The Microbial Endocrinology of Pseudomonas aeruginosa: Inflammatory and Immune Perspectives

Alcaniz L, Vega A, Chacón P et al (2013) Histamine production by human neutrophils. FASEB J 27:2902–2910 Anas AA, van Lieshout MH, Claushuis TA et al (2016) Lung epithelial MyD88 drives early pulmonary clearance of Pseudomonas aeruginosa by a flagellin dependent mechanism. Am J Physiol Lung Cell Mol Physiol 311:L219–L228 Beury-Cirou A, Tannières M, Minard C et al (2013) At a supra-physiological concentration, human sexual hormones act as quorum-sensing inhibitors. PLoS One 8:e83564 Blier AS, Veron W, Bazire A et al (2011) C-type natriuretic peptide modulates quorum sensing molecule and toxin production in Pseudomonas aeruginosa. Microbiology 157(Pt 7):1929–1944 Brunelleschi S (2016) Immune response and auto-immune diseases: gender does matter and makes the difference. Italian J Gender Specific Med 2:5–14 Chotirmall SH (2014) The microbiological gender gap in cystic fibrosis. J Womens Health 23:995–996 Chotirmall SH, Greene CM, Oglesby IK et al (2010) 17Beta-estradiol inhibits IL-8 in cystic fibrosis by up-regulating secretory leucoprotease inhibitor. Am J Respir Crit Care Med 182:62–72 Chotirmall SH, Smith SG, Gunaratnam C et al (2012) Effect of estrogen on pseudomonas mucoidy and exacerbations in cystic fibrosis. N Engl J Med 366:1978–1986 Cinel I, Dellinger RP (2007) Advances in pathogenesis and management of sepsis. Curr Opin Infect Dis 20:345–352 Ciofu O, Riis B, Pressler T et al (2005) Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob Agents Chemother 49:2276–2282 Clamens T, Rosay T, Crépin A et al (2017) The aliphatic amidase AmiE is involved in regulation of Pseudomonas aeruginosa virulence. Sci Rep 7:41178 Cole JN, Nizet V (2016) Bacterial evasion of host antimicrobial peptide defenses. Microbiol Spectr 4:413–443 Cosgrove S, Chotirmall SH, Greene CM et al (2011) Pulmonary proteases in the cystic fibrosis lung induce interleukin 8 expression from bronchial epithelial cells via a heme/meprin/epidermal growth factor receptor/Toll-like receptor pathway. J Biol Chem 286:7692–7704 Costerton W, Veeh R, Shirtliff M et al (2003) The application of biofilm science to the study and control of chronic bacterial infections. J Clin Invest 112:1466–1477 Crousilles A, Maunders E, Bartlett S et al (2015) Which microbial factors really are important in Pseudomonas aeruginosa infections? Future Microbiol 10:1825–1836 Deng HP, Chai JK (2009) The effects and mechanisms of insulin on systemic inflammatory response and immune cells in severe trauma, burn injury, and sepsis. Int Immunopharmacol 9:1251–1259 Deng JC, Cheng G, Newstead MW et al (2006) Sepsis-induced suppression of lung innate immunity is mediated by IRAK-M. J Clin Invest 116:2532–2542 Dietrich LE, Teal TK, Price-Whelan A et al (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203–1206 Diggle SP, Matthijs S, Wright VJ et al (2007) The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14:87–96 Djonovic S, Urbach JM, Drenkard E et al (2013) Trehalose biosynthesis promotes Pseudomonas aeruginosa pathogenicity in plants. PLoS Pathog 9:e1003217 Elenkov IJ (2007) Effects of catecholamines on the immune response. NeuroImmune Biol 7:189–206 Elkins CA, Mullis LB (2006) Mammalian steroid hormones are substrates for the major RND- and MFS-type tripartite multidrug efflux pumps of Escherichia coli. J Bacteriol 188:1191–1195 Fargier E, Mac Aogáin M, Mooij MJ et al (2012) MexT functions as a redox-responsive regulator modulating disulfide stress resistance in Pseudomonas aeruginosa. J Bacteriol 194:3502–3511 Flierl MA, Rittirsch D, Huber-Lang M et al (2008) Catecholamines-crafty weapons in the inflammatory arsenal of immune/inflammatory cells or opening pandora’s box? Mol Med 14:195–204 Foo YZ, Nakagawa S, Rhodes G et al (2017) The effects of sex hormones on immune function: a meta-analysis. Biol Rev Camb Philos Soc 92:551–571 Franchi L, Munoz-Planillo R, Nunez G (2012) Sensing and reacting to microbes through the inflammasomes. Nat Immunol 13:325–332 Freestone P (2013) Communication between bacteria and their hosts. Scientifica 2013:361073 Freestone PP, Hirst RA, Sandrini SM et al (2012) Pseudomonas aeruginosa-catecholamine inotrope interactions: a contributory factor in the development of ventilator-associated pneumonia? Chest 142:1200–1210 Garcia-Gomez E, Gonzalez-Pedrajo B, Camacho-Arroyo I (2013) Role of sex steroid hormones in bacterial-host interactions. Biomed Res Int 2013:928290 Gein SV (2014) Dynorphins in regulation of immune system functions. Biochemistry 79:397–405 Gellatly SL, Hancock RE (2013) Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 67:159–173 Ghafoor A, Hay ID, Rehm BH (2011) Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 77:5238–5246 Gibson RL, Burns JL, Ramsey BW (2003) Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 168:918–951 Gómez MI, Prince A (2007) Opportunistic infections in lung disease: Pseudomonas infections in cystic fibrosis. Curr Opin Pharmacol 7:244–251 Grisanti LA, Woster AP, Dahlman J et al (2011) Alpha1-adrenergic receptors positively regulate Toll-like receptor cytokine production from human monocytes and macrophages. J Pharmacol Exp Ther 338:648–657 Guttenplan SB, Kearns DB (2013) Regulation of flagellar motility during biofilm formation. FEMS Microbiol Rev 37:849–871 Hall S, McDermott C, Anoopkumar-Dukie S et al (2016) Cellular effects of pyocyanin, a secreted virulence factor of Pseudomonas aeruginosa. Toxins 8(8):236. https://doi.org/10.3390/toxins8080236 Harness-Brumley CL, Elliott AC, Rosenbluth DB et al (2014) Gender differences in outcomes of patients with cystic fibrosis. J Womens Health 23:1012–1020 Hartl D, Griese M, Kappler M et al (2006) Pulmonary T(H)2 response in Pseudomonas aeruginosa-infected patients with cystic fibrosis. J Allergy Clin Immunol 117:204–211 Hector A, Schäfer H, Pöschel S et al (2015) Regulatory T-cell impairment in cystic fibrosis patients with chronic pseudomonas infection. Am J Respir Crit Care Med 191:914–923 Herr N, Bode C, Duerschmied D (2017) The effects of serotonin in immune cells. Front Cardiovasc Med 4:48 Hughes DT, Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and their hosts. Nat Rev Microbiol 6:111–120 Jansen ASP, Van Nguyen X, Karpitskiy V et al (1995) Central command neurons of the sympathetic nervous system: basis of the fight-or-flight response. Science 270:644–646 Jensen PO, Givskov M, Bjarnsholt T et al (2010) The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol Med Microbiol 59:292–305 Jimenez PN, Koch G, Thompson JA et al (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76:46–65 Jones RN (2010) Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clin Infect Dis 51(Suppl 1):S81–S87 Kiseleva E, Novik G (2015) Role of type III secretory system and related exotoxins in infections induced by an opportunistic pathogen Pseudomonas aeruginosa. In: Méndez-Vilas A (ed) The battle against microbial pathogens: basic science, technological advances and educational programs. FORMATEX microbiology series N 5, vol 2. pp 733–744 Klein SL, Flanagan KL (2016) Sex differences in immune responses. Nat Rev Immunol 16:626–638 Knecht LD, O’Connor G, Mittal R et al (2016) Serotonin activates bacterial quorum sensing and enhances the virulence of Pseudomonas aeruginosa in the host. EBioMedicine 9:161–169 Lagoumintzis G, Christofidou M, Dimitracopoulos G et al (2003) Pseudomonas aeruginosa slime glycolipoprotein is a potent stimulant of tumor necrosis factor alpha gene expression and activation of transcription activators nuclear factor κB and activator protein 1 in human monocytes. Infect Immun 71:4614–4622 Lagoumintzis G, Xaplanteri P, Dimitracopoulos G et al (2008) TNF-alpha induction by Pseudomonas aeruginosa lipopolysaccharide or slime-glycolipoprotein in human monocytes is regulated at the level of Mitogen-activated Protein Kinase activity: a distinct role of Toll-like receptor 2 and 4. Scand J Immunol 67:193–203 Lavoie EG, Wangdi T, Kazmierczak BI (2011) Innate immune responses to Pseudomonas aeruginosa infection. Microbes Infect 13:1133–1145 Lecaille F, Lalmanach G, Andrault PM (2016) Antimicrobial proteins and peptides in human lung diseases: a friend and foe partnership with host proteases. Biochimie 122:151–168 Lee J, Zhang L (2015) The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6:26–41 Leone M, Textoris J, Capo C and Mege J-L (2012) Sex hormones and bacterial infections. In: Dubey R (ed) Sex hormones. InTech. https://doi.org/10.5772/26871. https://pdfs.semanticscholar.org/a7cc/19ed33b3596e9536f7951a399ad58cc22194.pdf. Accessed 8 July 2017 Leung JM, Tiew PY, Mac Aogáin M et al (2017) The role of acute and chronic respiratory colonization and infections in the pathogenesis of COPD. Respirology 22:634–650 Li W, Lyte M, Freestone PP et al (2009) Norepinephrine represses the expression of toxA and the siderophore genes in Pseudomonas aeruginosa. FEMS Microbiol Lett 299:100–109 Lore NI, Cigana C, Riva C et al (2016) IL-17A impairs host tolerance during airway chronic infection by Pseudomonas aeruginosa. Sci Rep 6:25937 Lyte M (2013) Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. PLoS Pathog 9:e1003726 Lyte M, Ernst S (1992) Catecholamine induced growth of gram negative bacteria. Life Sci 50:203–212 Mahdy AM, Webster NR (2011) Histamine and antihistamines. Anaesth Intensive Care Med 12:324–329 Maseda H, Sawada I, Saito K et al (2004) Enhancement of the mexAB-oprM efflux pump expression by a quorum-sensing autoinducer and its cancellation by a regulator, MexT, of the mexEF-oprN efflux pump operon in Pseudomonas aeruginosa. Antimicrob Agents Chemother 48:1320–1328 Miao EA, Mao DP, Yudkovsky N et al (2010) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 107:3076–3080 Mogensen TH (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22:240–273 Mulcahy LR, Isabella VM, Lewis K (2014) Pseudomonas aeruginosa biofilms in disease. Microb Ecol 68:1–12 Mund A, Diggle SP, Harrison F (2017) The fitness of Pseudomonas aeruginosa quorum sensing signal cheats is influenced by the diffusivity of the environment. MBio 8(3):e00353-17. https://doi.org/10.1128/mBio.00353-17 Murray MA, Chotirmall SH (2015) The impact of immunosenescence on pulmonary disease. Mediators Inflamm 2015:692546 Nakanishi K, Tajima F, Itoh H et al (1999) Expression of C-type natriuretic peptide during development of rat lung. Am J Physiol 277(5 Pt 1):L996–L1002 O’Loughlin CT, Miller LC, Siryaporn A et al (2013) A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci USA 110:17981–17986 Ortona E, Delunardo F, Maselli A et al (2015) Sex hormones and gender disparity in immunity and autoimmunity. Italian J Gender Specific Med 1:45–50 Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 14:576–588 Parkins MD, Gregson DB, Pitout JD et al (2010) Population-based study of the epidemiology and the risk factors for Pseudomonas aeruginosa bloodstream infection. Infection 38:25–32 Peek ME, Bhatnagar A, McCarty NA et al (2012) Pyoverdine, the major siderophore in Pseudomonas aeruginosa, evades NGAL recognition. Interdiscip Perspect Infect Dis 2012:843509 Pu Q, Gan C, Li R et al (2017) Atg7 Deficiency intensifies inflammasome activation and pyroptosis in Pseudomonas sepsis. J Immunol 198:3205–3213 Quick J, Cumley N, Wearn CM et al (2014) Seeking the source of Pseudomonas aeruginosa infections in a recently opened hospital: an observational study using whole-genome sequencing. BMJ Open 4:e006278 Rabin N, Zheng Y, Opoku-Temeng C et al (2015) Biofilm formation mechanisms and targets for developing antibiofilm agents. Future Med Chem 7:493–512 Rada B (2017) Interactions between neutrophils and Pseudomonas aeruginosa in cystic fibrosis. Pathogens 6(1):E10. https://doi.org/10.3390/pathogens6010010 Rosay T, Bazire A, Diaz S et al. (2015) Pseudomonas aeruginosa expresses a functional human natriuretic peptide receptor ortholog: involvement in biofilm formation. MBio 6(4):e01033-15. https://doi.org/10.1128/mBio.01033-15 Sakhtah H, Koyama L, Zhang Y et al (2016) The Pseudomonas aeruginosa efflux pump MexGHI-OpmD transports a natural phenazine that controls gene expression and biofilm development. Proc Natl Acad Sci USA 113:E3538–E3547 Schwarzer C (2009) 30 years of dynorphins—new insights on their functions in neuropsychiatric diseases. Pharmacol Ther 123:353–370 Shajib MS, Khan WI (2015) The role of serotonin and its receptors in activation of immune responses and inflammation. Acta Physiol 213:561–574 Silva Filho LV, Ferreira Fde A, Reis FJ et al (2013) Pseudomonas aeruginosa infection in patients with cystic fibrosis: scientific evidence regarding clinical impact, diagnosis, and treatment. J Bras Pneumol 39:495–512 Singh PK, Parsek MR, Greenberg EP et al (2002) A component of innate immunity prevents bacterial biofilm development. Nature 417:552–555 Skerrett SJ, Liggitt HD, Hajjar AM et al (2004) Cutting Edge: Myeloid differentiation factor 88 is essential for pulmonary host defense against Pseudomonas aeruginosa but not Staphylococcus aureus. J Immunol 172:3377–3381 Sun J, Deng Z, Yan A (2014) Bacterial multidrug efflux pumps: mechanisms, physiology and pharmacological exploitations. Biochem Biophys Res Commun 453:254–267 Tateda K, Ishii Y, Horikawa M et al (2003) The Pseudomonas aeruginosa autoinducer N-3-Oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect Immun 71:5785–5793 Tian ZX, Fargier E, Mac Aogain M et al (2009) Transcriptome profiling defines a novel regulon modulated by the LysR-type transcriptional regulator MexT in Pseudomonas aeruginosa. Nucleic Acids Res 37:7546–7559 Tiringer K, Treis A, Fucik P et al (2013) A Th17- and Th2-skewed cytokine profile in cystic fibrosis lungs represents a potential risk factor for Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 187:621–629 Tredget EE, Shankowsky HA, Rennie R et al (2004) Pseudomonas infections in the thermally injured patient. Burns 30:3–26 Trigunaite A, Dimo J, Jørgensen TN (2015) Suppressive effects of androgens on the immune system. Cell Immunol 294:87–94 Tumbarello M, Repetto E, Trecarichi EM et al (2011) Multidrug-resistant Pseudomonas aeruginosa bloodstream infections: risk factors and mortality. Epidemiol Infect 139:1740–1749 Valentino RJ, Van Bockstaele E (2015) Endogenous opioids: the downside of opposing stress. Neurobiol Stress 1:23–32 Veesenmeyer JL, Hauser AR, Lisboa T et al (2009) Pseudomonas aeruginosa virulence and therapy: evolving translational strategies. Crit Care Med 37:1777–1786 Veron W, Lesouhaitier O, Pennanec X et al (2007) Natriuretic peptides affect Pseudomonas aeruginosa and specifically modify lipopolysaccharide biosynthesis. FEBS J 274:5852–5864 Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15:22–30 Vital-Lopez FG, Reifman J, Wallqvist A (2015) Biofilm formation mechanisms of Pseudomonas aeruginosa predicted via genome-scale kinetic models of bacterial metabolism. PLoS Comput Biol 11:e1004452 Vogel G (2017) Meet WHO’s dirty dozen: the 12 bacteria for which new drugs are most urgently needed. Science Magazine, 27 Feb 2017. https://doi.org/10.1126/science.aal0829 vom Steeg LG, Klein SL (2017) Sex steroids mediate bidirectional interactions between hosts and microbes. Horm Behav 88:45–51 Wang Y, Cela E, Gagnon S et al (2010) Estrogen aggravates inflammation in Pseudomonas aeruginosa pneumonia in cystic fibrosis mice. Respir Res 11:166 Watters C, Everett JA, Haley C et al (2014) Insulin treatment modulates the host immune system to enhance Pseudomonas aeruginosa wound biofilms. Infect Immun 82:92–100 Weiner LM, Webb AK, Limbago B et al (2016) Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2011–2014. Infect Control Hosp Epidemiol 37:1288–1301 Williams IR, Parkos CA (2007) Colonic neutrophils in inflammatory bowel disease: double-edged swords of the innate immune system with protective and destructive capacity. Gastroenterology 133:2049–2052 Wisplinghoff H, Bischoff T, Tallent SM et al (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39:309–317 Xaplanteri P, Lagoumintzis G, Dimitracopoulos G et al (2009) Synergistic regulation of Pseudomonas aeruginosa-induced cytokine production in human monocytes by mannose receptor and TLR2. Eur J Immunol 39:730–740 Xu X, Zhang H, Song Y et al (2012) Strain-dependent induction of neutrophil histamine production and cell death by Pseudomonas aeruginosa. J Leukoc Biol 91:275–284 Zaborina O, Lepine F, Xiao G et al (2007) Dynorphin activates quorum sensing quinolone signaling in Pseudomonas aeruginosa. PLoS Pathog 3:e35 Zhang Z, Louboutin JP, Weiner DJ et al (2005) Human airway epithelial cells sense Pseudomonas aeruginosa infection via recognition of flagellin by Toll-like receptor 5. Infect Immun 73:7151–7160 Zhu J, Yamane H, Paul WE (2010) Differentiation of effector CD4 T cell populations. Annu Rev Immunol 28:445–489