Helicobacter pylori neutrophil-activating protein: From molecular pathogenesis to clinical applications

World Journal of Gastroenterology

Volumn 20, Issue 18, 2014, Pages 5294-5301

  Fu, Hua Wen ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

Clinical application; Diagnosis; Drug development; Helicobacter pylori; Helicobacter pylori neutrophil activating protein; Immunomodulation; Immunotherapy; T helper cell type I II; Vaccine

Indexed keywords

CD18 ANTIGEN; GROWTH FACTOR; HELICOBACTER PYLORI NEUTROPHIL ACTIVATING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; RECOMBINANT HELICOBACTER PYLORI NEUTROPHIL ACTIVATING PROTEIN; RECOMBINANT PROTEIN; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL VACCINE; NEUTROPHIL-ACTIVATING PROTEIN A, HELICOBACTER PYLORI;

ARTICLE; BACTERIAL COLONIZATION; CELL INFILTRATION; DISEASE ASSOCIATION; DNA DAMAGE; ENZYME LINKED IMMUNOSORBENT ASSAY; HELICOBACTER INFECTION; HELPER CELL; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; INFLAMMATION; NONHUMAN; SIGNAL TRANSDUCTION; ANIMAL; AUTOCRINE EFFECT; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LEUKOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; NEUTROPHIL; PATHOGENICITY;

ANIMALS; AUTOCRINE COMMUNICATION; BACTERIAL PROTEINS; BACTERIAL VACCINES; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; NEUTROPHIL ACTIVATION; NEUTROPHILS; SIGNAL TRANSDUCTION;

EID: 84900442087     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i18.5294     Document Type: Article

References (69)

1. Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984; 1: 1311-1315 [PMID: 6145023 DOI: 10.1016/ S0140-6736(84)91816-6]
2. Brown LM. Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev 2000; 22: 283-297 [PMID: 11218379 DOI: 10.1093/oxfordjournals.epirev.a018040]
3. Go MF. Review article: natural history and epidemiology of Helicobacter pylori infection. Aliment Pharmacol Ther 2002; 16 Suppl 1: 3-15 [PMID: 11849122 DOI: 10.1046/j.1365-2036.2002.0160s1003.x]
4. Dunn BE, Cohen H, Blaser MJ. Helicobacter pylori. Clin Microbiol Rev 1997; 10: 720-741 [PMID: 9336670]
5. Montecucco C, Rappuoli R. Living dangerously: how Helicobacter pylori survives in the human stomach. Nat Rev Mol Cell Biol 2001; 2: 457-466 [PMID: 11389469 DOI: 10.1038/35073084]
6. Montecucco C, de Bernard M. Molecular and cellular mechanisms of action of the vacuolating cytotoxin (VacA) and neutrophil-activating protein (HP-NAP) virulence factors of Helicobacter pylori. Microbes Infect 2003; 5: 715-721 [PMID: 12814772 DOI: 10.1016/S1286-4579(03)00124-2]
7. Del Giudice G, Malfertheiner P, Rappuoli R. Development of vaccines against Helicobacter pylori. Expert Rev Vaccines 2009; 8: 1037-1049 [PMID: 19627186 DOI: 10.1586/erv.09.62]
8. Evans DJ, Evans DG, Takemura T, Nakano H, Lampert HC, Graham DY, Granger DN, Kvietys PR. Characterization of a Helicobacter pylori neutrophil-activating protein. Infect Immun 1995; 63: 2213-2220 [PMID: 7768601]
9. Blom K, Lundin BS, Bölin I, Svennerholm A. Flow cytometric analysis of the localization of Helicobacter pylori antigens during different growth phases. FEMS Immunol Med Microbiol 2001; 30: 173-179 [PMID: 11335135 DOI: 10.1111/ j.1574-695X.2001.tb01567.x]
10. Teneberg S, Miller-Podraza H, Lampert HC, Evans DJ, Evans DG, Danielsson D, Karlsson KA. Carbohydrate binding specificity of the neutrophil-activating protein of Helicobacter pylori. J Biol Chem 1997; 272: 19067-19071 [PMID: 9228091 DOI: 10.1074/jbc.272.30.19067]
11. Namavar F, Sparrius M, Veerman EC, Appelmelk BJ, Vandenbroucke-Grauls CM. Neutrophil-activating protein mediates adhesion of Helicobacter pylori to sulfated carbohydrates on high-molecular-weight salivary mucin. Infect Immun 1998; 66: 444-447 [PMID: 9453593]
12. Tonello F, Dundon WG, Satin B, Molinari M, Tognon G, Grandi G, Del Giudice G, Rappuoli R, Montecucco C. The Helicobacter pylori neutrophil-activating protein is an iron-binding protein with dodecameric structure. Mol Microbiol 1999; 34: 238-246 [PMID: 10564468 DOI: 10.1046/ j.1365-2958.1999.01584.x]
13. Zanotti G, Papinutto E, Dundon W, Battistutta R, Seveso M, Giudice G, Rappuoli R, Montecucco C. Structure of the neutrophil-activating protein from Helicobacter pylori. J Mol Biol 2002; 323: 125-130 [PMID: 12368104 DOI: 10.1016/ S0022-2836(02)00879-3]
14. Dundon WG, Nishioka H, Polenghi A, Papinutto E, Zanotti G, Montemurro P, Del GG, Rappuoli R, Montecucco C. The neutrophil-activating protein of Helicobacter pylori. Int J Med Microbiol 2002; 291: 545-550 [PMID: 11890556 DOI: 10.1078/1438-4221-00165]
15. Petersson C, Forsberg M, Aspholm M, Olfat FO, Forslund T, Borén T, Magnusson KE. Helicobacter pylori SabA adhesin evokes a strong inflammatory response in human neutrophils which is down-regulated by the neutrophil-activating protein. Med Microbiol Immunol 2006; 195: 195-206 [PMID: 16758245 DOI: 10.1007/s00430-006-0018-x]
16. Wang G, Hong Y, Olczak A, Maier SE, Maier RJ. Dual Roles of Helicobacter pylori NapA in inducing and combating oxidative stress. Infect Immun 2006; 74: 6839-6846 [PMID: 17030577 DOI: 10.1128/IAI.00991-06]
17. Ceci P, Mangiarotti L, Rivetti C, Chiancone E. The neutrophil-activating Dps protein of Helicobacter pylori, HPNAP, adopts a mechanism different from Escherichia coli Dps to bind and condense DNA. Nucleic Acids Res 2007; 35: 2247-2256 [PMID: 17371778 DOI: 10.1093/nar/gkm077]
18. Ceci P, Cellai S, Falvo E, Rivetti C, Rossi GL, Chiancone E. DNA condensation and self-aggregation of Escherichia coli Dps are coupled phenomena related to the properties of the N-terminus. Nucleic Acids Res 2004; 32: 5935-5944 [PMID: 15534364 DOI: 10.1093/nar/gkh915]
19. Kottakis F, Papadopoulos G, Pappa EV, Cordopatis P, Pentas S, Choli-Papadopoulou T. Helicobacter pylori neutrophil-activating protein activates neutrophils by its C-terminal region even without dodecamer formation, which is a prerequisite for DNA protection--novel approaches against Helicobacter pylori inflammation. FEBS J 2008; 275: 302-317 [PMID: 18076649 DOI: 10.1111/j.1742-4658.2007.06201.x]
20. Warren JR, Marshall BJ. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1983; 1: 1273-1275 [PMID: 6134060]
21. Fiocca R, Luinetti O, Villani L, Chiaravalli AM, Capella C, Solcia E. Epithelial cytotoxicity, immune responses, and inflammatory components of Helicobacter pylori gastritis. Scand J Gastroenterol Suppl 1994; 205: 11-21 [PMID: 7863237 DOI: 10.3109/00365529409091404]
22. Wang CA, Liu YC, Du SY, Lin CW, Fu HW. Helicobacter pylori neutrophil-activating protein promotes myeloperoxidase release from human neutrophils. Biochem Biophys Res Commun 2008; 377: 52-56 [PMID: 18823946 DOI: 10.1016/ j.bbrc.2008.09.072]
23. Satin B, Del Giudice G, Della Bianca V, Dusi S, Laudanna C, Tonello F, Kelleher D, Rappuoli R, Montecucco C, Rossi F. The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a protective antigen and a major virulence factor. J Exp Med 2000; 191: 1467-1476 [PMID: 10790422 DOI: 10.1084/jem.191.9.1467]
24. Polenghi A, Bossi F, Fischetti F, Durigutto P, Cabrelle A, Tamassia N, Cassatella MA, Montecucco C, Tedesco F, de Bernard M. The neutrophil-activating protein of Helicobacter pylori crosses endothelia to promote neutrophil adhesion in vivo. J Immunol 2007; 178: 1312-1320 [PMID: 17237377]
25. Brisslert M, Enarsson K, Lundin S, Karlsson A, Kusters JG, Svennerholm AM, Backert S, Quiding-Järbrink M. Helicobacter pylori induce neutrophil transendothelial migration: role of the bacterial HP-NAP. FEMS Microbiol Lett 2005; 249: 95-103 [PMID: 16000239 DOI: 10.1016/j.femsle.2005.06.008]
26. Cappon A, Babolin C, Segat D, Cancian L, Amedei A, Calzetti F, Cassatella MA, D'Elios MM, de Bernard M. Helicobacter pylori-derived neutrophil-activating protein increases the lifespan of monocytes and neutrophils. Cell Microbiol 2010; 12: 754-764 [PMID: 20070310 DOI: 10.1111/j.1462-5822.2010.01431. x]
27. Montemurro P, Barbuti G, Dundon WG, Del Giudice G, Rappuoli R, Colucci M, De Rinaldis P, Montecucco C, Semeraro N, Papini E. Helicobacter pylori neutrophil-activating protein stimulates tissue factor and plasminogen activator inhibitor-2 production by human blood mononuclear cells. J Infect Dis 2001; 183: 1055-1062 [PMID: 11237830 DOI: 10.1086/319280]
28. Amedei A, Cappon A, Codolo G, Cabrelle A, Polenghi A, Benagiano M, Tasca E, Azzurri A, D'Elios MM, Del Prete G, de Bernard M. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J Clin Invest 2006; 116: 1092-1101 [PMID: 16543949 DOI: 10.1172/ JCI27177]
29. Montemurro P, Nishioka H, Dundon WG, de Bernard M, Del Giudice G, Rappuoli R, Montecucco C. The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a potent stimulant of mast cells. Eur J Immunol 2002; 32: 671-676 [PMID: 11857341]
30. D'Elios M, Del Prete G. Th1/Th2 balance in human disease. Transplant Proc 1998; 30: 2373-2377 [PMID: 9723509 DOI: 10.1016/S0041-1345(98)00659-9]
31. D'Elios MM, Manghetti M, De Carli M, Costa F, Baldari CT, Burroni D, Telford JL, Romagnani S, Del Prete G. T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J Immunol 1997; 158: 962-967 [PMID: 8993017]
32. Bamford KB, Fan X, Crowe SE, Leary JF, Gourley WK, Luthra GK, Brooks EG, Graham DY, Reyes VE, Ernst PB. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 1998; 114: 482-492 [PMID: 9496938 DOI: 10.1016/ S0016-5085(98)70531-1]
33. D'Elios MM, Amedei A, Cappon A, Del Prete G, de Bernard M. The neutrophil-activating protein of Helicobacter pylori (HP-NAP) as an immune modulating agent. FEMS Immunol Med Microbiol 2007; 50: 157-164 [PMID: 17521355 DOI: 10.1111/j.1574-695X.2007.00258.x]
34. D'Elios MM, Montecucco C, de Bernard M. VacA and HPNAP, Ying and Yang of Helicobacter pylori-associated gastric inflammation. Clin Chim Acta 2007; 381: 32-38 [PMID: 17368441 DOI: 10.1016/j.cca.2007.02.026]
35. de Bernard M, D'Elios MM. The immune modulating activity of the Helicobacter pylori HP-NAP: Friend or foe? Toxicon 2010; 56: 1186-1192 [PMID: 19818802 DOI: 10.1016/ j.toxicon.2009.09.020]
36. Nishioka H, Baesso I, Semenzato G, Trentin L, Rappuoli R, Del Giudice G, Montecucco C. The neutrophil-activating protein of Helicobacter pylori (HP-NAP) activates the MAPK pathway in human neutrophils. Eur J Immunol 2003; 33: 840-849 [PMID: 12672049]
37. Del Prete G, Chiumiento L, Amedei A, Piazza M, D'Elios MM, Codolo G, de Bernard M, Masetti M, Bruschi F. Immunosuppression of TH2 responses in Trichinella spiralis infection by Helicobacter pylori neutrophil-activating protein. J Allergy Clin Immunol 2008; 122: 908-913. e5 [PMID: 18804852 DOI: 10.1016/j.jaci.2008.08.016]
38. Pellicano R, Franceschi F, Saracco G, Fagoonee S, Roccarina D, Gasbarrini A. Helicobacters and extragastric diseases. Helicobacter 2009; 14 Suppl 1: 58-68 [PMID: 19712170 DOI: 10.1111/j.1523-5378.2009.00699.x]
39. Long M, Luo J, Li Y, Zeng FY, Li M. Detection and evaluation of antibodies against neutrophil-activating protein of Helicobacter pylori in patients with gastric cancer. World J Gastroenterol 2009; 15: 2381-2388 [PMID: 19452583]
40. Codolo G, Bossi F, Durigutto P, Bella CD, Fischetti F, Amedei A, Tedesco F, D'Elios S, Cimmino M, Micheletti A, Cassatella MA, D'Elios MM, de Bernard M. Orchestration of inflammation and adaptive immunity in Borrelia burgdorferi-induced arthritis by neutrophil-activating protein A. Arthritis Rheum 2013; 65: 1232-1242 [PMID: 23371320 DOI: 10.1002/art.37875]
41. Yokota S, Toita N, Yamamoto S, Fujii N, Konno M. Positive relationship between a polymorphism in Helicobacter pylori neutrophil-activating protein a gene and iron-deficiency anemia. Helicobacter 2013; 18: 112-116 [PMID: 23067298 DOI: 10.1111/hel.12011]
42. Li W, Minohara M, Piao H, Matsushita T, Masaki K, Matsuoka T, Isobe N, Su JJ, Ohyagi Y, Kira J. Association of anti-Helicobacter pylori neutrophil-activating protein antibody response with anti-aquaporin-4 autoimmunity in Japanese patients with multiple sclerosis and neuromyelitis optica. Mult Scler 2009; 15: 1411-1421 [PMID: 19965522 DOI: 10.1177 /1352458509348961]
43. Shih KS, Lin CC, Hung HF, Yang YC, Wang CA, Jeng KC, Fu HW. One-step chromatographic purification of Helicobacter pylori neutrophil-activating protein expressed in Bacillus subtilis. PLoS One 2013; 8: e60786 [PMID: 23577158 DOI: 10.1371/journal.pone.0060786]
44. Grandi G, inventor; Chiron SRL, assignee. Enrichment process for H. pylori neutrophil activating protein (NAP) utilizing metal chelate chromatography. United States patent US 7038012 B1. 2006 May 2
45. Velin D, Michetti P. Advances in vaccination against Helicobacter pylori. Expert Rev Gastroenterol Hepatol 2010; 4: 157-166 [PMID: 20350263 DOI: 10.1586/egh.10.6]
46. D'Elios MM, Andersen LP. Inflammation, immunity, and vaccines for Helicobacter pylori. Helicobacter 2009; 14 Suppl 1: 21-28 [PMID: 19712164 DOI: 10.1111/j.1523-5378.2009.00698. x]
47. Vajdy M, Singh M, Ugozzoli M, Briones M, Soenawan E, Cuadra L, Kazzaz J, Ruggiero P, Peppoloni S, Norelli F, del Giudice G, O'Hagan D. Enhanced mucosal and systemic immune responses to Helicobacter pylori antigens through mucosal priming followed by systemic boosting immunizations. Immunology 2003; 110: 86-94 [PMID: 12941145]
48. Rossi G, Ruggiero P, Peppoloni S, Pancotto L, Fortuna D, Lauretti L, Volpini G, Mancianti S, Corazza M, Taccini E, Di Pisa F, Rappuoli R, Del Giudice G. Therapeutic vaccination against Helicobacter pylori in the beagle dog experimental model: safety, immunogenicity, and efficacy. Infect Immun 2004; 72: 3252-3259 [PMID: 15155627]
49. Malfertheiner P, Schultze V, Rosenkranz B, Kaufmann SH, Ulrichs T, Novicki D, Norelli F, Contorni M, Peppoloni S, Berti D, Tornese D, Ganju J, Palla E, Rappuoli R, Scharschmidt BF, Del Giudice G. Safety and immunogenicity of an intramuscular Helicobacter pylori vaccine in noninfected volunteers: a phase I study. Gastroenterology 2008; 135: 787-795 [PMID: 18619971 DOI: 10.1053/j.gastro.2008.05.054]
50. Sun B, Li ZS, Tu ZX, Xu GM, Du YQ. Construction of an oral recombinant DNA vaccine from H pylori neutrophil activating protein and its immunogenicity. World J Gastroenterol 2006; 12: 7042-7046 [PMID: 17109503]
51. Li JF, Peng Zh, Xiao HJ, Luo N, Yang ZF, Li JF, Xu WM. Expression of Helicobacter pylori napA gene in Lactococcus lactis and its immunogenicity analysis. Zhongguo Shengwu Gongcheng Zazhi 2008; 28: 77-83
52. Iankov ID, Haralambieva IH, Galanis E. Immunogenicity of attenuated measles virus engineered to express Helicobacter pylori neutrophil-activating protein. Vaccine 2011; 29: 1710-1720 [PMID: 21182995 DOI: 10.1016/j.vaccine.2010.12.020]
53. Iankov ID, Federspiel MJ, Galanis E. Measles virus expressed Helicobacter pylori neutrophil-activating protein significantly enhances the immunogenicity of poor immunogens. Vaccine 2013; 31: 4795-4801 [PMID: 23948230 DOI: 10.1016/j.vaccine.2013.07.085]
54. Mégraud F, Lehours P. Helicobacter pylori detection and antimicrobial susceptibility testing. Clin Microbiol Rev 2007; 20: 280-322 [PMID: 17428887]
55. Rahman SH, Azam MG, Rahman MA, Arfin MS, Alam MM, Bhuiyan TM, Ahmed N, Rahman M, Nahar S, Hassan MS. Non-invasive diagnosis of H pylori infection: evaluation of serological tests with and without current infection marker CIM. World J Gastroenterol 2008; 14: 1231-1236 [PMID: 18300349]
56. Wang XY, Yang Y, Shi RH, Ho B, Wang HD, Zhang GX. An evaluation of a serologic test with a current infection marker of Helicobacter pylori before and after eradication therapy in Chinese. Helicobacter 2008; 13: 49-55 [PMID: 18205666 DOI: 10.1111/j.1523-5378.2008.00578.x]
57. Tang RX, Luo DJ, Sun AH, Yan J. Diversity of Helicobacter pylori isolates in expression of antigens and induction of antibodies. World J Gastroenterol 2008; 14: 4816-4822 [PMID: 18720546]
58. Khoder G, Yamaoka Y, Fauchère JL, Burucoa C, Atanassov C. Proteomic Helicobacter pylori biomarkers discriminating between duodenal ulcer and gastric cancer. J Chromatogr B Analyt Technol Biomed Life Sci 2009; 877: 1193-1199 [PMID: 19328750 DOI: 10.1016/j.jchromb.2009.03.003]
59. Iankov ID, Penheiter AR, Carlson SK, Galanis E. Development of monoclonal antibody-based immunoassays for detection of Helicobacter pylori neutrophil-activating protein. J Immunol Methods 2012; 384: 1-9 [PMID: 22750540 DOI: 10.1016/j.jim.2012.06.010]
60. Malfertheiner P, Megraud F, O'Morain CA, Atherton J, Axon AT, Bazzoli F, Gensini GF, Gisbert JP, Graham DY, Rokkas T, El-Omar EM, Kuipers EJ. Management of Helicobacter pylori infection--the Maastricht IV/ Florence Consensus Report. Gut 2012; 61: 646-664 [PMID: 22491499 DOI: 10.1136/ gutjnl-2012-302084]
61. Malfertheiner P, Selgrad M. Helicobacter pylori infection and current clinical areas of contention. Curr Opin Gastroenterol 2010; 26: 618-623 [PMID: 20827182 DOI: 10.1097/ MOG.0b013e32833efede]
62. Tsang CN, Bianga J, Sun H, Szpunar J, Lobinski R. Probing of bismuth antiulcer drug targets in H. pylori by laser ablationinductively coupled plasma mass spectrometry. Metallomics 2012; 4: 277-283 [PMID: 22286050 DOI: 10.1039/c2mt00169a]
63. Choli-Papadopoulou T, Kottakis F, Papadopoulos G, Pendas S. Helicobacter pylori neutrophil activating protein as target for new drugs against H. pylori inflammation. World J Gastroenterol 2011; 17: 2585-2591 [PMID: 21677824 DOI: 10.3748/wjg.v17.i21.2585]
64. Kottakis F, Befani C, Asiminas A, Kontou M, Koliakos G, Choli-Papadopoulou T. The C-terminal region of HPNAP activates neutrophils and promotes their adhesion to endothelial cells. Helicobacter 2009; 14: 177-179 [PMID: 19702847 DOI: 10.1111/j.1523-5378.2009.00678.x]
65. Kottakis F, Kouzi-Koliakou K, Pendas S, Kountouras J, Choli-Papadopoulou T. Effects of mastic gum Pistacia lentiscus var. Chia on innate cellular immune effectors. Eur J Gastroenterol Hepatol 2009; 21: 143-149 [PMID: 19212203 DOI: 10.1097/MEG.0b013e32831c50c9]
66. Codolo G, Mazzi P, Amedei A, Del Prete G, Berton G, D'Elios MM, de Bernard M. The neutrophil-activating protein of Helicobacter pylori down-modulates Th2 inflammation in ovalbumin-induced allergic asthma. Cell Microbiol 2008; 10: 2355-2363 [PMID: 18671823 DOI: 10.1111/j.1462-5822.2008.01217.x]
67. Codolo G, Fassan M, Munari F, Volpe A, Bassi P, Rugge M, Pagano F, D'Elios MM, de Bernard M. HP-NAP inhibits the growth of bladder cancer in mice by activating a cytotoxic Th1 response. Cancer Immunol Immunother 2012; 61: 31-40 [PMID: 21833592 DOI: 10.1007/s00262-011-1087-2]
68. Iankov ID, Allen C, Federspiel MJ, Myers RM, Peng KW, Ingle JN, Russell SJ, Galanis E. Expression of immunomodulatory neutrophil-activating protein of Helicobacter pylori enhances the antitumor activity of oncolytic measles virus. Mol Ther 2012; 20: 1139-1147 [PMID: 22334023 DOI: 10.1038/ mt.2012.4]
69. Ramachandran M, Yu D, Wanders A, Essand M, Eriksson F. An infection-enhanced oncolytic adenovirus secreting H. pylori neutrophil-activating protein with therapeutic effects on neuroendocrine tumors. Mol Ther 2013; 21: 2008-2018 [PMID: 23817216 DOI: 10.1038/mt.2013.153]