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CLC number: S816.3

On-line Access: 2018-09-30

Received: 2017-10-08

Revision Accepted: 2017-12-28

Crosschecked: 2018-09-10

Cited: 0

Clicked: 4114

Citations:  Bibtex RefMan EndNote GB/T7714

 ORCID:

Wei-fen Li

https://orcid.org/0000-0001-8159-9876

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Journal of Zhejiang University SCIENCE B 2018 Vol.19 No.10 P.785-795

http://doi.org/10.1631/jzus.B1700506


Glycyrrhizic acid activates chicken macrophages and enhances their Salmonella-killing capacity in vitro


Author(s):  Bai-kui Wang, Yu-long Mao, Li Gong, Xin Xu, Shou-qun Jiang, Yi-bing Wang, Wei-fen Li

Affiliation(s):  Key Laboratory of Animal Molecular Nutrition of Education of Ministry, Key Laboratory of Animal Feed and Nutrition of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou 310058, China; more

Corresponding email(s):   wfli@zju.edu.cn

Key Words:  Glycyrrhizic acid, Chicken macrophage, Macrophage activation, Salmonella Typhimurium, Nuclear factor κ, B (NF-κ, B), c-Jun N-terminal kinase (JNK)


Bai-kui Wang, Yu-long Mao, Li Gong, Xin Xu, Shou-qun Jiang, Yi-bing Wang, Wei-fen Li. Glycyrrhizic acid activates chicken macrophages and enhances their Salmonella-killing capacity in vitro[J]. Journal of Zhejiang University Science B, 2018, 19(10): 785-795.

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author="Bai-kui Wang, Yu-long Mao, Li Gong, Xin Xu, Shou-qun Jiang, Yi-bing Wang, Wei-fen Li",
journal="Journal of Zhejiang University Science B",
volume="19",
number="10",
pages="785-795",
year="2018",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1700506"
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%0 Journal Article
%T Glycyrrhizic acid activates chicken macrophages and enhances their Salmonella-killing capacity in vitro
%A Bai-kui Wang
%A Yu-long Mao
%A Li Gong
%A Xin Xu
%A Shou-qun Jiang
%A Yi-bing Wang
%A Wei-fen Li
%J Journal of Zhejiang University SCIENCE B
%V 19
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%@ 1673-1581
%D 2018
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1700506

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T1 - Glycyrrhizic acid activates chicken macrophages and enhances their Salmonella-killing capacity in vitro
A1 - Bai-kui Wang
A1 - Yu-long Mao
A1 - Li Gong
A1 - Xin Xu
A1 - Shou-qun Jiang
A1 - Yi-bing Wang
A1 - Wei-fen Li
J0 - Journal of Zhejiang University Science B
VL - 19
IS - 10
SP - 785
EP - 795
%@ 1673-1581
Y1 - 2018
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1700506


Abstract: 
Objective: Salmonella enterica remains a major cause of food-borne disease in humans, and Salmonella Typhimurium (ST) contamination of poultry products is a worldwide problem. Since macrophages play an essential role in controlling Salmonella infection, the aim of this study was to evaluate the effect of glycyrrhizic acid (GA) on immune function of chicken HD11 macrophages. Methods: Chicken HD11 macrophages were treated with GA (0, 12.5, 25, 50, 100, 200, 400, or 800 μg/ml) and lipopolysaccharide (LPS, 500 ng/ml) for 3, 6, 12, 24, or 48 h. Evaluated responses included phagocytosis, bacteria-killing, gene expression of cell surface molecules (cluster of differentiation 40 (CD40), CD80, CD83, and CD197) and antimicrobial effectors (inducible nitric oxide synthase (iNOS), NADPH oxidase-1 (NOX-1), interferon-γ (IFN-γ), LPS-induced tumor necrosis factor (TNF)-α factor (LITAF), interleukin-6 (IL-6), and IL-10), and production of nitric oxide (NO) and hydrogen peroxide (H2O2). Results: GA increased the internalization of both fluorescein isothiocyanate (FITC)-dextran and ST by HD11 cells and markedly decreased the intracellular survival of ST. We found that the messenger RNA (mRNA) expression of cell surface molecules (CD40, CD80, CD83, and CD197) and cytokines (IFN-γ, IL-6, and IL-10) of HD11 cells was up-regulated following GA exposure. The expression of iNOS and NOX-1 was induced by GA and thereby the productions of NO and H2O2 in HD11 cells were enhanced. Notably, it was verified that nuclear factor-κb (NF-κ;b) and c-Jun N-terminal kinase (JNK) pathways were responsible for GA-induced synthesis of NO and IFN-γ gene expression. Conclusions: Taken together, these results suggested that GA exhibits a potent immune regulatory effect to activate chicken macrophages and enhances Salmonella-killing capacity.

甘草酸对体外鸡巨噬细胞免疫和杀菌功能的影响

目的:探究甘草酸能否激活体外鸡巨噬细胞并增强其免疫和吞噬杀菌功能.
创新点:甘草酸通过核因子κB(NF-κB)和c-Jun氨基端激酶(JNK)信号通路提高一氧化氮(NO)和过氧化氢(H2O2)产生量,增强了其吞噬和杀菌的功能.
方法:以不同浓度的甘草酸(0、12.5、25、50、100、200、400和800 µg/ml)处理鸡巨噬细胞系HD11,采用荧光定量聚合酶链式反应(qPCR)和一氧化氮及过氧化氢测定试剂盒评价甘草酸对鸡巨噬细胞活化和免疫的影响,采用流式细胞技术和涂板计数法测定鸡巨噬细胞吞噬和杀菌能力.
结论:甘草酸通过NF-κB和JNK信号通路激活鸡巨噬细胞,提高免疫细胞因子等基因的表达水平和NO及H2O2的产生量,从而增强了鸡巨噬细胞吞噬和清除胞内沙门氏菌的能力.

关键词:甘草酸;鸡巨噬细胞;巨噬细胞活化;鼠伤寒沙门氏菌;核因子κB(NF-κB);c-Jun氨基端激酶(JNK)

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]Barrow PA, Huggins MB, Lovell MA, 1994. Host specificity of Salmonella infection in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system. Infect Immun, 62(10):4602-4610.

[2]Beal RK, Powers C, Wigley P, et al., 2004. Temporal dynamics of the cellular, humoral and cytokine responses in chickens during primary and secondary infection with Salmonella enterica serovar Typhimurium. Avian Pathol, 33(1):25-33.

[3]Bhattacharjee S, Bhattacharjee A, Majumder S, et al., 2012. Glycyrrhizic acid suppresses Cox-2-mediated anti-inflammatory responses during Leishmania donovani infection. J Antimicrob Chemother, 67(8):1905-1914.

[4]Bogdan C, 2001. Nitric oxide and the immune response. Nat Immunol, 2(10):907-916.

[5]Braukmann M, Methner U, Berndt A, 2015. Immune reaction and survivability of Salmonella Typhimurium and Salmonella infantis after infection of primary avian macrophages. PLoS ONE, 10(3):e0122540.

[6]Brown BN, Valentin JE, Stewart-Akers AM, et al., 2009. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials, 30(8):1482-1491.

[7]Bustin SA, Benes V, Garson JA, et al., 2009. The MIQE guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments. Clin Chem, 55(4):611-622.

[8]Cinatl J, Morgenstern B, Bauer G, et al., 2003. Glycyrrhizin, an active component of liquorice roots, and replication of SARS-associated coronavirus. Lancet, 361(9374):2045-2046.

[9]Dai JH, Iwatani Y, Ishida T, et al., 2001. Glycyrrhizin enhances interleukin-12 production in peritoneal macrophages. Immunology, 103(2):235-243.

[10]Ding AH, Nathan CF, Stuehr DJ, 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol, 141(7):2407-2412.

[11]Han Y, Niu MS, An LJ, et al., 2009. Upregulation of proinflammatory cytokines and NO production in BV-activated avian macrophage-like cell line (HD11) requires MAPK and NF-κB pathways. Int Immunopharmacol, 9(7-8):817-823.

[12]Haraga A, Ohlson MB, Miller SI, 2008. Salmonellae interplay with host cells. Nat Rev Microbiol, 6(1):53-66.

[13]He HQ, Kogut MH, 2003. CpG-ODN-induced nitric oxide production is mediated through clathrin-dependent endocytosis, endosomal maturation, and activation of PKC, MEK1/2 and p38 MAPK, and NF-κB pathways in avian macrophage cells (HD11). Cell Signal, 15(10):911-917.

[14]He HQ, Genovese KJ, Swaggerty CL, et al., 2012. A comparative study on invasion, survival, modulation of oxidative burst, and nitric oxide responses of macrophages (HD11), and systemic infection in chickens by prevalent poultry Salmonella serovars. Foodborne Pathog Dis, 9(12):1104-1110.

[15]Held TK, Xiao WH, Liang Y, et al., 1999. Gamma interferon augments macrophage activation by lipopolysaccharide by two distinct mechanisms, at the signal transduction level and via an autocrine mechanism involving tumor necrosis factor alpha and interleukin-1. Infect Immun, 67(1):206-212.

[16]Honda H, Nagai Y, Matsunaga T, et al., 2012. Glycyrrhizin and isoliquiritigenin suppress the LPS sensor Toll-like receptor 4/MD-2 complex signaling in a different manner. J Leukoc Biol, 91(6):967-976.

[17]Hua H, Liang ZF, Li WW, et al., 2012. Phenotypic and functional maturation of murine dendritic cells (DCs) induced by purified Glycyrrhizin (GL). Int Immunopharmacol, 12(3):518-525.

[18]Ibuki M, Kovacs-Nolan J, Fukui K, et al., 2011. β 1-4 mannobiose enhances Salmonella-killing activity and activates innate immune responses in chicken macrophages. Vet Immunol Immunopathol, 139(2-4):289-295.

[19]Li YL, Wang YY, Wu YP, et al., 2017. Echinacea pupurea extracts promote murine dendritic cell maturation by activation of JNK, p38 MAPK and NF-κB pathways. Dev Comp Immunol, 73:21-26.

[20]Mao YL, Wang BK, Xu X, et al., 2015. Glycyrrhizic acid promotes M1 macrophage polarization in murine bone marrow-derived macrophages associated with the activation of JNK and NF-κB. Mediators Inflamm, 2015:372931.

[21]Mastroeni P, Vazquez-Torres A, Fang FC, et al., 2000. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J Exp Med, 192(2):237-248.

[22]Matsui S, Matsumoto H, Sonoda Y, et al., 2004. Glycyrrhizin and related compounds down-regulate production of inflammatory chemokines IL-8 and eotaxin 1 in a human lung fibroblast cell line. Int Immunopharmacol, 4(13):1633-1644.

[23]Michaelis M, Geiler J, Naczk P, et al., 2010. Glycyrrhizin inhibits highly pathogenic H5N1 influenza A virus-induced pro-inflammatory cytokine and chemokine expression in human macrophages. Med Microbiol Immunol, 199(4):291-297.

[24]Mosser DM, Edwards JP, 2008. Exploring the full spectrum of macrophage activation. Nat Rev Immunol, 8(12):958-969.

[25]Nolan A, Weiden M, Kelly A, et al., 2008. CD40 and CD80/86 act synergistically to regulate inflammation and mortality in polymicrobial sepsis. Am J Respir Crit Care Med, 177(3):301-308.

[26]Pugh ND, Balachandran P, Lata H, et al., 2005. Melanin: dietary mucosal immune modulator from Echinacea and other botanical supplements. Int Immunopharmacol, 5(4):637-647.

[27]Revolledo L, Ferreira CSA, Ferreira AJP, 2009. Prevention of Salmonella Typhimurium colonization and organ invasion by combination treatment in broiler chicks. Poult Sci, 88(4):734-743.

[28]Rimaniol AC, Gras G, Clayette P, 2007. In vitro interactions between macrophages and aluminum-containing adjuvants. Vaccine, 25(37-38):6784-6792.

[29]Rosenberger CM, Finlay BB, 2002. Macrophages inhibit Salmonella Typhimurium replication through MEK/ERK kinase and phagocyte NADPH oxidase activities. J Biol Chem, 277(21):18753-18762.

[30]Scallan E, Hoekstra RM, Mahon BE, et al., 2015. An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiol Infect, 143(13):2795-2804.

[31]Setta A, Barrow PA, Kaiser P, et al., 2012. Immune dynamics following infection of avian macrophages and epithelial cells with typhoidal and non-typhoidal Salmonella enterica serovars; bacterial invasion and persistence, nitric oxide and oxygen production, differential host gene expression, NF-κB signalling and cell cytotoxicity. Vet Immunol Immunopathol, 146(3-4):212-224.

[32]Sweet MJ, Stacey KJ, Kakuda DK, et al., 1998. IFN-γ primes macrophage responses to bacterial DNA. J Interferon Cytokine Res, 18(4):263-271.

[33]Tang LL, Zhang Z, Zheng JS, et al., 2005. Phenotypic and functional characteristics of dendritic cells derived from human peripheral blood monocytes. J Zhejiang Univ-Sci B, 6(12):1176-1181.

[34]Wang LQ, He Y, Wan HF, et al., 2017. Protective mechanisms of hypaconitine and glycyrrhetinic acid compatibility in oxygen and glucose deprivation injury. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 18(7):586-596.

[35]Withanage GSK, Wigley P, Kaiser P, et al., 2005. Cytokine and chemokine responses associated with clearance of a primary Salmonella enterica serovar Typhimurium infection in the chicken and in protective immunity to rechallenge. Infect Immun, 73(8):5173-5182.

[36]List of electronic supplementary materials

[37]Fig. S1 In vitro antibacterial activity of glycyrrhizic acid against Salmonella Typhimurium

[38]Fig. S2 Effect of glycyrrhizic acid on Salmonella Typhimurium virulence gene expression in vitro

[39]Table S1 List of real-time PCR primers

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