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01-04-2019 | Original Article

Magnesium sulfate inhibits binding of lipopolysaccharide to THP-1 cells by reducing expression of cluster of differentiation 14

Authors: Ya-Ying Chang, Tzu-Yu Lin, Ming-Chang Kao, Tsung-Ying Chen, Ching-Feng Cheng, Chih-Shung Wong, Chun-Jen Huang

Published in: Inflammopharmacology | Issue 2/2019

Abstract

We investigated effects of magnesium sulfate (MgSO₄) on modulating lipopolysaccharide (LPS)–macrophage binding and cluster of differentiation 14 (CD14) expression. Flow cytometry data revealed that the mean levels of LPS-macrophage binding and membrane-bound CD14 expression (mCD14) in differentiated THP-1 cells (a human monocytic cell line) treated with LPS plus MgSO₄ (the LPS + M group) decreased by 28.2% and 25.3% compared with those THP-1 cells treated with LPS only (the LPS group) (P < 0.001 and P = 0.037), indicating that MgSO₄ significantly inhibits LPS–macrophage binding and mCD14 expression. Notably, these effects of MgSO₄ were counteracted by L-type calcium channel activation. Moreover, the mean level of soluble CD14 (sCD14; proteolytic cleavage product of CD14) in the LPS + M group was 25.6% higher than in the LPS group (P < 0.001), indicating that MgSO₄ significantly enhances CD14 proteolytic cleavage. Of note, serine protease inhibition mitigated effects of MgSO₄ on both decreasing mCD14 and increasing sCD14. In conclusion, MgSO₄ inhibits LPS–macrophage binding through reducing CD14 expression. The mechanisms may involve antagonizing L-type calcium channels and activating serine proteases.

Ahmed LA (2012) Protective effects of magnesium supplementation on metabolic energy derangements in lipopolysaccharide-induced cardiotoxicity in mice. Eur J Pharmacol 694(1–3):75–81CrossRefPubMed

Bufler P, Stiegler G, Schuchmann M, Hess S, Kruger C, Stelter F et al (1995) Soluble lipopolysaccharide receptor (CD14) is released via two different mechanisms from human monocytes and CD14 transfectants. Eur J Immunol 25(2):604–610CrossRefPubMed

Cai C, Shi X, Korff S, Zhang J, Loughran PA, Ruan X et al (2013) CD14 contributes to warm hepatic ischemia-reperfusion injury in mice. Shock 40(2):115–121CrossRefPubMedPubMedCentral

Chen CP, Tsai PS, Huang CJ (2012) Anti-inflammation effect of human placental multipotent mesenchymal stromal cells is mediated by prostaglandin E2 via a myeloid differentiation primary response gene 88-dependent pathway. Anesthesiology 117(3):568–579CrossRefPubMed

Chen Z, Shao Z, Mei S, Yan Z, Ding X, Billiar T, Li Q (2018) Sepsis upregulates CD14 expression in a MyD88-dependent and Trif-independent pathway. Shock 49(1):82–89CrossRefPubMed

Chmielinska JJ, Tejerro-Taldo MI, Mak IT, Weglicki WB (2005) Intestinal and cardiac inflammatory response shows enhanced endotoxin receptor (CD14) expression in magnesium deficiency. Mol Cell Biochem 278(1–2):53–57CrossRefPubMed

Dong JF, Cruz MA, Aboulfatova K, Martin C, Choi H, Bergeron AL et al (2008) Magnesium maintains endothelial integrity, up-regulates proteolysis of ultra-large von Willebrand factor, and reduces platelet aggregation underflow conditions. Thromb Haemost 99(3):586–593CrossRefPubMed

El-Tanbouly DM, Abdelsalam RM, Attia AS, Abdel-Aziz MT (2015) Pretreatment with magnesium ameliorates lipopolysaccharide-induced liver injury in mice. Pharmacol Rep 67(5):914–920CrossRefPubMed

Ferrero E, Jiao D, Tsuberi BZ, Tesio L, Rong GW, Haziot A et al (1993) Transgenic mice expressing human CD14 are hypersensitive to lipopolysaccharide. Proc Natl Acad Sci USA 90:2380–2384CrossRefPubMed

Gao F, Ding B, Zhou L, Gao X, Guo H, Xu H (2013) Magnesium sulfate provides neuroprotection in lipopolysaccharide-activated primary microglia by inhibiting NF-kappaB pathway. J Surg Res 184(2):944–950CrossRefPubMed

Hopkins HA, Monick MM, Hunninghake GW (1995) Lipopolysaccharide upregulates surface expression of CD14 on human alveolar macrophages. Am J Physiol 269(6Pt1):L849–L854PubMed

Kew KM, Kirtchuk L, Michell CI (2014) Intravenous magnesium sulfate for treating adults with acute asthma in the emergency department. Cochrane Database Syst Rev 5:CD010909

Landmann R, Knorf HP, Link S, Sansano S, Schumann R, Zimmerli W (1996) Human monocyte CD14 is upregulated by lipopolysaccharide. Infect Immun 64(5):1762–1769PubMedPubMedCentral

Le-Barillec K, Si-Tahar M, Balloy V, Chignard M (1999) Proteolysis of monocyte CD14 by human leukocyte elastase inhibits lipopolysaccharide-mediated cell activation. J Clin Investig 103(7):1039–1046CrossRefPubMed

Le-Barillec K, Pidard D, Balloy V, Chignard M (2000) Human neutrophil cathepsin G down-regulates LPS-mediated monocyte activation through CD14 proteolysis. J Leukoc Biol 68(2):209–215PubMed

Lee MY, Huang CH, Kuo CJ, Lin CL, Lai WT, Chiou SH (2015) Clinical proteomics identifies urinary CD14 as a potential biomarker for diagnosis of stable coronary artery disease. PLoS One 10(2):e0117169CrossRefPubMedPubMedCentral

Lin CY, Tsai PS, Hung YC, Huang CJ (2010) L-type calcium channels are involved in mediating the anti-inflammatory effects of magnesium sulphate. Br J Anaesth 104(1):44–51CrossRefPubMed

Lopez-Castejon G, Brough D (2011) Understanding the mechanism of IL-1β secretion. Cytokine Growth Factor Rev 22(4):189–195CrossRefPubMedPubMedCentral

Ma L, Wu X-Y, Zhang L-H, Chen W-M, Uchiyama A, Mashimo T et al (2013) Propofol exerts anti-inflammatory effects in rats with lipopolysaccharide-induced acute lung injury by inhibition of CD14 and TLR4 expression. Braz J Med Biol Res 46(3):299–305CrossRefPubMedPubMedCentral

Ma S, Chen C, Cao T, Bi Y, Zhou J, Li X et al (2017) Mitigation effect of proanthocyanidin on secondary heart injury in rats caused by mechanical trauma. Sci Rep 7:44623CrossRefPubMedPubMedCentral

Molteni M, Gemma S, Rossetti C (2016) The role of Toll-like receptor 4 in infections and noninfectious inflammation. Mediat Inflamm 2016:6978936CrossRef

Park BS, Lee JO (2013) Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp Mol Med 45:e66CrossRefPubMedPubMedCentral

Pedrinaci S, Ruiz-Cabello F, Gomez O, Collado A, Garrido F (1990) Protein kinase C-mediated regulation of the expression of CD14 and CD11/CD18 in U937 cells. Int J Cancer 45(2):294–298CrossRefPubMed

Pham CT (2008) Neutrophil serine proteases fine-tune the inflammatory response. Int J Biochem Cell Biol 40(6–7):1317–1333CrossRefPubMed

Prestigiacomo V, Weston A, Messner S, Lampart F, Suter-Dick L (2017) Pro-fibrotic compounds induce stellate cell activation, ECM-remodelling and Nrf2 activation in a human 3D-multicellular model of liver fibrosis. PLoS One 12(6):e0179995CrossRefPubMedPubMedCentral

Rosadini CV, Kagan JC (2017) Early innate immune responses to bacterial LPS. Curr Opin Immunol 44:14–19CrossRefPubMed

Senft AP, Korfhagen TR, Whitsett JA, Shapiro SD, Levine AM (2005) Surfactant protein-D regulates soluble CD14 through matrix metalloproteinase-12. J Immunol 174(8):4953–4959CrossRefPubMed

Shin MK, Shin SW, Jung M, Park H, Park HE, Too HS (2015) Host gene expression for Mycobacterium avium subsp. paratuberculosis infection in human THP-1 macrophages. Pathog Dis 73(5):ftv031

Sonna LA, Hirshman CA, Croxton TL (1996) Role of calcium channel blockade in relaxation of tracheal smooth muscle by extracellular Mg²⁺. Am J Physiol 271(2 Pt 1):L251–L257PubMed

Su SC, Lin CC, Tai HC, Chang MY, Ho MR, Babu CS et al (2016) Structural basis for the magnesium-dependent activation and hexamerization of the Lon AAA+ protease. Structure 24:676–686CrossRefPubMed

Sugawara S, Nemoto E, Tada H, Miyake K, Imamura T, Takada H (2000) Proteolysis of human monocyte CD14 by cysteine proteinases (gingipains) from Porphyromonas gingivalis leading to lipopolysaccharide hyporesponsiveness. J Immunol 165(1):411–418CrossRefPubMed

Sugimoto J, Romani AM, Valentin-Torres AM, Luciano AA, Ramirez Kitchen CM, Funderburg N et al (2012) Magnesium decreases inflammatory cytokine production: a novel innate immunomodulatory mechanism. J Immunol 188(12):6338–6346CrossRefPubMed

Sun X, Zemel MB (2008) Calcitriol and calcium regulate cytokine production and adipocyte-macrophage cross-talk. J Nutr Biochem 19(6):392–399CrossRefPubMed

Tada H, Sugawara S, Nemoto E, Takahashi N, Imamura T, Potempa J, Travis J, Shimauchi H, Takada H (2002) Proteolysis of CD14 on human gingival fibroblasts by arginine-specific cysteine proteinases from Porphyromonas gingivalis leading to down-regulation of lipopolysaccharide-induced interleukin-8 production. Infect Immun 70(6):3304–3307CrossRefPubMedPubMedCentral

Takeshita S, Nakatani K, Kawase H, Seki S, Yamamoto M, Sekine I et al (1999) The role of bacterial lipopolysaccharide-bound neutrophils in the pathogenesis of Kawasaki disease. J Infect Dis 179(2):508–512CrossRefPubMed

Takeshita S, Nakatani K, Tsujimoto H, Kawamura Y, Sekihe I (2000) Detection of circulating lipopolysaccharide-bound monocytes in children with gram-negative sepsis. J Infect Dis 182(5):1549–1552CrossRefPubMed

Troelstra A, Antal-Szalmas P, de Graaf-Miltenburg LA, Weersink AJ, Verhoef J, Van Kessel KP et al (1997) Saturable CD14-dependent binding of fluorescein-labeled lipopolysaccharide to human monocytes. Infect Immun 65(6):2272–2277PubMedPubMedCentral

Weglicki WB, Mak IT, Chmielinska JJ, Tejero-Taldo MI, Komarov A, Kramer JH (2010) The role of magnesium deficiency in cardiovascular and intestinal inflammation. Magnes Res 23(4):S199–S206PubMedPubMedCentral

Wei Y, Chen J, Hu Y, Lu W, Zhang X, Wang R, Chu K (2018) Rosmarinic acid mitigates lipopolysaccharide-induced neuroinflammatory responses through the inhibition of TLR4 and CD14 expression and NF-κB and NLRP3 inflammasome activation. Inflammation 41(2):732–740CrossRefPubMed

Zhu T, Zhang L, Ling S, Duan J, Qian F, Li Y et al (2014) Scropolioside B inhibits IL-1β and cytokines expression through NF-kappaB and inflammasome NLRP3 pathways. Mediat Inflamm 2014:819053CrossRef

Title: Magnesium sulfate inhibits binding of lipopolysaccharide to THP-1 cells by reducing expression of cluster of differentiation 14
Authors: Ya-Ying Chang
Tzu-Yu Lin
Ming-Chang Kao
Tsung-Ying Chen
Ching-Feng Cheng
Chih-Shung Wong
Chun-Jen Huang
Publication date: 01-04-2019
Publisher: Springer International Publishing
Published in: Inflammopharmacology / Issue 2/2019
Print ISSN: 0925-4692
Electronic ISSN: 1568-5608
DOI: https://doi.org/10.1007/s10787-019-00568-7

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Magnesium sulfate inhibits binding of lipopolysaccharide to THP-1 cells by reducing expression of cluster of differentiation 14

Abstract

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