Efonidipine Inhibits JNK and NF-κB Pathway to Attenuate Inflammation and Cell Migration Induced by Lipopolysaccharide in Microglial Cells |
Nguyen, Ngoc Minh
(College of Pharmacy and Integrated Research Institute for Drug Development, Dongguk University-Seoul)
Duong, Men Thi Hoai (College of Pharmacy and Integrated Research Institute for Drug Development, Dongguk University-Seoul) Nguyen, Phuong Linh (College of Pharmacy and Integrated Research Institute for Drug Development, Dongguk University-Seoul) Bui, Bich Phuong (College of Pharmacy and Integrated Research Institute for Drug Development, Dongguk University-Seoul) Ahn, Hee-Chul (College of Pharmacy and Integrated Research Institute for Drug Development, Dongguk University-Seoul) Cho, Jungsook (College of Pharmacy and Integrated Research Institute for Drug Development, Dongguk University-Seoul) |
1 | Park, S. E., Sapkota, K., Kim, S., Kim, H. and Kim, S. J. (2011) Kaempferol acts through mitogen-activated protein kinases and protein kinase B/AKT to elicit protection in a model of neuroinflammation in BV2 microglial cells. Br. J. Pharmacol. 164, 1008-1025. DOI |
2 | Resnick, L. and Fennell, M. (2004) Targeting JNK3 for the treatment of neurodegenerative disorders. Drug Discov. Today 9, 932-939. DOI |
3 | Shabab, T., Khanabdali, R., Moghadamtousi, S. Z., Kadir, H. A. and Mohan, G. (2017) Neuroinflammation pathways: a general review. Int. J. Neurosci. 127, 624-633. DOI |
4 | Trott, O. and Olson, A. J. (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461. |
5 | Zhu, X., Castellani, R. J., Takeda, A., Nunomura, A., Atwood, C. S., Perry, G. and Smith, M. A. (2001) Differential activation of neuronal ERK, JNK/SAPK and p38 in Alzheimer disease: the 'two hit' hypothesis. Mech. Ageing Dev. 123, 39-46. DOI |
6 | Soufli, I., Toumi, R., Rafa, H. and Touil-Boukoffa, C. (2016) Overview of cytokines and nitric oxide involvement in immuno-pathogenesis of inflammatory bowel diseases. World J. Gastrointest. Pharmacol. Ther. 7, 353-360. DOI |
7 | Do, H. T. T., Bui, B. P., Sim, S., Jung, J.-K., Lee, H. and Cho, J. (2020) Anti-inflammatory and anti-migratory activities of isoquinoline-1-carboxamide derivatives in LPS-treated BV2 microglial cells via inhibition of MAPKs/NF-κB pathway. Int. J. Mol. Sci. 21, 2319. |
8 | Dou, Y., Wu, H. J., Li, H. Q., Qin, S., Wang, Y. E., Li, J., Lou, H. F., Chen, Z., Li, X. M., Luo, Q. M. and Duan, S. (2012) Microglial migration mediated by ATP-induced ATP release from lysosomes. Cell Res. 22, 1022-1033. DOI |
9 | Gupta, S., Barrett, T., Whitmarsh, A. J., Cavanagh, J., Sluss, H. K., Derijard, B. and Davis, R. J. (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15, 2760-2770. DOI |
10 | El Khoury, J. (2010) Neurodegeneration and the neuroimmune system. Nat. Med. 16, 1369-1370. DOI |
11 | Haddad, J. J. (2002) Cytokines and related receptor-mediated signaling pathways. Biochem. Biophys. Res. Commun. 297, 700-713. DOI |
12 | Huang, B.-R., Chang, P.-C., Yeh, W.-L., Lee, C.-H., Tsai, C.-F., Lin, C., Lin, H.-Y., Liu, Y.-S., Wu, C. Y.-J., Ko, P.-Y., Huang, S.-S., Hsu, H.-C. and Lu, D.-Y. (2014) Anti-neuroinflammatory effects of the calcium channel blocker nicardipine on microglial cells: implications for neuroprotection. PLoS ONE 9, e91167. |
13 | Jourdan, J.-P., Bureau, R., Rochais, C. and Dallemagne, P. (2020) Drug repositioning: a brief overview. J. Pharm. Pharmacol. 72, 1145-1151. DOI |
14 | Kettenmann, H., Hanisch, U.-K., Noda, M. and Verkhratsky, A. (2011) Physiology of microglia. Physiol. Rev. 91, 461-553. DOI |
15 | Wang, D., Fei, Z., Luo, S. and Wang, H. (2020) MiR-335-5p inhibits β-Amyloid (Aβ) accumulation to attenuate cognitive deficits through targeting c-jun-N-terminal kinase 3 in Alzheimer's disease. Curr. Neurovasc. Res. 17, 93-101. DOI |
16 | Ashburn, T. T. and Thor, K. B. (2004) Drug repositioning: identifying and developing new uses for existing drugs. Nat. Rev. Drug Discov. 3, 673-683. DOI |
17 | Bogoyevitch, M. A. (2006) The isoform-specific functions of the c-Jun N-terminal Kinases (JNKs): differences revealed by gene targeting. BioEssays 28, 923-934. DOI |
18 | Brough, D. and Rothwell, N. J. (2007) Caspase-1-dependent processing of pro-interleukin-1β is cytosolic and precedes cell death. J. Cell Sci. 120, 772-781. DOI |
19 | Kloss, C. U. A., Bohatschek, M., Kreutzberg, G. W. and Raivich, G. (2001) Effect of lipopolysaccharide on the morphology and integrin immunoreactivity of ramified microglia in the mouse brain and in cell culture. Exp. Neurol. 168, 32-46. DOI |
20 | Li, Y., Hu, X., Liu, Y., Bao, Y. and An, L. (2009) Nimodipine protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation. Neuropharmacology 56, 580-589. DOI |
21 | Zulfiqar, Z., Shah, F.A., Shafique, S., Alattar, A., Ali, T., Alvi, A.M., Rashid, S. and Li, S. (2020) Repurposing FDA approved drugs as JNK3 inhibitor for prevention of neuroinflammation induced by MCAO in rats. J. Inflamm. Res. 13, 1185-1205. DOI |
22 | Kempuraj, D., Thangavel, R., Natteru, P. A., Selvakumar, G. P., Saeed, D., Zahoor, H., Zaheer, S., Iyer, S. S. and Zaheer, A. (2016) Neuroinflammation induces neurodegeneration. J. Neurol. Neurosurg. Spine 1, 1003. |
23 | Dou, X., Huang, H., Li, Y., Jiang, L., Wang, Y., Jin, H., Jiao, N., Zhang, L., Zhang, L. and Liu, Z. (2019) Multistage screening reveals 3-substituted indolin-2-one derivatives as novel and isoform-selective c-Jun N-terminal Kinase 3 (JNK3) inhibitors: implications to drug discovery for potential treatment of neurodegenerative diseases. J. Med. Chem. 62, 6645-6664. DOI |
24 | Gourmaud, S., Paquet, C., Dumurgier, J., Pace, C., Bouras, C., Gray, F., Laplanche, J.-L., Meurs, E. F., Mouton-Liger, F. and Hugon, J. (2015) Increased levels of cerebrospinal fluid JNK3 associated with amyloid pathology: links to cognitive decline. J. Psychiatry Neurosci. 40, 151-161. DOI |
25 | Heneka, M. T. and Feinstein, D. L. (2001) Expression and function of inducible nitric oxide synthase in neurons. J. Neuroimmunol. 114, 8-18. DOI |
26 | Lepiarz, I. and Olajide, O. (2019) The human microglia (HMC-3) as a cellular model of neuroinflammation. IBRO Rep. 6, S92. |
27 | Lopez-Castejon, G. and Brough, D. (2011) Understanding the mechanism of IL-1β secretion. Cytokine Growth Factor Rev. 22, 189-195. DOI |
28 | Nguyen, P. L., Bui, B. P., Lee, H. and Cho, J. (2021b) A novel 1,8-naphthyridine-2-carboxamide derivative attenuates inflammatory responses and cell migration in LPS-treated BV2 cells via the suppression of ROS generation and TLR4/Myd88/NF-κB signaling pathway. Int. J. Mol. Sci. 22, 2527. |
29 | Nagai, A., Nakagawa, E., Hatori, K., Choi, H. B., McLarnon, J. G., Lee, M. A. and Kim, S. U. (2001) Generation and characterization of immortalized human microglial cell lines: expression of cytokines and chemokines. Neurobiol. Dis. 8, 1057-1068. DOI |
30 | Liang, X., Wu, L., Wang, Q., Hand, T., Bilak, M., McCullough, L. and Andreasson, K. (2007) Function of COX-2 and prostaglandins in neurological disease. J. Mol. Neurosci. 33, 94-99. DOI |
31 | Nguyen, P. L., Bui, B. P., Duong, M. T. H., Lee, K., Ahn, H. C. and Cho, J. (2021a) Suppression of LPS-induced inflammation and cell migration by azelastine through inhibition of JNK/NF-κB pathway in BV2 microglial cells. Int. J. Mol. Sci. 22, 9061. |
32 | Okun, E., Griffioen, K. J., Lathia, J. D., Tang, S.-C., Mattson, M. P. and Arumugam, T. V. (2009) Toll-like receptors in neurodegeneration. Brain Res. Rev. 59, 278-292. DOI |
33 | Pan, J., Wang, G., Yang, H. Q., Hong, Z., Xiao, Q., Ren, R. J., Zhou, H. Y., Bai, L. and Chen, S. D. (2007) K252a prevents nigral dopaminergic cell death induced by 6-hydroxydopamine through inhibition of both mixed-lineage kinase 3/c-Jun NH2-terminal kinase 3 (JNK3) and apoptosis-inducing kinase 1/JNK3 signaling pathways. Mol. Pharmacol. 72, 1607-1618. DOI |
34 | Carson, M. J., Thrash, J. C. and Walter, B. (2006) The cellular response in neuroinflammation: the role of leukocytes, microglia and astrocytes in neuronal death and survival. Clin. Neurosci. Res. 6, 237-245. DOI |
35 | Boraschi, D., Cifone, M. G., Falk, W., Flad, H., Tagliabue, A. and Martin, M. (1998) Cytokines in inflammation. Eur. Cytokine Netw. 9, 205-212. |
36 | Bui, B. P., Oh, Y., Lee, H. and Cho, J. (2020) Inhibition of inflammatory mediators and cell migration by 1,2,3,4-tetrahydroquinoline derivatives in LPS-stimulated BV2 microglial cells via suppression of NF-κB and JNK pathway. Int. Immunopharmacol. 80, 106231. |
37 | DiSabato, D. J., Quan, N. and Godbout, J. P. (2016) Neuroinflammation: the devil is in the details. J. Neurochem. 139 Suppl 2, 136-153. DOI |
38 | Choi, W. S., Abel, G., Klintworth, H., Flavell, R. A. and Xia, Z. (2010) JNK3 mediates paraquat- and rotenone-induced dopaminergic neuron death. J. Neuropathol. Exp. Neurol. 69, 511-520. DOI |
39 | Cui, J., Zhang, M., Zhang, Y. Q. and Xu, Z. H. (2007) JNK pathway: diseases and therapeutic potential. Acta Pharmacol. Sin. 28, 601-608. DOI |
40 | Dawson, T. M. and Dawson, V. L. (2018) Nitric oxide signaling in neurodegeneration and cell death. Adv. Pharmacol. 82, 57-83. DOI |
41 | Tanaka, H. and Shigenobu, K. (2002) Efonidipine hydrochloride: a dual blocker of L- and T-type Ca(2+) channels. Cardiovasc. Drug Rev. 20, 81-92. DOI |
42 | Deng, Z., Yuan, C., Yang, J., Peng, Y., Wang, W., Wang, Y. and Gao, W. (2018) Behavioral defects induced by chronic social defeat stress are protected by Momordica charantia polysaccharides via attenuation of JNK3/PI3K/AKT neuroinflammatory pathway. Ann. Transl. Med. 7, 6. |
43 | Prakash, P., Jethava, K. P., Korte, N., Izquierdo, P., Favuzzi, E., Rose, I. V. L., Guttenplan, K. A., Manchanda, P., Dutta, S., Rochet, J. C., Fishell, G., Liddelow, S. A., Attwell, D. and Chopra, G. (2021) Monitoring phagocytic uptake of amyloid β into glial cell lysosomes in real time. Chem. Sci. 12, 10901-10918. DOI |
44 | Rajan, R. K. and Ramanathan, M. (2020) Identification and neuroprotective evaluation of a potential c-Jun N-terminal kinase 3 inhibitor through structure-based virtual screening and in-vitro assay. J. Comput. Aided Mol. Des. 34, 671-682. DOI |
45 | Salter, M. W. and Stevens, B. (2017) Microglia emerge as central players in brain disease. Nat. Med. 23, 1018-1027. DOI |
46 | Singh, S. S., Rai, S. N., Birla, H., Zahra, W., Rathore, A. S. and Singh, S. P. (2020) NF-κB-mediated neuroinflammation in Parkinson's disease and potential therapeutic effect of polyphenols. Neurotox. Res. 37, 491-507. DOI |
47 | Smith, A. M. and Dragunow, M. (2014) The human side of microglia. Trends Neurosci. 37, 125-135. DOI |
48 | Tai, C.-H., Yang, Y.-C., Pan, M.-K., Huang, C.-S. and Kuo, C.-C. (2011) Modulation of subthalamic T-type Ca2+ channels remedies locomotor deficits in a rat model of Parkinson disease. J. Clin. Invest. 121, 3289-3305. DOI |
49 | Waetzig, V., Czeloth, K., Hidding, U., Mielke, K., Kanzow, M., Brecht, S., Goetz, M., Lucius, R., Herdegen, T. and Hanisch, U.-K. (2005) c-Jun N-terminal kinases (JNKs) mediate pro-inflammatory actions of microglia. Glia 50, 235-246. DOI |
50 | Saini, R. and Singh, S. (2019) Inducible nitric oxide synthase: an asset to neutrophils. J. Leukoc. Biol. 105, 49-61. DOI |