L-F001, a novel multifunctional ROCK inhibitor, suppresses neuroinflammation in vitro and in vivo: Involvement of NF-κB inhibition and Nrf2 pathway activation

European Journal of Pharmacology

Volumn 806, Issue , 2017, Pages 1-9

  Chen, Jingkao ^a,b,c   Yin, Wei ^c   Tu, Yalin ^a,b   Wang, Shengnan ^a,b   Yang, Xiaohong ^a,b   Chen, Qiuhe ^a,b   Zhang, Xiao ^a,d   Han, Yifan ^b,e   Pi, Rongbiao ^a,b,c  

^a SUN YAT SEN UNIVERSITY   (China)

^b International Joint Laboratory (SYSU PolyU HK) of Novel Anti Dementia Drugs of Guangdong   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

^e HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

Author keywords

Astrocytes; Inflammation; Microglia; NF B; Nrf2 pathway; ROCK inhibitor

Indexed keywords

CD16 ANTIGEN; CD206 ANTIGEN; CD32 ANTIGEN; CYCLOOXYGENASE 2; FASUDIL; GLUTAMATE CYSTEINE LIGASE; HEME OXYGENASE 1; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; L F 001; LIPOPOLYSACCHARIDE; LYMPHOCYTE ANTIGEN; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; RHO KINASE INHIBITOR; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; WORTMANNIN; AZEPINE DERIVATIVE; L-F001 COMPOUND; NFE2L2 PROTEIN, MOUSE; PROTEIN KINASE INHIBITOR; RHO KINASE; SULFONAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DRUG STRUCTURE; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; CELL NUCLEUS; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; INFLAMMATION; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; PATHOLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ASTROCYTES; AZEPINES; CELL LINE; CELL NUCLEUS; CELL SURVIVAL; CYCLOOXYGENASE 2; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INFLAMMATION; MICE, INBRED C57BL; MICROGLIA; NF-E2-RELATED FACTOR 2; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; SULFONAMIDES; TRANSCRIPTION FACTOR RELA;

EID: 85015407420     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2017.03.025     Document Type: Article

References (50)

1. Agostinho, P., Cunha, R.A., Oliveira, C., Neuroinflammation, oxidative stress and the pathogenesis of Alzheimer's disease. Curr. Pharm. Des. 16 (2010), 2766–2778.
2. Ajmone-Cat, M.A., Mancini, M., De Simone, R., Cilli, P., Minghetti, L., Microglial polarization and plasticity: evidence from organotypic hippocampal slice cultures. Glia 61 (2013), 1698–1711.
3. Birch, A.M., Katsouri, L., Sastre, M., Modulation of inflammation in transgenic models of Alzheimer's disease. J. Neuroinflamm., 11, 2014 (25-25).
4. Brambilla, R., Morton, P.D., Ashbaugh, J.J., Karmally, S., Lambertsen, K.L., Bethea, J.R., Astrocytes play a key role in EAE pathophysiology by orchestrating in the CNS the inflammatory response of resident and peripheral immune cells and by suppressing remyelination. Glia 62 (2014), 452–467.
5. Buendia, I., Michalska, P., Navarro, E., Gameiro, I., Egea, J., León, R., Nrf2–ARE pathway: an emerging target against oxidative stress and neuroinflammation in neurodegenerative diseases. Pharmacol. Ther. 157 (2016), 84–104.
6. Cantarella, G., Benedetto, G.D., Puzzo, D., Privitera, L., Loreto, C., Saccone, S., Giunta, S., Palmeri, A., Bernardini, R., Neutralization of TNFSF10 ameliorates functional outcome in a murine model of Alzheimer's disease. Brain: J. Neurol. 138 (2014), 203–216.
7. Chang, H.J., Lee, W.J., Hwang, J.Y., Seol, S.M., Yun, M.K., Lee, Y.L., Ji, H.A., Park, J.Y., The role of Rho/Rho-kinase pathway in the expression of ICAM-1 by linoleic acid in human aortic endothelial cells. Inflammation 35 (2012), 1041–1048.
8. Chen, J., Dou, Y., Zheng, X., Leng, T., Lu, X., Ouyang, Y., Sun, H., Xing, F., Mai, J., Gu, J., TRPM7 channel inhibition mediates midazolam-induced proliferation loss in human malignant glioma. Tumor Biol., 2016, 1–11.
9. Chen, M., Liu, A., Ouyang, Y., Huang, Y., Chao, X., Pi, R., Fasudil and its analogs: a new powerful weapon in the long war against central nervous system disorders?. Expert Opin. Investig. Drugs 22 (2013), 537–550.
10. Chen, M., Liu, Q., Liu, A., Tan, M., Xie, Z., Uri, A., Chen, Z., Huang, G., Sun, Y., Ge, H., Simply combining fasudil and lipoic acid in a novel multitargeted chemical entity potentially useful in central nervous system disorders. Rsc Adv. 4 (2014), 37266–37269.
11. Doens, D., Fernández, P.L., Microglia receptors and their implications in the response to amyloid β for Alzheimer's disease pathogenesis. J. Neuroinflamm. 11 (2014), 1–14.
12. Glass, C.K., Saijo, K., Winner, B., Marchetto, M.C., Gage, F.H., Mechanisms underlying inflammation in neurodegeneration. Cell 140 (2010), 918–934.
13. Grasso, S., Bramanti, V., Tomassoni, D., Bronzi, D., Malfa, G., Traini, E., Napoli, M., Renis, M., Amenta, F., Avola, R., Effect of lipoic acid and α-glyceryl-phosphoryl-choline on astroglial cell proliferation and differentiation in primary culture. J. Neureactive Oxyg. Species. Res. 92 (2014), 86–94.
14. H, H., Y, Z., T, L., A, L., Y, W., X, Y., J, C., L, T., W, C., P, Q., The major cholesterol metabolite cholestane-3β,5α,6β-triol functions as an endogenous neuroprotectant. J. Neureactive Oxyg. Speciesci.: Off. J. Soc. Neureactive Oxyg. Speciesci. 34 (2014), 11426–11438.
15. Heneka, M.T., Carson, M.J., El Khoury, J., Landreth, G.E., Breactive oxygen speciesseron, F, Feinstein, D.L., Jacobs, A.H., Wyss-Coray, T., Vitorica, J., Ransohoff, R.M., Neuroinflammation in Alzheimer's disease. Lancet Neurol. 14 (2015), 388–405.
16. Hybertson, B.M., Gao, B., Bose, S.K., Mccord, J.M., Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Mol. Asp. Med. 32 (2011), 234–246.
17. Iizumi, T., Takahashi, S., Mashima, K., Minami, K., Izawa, Y., Abe, T., Hishiki, T., Suematsu, M., Kajimura, M., Suzuki, N., A possible role of microglia-derived nitric oxide by lipopolysaccharide in activation of astroglial pentose-phosphate pathway via the Keap1/Nrf2 system. J. Neuroinflamm. 13 (2016), 1–20.
18. Jenkinson, M.L., Bliss, M.R., Brain, A.T., Scott, D.L., Rheumatoid arthritis and senile dementia of the Alzheimer's type. Br. J. Rheumatol. 28 (1989), 86–88.
19. Kang, C.H., Choi, Y.H., Moon, S.K., Kim, W.J., Kim, G.Y., Quercetin inhibits lipopolysaccharide-induced nitric oxide production in BV2 microglial cells by suppressing the NF-kappaB pathway and activating the Nrf2-dependent HO-1 pathway. Int. Immunopharmacol. 17 (2013), 808–813.
20. Kanninen, K., Malm, T.M., Jyrkkänen, H.-K., Goldsteins, G., Keksa-Goldsteine, V., Tanila, H., Yamamoto, M., Ylä-Herttuala, S., Levonen, A.-L., Koistinaho, J., Nuclear factor erythroid 2-related factor 2 protects against beta amyloid. Mol. Cell. Neureactive Oxyg. Speciesci. 39 (2008), 302–313.
21. Kroner, A., Greenhalgh, A.D., Zarruk, J.G., Passos Dos Santos, R., Gaestel, M., David, S., TNF and increased intracellular iron alter macrophage polarization to a detrimental M1 phenotype in the injured spinal cord. Neuron 83 (2014), 1098–1116.
22. Lastres-Becker, I., Innamorato, N.G., Jaworski, T., Rábano, A., Kügler, S., Van, L.F., Cuadrado, A., Fractalkine activates NRF2/NFE2L2 and heme oxygenase 1 to restrain tauopathy-induced microgliosis. Brain: J. Neurol. 137 (2014), 78–91.
23. Lefort, R., Reversing synapse loss in Alzheimer's disease: rho-guanosine triphosphatases and insights from other brain disorders. J. Am. Soc. Exp. Neurother. 12 (2015), 19–28.
24. Li, W., Khor, T.O., Xu, C., Shen, G., Jeong, W.S., Yu, S., Kong, A.N., Activation of Nrf2-antioxidant signaling attenuates NFκB-inflammatory response and elicits apoptosis. Biochem. Pharmacol. 76 (2008), 1485–1489.
25. Liu, C., Li, Y., Yu, J., Feng, L., Hou, S., Liu, Y., Guo, M., Xie, Y., Meng, J., Zhang, H., Targeting the shift from M1 to M2 macrophages in experimental autoimmune encephalomyelitis mice treated with fasudil. PLoS One, 8, 2013, e54841.
26. Liu, C., Li, Y., Yu, J., Feng, L., Hou, S., Liu, Y., Guo, M., Xie, Y., Meng, J., Zhang, H., Xiao, B., Ma, C., Targeting the shift from M1 to M2 macrophages in experimental autoimmune encephalomyelitis mice treated with fasudil. PLoS One, 8, 2013, e54841.
27. Liu, G.H., Qu, J., Shen, X., NF-κB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim. Biophys. Acta 1783 (2008), 713–727.
28. Liu, X., Zhou, W., Zhang, X., Lu, P., Du, Q., Tao, L., Ding, Y., Wang, Y., Hu, R., Dimethyl fumarate ameliorates dextran sulfate sodium-induced murine experimental colitis by activating Nrf2 and suppressing NLRP3 inflammasome activation. Biochem Pharmacol. 112 (2016), 37–49.
29. Ma, Q., Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 53 (2013), 401–426.
30. Maczurek, A., Hager, K., Kenklies, M., Sharman, M., Martins, R., Engel, J., Carlson, D.A., Münch, G., Lipoic acid as an anti-inflammatory and neuroprotective treatment for Alzheimer's disease. Adv. Drug Deliv. Rev. 60 (2008), 1463–1470.
31. Mattson, M.P., Magnus, T., Ageing and neuronal vulnerability. Nat. Rev. Neureactive Oxyg. Speciesci. 7 (2006), 278–294.
32. Mueller, B.K., Mack, H., Teusch, N., Rho kinase, a promising drug target for neurological disorders. Nat. Rev. Drug Discov. 4 (2005), 387–398.
33. Nath, J., Powledge, A., Modulation of human neutrophil inflammatory responses by nitric oxide: studies in unprimed and LPS-primed cells. J. Leukoc. Biol. 62 (1997), 805–816.
34. Qin, L., Wu, X., Block, M.L., Liu, Y., Breese, G.R., Hong, J.S., Knapp, D.J., Crews, F.T., Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55 (2007), 453–462.
35. Quintanilla, R.A., Orellana, J.A., Bernhardi, R.V., Understanding risk factors for Alzheimer's disease: interplay of neuroinflammation, connexin-based communication and oxidative stress. Arch. Med. Res. 43 (2012), 632–644.
36. Segain, J.P., Blétière, D.R.D.L., Sauzeau, V., Bourreille, A., Hilaret, G., Cario-Toumaniantz, C., Pacaud, P., Rho kinase blockade prevents inflammation via nuclear factor kappa B inhibition: evidence in Crohn's disease and experimental colitis. Gastroenterology 124 (2003), 1180–1187.
37. Shen, W., Wang, L., Pi, R., Li, Z., Rikang, W., L-F001, a multifunctional ROCK inhibitor prevents paraquat-induced cell death through attenuating ER stress and mitochondrial dysfunction in PC12 cells. Biochem. Biophys. Res. Commun. 464 (2015), 794–799.
38. Silvia, D., Daniel, A., Arti, P., Patrice, H., Rumana, Y., Doseff, A.I., Apigenin protects endothelial cells from lipopolysaccharide (LPS)-induced inflammation by decreasing Caspase-3 activation and modulating mitochondrial function. Int. J. Mol. Sci. 14 (2013), 17664–17679.
39. Sonkar, V.K., Kulkarni, P.P., Dash, D., Amyloid β peptide stimulates platelet activation through RhoA-dependent modulation of actomyosin organization. Faseb J. 28 (2014), 1819–1829.
40. Spires-Jones, T., Hyman, B., The intersection of amyloid beta and tau at synapses in Alzheimer's disease. Neuron 82 (2014), 756–771.
41. Tan, Z.S., Beiser, A.S., Vasan, R.S., Roubenoff, R., Dinarello, C.A., Harris, T.B., Benjamin, E.J., Au, R., Kiel, D.P., Wolf, P.A., Inflammatory markers and the risk of Alzheimer disease: the Framingham Study. Neurology 70 (2007), 1902–1908.
42. Tang, C.H., Hsu, C.J., Yang, W.H., Fong, Y.C., Lipoteichoic acid enhances IL-6 production in human synovial fibroblasts via TLR2 receptor, PKCδ and c-Src dependent pathways. Biochem. Pharmacol. 79 (2010), 1648–1657.
43. Tornatore, L., Thotakura, A.K., Bennett, J., Moretti, M., Franzoso, G., The nuclear factor kappa B signaling pathway: integrating metabolism with inflammation. Trends Cell Biol. 22 (2012), 557–566.
44. Winklewski, P.J., Radkowski, M., Demkow, U., Creactive oxygen speciess-talk between the inflammatory response, sympathetic activation and pulmonary infection in the ischemic stroke. J. Neuroinflamm., 11, 2014 (2-2).
45. Xie, T., Luo, G., Zhang, Y., Wang, X., Wang, X., Wu, M., Li, G., Rho‐kinase inhibitor fasudil reduces allergic airway inflammation andmucus hypersecretion by regulating STAT6 and NFκB. Clin. Exp. Allergy 45 (2015), 1812–1822.
46. Yang, C., Zhao, J., Cheng, Y., Le, X.C., Rong, J., N-Propargyl caffeate amide (PACA) potentiates nerve growth factor (NGF)-induced neurite outgrowth and attenuates 6-Hydroxydopamine (6-OHDA)-induced toxicity by activating the Nrf2/HO-1 pathway. Acs Chem. Neureactive Oxyg. Species. 6 (2015), 1560–1569.
47. Zhang, H., Li, Y., Yu, J., Guo, M., Meng, J., Liu, C., Xie, Y., Feng, L., Xiao, B., Ma, C., Rho kinase inhibitor fasudil regulates microglia polarization and function. Neuroimmunomodulation 20 (2013), 313–322.
48. Zhang, H.F., Guo, M.F., Meng, J., Liu, C.Y., Yan-Hua, L.I., Jie-Zhong, Y.U., Hou, S.W., Feng, L., Xiao, B.G., Cun-Gen, M.A., Effect of Fasudil on the phenotype conversion of LPS-stimulated BV-2 microglia. Chin. J. Cell. Mol. Immunol. 28 (2012), 818–821.
49. Zhang, R., Xu, M., Wang, Y., Xie, F., Zhang, G., Qin, X., Nrf2—a promising therapeutic target for Defensing Against oxidative stress in stroke. Mol. Neurobiol., 2016, 1–12.
50. Zhao, Z., Gong, S., Wang, S., Ma, C., Effect and mechanism of evodiamine against ethanol-induced gastric ulcer in mice by suppressing Rho/NF-кB pathway. Int. Immunopharmacol. 28 (2015), 588–595.