The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a protective antigen and a major virulence factor

Journal of Experimental Medicine

Volumn 191, Issue 9, 2000, Pages 1467-1476

  Satin, Barbara ^a   Del Giudice, Giuseppe ^b   Della Bianca, Vittorina ^c   Dusi, Stefano ^c   Laudanna, Carlo ^c   Tonello, Fiorella ^a   Kelleher, Dermot ^d   Rappuoli, Rino ^b   Montecucco, Cesare ^a   Rossi, Filippo ^c  

^a UNIVERSITY OF PADOVA   (Italy)

^b CHIRON VACCINES   (Italy)

^c UNIVERSITY OF VERONA   (Italy)

^d TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Chemotaxis; Helicobacter; Monocytes; NADPH oxidase; Neutrophils

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CALCIUM; FURA 2; GAMMA INTERFERON; HOMOVANILLIC ACID; HORSERADISH PEROXIDASE; PERTUSSIS TOXIN; PHOSPHOPROTEIN PHOSPHATASE 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TUMOR NECROSIS FACTOR ALPHA; VIRULENCE FACTOR; WORTMANNIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; BACTERIAL VIRULENCE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOSOL; GRAM NEGATIVE INFECTION; HELICOBACTER PYLORI; INFLAMMATORY INFILTRATE; LEUKOCYTE ACTIVATION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; STOMACH MUCOSA; VACCINATION; VACCINE PRODUCTION;

ANDROSTADIENES; ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CALCIUM SIGNALING; CHEMOTAXIS, LEUKOCYTE; CYTOSOL; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INTEGRINS; MICE; MONOCYTES; NADPH OXIDASE; NEUTROPHILS; PERTUSSIS TOXIN; PROTEINS; REACTIVE OXYGEN SPECIES; VACCINATION; VIRULENCE FACTORS, BORDETELLA;

EID: 0034193362     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.9.1467     Document Type: Article

References (69)

1. Warren, J.D., and B.J. Marshall. 1983. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1:1273-1275.
2. Marshall, B.J., J.A. Armstrong, D.B. McGechie, and R.J. Glancy. 1985. Attempt to fulfill Koch's postulates for pyloric Campylobacter. Med. J. Austr. 142:436-439.
3. Goodwin, C.S. 1997. Helicobacter pylori gastritis, peptic ulcer and gastric cancer: clinical and molecular aspects. Clin. Infect. Dis. 25:1017-1019.
4. Bayerdorffer, E., N. Lehn, R. Hatz, G.A. Mannes, H. Oertel, T. Sauerbruch, and M. Stolte. 1992. Difference in expression of Helicobacter pylori gastritis in antrum and body. Gastroenterology. 102:1575-1582.
5. Fiocca, R., L. Villani, O. Luinetti, A. Gianotti, M. Perego, C. Alvisi, F. Turpini, and E. Solcia. 1992. Helicobacter colonization and histopathological profile of chronic gastritis in patients with or without dyspepsia, mucosal erosion and peptic ulcer: a morphological approach to the study of ulcerogenesis in man. Virchows Archiv. A Pathol. Anat. Histopathol. 420:489-492.
6. Davies, G.R., N.J. Simmod, T.R. Stevens, A. Grandinson, D.R. Blake, and D.S. Rampton. 1992. Mucosal reactive oxygen metabolite production in duodenal ulcer disease. Gut. 33:1467-1472.
7. Fiocca, R., O. Luinetti, L. Villani, A.M. Chiaravelli, C. Capella, and E. Solcia. 1994. Epithelial cytotoxicity, immune response, and inflammatory components of Helicobacter pylori gastritis. Scand. J. Gastroenterol. 205:11-21.
8. Karttunen, R., G. Anderson, K. Poikonen, T.U. Kosunen, T. Karttunen, K. Juutinen, and S. Niemela. 1990. Helicobacter pylori induces lymphocyte activation in peripheral blood culture. Clin. Exp. Immunol. 82:485-488.
9. Mai, U.E., G.I. Perez-Perez, L.M. Wahl, S.M. Wahl, M.J. Blaser, and P.D. Smith. 1991. Soluble surface protein from Helicobacter pylori activate monocytes/macrophages by lipopolysaccharide-independent mechanism. J. Clin. Invest. 87: 894-900.
10. Mai, U.E., G.I. Perez-Perez, J.B. Allen, S.M. Wahl, M.J. Blaser, and P.D. Smith. 1992. Surface proteins from Helicobacter pylori exhibit chemotactic activity for human leukocytes and are present in gastric mucosa. J. Exp. Med. 175:517-525.
11. Craig, P.M., M.C. Territo, W.E. Karnes, and J.H. Walsh. 1992. Helicobacter pylori secretes a chemotactic factor for monocytes and neutrophils. Gut. 33:1020-1023.
12. Nielsen, H., and L.P. Andersen. 1992. Activation of human phagocytes oxidative metabolism by Helicobacter pylori. Gastroenterology. 103:1747-1753.
13. Nielsen, H., and L.P. Andersen. 1992. Chemotactic activity of Helicobacter pylori sonicate for human polymorphonuclear leukocytes and monocytes. Gut. 33:738-742.
14. Reymunde, A., J. Deren, I. Nachamkin, D. Oppenheim, and G. Weinbaum. 1993. Production of chemoattractant by Helicobacter pylori. Dig. Dis. Sci. 38:1697-1701.
15. Kozol, R., B. McCurdy, and R. Czanko. 1993. A neutrophil chemotactic factor present in Helicobacter pylori but absent in Helicobacter mustelae. Dig. Dis. Sci. 38:137-141.
16. Marchetti, M., B. Aricò, D. Burroni, N. Figura, R. Rappuoli, and P. Ghiara. 1995. Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science. 267:1655-1658.
17. Evans, D.J., Jr., D.J. Evans, H.C. Lampert, and H. Nakano. 1995. Identification of four new prokaryotic bacterioferritins, from Hilicobacter pylori, Anabaena variabilis, Bacillus subtilis and Treponema pallidum, by analysis of gene sequences. Gene. 153: 123-127.
18. Rautelin, H., B. Blomberg, H. Fredlund, G. Jarnerot, and D. Danielsson. 1993. Incidence of Helicobacter pylori strains activating neutrophils in patients with peptic ulcer disease. Gut. 34:599-603.
19. Yoshida, N., D.N. Granger, D.J. Evans, D.G. Evans, D.Y. Graham, D.C. Anderson, R.E. Wolf, and P.R. Kvietys. 1993. Mechanism involved in Helicobacter pylori-produced inflammation. Gastroenterology. 105:1431-1440.
20. Evans, D.J., Jr., D.G Evans, T. Takemura, H. Nakano, H.C. Lampert, D.Y. Graham, D.N. Dranger, and P.R. Kvietys. 1995. Characterization of a Helicobacter pylori neutrophil-activating protein. Infect. Immun. 63:2213-2220.
21. Cover, T.L., M.K.R. Tumurru, P. Cao, S.A. Thompson, and M.J. Blaser. 1994. Divergence of genetic sequences for the vacuolating cytotoxin among Helicobacter pylori strains. J. Biol. Chem. 269:10566-10573.
22. Namavar, F., M. Sparrius, E.C. Veerman, B.J. Appelmek, and C.M. Vandenbroucke-Grauls. 1998. Neutrophil-activating protein mediates adhesion of Helicobacter pylori to sulfated carbohydrates on high-molecular-weight salivary mucin. Infect. Immun. 66:444-447.
23. Phadnis, S.H., M.H. Parlow, M. Levy, D. Ilver, C.M. Caulkins, J.B. Connors, and B.E. Dunn. 1996. Surface localization of Helicobacter pylori urease and a heat shock protein homolog requires bacterial autolysis. Infect. Immun. 64:905-912.
24. Teneberg, S., H. Miller-Podraza, H.C. Lampert, D.J. Evans, D.G. Evans, D. Danielson, and K.A. Karlsson. 1997. Carbohydrate binding specificity of the neutrophil-activating protein of Helicobacter pylori. J. Biol. Chem. 272:19067-19071.
25. Tonello, F., W.G. Dundon, B. Satin, M. Molinari, G. Tognon, G. Grandi, G. Del Giudice, R. Rappuoli, and C. Montecucco. 1999. The Helicobacter pylori neutrophil-activating protein is an iron-binding protein with dodecameric structure. Mol. Microbiol. 34:238-246.
26. Marchetti, M., M. Rossi, V. Giannelli, M.M. Giuliani, M. Pizza, S. Censini, A. Covacci, P. Massari, C. Pagliaccia, R. Manetti, et al. 1998. Protection against Helicobacter pylori infection in mice by intragastric vaccination with H. pylori antigens is achieved using a non-toxic mutant of E. coli heat-labile enterotoxin (LT) as adjuvant. Vaccine. 16:33-37.
27. Rossi, G., M. Rossi, C.G. Vitali, D. Fortuna, D. Burroni, L. Pancotto, S. Capecchi, S. Sozzi, G. Renzoni, G. Braca, et al. 1999. A conventional beagle dog model for acute and chronic infection with Helicobacter pylori. Infect. Immun. 67: 3112-3120.
28. Giuliani, M.M., G. Del Giudice, V. Giannelli, G. Dougan, G. Douce, R. Rappuoli, and M. Pizza. 1998. Mucosal adjuvanticity and immunogenicity of LTR72, a novel mutant of Escherichia coli heat-labile enterotoxin with partial knockout of ADP-ribosyltransferase activity. J. Exp. Med. 187:1123-1132.
29. Tamura, M., K. Nogimori, S. Murai, M. Yajima, K. Ito, T. Katada, M. Ui, and S. Ishii. 1982. Subunit structure of islet-activating protein, pertussis toxin, in conformity with the A-B model. Biochemistry. 22:5516-5522.
30. Xiang, Z., M. Bugnoli, A. Ponzetto, A. Morgando, N. Figura, A. Covacci, R. Petracca, C. Pennatini, S. Censini, D. Armellini, and R. Rappuoli. 1993. Detection in an enzyme immunoassay of an immune response to a recombinant fragment of the 128 kilodalton protein (CagA) of Helicobacter pylori. Eur. J. Clin. Microbiol Infect. Dis. 12:739-745.
31. Constantin, G., C. Laudanna, P. Baron, and G. Berton. 1994. Sulfatides trigger cytokine gene expression and secretion in human monocytes. FEBS Lett. 350:66-70.
32. 1, and arachidonic acid release. J. Immunol. 142: 1652-1660.
33. Laudanna, C., D. Mochly-Rosen, T. Liron, G. Constantin, and E.C. Butcher. 1998. Evidence of ζ protein kinase C involvement in polymorphonuclear neutrophil integrin-dependent adhesion and chemotaxis. J. Biol. Chem. 273:30306-30315.
34. Valletta, E. A., and G. Berton. 1987. Desensitization of macrophage oxygen metabolism on immobilized ligands: different effect of immunoglobulin G and complement. J. Immunol. 138:4366-4373.
35. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440-3450.
36. phox. Biochem. J. 314:409-412.
37. Covacci, A., J.L. Telford, G. Del Giudice, J. Parsonnet, and R. Rappuoli. 1999. Helicobacter pylori virulence and genetic geography. Science. 284:1328-1333.
38. Suerbaum, S., and C. Josenhans. 1999. Virulence factors of Helicobacter pylori implications for vaccine development. Mol. Med. Today. 5:32-39.
39. Ghiara, P., M. Rossi, M. Marchetti, A. Di Tommaso, C. Vindigni, F. Ciampolini, A. Covacci, J.L. Telford, M.T. De Magistris, M. Pizza, et al. 1997. Therapeutic intragastric vaccination against Helicobacter pylori in mice eradicates an otherwise chronic infection and confers protection against reinfection. Infect. Immun. 65:4996-5002.
40. Michetti, P., C. Kreiss, K.L. Kotloff, N. Porta, J.L. Blanco, D. Bachmann, M. Herranz, P.F. Saldinger, I. Corthesy-Theulaz, G. Losonsky, et al. 1999. Oral immunization with urease and Escherichia coli heat-labile enterotoxin is safe and immunogenic in Helicobacter pylori-infected adults. Gastroenterology. 116:804-812.
41. Hughes, B.J., J.C. Hollers, E. Crockett-Torabi, and C.W. Smith. 1992. Recruitment of CD11b/CD18 to the neutrophil surface and adherence-dependent cell locomotion. J. Clin. Invest. 90:1687-1696.
42. Miller, L.J., D.F. Bainton, N. Borregaard, and T.A. Springer. 1987. Stimulated mobilization of monocyte Mac-1 and p150,95 adhesion proteins from an intracellular vesicular compartment to the cell surface. J. Clin. Invest. 80:535-544.
43. Borregaard, N., L.J. Miller, and T.A. Springer. 1987. Chemoattractant-regulated mobilization of a novel intracellular compartment in human neutrophils. Science. 237:1204-1206.
44. Joyce, E., R.S. Lehmeyer, and R.B. Johnston, Jr. 1979. Stimulation of neutrophil oxidative metabolism by chemotactic peptides: influence of calcium ion concentration and cytochalasin B and comparison with stimulation by phorbol myristate acetate. Blood. 54:35-45.
45. Nathan, C.F., H.W. Murray, M.E. Wiebe, and B.Y. Rubin. 1983. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158:670-689.
46. Shalaby, M.R., B.B. Aggarval, E. Rinderknecht, L.P. Svedersky, B.S. Finkle, and M.A. Palladino, Jr. 1985. Activation of human polymorphonuclear neutrophil functions by interferon-gamma and tumor necrosis factor. J. Immunol. 135: 2069-2073.
47. Klebanhoff, S.F., M.A. Vadas, J.M. Harlan, L.H. Sparks, J.R. Gamble, J.M. Agosti, and A.M. Waltersdorph. 1986. Stimulation of neutrophils by tumor necrosis factor. J. Immunol. 136:4220-4225.
48. Berkow, R.L., D. Wang, J.W. Larrick, R.W. Dodson, and T.H. Howard. 1987. Enhancement of neutrophil superoxide production by preincubation with recombinant human tumor necrosis factor. J. Immunol. 139:3783-3791.
49. --forming NADPH oxidase of the phagocytes: nature, mechanisms of activation and function. Biochim. Biophys. Acta. 853:65-89.
50. Chanock, S. J., J.E. Benna, M.R. Smith, and B.M. Babior. 1994. The respiratory burst oxidase. J. Biol. Chem. 269: 24519-24522.
51. Thelen, M., B. Dewald, and M. Baggiolini. 1993. Neutrophil signal transduction and activation of the respiratory burst. Physiol. Rev. 73:797-821.
52. Segal, A.W. 1996. The NADPH oxidase and chronic granulomatous disease. Mol. Med. Today. 2:129-135.
53. O'Donnell, V., D.G. Tew, T.G. Jones, and P.J. England. 1993. Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem. J. 290:41-49.
54. Rappuoli, R., and M.G. Pizza. 1997. Pertussis toxin (Bordetella pertussis). In Guidebook to Protein Toxins and Their Use in Cell Biology. R. Rappuoli and C. Montecucco, editors. Oxford University Press, Oxford. 34-35.
55. Cockcroft, S., and G.M. Thomas. 1992. Inositol-lipid-specific phospholipase C isoenzymes and their differential regulation by receptors. Biochem. J. 288:1-14.
56. Exton, J.H. 1997. Regulation of phosphoinositide phospholipase by G-proteins. Adv. Exp. Med. Biol. 400:3-8.
57. Ui, M., T. Okada, K. Hazeki, and O. Hazeki. 1995. Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase. Trends Biochem. Sci. 20:303-307.
58. Arcaro, A., and M.P. Wymann. 1993. Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-triphosphate in neutrophil responses. Biochem. J. 296:297-301.
59. Hanke, J.H., J.P. Gardner, R.L. Dow, P.S. Changelian, W.H. Brissette, E.J. Weringer, B.A. Pollok, and P.A. Connelly. 1996. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271:695-701.
60. Krause, K.H., K.P. Campbell, M.J. Welsh, and D.P. Lew. 1990. The calcium signal and neutrophil activation. Clin. Biochem. 23:159-166.
61. Cover, T.L., Y. Glupczynski, A.P. Lage, A. Burette, M.K. Tummuru, G.I. Perez-Perez, and M.J. Blaser. 1995. Serologic detection of infection with cagA+ Helicobacter pylori strains. J. Clin. Microbiol. 33:1496-1500.
62. Parsonnet, J., M. Replogle, S. Yang, and R. Hiatt. 1997. Seroprevalence of CagA-positive strains among Helicobacter pylori-infected, healthy young adults. J. Infect. Dis. 175:1240-1242.
63. D'Elios, M.M., M. Manghetti, F. Almerigogna, A. Amedei, F. Costa, D. Burroni, C.T. Baldari, S. Romagnani, J.L. Telford, and G. Del Prete. 1997. Different cytokine profile and antigen-specificity repertoire in Helicobacter pylori-specific T cell clones from the antrum of chronic gastritis patients with or without peptic ulcer. Eur. J. Immunol. 27:1151-1157.
64. Ermak, T.H., P.J. Giannasca, R. Nichols, G.A. Myers, J. Nedrud, R. Weltzin, C.K. Lee, H. Kleanthous, and T.P. Monath. 1998. Immunization of mice with urease vaccine affords protection against Helicobacter pylori infection in the absence of antibodies and is mediated by MHC class II-restricted responses. J. Exp. Med. 188:2277-2288.
65. De Leo, F.R., and M.T. Quinn. 1996. Assembly of the phagocyte NADPH oxidase: molecular interaction of oxidase proteins. J. Leukoc. Biol. 60:677-691.
66. Winrow, W.R., P.G. Winyard, C.J. Morris, and D.R. Blake. 1993. Free radicals in inflammation: second messengers and mediators of tissue destruction. Br. Med. Bull. 49:506-522.
67. Suzuki, Y.J., H.J. Forman, and A. Sevanian. 1997. Oxidants as stimulators of signal transduction. Free Rad. Biol. Med. 22: 269-285.
68. Suzuki, M., S. Miura, M. Suematsu, D. Fukumura, I. Kurose, H. Suzuki, A. Kai, Y. Kudoh, M. Ohashi, and M. Tsuchiya. 1992. Helicobacter pylori-associated ammonia production enhances neutrophil-dependent gastric mucosal cell injury. Am. J. Physiol. 263:G719-G725.
69. Mobley, H.L. 1996. The role of Helicobacter pylori urease in the pathogenesis of gastritis and peptic ulceration. Aliment. Pharmacol. Ther. 10:57-64.