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Published in: BMC Complementary Medicine and Therapies 1/2018

Open Access 01-12-2018 | Research article

Corylin inhibits LPS-induced inflammatory response and attenuates the activation of NLRP3 inflammasome in microglia

Authors: Ming-Yii Huang, Chia-En Tu, Shu-Chi Wang, Yung-Li Hung, Chia-Cheng Su, Shih-Hua Fang, Chi-Shuo Chen, Po-Len Liu, Wei-Chung Cheng, Yu-Wei Huang, Chia-Yang Li

Published in: BMC Complementary Medicine and Therapies | Issue 1/2018

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Abstract

Background

Inflammation has been found to be associated with many neurodegenerative diseases, including Parkinson’s and dementia. Attenuation of microglia-induced inflammation is a strategy that impedes the progression of neurodegenerative diseases.

Methods

We used lipopolysaccharide (LPS) to simulate murine microglia cells (BV2 cells) as an experimental model to mimic the inflammatory environment in the brain. In addition, we examined the anti-inflammatory ability of corylin, a main compound isolated from Psoralea corylifolia L. that is commonly used in Chinese herbal medicine. The production of nitric oxide (NO) by LPS-activated BV2 cells was measured using Griess reaction. The secretion of proinflammatory cytokines including tumor necrosis factor (TNF-α), interleukin-1β (IL-1β) and interleukin-6 (IL-6) by LPS-activated BV2 cells was analyzed using enzyme-linked immunosorbent assay (ELISA). The expression of inducible NO synthase (iNOS), cyclooxygenase-2 (COX-2), nucleotide-binding oligomerization domain-like receptor containing pyrin domain 3 (NLRP3), apoptosis-associated speck-like protein containing a caspase-activation and recruitment domain (ASC), caspase-1, IL-1β and mitogen-activated protein kinases (MAPKs) in LPS-activated BV2 cells was examined by Western blot.

Results

Our experimental results demonstrated that corylin suppressed the production of NO and proinflammatory cytokines by LPS-activated BV2 cells. In addition, corylin inhibited the expression of iNOS and COX-2, attenuated the phosphorylation of ERK, JNK and p38, decreased the expression of NLRP3 and ASC, and repressed the activation of caspase-1 and IL-1β by LPS-activated BV2 cells.

Conclusion

Our results indicate the anti-inflammatory effects of corylin acted through attenuating LPS-induced inflammation and inhibiting the activation of NLRP3 inflammasome in LPS-activated BV2 cells. These results suggest that corylin might have potential in treating brain inflammation and attenuating the progression of neurodegeneration diseases.
Literature
3.
go back to reference Lee KW, Jung SY, Choi SM, Yang EJ. Effects of ginsenoside re on LPS-induced inflammatory mediators in BV2 microglial cells. BMC Complement Altern Med. 2012;12:196.CrossRefPubMedPubMedCentral Lee KW, Jung SY, Choi SM, Yang EJ. Effects of ginsenoside re on LPS-induced inflammatory mediators in BV2 microglial cells. BMC Complement Altern Med. 2012;12:196.CrossRefPubMedPubMedCentral
4.
go back to reference Kempuraj D, Thangavel R, Natteru PA, Selvakumar GP, Saeed D, Zahoor H, Zaheer S, Iyer SS, Zaheer A. Neuroinflammation Induces Neurodegeneration. J Neurol Neurosurg Spine. 2016;1(1):1003.PubMedPubMedCentral Kempuraj D, Thangavel R, Natteru PA, Selvakumar GP, Saeed D, Zahoor H, Zaheer S, Iyer SS, Zaheer A. Neuroinflammation Induces Neurodegeneration. J Neurol Neurosurg Spine. 2016;1(1):1003.PubMedPubMedCentral
5.
go back to reference Kumagai N, Chiba Y, Hosono M, Fujii M, Kawamura N, Keino H, Yoshikawa K, Ishii S, Saitoh Y, Satoh M, et al. Involvement of pro-inflammatory cytokines and microglia in an age-associated neurodegeneration model, the SAMP10 mouse. Brain Res. 2007;1185:75–85.CrossRefPubMed Kumagai N, Chiba Y, Hosono M, Fujii M, Kawamura N, Keino H, Yoshikawa K, Ishii S, Saitoh Y, Satoh M, et al. Involvement of pro-inflammatory cytokines and microglia in an age-associated neurodegeneration model, the SAMP10 mouse. Brain Res. 2007;1185:75–85.CrossRefPubMed
6.
go back to reference Liberatore GT, Jackson-Lewis V, Vukosavic S, Mandir AS, Vila M, McAuliffe WG, Dawson VL, Dawson TM, Przedborski S. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med. 1999;5(12):1403–9.CrossRefPubMed Liberatore GT, Jackson-Lewis V, Vukosavic S, Mandir AS, Vila M, McAuliffe WG, Dawson VL, Dawson TM, Przedborski S. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat Med. 1999;5(12):1403–9.CrossRefPubMed
7.
go back to reference Bruccoleri A, Harry GJ. Chemical-induced hippocampal neurodegeneration and elevations in TNFalpha, TNFbeta, IL-1alpha, IP-10, and MCP-1 mRNA in osteopetrotic (op/op) mice. J Neurosci Res. 2000;62(1):146–55.CrossRefPubMed Bruccoleri A, Harry GJ. Chemical-induced hippocampal neurodegeneration and elevations in TNFalpha, TNFbeta, IL-1alpha, IP-10, and MCP-1 mRNA in osteopetrotic (op/op) mice. J Neurosci Res. 2000;62(1):146–55.CrossRefPubMed
8.
go back to reference Reed-Geaghan EG, Savage JC, Hise AG, Landreth GE. CD14 and toll-like receptors 2 and 4 are required for fibrillar A{beta}-stimulated microglial activation. J Neurosci. 2009;29(38):11982–92.CrossRefPubMedPubMedCentral Reed-Geaghan EG, Savage JC, Hise AG, Landreth GE. CD14 and toll-like receptors 2 and 4 are required for fibrillar A{beta}-stimulated microglial activation. J Neurosci. 2009;29(38):11982–92.CrossRefPubMedPubMedCentral
9.
go back to reference Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T. Activation of innate immunity in the CNS triggers neurodegeneration through a toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A. 2003;100(14):8514–9.CrossRefPubMedPubMedCentral Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T. Activation of innate immunity in the CNS triggers neurodegeneration through a toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A. 2003;100(14):8514–9.CrossRefPubMedPubMedCentral
10.
go back to reference Lehnardt S, Schott E, Trimbuch T, Laubisch D, Krueger C, Wulczyn G, Nitsch R, Weber JR. A vicious cycle involving release of heat shock protein 60 from injured cells and activation of toll-like receptor 4 mediates neurodegeneration in the CNS. J Neurosci. 2008;28(10):2320–31.CrossRefPubMed Lehnardt S, Schott E, Trimbuch T, Laubisch D, Krueger C, Wulczyn G, Nitsch R, Weber JR. A vicious cycle involving release of heat shock protein 60 from injured cells and activation of toll-like receptor 4 mediates neurodegeneration in the CNS. J Neurosci. 2008;28(10):2320–31.CrossRefPubMed
11.
go back to reference Huang NQ, Jin H, Zhou SY, Shi JS, Jin F. TLR4 is a link between diabetes and Alzheimer’s disease. Behav Brain Res. 2017;316:234–44.CrossRefPubMed Huang NQ, Jin H, Zhou SY, Shi JS, Jin F. TLR4 is a link between diabetes and Alzheimer’s disease. Behav Brain Res. 2017;316:234–44.CrossRefPubMed
12.
go back to reference Zhao XD, Wang FX, Cao WF, Zhang YH, Li Y. TLR4 signaling mediates AP-1 activation in an MPTP-induced mouse model of Parkinson's disease. Int Immunopharmacol. 2016;32:96–102.CrossRefPubMed Zhao XD, Wang FX, Cao WF, Zhang YH, Li Y. TLR4 signaling mediates AP-1 activation in an MPTP-induced mouse model of Parkinson's disease. Int Immunopharmacol. 2016;32:96–102.CrossRefPubMed
14.
go back to reference Roy A, Srivastava M, Saqib U, Liu D, Faisal SM, Sugathan S, Bishnoi S, Baig MS. Potential therapeutic targets for inflammation in toll-like receptor 4 (TLR4)-mediated signaling pathways. Int Immunopharmacol. 2016;40:79–89.CrossRefPubMed Roy A, Srivastava M, Saqib U, Liu D, Faisal SM, Sugathan S, Bishnoi S, Baig MS. Potential therapeutic targets for inflammation in toll-like receptor 4 (TLR4)-mediated signaling pathways. Int Immunopharmacol. 2016;40:79–89.CrossRefPubMed
15.
go back to reference Murakami A, Ohigashi H. Targeting NOX, INOS and COX-2 in inflammatory cells: chemoprevention using food phytochemicals. Int J Cancer. 2007;121(11):2357–63.CrossRefPubMed Murakami A, Ohigashi H. Targeting NOX, INOS and COX-2 in inflammatory cells: chemoprevention using food phytochemicals. Int J Cancer. 2007;121(11):2357–63.CrossRefPubMed
16.
go back to reference Rahimifard M, Maqbool F, Moeini-Nodeh S, Niaz K, Abdollahi M, Braidy N, Nabavi SM, Nabavi SF. Targeting the TLR4 signaling pathway by polyphenols: a novel therapeutic strategy for neuroinflammation. Ageing Res Rev. 2017;36:11–9.CrossRefPubMed Rahimifard M, Maqbool F, Moeini-Nodeh S, Niaz K, Abdollahi M, Braidy N, Nabavi SM, Nabavi SF. Targeting the TLR4 signaling pathway by polyphenols: a novel therapeutic strategy for neuroinflammation. Ageing Res Rev. 2017;36:11–9.CrossRefPubMed
18.
go back to reference Bian F, Xiao Y, Zaheer M, Volpe EA, Pflugfelder SC, Li DQ, de Paiva CS. Inhibition of NLRP3 Inflammasome pathway by butyrate improves corneal wound healing in corneal alkali burn. Int J Mol Sci. 2017;18(3). Bian F, Xiao Y, Zaheer M, Volpe EA, Pflugfelder SC, Li DQ, de Paiva CS. Inhibition of NLRP3 Inflammasome pathway by butyrate improves corneal wound healing in corneal alkali burn. Int J Mol Sci. 2017;18(3).
19.
go back to reference Tan MS, Yu JT, Jiang T, Zhu XC, Tan L. The NLRP3 inflammasome in Alzheimer's disease. Mol Neurobiol. 2013;48(3):875–82.CrossRefPubMed Tan MS, Yu JT, Jiang T, Zhu XC, Tan L. The NLRP3 inflammasome in Alzheimer's disease. Mol Neurobiol. 2013;48(3):875–82.CrossRefPubMed
20.
go back to reference Yang JW, Yang SJ, Na JM, Hahn HG, Cho SW. 3-(Naphthalen-2-yl(propoxy)methyl)azetidine hydrochloride attenuates NLRP3 inflammasome-mediated signaling pathway in lipopolysaccharide-stimulated BV2 microglial cells. Biochem Biophys Res Commun. 2018;495(1):151–6.CrossRefPubMed Yang JW, Yang SJ, Na JM, Hahn HG, Cho SW. 3-(Naphthalen-2-yl(propoxy)methyl)azetidine hydrochloride attenuates NLRP3 inflammasome-mediated signaling pathway in lipopolysaccharide-stimulated BV2 microglial cells. Biochem Biophys Res Commun. 2018;495(1):151–6.CrossRefPubMed
21.
go back to reference Pan MH, Lai CS, Ho CT. Anti-inflammatory activity of natural dietary flavonoids. Food Funct. 2010;1(1):15–31.CrossRefPubMed Pan MH, Lai CS, Ho CT. Anti-inflammatory activity of natural dietary flavonoids. Food Funct. 2010;1(1):15–31.CrossRefPubMed
22.
go back to reference Leyva-Lopez N, Gutierrez-Grijalva EP, Ambriz-Perez DL, Heredia JB. Flavonoids as cytokine modulators: a possible therapy for inflammation-related diseases. Int J Mol Sci. 2016;17(6). Leyva-Lopez N, Gutierrez-Grijalva EP, Ambriz-Perez DL, Heredia JB. Flavonoids as cytokine modulators: a possible therapy for inflammation-related diseases. Int J Mol Sci. 2016;17(6).
23.
go back to reference Qin Z, Li S, Yao Z, Hong X, Xu J, Lin P, Zhao G, Gonzalez FJ, Yao X. Metabolic profiling of corylin in vivo and in vitro. J Pharm Biomed Anal. 2018;155:157–68.CrossRefPubMed Qin Z, Li S, Yao Z, Hong X, Xu J, Lin P, Zhao G, Gonzalez FJ, Yao X. Metabolic profiling of corylin in vivo and in vitro. J Pharm Biomed Anal. 2018;155:157–68.CrossRefPubMed
24.
go back to reference Chopra B, Dhingra AK, Dhar KL. Psoralea corylifolia L. (Buguchi) - folklore to modern evidence: review. Fitoterapia. 2013;90:44–56.CrossRefPubMed Chopra B, Dhingra AK, Dhar KL. Psoralea corylifolia L. (Buguchi) - folklore to modern evidence: review. Fitoterapia. 2013;90:44–56.CrossRefPubMed
25.
go back to reference Chen CC, Chen CY, Ueng SH, Hsueh C, Yeh CT, Ho JY, Chou LF, Wang TH. Corylin increases the sensitivity of hepatocellular carcinoma cells to chemotherapy through long noncoding RNA RAD51-AS1-mediated inhibition of DNA repair. Cell Death Dis. 2018;9(5):543.CrossRefPubMedPubMedCentral Chen CC, Chen CY, Ueng SH, Hsueh C, Yeh CT, Ho JY, Chou LF, Wang TH. Corylin increases the sensitivity of hepatocellular carcinoma cells to chemotherapy through long noncoding RNA RAD51-AS1-mediated inhibition of DNA repair. Cell Death Dis. 2018;9(5):543.CrossRefPubMedPubMedCentral
26.
go back to reference Chen CY, Chen CC, Shieh TM, Hsueh C, Wang SH, Leu YL, Lian JH, Wang TH. Corylin suppresses hepatocellular carcinoma progression via the inhibition of epithelial-Mesenchymal transition, mediated by long noncoding RNA GAS5. Int J Mol Sci. 2018;19(2). Chen CY, Chen CC, Shieh TM, Hsueh C, Wang SH, Leu YL, Lian JH, Wang TH. Corylin suppresses hepatocellular carcinoma progression via the inhibition of epithelial-Mesenchymal transition, mediated by long noncoding RNA GAS5. Int J Mol Sci. 2018;19(2).
27.
go back to reference Lee SW, Yun BR, Kim MH, Park CS, Lee WS, Oh HM, Rho MC. Phenolic compounds isolated from Psoralea corylifolia inhibit IL-6-induced STAT3 activation. Planta Med. 2012;78(9):903–6.CrossRefPubMed Lee SW, Yun BR, Kim MH, Park CS, Lee WS, Oh HM, Rho MC. Phenolic compounds isolated from Psoralea corylifolia inhibit IL-6-induced STAT3 activation. Planta Med. 2012;78(9):903–6.CrossRefPubMed
28.
go back to reference Hung YL, Fang SH, Wang SC, Cheng WC, Liu PL, Su CC, Chen CS, Huang MY, Hua KF, Shen KH, et al. Corylin protects LPS-induced sepsis and attenuates LPS-induced inflammatory response. Sci Rep. 2017;7:46299.CrossRefPubMedPubMedCentral Hung YL, Fang SH, Wang SC, Cheng WC, Liu PL, Su CC, Chen CS, Huang MY, Hua KF, Shen KH, et al. Corylin protects LPS-induced sepsis and attenuates LPS-induced inflammatory response. Sci Rep. 2017;7:46299.CrossRefPubMedPubMedCentral
29.
go back to reference Kim EK, Choi EJ. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta. 2010;1802(4):396–405.CrossRefPubMed Kim EK, Choi EJ. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta. 2010;1802(4):396–405.CrossRefPubMed
30.
go back to reference Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol. 2009;27:519–50.CrossRefPubMed Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol. 2009;27:519–50.CrossRefPubMed
31.
go back to reference Song L, Pei L, Yao S, Wu Y, Shang Y. NLRP3 Inflammasome in neurological diseases, from functions to therapies. Front Cell Neurosci. 2017;11:63.PubMedPubMedCentral Song L, Pei L, Yao S, Wu Y, Shang Y. NLRP3 Inflammasome in neurological diseases, from functions to therapies. Front Cell Neurosci. 2017;11:63.PubMedPubMedCentral
32.
go back to reference Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8(1):57–69.CrossRefPubMed Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8(1):57–69.CrossRefPubMed
34.
go back to reference Andreasson K. Emerging roles of PGE2 receptors in models of neurological disease. Prostaglandins Other Lipid Mediat. 2010;91(3–4):104–12.CrossRefPubMed Andreasson K. Emerging roles of PGE2 receptors in models of neurological disease. Prostaglandins Other Lipid Mediat. 2010;91(3–4):104–12.CrossRefPubMed
35.
go back to reference Ryan JC, Cross CA, Van Dolah FM. Effects of COX inhibitors on neurodegeneration and survival in mice exposed to the marine neurotoxin domoic acid. Neurosci Lett. 2011;487(1):83–7.CrossRefPubMed Ryan JC, Cross CA, Van Dolah FM. Effects of COX inhibitors on neurodegeneration and survival in mice exposed to the marine neurotoxin domoic acid. Neurosci Lett. 2011;487(1):83–7.CrossRefPubMed
36.
go back to reference Consonni A, Morara S, Codazzi F, Grohovaz F, Zacchetti D. Inhibition of lipopolysaccharide-induced microglia activation by calcitonin gene related peptide and adrenomedullin. Mol Cell Neurosci. 2011;48(2):151–60.CrossRefPubMedPubMedCentral Consonni A, Morara S, Codazzi F, Grohovaz F, Zacchetti D. Inhibition of lipopolysaccharide-induced microglia activation by calcitonin gene related peptide and adrenomedullin. Mol Cell Neurosci. 2011;48(2):151–60.CrossRefPubMedPubMedCentral
37.
go back to reference Scheiblich H, Schlutter A, Golenbock DT, Latz E, Martinez-Martinez P, Heneka MT. Activation of the NLRP3 inflammasome in microglia: the role of ceramide. J Neurochem. 2017;143(5):534–50.CrossRefPubMed Scheiblich H, Schlutter A, Golenbock DT, Latz E, Martinez-Martinez P, Heneka MT. Activation of the NLRP3 inflammasome in microglia: the role of ceramide. J Neurochem. 2017;143(5):534–50.CrossRefPubMed
Metadata
Title
Corylin inhibits LPS-induced inflammatory response and attenuates the activation of NLRP3 inflammasome in microglia
Authors
Ming-Yii Huang
Chia-En Tu
Shu-Chi Wang
Yung-Li Hung
Chia-Cheng Su
Shih-Hua Fang
Chi-Shuo Chen
Po-Len Liu
Wei-Chung Cheng
Yu-Wei Huang
Chia-Yang Li
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2018
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-018-2287-5

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