Outer membrane vesicles from Haemophilus parasuis activate caspase-11 and NLRP3 inflammasome to induce the secretion of IL-1β and IL-18
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  • LI Yan

    LI Yan

    Institute of Animal Health, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, Guangdong, China;Key Laboratory of Livestock Disease Prevention of Guangdong Province, Guangzhou 510640, Guangdong, China;Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, Guangdong, China;Maoming Branch Center of Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, Guangdong, China
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  • YANG Jun

    YANG Jun

    Institute of Animal Health, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, Guangdong, China;Key Laboratory of Livestock Disease Prevention of Guangdong Province, Guangzhou 510640, Guangdong, China;Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, Guangdong, China;Maoming Branch Center of Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, Guangdong, China
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  • ZHAI Shaolun

    ZHAI Shaolun

    Institute of Animal Health, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, Guangdong, China;Key Laboratory of Livestock Disease Prevention of Guangdong Province, Guangzhou 510640, Guangdong, China;Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, Guangdong, China;Maoming Branch Center of Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, Guangdong, China
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  • CHU Pinpin

    CHU Pinpin

    Institute of Animal Health, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, Guangdong, China;Key Laboratory of Livestock Disease Prevention of Guangdong Province, Guangzhou 510640, Guangdong, China;Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, Guangdong, China;Maoming Branch Center of Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, Guangdong, China
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  • BIAN Zhibiao

    BIAN Zhibiao

    Institute of Animal Health, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, Guangdong, China;Key Laboratory of Livestock Disease Prevention of Guangdong Province, Guangzhou 510640, Guangdong, China;Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, Guangdong, China;Maoming Branch Center of Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, Guangdong, China
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  • ZHANG Kunli

    ZHANG Kunli

    Institute of Animal Health, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, Guangdong, China;Key Laboratory of Livestock Disease Prevention of Guangdong Province, Guangzhou 510640, Guangdong, China;Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, Guangdong, China;Maoming Branch Center of Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, Guangdong, China
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  • LI Chunling

    LI Chunling

    Institute of Animal Health, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, Guangdong, China;Key Laboratory of Livestock Disease Prevention of Guangdong Province, Guangzhou 510640, Guangdong, China;Scientific Observation and Experiment Station of Veterinary Drugs and Diagnostic Techniques of Guangdong Province, Ministry of Agriculture and Rural Affairs, Guangzhou 510640, Guangdong, China;Maoming Branch Center of Guangdong Laboratory for Lingnan Modern Agricultural Science and Technology, Maoming 525000, Guangdong, China
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    Abstract:

    [Background] Haemophilus parasuis can cause a variety of inflammatory reactions and high mortality, while the inflammatory mechanism remains unclear.[Objective] To study the activation of caspase-11 and NOD-like receptor family pyrin domain containing protein 3 (NLRP3) inflammasome in RAW264.7 cells by H.parasuis outer membrane vesicles (OMVs) and the key role of caspase-11 in the OMVs-induced expression of inflammatory cytokines. [Methods] The RAW264.7 cells were infected with H.parasuis OMVs and collected 6, 12, and 24 h post infection. RT-PCR was employed to determine the mRNA levels of caspase-11, NLRP3, apoptosis-associated speck-like protein containing a caspase recruitment domain (ASC), and caspase-1. Western blotting was employed to determine the protein levels of caspase-11, NLRP3, ASC, and caspase-1 48 h post infection. Enzyme-linked immunosorbent assay (ELISA) was employed to determine the levels of interleukin-1β (IL-1β) and IL-18 in the cell supernatants 6, 12, 24, 48, and 72 h post infection. After the RAW264.7 cells were stimulated with different concentrations of OMVs (0, 2.5, 10, 25, 50, and 100 μg/mL) for 24 h, the cell supernatants were collected for the measurement of IL-1β and IL-18 levels by ELISA. The RAW264.7 cells with the silencing of caspase-11 were established and then infected with OMVs, and the supernatants were collected for the measurement of IL-1β and IL-18 levels 12, 24 and 48 h post infection. [Results] The mRNA level of caspase-11 was up-regulated in the RAW264.7 cells 6, 12 and 24 h post infection with OMVs (P<0.01). The mRNA level of NLRP3 was higher than that in the control group 6 and 24 h post infection (P<0.01). The mRNA level of ASC was significantly lower than that in the control group 12 and 24 h post infection (P<0.05). The mRNA level of caspase-1 was significantly higher than that in the control group 6, 12, and 24 h post infection (P<0.05). Western blotting showed that the expression levels of caspase-11, NLRP3, ASC, and caspase-1 were up-regulated after infection with OMVs. The level of IL-1β elevated in a time-dependent manner after the cells were stimulated with OMVs for 12, 24, 48 and 72 h and was higher than that in the control group (P<0.01), and the level of IL-18 was higher than that in the control group at the time points of 6, 12, 24, 48 and 72 h (P<0.05). When the cells were stimulated with different concentrations of OMVs, the inflammatory effect increased in a dose-dependent manner. The level of IL-1β in the caspase-11-silenced cells stimulated with OMVs was lower than that in the non-silenced group at the time points of 12, 24 and 48 h (P<0.05), and the level of IL-18 showed the same trend as that of IL-1β at the time points of 24 and 48 h (P<0.05). [Conclusion] The OMVs of H.parasuis play an important role in the inflammatory response induced by H. parasuis. OMVs can induce the activation of non-canonical NLRP3 inflammasome signaling pathway mediated by caspase-11 in RAW264.7 cells.

    Reference
    [1] Macedo N, Rovira A, Torremorell M. Haemophilus parasuis:infection, immunity and enrofloxacin[J]. Veterinary Research, 2015, 46:128
    [2] Rafiee M, Blackall PJ. Establishment, validation and use of the Kielstein-Rapp-Gabrielson serotyping scheme for Haemophilus parasuis[J]. Australian Veterinary Journal, 2000, 78(3):172-174
    [3] Del Río ML, Gutiérrez CB, Rodríguez Ferri EF. Value of indirect hemagglutination and coagglutination tests for serotyping Haemophilus parasuis[J]. Journal of Clinical Microbiology, 2003, 41(2):880-882
    [4] Kotas ME, Medzhitov R. Homeostasis, inflammation, and disease susceptibility[J]. Cell, 2015, 160(5):816-827
    [5] Mangan MSJ, Olhava EJ, Roush WR, Seidel HM, Glick GD, Latz E. Targeting the NLRP3 inflammasome in inflammatory diseases[J]. Nature Reviews Drug Discovery, 2018, 17(8):588-606
    [6] Broz P, Dixit VM. Inflammasomes:mechanism of assembly, regulation and signalling[J]. Nature Reviews Immunology, 2016, 16(7):407-420
    [7] Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA. Cytoplasmic LPS activates caspase-11:implications in TLR4-independent endotoxic shock[J]. Science, 2013, 341(6151):1250-1253
    [8] Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, Miyake K, Zhang J, Lee WP, Muszyński A, et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4[J]. Science, 2013, 341(6151):1246-1249
    [9] O՚Donoghue EJ, Krachler AM. Mechanisms of outer membrane vesicle entry into host cells[J]. Cellular Microbiology, 2016, 18(11):1508-1517
    [10] Bitto NJ, Kaparakis-Liaskos M. The therapeutic benefit of bacterial membrane vesicles[J]. International Journal of Molecular Sciences, 2017, 18(6):1287
    [11] Ünal CM, Schaar V, Riesbeck K. Bacterial outer membrane vesicles in disease and preventive medicine[J]. Seminars in Immunopathology, 2011, 33(5):395-408
    [12] Pathirana RD, Kaparakis-Liaskos M. Bacterial membrane vesicles:biogenesis, immune regulation and pathogenesis[J]. Cellular Microbiology, 2016, 18(11):1518-1524
    [13] Bouchet B, Vanier G, Jacques M, Gottschalk M. Interactions of Haemophilus parasuis and its LOS with porcine brain microvascular endothelial cells[J]. Veterinary Research, 2008, 39(5):42
    [14] Fu SL, Xu L, Li SL, Qiu YS, Liu Y, Wu ZY, Ye C, Hou YQ, Hu CAA. Baicalin suppresses NLRP3 inflammasome and nuclear factor-kappa B (NF-κB) signaling during Haemophilus parasuis infection[J]. Veterinary Research, 2016, 47(1):80
    [15] Ma B, Hua KX, Zhou SS, Zhou HF, Chen YS, Luo R, Bi DR, Zhou R, He QG, Jin H. Haemophilus parasuis infection activates NOD1/2-RIP2 signaling pathway in PK-15 cells[J]. Developmental and Comparative Immunology, 2018, 79:158-165
    [16] Bishop DG, Work E. An extracellular glycolipid produced by Escherichia coli grown under lysine-limiting conditions[J]. The Biochemical Journal, 1965, 96(2):567-576
    [17] Jan AT. Outer membrane vesicles (OMVs) of gram-negative bacteria:a perspective update[J]. Frontiers in Microbiology, 2017, 8:1053
    [18] Sartorio MG, Pardue EJ, Feldman MF, Haurat MF. Bacterial outer membrane vesicles:from discovery to applications[J]. Annual Review of Microbiology, 2021, 75:609-630
    [19] Cecil JD, O՚brien-Simpson NM, Lenzo JC, Holden JA, Singleton W, Perez-Gonzalez A, Mansell A, Reynolds EC. Outer membrane vesicles prime and activate macrophage inflammasomes and cytokine secretion in vitro and in vivo[J]. Frontiers in Immunology, 2017, 8:1017
    [20] Yu YJ, Wang XH, Fan GC. Versatile effects of bacterium-released membrane vesicles on mammalian cells and infectious/inflammatory diseases[J]. Acta Pharmacologica Sinica, 2018, 39(4):514-533
    [21] 朱宏亮, 陈帆, 吴豫, 易伟, 杨志刚. 铜绿假单胞菌外膜囊泡经TLR4/NF-κB通路诱导巨噬细胞炎症反应[J]. 国际免疫学杂志, 2020, 43(3):257-262. Zhu HL, Chen F, Wu Y, Yi W, Yang ZG. Pseudomonas aeruginosa outer membrane vesicles induces the inflammatory response in macrophages via the TLR4/NF-κB pathways[J]. International Journal of Immunology, 2020, 43(3):257-262(in Chinese)
    [22] Zhao KL, Deng X, He C, Yue BS, Wu M. Pseudomonas aeruginosa outer membrane vesicles modulate host immune responses by targeting the toll-like receptor 4 signaling pathway[J]. Infection and Immunity, 2013, 81(12):4509洭椴挵攱?愼晢瑲放牛′栳敝洠慆瑬潥灥潴楷敯瑯楤挠?獊琬攠浌?捥攠汍汋?琬爠慓湩獮灧汬慥湴瑯慮琠楗漬渠孁?嵨??卨捡楮攠湁琬椠晌楥捥?前敃瀬漠牏琦猣?″祝?????????????扯牮?孎??崠?卯睯慫渠獁潄測??噵???敹渠杁????呡楳湨杰??倠奓??吠桒敥?乮?剬偤??楅湃昬氠慥浴洠慡獬漮洠敍?浴潡汢敯捬畩汣愠牲?慭捯瑤楥癬慩瑮楧漬渠?慮湦摬?牭敭条畳汯慭瑥椠潡湣?瑩潶?瑴桩敯牮愬瀠敡畮瑤椠捰獹孲?嵰??乳慩瑳甠物敮?剭敡癣楲敯睰獨??浥浳甠湳潴汩潭杵祬???つㄠ?????????????????扡牳?孧??嵧??慡瑬楩歳愼椯湩放渠?卮??乩祴浳愠湯?呴????祥灭牢祲歡?坥???畳湩捣瑬楥潳湛?慝渮搠?牲敯杮畴汩慥瑲楳漠湩?漠晃?湬潬湵捬慡湲漠湡楮捤愠汉?捦慥獣灴慩獯敮????????楯湬景汧慹洬洠愲猰漱洷攬嬠?崺?‵?漼畢牲渾慛氲?潝映??浮浧甠湗潗氬漠杇祵??慂氬琠楊浩潡爠敗???摊??????????は???べ????????????ど???扩牳?嬯??崭?噥慲湩慶橥慤?卯???割甠獭獥潭??????敶桥汳?????愠湰敲牯橭敯整????奬慣湩武潩癣慡?????敯獦栠浶畡歳档?卬???剳慭瑯桯楴湨愠浭?噳?????慥捬瑬敳爠楴慨汲?潵畧瑨攠牅?测攱洯戲爭慒湕敎?瘲敛獊楝挮氠敆獅?浓攠摏楰慥瑮攠?捩祯琬漠猲漰氱椶挬?氶漨挱愲氩椺稱愳琱椰漭渱″漱昹??偲匾?愲渵摝?捆慲獩灥慤獲敩??ㄠ?愬挠瑇楲癵慢瑥楲漠湃嬬?嵎???整汨氠??㈠ぐ?????????????に??ㄠ????扯牳?孨??崬??汬楴穭慡杮慮爠慆礬??????潥浲攠獐??呁剮???畫楨浯慶爠慏攬猠??卨??創畭浬戻潦?????漮稠扏潵牴?????佭汢楲癡敮楥爠慶?即????潳爠敯湦漠?????慮湮潥湲楥捬慬污?慦湯摲?湹潴湨?捡愼港潩渾椺换慩汯?楥湮晥汳慩浳洬愠獣潯浭数?慳捩瑴楩癯慮琬椠潡湮?戠祶?潲畵瑬敥牮?浥敛浊扝爮愠湍敯?癥散獵楬捡汲攠獏?摡敬爠楍癩散摲?晢物潯浬??楹??漲爰搱攵琬攠氳氰愨?瀩攺爴琵由猭猴椷猳??楲?孛?崶???物潲湬瑡楳敨牡獲?椠湍??洠浈甦湯潳汬潡杳票???べ㈠ぅ??ㄠ??????J, Lyberg T. Outer membrane vesicles from Neisseria meningitidis:effects on cytokine production in human whole blood[J]. Cytokine, 2001, 13(2):91-97
    [27] Chmiela M, Walczak N, Rudnicka K. Helicobacter pylori outer membrane vesicles involvement in the infection development and Helicobacter pylori-related diseases[J]. Journal of Biomedical Science, 2018, 25(1):78
    [28] Zhang KL, Chu PP, Song S, Yang DX, Bian ZB, Li Y, Gou HC, Jiang ZY, Cai RJ, Li CL. Proteome analysis of outer membrane vesicles from a highly virulent strain of Haemophilus parasuis[J]. Frontiers in Veterinary Science, 2021, 8:756764
    [29] Broz P. Inflammasome assembly:the wheels are turning[J]. Cell Research, 2015, 25(12):1277-1278
    [30] Palazon-Riquelme P, Lopez-Castejon G. The inflammasomes, immune guardians at defence barriers[J]. Immunology, 2018, 155(3):320-330
    [31] Lamkanfi M, Dixit VM. Mechanisms and functions of inflammasomes[J]. Cell, 2014, 157(5):1013-1022
    [32] Qiao JL, Huang YJ, Xia Y, Chu PP, Yao HN, Xu LY, Qi KM, Liu Y, Xu KL, Zeng LY. Busulfan and cyclosphamide induce liver inflammation through NLRP3 activation in
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LI Yan, YANG Jun, ZHAI Shaolun, CHU Pinpin, BIAN Zhibiao, ZHANG Kunli, LI Chunling. Outer membrane vesicles from Haemophilus parasuis activate caspase-11 and NLRP3 inflammasome to induce the secretion of IL-1β and IL-18[J]. Microbiology China, 2022, 49(12): 5171-5183

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History
  • Received:July 13,2022
  • Revised:September 21,2022
  • Online: December 06,2022
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