. 1995. Dependence and reversal of nitric oxide production on NF-κB in silica and lipopolysaccharide-induced macrophages.Biochem. Biophys. Res. Commun. 214: 839-846.
    Pubmed CrossRef
  27. Jimi E , Ghosh S. 2005. Role of n uclear f actor-κB in the immune system and bone. Immunol. Rev. 208: 80-87.
    Pubmed CrossRef
  28. Sohn KH, Jo MJ, Cho WJ, Lee JR, Cho IJ, Kim SC, et al. 2012. Bojesodok-eum, a herbal prescription, ameliorates acute inflammation in association with the inhibition of NFκB-mediated nitric oxide and proinflammatory cytokine production. Evid. Based Complement. Alternat. Med. 2012: 1-12.
    Pubmed PMC CrossRef
  29. Jiang JX, Zhang Y, Ji SH, Zhu P, Wang ZG. 2002. Kinetics of mitogen-activated protein kinase family in lipopolysaccharidestimulated mouse Kupffer cells and their role in cytokine production. Shock 18: 336-341.
    Pubmed CrossRef
  30. Bondeson J. 1997. The mechanisms of action of diseasemodifying antirheumatic drugs: a review with emphasis on macrophage signal transduction and the induction of proinflammatory cytokines. Gen. Pharmacol. 29: 127-150.
    CrossRef
  31. Choi K, Kim M, Ryu J, Choi C. 2007. Ginsenosides compound K and Rh(2) inhibit tumor necrosis factor-alpha-induced activation of the NF-kappaB and JNK pathways in human astroglial cells. Neurosci. Lett. 421: 37-41.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(9): 1628-1638

Published online September 28, 2017 https://doi.org/10.4014/jmb.1701.01067

Copyright © The Korean Society for Microbiology and Biotechnology.

Protective Effects of the Ethanol Extract of Viola tianshanica Maxim against Acute Lung Injury Induced by Lipopolysaccharides in Mice

Xue Wang 1, Qiao-Li Yang 1, Yu-Zhu Shi 1, Bi-Yu Hou 2, Sheng-Qian Yang 2, Hua Huang 1, Li Zhang 2 and Guan-Hua Du 2*

1Xinjiang Key Laboratory for Uighur Medicine, Xinjiang Institute of Materia Medica, Urumqi 830004, P.R. China, 2Beijing Key Laboratory of Drug Target Identification and Drug Screening, Institute of Materia Medica, Chinese Academy of Medical Sciences, Beijing 100050, P.R. China

Received: January 26, 2017; Accepted: July 28, 2017

Abstract

Viola tianshanica Maxim, belonging to the Violaceae plant family, is traditionally used in
Uighur medicine for treating pneumonia, headache, and fever. There is, however, a lack of
basic understanding of its pharmacological activities. This study was designed to observe the
effects of the ethanol extract (TSM) from Viola tianshanica Maxim on the inflammation
response in acute lung injury (ALI) induced by LPS and the possible underlying mechanisms.
We found that TSM (200 and 500 mg/kg) significantly decreased inflammatory cytokine
production and the number of inflammatory cells, including macrophages and neutrophils, in
bronchoalveolar lavage fluid. TSM also markedly inhibited the lung wet-to-dry ratio and
alleviated pathological changes in lung tissues. In vitro, after TSM (12.5-100 μg/ml) treatment
to RAW 264.7 cells for 1 h, LPS (1 μg/ml) was added and the cells were further incubated for
24 h. TSM dose-dependently inhibited the levels of proinflammatory cytokines, such as NO,
PGE2, TNF-α, IL-6, and IL-1β, and remarkably decreased the protein and mRNA expression of
TNF-α and IL-6 in LPS-stimulated RAW 264.7 cells. TSM also suppressed protein expression
of p-IκBa and p-ERK1/2 and blocked nuclear translocation of NF-κB p65. The results indicate
that TSM exerts anti-inflammatory effects related with inhibition on NF-κB and MAPK
(p-ERK1/2) signaling pathways. In conclusion, our data demonstrate that TSM might be a
potential agent for the treatment of ALI.

Keywords: Viola tianshanica Maxim, acute lung injury, anti-inflammation effect

References

  1. Yang J, Qu JM, Summah H, Zhang J, Zhu YG, Jiang HN. 2010. Protective effects of imipramine in murine endotoxin induced acute lung injury. Eur. J. Pharmacol. 638: 128-133.
    Pubmed CrossRef
  2. Bhatia M, Moochhala S. 2004. Role of inflammatory mediators in the pathophysiology of acute respiratory distress syndrome. J. Pathol. 202: 145-156.
    Pubmed CrossRef
  3. Ware LB, Matthay MA. 2000. The acute respiratory distress syndrome. N. Engl. J. Med. 342: 1334-1349.
    Pubmed CrossRef
  4. Chu X, Song K, Xu K, Zhang X, Song Y, Wang D, et al. 2010. Ceftiofur attenuates lipopolysaccharide-induced acute lung injury. Int. Immunopharmacol. 10: 600-604.
    Pubmed CrossRef
  5. Chen H , Bai C, Wang X. 2010. The value o f the lipopolysaccharide-induced acute lung injury model in respiratory medicine. Expert Rev Respir. Med. 4: 773-783.
    Pubmed CrossRef
  6. Wang G, Huang X, Li Y, Guo K, Ning P, Zhang Y. 2013. PARP-1 inhibitor, DPQ, attenuates LPS-induced acute lung injury through inhibiting NF-κB-mediated inflammatory response. PLoS One 8: e79757.
    Pubmed KoreaMed CrossRef
  7. Liu YM. 1999. Pharmacography of Uighur, Part 1, pp. 35-37. Xinjiang Science & Technology & Hygiene Publishing House, Urumuqi, China.
  8. Chinese Pharmacopoeia Commission of Sanitary Ministry of People’s Republic of China. 2010. Chinese Pharmacopoeia, Part 1. Chemical Industry Publishing House, Beijing, China.
  9. Kim YW, Zhao RJ, Park SJ, Lee JR, Cho IJ, Yang CH, et al. 2008. Anti-inflammatory effects of liquiritigenin as a consequence of the inhibition of NF-κB-dependent iNOS and proinflammatory cytokines production. Br. J. Pharmacol. 154: 165-173.
    Pubmed KoreaMed CrossRef
  10. Xie C, Kang J, Li Z, Schauss AG, Badger TM, Nagarajan S, et al. 2012. The acai flavonoid velutin is a potent antiinflammatory agent: blockade of LPS-mediated TNF-α and IL-6 production through inhibiting NF-κB activation and MAPK pathway. J. Nutr. Biochem. 23: 1184-1191.
    Pubmed CrossRef
  11. Kim KS, Cui X, Lee DS, Ko W, Sohn JH, Yim JH, et al. 2014. Inhibitory effects of benzaldehyde derivatives from the marine fungus Eurotium sp. SF-5989 on inflammatory mediators via the induction of heme oxygenase-1 in lipopolysaccharide-stimulated RAW264.7 macrophages. Int. J. Mol. Sci. 15: 23749-23765.
    Pubmed KoreaMed CrossRef
  12. Kim KH, Kim DH, Jeong N, Kim KI, Kim YH, Lee M, et al. 2013. Therapeutic effect of Chung-Pae, an experimental herbal formula, on acute lung inflammation is associated with suppression of NF-κB and activation of Nrf2. Evid. Based Complement. Alternat. Med. 2013: 1-11.
    CrossRef
  13. von Bismarck P, Klemm K, Garcia Wistadt CF, Winoto MS, Schutze S, Krause MF. 2009. Selective NF-κB inhibition, but not dexamethasone, decreases acute lung injury in a newborn piglet airway inflammation model. Pulm. Pharmacol. Ther. 22: 297-304.
    Pubmed CrossRef
  14. Meduri GU, Tolley EA, Chrousos GP, Stentz F. 2002. Prolonged methylprednisolone treatment suppresses systemic inflammation in patients with unresolving acute respiratory distress syndrome: evidence for inadequate endogenous glucocorticoid secretion and inflammation-induced immune cell resistance to glucocorticoids. Am. J. Respir. Crit. Care Med. 165: 983-991.
    Pubmed CrossRef
  15. San Z, Fu Y, Li W, Zhou E, Li Y, Song X, et al. 2014. Protective effect of taraxasterol on acute lung injury induced by lipopolysaccharide in mice. Int. Immunopharmacol. 19: 342-350.
    Pubmed CrossRef
  16. Kalyan KG, Dhamotharan R, Kulkarni NM, Mahat MY, Gunasekaran J, Ashfaque M. 2011. Embelin reduces cutaneous TNF-α level and ameliorates skin edema in acute and chronic model of skin inflammation in mice. Eur. J. Pharmacol. 662: 63-69.
    Pubmed CrossRef
  17. Tureyen K, Bowen K, Liang J, Dempsey RJ, Vemuganti R. 2011. Exacerbated brain damage, edema and inflammation in type-2 diabetic mice subjected to focal ischemia. J. Neurochem. 116: 499-507.
    Pubmed KoreaMed CrossRef
  18. Aderem A, Ulevitch RJ. 2000. Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
    Pubmed CrossRef
  19. Nantel F, Denis D, Gordon R, Northey A, Cirino M, Metters KM, Chan CC. 1999. Distribution and regulation of cyclooxygenase-2 in carrageenan-induced inflammation. Br. J. Pharmacol. 128: 853-859.
    Pubmed KoreaMed CrossRef
  20. Moynagh PN. 2005. The NF-κB pathway. J. Cell Sci. 118: 4589-4592.
    Pubmed CrossRef
  21. Goodman RB, Pugin J, Lee JS, Matthay MA. 2003. Cytokinemediated inflammation in acute lung injury. Cytokine Growth Factor Rev. 14: 523-535.
    CrossRef
  22. Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E. 2004. Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-κB. J. Immunol. 172: 2522-2529.
    Pubmed CrossRef
  23. Chen X, Zhang S, Xuan Z, Ge D, Chen X, Zhang J, et al. 2017. The phenolic fraction of Mentha haplocalyx and its constituent linarin ameliorate inflammatory response through inactivation of NF-κB and MAPKs in lipopolysaccharideinduced RAW264.7 cells. Molecules 22: 811.
    Pubmed CrossRef
  24. Guan F, Wang H, Shan Y, Chen Y, Wang M, Wang Q, et al. 2014. Inhibition o f COX-2 a nd P GE2 in LPS-stimulated RAW264.7 cells by lonimacranthoide VI, achlorogenic acid ester saponin. Biomed. Rep. 2: 760-764.
    Pubmed KoreaMed CrossRef
  25. Bose S, Kar N, Maitra R, DiDonato JA, Banerjee AK. 2003. Temporal activation of NF-κB regulates an interferon independent innate antiviral response against cytoplasmic RNA viruses. Proc. Natl. Acad. Sci. USA 100: 10890-10895.
    Pubmed KoreaMed CrossRef
  26. Chen F, Kuhn DC, Sun SC, Gaydos LJ, Demers LM. 1995. Dependence and reversal of nitric oxide production on NF-κB in silica and lipopolysaccharide-induced macrophages.Biochem. Biophys. Res. Commun. 214: 839-846.
    Pubmed CrossRef
  27. Jimi E , Ghosh S. 2005. Role of n uclear f actor-κB in the immune system and bone. Immunol. Rev. 208: 80-87.
    Pubmed CrossRef
  28. Sohn KH, Jo MJ, Cho WJ, Lee JR, Cho IJ, Kim SC, et al. 2012. Bojesodok-eum, a herbal prescription, ameliorates acute inflammation in association with the inhibition of NFκB-mediated nitric oxide and proinflammatory cytokine production. Evid. Based Complement. Alternat. Med. 2012: 1-12.
    Pubmed KoreaMed CrossRef
  29. Jiang JX, Zhang Y, Ji SH, Zhu P, Wang ZG. 2002. Kinetics of mitogen-activated protein kinase family in lipopolysaccharidestimulated mouse Kupffer cells and their role in cytokine production. Shock 18: 336-341.
    Pubmed CrossRef
  30. Bondeson J. 1997. The mechanisms of action of diseasemodifying antirheumatic drugs: a review with emphasis on macrophage signal transduction and the induction of proinflammatory cytokines. Gen. Pharmacol. 29: 127-150.
    CrossRef
  31. Choi K, Kim M, Ryu J, Choi C. 2007. Ginsenosides compound K and Rh(2) inhibit tumor necrosis factor-alpha-induced activation of the NF-kappaB and JNK pathways in human astroglial cells. Neurosci. Lett. 421: 37-41.
    Pubmed CrossRef