Interleukin-6 induction by Helicobacter pylori in human macrophages is dependent on phagocytosis

Helicobacter

Volumn 11, Issue 3, 2006, Pages 196-207

  Odenbreit, Stefan ^a   Linder, Stefan ^a   Gebert Vogl, Bettina ^a   Rieder, Gabriele ^a   Moran, Anthony P ^b   Haas, Rainer ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Helicobacter pylori; Interleukin 6; Lipopolysaccharide; Macrophage; Phagocytosis

Indexed keywords

ACTIN; CYTOKINE; INTERLEUKIN 1; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EVALUATION; GRANULOCYTE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; MACROPHAGE ACTIVATION; MONOCYTE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; RISK FACTOR; SIGNAL TRANSDUCTION; STOMACH MUCOSA;

ANIMALS; CELL LINE; GASTRIC MUCOSA; HELICOBACTER PYLORI; HL-60 CELLS; HUMANS; INTERLEUKIN-6; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; PHAGOCYTOSIS;

ANIMALIA; ESCHERICHIA COLI; HELICOBACTER; HELICOBACTER PYLORI; MURINAE;

EID: 33646712560     PISSN: 10834389     EISSN: 15235378     Source Type: Journal    
DOI: 10.1111/j.1523-5378.2006.00400.x     Document Type: Article

References (60)

1. Ernst PB Gold BD The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer Annu Rev Microbiol 2000 54 615 40
2. Lindholm C Quiding-Jarbrink M Lonroth H Hamlet A Svennerholm AM Local cytokine response in Helicobacter pylori-infected subjects Infect Immun 1998 66 5964 71
3. Bodger K Crabtree JE Helicobacter pylori and gastric inflammation Br Med Bull 1998 54 139 50
4. Odenbreit S Püls J Sedlmaier B Gerland E Fischer W Haas R Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion Science 2000 287 1497 500
5. Odenbreit S Gebert B Püls J Fischer W Haas R Interaction of Helicobacter pylori with professional phagocytes: role of the Cag pathogenicity island and translocation, phosphorylation and processing of CagA Cell Microbiol 2001 3 21 31
6. Fischer W Püls J Buhrdorf R Gebert B Odenbreit S Haas R Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8 Mol Microbiol 2001 42 1337 48
7. Viala J Chaput C Boneca IG et al Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island Nat Immunol 2004 5 1166 74
8. Yamaoka Y Kwon DH Graham DY A M(r) 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori Proc Natl Acad Sci U S A 2000 97 7533 8
9. Naka T Nishimoto N Kishimoto T The paradigm of IL-6: from basic science to medicine Arthritis Res 2002 4 S233 42
10. de Man P van Kooten C Aarden L Engberg I Linder H Svanborg EC Interleukin-6 induced at mucosal surfaces by Gram-negative bacterial infection Infect Immun 1989 57 3383 8
11. Kotloff RM Little J Elias JA Human alveolar macrophage and blood monocyte interleukin-6 production Am J Respir Cell Mol Biol 1990 3 497 505
12. Heumann D Barras C Severin A Glauser MP Tomasz A Gram-positive cell walls stimulate synthesis of tumor necrosis factor alpha and interleukin-6 by human monocytes Infect Immun 1994 62 2715 21
13. Dokter WH Dijkstra AJ Koopmans SB Mulder AB Stulp BK Halie MR Keck W Vellenga E G(AnH)MTetra, a naturally occurring 1,6-anhydro muramyl dipeptide, induces granulocyte colony-stimulating factor expression in human monocytes: a molecular analysis Infect Immun 1994 62 2953 7
14. Galdiero M D'Isanto M Vitiello M Finamore E Peluso L Galdiero M Porins from Salmonella enterica serovar Typhimurium induce TNF-alpha, IL-6 and IL-8 release by CD14-independent and CD11a/CD18-dependent mechanisms Microbiology 2001 147 2697 704
15. Wullt B The role of P fimbriae for Escherichia coli establishment and mucosal inflammation in the human urinary tract Int J Antimicrob Agents 2003 21 605 21
16. Zhang Y Broser M Rom WN Activation of the interleukin 6 gene by Mycobacterium tuberculosis or lipopolysaccharide is mediated by nuclear factors NF-IL6 and NF-kappa B Proc Natl Acad Sci U S A 1994 91 2225 9
17. Pritts T Hungness E Wang Q Robb B Hershko D Hasselgren PO Mucosal and enterocyte IL-6 production during sepsis and endotoxemia - role of transcription factors and regulation by the stress response Am J Surg 2002 183 372 83
18. Crabtree JE Shallcross TM Heatley RV Wyatt JI Mucosal tumour necrosis factor alpha and interleukin-6 in patients with Helicobacter pylori associated gastritis Gut 1991 32 1473 7
19. Lindholm C Quiding-Jarbrink M Lonroth H Svennerholm AM Induction of chemokine and cytokine responses by Helicobacter pylori in human stomach explants Scand J Gastroenterol 2001 36 1022 9
20. Guiraldes E Duarte I Pena A Godoy A Espinosa MN Bravo R Larrain F Schultz M Harris P Proinflammatory cytokine expression in gastric tissue from children with Helicobacter pylori-associated gastritis J Pediatr Gastroenterol Nutr 2001 33 127 32
21. Gobert AP Bambou JC Werts C Balloy V Chignard M Moran AP Ferrero RL Helicobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism J Biol Chem 2004 279 245 50
22. Leying H Suerbaum S Geis G Haas R Cloning and genetic characterization of a Helicobacter pylori flagellin gene Mol Microbiol 1992 6 2863 74
23. Kahrs AF Odenbreit S Schmitt W Heuermann D Meyer TF Haas R An improved TnMax mini-transposon system suitable for sequencing, shuttle mutagenesis and gene fusions Gene 1995 167 53 7
24. Labigne A Cussac V Courcoux P Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity J Bacteriol 1991 173 1920 31
25. Hauert AB Martinelli S Marone C Niggli V Differentiated HL-60 cells are a valid model system for the analysis of human neutrophil migration and chemotaxis Int J Biochem Cell Biol 2002 34 838 54
26. Linder S Nelson D Weiss M Aepfelbacher M Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages Proc Natl Acad Sci U S A 1999 96 9648 53
27. Bradford MM A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 1976 72 248 54
28. Odenbreit S Faller G Haas R Role of the AlpAB proteins and lipopolysaccharide in adhesion of Helicobacter pylori to human gastric tissue Int J Med Microbiol 2002 292 247 56
29. Moran AP Helander IM Kosunen TU Compositional analysis of Helicobacter pylori rough-form lipopolysaccharides J Bacteriol 1992 174 1370 7
30. Moran AP Knirel YA Senchenkova SN Widmalm G Hynes SO Jansson PE Phenotypic variation in molecular mimicry between Helicobacter pylori lipopolysaccharides and human gastric epithelial cell surface glycoforms. Acid-induced phase variation in Lewis(x) and Lewis(y) expression by H. pylori lipopolysaccharides J Biol Chem 2002 277 5785 95
31. Bazil V Baudys M Hilgert I Stefanova I Low MG Zbrozek J Horejsi V Structural relationship between the soluble and membrane-bound forms of human monocyte surface glycoprotein CD14 Mol Immunol 1989 26 657 62
32. Moran AP Molecular structure, biosynthesis, and pathogenic roles of lipopolysaccharides In Mobley HLT Mendz GL Hazell SL eds Helicobacter pylori: Physiology and Genetics Washington DC ASM Press 2001 81 95
33. da Silva CJ Soldau K Christen U Tobias PS Ulevitch RJ Lipopolysaccharide is in close proximity to each of the proteins in its membrane receptor complex. Transfer from CD14 to TLR4 and MD-2 J Biol Chem 2001 276 21129 35
34. Bauer S Kirschning CJ Hacker H Redecke V Hausmann S Akira S Wagner H Lipford GB Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition Proc Natl Acad Sci U S A 2001 98 9237 42
35. Whitney AE Emory TS Marty AM O'Shea PA Newman GW Gold BD Increased macrophage infiltration of gastric mucosa in Helicobacter pylori-infected children Dig Dis Sci 2000 45 1337 42
36. Suzuki T Kato K Ohara S Noguchi K Sekine H Nagura H Shimosegawa T Localization of antigen-presenting cells in Helicobacter pylori-infected gastric mucosa Pathol Int 2002 52 265 71
37. Crabtree JE Mahony MJ Taylor JD Heatley RV Littlewood JM Tompkins DS Immune responses to Helicobacter pylori in children with recurrent abdominal pain J Clin Pathol 1991 44 768 71
38. Bazillou M Fendri C Castel O Ingrand P Fauchere JL Serum antibody response to the superficial and released components of Helicobacter pylori Clin Diagn Lab Immunol 1994 1 310 7
39. Muotiala A Helander IM Phyälä L Kosunen TU Moran AP Low biological activity of Helicobacter pylori lipopolysaccharide Infect Immun 1992 60 1714 6
40. Birkholz S Knipp U Nietzki C Adamek RJ Opferkuch W Immunological activity of lipopolysaccharide of Helicobacter pylori on human peripheral mononuclear blood cells in comparison to lipopolysaccharides of other intestinal bacteria FEMS Immunol Med Microbiol 1993 6 317 24
41. Ogawa T Suda Y Kashihara W Hayashi T Shimoyama T Kusumoto S Tamura T Immunobiological activities of chemically defined lipid A from Helicobacter pylori LPS in comparison with Porphyromonas gingivalis lipid A and Escherichia coli-type synthetic lipid A (compound 506) Vaccine 1997 15 1598 605
42. Moran AP Lindner B Walsh EJ Structural characterization of the lipid A component of Helicobacter pylori rough- and smooth-form lipopolysaccharides J Bacteriol 1997 179 6453 63
43. Suda Y Kim YM Ogawa T et al. Chemical structure and biological activity of a lipid A component from Helicobacter pylori strain 206 J Endotoxin Res 2001 7 95 104
44. Schromm AB Brandenburg K Loppnow H Moran AP Koch MH Rietschel ET Seydel U Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion Eur J Biochem 2000 267 2008 13
45. Schromm AB Brandenburg K Loppnow H Zahringer U Rietschel ET Carroll SF Koch MH Kusumoto S Seydel U The charge of endotoxin molecules influences their conformation and IL-6-inducing capacity J Immunol 1998 161 5464 71
46. Zähringer U Salvetzki R Wagner F Lindner B Ulmer AJ Structural and biological characterisation of a novel tetra-acyl lipid A from Escherichia coli F515 lipopolysaccharide acting as endotoxin antagonist in human monocytes J Endotoxin Res 2001 7 133 46
47. Cunningham MD Seachord C Ratcliffe K Bainbridge B Aruffo A Darveau RP Helicobacter pylori and Porphyromonas gingivalis lipopolysaccharides are poorly transferred to recombinant soluble CD14 Infect Immun 1996 64 3601 8
48. Mandell L Moran AP Cocchiarella A Houghton J Taylor N Fox JG Wang TC Kurt-Jones EA Intact Gram-negative Helicobacter pylori, Helicobacter felis, and Helicobacter hepaticus bacteria activate innate immunity via toll-like receptor 2 but not toll-like receptor 4 Infect Immun 2004 72 6446 54
49. Galdiero M Galdiero M Finamore E Rossano F Gambuzza M Catania MR Teti G Midiri A Mancuso G Haemophilus influenzae porin induces Toll-like receptor 2-mediated cytokine production in human monocytes and mouse macrophages Infect Immun 2004 72 1204 9
50. Ahmad-Nejad P Hacker H Rutz M Bauer S Vabulas RM Wagner H Bacterial CpG-DNA and lipopolysaccharides activate toll-like receptors at distinct cellular compartments Eur J Immunol 2002 32 1958 68
51. Schmaußer B Andrulis M Endrich S Lee SK Josenhans C Muller-Hermelink HK Eck M Expression and subcellular distribution of toll-like receptors TLR4, TLR5 and TLR9 on the gastric epithelium in Helicobacter pylori infection Clin Exp Immunol 2004 136 521 6
52. Harris PR Ernst PB Kawabata S Kiyono H Graham MF Smith PD Recombinant Helicobacter pylori urease activates primary mucosal macrophages J Infect Dis 1998 178 1516 20
53. Münzenmaier A Lange C Glocker E Covacci A Moran A Bereswill S Baeuerle PA Kist M Pahl HL A secreted/shed product of Helicobacter pylori activates transcription factor nuclear factor-kappa B J Immunol 1997 159 6140 7
54. Haas R Meyer TF van Putten JPM Aflagellated mutants of Helicobacter pylori generated by genetic transformation of naturally competent strains using transposon shuttle mutagenesis Mol Microbiol 1993 8 753 60
55. Schmitt W Haas R Genetic analysis of the Helicobacter pylori vacuolating cytotoxin: structural similarities with IgA protease type of exported protein Mol Microbiol 1994 12 307 19
56. Tomb JF White O Kerlavage AR et al The complete genome sequence of the gastric pathogen Helicobacter pylori Nature 1997 388 539 47
57. Alm RA Ling LS Moir DT et al Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori Nature 1999 397 176 80
58. Heep M Odenbreit S Beck D Decker J Prohaska E Rieger U Lehn N Mutations at four distinct regions of the rpoB gene can reduce the susceptibility of Helicobacter pylori to rifamycins Antimicrob Agents Chemother 2000 44 1713 5
59. Dubois A Berg DE Incecik ET Fiala N Heman-Ackah LM Del Valle J Yang M Wirth HP Perez-Perez GI Blaser MJ Host specificity of Helicobacter pylori strains and host responses in experimentally challenged nonhuman primates Gastroenterol 1999 116 90 6
60. Kwon DH Woo JS Perng CL Go MF Graham DY El-Zaatari FA The effect of galE gene inactivation on lipopolysaccharide profile of Helicobacter pylori Curr Microbiol 1998 37 144 8