Decisive role of lipopolysaccharide in activating nitric oxide and cytokine production by the probiotic escherichia coli strain nissle 1917

Folia Microbiologica

Volumn 55, Issue 2, 2010, Pages 181-189

  Zidek Z ^a   Kmonickova E ^a   Kostecka P ^a   Tlaskalova Hogenova H ^b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; LIPOPOLYSACCHARIDE; NITRIC OXIDE; PROBIOTIC AGENT;

ANIMAL; ARTICLE; BACTERIAL INFECTION; CELL CULTURE; CYTOLOGY; DISEASE MODEL; ESCHERICHIA COLI; FEMALE; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PERITONEAL CAVITY; RAT; WISTAR RAT;

ANIMALS; BACTERIAL INFECTIONS; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; FEMALE; HUMANS; LIPOPOLYSACCHARIDES; NITRIC OXIDE; PERITONEAL CAVITY; PROBIOTICS; RATS; RATS, WISTAR;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; ESCHERICHIA COLI NISSLE 1917; NEGIBACTERIA; RATTUS;

EID: 77952627720     PISSN: 00155632     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12223-010-0027-4     Document Type: Article

References (53)

1. Altenhoefer A., Oswald S., Sonnenborn U., Enders C., Schulze J., Hacker J., Oelschlaeger T. A.: The probiotic Escherichia coli strain Nissle 1917 interferes with invasion of human intestinal epithelial cells by different enteroinvasive bacterial pathogens. FEMS Immunol. Med. Microbiol. 40, 223-229 (2004).
2. Bogdan C., Röllinghof M., Vodovotz Y., Xie Q. W., Nathan C.: Regulation of inducible nitric oxide synthase in macrophages by cytokines and microbial products, pp. 37-54 in Immunotherapy of Infections (K. N. Masihi, Ed.). Marcel Dekker, New York 1994.
3. Bogdan C., Vodovotz Y., Nathan C.: Macrophage deactivation by interleukin 10. J. Exp. Med. 174, 1549-1555 (1991).
4. 2 production. J. Biomed. Sci. 6, 425-432 (1999).
5. Chen C.-C., Wang J.-K.: p38 but not p44/42 mitogen-activated protein kinase is required for nitric oxide synthase induction mediated by lipopolysaccharide in RAW 264. 7 macrophages. Mol. Pharmacol. 55, 481-488 (1999).
6. Connelly L., Palacios-Callender M., Ameixa C., Moncada S., Hobbs A. J.: Biphasic regulation of NF-κB activity underlies the pro- and anti-inflammatory actions of nitric oxide. J. Immunol. 166, 3873-3881 (2001).
7. Cross M. L., Ganner A., Teilab D., Fray L. M.: Patterns of cytokine induction by Gram-positive and Gram-negative probiotic bacteria. FEMS Immunol. Med. Microbiol. 42, 173-180 (2004).
8. Deakin A. M., Payne A. N., Whittle B. J., Moncada S.: The modulation of IL-6 and TNF-α release by nitric oxide following stimulation of J774 cells with LPS and IFN-γ. Cytokine7, 406-416 (1995).
9. Ding A. H., Nathan C. F., Stuehr D. J.: Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141, 2407-2412 (1988).
10. Duhé R. J., Evans G. A., Erwin R. A., Kirken R. A., Cox G. W., Farrar W. L.: Nitric oxide and thiol redox regulation of Janus kinase activity. Proc. Nat. Acad. Sci. USA95, 126-131 (1998).
11. Fiorucci S., Santucci L., Cirino G., Mencarelli A., Familiari L., Del Soldato P., Morelli A.: IL-1β converting enzyme is a target for nitric oxide-releasing aspirin: new insights in the anti-inflammatory mechanism of nitric oxide-releasing nonsteroidal anti-inflammatory drugs. J. Immunol. 165, 5245-5254 (2000).
12. Förstermann U., Kleinert H.: Nitric oxide synthase: expression and expressional control of the three isoforms. Naunyn-Schmiedeberg's Arch. Pharmacol. 352, 351-364 (1995).
13. Gaillard T., Mülsch A., Klein H., Decker K.: Regulation by prostaglandin E2 of cytokine-elicited nitric oxide synthesis in rat liver macrophages. Biol. Chem. Hoppe-Seyler373, 897-902 (1992).
14. Gao J. J., Zuvanich E. G., Xue Q., Horn D. L., Silverstein R., Morrison D. C.: Bacterial DNA and LPS act in synergy in inducing nitric oxide production in RAW 264. 7 macrophages. J. Immunol. 163, 4095-4099 (1999).
15. Grozdanov L., Raasch C., Schulze J., Sonnenborn U., Gottschalk G., Hacker J., Dobrindt U.: Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J. Bacteriol. 186, 5432-5441 (2004).
16. Grozdanov L., Zähringer U., Blum-Oehler G., Brade L., Henne A., Knirel Y. A., Schombel U., Schulze J., Sonnenborn U., Gottschalk G., Hacker J., Rietschel E. T., Dobrindt U.: A single nucleotide exchange in the wzy gene is responsible for the semirough O6 lipopolysaccharide phenotype and serum sensitivity of Escherichia coli strain Nissle 1917. J. Bacteriol. 184, 5912-5925 (2002).
17. Hafez M., Hayes K., Goldrick M., Warhurst G., Grencis R., Roberts I. S.: The K5 capsule of Escherichia coli strain Nissle 1917 is important in mediating interactions with intestinal epithelial cells and chemokine induction. Infect. Immun. 77, 2995-3003 (2009).
18. Helwig U., Lammers K. M., Rizzello F., Brigidi P., Rohleder V., Caramelli E., Gionchetti P., Schrezenmeir J., Foelsch U. R., Schreiber S., Campieri M.: Lactobacilli, bifidobacteria and E. coli Nissle induce pro- and anti-inflammatory cytokines in peripheral blood mononuclear cells. World J. Gastroenterol. 12, 5978-5986 (2006).
19. Henker J., Laass M., Blokhin B. M., Bolbot Y. K., Maydannik V. G., Elze M., Wolff C., Schulze J.: The probiotic Escherichia coli strain Nissle 1917 (EcN) stops acute diarrhea in infants and toddlers. Eur. J. Pediatr. 166, 311-318 (2007).
20. Hockertz S.: Immunomodulating effect of killed, apathogenic Escherichia coli, strain Nissle 1917, on the macrophage system. Arzneimittelforschung41, 1108-1112 (1991).
21. Ivec M., Botić T., Koren S., Jakobsen M., Weingartl H., Cencic A.: Interactions of macrophages with probiotic bacteria lead to increased antiviral response against vesicular stomatitis virus. Antiviral Res. 75, 266-274 (2007).
22. Kallmann B. A., Malzkorn R., Kolb H.: Exogenous nitric oxide modulates cytokine production in human leukocytes. Life Sci. 65, 1787-1794 (1999).
23. Kamada N., Maeda K., Inoue N., Hisamatsu T., Okamoto S., Hong K. S., Yamada T., Watanabe N., Tsuchimoto K., Ogata H., Hibi T.: Nonpathogenic Escherichia coli strain Nissle 1917 inhibits signal transduction in intestinal epithelial cells. Infect. Immun. 76, 214-220 (2008).
24. Kruis W., Fric P., Pokrotnieks J., Lukás M., Fixa B., Kascák M., Kamm M. A., Weismueller J., Beglinger C., Stolte M., Wolff C., Schulze J.: Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut53, 1617-1623 (2004).
25. Lammers K. M., Helwig U., Swennen E., Rizzello F., Venturi A., Caramelli E., Kamm M. A., Brigidi P., Gionchetti P., Campieri M.: Effect of probiotic strains on interleukin 8 production by HT29/19A cells. Am. J. Gastroenterol. 97, 1182-1186 (2002).
26. Lander H. M.: An essential role for free radicals and derived species in signal transduction. FASEB J. 11, 118-124 (1997).
27. Malchow H. A.: Crohn's disease and Escherichia coli. A new approach in therapy to maintain remission of colonic Crohn's disease? J. Clin. Gastroenterol. 25, 653-658 (1997).
28. Marcinkiewicz J., Grabowsky A., Chain B.: Nitric oxide up-regulates the release of inflammatory mediators by mouse macrophages. Eur. J. Immunol. 25, 947-951 (1995).
29. Mercenier A., Pavan S., Pot B.: Probiotics as biotherapeutic agents: present knowledge and future prospects. Curr. Pharm. Des. 9, 175-191 (2003).
30. Mondel M., Schroeder B. O., Zimmermann K., Huber H., Nuding S., Beisner J., Fellermann K., Stange E. F., Wehkamp J.: Probiotic E. coli treatment mediates antimicrobial human β-defensin synthesis and fecal excretion in humans. Mucosal Immunol. 2, 166-172 (2009).
31. Nissle A.: Weiters über Grundlagen und Praxis der Mutaflorbehandlung. Deutsch. Med. Wochenschr. 44, 1809-1813 (1925).
32. Obermeier F., Gros, V., Schölmeric J., Falk W.: Interleukin-1 production by mouse macrophages is regulated in a feedback fashion by nitric oxide. J. Leukoc. Biol. 66, 829-836 (1999).
33. Otte J.-M., Podolsky D. K.: Functional modulation of enterocytes by Gram-positive and Gram-negative microorganisms. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G613-G626 (2004).
34. Ouadrhiri Y., Sibille Y., Tulkens P. M.: Modulation of intracellular growth of Listeria monocytogenes in human enterocyte Caco-2 cells by interferon-γ and interleukin-6: role of nitric oxide and cooperation with antibiotics. J. Infect. Dis. 180, 1195-1204 (1999).
35. Paoliello-Paschoalato A. B., Oliveira S. H., Cunha F. Q.: Interleukin 4 induces the expression of inducible nitric oxide synthase in eosinophils. Cytokine30, 116-124 (2005).
36. Patzer S. I., Baquero M. R., Bravo D., Moreno F., Hantke K.: The colicin G, H and X determinants encode microcins M and H47, which might utilize the catecholate siderophore receptors FepA, Cir, Fiu and IroN. Microbiology149, 2557-2570 (2003).
37. Peraldi P., Frodin M., Barnier J. V., Calleja V., Sciemeca J. C., Filloux C., Calothy G., van Obberghen E.: Regulation of the MAP kinase cascade in PC12 cells: B-Raf activates MEK-1 (MAP kinase or ERK kinase) and is inhibited by cAMP. FEBS Lett. 357, 290-296 (1995).
38. Rogerio F., Teixeira S. A., Junior H. J., Maria C. C., Vieira A. S., De Rezende A. C., Pereira G. A., Muscara M. N., Langone F.: mRNA and protein expression and activities of nitric oxide synthases in the lumbar spinal cord of neonatal rats after sciatic nerve transection and melatonin administration. Neurosci. Lett. 407, 182-187 (2006).
39. Ryu Y. H., Baik J. E., Yang J. S., Kang S. S., Im J., Yun C. H., Kim D. W., Lee K., Chung D. K., Ju H. R., Han S. H.: Differential immunostimulatory effects of Gram-positive bacteria due to their lipoteichoic acids. Internat. Immunopharmacol. 9, 127-133 (2009).
40. Salkowski C. A., Detore G., Mcnally R., van Rooijen N., Vogel S. N.: Regulation of inducible nitric oxide synthase messenger RNA expression and nitric oxide production by lipopolysaccharide in vivo. J. Immunol. 158, 905-912 (1997).
41. Schlee M., Wehkamp J., Altenhoefer A., Oelschlaeger T. A., Stange E. F., Fellermann K.: Induction of human β-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect. Immun. 75, 2399-2407 (2007).
42. Schultz M., Strauch U. G., Linde H. J., Watzl S., Obermeier F., Göttl C., Dunger N., Grunwald N., Schölmerich J., Rath H. C.: Preventive effects of Escherichia coli strain Nissle 1917 on acute and chronic intestinal inflammation in two different murine models of colitis. Clin. Diagn. Lab. Immunol. 11, 372-378 (2004).
43. Sirois J., Ménard G., Moses A. S., Bissonnette E. Y.: Importance of histamine in the cytokine network in the lung through H2 and H3 receptors: stimulation of IL-10 production. J. Immunol. 164, 2964-2970 (2000).
44. Sobko T., Huang L., Midtvedt T., Norin E., Gustafsson L. E., Norman M., Jansson E. A., Lundberg J. O.: Generation of NO by probiotic bacteria in the gastrointestinal tract. Free Radic. Biol. Med. 41, 985-991 (2006).
45. Stuehr D. J., Marletta M. A.: Induction of nitrite/nitrate synthesis in murine macrophages by BCG infection, lymphokines or interferon-γ. J. Immunol. 139, 518-525 (1987).
46. Sturm A., Rilling K., Baumgart D. C., Gargas K., Abou-Ghazalé T., Raupach B., Eckert J., Schumann R. R., Enders C., Sonnenborn U., Wiedenmann B., Dignass A. U.: Escherichia coli Nissle 1917 distinctively modulates T-cell cycling and expansion via toll-like receptor 2 signaling. Infect. Immun. 73, 1452-1465 (2005).
47. Tromm A., Niewerth U., Khoury M., Baestlein E., Wilhelms G., Schulze J., Stolte M.: The probiotic E. coli strain Nissle 1917 for the treatment of collagenous colitis: first results of an open-label trial. Z. Gastroenterol. 42, 365-369 (2004).
48. Ukena S. N., Westendorf A. M., Hansen W., Rohde M., Geffers R., Coldewey S., Suerbaum S., Buer J., Gunzer F.: The host response to the probiotic Escherichia coli strain Nissle 1917: specific up-regulation of the proinflammatory chemokine MCP-1. BMC Med. Genet. 6, 43 (2005).
49. Ukena S. N., Singh A., Dringenberg U., Engelhardt R., Seidler U., Hansen W., Bleich A., Bruder D., Franzke A., Rogler G., Suerbaum S., Buer J., Gunzer F., Westendorf A. M.: Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PloS One2, e1308 (2007).
50. Wang S., Yan L., Wesley R. A., Danner R. L.: Nitric oxide increases tumor necrosis factor production in differentiated U937 cells by decreasing cyclic AMP. J. Biol. Chem. 272, 5959-5965 (1997).
51. Westphal O., Luderitz O., Bister F.: Über die Extraktion von Bakterien mit Phenol/Wasser. Z. Naturforsch. 7, 148-155 (1952).
52. Xie Q.-W.: A novel lipopolysaccharide-response element contributes to induction of nitric oxide synthase. J. Biol. Chem. 272, 14867-14872 (1997).
53. Yang W. W., Krukoff T. L.: Nitric oxide regulates body temperature, neuronal activation and interleukin-1β gene expression in the hypothalamic paraventricular nucleus in response to immune stress. Neuropharmacology39, 2075-2089 (2000).