英-4作-2023-Asiatic acid and andrographolide reduce hippocampal injury through suppressing neuroinflammation caused by Salmonella typhimurium infection.pdf
[en] Damage caused by Salmonella is not only limited to the gastrointestinal tract, but also occurs in the central nervous system (CNS). The aim of this study was to explore the protective effects of asiatic acid (AA) and andrographolide (AD) on the CNS through simulating common infection in mice by oral administration of Salmonella typhimurium (S. typhimurium). The results showed that the neurons in the hippocampus of mice were damaged after S. typhimurium invaded CNS in mice, and the inflammation was increased, which was manifested by the increased expression of inflammatory factors interleukin (IL)-1β, tumor necrosis factor (TNF)-α, IL-6, interferon (IFN)-γ and IL-12b and the activation of NOD-, LRR- and pyrin domain-containing protein 3 (NLRP3) inflammasomes. The damage and inflammatory response of mouse hippocampal neurons were effectively reduced by AA or AD pretreatment. Furthermore, we observed the significant activation of microglia after S. typhimurium infection. AA and AD attenuated S. typhimurium -induced hippocampal injury by reducing the inflammatory response on microglia. The findings suggest that the AA and AD protect CNS from injury caused by S. typhimurium infection through inhibiting over expression of multiple neuroinflammatory mediators and NLRP3 inflammasome in mice.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Zou, Wenshu; Engineering and Technology Research Center of Traditional Chinese Veterinary Medicine of Gansu Province, Key Laboratory of Veterinary Pharmaceutical Development of Ministry of Agriculture and Rural Affairs of China, Lanzhou Institute of Husbandry and Pharmaceutical Sciences of Chinese Academy of Agricultural Sciences, Lanzhou, 730050, Gansu, China. Electronic address: zouwenshu080603@163.com
Zhang, Kai; Engineering and Technology Research Center of Traditional Chinese Veterinary Medicine of Gansu Province, Key Laboratory of Veterinary Pharmaceutical Development of Ministry of Agriculture and Rural Affairs of China, Lanzhou Institute of Husbandry and Pharmaceutical Sciences of Chinese Academy of Agricultural Sciences, Lanzhou, 730050, Gansu, China. Electronic address: fyjohn@sina.com
Qiu, Zhengying; Engineering and Technology Research Center of Traditional Chinese Veterinary Medicine of Gansu Province, Key Laboratory of Veterinary Pharmaceutical Development of Ministry of Agriculture and Rural Affairs of China, Lanzhou Institute of Husbandry and Pharmaceutical Sciences of Chinese Academy of Agricultural Sciences, Lanzhou, 730050, Gansu, China. Electronic address: qiumoying@163.com
Xin, Ruihua ; Université de Liège - ULiège > TERRA Research Centre ; Engineering and Technology Research Center of Traditional Chinese Veterinary Medicine of Gansu Province, Key Laboratory of Veterinary Pharmaceutical Development of Ministry of Agriculture and Rural Affairs of China, Lanzhou Institute of Husbandry and Pharmaceutical Sciences of Chinese Academy of Agricultural Sciences, Lanzhou, 730050, Gansu, China. Electronic address: xinruihua@caas.cn
Wang, Guibo; Engineering and Technology Research Center of Traditional Chinese Veterinary Medicine of Gansu Province, Key Laboratory of Veterinary Pharmaceutical Development of Ministry of Agriculture and Rural Affairs of China, Lanzhou Institute of Husbandry and Pharmaceutical Sciences of Chinese Academy of Agricultural Sciences, Lanzhou, 730050, Gansu, China. Electronic address: wangguibo2005@163.com
Zhang, Jingyan; Engineering and Technology Research Center of Traditional Chinese Veterinary Medicine of Gansu Province, Key Laboratory of Veterinary Pharmaceutical Development of Ministry of Agriculture and Rural Affairs of China, Lanzhou Institute of Husbandry and Pharmaceutical Sciences of Chinese Academy of Agricultural Sciences, Lanzhou, 730050, Gansu, China. Electronic address: zwzh1223@126.com
Li, Jianxi; Engineering and Technology Research Center of Traditional Chinese Veterinary Medicine of Gansu Province, Key Laboratory of Veterinary Pharmaceutical Development of Ministry of Agriculture and Rural Affairs of China, Lanzhou Institute of Husbandry and Pharmaceutical Sciences of Chinese Academy of Agricultural Sciences, Lanzhou, 730050, Gansu, China. Electronic address: lzjianxil@163.com
Language :
English
Title :
Asiatic acid and andrographolide reduce hippocampal injury through suppressing neuroinflammation caused by Salmonella typhimurium infection.
This work was supported by grants from The National key research and development program of China (NO. 2017YFE0114400 ), and The Agricultural Sciences and Technology Innovation Program ( ASTIP-2020 ), and Major Output Research Topics of Chinese Academy of Agricultural Sciences ( CAAS-ZDXT2018008 ).
Ahmed, T., Ahmed, T., Salmonella meningitis complicated by ventriculitis and brain abscesses in an HIV positive adult patient. Cureus, 12, 2020, e11223, 10.7759/cureus.11223.
Ahmed, S., Kwatra, M., Ranjan Panda, S., Murty, U.S.N., Naidu, V.G.M., Andrographolide suppresses NLRP3 inflammasome activation in microglia through induction of parkin-mediated mitophagy in in-vitro and in-vivo models of Parkinson disease. Brain Behav. Immun. 91 (2021), 142–158, 10.1016/j.bbi.2020.09.017.
Badimon, A., Strasburger, H.J., Ayata, P., Chen, X., Nair, A., Ikegami, A., Hwang, P., Chan, A.T., Graves, S.M., Uweru, J.O., Ledderose, C., Kutlu, M.G., Wheeler, M.A., Kahan, A., Ishikawa, M., Wang, Y.C., Loh, Y.E., Jiang, J.X., Surmeier, D.J., Robson, S.C., Junger, W.G., Sebra, R., Calipari, E.S., Kenny, P.J., Eyo, U.B., Colonna, M., Quintana, F.J., Wake, H., Gradinaru, V., Schaefer, A., Negative feedback control of neuronal activity by microglia. Nature 586 (2020), 417–423, 10.1038/s41586-020-2777-8.
Bai, M., Zhu, X., Zhang, Y., Zhang, S., Zhang, L., Xue, L., Yi, J., Yao, S., Zhang, X., Abnormal hippocampal BDNF and miR-16 expression is associated with depression-like behaviors induced by stress during early life. PLoS One, 7, 2012, e46921, 10.1371/journal.pone.0046921.
Bassett, B., Subramaniyam, S., Fan, Y., Varney, S., Pan, H., Carneiro, A.M.D., Chung, C.Y., Minocycline alleviates depression-like symptoms by rescuing decrease in neurogenesis in dorsal hippocampus via blocking microglia activation/phagocytosis. Brain Behav. Immun. 91 (2021), 519–530, 10.1016/j.bbi.2020.11.009.
Bukhari, H., Tu Zahra, S.F., Zahoor, S., Saqib, M.A., Afzal, M.S., A rare case of extensively drug-resistant Salmonella typhi meningitis in a 9-year old: a case report. Future Microbiol. 16 (2021), 931–933, 10.2217/fmb-2020-0257.
Carneiro, M.R.P., Patricio, M.I.A., Jain, S., Rodrigues, D.D.P., Fracalanzza, S.E.L., Meningitis caused by Salmonella enterica serotype Panama in Brazil: first case reported. Rev. Soc. Bras. Med. Trop. 51 (2018), 244–246, 10.1590/0037-8682-0367-2017.
Chao, P.C., Yin, M.C., Mong, M.C., Anti-apoptotic and anti-glycative effects of asiatic acid in the brain of D-galactose treated mice. Food Funct. 6 (2015), 542–548, 10.1039/c4fo00862f.
Chaudhuri, D., Chowdhury, A.R., Biswas, B., Chakrayortty, D., Salmonella typhimurium infection leads to colonization of the mouse brain and is not completely cured with antibiotics. Front. Microbiol., 9, 2018, 10.3389/fmicb.2018.01632.
Chen, H., Chen, X.H., Sun, P., Wu, D., Yue, H., Pan, J.T., Li, X.X., Zhang, C., Wu, X.Y., Hua, L., Hu, W.H., Yang, Z.J., Discovery of dronedarone and its analogues as NLRP3 inflammasome inhibitors with potent anti-inflammation activity. Bioorg. Med. Chem. Lett, 46, 2021, 10.1016/j.bmcl.2021.128160.
Chiavegatto, S., Izidio, G.S., Mendes-Lana, A., Aneas, I., Freitas, T.A., Torrao, A.S., Conceicao, I.M., Britto, L.R.G., Ramos, A., Expression of alpha-synuclein is increased in the hippocampus of rats with high levels of innate anxiety. Mol. Psychiatr. 14 (2009), 894–905, 10.1038/mp.2008.43.
Conte, C., Possible link between SARS-CoV-2 infection and Parkinson's disease: the role of toll-like receptor 4. Int. J. Mol. Sci., 22, 2021, 10.3390/ijms22137135.
Dange, N.S., Sawant, V., Dash, L., Kondekar, A.S., A rare case of Salmonella meningitis and hemophagocytic lymphohistiocytosis. J. Global Infect. Dis. 13 (2021), 100–102, 10.4103/jgid.jgid_224_20.
Dolowschiak, T., Mueller, A.A., Pisan, L.J., Feigelman, R., Felmy, B., Sellin, M.E., Namineni, S., Nguyen, B.D., Wotzka, S.Y., Heikenwalder, M., von Mering, C., Mueller, C., Hardt, W.D., IFN-Gamma hinders recovery from mucosal inflammation during antibiotic therapy for Salmonella gut infection. Cell Host Microbe 20 (2016), 238–249, 10.1016/j.chom.2016.06.008.
Dong, N., Xue, C., Zhang, L., Zhang, T., Wang, C., Bi, C., Shan, A., Oleanolic acid enhances tight junctions and ameliorates inflammation in Salmonella typhimurium-induced diarrhea in mice via the TLR4/NF-kappaB and MAPK pathway. Food Funct. 11 (2020), 1122–1132, 10.1039/c9fo01718f.
Ekdahl, C.T., Claasen, J.H., Bonde, S., Kokaia, Z., Lindvall, O., Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. U.S.A. 100 (2003), 13632–13637, 10.1073/pnas.2234031100.
Galan, J.E., Salmonella Typhimurium and inflammation: a pathogen-centric affair. Nat. Rev. Microbiol. 19 (2021), 716–725, 10.1038/s41579-021-00561-4.
Goldmann, T., Tay, T.L., Prinz, M., Love and death: microglia, NLRP3 and the Alzheimer's brain. Cell Res. 23 (2013), 595–596, 10.1038/cr.2013.24.
Hansen, D.V., Hanson, J.E., Sheng, M., Microglia in Alzheimer's disease. J. Cell Biol. 217 (2018), 459–472, 10.1083/jcb.201709069.
Jia, X., Zhang, A., Li, Z., Peng, X., Tian, X., Gao, F., Activation of spinal PDGFRbeta in microglia promotes neuronal autophagy via p38 MAPK pathway in morphine-tolerant rats. J. Neurochem. 158 (2021), 373–390, 10.1111/jnc.15383.
Jolivel, V., Brun, S., Biname, F., Benyounes, J., Taleb, O., Bagnard, D., De Seze, J., Patte-Mensah, C., Mensah-Nyagan, A.G., Microglial cell morphology and phagocytic activity are critically regulated by the Neurosteroid allopregnanolone: a possible role in Neuroprotection. Cells, 10, 2021, 698, 10.3390/cells10030698.
Kaur, A., Chopra, K., Kaur, I.P., Rishi, P., Salmonella strain specificity determines post-typhoid central nervous system complications: intervention by lactiplantibacillus plantarum at gut-brain Axis. Front. Microbiol., 11, 2020, 1568, 10.3389/fmicb.2020.01568.
Kim, Y.K., Suh, I.B., Kim, H., Han, C.S., Lim, C.S., Choi, S.H., Licinio, J., The plasma levels of interleukin-12 in schizophrenia, major depression, and bipolar mania: effects of psychotropic drugs. Mol. Psychiatr. 7 (2002), 1107–1114, 10.1038/sj.mp.4001084.
Kim, M.J., Yoo, Y.C., Sung, N.Y., Lee, J., Park, S.R., Shon, E.J., Lee, B.D., Kim, M.R., Anti-inflammatory effects of liriope platyphylla in LPS-stimulated macrophages and endotoxemic mice. Am. J. Chin. Med. 44 (2016), 1127–1143, 10.1142/S0192415X16500634.
Kingsley, R.A., Msefula, C.L., Thomson, N.R., Kariuki, S., Holt, K.E., Gordon, M.A., Harris, D., Clarke, L., Whitehead, S., Sangal, V., Marsh, K., Achtman, M., Molyneux, M., Cormican, M., Parkhill, J., MacLennan, C.A., Heyderman, R.S., Dougan, G., Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res. 19 (2009), 2279–2287, 10.1101/gr.091017.109.
Klein, J.A., Grenz, J.R., Slauch, J.M., Knodler, L.A., Controlled activity of the Salmonella invasion-associated injectisome reveals its intracellular role in the cytosolic population. mBio, 8, 2017, 10.1128/mBio.01931-17 e01931-17.
Lemme-Dumit, J.M., Cazorla, S.I., Perdigon, G.D.V., Maldonado-Galdeano, C., Probiotic bacteria and their cell walls induce Th1-type immunity against Salmonella typhimurium challenge. Front. Immunol., 12, 2021, 660854, 10.3389/fimmu.2021.660854.
Li, T., Zhang, S.X., Microgliosis in the injured brain: infiltrating cells and reactive microglia both play a role. Neuroscientist 22 (2016), 165–170, 10.1177/1073858415572079.
Li, T., Zhao, J., Xie, W., Yuan, W., Guo, J., Pang, S., Gan, W.B., Gomez-Nicola, D., Zhang, S., Specific depletion of resident microglia in the early stage of stroke reduces cerebral ischemic damage. J. Neuroinflammation, 18, 2021, 81, 10.1186/s12974-021-02127-w.
Li, W.H., Liu, Y.L., Lun, J.C., He, Y.M., Tang, L.P., Heat stress inhibits TLR4-NF-kappaB and TLR4-TBK1 signaling pathways in broilers infected with Salmonella Typhimurium. Int. J. Biometeorol. 11 (2021), 1895–1903, 10.1007/s00484-021-02146-5.
Lu, C.Y., Li, C.C., Lii, C.K., Yao, H.T., Liu, K.L., Tsai, C.W., Chen, H.W., Andrographolide-induced pi class of glutathione S-transferase gene expression via PI3K/Akt pathway in rat primary hepatocytes. Food Chem. Toxicol. 49 (2011), 281–289, 10.1016/j.fct.2010.10.030.
Matta, S.M., Hill-Yardin, E.L., Crack, P.J., The influence of neuroinflammation in Autism Spectrum Disorder. Brain Behav. Immun. 79 (2019), 75–90, 10.1016/j.bbi.2019.04.037.
Miao, E.A., Mao, D.P., Yudkovsky, N., Bonneau, R., Lorang, C.G., Warren, S.E., Leaf, I.A., Aderem, A., Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. P Natl Acad Sci USA 107 (2010), 3076–3080, 10.1073/pnas.0913087107.
Momtaz, S., Hussein, A.A., Ostad, S.N., Abdollahi, M., Lall, N., Growth inhibition and induction of apoptosis in human cancerous HeLa cells by Maytenus procumbens. Food Chem. Toxicol. 51 (2013), 38–45, 10.1016/j.fct.2012.09.005.
Moyanova, S., De Fusco, A., Santolini, I., Celli, R., Bucci, D., Mastroiacovo, F., Battaglia, G., Nicoletti, F., Tchekalarova, J., Abnormal hippocampal melatoninergic system: a potential link between absence epilepsy and depression-like behavior in WAG/rij rats?. Int. J. Mol. Sci., 19, 2018, 1973, 10.3390/ijms19071973.
Nam, M.K., Shin, H.A., Han, J.H., Park, D.W., Rhim, H., Essential roles of mitochondrial depolarization in neuron loss through microglial activation and attraction toward neurons. Brain Res. 1505 (2013), 75–85, 10.1016/j.brainres.2013.02.005.
Noda, M., Ifuku, M., Mori, Y., Verkhratsky, A., Calcium influx through reversed NCX controls migration of microglia. Adv. Exp. Med. Biol. 961 (2013), 289–294, 10.1007/978-1-4614-4756-6_24.
Pereira, M., Tourlomousis, P., Wright, J., Monie, T.P., Bryant, C.E., CARD9 negatively regulates NLRP3-induced IL-1 beta production on Salmonella infection of macrophages. Nat. Commun., 7, 2016, 12874, 10.1038/ncomms12874.
Qian, Y.S., Xin, Z.C., Lv, Y.N., Wang, Z.W., Zuo, L., Huang, X., Li, Y.M., Xin, H.B., Asiatic acid suppresses neuroinflammation in BV2 microglia via modulation of the Sirt1/NF-kappa B signaling pathway. Food Funct. 9 (2018), 1048–1057, 10.1039/c7fo01442b.
Qin, X.Y., Fang, H., Shan, Q.H., Qi, C.C., Zhou, J.N., All-trans retinoic acid-induced abnormal hippocampal expression of synaptic genes SynDIG1 and DLG2 is correlated with anxiety or depression-like behavior in mice. Int. J. Mol. Sci., 21, 2020, 2677, 10.3390/ijms21082677.
Reinert, L.S., Lopusna, K., Winther, H., Sun, C.L., Thomsen, M.K., Nandakumar, R., Mogensen, T.H., Meyer, M., Vaegter, C., Nyengaard, J.R., Fitzgerald, K.A., Paludan, S.R., Sensing of HSV-1 by the cGAS-STING pathway in microglia orchestrates antiviral defence in the CNS. Nat. Commun., 7, 2016, 13348, 10.1038/ncomms13348.
Rivera-Chavez, F., Baumler, A.J., The pyromaniac inside you: Salmonella metabolism in the host gut. Annu. Rev. Microbiol. 69 (2015), 31–48, 10.1146/annurev-micro-091014-104108.
Ruby, T., McLaughlin, L., Gopinath, S., Monack, D., Salmonella's long-term relationship with its host. FEMS Microbiol. Rev. 36 (2012), 600–615, 10.1111/j.1574-6976.2012.00332.x.
Schafer, D.P., Lehrman, E.K., Stevens, B., The “quad-partite” synapse: microglia-synapse interactions in the developing and mature CNS. Glia 61 (2013), 24–36, 10.1002/glia.22389.
Schilling, M., Besselmann, M., Muller, M., Strecker, J.K., Ringelstein, E.B., Kiefer, R., Predominant phagocytic activity of resident microglia over hematogenous macrophages following transient focal cerebral ischemia: an investigation using green fluorescent protein transgenic bone marrow chimeric mice. Exp. Neurol. 196 (2005), 290–297, 10.1016/j.expneurol.2005.08.004.
Tang, H., Chen, W.X., Dou, Z.M., Chen, R.H., Hu, Y.Y., Chen, W.J., Chen, H.M., Antimicrobial effect of black pepper petroleum ether extract for the morphology of Listeria monocytogenes and Salmonella typhimurium. J Food Sci Tech Mys 54 (2017), 2067–2076, 10.1007/s13197-017-2644-2.
Taticchi, A., Urbani, S., Albi, E., Servili, M., Codini, M., Traina, G., Balloni, S., Patria, F.F., Perioli, L., Beccari, T., Conte, C., In vitro anti-inflammatory effects of phenolic compounds from moraiolo virgin olive Oil (MVOO) in brain cells via regulating the TLR4/NLRP3 Axis. Molecules, 24, 2019, 10.3390/molecules24244523.
Vilisaar, J., Kawabe, K., Braitch, M., Aram, J., Furtun, Y., Fahey, A.J., Chopra, M., Tanasescu, R., Tighe, P.J., Gran, B., Pothoulakis, C., Constantinescu, C.S., Reciprocal regulation of substance P and IL-12/IL-23 and the associated cytokines, IFNgamma/IL-17: a perspective on the relevance of this interaction to multiple sclerosis. J. Neuroimmune Pharmacol. 10 (2015), 457–467, 10.1007/s11481-015-9589-x.
Wandinger, K.P., Hagenah, J.M., Kluter, H., Rothermundt, M., Peters, M., Vieregge, P., Effects of amantadine treatment on in vitro production of interleukin-2 in de-novo patients with idiopathic Parkinson's disease. J. Neuroimmunol. 98 (1999), 214–220, 10.1016/s0165-5728(99)00093-4.
Wang, T., Nowrangi, D., Yu, L.Y., Lu, T., Tang, J.P., Han, B., Ding, Y.X., Fu, F.H., Zhang, J.H., Activation of dopamine D1 receptor decreased NLRP3-mediated inflammation in intracerebral hemorrhage mice. J. Neuroinflammation, 15, 2018, 2, 10.1186/s12974-017-1039-7.
Wang, L., Gong, X.L., Liu, Y., Du, T.S., Zhang, Z., Zhang, T., Wang, X.M., CD200 maintains the region-specific phenotype of microglia in the midbrain and its role in Parkinson's disease. Glia 68 (2020), 1874–1890, 10.1002/glia.23811.
Wickham, M.E., Brown, N.F., Provias, J., Finlay, B.B., Coombes, B.K., Oral infection of mice with Salmonella enterica serovar Typhimurium causes meningitis and infection of the brain. BMC Infect. Dis., 7, 2007, 65, 10.1186/1471-2334-7-65.
Wilms, H., Sievers, J., Rickert, U., Rostami-Yazdi, M., Mrowietz, U., Lucius, R., Dimethylfumarate inhibits microglial and astrocytic inflammation by suppressing the synthesis of nitric oxide, IL-1beta, TNF-alpha and IL-6 in an in-vitro model of brain inflammation. J. Neuroinflammation, 7, 2010, 30, 10.1186/1742-2094-7-30.
Wong, S.Y., Tan, M.G.K., Wong, P.T.H., Herr, D.R., Lai, M.K.P., Andrographolide induces Nrf2 and heme oxygenase 1 in astrocytes by activating p38 MAPK and ERK. J. Neuroinflammation, 13, 2016, 251, 10.1186/s12974-016-0723-3.
2022. Salmonella Typhimurium linked to chocolate products - Europe and the United States of America (World Health Organization). 2021/04/26 ed, World Health Organization.
Yu, H.B., Croxen, M.A., Marchiando, A.M., Ferreira, R.B., Cadwell, K., Foster, L.J., Finlay, B.B., Autophagy facilitates Salmonella replication in HeLa cells. mBio, 5, 2014, 10.1128/mBio.00865-14 e00865-00814.