Doxycycline Suppresses Microglial Activation by Inhibiting the p38 MAPK and NF-kB Signaling Pathways (original) (raw)
Abd-El-Basset E, Fedoroff S (1995) Effect of bacterial wall lipopolysaccharide (LPS) on morphology, motility, and cytoskeletal organization of microglia in cultures. J Neurosci Res 41:222–237 ArticleCASPubMed Google Scholar
Ahler E, Sullivan WJ, Cass A, Braas D, York AG, Bensinger SJ, Graeber TG, Christofk HR (2013) Doxycycline alters metabolism and proliferation of human cell lines. PLoS One 8:e64561 ArticleCASPubMedPubMed Central Google Scholar
Austin PJ, Moalem-Taylor G (2010) The neuro-immune balance in neuropathic pain: involvement of inflammatory immune cells, immune-like glial cells and cytokines. J Neuroimmunol 229:26–50 ArticleCASPubMed Google Scholar
Bachstetter AD, Eldik LJV (2010) The p38 MAP kinase family as regulators of proinflammatory cytokine production in degenerative diseases of the CNS. Aging dis 3:199–211 Google Scholar
Barnum CJ, Eskow KL, Dupre K, Blandino P Jr, Deak T, Bishop C (2008) Exogenous corticosterone reduces L-DOPA-induced dyskinesia in the hemi-parkinsonian rat: role for interleukin-1beta. Neuroscience 156:30–41 ArticleCASPubMedPubMed Central Google Scholar
Blackwell TS, Christman JW (1997) The role of nuclear factor-kappa B in cytokine gene regulation. Am J Respir Cell Mol Biol 17:3–9 ArticleCASPubMed Google Scholar
Block ML, Hong JS (2005) Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 76:77–98 ArticleCASPubMed Google Scholar
Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8:57–69 ArticleCASPubMed Google Scholar
Bortolanza M, Cavalcanti-Kiwiatkoski R, Padovan-Neto FE, da-Silva CA, Mitkovski M, Raisman-Vozari R, Del-Bel E (2014) Glial activation is associated with l-DOPA induced dyskinesia and blocked by a nitric oxide synthase inhibitor in a rat model of Parkinson’s disease. Neurobiol Dis. doi:10.1016/j.nbd.2014.10.017
Bosscher KD, Beck IM, Dejager L, Bougarne N, Gaigneaux A, Chateauvieux S et al (2014) Selective modulation of the glucocorticoid receptor can distinguish between transrepression of NF-κB and AP-1. Cell Mol Life Sci 71:143–163 ArticlePubMedPubMed Central Google Scholar
Butterfield DA, Kanski J (2001) Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins. Mech Ageing Dev 15:945–962 Article Google Scholar
Caldeira C, Oliveira AF, Cunha C, Vaz AR, Falcão AS, Fernandes A, Brites D (2014) Microglia change from a reactive to an age-like phenotype with the time in culture. Front Cell Neurosci. doi:10.3389/fncel.2014.00152 PubMedPubMed Central Google Scholar
Cho Y, Son HJ, Kim EM, Choi JH, Kim ST, Ji IJ, Choi DH, Joh TH, Kim YS, Hwang O (2009) Doxycycline is neuroprotective against nigral dopaminergic degeneration by a dual mechanism involving MMP-3. Neurotox Res 16:361–371 ArticleCASPubMed Google Scholar
Clark WM, Calcagno FA, Gabler WL, Smith JR, Coull BM (1994) Reduction of central nervous system reperfusion injury in rabbits using doxycycline treatment. Stroke 25:1411–1415 ArticleCASPubMed Google Scholar
Clark WM, Lessov N, Lauten JD, Hazel K (1997) Doxycycline treatment reduces ischemic brain damage in transient middle cerebral artery occlusion in the rat. J Mol Neurosci 9:103–108 ArticleCASPubMed Google Scholar
Cunha BA, Comer JB, Jonas M (1982) The tetracyclines. Med Clin North Am 66:293–302 CASPubMed Google Scholar
Cunningham C (2013) Microglia and neurodegeneration: the role of systemic inflammation. Glia 61:71–90 ArticlePubMed Google Scholar
Dendorfer U, Oettgen P, Libermann TA (1994) Multiple regulatory elements in the interleukin-6 gene mediate induction by prostaglandins, cyclic AMP, and lipopolysaccharide. Mol Cell Biol 14:4443–4454 ArticleCASPubMedPubMed Central Google Scholar
Dignam JD, Lebovitz RM, Roeder RG (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11:1475–1489 ArticleCASPubMedPubMed Central Google Scholar
Domercq M, Matute C (2004) Neuroprotection by tetracyclines. Trends Pharmacol Sci 25:609–612 ArticleCASPubMed Google Scholar
Dutta G, Zhang P, Liu B (2008) The lipopolysaccharide Parkinson’s disease animal model: mechanistic studies and drug discovery. Fundam Clin Pharmacol 22:453–464 ArticleCASPubMedPubMed Central Google Scholar
Edan RA, Luqmani YA, Masocha W (2013) COL-3, a chemically modified tetracycline, inhibits lipopolysaccharide-induced microglia activation and cytokine expression in the brain. PLoS One 8:e57827 ArticleCASPubMedPubMed Central Google Scholar
Emerit J, Edeas M, Bricaire F (2004) Neurodegenerative diseases and oxidative stress. Biomed Pharmacother 58:39–46 ArticleCASPubMed Google Scholar
Fan LW, Pang Y, Lin S, Rhodes PG, Cai Z (2005) Minocycline attenuates lipopolysaccharide-induced white matter injury in the neonatal rat brain. Neuroscience 133:159–168 ArticleCASPubMed Google Scholar
Gandhi S, Wood NW (2005) Molecular pathogenesis of Parkinson’s disease. Hum Mol Genet 2:2749–2755 Article Google Scholar
Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, Eggert K, Oertel W, Banati RB, Brooks DJ (2006) In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson’s disease. Neurobiol Aging 21:404–412 CAS Google Scholar
Giasson BI, Ischiropoulos H, Lee VM, Trojanowski JQ (2002) The relationship between oxidative/nitrative stress and pathological inclusions in Alzheimer’s and Parkinson’s diseases. Free Radic Biol Med 32:1264–1275 ArticleCASPubMed Google Scholar
Gordon PH, Moore DH, Gelinas DF, Qualls C, Meister ME, Werner J, Mendoza M, Mass J, Kushner G, Miller RG (2004) Placebo-controlled phase I/II studies of minocycline in amyotrophic lateral sclerosis. Neurology 62:1845–1847 ArticleCASPubMed Google Scholar
Henry CJ, Huang Y, Wynne A, Hanke M, Himler J, Bailey MT, Sheridan JF, Godbout JP (2008) Minocycline attenuates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior, and anhedonia. J Neuroinflamm 5:15 Article Google Scholar
Henry CJ, Huang Y, Wynne AM, Godbout JP (2009) Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines. Brain Behav Immun 23:309–317 ArticleCASPubMedPubMed Central Google Scholar
Hirsch EC, Hunot S, Damier P, Faucheux B (1998) Glial cells and inflammation in Parkinson’s disease: a role in neurodegeneration? Ann Neurol 44:115–120 Article Google Scholar
Horvath RJ, Nutile-McMenemy N, Alkaitis MS, Deleo JA (2008) Differential migration, LPS-induced cytokine, chemokine, and NO expression in immortal- ized BV-2 and HAPI cell lines and primary microglial cultures. J Neurochem 107:557–569 ArticleCASPubMedPubMed Central Google Scholar
Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S (1999) Cutting edge: toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the LPS gene product. J Immunol 162:3749–3752 CASPubMed Google Scholar
Huang Y, Li R, Chen X, Zhuo Y, Jin R, Qian XP, Jiang YQ, Zeng ZH, Zhang Y, Shao QX (2011) Doxycycline up-regulates the expression of IL-6 and GM-CSF via MAPK/ERK and NF-kappaB pathways in mouse thymic epithelial cells. Int Immunopharmacol 111:1143–1149
Ito D, Tanaka K, Suzuki S, Dembo T, Fukuuchi Y (2001) Transient focal cerebral ischemia in rat brain enhanced expression of iba 1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32:1208–1215 ArticleCASPubMed Google Scholar
Kaneko YS, Mori K, Nakashima A, Sawada M, Nagatsu I, Ota A (2005) Peripheral injection of lipopolysaccharide enhances expression of inflammatory cytokines in murine locus coeruleus: possible role of increased norepinephrine turnover. J Neurochem 94:393–404 ArticleCASPubMed Google Scholar
Kang YJ, Chen J, Otsuka M, Mols J, Ren S, Wang Y, Han J (2008) Macrophage deletion of p38α partially impairs lipopolysaccharide-induced cellular activation. J Immunol 180:5075–5082 ArticleCASPubMed Google Scholar
Kang SM, More SV, Park JY, Kim BW, In PJ, Yoon SH, Choi DK (2014) A novel synthetic HTB derivative, BECT inhibits lipopolysaccharide-mediated inflammatory response by suppressing the p38 MAPK/JNK and NF-kB activation pathways. Pharmacol Rep 66:471–479 ArticleCASPubMed Google Scholar
Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS (2000) Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 20:6309–6316 CASPubMed Google Scholar
Kim SS, Kong PJ, Kim BS, Sheen DH, Nam SY, Chun W (2004) Inhibitory action of minocycline on lipopolysaccharide-induced release of nitric oxide and prostaglandin E2 in BV2 microglial cells. Arch Pharm Res 27:314–318 ArticleCASPubMed Google Scholar
Langston JW, Forno LS, Tetrud J, Reeves AG, Kaplan JA, Karluk D (1999) Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann Neurol 46:598–605 ArticleCASPubMed Google Scholar
Lawson LJ, Perry VH, Dri P, Gordon S (1990) Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39:151–170 ArticleCASPubMed Google Scholar
Lazzarini M, Martin S, Mitkovski M, Vozari RR, Stuhmer W, Bel ED (2013) Doxycycline restrains glia and confers neuroprotection in a 6-OHDA Parkinson model. Glia 61:1084–1100 ArticlePubMed Google Scholar
Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T (2003) Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci USA 100:8514–8519 ArticleCASPubMedPubMed Central Google Scholar
Liu B, Hong JS (2003) Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther 304:1–7 ArticleCASPubMed Google Scholar
Lund S, Christensen KV, Hedtjarn M, Mortensen AL, Hagberg H, Falsig J, HasseldamH Schrattenholz A, Pörzgen P, Leist M (2006) The dynamics of the LPS triggered inflammatory response of murine microglia under different culture and in vivo conditions. J Neuroimmunol 180:71–87 ArticleCASPubMed Google Scholar
Matsusaka T, Fujikawa K, Nishio Y, Mukaida N, Matsushima K, Kishimoto T, Akira S (1993) Transcription factors NF-IL6 and NF-kappa B synergistically activate transcription of the inflammatory cytokines, interleukin 6 and interleukin 8. Proc Natl Acad Sci USA 90:193–197 Article Google Scholar
McGeer PL, Itagaki S, Boyes BE, McGeer EG (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson’s and Alzheimer’s disease brains. Neurology. doi:10.1212/WNL.38.8.1285 PubMed Google Scholar
Metz LM, Zhang Y, Yeung M, Patry DG, Bell RB, Stoian CA, Yong VW, Patten SB, Duquette P, Antel JP, Mitchell JR (2013) Minocycline reduces gadolinium-enhancing magnetic resonance imaging lesions in multiple sclerosis. Ann Neurol 55:756 Article Google Scholar
More SV, Kumar H, Kim IS, Song SY, Choi DK (2013) Cellular and molecular mediators of neuroinflammation in the pathogenesis of Parkinson’s disease. Mediators Inflamm. doi:10.1155/2013/952375 PubMedPubMed Central Google Scholar
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63 ArticleCASPubMed Google Scholar
Nikodemova M, Duncan ID, Watters JJ (2006) Minocycline exerts inhibitory effects on multiplemitogen-activated protein kinases and IΚBα degradation in a stimulus-specific manner in microglia. J Neurochem 96:314–323 ArticleCASPubMed Google Scholar
Ostrerova-Golts N, Petrucelli L, Hardy J, Lee JM, Farer M, Wolozin B (2000) The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity. J Neurosci 20:6048–6054 CASPubMed Google Scholar
Page TH, Brown A, Timms EM, Foxwell BM, Ray KP (2010) Inhibitors of p38 suppress cytokine production in rheumatoid arthritis synovial membranes: does variable inhibition of interleukin-6 production limit effectiveness in vivo? Arthritis Rheum 62:3221–3231 ArticleCASPubMed Google Scholar
Reasoner DK, Hindman BJ, Dexter F, Subieta A, Cutkomp J, Smith T (1997) Doxycycline reduces early neurologic impairment after cerebral arterial air embolism in the rabbit. Anesthesiology 87:569–576 ArticleCASPubMed Google Scholar
Roy A, Jana A, Yatish K, Freidt MB, Fung YK, Martinson JA, Pahan K (2008) Reactive oxygen species up-regulate CD11b in microglia via nitric oxide: implications for neurodegenerative diseases. Free Radic Biol Med 45:686–699 ArticleCASPubMedPubMed Central Google Scholar
Russo I, Bubacco L, Greggio E (2014) LRRK2 and neuroinflammation: partners in crime in Parkinson’s disease? J Neuroinflamm. doi:10.1186/1742-2094-11-52 Google Scholar
Sanchez-Guajardo V, Barnum CJ, Tansey MG, Romero-Ramos M (2013) Neuroimmunological processes in Parkinson’s disease and their relation to α-synuclein: microglia as the referee between neuronal processes and peripheral immunity. ASN Neuro 5:113–139 ArticleCASPubMed Google Scholar
Shi Q, Cheng L, Liu Z et al (2015) The p38 MAPK inhibitor SB203580 differentially modulates LPS-induced interleukin 6 expression in macrophages. Cent Eur J Immunol 40:276–282 ArticlePubMedPubMed Central Google Scholar
Singh V, Mitra S, Sharma AK, Gera R, Ghosh D (2014) Isolation and characterization of microglia from adult mouse brain: selected applications for ex vivo evaluation of immunotoxicological alterations following in vivo xenobiotic exposure. Chem Res Toxicol 27:895–903 ArticleCASPubMed Google Scholar
Skaper SD, Giusti P, Facci L (2012) Microglia and mast cells: two tracks on the road to neuroinflammation. FASEB J 26:3103–3117 ArticleCASPubMed Google Scholar
Smith K, Leyden JJ (2005) Safety of doxycycline and minocycline: a systematic review. Clin Ther 27:1329–1342 ArticleCASPubMed Google Scholar
Smith JA, Das A, Ray SK, Banik NL (2012) Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull 87:10–20 ArticleCASPubMed Google Scholar
Stolp HB, Dziegielewska KM (2009) Role of developmental inflammation and blood-brain barrier dysfunction in neurodevelopmental and neurodegenerative diseases. Neuropathol Appl Neurobiol 35:132–146 ArticleCASPubMed Google Scholar
Tarpey MM, Wink DA, Grisham MB (2004) Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations. Am J Physiol Regul Integr Comp Physiol 286:R431–R444 ArticleCASPubMed Google Scholar
Teismann P, Tieu K, Cohen O, Choi DK, Wu DC, Marks D, Vila M, Jackson-Lewis V, Przedborski S (2003) Pathogenic role of glial cells in Parkinson’s disease. Mov Disord 18:121–129 ArticlePubMed Google Scholar
Thomas M, Ashizawa T, Jankovic J (2004) Minocycline in Huntington’s disease: a pilot study. Mov Disord 19:692–695 ArticlePubMed Google Scholar
Wang PQ, Sun SG, Qiao X (2009) Protective effects of doxycycline upon dopaminergic neuron in LPS-induced rat model of Parkinson’s disease. Zhonghua Yi Xue Za Zhi 89:1346–1350 CASPubMed Google Scholar
Wojtera M, Sikorska B, Sobow T, Liberski PP (2005) Microglial cells in neurodegenerative disorders. Folia Neuropathol 43:311–332 CASPubMed Google Scholar
Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi DK, Ischiropoulos H, Przedborski S (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 22:1763–1771 CASPubMed Google Scholar
Yim CW, Flynn NM, Fitzgerald FT (1985) Penetration of oral doxycycline into the cerebrospinal fluid of patients with latent or neurosyphilis. Antimicrob Agents Chemother 28:347–348 ArticleCASPubMedPubMed Central Google Scholar
Yrjänheikki J, Keinänen R, Pellikka M, Hökfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95:15769–15774 ArticlePubMedPubMed Central Google Scholar
Zecca L, Casella L, Albertini A, Bellei C, Zucca FA, Engelen M, Zadlo A, Szewczyk G, Zareba M, Sarna T (2008) Neuromelanin can protect against iron-mediated oxidative damage in system modeling iron overload of brain aging and Parkinson’s disease. J Neurochem. doi:10.1111/j.1471-4159.2008.05541.x Google Scholar
Zhang Y, Dawson VL, Dawson TM (2000) Oxidative stress and genetics in the pathogenesis of Parkinson’s disease. Neurobiol Dis 7:240–250 ArticleCASPubMed Google Scholar
Zhang R, Zhao M, Ji HJ, Yuan YH, Chen NH (2013) Study on the dynamic changes in synaptic vesicle-associated protein and axonal transport protein combined with LPS neuroinflammation model. ISRN Neurol. doi:10.1155/2013/496079 Google Scholar