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Review

Impact of quorum sensing signaling molecules in gram-negative bacteria on host cells: current understanding and future perspectives

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Article: 2039048 | Received 08 Oct 2021, Accepted 31 Jan 2022, Published online: 19 Feb 2022

References

  • Dunny GM, Leonard BA. Cell-cell communication in gram-positive bacteria. Annu Rev Microbiol. 1997;51:527–19. doi:10.1146/annurev.micro.51.1.527.
  • Surette MG, Bassler BL. Regulation of autoinducer production in salmonella typhimurium. Mol Microbiol. 1999;31:585–595. doi:10.1046/j.1365-2958.1999.01199.x.
  • Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol. 1994;176:269–275. doi:10.1128/jb.176.2.269-275.1994.
  • Whiteley M, Diggle SP, Greenberg EP. Progress in and promise of bacterial quorum sensing research. Nature. 2017;551:313–320. doi:10.1038/nature24624.
  • Tomasz A. Control of the competent state in Pneumococcus by a hormone-like cell product: an example for a new type of regulatory mechanism in bacteria. Nature. 1965;208:155–159. doi:10.1038/208155a0.
  • Thompson JA, Oliveira RA, Djukovic A, Ubeda C, Xavier KB. Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota. Cell Rep. 2015;10:1861–1871. doi:10.1016/j.celrep.2015.02.049.
  • Papenfort K, Bassler BL. Quorum sensing signal–response systems in Gram-negative bacteria. Nat Rev Microbiol. 2016;14(9):576–588. doi:10.1038/nrmicro.2016.89.
  • Schuster M, Sexton DJ, Diggle SP, Greenberg EP. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol. 2013;67(1):43–63. doi:10.1146/annurev-micro-092412-155635.
  • Nealson KH. Autoinduction of bacterial luciferase. Occurrence, mechanism and significance. Arch Microbiol. 1977;112:73–79. doi:10.1007/BF00446657.
  • Smith D, Wang JH, Swatton JE, Davenport P, Price B, Mikkelsen H, Stickland H, Nishikawa K, Gardiol N, Spring DR, et al. Variations on a theme: diverse N-acyl homoserine lactone-mediated quorum sensing mechanisms in gram-negative bacteria. Sci Prog. 2006;89:167–211. doi:10.3184/003685006783238335.
  • Nievas F, Bogino P, Sorroche F, Giordano W. Detection, characterization, and biological effect of quorum-sensing signaling molecules in peanut-nodulating bradyrhizobia. Sensors. 2012;12:2851–2873. doi:10.3390/s120302851.
  • Brelles-Marino G, Bedmar EJ. Detection, purification and characterisation of quorum-sensing signal molecules in plant-associated bacteria. J Biotechnol. 2001;91:197–209. doi:10.1016/S0168-1656(01)00330-3.
  • Antonioli L, Blandizzi C, Pacher P, Guilliams M, Hasko G. Quorum sensing in the immune system. Nat Rev Immunol. 2018;18(9):563–568. doi:10.1038/s41577-018-0040-4.
  • Bandyopadhaya A, Tzika AA, and Rahme LG. Pseudomonas aeruginosa quorum sensing molecule alters skeletal muscle protein homeostasis by perturbing the antioxidant defense system. mBio, 10 : 2019;e02211–19. doi:10.1128/mBio.02211-19.
  • Kariminik A, Baseri-Salehi M, Kheirkhah B. Pseudomonas aeruginosa quorum sensing modulates immune responses: an updated review article. Immunol Lett. 2017;190:1–6. doi:10.1016/j.imlet.2017.07.002.
  • Kendall MM, Sperandio V. What a dinner party! mechanisms and functions of interkingdom signaling in host-pathogen associations. mBio 2016. 7:e01748.10.1128/mBio.01748-15.
  • Patankar AV, Gonzalez JE. Orphan LuxR regulators of quorum sensing. FEMS Microbiol Rev. 2009;33:739–756. doi:10.1111/j.1574-6976.2009.00163.x.
  • Chong G, Kimyon O, Manefield M. Quorum sensing signal synthesis may represent a selective advantage independent of its role in regulation of bioluminescence in vibrio fischeri. PloS one. 2013;8:e67443. doi:10.1371/journal.pone.0067443.
  • Bruger EL, Waters CM, Elliot MA. Bacterial quorum sensing stabilizes cooperation by optimizing growth strategies. Appl Environ Microbiol. 2016;82:6498–6506. doi:10.1128/AEM.01945-16.
  • Venturi V, Bertani I, Kerenyi A, Netotea S, Pongor S, Herman C. Co-swarming and local collapse: quorum sensing conveys resilience to bacterial communities by localizing cheater mutants in Pseudomonas aeruginosa. PloS one. 2010;5:e9998. doi:10.1371/journal.pone.0009998.
  • Popat R, Crusz SA, Messina M, Williams P, West SA, and Diggle SP. Quorum-sensing and cheating in bacterial biofilms. Proceedings Biological sciences . 2012; 279(1748) :4765–4771. doi:10.1098/rspb.2012.1976.
  • Harrison F, Muruli A, Higgins S, Diggle SP, McCormick BA. Development of and ex vivo porcine lung model for studying growth, virulence, and signaling of pseudomonas aeruginosa. Infect Immun. 2014;82:3312–3323. doi:10.1128/IAI.01554-14.
  • Valiente E, Bruhn JB, Nielsen KF, Larsen JL, Roig FJ, Gram L, Amaro C. Vibrio vulnificus produces quorum sensing signals of the AHL-class. FEMS Microbiol Ecol. 2009;69:16–26. doi:10.1111/j.1574-6941.2009.00691.x.
  • Elmahdi S, DaSilva LV, Parveen S. Antibiotic resistance of vibrio parahaemolyticus and vibrio vulnificus in various countries: a review. Food Microbiol. 2016;57:128–134. doi:10.1016/j.fm.2016.02.008.
  • Bruhn JB, Dalsgaard I, Nielsen KF, Buchholtz C, Larsen JL, Gram L. Quorum sensing signal molecules (acylated homoserine lactones) in gram-negative fish pathogenic bacteria. Dis Aquat Organ. 2005;65:43–52. doi:10.3354/dao065043.
  • Vincent AT, Hosseini N, Charette SJ. The Aeromonas salmonicida plasmidome: a model of modular evolution and genetic diversity. Ann N Y Acad Sci. 2021;1488:16–32. doi:10.1111/nyas.14503.
  • Wrobel A, Leo JC, and Linke D. Overcoming fish defences: the virulence factors of yersinia ruckeri. Genes. 2019;10: 700 doi: 10.3390/genes10090700.
  • Lang J, Faure D. Functions and regulation of quorum-sensing in agrobacterium tumefaciens. Front Plant Sci. 2014;5:14. doi:10.3389/fpls.2014.00014.
  • Milton DL, Hardman A, Camara M, Chhabra SR, Bycroft BW, Stewart GS, Williams, P . Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone. J Bacteriol. 1997;179:3004–3012. doi:10.1128/jb.179.9.3004-3012.1997.
  • Engebrecht J, and Silverman M. Identification of genes and gene products necessary for bacterial bioluminescence. Proceedings of the National Academy of Sciences of the United States of America. 1984,P NATL ACAD SCI USA; 81 :4154–4158.
  • Fuqua C, Winans SC, Greenberg EP. Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol. 1996;50:727–751. doi:10.1146/annurev.micro.50.1.727.
  • Hanzelka BL, Greenberg EP. Evidence that the N-terminal region of the vibrio fischeri luxr protein constitutes an autoinducer-binding domain. J Bacteriol. 1995;177:815–817. doi:10.1128/jb.177.3.815-817.1995.
  • Zhu J, and Winans SC. The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proceedings of the National Academy of Sciences of the United States of America. P NATL ACAD SCI USA ,2001; 98:1507–1512.
  • Winson MK, Swift S, Fish L, Throup JP, Jorgensen F, Chhabra SR, Bycroft BW, Williams P, Stewart GS . Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett. 1998;163:185–192. doi:10.1111/j.1574-6968.1998.tb13044.x.
  • Ahmer BM. Cell-to-cell signalling in escherichia coli and salmonella enterica. Mol Microbiol. 2004;52:933–945. doi:10.1111/j.1365-2958.2004.04054.x.
  • Lee J, Maeda T, Hong SH, Wood TK. Reconfiguring the quorum-sensing regulator SdiA of escherichia coli to control biofilm formation via indole and N-acylhomoserine lactones. Appl Environ Microbiol. 2009;75:1703–1716. doi:10.1128/AEM.02081-08.
  • Lee J, Wu J, Deng Y, Wang J, Wang C, Wang J, Chang C, Dong Y, Williams P, Zhang L-H, et al. A cell-cell communication signal integrates quorum sensing and stress response. Nat Chem Biol. 2013;9(5):339–343. doi:10.1038/nchembio.1225.
  • Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH, Quax WJ. The multiple signaling systems regulating virulence in pseudomonas aeruginosa. Microbiology and Molecular Biology Reviews: MMBR. 2012;76(1):46–65. doi:10.1128/MMBR.05007-11.
  • Farrow JM 3rd, Pesci EC. Two distinct pathways supply anthranilate as a precursor of the pseudomonas quinolone signal. J Bacteriol. 2007;189(9):3312–3333. doi:10.1128/JB.00209-07.
  • Bredenbruch F, Nimtz M, Wray V, Morr M, Muller R, Haussler S. Biosynthetic pathway of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines. J Bacteriol. 2005;187:3630–3635. doi:10.1128/JB.187.11.3630-3635.2005.
  • Ventre I, Goodman AL, Vallet-Gely I, Vasseur P, Soscia C, Molin S, Bleves S, Lazdunski A, Lory S, Filloux A . Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proceedings of the National Academy of Sciences of the United States of America. P NATL ACAD SCI USA, 2006; 103:171–176.
  • Ritchie AJ, Whittall C, Lazenby JJ, Chhabra SR, Pritchard DI, Cooley MA. The immunomodulatory Pseudomonas aeruginosa signalling molecule N-(3-oxododecanoyl)-L-homoserine lactone enters mammalian cells in an unregulated fashion. Immunol Cell Biol. 2007;85:596–602. doi:10.1038/sj.icb.7100090.
  • Schwarzer C, Fu Z, Shuai S, Babbar S, Zhao G, Li C, Machen TE . Pseudomonas aeruginosa homoserine lactone triggers apoptosis and Bak/Bax-independent release of mitochondrial cytochrome C in fibroblasts. Cell Microbiol. 2014;16:1094–1104. doi:10.1111/cmi.12263.
  • Schwarzer C, Ravishankar B, Patanwala M, Shuai S, Fu Z, Illek B, Fischer H, Machen TE . Thapsigargin blocks Pseudomonas aeruginosa homoserine lactone-induced apoptosis in airway epithelia. Am J Physiol Cell Physiol. 2014;306:C844–55. doi:10.1152/ajpcell.00002.2014.
  • Taguchi R, Tanaka S, Joe GH, Maseda H, Nomura N, Ohnishi J, Ishizuka S, Shimizu H, Miyazaki H. Mucin 3 is involved in intestinal epithelial cell apoptosis via N -(3-oxododecanoyl)- -homoserine lactone-induced suppression of Akt phosphorylation. Am J Physiol Cell Physiol. 2014;307:C162–8. doi:10.1152/ajpcell.00271.2013.
  • Shimizu H, Baba N, Nose T, Taguchi R, Tanaka S, Joe GH, Maseda H, Nomura N, Hagio M, Lee JY . Activity of ERK regulates mucin 3 expression and is involved in undifferentiated Caco-2 cell death induced by 3-oxo-C12-homoserine lactone. Bioscience, Biotechnology, and Biochemistry. 2015;79:937–942. doi:10.1080/09168451.2015.1006570.
  • Holm A, Magnusson KE, Vikstrom E. Pseudomonas aeruginosa N-3-oxo-dodecanoyl-homoserine lactone elicits changes in cell volume, morphology, and AQP9 characteristics in macrophages. Front Cell Infect Microbiol. 2016;6:32. doi:10.3389/fcimb.2016.00032.
  • Vikstrom 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. Microbes and Infection. 2005;7:1512–1518. doi:10.1016/j.micinf.2005.05.012.
  • Kaufmann GF, Park J, Mee JM, Ulevitch RJ, Janda KD. The quorum quenching antibody RS2-1G9 protects macrophages from the cytotoxic effects of the Pseudomonas aeruginosa quorum sensing signalling molecule N-3-oxo-dodecanoyl-homoserine lactone. Mol Immunol. 2008;45:2710–2714. doi:10.1016/j.molimm.2008.01.010.
  • Horikawa M, Tateda K, Tuzuki E, Ishii Y, Ueda C, Takabatake T, Miyairi S, Yamaguchi K, Ishiguro M. Synthesis of Pseudomonas quorum-sensing autoinducer analogs and structural entities required for induction of apoptosis in macrophages. Bioorg Med Chem Lett. 2006;16:2130–2133. doi:10.1016/j.bmcl.2006.01.054.
  • Rennemeier C, Frambach T, Hennicke F, Dietl J, Staib P. Microbial quorum-sensing molecules induce acrosome loss and cell death in human spermatozoa. Infect Immun. 2009;77:4990–4997. doi:10.1128/IAI.00586-09.
  • Scheper MA, Shirtliff ME, Meiller TF, Peters BM, Jabra-Rizk MA. Farnesol, a fungal quorum-sensing molecule triggers apoptosis in human oral squamous carcinoma cells. Neoplasia. 2008;10:954–963. doi:10.1593/neo.08444.
  • Glucksam-Galnoy Y, Sananes R, Silberstein N, Krief P, Kravchenko M VV, Meijler, MM MM, Zor T. The bacterial quorum-sensing signal molecule -3-oxo-dodecanoyl-l-homoserine lactone reciprocally modulates pro- and anti-inflammatory cytokines in activated macrophages. Journal of Immunology. 2013;191:337–344. doi:10.4049/jimmunol.1300368.
  • Holm A, Karlsson T, Vikstrom E. Pseudomonas aeruginosa lasI/rhlI quorum sensing genes promote phagocytosis and aquaporin 9 redistribution to the leading and trailing regions in macrophages. Front Microbiol. 2015;6:915. doi:10.3389/fmicb.2015.00915.
  • Guo J, Yoshida K, Ikegame M, Okamura H. Quorum sensing molecule N-(3-oxododecanoyl)-l-homoserine lactone: an all-rounder in mammalian cell modification. Journal of Oral Biosciences. 2020;62(1):16–29. doi:10.1016/j.job.2020.01.001.
  • Skindersoe ME, Zeuthen LH, Brix S, Fink LN, Lazenby J, Whittall C, Williams P, Diggle SP, Froekiaer H, Cooley M . Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation. FEMS Immunol Med Microbiol. 2009;55:335–345. doi:10.1111/j.1574-695X.2008.00533.x.
  • Li Y, Zhou H, Zhang Y, Chen C, Huang B, Qu P, Zeng J, Shunmei E, Zhang X, Liu J . N-3-(oxododecanoyl)-L-homoserine lactone promotes the induction of regulatory T-cells by preventing human dendritic cell maturation. Exp Biol Med. 2015;240:896–903. doi:10.1177/1535370214564742.
  • Ritchie AJ, Yam AO, Tanabe KM, Rice SA, Cooley MA. Modification of in vivo and in vitro T- and B-cell-mediated immune responses by the Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Infect Immun. 2003;71:4421–4431. doi:10.1128/IAI.71.8.4421-4431.2003.
  • Ritchie AJ, Jansson A, Stallberg J, Nilsson P, Lysaght P, Cooley MA. The Pseudomonas aeruginosa quorum-sensing molecule N-3-(oxododecanoyl)-L-homoserine lactone inhibits T-cell differentiation and cytokine production by a mechanism involving an early step in T-cell activation. Infect Immun. 2005;73:1648–1655. doi:10.1128/IAI.73.3.1648-1655.2005.
  • Telford G, Wheeler D, Williams P, Tomkins PT, Appleby P, Sewell H, Stewart GS, Bycroft BW, Pritchard DI . The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity. Infect Immun. 1998;66:36–42. doi:10.1128/IAI.66.1.36-42.1998.
  • Jacobi CA, Schiffner F, Henkel M, Waibel M, Stork B, Daubrawa M, Eberl L, Gregor M, Wesselborg S . Effects of bacterial N-acyl homoserine lactones on human Jurkat T lymphocytes-OdDHL induces apoptosis via the mitochondrial pathway. International Journal of Medical Microbiology: IJMM. 2009;299:509–519. doi:10.1016/j.ijmm.2009.03.005.
  • Hooi DS, Bycroft BW, Chhabra SR, Williams P, Pritchard DI. Differential immune modulatory activity of Pseudomonas aeruginosa quorum-sensing signal molecules. Infect Immun. 2004;72:6463–6470. doi:10.1128/IAI.72.11.6463-6470.2004.
  • Gupta RK, Chhibber S, Harjai K, DeLeo FR. Acyl homoserine lactones from culture supernatants of Pseudomonas aeruginosa accelerate host immunomodulation. PloS one. 2011;6:e20860. doi:10.1371/journal.pone.0020860.
  • Tateda K, Ishii Y, Horikawa M, Matsumoto T, Miyairi S, Pechere JC, Standiford TJ, Ishiguro M, Yamaguchi K. The Pseudomonas aeruginosa autoinducer N −3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect Immun. 2003;71:5785–5793. doi:10.1128/IAI.71.10.5785-5793.2003.
  • Schwarzer C, Fu Z, Patanwala M, Hum L, Lopez-Guzman M, Illek B, Kong W, Lynch SV, Machen TE . Pseudomonas aeruginosa biofilm-associated homoserine lactone C12 rapidly activates apoptosis in airway epithelia. Cell Microbiol. 2012;14:698–709. doi:10.1111/j.1462-5822.2012.01753.x.
  • Li L, Hooi D, Chhabra SR, Pritchard D, Shaw PE. Bacterial N-acylhomoserine lactone-induced apoptosis in breast carcinoma cells correlated with down-modulation of STAT3. Oncogene. 2004;23:4894–4902. doi:10.1038/sj.onc.1207612.
  • Shiner EK, Terentyev D, Bryan A, Sennoune S, Martinez-Zaguilan R, Li G, Gyorke S, Williams SC, Rumbaugh KP . Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling. Cell Microbiol. 2006;8:1601–1610. doi:10.1111/j.1462-5822.2006.00734.x.
  • Valentine CD, Anderson MO, Papa FR, Haggie PM, Parsek MR. X-box binding protein 1 (XBP1s) is a critical determinant of Pseudomonas aeruginosa homoserine lactone-mediated apoptosis. PLoS Pathog. 2013;9:e1003576. doi:10.1371/journal.ppat.1003576.
  • Smith RS, Fedyk ER, Springer TA, Mukaida N, Iglewski BH, Phipps RP. 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. Journal of Immunology. 2001;167:366–374. doi:10.4049/jimmunol.167.1.366.
  • DiMango E, Zar HJ, Bryan R, Prince A. Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. J Clin Invest. 1995;96:2204–2210. doi:10.1172/JCI118275.
  • Mayer ML, Sheridan JA, Blohmke CJ, Turvey SE, Hancock RE. The Pseudomonas aeruginosa autoinducer 3O-C12 homoserine lactone provokes hyperinflammatory responses from cystic fibrosis airway epithelial cells. PloS one. 2011;6:e16246. doi:10.1371/journal.pone.0016246.
  • Valentine CD, Zhang H, Phuan PW, Nguyen J, Verkman AS, Haggie PM. Small molecule screen yields inhibitors of Pseudomonas homoserine lactone-induced host responses. Cell Microbiol. 2014;16:1–14.
  • Grabiner MA, Fu Z, Wu T, Barry KC, Schwarzer C, Machen TE. Pseudomonas aeruginosa quorum-sensing molecule homoserine lactone modulates inflammatory signaling through PERK and eI-F2alpha. Journal of Immunology. 2014;193:1459–1467. doi:10.4049/jimmunol.1303437.
  • Zhang J, Gong F, Li L, Zhao M, Song J. Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl) homoserine lactone attenuates lipopolysaccharide-induced inflammation by activating the unfolded protein response. Biomedical Reports. 2014;2:233–238. doi:10.3892/br.2014.225.
  • Miyairi S, Tateda K, Fuse ET, Ueda C, Saito H, Takabatake T, Ishii Y, Horikawa M, Ishiguro M, Standiford TJ . Immunization with 3-oxododecanoyl-L-homoserine lactone-protein conjugate protects mice from lethal Pseudomonas aeruginosa lung infection. J Med Microbiol. 2006;55:1381–1387. doi:10.1099/jmm.0.46658-0.
  • Horke S, Xiao J, Schutz EM, Kramer GL, Wilgenbus P, Witte I, Selbach M, Teiber JF . Novel paraoxonase 2-dependent mechanism mediating the biological effects of the pseudomonas aeruginosa quorum-sensing molecule N-(3-oxo-dodecanoyl)-L-homoserine lactone. Infect Immun. 2015;83:3369–3380. doi:10.1128/IAI.00141-15.
  • Vikstrom E, Bui L, Konradsson P, Magnusson KE. The junctional integrity of epithelial cells is modulated by Pseudomonas aeruginosa quorum sensing molecule through phosphorylation-dependent mechanisms. Exp Cell Res. 2009;315:313–326. doi:10.1016/j.yexcr.2008.10.044.
  • Zaborina O, Kohler JE, Wang Y, Bethel C, Shevchenko O, Wu L, Turner JR, Alverdy JC . Identification of multi-drug resistant Pseudomonas aeruginosa clinical isolates that are highly disruptive to the intestinal epithelial barrier. Ann Clin Microbiol Antimicrob. 2006;5:14. doi:10.1186/1476-0711-5-14.
  • Charlton TS, de Nys R, Netting A, Kumar N, Hentzer M, Givskov M, Kjelleberg S. A novel and sensitive method for the quantification of N −3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ Microbiol. 2000;2:530–541. doi:10.1046/j.1462-2920.2000.00136.x.
  • Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124:783–801.
  • Wagner C, Zimmermann S, Brenner-Weiss G, Hug F, Prior B, Obst U, Hänsch GM . The quorum-sensing molecule N-3-oxododecanoyl homoserine lactone (3OC12-HSL) enhances the host defence by activating human polymorphonuclear neutrophils (PMN). Anal Bioanal Chem. 2007;387:481–487. doi:10.1007/s00216-006-0698-5.
  • Smith RS, Harris SG, Phipps R, Iglewski B. The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)homoserine lactone contributes to virulence and induces inflammation in vivo. J Bacteriol. 2002;184:1132–1139. doi:10.1128/jb.184.4.1132-1139.2002.
  • Kravchenko K VV, Mathison GF, Scott JC, Katz DA, Grauer AZ, Grauer, DC DC, Lehmann M, Meijler MM, Janda KD, et al. Modulation of gene expression via disruption of NF-kappaB signaling by a bacterial small molecule. Science. 2008;321:259–263. doi:10.1126/science.1156499.
  • Kravchenko K VV, Mathison GF, Scott JC, Katz DA, Wood AZ, Wood, MR MR, Brogan AP, Lehmann M, Mee JM, 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 Biol Chem. 2006;281:28822–28830. doi:10.1074/jbc.M606613200.
  • Tao S, Sun Q, Cai L, Geng Y, Hua C, Ni Y, Zhao R. Caspase-1-dependent mechanism mediating the harmful impacts of the quorum-sensing molecule N-(3-oxo-dodecanoyl)- -homoserine lactone on the intestinal cells. J Cell Physiol. 2019;234:3621–3633. doi:10.1002/jcp.27132.
  • Sonnino S, Prinetti A. Membrane domains and the ”lipid raft” concept. Curr Med Chem. 2013;20:4–21.
  • Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science. 2010;327:46–50. doi:10.1126/science.1174621.
  • Sezgin E, Levental I, Mayor S, Eggeling C. The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat Rev Mol Cell Biol. 2017;18(6):361–374. doi:10.1038/nrm.2017.16.
  • Lee S-J, Jung YH, Oh SY, Jang KK, Lee HS, Choi SH, Han HJ. Vibrio vulnificus VvpE inhibits mucin 2 expression by hypermethylation via lipid raft-mediated ROS signaling in intestinal epithelial cells. Cell Death Dis. 2015;6(6):e1787. doi:10.1038/cddis.2015.152.
  • Eum SY, Jaraki D, Bertrand L, Andras IE, Toborek M. Disruption of epithelial barrier by quorum-sensing N −3-(oxododecanoyl)-homoserine lactone is mediated by matrix metalloproteinases. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2014;306(11):G992–G1001. doi:10.1152/ajpgi.00016.2014.
  • Jahoor A, Patel R, Bryan A, Do C, Krier J, Watters C, Wahli W, Li G, Williams SC, Rumbaugh KP, et al. Peroxisome proliferator-activated receptors mediate host cell proinflammatory responses to Pseudomonas aeruginosa autoinducer. J Bacteriol. 2008;190:4408–4415. doi:10.1128/JB.01444-07.
  • Harris SG, Phipps RP. The nuclear receptor PPAR gamma is expressed by mouse T lymphocytes and PPAR gamma agonists induce apoptosis. Eur J Immunol. 2001;31:1098–1105. doi:10.1002/1521-4141(200104)31:4<1098::AID-IMMU1098>3.0.CO;2-I.
  • Ramer R, Heinemann K, Merkord J, Rohde H, Salamon A, Linnebacher M, Hinz B. COX-2 and PPAR-gamma confer cannabidiol-induced apoptosis of human lung cancer cells. Mol Cancer Ther. 2013;12:69–82. doi:10.1158/1535-7163.MCT-12-0335.
  • Wu JS, Lin TN, Wu KK. Rosiglitazone and PPAR-gamma overexpression protect mitochondrial membrane potential and prevent apoptosis by upregulating anti-apoptotic Bcl-2 family proteins. J Cell Physiol. 2009;220:58–71. doi:10.1002/jcp.21730.
  • Horke S, Witte I, Wilgenbus P, Kruger M, Strand D, Forstermann U. Paraoxonase-2 reduces oxidative stress in vascular cells and decreases endoplasmic reticulum stress-induced caspase activation. Circulation. 2007;115:2055–2064. doi:10.1161/CIRCULATIONAHA.106.681700.
  • Kim JB, Xia YR, Romanoski CE, Lee S, Meng Y, Shi YS, Bourquard N, Gong KW, Port Z, Grijalva V . Paraoxonase-2 modulates stress response of endothelial cells to oxidized phospholipids and a bacterial quorum-sensing molecule. Arterioscler Thromb Vasc Biol. 2011;31:2624–2633. doi:10.1161/ATVBAHA.111.232827.
  • Devarajan A, Bourquard N, Grijalva VR, Gao F, Ganapathy E, Verma J, Reddy ST. Role of PON2 in innate immune response in an acute infection model. Mol Genet Metab. 2013;110:362–370. doi:10.1016/j.ymgme.2013.07.003.
  • Schwarzer C, Fu Z, Morita T, Whitt AG, Neely AM, Li C, Machen TE . Paraoxonase 2 serves a proapopotic function in mouse and human cells in response to the Pseudomonas aeruginosa quorum-sensing molecule N-(3-Oxododecanoyl)-homoserine lactone. J Biol Chem. 2015;290(11):7247–7258. doi:10.1074/jbc.M114.620039.
  • Gupta SC, Singh R, Pochampally R, Watabe K, Mo YY. Acidosis promotes invasiveness of breast cancer cells through ROS-AKT-NF-kappaB pathway. Oncotarget. 2014;5:12070–12082. doi:10.18632/oncotarget.2514.
  • Song D, Meng J, Cheng J, Fan Z, Chen P, Ruan H, Tu Z, Kang N, Li N, Xu Y, et al. Pseudomonas aeruginosa quorum-sensing metabolite induces host immune cell death through cell surface lipid domain dissolution. Nature Microbiology. 2019;4:97–111. doi:10.1038/s41564-018-0290-8.
  • Jacobi CA, Bach A, Eberl L, Steidle A, Heesemann J. Detection of N-(3-oxohexanoyl)-L-homoserine lactone in mice infected with Yersinia enterocolitica serotype O8. Infect Immun. 2003;71:6624–6626. doi:10.1128/IAI.71.11.6624-6626.2003.
  • Erickson DL, Nsereko VL, Morgavi DP, Selinger LB, Rode LM, Beauchemin KA. Evidence of quorum sensing in the rumen ecosystem: detection of N-acyl homoserine lactone autoinducers in ruminal contents. Can J Microbiol. 2002;48:374–378. doi:10.1139/w02-022.
  • Swearingen MC, Sabag-Daigle A, Ahmer BM. Are there acyl-homoserine lactones within mammalian intestines? J Bacteriol. 2013;195:173–179. doi:10.1128/JB.01341-12.
  • Kumari A, Pasini P, Deo SK, Flomenhoft D, Shashidhar H, Daunert S. Biosensing systems for the detection of bacterial quorum signaling molecules. Anal Chem. 2006;78:7603–7609.
  • Lepine F, Milot S, Groleau MC, Deziel E. Liquid chromatography/mass spectrometry (LC/MS) for the detection and quantification of N-Acyl-L-homoserine lactones (AHLs) and 4-hydroxy-2-alkylquinolines (HAQs). Methods in Molecular Biology. 2018;1673:49–59.
  • Lepine F, Deziel E. Liquid chromatography/mass spectrometry for the detection and quantification of N-acyl-L-homoserine lactones and 4-hydroxy-2-alkylquinolines. Methods in Molecular Biology. 2011;692:61–69.
  • Patel NM, Moore JD, Blackwell HE, Amador-Noguez D, Omri A. Identification of unanticipated and novel n-acyl l-homoserine lactones (ahls) using a sensitive non-targeted LC-MS/MS method. PloS one. 2016;11:e0163469. doi:10.1371/journal.pone.0163469.
  • Wang J, Ding L, Li K, Schmieder W, Geng J, Xu K, Zhang Y, Ren H. Development of an extraction method and LC-MS analysis for N-acylated-l-homoserine lactones (AHLs) in wastewater treatment biofilms. J Chromatogr B Analyt Technol Biomed Life Sci. 2017;1041-1042:37–44. doi:10.1016/j.jchromb.2016.11.029.
  • Xue J, Chi L, Tu P, Lai Y, Liu CW, Ru H, Lu K . Detection of gut microbiota and pathogen produced N-acyl homoserine in host circulation and tissues. NPJ Biofilms and Microbiomes. 2021;7:53. doi:10.1038/s41522-021-00224-5.
  • Landman C, Grill J-P, Mallet J-M, Marteau P, Humbert L, Le Balc’h E, Maubert MA, Perez K, Chaara W, Brot L . Inter-kingdom effect on epithelial cells of the N-Acyl homoserine lactone 3-oxo-C12:2, a major quorum-sensing molecule from gut microbiota. PloS one. 2018;13(8):e0202587. doi:10.1371/journal.pone.0202587.
  • Morgante M, Stelletta C, Berzaghi P, Gianesella M, Andrighetto I. Subacute rumen acidosis in lactating cows: an investigation in intensive Italian dairy herds. J Anim Physiol Anim Nutr (Berl). 2007;91(5–6):527–564. doi:10.1111/j.1439-0396.2007.00696.x.
  • Plaizier JC, Krause DO, Gozho GN, McBride BW. Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. Veterinary Journal. 2008;176:21–31. doi:10.1016/j.tvjl.2007.12.016.
  • Gozho GN, Krause DO, Plaizier JC. Ruminal lipopolysaccharide concentration and inflammatory response during grain-induced subacute ruminal acidosis in dairy cows. J Dairy Sci. 2007;90:856–866. doi:10.3168/jds.S0022-0302(07)71569-2.
  • Penner GB, Beauchemin KA, Mutsvangwa T. Severity of ruminal acidosis in primiparous Holstein cows during the periparturient period. J Dairy Sci. 2007;90:365–375. doi:10.3168/jds.S0022-0302(07)72638-3.
  • Penner GB, Taniguchi M, Guan LL, Beauchemin KA, Oba M. Effect of dietary forage to concentrate ratio on volatile fatty acid absorption and the expression of genes related to volatile fatty acid absorption and metabolism in ruminal tissue. J Dairy Sci. 2009;92:2767–2781. doi:10.3168/jds.2008-1716.
  • Bevans DW, Beauchemin KA, Schwartzkopf-Genswein KS, McKinnon JJ, McAllister TA. Effect of rapid or gradual grain adaptation on subacute acidosis and feed intake by feedlot cattle. J Anim Sci. 2005;83:1116–1132. doi:10.2527/2005.8351116x.
  • Steele MA, AlZahal O, Hook SE, Croom J, McBride BW. Ruminal acidosis and the rapid onset of ruminal parakeratosis in a mature dairy cow: a case report. Acta Vet Scand. 2009;51:39. doi:10.1186/1751-0147-51-39.
  • Kleen JL, Hooijer GA, Rehage J, Noordhuizen JP. Subacute ruminal acidosis (SARA): a review. J Vet Med A Physiol Pathol Clin Med. 2003;50:406–414. doi:10.1046/j.1439-0442.2003.00569.x.
  • Kleen JL, Hooijer GA, Rehage J, Noordhuizen JP. Subacute ruminal acidosis in Dutch dairy herds. Vet Rec. 2009;164:681–683. doi:10.1136/vr.164.22.681.
  • Nagaraja TG, Titgemeyer EC. Ruminal acidosis in beef cattle: the current microbiological and nutritional outlook. J Dairy Sci. 2007;90(1):E17–38. doi:10.3168/jds.2006-478.
  • Nocek JE. Bovine acidosis: implications on laminitis. J Dairy Sci. 1997;80:1005–1028. doi:10.3168/jds.S0022-0302(97)76026-0.
  • Enemark JM. The monitoring, prevention and treatment of sub-acute ruminal acidosis (SARA): a review. Veterinary Journal. 2008;176:32–43. doi:10.1016/j.tvjl.2007.12.021.
  • Edrington TS, Farrow RL, Sperandio V, Hughes DT, Lawrence TE, Callaway TR, Anderson RC, Nisbet DJ . Acyl-homoserine-lactone autoinducer in the gastrointestinal [corrected] tract of feedlot cattle and correlation to season, E. coli O157:H7 prevalence, and diet. Curr Microbiol. 2009;58:227–232.
  • Tao S, Tian P, Luo Y, Tian J, Hua C, Geng Y, Cong R, Ni Y, Zhao R . Microbiome-Metabolome responses to a high-grain diet associated with the hind-gut health of goats. Front Microbiol. 2017;8:1764. doi:10.3389/fmicb.2017.01764.
  • Tao S, Han Z, Tian J, Cong R, Duanmu Y, Dong H, Ni Y, Zhao R . Downregulation of prostaglandin E2 is involved in hindgut mucosal damage in lactating goats fed a high-concentrate diet. Exp Physiol. 2016;101:272–281. doi:10.1113/EP085256.
  • Tao S, Duanmu Y, Dong H, Ni Y, Chen J, Shen X, Zhao R. High concentrate diet induced mucosal injuries by enhancing epithelial apoptosis and inflammatory response in the hindgut of goats. PloS one. 2014;9:e111596. doi:10.1371/journal.pone.0111596.
  • Tao S, Duanmu Y, Dong H, Tian J, Ni Y, Zhao R. A high-concentrate diet induced colonic epithelial barrier disruption is associated with the activating of cell apoptosis in lactating goats. BMC Vet Res. 2014;10:235. doi:10.1186/s12917-014-0235-2.
  • Tao S, Tian J, Cong R, Sun L, Duanmu Y, Dong H, Ni Y, Zhao R. Activation of cellular apoptosis in the caecal epithelium is associated with increased oxidative reactions in lactating goats after feeding a high-concentrate diet. Exp Physiol. 2015;100:278–287. doi:10.1113/expphysiol.2014.083352.
  • Quesnel H, Brossard L, Valancogne A, Quiniou N. Influence of some sow characteristics on within-litter variation of piglet birth weight. Animal: An International Journal of Animal Bioscience. 2008;2:1842–1849. doi:10.1017/S175173110800308X.
  • Yuan T-L, Zhu Y-H, Shi M, Li -T-T, Li N, Wu G-Y, Bazer FW, Zang -J-J, Wang F-L, Wang -J-J, et al. 母猪营养状态对仔猪初生重窝内变异的影响. Journal of Zhejiang University-SCIENCE B. 2015;16(6):417–435. doi:10.1631/jzus.B1500010.
  • Wang J, Feng C, Liu T, Shi M, Wu G, Bazer FW. Physiological alterations associated with intrauterine growth restriction in fetal pigs: causes and insights for nutritional optimization. Mol Reprod Dev. 2017;84:897–904. doi:10.1002/mrd.22842.
  • Wu G, Bazer FW, Wallace JM, Spencer TE. Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci. 2006;84:2316–2337. doi:10.2527/jas.2006-156.
  • Hu Y, Hu L, Gong D, Lu H, Xuan Y, Wang R, Wu D, Chen D, Zhang K, Gao F, et al. Genome-wide DNA methylation analysis in jejunum of Sus scrofa with intrauterine growth restriction. Molecular Genetics and Genomics: MGG. 2018;293:807–818. doi:10.1007/s00438-018-1422-9.
  • Su W, Zhang H, Ying Z, Li Y, Zhou L, Wang F, Zhang L, Wang T. Effects of dietary L-methionine supplementation on intestinal integrity and oxidative status in intrauterine growth-retarded weanling piglets. Eur J Nutr. 2018;57:2735–2745. doi:10.1007/s00394-017-1539-3.
  • Wang W, Degroote J, Van Ginneken C, Van Poucke M, Vergauwen H, Dam TM, Vanrompay D, Peelman LJ, Smet SD, Michiels J . Intrauterine growth restriction in neonatal piglets affects small intestinal mucosal permeability and mRNA expression of redox-sensitive genes. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology. 2016;30:863–873. doi:10.1096/fj.15-274779.
  • Shen L, Gan M, Zhang S, Ma J, Tang G, Jiang Y, Li M, Wang J, Li X, Che L . Transcriptome analyses reveal adult metabolic syndrome with intrauterine growth restriction in pig models. Front Genet. 2018;9:291. doi:10.3389/fgene.2018.00291.
  • Shen L, Zhang S, Li Q, Fu Y, Tang G, Jiang Y, Li, M, Wang, J, Li, X, Che, L . The landscape of non-coding rna in an adult pig model of intrauterine growth restriction. Cellular Physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology. 2018;50:1764–1778. doi:10.1159/000494794.
  • Bjuland KJ, Rimol LM, Lohaugen GC, Skranes J. Brain volumes and cognitive function in very-low-birth-weight (VLBW) young adults. European Journal of Paediatric Neurology: EJPN: Official Journal of the European Paediatric Neurology Society. 2014;18:578–590. doi:10.1016/j.ejpn.2014.04.004.
  • Jensen CB, Storgaard H, Madsbad S, Richter EA, Vaag AA, Bjuland KJ, Rimol LM, Løhaugen GCC, Skranes J. Altered skeletal muscle fiber composition and size precede whole-body insulin resistance in young men with low birth weight. J Clin Endocrinol Metab. 2007;92:1530–1534. doi:10.1210/jc.2006-2360.
  • Longhi S, Mercolini F, Carloni L, Nguyen L, Fanolla A, Radetti G. Prematurity and low birth weight lead to altered bone geometry, strength, and quality in children. J Endocrinol Invest. 2015;38:563–568. doi:10.1007/s40618-014-0230-2.
  • Tao S, Bai Y, Li T, Li N, Wang J. Original low birth weight deteriorates the hindgut epithelial barrier function in pigs at the growing stage. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology. 2019;33:9897–9912. doi:10.1096/fj.201900204RR.
  • Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C. Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol. 2011;8:36–45. doi:10.1038/nchembio.741.
  • Li N, Huang S, Jiang L, Wang W, Li T, Zuo B, Li Z, Wang J. Differences in the gut microbiota establishment and metabolome characteristics between low- and normal-birth-weight piglets during early-life. Front Microbiol. 2018;9:1798. doi:10.3389/fmicb.2018.01798.
  • Tao S, Xiong Y, Wang Z, Wu Y, Li N, Pi Y, Han D, Zhao J, Wang J. N -Acyl-homoserine lactones may affect the gut health of low-birth-weight piglets by altering intestinal epithelial cell barrier function and amino acid metabolism. J Nutr. 2021. doi:10.1093/jn/nxab104.
  • Kim YS, Ho SB. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep. 2010;12:319–330. doi:10.1007/s11894-010-0131-2.
  • Johansson ME, Sjovall H, Hansson GC. The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol. 2013;10:352–361. doi:10.1038/nrgastro.2013.35.
  • Ermund A, Schutte A, Johansson ME, Gustafsson JK, Hansson GC. Studies of mucus in mouse stomach, small intestine, and colon. I. Gastrointestinal mucus layers have different properties depending on location as well as over the Peyer’s patches. Am J Physiol Gastrointest Liver Physiol. 2013;305:G341–7. doi:10.1152/ajpgi.00046.2013.
  • Holmen Larsson JM, Thomsson KA, Rodriguez-Pineiro AM, Karlsson H, Hansson GC. Studies of mucus in mouse stomach, small intestine, and colon. III. gastrointestinal Muc5ac and Muc2 mucin O-glycan patterns reveal a regiospecific distribution. Am J Physiol Gastrointest Liver Physiol. 2013;305:G357–63. doi:10.1152/ajpgi.00048.2013.
  • Rodriguez-Pineiro AM, Bergstrom JH, Ermund A, Gustafsson JK, Schutte A, Johansson ME, Hansson, GC . Studies of mucus in mouse stomach, small intestine, and colon. II. Gastrointestinal mucus proteome reveals Muc2 and Muc5ac accompanied by a set of core proteins. Am J Physiol Gastrointest Liver Physiol. 2013;305:G348–56. doi:10.1152/ajpgi.00047.2013.
  • Johansson ME, Gustafsson JK, Holmen-Larsson J, Jabbar KS, Xia L, Xu H, Ghishan FK, Carvalho FA, Gewirtz AT, Sjövall H, et al. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut. 2014;63:281–291. doi:10.1136/gutjnl-2012-303207.
  • McElroy SJ, Prince LS, Weitkamp JH, Reese J, Slaughter JC, Polk DB. Tumor necrosis factor receptor 1-dependent depletion of mucus in immature small intestine: a potential role in neonatal necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol. 2011;301:G656–66. doi:10.1152/ajpgi.00550.2010.
  • der Sluis M V, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Büller HA, Dekker J, Van Seuningen I, Renes IB, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131:117–129. doi:10.1053/j.gastro.2006.04.020.
  • Tao S, Niu L, Cai L, Geng Y, Hua C, Ni Y, Zhao R . N-(3-oxododecanoyl)-l-homoserine lactone modulates mitochondrial function and suppresses proliferation in intestinal goblet cells. Life Sci. 2018;201:81–88.
  • Tao S, Luo Y, Bin H, Liu J, Qian X, Ni Y, Zhao R. Paraoxonase 2 modulates a proapoptotic function in LS174T cells in response to quorum sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Sci Rep. 2016;6:28778. doi:10.1038/srep28778.
  • John LJ, Fromm M, Schulzke JD. Epithelial barriers in intestinal inflammation. Antioxid Redox Signal. 2011;15:1255–1270. doi:10.1089/ars.2011.3892.
  • Gareau MG, Silva MA, Perdue MH. Pathophysiological mechanisms of stress-induced intestinal damage. Curr Mol Med. 2008;8:274–281. doi:10.2174/156652408784533760.
  • Ballard ST, Hunter JH, Taylor AE. Regulation of tight-junction permeability during nutrient absorption across the intestinal epithelium. Annu Rev Nutr. 1995;15:35–55. doi:10.1146/annurev.nu.15.070195.000343.
  • Schneeberger EE, Lynch RD. The tight junction: a multifunctional complex. Am J Physiol Cell Physiol. 2004;286:C1213–28. doi:10.1152/ajpcell.00558.2003.
  • Vikstrom E, Tafazoli F, Magnusson KE. Pseudomonas aeruginosa quorum sensing molecule N-(3 oxododecanoyl)-l-homoserine lactone disrupts epithelial barrier integrity of Caco-2 cells. FEBS Lett. 2006;580:6921–6928. doi:10.1016/j.febslet.2006.11.057.
  • Tao S, Xiong Y, Han D, Pi Y, Zhang H, Wang J. N -(3-oxododecanoyl)- -homoserine lactone disrupts intestinal epithelial barrier through triggering apoptosis and collapsing extracellular matrix and tight junction. J Cell Physiol. 2021;236(8):5771–5784. doi:10.1002/jcp.30261.
  • Cheng W, Wang Z, Xiong Y, Wu Z, Tan X, Yang Y, Zhang H, Zhu X, Wei H, Tao S, et al. N-(3-oxododecanoyl)-homoserine lactone disrupts intestinal barrier and induces systemic inflammation through perturbing gut microbiome in mice. Sci Total Environ. 2021;778:146347. doi:10.1016/j.scitotenv.2021.146347.