Research progress on bacterial quorum sensing signal on host immune regulation mechanism

doi:10.3877/cma.j.issn.1674-1366.2023.02.013

Abstract

Abstract:

Quorum sensing (QS) is a system that bacteria can regulate the gene expression and change the behavior of microbiome by sensing the concentration threshold of specific quorum sensing signal molecules (QSSMs). This regulatory mechanism also plays an important role in the interaction between bacteria and host. The release of QSSMs by bacteria is sensed by the host, which initiates relevant signaling pathways to activate or inhibit gene expression. Current researches have shown that various structures of the host cells, including the cell membrane, cytoplasm, organelles and nucleus are involved in multiple signaling pathways irritated by QSSMs, and mediate relevant host immune responses. In this article, the classification of QSSMs, the research progress of the pathway and effects on hosts were reviewed.

Key words: Bacteria, Host, Quorum sensing, Immunomodulation

Xinyi Deng, Zhenyu Zeng, Xiaolan Li. Research progress on bacterial quorum sensing signal on host immune regulation mechanism[J]. Chinese Journal of Stomatological Research(Electronic Edition), 2023, 17(02): 140-147.

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References 59

[1]	Li Q，Ren Y，Fu X. Inter-kingdom signaling between gut microbiota and their host[J]. Cell Mol Life Sci，2019，76（12）：2383-2389. DOI：10.1007/s00018-019-03076-7.
[2]	Mark Welch JL，Ramírez-Puebla ST，Borisy GG. Oral microbiome geography：Micron-scale habitat and niche[J]. Cell Host Microbe，2020，28（2）：160-168. DOI：10.1016/j.chom.2020.07.009.
[3]	Xiao Y，Zou H，Li J，et al. Impact of quorum sensing signaling molecules in gram-negative bacteria on host cells：Current understanding and future perspectives[J]. Gut Microbes，2022，14（1）：2039048. DOI：10.1080/19490976.2022.2039048.
[4]	Başkan C，Sırıken B，Tüfekci EF，et al. Presence of quorum sensing system，virulence genes，biofilm formation and relationship among them and class 1 integron in carbapenem-resistant clinical Pseudomonas aeruginosa isolates[J]. Arch Microbiol，2022，204（8）：464. DOI：10.1007/s00203-022-03061-y.
[5]	Song S，Wood TK. The primary physiological roles of autoinducer 2 in escherichia coli are chemotaxis and biofilm formation[J]. Microorganisms，2021，9（2）：386. DOI：10.3390/microorganisms9020386
[6]	Vasquez JK，Tal-Gan Y，Cornilescu G，et al. Simplified AIP-Ⅱ peptidomimetics are potent inhibitors of Staphylococcus aureus AgrC quorum sensing receptors[J]. Chembiochem，2017，18（4）：413-423. DOI：10.1002/cbic.201600516.
[7]	Ma R，Qiu S，Jiang Q，et al. AI-2 quorum sensing negatively regulates rbf expression and biofilm formation in Staphylococcus aureus[J]. Int J Med Microbiol，2017，307（4/5）：257-267. DOI：10.1016/j.ijmm.2017.03.003.
[8]	Torres-Cerna CE，Morales JA，Hernandez-Vargas EA. Modeling quorum sensing dynamics and interference on Escherichia coli[J]. Front Microbiol，2019，10：1835. DOI：10.3389/fmicb.2019.01835.
[9]	Parker CT，Russell R，Njoroge JW，et al. Genetic and mechanistic analyses of the periplasmic domain of the enterohemorrhagic Escherichia coli QseC histidine sensor kinase[J]. J Bacteriol，2017，199（8）：e00861-16. DOI：10.1128/JB.00861-16.
[10]	Kravchenko VV，Kaufmann GF，Mathison JC，et al. N-（3-oxo-acyl）homoserine lactones signal cell activation through a mechanism distinct from the canonical pathogen-associated molecular pattern recognition receptor pathways[J]. J Biol Chem，2006，281（39）：28822-28830. DOI：10.1074/jbc.M606613200.
[11]	Kravchenko VV，Kaufmann GF，Mathison JC，et al. Modulation of gene expression via disruption of NF-kappaB signaling by a bacterial small molecule[J]. Science，2008，321（5886）：259-263. DOI：10.1126/science.1156499.
[12]	Khambati I，Han S，Pijnenburg D，et al. The bacterial quorum-sensing molecule，N-3-oxo-dodecanoyl-L-homoserine lactone，inhibits mediator release and chemotaxis of murine mast cells[J]. Inflamm Res，2017，66（3）：259-268. DOI：10.1007/s00011-016-1013-3.
[13]	Jaggupilli A，Singh N，de Jesus VC，et al. Characterization of the binding sites for bacterial acyl homoserine lactones（AHLs）on human bitter taste receptors（T2Rs）[J]. ACS Infect Dis，2018，4（7）：1146-1156. DOI：10.1021/acsinfecdis.8b00094.
[14]	Mcmahon DB，Kuek LE，Johnson ME，et al. The bitter end：T2R bitter receptor agonists elevate nuclear calcium and induce apoptosis in non-ciliated airway epithelial cells[J]. Cell Calcium，2022，101：102499. DOI：10.1016/j.ceca.2021.102499.
[15]	Song D，Meng J，Cheng J，et al. Pseudomonas aeruginosa quorum-sensing metabolite induces host immune cell death through cell surface lipid domain dissolution[J]. Nat Microbiol，2019，4（1）：97-111. DOI：10.1038/s41564-018-0290-8.
[16]	Moura-Alves P，Puyskens A，Stinn A，et al. Host monitoring of quorum sensing during Pseudomonas aeruginosa infection[J]. Science，2019，366（6472）：aaw1629. DOI：10.1126/science.aaw1629.
[17]	Neavin DR，Liu D，Ray B，et al. The role of the aryl hydrocarbon receptor（AHR）in immune and inflammatory diseases[J]. Int J Mol Sci，2018，19（12）：3851. DOI：10.3390/ijms19123851.
[18]	Tiaden A，Hilbi H. α-hydroxyketone synthesis and sensing by legionella and vibrio[J]. Sensors（Basel），2012，12（3）：2899-2919. DOI：10.3390/s120302899.
[19]	Simon S，Schell U，Heuer N，et al. Inter-kingdom signaling by the legionella quorum sensing molecule LAI-1 modulates cell migration through an IQGAP1-Cdc42-ARHGEF9-dependent pathway[J]. PLoS Pathog，2015，11（12）：e1005307. DOI：10.1371/journal.ppat.1005307.
[20]	Shiner EK，Terentyev D，Bryan A，et al. Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling[J]. Cell Microbiol，2006，8（10）：1601-1610. DOI：10.1111/j.1462-5822.2006.00734.x.
[21]	Schwarzer C，Ravishankar B，Patanwala M，et al. Thapsigargin blocks Pseudomonas aeruginosa homoserine lactone-induced apoptosis in airway epithelia[J]. Am J Physiol Cell Physiol，2014，306（9）：C844-C855. DOI：10.1152/ajpcell.00002.2014.
[22]	Jacobi CA，Schiffner F，Henkel M，et al. Effects of bacterial N-acyl homoserine lactones on human Jurkat T lymphocytes-OdDHL induces apoptosis via the mitochondrial pathway[J]. Int J Med Microbiol，2009，299（7）：509-519. DOI：10.1016/j.ijmm.2009.03.005.
[23]	Singh PK，Yadav VK，Kalia M，et al. Pseudomonas aeruginosa quorum-sensing molecule N-（3-oxo-dodecanoyl）-L-homoserine lactone triggers mitochondrial dysfunction and apoptosis in neutrophils through calcium signaling[J]. Med Microbiol Immunol，2019，208（6）：855-868. DOI：10.1007/s00430-019-00631-8.
[24]	Josephson H，Ntzouni M，Skoglund C，et al. Pseudomonas aeruginosa N-3-oxo-dodecanoyl-homoserine lactone impacts mitochondrial networks morphology，energetics，and proteome in host cells[J]. Front Microbiol，2020，11：1069. DOI：10.3389/fmicb.2020.01069.
[25]	Jahoor A，Patel R，Bryan A，et al. Peroxisome proliferator-activated receptors mediate host cell proinflammatory responses to Pseudomonas aeruginosa autoinducer[J]. J Bacteriol，2008，190（13）：4408-4415. DOI：10.1128/JB.01444-07.
[26]	Williams SC，Patterson EK，Carty NL，et al. Pseudomonas aeruginosa autoinducer enters and functions in mammalian cells[J]. J Bacteriol，2004，186（8）：2281-2287. DOI：10.1128/JB.186.8.2281-2287.2004.
[27]	Smith RS，Fedyk ER，Springer TA，et al. IL-8 production in human lung fibroblasts and epithelial cells activated by the Pseudomonas autoinducer N-3-oxododecanoyl homoserine lactone is transcriptionally regulated by NF-kappa B and activator protein-2[J]. J Immunol，2001，167（1）：366-374. DOI：10.4049/jimmunol.167.1.366.
[28]	Toobian D，Ghosh P，Katkar GD. Parsing the role of PPARs in macrophage processes[J]. Front Immunol，2021，12：783780. DOI：10.3389/fimmu.2021.783780.
[29]	Griffin PE，Roddam LF，Belessis YC，et al. Expression of PPARγ and paraoxonase 2 correlated with Pseudomonas aeruginosa infection in cystic fibrosis[J]. PLoS One，2012，7（7）：e42241. DOI：10.1371/journal.pone.0042241.
[30]	Cooley MA，Whittall C，Rolph MS. Pseudomonas signal molecule 3-oxo-C12-homoserine lactone interferes with binding of rosiglitazone to human PPARgamma[J]. Microbes Infect，2010，12（3）：231-237. DOI：10.1016/j.micinf.2009.12.009.
[31]	Pundir P，Liu R，Vasavda C，et al. A connective tissue mast-cell-specific receptor detects bacterial quorum-sensing molecules and mediates antibacterial immunity[J]. Cell Host Microbe，2019，26（1）：114-122.e1-e8. DOI：10.1016/j.chom.2019.06.003.
[32]	Medapati MR，Singh N，Bhagirath AY，et al. Bitter taste receptor T2R14 detects quorum sensing molecules from cariogenic Streptococcus mutans and mediates innate immune responses in gingival epithelial cells[J]. FASEB J，2021，35（3）：e21375. DOI：10.1096/fj.202000208R.
[33]	Ji YC，Sun Q，Fu CY，et al. Exogenous autoinducer-2 rescues intestinal dysbiosis and intestinal inflammation in a neonatal mouse necrotizing enterocolitis model[J]. Front Cell Infect Microbiol，2021，11：694395. DOI：10.3389/fcimb.2021.694395.
[34]	Medina-Rodriguez EM，Madorma D，O′connor G，et al. Identification of a signaling mechanism by which the microbiome regulates Th17 cell-mediated depressive-like behaviors in mice[J]. Am J Psychiatry，2020，177（10）：974-990. DOI：10.1176/appi.ajp.2020.19090960.
[35]	Elmanfi S，Ma X，Sintim HO，et al. Quorum-sensing molecule dihydroxy-2，3-pentanedione and its analogs as regulators of epithelial integrity[J]. J Periodontal Res，2018，53（3）：414-421. DOI：10.1111/jre.12528.
[36]	Fteita D，Könönen E，Gürsoy M，et al. Quorum sensing molecules regulate epithelial cytokine response and biofilm-related virulence of three Prevotella species[J]. Anaerobe，2018，54：128-135. DOI：10.1016/j.anaerobe.2018.09.001.
[37]	Sperandio V，Torres AG，Jarvis B，et al. Bacteria-host communication：The language of hormones[J]. Proc Natl Acad Sci U S A，2003，100（15）：8951-8956. DOI：10.1073/pnas.1537100100.
[38]	Lustri BC，Sperandio V，Moreira CG. Bacterial Chat：Intestinal metabolites and signals in host-microbiota-pathogen interactions[J]. Infect Immun，2017，85（12）：e00476-17. DOI：10.1128/IAI.00476-17.
[39]	Barrasso K，Watve S，Simpson CA，et al. Dual-function quorum-sensing systems in bacterial pathogens and symbionts[J]. PLoS Pathog，2020，16（10）：e1008934. DOI：10.1371/journal.ppat.1008934.
[40]	Bao L，Yu J，Zhong H，et al. Expression of toll-like receptors in T lymphocytes stimulated with N-（3-oxododecanoyl）-L-homoserine lactone from Pseudomonas aeruginosa[J]. Apmis，2017，125（6）：553-557. DOI：10.1111/apm.12690.
[41]	Vikström E，Magnusson KE，Pivoriunas A. The Pseudomonas aeruginosa quorum-sensing molecule N-（3-oxododecanoyl）-L-homoserine lactone stimulates phagocytic activity in human macrophages through the p38 MAPK pathway[J]. Microbes Infect，2005，7（15）：1512-1518. DOI：10.1016/j.micinf.2005.05.012.
[42]	Wagner C，Zimmermann S，Brenner-Weiss G，et al. The quorum-sensing molecule N-3-oxododecanoyl homoserine lactone（3OC12-HSL）enhances the host defence by activating human polymorphonuclear neutrophils（PMN）[J]. Anal Bioanal Chem，2007，387（2）：481-487. DOI：10.1007/s00216-006-0698-5.
[43]	Shin J，Ahn SH，Kim SH，et al. N-3-oxododecanoyl homoserine lactone exacerbates endothelial cell death by inducing receptor-interacting protein kinase 1-dependent apoptosis[J]. Am J Physiol Cell Physiol，2021，321（4）：C644-C653. DOI：10.1152/ajpcell.00094.2021.
[44]	Tao S，Xiong Y，Han D，et al. N-（3-oxododecanoyl）-l-homoserine lactone disrupts intestinal epithelial barrier through triggering apoptosis and collapsing extracellular matrix and tight junction[J]. J Cell Physiol，2021，236（8）：5771-5784. DOI：10.1002/jcp.30261.
[45]	Zimmermann S，Wagner C，Müller W，et al. Induction of neutrophil chemotaxis by the quorum-sensing molecule N-（3-oxododecanoyl）-L-homoserine lactone[J]. Infect Immun，2006，74（10）：5687-5692. DOI：10.1128/IAI.01940-05.
[46]	Guo J，Yoshida K，Ikegame M，et al. Quorum sensing molecule N-（3-oxododecanoyl）-L-homoserine lactone：An all-rounder in mammalian cell modification[J]. J Oral Biosci，2020，62（1）：16-29. DOI：10.1016/j.job.2020.01.001.
[47]	Zargar A，Quan DN，Carter KK，et al. Bacterial secretions of nonpathogenic Escherichia coli elicit inflammatory pathways：A closer investigation of interkingdom signaling[J]. mBio，2015，6（2）：e00025. DOI：10.1128/mBio.00025-15.
[48]	Sears CL. The who，where and how of fusobacteria and colon cancer[J]. Elife，2018，7：e28434. DOI：10.7554/eLife.28434.
[49]	Wu J，Li K，Peng W，et al. Autoinducer-2 of Fusobacterium nucleatum promotes macrophage M1 polarization via TNFSF9/IL-1β signaling[J]. Int Immunopharmacol，2019，74：105724. DOI：10.1016/j.intimp.2019.105724.
[50]	den Breems NY，Eftimie R. The re-polarisation of M2 and M1 macrophages and its role on cancer outcomes[J]. J Theor Biol，2016，390：23-39. DOI：10.1016/j.jtbi.2015.10.034.
[51]	Li Q，Peng W，Wu J，et al. Autoinducer-2 of gut microbiota，a potential novel marker for human colorectal cancer，is associated with the activation of TNFSF9 signaling in macrophages[J]. Oncoimmunology，2019，8（10）：e1626192. DOI：10.1080/2162402X.2019.1626192.
[52]	Wu J，Wang Y，Jiang Z. Immune induction identified by TMT proteomics analysis in Fusobacterium nucleatum autoinducer-2 treated macrophages[J]. Expert Rev Proteomics，2020，17（2）：175-185. DOI：10.1080/14789450.2020.1738223.
[53]	Tateda K，Ishii Y，Horikawa M，et al. The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils[J]. Infect Immun，2003，71（10）：5785-5793. DOI：10.1128/IAI.71.10.5785-5793.2003.
[54]	Guo J，Wang Z，Weng Y，et al. N-（3-oxododecanoyl）-homoserine lactone regulates osteoblast apoptosis and differentiation by mediating intracellular calcium[J]. Cell Signal，2020，75：109740. DOI：10.1016/j.cellsig.2020.109740.
[55]	Kumar SR，Bryan JN，Eaton AM，et al. Differential modulation of transcription factors and cytoskeletal proteins in prostate carcinoma cells by a bacterial lactone[J]. Biomed Res Int，2018：6430504. DOI：10.1155/2018/6430504.
[56]	Nandakumar N，Dandela R，Gopas J，et al. Quorum sensing modulators exhibit cytotoxicity in Hodgkin′s lymphoma cells and interfere with NF-κB signaling[J]. Bioorg Med Chem Lett，2017，27（13）：2967-2973. DOI：10.1016/j.bmcl.2017.05.012.
[57]	Balhouse BN，Patterson L，Schmelz EM，et al. N-（3-oxododecanoyl）-L-homoserine lactone interactions in the breast tumor microenvironment：Implications for breast cancer viability and proliferation in vitro[J]. PLoS One，2017，12（7）：e0180372. DOI：10.1371/journal.pone.0180372.
[58]	Chai H，Hazawa M，Shirai N，et al. Functional properties of synthetic N-acyl-L-homoserine lactone analogs of quorum-sensing gram-negative bacteria on the growth of human oral squamous carcinoma cells[J]. Invest New Drugs，2012，30（1）：157-163. DOI：10.1007/s10637-010-9544-x.
[59]	Scheper MA，Shirtliff ME，Meiller TF，et al. Farnesol，a fungal quorum-sensing molecule triggers apoptosis in human oral squamous carcinoma cells[J]. Neoplasia，2008，10（9）：954-963. DOI：10.1593/neo.08444.

QSSM	来源	结构特点	分泌方式
AI-1	G^-菌 eg.铜绿假单胞菌	AHL之间的主要差异是N侧链的长度、3-碳位置的取代基以及侧链中不饱和键的数量	自由扩散
AIP	G⁺菌 eg.金黄色葡萄球菌	7 ~ 9个残基组成的短肽，由C末端的羧酸和距离C末端4个氨基酸的半胱氨酸残基形成功能硫酯键，与短N末端共同构成	膜通道蛋白
AI-2	G⁺菌/G^-菌eg.哈氏弧菌	不稳定前体DPD重排成的不同结构的分子	自由扩散
AI-3	肠出血性大肠埃希菌	-	-

QSSM	来源	结构特点	分泌方式
AI-1	G^-菌 eg.铜绿假单胞菌	AHL之间的主要差异是N侧链的长度、3-碳位置的取代基以及侧链中不饱和键的数量	自由扩散
AIP	G⁺菌 eg.金黄色葡萄球菌	7 ~ 9个残基组成的短肽，由C末端的羧酸和距离C末端4个氨基酸的半胱氨酸残基形成功能硫酯键，与短N末端共同构成	膜通道蛋白
AI-2	G⁺菌/G^-菌eg.哈氏弧菌	不稳定前体DPD重排成的不同结构的分子	自由扩散
AI-3	肠出血性大肠埃希菌	-	-

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