Interplay between enterohaemorrhagic Escherichia coli and nitric oxide during the infectious process

References

• Wurzner R, Riedl M, Rosales A, et al. Treatment of enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome (eHUS). Semin Thromb Hemost. 2014;40(4):508–516.
   PubMed Web of Science ®Google Scholar
• Tarr PI, Gordon CA, Chandler WL. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet. 2005 Mar 19–25;365(9464):1073–1086.
   PubMed Web of Science ®Google Scholar
• Frenzen PD, Drake A, Angulo FJ. Economic cost of illness due to Escherichia coli O157 infections in the United States. J Food Prot. 2005 Dec;68(12):2623–2630.
   PubMed Web of Science ®Google Scholar
• Jubelin G, Desvaux M, Schuller S, et al. Modulation of enterohaemorrhagic Escherichia coli survival and virulence in the human gastrointestinal tract. Microorganisms. 2018 Nov 19;6(4):115.
   PubMed Web of Science ®Google Scholar
• Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004 Feb;2(2):123–140.
   PubMed Web of Science ®Google Scholar
• McDaniel TK, Jarvis KG, Donnenberg MS, et al. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA. 1995 Feb 28;92(5):1664–1668.
   PubMed Web of Science ®Google Scholar
• Wong AR, Pearson JS, Bright MD, et al. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol. 2011 Jun;80(6):1420–1438.
   PubMed Web of Science ®Google Scholar
• Melton-Celsa AR. Shiga toxin (Stx) classification, structure, and function. Microbiol Spectr. 2014 Aug;2(4):EHEC-0024-2013.
   PubMedGoogle Scholar
• Siegler RL, Obrig TG, Pysher TJ, et al. Response to Shiga toxin 1 and 2 in a baboon model of hemolytic uremic syndrome. Pediatr Nephrol. 2003 Feb;18(2):92–96.
   PubMed Web of Science ®Google Scholar
• Herold S, Karch H, Schmidt H. Shiga toxin-encoding bacteriophages–genomes in motion. Int J Med Microbiol. 2004 Sep;294(2–3):115–121.
   PubMed Web of Science ®Google Scholar
• Paton JC, Paton AW. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev. 1998 Jul;11(3):450–479.
   PubMed Web of Science ®Google Scholar
• Hughes AK, Ergonul Z, Stricklett PK, et al. Molecular basis for high renal cell sensitivity to the cytotoxic effects of shigatoxin-1: upregulation of globotriaosylceramide expression. J Am Soc Nephrol. 2002 Sep;13(9):2239–2245.
   PubMed Web of Science ®Google Scholar
• Trachtman H, Austin C, Lewinski M, et al. Renal and neurological involvement in typical Shiga toxin-associated HUS. Nat Rev Nephrol. 2012 Nov;8(11):658–669.
   PubMed Web of Science ®Google Scholar
• Schairer DO, Chouake JS, Nosanchuk JD, et al. The potential of nitric oxide releasing therapies as antimicrobial agents. Virulence. 2012 May 1;3(3):271–279.
   PubMed Web of Science ®Google Scholar
• Flint A, Butcher J, Stintzi A. Stress responses, adaptation, and virulence of bacterial pathogens during host gastrointestinal colonization. Microbiol Spectr. 2016 Apr;4(2): VMBF-0007-2015.
   PubMed Web of Science ®Google Scholar
• Arai H, Iiyama K. Role of nitric oxide-detoxifying enzymes in the virulence of Pseudomonas aeruginosa against the silkworm, Bombyx mori. Biosci Biotechnol Biochem. 2013;77(1):198–200.
   PubMed Web of Science ®Google Scholar
• Shimizu T, Tsutsuki H, Matsumoto A, et al. The nitric oxide reductase of enterohaemorrhagic Escherichia coli plays an important role for the survival within macrophages. Mol Microbiol. 2012 Aug;85(3):492–512.
   PubMed Web of Science ®Google Scholar
• Stevanin TM, Poole RK, Demoncheaux EA, et al. Flavohemoglobin Hmp protects Salmonella enterica serovar typhimurium from nitric oxide-related killing by human macrophages. Infect Immun. 2002 Aug;70(8):4399–4405.
   PubMed Web of Science ®Google Scholar
• Vareille M, de Sablet T, Hindre T, et al. Nitric oxide inhibits Shiga-toxin synthesis by enterohemorrhagic Escherichia coli. Proc Natl Acad Sci USA. 2007 Jun 12;104(24):10199–10204.
   PubMed Web of Science ®Google Scholar
• Branchu P, Matrat S, Vareille M, et al. Nsrr, GadE, and GadX interplay in repressing expression of the Escherichia coli O157:H7 LEE pathogenicity island in response to nitric oxide. PLoS Pathog. 2014 Jan;10(1):e1003874.
   PubMed Web of Science ®Google Scholar
• Osorio CG, Crawford JA, Michalski J, et al. Second-generation recombination-based in vivo expression technology for large-scale screening for Vibrio cholerae genes induced during infection of the mouse small intestine. Infect Immun. 2005 Feb;73(2):972–980.
   PubMed Web of Science ®Google Scholar
• Justino MC, Vicente JB, Teixeira M, et al. New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide. J Biol Chem. 2005 Jan 28;280(4):2636–2643.
   PubMed Web of Science ®Google Scholar
• Gardette M, Le Hello S, Mariani-Kurkdjian P, et al. Identification and prevalence of in vivo-induced genes in enterohaemorrhagic Escherichia coli. Virulence. 2019 Dec;10(1):180–193.
   PubMed Web of Science ®Google Scholar
• Zhang X, McDaniel AD, Wolf LE, et al. Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J Infect Dis. 2000 Feb;181(2):664–670.
   PubMed Web of Science ®Google Scholar
• Quinones B, Massey S, Friedman M, et al. Novel cell-based method to detect Shiga toxin 2 from Escherichia coli O157:H7 and inhibitors of toxin activity. Appl Environ Microbiol. 2009 Mar;75(5):1410–1416.
   PubMed Web of Science ®Google Scholar
• Bodenmiller DM, Spiro S. The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J Bacteriol. 2006 Feb;188(3):874–881.
   PubMed Web of Science ®Google Scholar
• de Sablet T, Bertin Y, Vareille M, et al. Differential expression of stx2 variants in Shiga toxin-producing Escherichia coli belonging to seropathotypes A and C. Microbiology. 2008 Jan;154(Pt 1):176–186.
   PubMed Web of Science ®Google Scholar
• Eaton KA, Friedman DI, Francis GJ, et al. Pathogenesis of renal disease due to enterohemorrhagic Escherichia coli in germ-free mice. Infect Immun. 2008 Jul;76(7):3054–3063.
   PubMed Web of Science ®Google Scholar
• Tyler JS, Beeri K, Reynolds JL, et al. Prophage induction is enhanced and required for renal disease and lethality in an EHEC mouse model. PLoS Pathog. 2013 Mar;9(3):e1003236.
   PubMed Web of Science ®Google Scholar
• Bogdan C. Nitric oxide and the immune response. Nat Immunol. 2001 Oct;2(10):907–916.
   PubMed Web of Science ®Google Scholar
• Nathan C, Shiloh MU. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA. 2000 Aug 1;97(16):8841–8848.
   PubMed Web of Science ®Google Scholar
• Enocksson A, Lundberg J, Weitzberg E, et al. Rectal nitric oxide gas and stool cytokine levels during the course of infectious gastroenteritis. Clin Diagn Lab Immunol. 2004 Mar;11(2):250–254.
   PubMedGoogle Scholar
• Witthoft T, Eckmann L, Kim JM, et al. Enteroinvasive bacteria directly activate expression of iNOS and NO production in human colon epithelial cells. Am J Physiol. 1998 Sep;275(3):G564–G571.
   PubMedGoogle Scholar
• Shah V, Lyford G, Gores G, et al. Nitric oxide in gastrointestinal health and disease. Gastroenterology. 2004 Mar;126(3):903–913.
   PubMed Web of Science ®Google Scholar
• John M, Kudva IT, Griffin RW, et al. Use of in vivo-induced antigen technology for identification of Escherichia coli O157:H7 proteins expressed during human infection. Infect Immun. 2005 May;73(5):2665–2679.
   PubMed Web of Science ®Google Scholar
• Ramirez VT, Godinez DR, Brust-Mascher I, et al. T-cell derived acetylcholine aids host defenses during enteric bacterial infection with Citrobacter rodentium. PLoS Pathog. 2019 Apr;15(4):e1007719.
   PubMed Web of Science ®Google Scholar
• Vallance BA, Deng W, De Grado M, et al. Modulation of inducible nitric oxide synthase expression by the attaching and effacing bacterial pathogen Citrobacter rodentium in infected mice. Infect Immun. 2002 Nov;70(11):6424–6435.
   PubMed Web of Science ®Google Scholar
• Matziouridou C, Rocha SDC, Haabeth OA, et al. iNOS- and NOX1-dependent ROS production maintains bacterial homeostasis in the ileum of mice. Mucosal Immunol. 2018 May;11(3):774–784.
   PubMed Web of Science ®Google Scholar
• Green J, Rolfe MD, Smith LJ. Transcriptional regulation of bacterial virulence gene expression by molecular oxygen and nitric oxide. Virulence. 2014;5(8):794–809.
   PubMed Web of Science ®Google Scholar
• Spiro S. Regulators of bacterial responses to nitric oxide. FEMS Microbiol Rev. 2007 Mar;31(2):193–211.
   PubMed Web of Science ®Google Scholar
• Yang B, Feng L, Wang F, et al. Enterohemorrhagic Escherichia coli senses low biotin status in the large intestine for colonization and infection. Nat Commun. 2015 Mar 20;6:6592.
   PubMed Web of Science ®Google Scholar
• Wan B, Zhang Q, Ni J, et al. Type VI secretion system contributes to enterohemorrhagic Escherichia coli virulence by secreting catalase against host reactive oxygen species (ROS). PLoS Pathog. 2017 Mar;13(3):e1006246.
   PubMed Web of Science ®Google Scholar
• Nichols SP, Schoenfisch MH. Nitric oxide-flux dependent bacterial adhesion and viability at fibrinogen-coated surfaces. Biomater Sci. 2013 Nov 1;1(11):1151.
   Web of Science ®Google Scholar
• Ichimura K, Shimizu T, Matsumoto A, et al. Nitric oxide-enhanced Shiga toxin production was regulated by Fur and RecA in enterohemorrhagic Escherichia coli O157. Microbiologyopen. 2017 Aug;6(4):e461.
   Web of Science ®Google Scholar
• Unno N, Wang H, Menconi MJ, et al. Inhibition of inducible nitric oxide synthase ameliorates endotoxin-induced gut mucosal barrier dysfunction in rats. Gastroenterology. 1997 Oct;113(4):1246–1257.
   PubMed Web of Science ®Google Scholar
• Quirino IE, Cardoso VN, Santos R, et al. The role of L-arginine and inducible nitric oxide synthase in intestinal permeability and bacterial translocation. JPEN J Parenter Enteral Nutr. 2013 May–Jun;37(3):392–400.
   PubMed Web of Science ®Google Scholar
• Bachmann S, Mundel P. Nitric oxide in the kidney: synthesis, localization, and function. Am J Kidney Dis. 1994 Jul;24(1):112–129.
   PubMed Web of Science ®Google Scholar
• Jover B, Mimran A. Nitric oxide inhibition and renal alterations. J Cardiovasc Pharmacol. 2001 Nov;38(Suppl 2):S65–S70.
   PubMed Web of Science ®Google Scholar
• Bogdan C. Nitric oxide synthase in innate and adaptive immunity: an update. Trends Immunol. 2015 Mar;36(3):161–178.
   PubMed Web of Science ®Google Scholar
• Umezawa K, Akaike T, Fujii S, et al. Induction of nitric oxide synthesis and xanthine oxidase and their roles in the antimicrobial mechanism against Salmonella typhimurium infection in mice. Infect Immun. 1997 Jul;65(7):2932–2940.
   PubMed Web of Science ®Google Scholar
• Mallick EM, McBee ME, Vanguri VK, et al. A novel murine infection model for Shiga toxin-producing Escherichia coli. J Clin Invest. 2012 Nov;122(11):4012–4024.
   PubMed Web of Science ®Google Scholar
• Montesanto A, Crocco P, Tallaro F, et al. Common polymorphisms in nitric oxide synthase (NOS) genes influence quality of aging and longevity in humans. Biogerontology. 2013 Apr;14(2):177–186.
   PubMed Web of Science ®Google Scholar
• MacMicking JD, Nathan C, Hom G, et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell. 1995 May 19;81(4):641–650.
   PubMed Web of Science ®Google Scholar
• Blos M, Schleicher U, Soares Rocha FJ, et al. Organ-specific and stage-dependent control of Leishmania major infection by inducible nitric oxide synthase and phagocyte NADPH oxidase. Eur J Immunol. 2003 May;33(5):1224–1234.
   PubMed Web of Science ®Google Scholar
• Mastroeni P, Vazquez-Torres A, Fang FC, et al. 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. 2000 Jul 17;192(2):237–248.
   PubMed Web of Science ®Google Scholar
• Alam MS, Zaki MH, Sawa T, et al. Nitric oxide produced in Peyer's patches exhibits antiapoptotic activity contributing to an antimicrobial effect in murine salmonellosis. Microbiol Immunol. 2008 Apr;52(4):197–208.
   PubMed Web of Science ®Google Scholar
• Henard CA, Vazquez-Torres A. Nitric oxide and Salmonella pathogenesis. Front Microbiol. 2011;2:84.
   PubMed Web of Science ®Google Scholar
• Stecher B, Robbiani R, Walker AW, et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 2007 Oct;5(10):2177–2189.
   PubMed Web of Science ®Google Scholar
• Winkler F, Koedel U, Kastenbauer S, et al. Differential expression of nitric oxide synthases in bacterial meningitis: role of the inducible isoform for blood-brain barrier breakdown. J Infect Dis. 2001 Jun 15;183(12):1749–1759.
   PubMed Web of Science ®Google Scholar
• Mittal R, Gonzalez-Gomez I, Goth KA, et al. Inhibition of inducible nitric oxide controls pathogen load and brain damage by enhancing phagocytosis of Escherichia coli K1 in neonatal meningitis. Am J Pathol. 2010 Mar;176(3):1292–1305.
   PubMed Web of Science ®Google Scholar