1887

Abstract

is an avian enterohepatic species that, more recently, has also been found as a naturally acquired infection in mice and rats, and isolated from patients with gastrointestinal and hepatobiliary diseases. In this work, the interaction between and murine macrophages was examined. Firstly, the impact of nitric oxide, which is an antimicrobial produced by mammalian macrophages, on 6350-92 viability and morphology was studied by colony-forming assays and light microscopy, respectively. Exposure to nitric oxide lowered viability, in a growth-phase-dependent manner, and decreased the mean cell size. However, the number of coccoid forms remained low, contrasting with what has been observed for other species. Confocal microscopy showed that is internalized by murine macrophages, triggering nitric oxide production that promotes phagocytosis and killing of the pathogen. Interaction between and macrophages stimulated secretion of pro-inflammatory cytokines, such as TNF-α, IL-1β, IL-6 and MIP-2. These results show that is able to infect mammalian murine cells triggering an inflammatory response.

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2016-03-01
2024-04-19
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References

  1. Benaissa M., Babin P., Quellard N., Pezennec L., Cenatiempo Y., Fauchère J. L. 1996; Changes in Helicobacter pyloriultrastructure and antigens during conversion from the bacillary to the coccoid form. Infect Immun 64:2331–2335[PubMed]
    [Google Scholar]
  2. Bishayi B., Bandyopadhyay D., Majhi A., Adhikary R. 2015; Effect of exogenous MCP-1 on TLR-2 neutralized murine macrophages and possible mechanisms of CCR-2/TLR-2 and MCP-1 signalling during Staphylococcus aureus infection. Immunobiology 220:350–362 [View Article][PubMed]
    [Google Scholar]
  3. Borges V., Santos A., Correia C. B., Saraiva M., Ménard A., Vieira L., Sampaio D. A., Pinheiro M., Gomes J. P., Oleastro M. 2015; Helicobacter pullorum isolated from fresh chicken meat: antibiotic resistance and genomic traits of an emerging foodborne pathogen. Appl Environ Microbiol 81:8155–8163 [View Article][PubMed]
    [Google Scholar]
  4. Boutin S. R., Shen Z., Roesch P. L., Stiefel S. M., Sanderson A. E., Multari H. M., Pridhoko E. A., Smith J. C., Taylor N. S., other authors. 2010; Helicobacter pullorum outbreak in C57BL/6NTac and C3H/HeNTac barrier-maintained mice. J Clin Microbiol 48:1908–1910 [View Article][PubMed]
    [Google Scholar]
  5. Broniowska K. A., Diers A. R., Hogg N. 2013; S-Nitrosoglutathione. Biochim Biophys Acta 1830:3173–3181 [View Article][PubMed]
    [Google Scholar]
  6. Burnens A. P., Stanley J., Morgenstern R., Nicolet J. 1994; Gastroenteritis associated with Helicobacter pullorum . Lancet 344:1569–1570 [View Article][PubMed]
    [Google Scholar]
  7. Cacioppo L. D., Shen Z., Parry N. M., Fox J. G. 2012a; Resistance of Sprague-Dawley rats to infection with Helicobacter pullorum . J Am Assoc Lab Anim Sci 51:803–807[PubMed]
    [Google Scholar]
  8. Cacioppo L. D., Turk M. L., Shen Z., Ge Z., Parry N., Whary M. T., Boutin S. R., Klein H. J., Fox J. G. 2012b; Natural and experimental Helicobacter pullorum infection in brown Norway rats. J Med Microbiol 61:1319–1323 [View Article][PubMed]
    [Google Scholar]
  9. Castéra L., Pedeboscq A., Rocha M., LeBail B., Asencio C., deLédinghen V., Bernard P. H., Laurent C., Lafon M. E., other authors. 2006; Relationship between the severity of hepatitis C virus-related liver disease and the presence of Helicobacter species in the liver: a prospective study. World J Gastroenterol 12:7278–7284[PubMed] [CrossRef]
    [Google Scholar]
  10. Ceelen L., Decostere A., Martel A., Pasmans F., Haesebrouck F. 2006a; First report of Helicobacter pullorum in the faeces of a diarrhoeic psittacine bird (Psephotus haematogaster). Vet Rec 159:389–390 [View Article][PubMed]
    [Google Scholar]
  11. Ceelen L. M., Haesebrouck F., Favoreel H., Ducatelle R., Decostere A. 2006b; The cytolethal distending toxin among Helicobacter pullorum strains from human and poultry origin. Vet Microbiol 113:45–53 [View Article][PubMed]
    [Google Scholar]
  12. Cherdantseva L. A., Potapova O. V., Sharkova T. V., Belyaeva Y. Y., Shkurupiy V. A. 2014; Association of Helicobacter pylori and iNOS production by macrophages and lymphocytes in the gastric mucosa in chronic gastritis. J Immunol Res 2014:762514 [CrossRef]
    [Google Scholar]
  13. Cole S. P., Kharitonov V. F., Guiney D. G. 1999; Effect of nitric oxide on Helicobacter pylori morphology. J Infect Dis 180:1713–1717 [View Article][PubMed]
    [Google Scholar]
  14. Fox J. G., Dewhirst F. E., Shen Z., Feng Y., Taylor N. S., Paster B. J., Ericson R. L., Lau C. N., Correa P., other authors. 1998; Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 114:755–763 [View Article][PubMed]
    [Google Scholar]
  15. Hughes M. N. 2008; Chemistry of nitric oxide and related species. Methods Enzymol 436:3–19 [View Article][PubMed]
    [Google Scholar]
  16. Hynes S. O., Ferris J. A., Szponar B., Wadström T., Fox J. G., O'Rourke J., Larsson L., Yaquian E., Ljungh A., other authors. 2004; Comparative chemical and biological characterization of the lipopolysaccharides of gastric and enterohepatic helicobacters. Helicobacter 9:313–323 [View Article][PubMed]
    [Google Scholar]
  17. Justino M. C., Ecobichon C., Fernandes A. F., Boneca I. G., Saraiva L. M. 2012; Helicobacter pylori has an unprecedented nitric oxide detoxifying system. Antioxid Redox Signal 17:1190–1200 [View Article][PubMed]
    [Google Scholar]
  18. Justino M. C., Parente M. R., Boneca I. G., Saraiva L. M. 2014; FrxA is an S-nitrosoglutathione reductase enzyme that contributes to Helicobacter pylori pathogenicity. FEBS J 281:4495–4505 [View Article][PubMed]
    [Google Scholar]
  19. Kleine M., Worbs T., Schrem H., Vondran F. W., Kaltenborn A., Klempnauer J., Förster R., Josenhans C., Suerbaum S., Bektas H. 2014; Helicobacter hepaticus induces an inflammatory response in primary human hepatocytes. PLoS One 9:e99713 [View Article][PubMed]
    [Google Scholar]
  20. Kusters J. G., Gerrits M. M., Van Strijp J. A., Vandenbroucke-Grauls C. M. 1997; Coccoid forms of Helicobacter pylori are the morphologic manifestation of cell death. Infect Immun 65:3672–3679[PubMed]
    [Google Scholar]
  21. Laharie D., Asencio C., Asselineau J., Bulois P., Bourreille A., Moreau J., Bonjean P., Lamarque D., Pariente A., other authors. 2009; Association between entero-hepatic Helicobacter species and Crohn's disease: a prospective cross-sectional study. Aliment Pharmacol Ther 30:283–293 [View Article][PubMed]
    [Google Scholar]
  22. Lutay N., Nilsson I., Wadström T., Ljungh A. 2011; Effect of heparin, fucoidan and other polysaccharides on adhesion of enterohepatic Helicobacter species to murine macrophages. Appl Biochem Biotechnol 164:1–9 [View Article][PubMed]
    [Google Scholar]
  23. MacMicking J., Xie Q. W., Nathan C. 1997; Nitric oxide and macrophage function. Annu Rev Immunol 15:323–350 [View Article][PubMed]
    [Google Scholar]
  24. Melito P. L., Woodward D. L., Bernard K. A., Price L., Khakhria R., Johnson W. M., Rodgers F. G. 2000; Differentiation of clinical Helicobacter pullorum isolates from related Helicobacter and Campylobacter species. Helicobacter 5:142–147 [View Article][PubMed]
    [Google Scholar]
  25. Nebbia P., Tramuta C., Ortoffi M., Bert E., Cerruti Sola S., Robino P. 2007; Identification of enteric Helicobacter in avian species. Schweiz Arch Tierheilkd 149:403–407 [View Article][PubMed]
    [Google Scholar]
  26. Olken N. M., Marletta M. A. 1993; NG-Methyl-L-arginine functions as an alternate substrate and mechanism-based inhibitor of nitric oxide synthase. Biochemistry 32:9677–9685 [View Article][PubMed]
    [Google Scholar]
  27. Olken N. M., Rusche K. M., Richards M. K., Marletta M. A. 1991; Inactivation of macrophage nitric oxide synthase activity by NG-methyl-L-arginine. Biochem Biophys Res Commun 177:828–833 [View Article][PubMed]
    [Google Scholar]
  28. Pautz A., Art J., Hahn S., Nowag S., Voss C., Kleinert H. (2010); Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide 23:75–93 [CrossRef]
    [Google Scholar]
  29. Qu W., Zhou Y., Sun Y., Fang M., Yu H., Li W., Liu Z., Zeng J., Chen C., other authors. 2011; Identification of S-nitrosylation of proteins of Helicobacter pylori in response to nitric oxide stress. J Microbiol 49:251–256 [View Article][PubMed]
    [Google Scholar]
  30. Rizwan M., Alvi A., Ahmed N. 2008; Novel protein antigen (JHP940) from the genomic plasticity region of Helicobacter pylori induces tumor necrosis factor alpha and interleukin-8 secretion by human macrophages. J Bacteriol 190:1146–1151 [View Article][PubMed]
    [Google Scholar]
  31. Rocha M., Avenaud P., Ménard A., Le Bail B., Balabaud C., Bioulac-Sage P., de Magalhães Queiroz D. M., Mégraud F. 2005; Association of Helicobacter species with hepatitis C cirrhosis with or without hepatocellular carcinoma. Gut 54:396–401 [View Article][PubMed]
    [Google Scholar]
  32. Schneider C. A., Rasband W. S., Eliceiri K. W. 2012; NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675 [View Article][PubMed]
    [Google Scholar]
  33. Siegele D. A., Kolter R. 1992; Life after log. J Bacteriol 174:345–348[PubMed]
    [Google Scholar]
  34. Sirianni A., Kaakoush N. O., Raftery M. J., Mitchell H. M. 2013; The pathogenic potential of Helicobacter pullorum: possible role for the type VI secretion system. Helicobacter 18:102–111 [View Article][PubMed]
    [Google Scholar]
  35. Srisuwan S., Tongtawe P., Srimanote P., Voravuthikunchai S. P. 2014; Rhodomyrtone modulates innate immune responses of THP-1 monocytes to assist in clearing methicillin-resistant Staphylococcus aureus . PLoS One 9:e110321 [View Article][PubMed]
    [Google Scholar]
  36. Stanley J., Linton D., Burnens A. P., Dewhirst F. E., On S. L. W., Porter A., Owen R. J., Costas M. 1994; Helicobacter pullorum sp. nov.– genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology 140:3441–3449 [View Article][PubMed]
    [Google Scholar]
  37. Steinbrueckner B., Haerter G., Pelz K., Weiner S., Rump J. A., Deissler W., Bereswill S., Kist M. 1997; Isolation of Helicobacter pullorum from patients with enteritis. Scand J Infect Dis 29:315–318 [View Article][PubMed]
    [Google Scholar]
  38. Taneera J., Moran A. P., Hynes S. O., Nilsson H.-O., abu Al-Soud W., Wadström T. 2002; Influence of activated charcoal, porcine gastric mucin and β-cyclodextrin on the morphology and growth of intestinal and gastric Helicobacter spp. Microbiology 148:677–684 [View Article][PubMed]
    [Google Scholar]
  39. Tekamp-Olson P., Gallegos C., Bauer D., McClain J., Sherry B., Fabre M., van Deventer S., Cerami A. 1990; Cloning and characterization of cDNAs for murine macrophage inflammatory protein 2 and its human homologues. J Exp Med 172:911–919 [View Article][PubMed]
    [Google Scholar]
  40. Thomas D. D., Miranda K. M., Espey M. G., Citrin D., Jourd'heuil D., Paolocci N., Hewett S. J., Colton C. A., Grisham M. B., other authors. 2002; Guide for the use of nitric oxide (NO) donors as probes of the chemistry of NO and related redox species in biological systems. Methods Enzymol 359:84–105 [View Article][PubMed]
    [Google Scholar]
  41. Turk M. L., Cacioppo L. D., Ge Z., Shen Z., Whary M. T., Parry N., Boutin S. R., Klein H. J., Fox J. G. 2012; Persistent Helicobacter pullorum colonization in C57BL/6NTac mice: a new mouse model for an emerging zoonosis. J Med Microbiol 61:720–728 [View Article][PubMed]
    [Google Scholar]
  42. Varon C., Duriez A., Lehours P., Ménard A., Layé S., Zerbib F., Mégraud F., Laharie D. 2009; Study of Helicobacter pullorum proinflammatory properties on human epithelial cells in vitro . Gut 58:629–635 [View Article][PubMed]
    [Google Scholar]
  43. Varon C., Mocan I., Mihi B., Péré-Védrenne C., Aboubacar A., Moraté C., Oleastro M., Doignon F., Laharie D., other authors. 2014; Helicobacter pullorum cytolethal distending toxin targets vinculin and cortactin and triggers formation of lamellipodia in intestinal epithelial cells. J Infect Dis 209:588–599 [View Article][PubMed]
    [Google Scholar]
  44. Veijola L., Nilsson I., Halme L., abu Al-Soud W. A., Mäkinen J., Ljungh A., Rautelin H. 2007; Detection of Helicobacter species in chronic liver disease and chronic inflammatory bowel disease. Ann Med 39:554–560 [View Article][PubMed]
    [Google Scholar]
  45. Wroblewski L. E., Peek R. M. Jr., Wilson K. T. 2010; Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23:713–739 [View Article][PubMed]
    [Google Scholar]
  46. Yap L. P., Sancheti H., Ybanez M. D., Garcia J., Cadenas E., Han D. 2010; Determination of GSH, GSSG, and GSNO using HPLC with electrochemical detection. Methods Enzymol 473:137–147 [View Article][PubMed]
    [Google Scholar]
  47. Young V. B., Chien C. C., Knox K. A., Taylor N. S., Schauer D. B., Fox J. G. 2000; Cytolethal distending toxin in avian and human isolates of Helicobacter pullorum . J Infect Dis 182:620–623 [View Article][PubMed]
    [Google Scholar]
  48. Zanoni R. G., Piva S., Rossi M., Pasquali F., Lucchi A., De Cesare A., Manfreda G. 2011; Occurrence of Helicobacter pullorum in turkeys. Vet Microbiol 149:492–496 [View Article][PubMed]
    [Google Scholar]
  49. Zeng H., Guo G., Mao X. H., Tong W. D., Zou Q. M. 2008; Proteomic insights into Helicobacter pylori coccoid forms under oxidative stress. Curr Microbiol 57:281–286 [View Article][PubMed]
    [Google Scholar]
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