Involvement of NFƙB and MAPK signaling pathways in the preventive effects of Ganoderma lucidum on the inflammation of BV-2 microglial cells induced by LPS

Adli, 2010, IKKalpha and IKKbeta each function to regulate NF-kappaB activation in the TNF-induced/canonical pathway, PLoS One, 5, 10.1371/journal.pone.0009428 Akiyama, 2000, Inflammation and Alzheimer’s disease, Neurobiol. Aging, 21, 383, 10.1016/S0197-4580(00)00124-X Atreya, 2010, Chemokines in inflammatory bowel diseases, Dig. Dis., 28, 386, 10.1159/000320392 Azizi, 2012, The potential role of proinflammatory and anti-inflammatory cytokines in Alzheimer’s disease pathogenesis, Immunopharmacol. Immunotoxicol., 34, 881, 10.3109/08923973.2012.705292 Bamberger, 2003, A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation, J. Neurosci., 23, 2665, 10.1523/JNEUROSCI.23-07-02665.2003 Barbieri, 2017, Anticancer and anti-inflammatory properties of ganoderma lucidum extract effects on melanoma and triple-negative breast cancer treatment, Nutrients, 9, 10.3390/nu9030210 Batra, 2013, Probing Lingzhi or Reishi medicinal mushroom Ganoderma lucidum (higher basidiomycetes): a bitter mushroom with amazing health benefits, Int. J. Med. Mushrooms, 15, 127, 10.1615/IntJMedMushr.v15.i2.20 Blasi, 1990, Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus, J. Neuroimmunol., 27, 229, 10.1016/0165-5728(90)90073-V Block, 2005, Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism, Prog. Neurobiol., 76, 77, 10.1016/j.pneurobio.2005.06.004 Block, 2007, Microglia-mediated neurotoxicity: uncovering the molecular mechanisms, Nat. Rev. Neurosci., 8, 57, 10.1038/nrn2038 Cai, 2017, Polysaccharides from Ganoderma lucidum attenuate microglia-mediated neuroinflammation and modulate microglial phagocytosis and behavioral response, J. Neuroinflammation, 14, 63, 10.1186/s12974-017-0839-0 Chandra, 2016, Neutralization of RANTES and Eotaxin prevents the loss of dopaminergic neurons in a mouse model of Parkinson’s disease, J. Biol. Chem., 291, 15267, 10.1074/jbc.M116.714824 Chen, 2007, Chinese herbs and herbal extracts for neuroprotection of dopaminergic neurons and potential therapeutic treatment of Parkinson’s disease, CNS Neurol. Disord. Drug Targets, 6, 273, 10.2174/187152707781387288 Chen, 2016, Role of neuroinflammation in neurodegenerative diseases (review), Mol. Med. Rep., 13, 3391, 10.3892/mmr.2016.4948 Cheung, 2000, Ganoderma extract activates MAP kinases and induces the neuronal differentiation of rat pheochromocytoma PC12 cells, FEBS Lett., 486, 291, 10.1016/S0014-5793(00)02317-6 Cobourne-Duval, 2018, Thymoquinone increases the expression of neuroprotective proteins while decreasing the expression of pro-inflammatory cytokines and the gene expression NFkappaB pathway signaling targets in LPS/IFNgamma -activated BV-2 microglia cells, J. Neuroimmunol., 320, 87, 10.1016/j.jneuroim.2018.04.018 Collado Mateo, 2015, Ganoderma Lucidum improves physical fitness in women with fibromyalgia, Nutr. Hosp., 32, 2126 Combs, 2001, Beta-amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis, J. Neurosci., 21, 1179, 10.1523/JNEUROSCI.21-04-01179.2001 Comerford, 2010, An immune paradox: how can the same chemokine axis regulate both immune tolerance and activation?: CCR6/CCL20: a chemokine axis balancing immunological tolerance and inflammation in autoimmune disease, Bioessays, 32, 1067, 10.1002/bies.201000063 Ding, 2010, Ganoderma lucidum extract protects dopaminergic neurons by inhibiting the production of inflammatory mediators by activated microglia, Sheng Li Xue Bao, 62, 547 Farzi, 2015, Synergistic effects of NOD1 or NOD2 and TLR4 activation on mouse sickness behavior in relation to immune and brain activity markers, Brain Behav. Immun., 44, 106, 10.1016/j.bbi.2014.08.011 Gao, 2008, Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression, Trends Immunol., 29, 357, 10.1016/j.it.2008.05.002 Geng, 2019, Preventive and therapeutic effect of Ganoderma (Lingzhi) on renal diseases and clinical applications, Adv. Exp. Med. Biol., 1182, 243, 10.1007/978-981-32-9421-9_10 Gilmore, 2006, Introduction to NF-kappaB: players, pathways, perspectives, Oncogene, 25, 6680, 10.1038/sj.onc.1209954 Gonzalez-Scarano, 1999, Microglia as mediators of inflammatory and degenerative diseases, Annu. Rev. Neurosci., 22, 219, 10.1146/annurev.neuro.22.1.219 Hasnat, 2015, Anti-inflammatory activity on mice of an extract of Ganoderma lucidum grown on rice via modulation of MAPK and NF-kappaB pathways, Phytochemistry, 114, 125, 10.1016/j.phytochem.2014.10.019 Henn, 2009, The suitability of BV2 cells as an alternative model system for primary microglia cultures or animal experiments examining brain inflammation, ALTEX, 26, 83, 10.14573/altex.2009.2.83 Hommes, 2003, Mitogen-activated protein (MAP) kinase signal transduction pathways and novel anti-inflammatory targets, Gut, 52, 144, 10.1136/gut.52.1.144 Huang, 2009, Enlargement of Abeta aggregates through chemokine-dependent microglial clustering, Neurosci. Res., 63, 280, 10.1016/j.neures.2009.01.001 Huang, 2010, TGF-beta1 blockade of microglial chemotaxis toward Abeta aggregates involves SMAD signaling and down-regulation of CCL5, J. Neuroinflammation, 7, 28, 10.1186/1742-2094-7-28 Hui, 2018, Pristimerin inhibits LPS-triggered neurotoxicity in BV-2 microglia cells through modulating IRAK1/TRAF6/TAK1-mediated NF-kappaB and AP-1 signaling pathways in vitro, Neurotox. Res., 33, 268, 10.1007/s12640-017-9837-3 Ito, 2011, CCR6 as a mediator of immunity in the lung and gut, Exp. Cell Res., 317, 613, 10.1016/j.yexcr.2010.12.018 Kempuraj, 2016, Neuroinflammation induces neurodegeneration, J. Neurol. Neurosurg. Spine, 1 Kim, 2005, Microglia in health and disease, J. Neurosci. Res., 81, 302, 10.1002/jnr.20562 Kim, 2019, Anti-neuroinflammatory effects of vanillin through the regulation of inflammatory factors and NF-kappaB signaling in LPS-stimulated microglia, Appl. Biochem. Biotechnol., 187, 884, 10.1007/s12010-018-2857-5 Kim, 2019, Anti-neuroinflammatory effects of galangin in LPS-stimulated BV-2 microglia through regulation of IL-1beta production and the NF-kappaB signaling pathways, Mol. Cell. Biochem., 451, 145, 10.1007/s11010-018-3401-1 Lai, 2008, Antagonizing beta-amyloid peptide neurotoxicity of the anti-aging fungus Ganoderma lucidum, Brain Res., 1190, 215, 10.1016/j.brainres.2007.10.103 Lee, 2015, The relationship between CCR6 and its binding partners: does the CCR6-CCL20 axis have to be extended?, Cytokine, 72, 97, 10.1016/j.cyto.2014.11.029 Lefkowitz, 2008, Microglia and myeloperoxidase: a deadly partnership in neurodegenerative disease, Free Radic. Biol. Med., 45, 726, 10.1016/j.freeradbiomed.2008.05.021 Leszek, 2016, Inflammatory mechanisms and oxidative stress as key factors responsible for progression of neurodegeneration: role of brain innate immune system, CNS Neurol. Disord. Drug Targets, 15, 329, 10.2174/1871527315666160202125914 Liu, 2003, Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention, J. Pharmacol. Exp. Ther., 304, 1, 10.1124/jpet.102.035048 Liu, 2019, Preventive and therapeutic effect of ganoderma (Lingzhi) on diabetes, Adv. Exp. Med. Biol., 1182, 201, 10.1007/978-981-32-9421-9_8 Liu, 2014, Neuroinflammation in Alzheimer’s disease: chemokines produced by astrocytes and chemokine receptors, Int. J. Clin. Exp. Pathol., 7, 8342 Liu, 2015, Anti-inflammatory effects of ganoderma lucidum triterpenoid in human Crohn’s disease associated with downregulation of NF-kappaB signaling, Inflamm. Bowel Dis., 21, 1918, 10.1097/MIB.0000000000000439 Martinez-Montemayor, 2011, Ganoderma lucidum (Reishi) inhibits cancer cell growth and expression of key molecules in inflammatory breast cancer, Nutr. Cancer, 63, 1085, 10.1080/01635581.2011.601845 Mendonca, 2017, The attenuating effects of 1,2,3,4,6 penta-O-galloyl-beta-d-glucose on inflammatory cytokines release from activated BV-2 microglial cells, J. Neuroimmunol., 305, 9, 10.1016/j.jneuroim.2017.01.011 Mendonca, 2018, The attenuating effects of 1,2,3,4,6 penta-O-galloyl-beta-d-glucose on pro-inflammatory responses of LPS/IFNgamma-activated BV-2 microglial cells through NFkB and MAPK signaling pathways, J. Neuroimmunol., 324, 43, 10.1016/j.jneuroim.2018.09.004 Mendonca, 2019, Proteomic analysis of the effect of the polyphenol pentagalloyl glucose on proteins involved in neurodegenerative diseases in activated BV2 microglial cells, Mol. Med. Rep., 20, 1736 Pezoldt, 2016, Tissue-specific induction of CCR6 and Nrp1 during early CD4(+) T cell differentiation, Eur. J. Microbiol. Immunol. (Bp), 6, 219, 10.1556/1886.2016.00018 Proudfoot, 2002, Chemokine receptors: multifaceted therapeutic targets, Nat. Rev. Immunol., 2, 106, 10.1038/nri722 Ranasinghe, 2018, Pleiotropic immune functions of chemokine receptor 6 in health and disease, Medicines (Basel), 5 Ransohoff, 2009, Microglial physiology: unique stimuli, specialized responses, Annu. Rev. Immunol., 27, 119, 10.1146/annurev.immunol.021908.132528 Rojo, 2008, Neuroinflammation: implications for the pathogenesis and molecular diagnosis of Alzheimer’s disease, Arch. Med. Res., 39, 1, 10.1016/j.arcmed.2007.10.001 Sarkar, 2018, Characterization and comparative analysis of a new mouse microglial cell model for studying neuroinflammatory mechanisms during neurotoxic insults, Neurotoxicology, 67, 129, 10.1016/j.neuro.2018.05.002 Scheerens, 2001, Characterization of chemokines and chemokine receptors in two murine models of inflammatory bowel disease: IL-10−/− mice and Rag-2−/− mice reconstituted with CD4+CD45RBhigh T cells, Eur. J. Immunol., 31, 1465, 10.1002/1521-4141(200105)31:5<1465::AID-IMMU1465>3.0.CO;2-E Scheidereit, 2006, IkappaB kinase complexes: gateways to NF-kappaB activation and transcription, Oncogene, 25, 6685, 10.1038/sj.onc.1209934 Schwab, 2004, Microglia rules insights into microglial-neuronal signaling, Cell Death Differ., 11, 1245, 10.1038/sj.cdd.4401487 Shen, 2013, An in vitro study of neuroprotective properties of traditional Chinese herbal medicines thought to promote healthy ageing and longevity, BMC Complement. Altern. Med., 13, 373, 10.1186/1472-6882-13-373 Sheng, 2003, Lipopolysaccharide-induced-neuroinflammation increases intracellular accumulation of amyloid precursor protein and amyloid beta-peptide in APPswe transgenic mice, Neurobiol. Dis., 14, 133, 10.1016/S0969-9961(03)00069-X Sheng, 2019, Deacetyl ganoderic acid F inhibits LPS-induced neural inflammation via NF-κB pathway both in vitro and in vivo, Nutrients, 12, 85, 10.3390/nu12010085 Streit, 2004, Microglia and neuroinflammation: a pathological perspective, J. Neuroinflammation, 1, 14, 10.1186/1742-2094-1-14 Suarez-Arroyo, 2013, Anti-tumor effects of Ganoderma lucidum (reishi) in inflammatory breast cancer in in vivo and in vitro models, PLoS One, 8, 10.1371/journal.pone.0057431 Subedi, 2016, Anti-neuroinflammatory and neuroprotective effects of the Lindera neesiana fruit in vitro, Phytomedicine, 23, 872, 10.1016/j.phymed.2016.05.002 Teramoto, 2005, Increased lymphocyte trafficking to colonic microvessels is dependent on MAdCAM-1 and C-C chemokine mLARC/CCL20 in DSS-induced mice colitis, Clin. Exp. Immunol., 139, 421, 10.1111/j.1365-2249.2004.02716.x Tilstra, 2011, NF-kappaB in aging and disease, Aging Dis., 2, 449 Tripathy, 2010, RANTES upregulation in the Alzheimer’s disease brain: a possible neuroprotective role, Neurobiol. Aging, 31, 8, 10.1016/j.neurobiolaging.2008.03.009 Von Bernhardi, 2015, Microglial cell dysregulation in brain aging and neurodegeneration, Front. Aging Neurosci., 7, 124, 10.3389/fnagi.2015.00124 Wang, 2018, A retrospective study of Ganoderma Lucidum spore powder for patients with epilepsy, Medicine (Baltimore), 97 Wang, 2018, Spore powder of Ganoderma lucidum for the treatment of Alzheimer’s disease: a pilot study, Medicine (Baltimore), 97 Woo, 2005, Ganoderma lucidum inhibits inducible nitric oxide synthase expression in macrophages, Mol. Cell. Biochem., 275, 165, 10.1007/s11010-005-1352-9 Yin, 2019, Preventive and therapeutic effect of Ganoderma (Lingzhi) on skin diseases and care, Adv. Exp. Med. Biol., 1182, 311, 10.1007/978-981-32-9421-9_14 Yoon, 2013, Ganoderma lucidum ethanol extract inhibits the inflammatory response by suppressing the NF-kappaB and toll-like receptor pathways in lipopolysaccharide-stimulated BV2 microglial cells, Exp. Ther. Med., 5, 957, 10.3892/etm.2013.895 Zandi, 1997, The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation, Cell, 91, 243, 10.1016/S0092-8674(00)80406-7 Zhao, 2004, Polysaccharide extract isolated from Ganoderma lucidum protects rat cerebral cortical neurons from hypoxia/reoxygenation injury, J. Pharmacol. Sci., 95, 294, 10.1254/jphs.SC0040011 Zhou, 2010, Neuroprotective effects of water-soluble Ganoderma lucidum polysaccharides on cerebral ischemic injury in rats, J. Ethnopharmacol., 131, 154, 10.1016/j.jep.2010.06.023 Zhu, 2002, The role of mitogen-activated protein kinase pathways in Alzheimer’s disease, Neurosignals, 11, 270, 10.1159/000067426