Ciprofloxacin and levofloxacin attenuate microglia inflammatory response via TLR4/NF-kB pathway

Skaper SD, Facci L, Zusso M, Giusti P. An inflammation-centric view of neurological disease: beyond the neuron. Front Cell Neurosci. 2018;12:72.

Lucas SM, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol. 2006;147(Suppl 1):S232–40.

Brown GC, Vilalta A. How microglia kill neurons. Brain Res. 1628;2015:288–97.

Colonna M, Butovsky O. Microglia function in the central nervous system during health and neurodegeneration. Annu Rev Immunol. 2017;35:441–68.

Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol. 2010;11:373–84.

Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282:2085–8.

Park BS, Lee JO. Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp Mol Med. 2013;45:e66.

Shimazu R, Akashi S, Ogata H, Nagai Y, Fukudome K, Miyake K, et al. MD-2, a molecule that confers lipopolysaccharide responsiveness on toll-like receptor 4. J Exp Med. 1999;189:1777–82.

Ohto U, Fukase K, Miyake K, Satow Y. Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science. 2007;316:1632–4.

Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature. 2009;458:1191–5.

Bryant CE, Spring DR, Gangloff M, Gay NJ. The molecular basis of the host response to lipopolysaccharide. Nat Rev Microbiol. 2010;8:8–14.

Begum AN, Jones MR, Lim GP, Morihara T, Kim P, Heath DD, et al. Curcumin structure-function, bioavailability, and efficacy in models of neuroinflammation and Alzheimer’s disease. J Pharmacol Exp Ther. 2008;326:196–208.

Sorrenti V, Contarini G, Sut S, Dall'Acqua S, Confortin F, Pagetta A, et al. Curcumin prevents acute neuroinflammation and long-term memory impairment induced by systemic lipopolysaccharide in mice. Front Pharmacol. 2018;9:183.

Gupta SC, Patchva S, Aggarwal BB. Therapeutic roles of curcumin: lessons learned from clinical trials. AAPS J. 2013;15:195–218.

Tasneem S, Liu B, Li B, Choudhary MI, Wang W. Molecular pharmacology of inflammation: medicinal plants as anti-inflammatory agents. Pharmacol Res. 2019;139:126–40.

Zhu HT, Bian C, Yuan JC, Chu WH, Xiang X, Chen F, et al. Curcumin attenuates acute inflammatory injury by inhibiting the TLR4/MyD88/NF-κB signaling pathway in experimental traumatic brain injury. J Neuroinflammation. 2014;11:59.

Youn HS, Saitoh SI, Miyake K, Hwang DH. Inhibition of homodimerization of toll-like receptor 4 by curcumin. Biochem Pharmacol. 2006;72:62–9.

Zusso M, Mercanti G, Belluti F, Di Martino RMC, Pagetta A, Marinelli C, et al. Phenolic 1,3-diketones attenuate lipopolysaccharide-induced inflammatory response by an alternative magnesium-mediated mechanism. Br J Pharmacol. 2017;174:1090–103.

Ezelarab HAA, Abbas SH, Hassan HA, Abuo-Rahma GEA. Recent updates of fluoroquinolones as antibacterial agents. Arch Pharm (Weinheim). 2018;351:e1800141.

Tauber SC, Nau R. Immunomodulatory properties of antibiotics. Curr Mol Pharmacol. 2008;1:68–79.

Dalhoff A, Shalit I. Immunomodulatory effects of quinolones. Lancet Infect Dis. 2003;3:359–71.

Dalhoff A. Immunomodulatory activities of fluoroquinolones. Infection. 2005;33(Suppl 2):55–70.

Ogino H, Fujii M, Ono M, Maezawa K, Hori S, Kizu J. In vivo and in vitro effects of fluoroquinolones on lipopolysaccharide-induced pro-inflammatory cytokine production. J Infect Chemother. 2009;15:168–73.

Zhang JZ, Ward KW. Besifloxacin, a novel fluoroquinolone antimicrobial agent, exhibits potent inhibition of pro-inflammatory cytokines in human THP-1 monocytes. J Antimicrob Chemother. 2008;61:111–6.

Khan AA, Slifer TR, Araujo FG, Suzuki Y, Remington JS. Protection against lipopolysaccharide-induced death by fluoroquinolones. Antimicrob Agents Chemother. 2000;44:3169–73.

Bode C, Diedrich B, Muenster S, Hentschel V, Weisheit C, Rommelsheim K, et al. Antibiotics regulate the immune response in both presence and absence of lipopolysaccharide through modulation of toll-like receptors, cytokine production and phagocytosis in vitro. Int Immunopharmacol. 2014;18:27–34.

Saitoh S, Akashi S, Yamada T, Tanimura N, Kobayashi M, Konno K, et al. Lipid A antagonist, lipid IVa, is distinct from lipid a in interaction with toll-like receptor 4 (TLR4)-MD-2 and ligand-induced TLR4 oligomerization. Int Immunol. 2004;16:961–9.

Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM Jr, Ferguson DM, et al. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J Am Chem Soc. 1995;117:5179–97.

Baxter CA, Murray CW, Clark DE, Westhead DR, Eldridge MD. Flexible docking using Tabu search and an empirical estimate of binding affinity. Proteins. 1998;33:367–82.

Halgren TA. Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. J Comp Chem. 1996;17:490–519.

Stewart JJP. MOPAC 7. Tokyo: Fujitsu Limited; 1993.

Wojciechowski M, Lesyng B. Generalized born model: analysis, refinement, and applications to proteins. J Phys Chem B. 2004;108:18368–76.

Skaper SD, Argentini C, Barbierato M. Culture of neonatal rodent microglia, astrocytes, and oligodendrocytes from cortex and spinal cord. Methods Mol Biol. 2012;846:67–77.

Mercanti G, Ragazzi E, Toffano G, Giusti P, Zusso M. Phosphatidylserine and curcumin act synergistically to down-regulate release of interleukin-1β from lipopolysaccharide-stimulated cortical primary microglial cells. CNS Neurol Disord Drug Targets. 2014;13:792–800.

Zusso M, Methot L, Lo R, Greenhalgh AD, David S, Stifani S. Regulation of postnatal forebrain amoeboid microglial cell proliferation and development by the transcription factor Runx1. J Neurosci. 2012;32:11285–98.

Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and citotoxicity assays. J Immunol Methods. 1983;65:55–63.

Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, et al. New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst. 1990;82:1107–12.

Facci L, Skaper SD. Cell enumeration assays: application of the MTT and sulforhodamine B assays to lipopolysaccharide-stimulated neonatal rodent microglia. Methods Mol Biol. 1727;2018:167–78.

Strober W. Trypan blue exclusion test of cell viability. Curr Protoc Immunol. 2001; Appendix 3:Appendix 3B.

Honda H, Nagai Y, Matsunaga T, Saitoh S, Akashi-Takamura S, Hayashi H, et al. Glycyrrhizin and isoliquiritigenin suppress the LPS sensor toll-like receptor 4/MD-2 complex signaling in a different manner. J Leukoc Biol. 2012;91:967–76.

Barbierato M, Facci L, Marinelli C, Zusso M, Argentini C, Skaper SD, et al. Co-ultramicronized Palmitoylethanolamide/Luteolin Promotes the Maturation of Oligodendrocyte Precursor Cells. Sci Rep. 2015;5:16676.

Liu G, Fan G, Guo G, Kang W, Wang D, Xu B, et al. FK506 attenuates the inflammation in rat spinal cord injury by inhibiting the activation of NF-κB in microglia cells. Cell Mol Neurobiol. 2017;37:843–55.

Molteni M, Gemma S, Rossetti C. The role of toll-like receptor 4 in infectious and noninfectious inflammation. Mediat Inflamm. 2016;2016:6978936.

Palù G, Valisena S, Ciarrocchi G, Gatto B, Palumbo M. Quinolone binding to DNA is mediated by magnesium ions. Proc Natl Acad Sci U S A. 1992;89:9671–5.

Ma HH, Chiu FC, Li RC. Mechanistic investigation of the reduction in antimicrobial activity of ciprofloxacin by metal cations. Pharm Res. 1997;14:366–70.

Idowu T, Schweizer F. Ubiquitous nature of fluoroquinolones: the oscillation between antibacterial and anticancer activities. Antibiotics (Basel). 2017;6:26.

Zhang GF, Zhang S, Pan B, Liu X, Feng LS. 4-Quinolone derivatives and their activities against Gram positive pathogens. Eur J Med Chem. 2018;143:710–23.

Shalit I. Immunological aspects of new quinolones. Eur J Clin Microbiol Infect Dis. 1991;10:262–6.

Yoshimura T, Kurita C, Usami E, Nakao T, Watanabe S, Kobayashi J, et al. Immunomodulatory action of levofloxacin on cytokine production by human peripheral blood mononuclear cells. Chemotherapy. 1996;42:459–64.

Pozzolini M, Scarfi S, Benatti U, Giovine M. Interference in MTT cell viability assay in activated macrophage cell line. Anal Biochem. 2003;313:338–41.

Vichai V, Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc. 2006;1:1112–6.

Zapater P, González-Navajas JM, Such J, Francés R. Immunomodulating effects of antibiotics used in the prophylaxis of bacterial infections in advanced cirrhosis. World J Gastroenterol. 2015;21:11493–501.

Lu YC, Yeh WC, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine. 2008;42:145–51.

Kawai T, Akira S. Signaling to NF-kappaB by toll-like receptors. Trends Mol Med. 2007;13:460–9.

Smolders S, Kessels S, Smolders SM, Poulhes F, Zelphati O, Sapet C, et al. Magnetofection is superior to other chemical transfection methods in a microglial cell line. J Neurosci Methods. 2018;293:169–73.

Liu FY, Cai J, Wang C, Ruan W, Guan GP, Pan HZ, et al. Fluoxetine attenuates neuroinflammation in early brain injury after subarachnoid hemorrhage: a possible role for the regulation of TLR4/MyD88/NF-κB signaling pathway. J Neuroinflammation. 2018;15:347.

Zhou J, Deng Y, Li F, Yin C, Shi J, Gong Q. Icariside II attenuates lipopolysaccharide-induced neuroinflammation through inhibiting TLR4/MyD88/NF-κB pathway in rats. Biomed Pharmacother. 2019;111:315–24.