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Molecular Pathogenesis and Signal Transduction by Helicobacter pylori pp 1–26Cite as

The Human Stomach in Health and Disease: Infection Strategies by Helicobacter pylori

Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY,volume 400)

Abstract

Helicobacter pylori is a bacterial pathogen which commonly colonizes the human gastric mucosa from early childhood and persists throughout life. In the vast majority of cases, the infection is asymptomatic. H. pylori is the leading cause of peptic ulcer disease and gastric cancer, however, and these outcomes occur in 10–15% of those infected. Gastric adenocarcinoma is the third most common cause of cancer-associated death, and peptic ulcer disease is a significant cause of morbidity. Disease risk is related to the interplay of numerous bacterial host and environmental factors, many of which influence chronic inflammation and damage to the gastric mucosa. This chapter summarizes what is known about health and disease in H. pylori infection, and highlights the need for additional research in this area.

Keywords

  • Helicobacter pylori
  • Inflammation
  • Mucosal immunity
  • Peptic ulcer disease
  • Gastric cancer

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References

  • Ai TL, Solomon BD, Hsieh CS (2014) T-cell selection and intestinal homeostasis. Immunol Rev 259(1):60–74. doi:10.1111/imr.12171

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Aihara E, Closson C, Matthis AL, Schumacher MA, Engevik AC, Zavros Y, Ottemann KM, Montrose MH (2014) Motility and chemotaxis mediate the preferential colonization of gastric injury sites by Helicobacter pylori. PLoS Pathog 10(7):e1004275. doi:10.1371/journal.ppat.1004275

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Akada JK, Aoki H, Torigoe Y, Kitagawa T, Kurazono H, Hoshida H, Nishikawa J, Terai S, Matsuzaki M, Hirayama T, Nakazawa T, Akada R, Nakamura K (2010) Helicobacter pylori CagA inhibits endocytosis of cytotoxin VacA in host cells. Disease models & mechanisms 3(9–10):605–617. doi:10.1242/dmm.004879

  • Amieva M, Peek RM Jr (2016) Pathobiology of Helicobacter pylori-induced gastric cancer. Gastroenterology 150(1):64–78. doi:10.1053/j.gastro.2015.09.004

  • Amieva MR, Vogelmann R, Covacci A, Tompkins LS, Nelson WJ, Falkow S (2003) Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300(5624):1430–1434

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Amilon KR, Letley DP, Winter JA, Robinson K, Atherton JC (2015) Expression of the Helicobacter pylori virulence factor vacuolating cytotoxin A (vacA) is influenced by a potential stem-loop structure in the 5′ untranslated region of the transcript. Mol Microbiol 98(5):831–846. doi:10.1111/mmi.13160

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderl F, Gerhard M (2014) Helicobacter pylori vaccination: is there a path to protection? World J Gastroenterology : WJG 20(34):11939–11949. doi:10.3748/wjg.v20.i34.11939

  • Argent RH, Thomas RJ, Letley DP, Rittig MG, Hardie KR, Atherton JC (2008) Functional association between the Helicobacter pylori virulence factors VacA and CagA. J Med Microbiol 57(Pt 2):145–150. doi:10.1099/jmm.0.47465-0

    CrossRef  CAS  PubMed  Google Scholar 

  • Asahi M, Tanaka Y, Izumi T, Ito Y, Naiki H, Kersulyte D, Tsujikawa K, Saito M, Sada K, Yanagi S, Fujikawa A, Noda M, Itokawa Y (2003) Helicobacter pylori CagA containing ITAM-like sequences localized to lipid rafts negatively regulates VacA-induced signaling in vivo. Helicobacter 8(1):1–14

    Google Scholar 

  • Atherton JC (2006) The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Ann Rev Pathol 1:63–96. doi:10.1146/annurev.pathol.1.110304.100125

    CrossRef  CAS  Google Scholar 

  • Atherton JC, Blaser MJ (2009) Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest 119(9):2475–2487. doi:10.1172/JCI38605

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Atherton JC, Cao P, Peek RM Jr, Tummuru MK, Blaser MJ, Cover TL (1995) Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem 270(30):17771–17777

    CrossRef  CAS  PubMed  Google Scholar 

  • Backert S, Tegtmeyer N, Selbach M (2010) The versatility of Helicobacter pylori CagA effector protein functions: the master key hypothesis. Helicobacter 15(3):163–176. doi:10.1111/j.1523-5378.2010.00759.x

    CrossRef  CAS  PubMed  Google Scholar 

  • Baron JH, Sonnenberg A (2001) Period- and cohort-age contours of deaths from gastric and duodenal ulcer in New York 1804–1998. Am J Gastroenterol 96(10):2887–2891. doi:10.1111/j.1572-0241.2001.04243.x

    CAS  PubMed  Google Scholar 

  • Bauer B, Pang E, Holland C, Kessler M, Bartfeld S, Meyer TF (2012) The Helicobacter pylori virulence effector CagA abrogates human beta-defensin 3 expression via inactivation of EGFR signaling. Cell Host Microbe 11(6):576–586. doi:10.1016/j.chom.2012.04.013

    CrossRef  CAS  PubMed  Google Scholar 

  • Bimczok D, Kao JY, Zhang M, Cochrun S, Mannon P, Peter S, Wilcox CM, Monkemuller KE, Harris PR, Grams JM, Stahl RD, Smith PD, Smythies LE (2015) Human gastric epithelial cells contribute to gastric immune regulation by providing retinoic acid to dendritic cells. Mucosal Immunol. doi:10.1038/mi.2014.86

    PubMed  Google Scholar 

  • Blanchard TG, Nedrud JG (2010) Helicobacter pylori vaccines. In: Sutton P, Mitchell H (eds) Helicobacter pylori in the 21st century. CAB International, Cambridge, pp 167–189

    CrossRef  Google Scholar 

  • Blaser MJ, Nomura A, Lee J, Stemmerman GN, Perez-Perez GI (2007) Early-life family structure and microbially induced cancer risk. PLoS Med 4(1):e7. doi:10.1371/journal.pmed.0040007

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Boncristiano M, Paccani SR, Barone S, Ulivieri C, Patrussi L, Ilver D, Amedei A, D’Elios MM, Telford JL, Baldari CT (2003) The Helicobacter pylori vacuolating toxin inhibits T cell activation by two independent mechanisms. J Exp Med 198(12):1887–1897

    Google Scholar 

  • Breckan RK, Paulssen EJ, Asfeldt AM, Kvamme JM, Straume B, Florholmen J (2016) The all-age prevalence of Helicobacter pylori infection and potential transmission routes. A population-based study. Helicobacter 21(6):586–595. doi:10.1111/hel.12316

  • Celli JP, Turner BS, Afdhal NH, Keates S, Ghiran I, Kelly CP, Ewoldt RH, McKinley GH, So P, Erramilli S, Bansil R (2009) Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proc Natl Acad Sci U S A 106(34):14321–14326. doi:10.1073/pnas.0903438106

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Gong TT, Wu QJ (2016) Parity and gastric cancer risk: a systematic review and dose-response meta-analysis of prospective cohort studies. Sci Rep 6:18766. doi:10.1038/srep18766

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Colquhoun A, Arnold M, Ferlay J, Goodman KJ, Forman D, Soerjomataram I (2015) Global patterns of cardia and non-cardia gastric cancer incidence in 2012. Gut 64(12):1881–1888. doi:10.1136/gutjnl-2014-308915

  • Cook KW, Letley DP, Ingram RJ, Staples E, Skjoldmose H, Atherton JC, Robinson K (2014) CCL20/CCR6-mediated migration of regulatory T cells to the Helicobacter pylori-infected human gastric mucosa. Gut 63(10):1550–1559. doi:10.1136/gutjnl-2013-306253

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • de Bernard M, D’Elios MM (2010) The immune modulating activity of the Helicobacter pylori HP-NAP: friend or foe? Toxicon (Official Journal of the International Society on Toxinology) 56(7):1186–1192. doi:10.1016/j.toxicon.2009.09.020

    CrossRef  CAS  Google Scholar 

  • den Hoed CM, Kuipers EJ (2016) Gastric cancer: how can we reduce the incidence of this disease? Curr Gastroenterol Rep 18(7):34. doi:10.1007/s11894-016-0506-0

    CrossRef  Google Scholar 

  • Du MQ, Atherton JC (2006) Molecular subtyping of gastric MALT lymphomas: implications for prognosis and management. Gut 55(6):886–893

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Omar EM, Ng MT, Hold GL (2008) Polymorphisms in toll-like receptor genes and risk of cancer. Oncogene 27(2):244–252

    CrossRef  CAS  PubMed  Google Scholar 

  • Fang X, Wei J, He X, An P, Wang H, Jiang L, Shao D, Liang H, Li Y, Wang F, Min J (2015) Landscape of dietary factors associated with risk of gastric cancer: a systematic review and dose-response meta-analysis of prospective cohort studies. Eur J Cancer 51(18):2820–2832. doi:10.1016/j.ejca.2015.09.010

    CrossRef  PubMed  Google Scholar 

  • Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136(5):E359–E386. doi:10.1002/ijc.29210

    CrossRef  CAS  PubMed  Google Scholar 

  • Fischbach W (2014) Gastric MALT lymphoma—update on diagnosis and treatment. Best Pract Res Clin Gastroenterol 28(6):1069–1077. doi:10.1016/j.bpg.2014.09.006

    CrossRef  PubMed  Google Scholar 

  • Foegeding NJ, Caston RR, McClain MS, Ohi MD, Cover TL (2016) An overview of Helicobacter pylori VacA toxin biology. Toxins 8(6). doi:10.3390/toxins8060173

  • Ford AC, Gurusamy KS, Delaney B, Forman D, Moayyedi P (2016) Eradication therapy for peptic ulcer disease in Helicobacter pylori-positive people. Cochrane Database Syst Rev 4:CD003840. doi:10.1002/14651858.CD003840.pub5

  • Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB, Neish AS, Collier-Hyams L, Perez-Perez GI, Hatakeyama M, Whitehead R, Gaus K, O’Brien DP, Romero-Gallo J, Peek RM Jr (2005) Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci U S A 102(30):10646–10651. doi:10.1073/pnas.0504927102 0504927102 [pii]

  • Fujikawa A, Shirasaka D, Yamamoto S, Ota H, Yahiro K, Fukada M, Shintani T, Wada A, Aoyama N, Hirayama T, Fukamachi H, Noda M (2003) Mice deficient in protein tyrosine phosphatase receptor type Z are resistant to gastric ulcer induction by VacA of Helicobacter pylori. Nature Genetics 33(3):375–381. doi:10.1038/ng1112

  • Garhart CA, Redline RW, Nedrud JG, Czinn SJ (2002) Clearance of Helicobacter pylori infection and resolution of postimmunization gastritis in a kinetic study of prophylactically immunized mice. Infect Immun 70(7):3529–3538

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Gebert B, Fischer W, Weiss E, Hoffmann R, Haas R (2003) Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301(5636):1099–1102

    CrossRef  CAS  PubMed  Google Scholar 

  • Genta RM, Hamner HW, Graham DY (1993) Gastric lymphoid follicles in Helicobacter pylori infection: frequency, distribution, and response to triple therapy. Hum Pathol 24(6):577–583

    CrossRef  CAS  PubMed  Google Scholar 

  • Global Burden of Disease Cancer C, Fitzmaurice C, Dicker D, Pain A, Hamavid H, Moradi-Lakeh M, MacIntyre MF, Allen C, Hansen G, Woodbrook R, Wolfe C, Hamadeh RR, Moore A, Werdecker A, Gessner BD, Te Ao B, McMahon B, Karimkhani C, Yu C, Cooke GS, Schwebel DC, Carpenter DO, Pereira DM, Nash D, Kazi DS, De Leo D, Plass D, Ukwaja KN, Thurston GD, Yun Jin K, Simard EP, Mills E, Park EK, Catala-Lopez F, deVeber G, Gotay C, Khan G, Hosgood HD III, Santos IS, Leasher JL, Singh J, Leigh J, Jonas JB, Sanabria J, Beardsley J, Jacobsen KH, Takahashi K, Franklin RC, Ronfani L, Montico M, Naldi L, Tonelli M, Geleijnse J, Petzold M, Shrime MG, Younis M, Yonemoto N, Breitborde N, Yip P, Pourmalek F, Lotufo PA, Esteghamati A, Hankey GJ, Ali R, Lunevicius R, Malekzadeh R, Dellavalle R, Weintraub R, Lucas R, Hay R, Rojas-Rueda D, Westerman R, Sepanlou SG, Nolte S, Patten S, Weichenthal S, Abera SF, Fereshtehnejad SM, Shiue I, Driscoll T, Vasankari T, Alsharif U, Rahimi-Movaghar V, Vlassov VV, Marcenes WS, Mekonnen W, Melaku YA, Yano Y, Artaman A, Campos I, MacLachlan J, Mueller U, Kim D, Trillini M, Eshrati B, Williams HC, Shibuya K, Dandona R, Murthy K, Cowie B, Amare AT, Antonio CA, Castaneda-Orjuela C, van Gool CH, Violante F, Oh IH, Deribe K, Soreide K, Knibbs L, Kereselidze M, Green M, Cardenas R, Roy N, Tillmann T, Li Y, Krueger H, Monasta L, Dey S, Sheikhbahaei S, Hafezi-Nejad N, Kumar GA, Sreeramareddy CT, Dandona L, Wang H, Vollset SE, Mokdad A, Salomon JA, Lozano R, Vos T, Forouzanfar M, Lopez A, Murray C, Naghavi M (2015) The global burden of cancer 2013. JAMA Oncol 1(4):505–527. doi:10.1001/jamaoncol.2015.0735

  • Gobert AP, McGee DJ, Akhtar M, Mendz GL, Newton JC, Cheng Y, Mobley HL, Wilson KT (2001) Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc Natl Acad Sci U S A 98(24):13844–13849

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Goncalves RB, Coletta RD, Silverio KG, Benevides L, Casati MZ, da Silva JS, Nociti FH Jr (2011) Impact of smoking on inflammation: overview of molecular mechanisms. Inflamm Res (Official Journal of the European Histamine Research Society [et al]) 60(5):409–424. doi:10.1007/s00011-011-0308-7

    CAS  Google Scholar 

  • Gorrell RJ, Guan J, Xin Y, Tafreshi MA, Hutton ML, McGuckin MA, Ferrero RL, Kwok T (2013) A novel NOD1- and CagA-independent pathway of interleukin-8 induction mediated by the Helicobacter pylori type IV secretion system. Cell Microbiol 15(4):554–570. doi:10.1111/cmi.12055

    CrossRef  CAS  PubMed  Google Scholar 

  • Graham DY, Opekun AR, Osato MS, El-Zimaity HM, Lee CK, Yamaoka Y, Qureshi WA, Cadoz M, Monath TP (2004) Challenge model for Helicobacter pylori infection in human volunteers. Gut 53(9):1235–1243. doi:10.1136/gut.2003.037499

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham DY, Lu H, Yamaoka Y (2009) African, Asian or Indian enigma, the East Asian Helicobacter pylori: facts or medical myths. J Dig Dis 10(2):77–84. doi:10.1111/j.1751-2980.2009.00368.x

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • He C, Yang Z, Lu N (2016) Imbalance of gastrointestinal microbiota in the pathogenesis of Helicobacter pylori-associated diseases. Helicobacter 21(5):337–348. doi:10.1111/hel.12297

    Google Scholar 

  • Herrero R, Park JY, Forman D (2014) The fight against gastric cancer—the IARC Working Group report. Best Pract Res Clin Gastroenterol 28(6):1107–1114. doi:10.1016/j.bpg.2014.10.003

    CrossRef  PubMed  Google Scholar 

  • Hitzler I, Kohler E, Engler DB, Yazgan AS, Muller A (2012) The role of Th cell subsets in the control of Helicobacter infections and in T cell-driven gastric immunopathology. Front Immunol 3:142. doi:10.3389/fimmu.2012.00142

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Hou J, Yu Z, Xiang R, Li C, Wang L, Chen S, Li Q, Chen M, Wang L (2014) Correlation between infiltration of FOXP3+ regulatory T cells and expression of B7-H1 in the tumor tissues of gastric cancer. Exp Mol Pathol 96(3):284–291. doi:10.1016/j.yexmp.2014.03.005

    CrossRef  CAS  PubMed  Google Scholar 

  • Huang JY, Sweeney EG, Sigal M, Zhang HC, Remington SJ, Cantrell MA, Kuo CJ, Guillemin K, Amieva MR (2015) Chemodetection and destruction of host urea allows Helicobacter pylori to locate the epithelium. Cell Host Microbe 18(2):147–156. doi:10.1016/j.chom.2015.07.002

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussein NR, Argent RH, Marx CK, Patel SR, Robinson K, Atherton JC (2010) Helicobacter pylori dupA is polymorphic, and its active form induces proinflammatory cytokine secretion by mononuclear cells. J Infect Dis 202(2):261–269. doi:10.1086/653587

    CrossRef  CAS  PubMed  Google Scholar 

  • Ikewaki J, Nishizono A, Goto T, Fujioka T, Mifune K (2000) Therapeutic oral vaccination induces mucosal immune response sufficient to eliminate long-term Helicobacter pylori infection. Microbiol Immunol 44(1):29–39

    CrossRef  CAS  PubMed  Google Scholar 

  • Ilver D, Arnqvist A, Ogren J, Frick IM, Kersulyte D, Incecik ET, Berg DE, Covacci A, Engstrand L, Boren T (1998) Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279(5349):373–377

    CrossRef  CAS  PubMed  Google Scholar 

  • Italiani P, Boraschi D (2014) From monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation. Front Immunol 5:514. doi:10.3389/fimmu.2014.00514

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Keilberg D, Ottemann KM (2016) How Helicobacter pylori senses, targets and interacts with the gastric epithelium. Environ Microbiol 18(3):791–806. doi:10.1111/1462-2920.13222

    CrossRef  PubMed  Google Scholar 

  • Kim IJ, Blanke SR (2012) Remodeling the host environment: modulation of the gastric epithelium by the Helicobacter pylori vacuolating toxin (VacA). Front Cell Infect Microbiol 2:37. doi:10.3389/fcimb.2012.00037

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim DJ, Park JH, Franchi L, Backert S, Núñez G (2013) The Cag pathogenicity island and interaction between TLR2/NOD2 and NLRP3 regulate IL-1β production in Helicobacter pylori infected dendritic cells. Eur J Immunol 43(10):2650–2658. doi:10.1002/eji.201243281

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Kodaman N, Pazos A, Schneider BG, Piazuelo MB, Mera R, Sobota RS, Sicinschi LA, Shaffer CL, Romero-Gallo J, de Sablet T, Harder RH, Bravo LE, Peek RM Jr, Wilson KT, Cover TL, Williams SM, Correa P (2014) Human and Helicobacter pylori coevolution shapes the risk of gastric disease. Proc Natl Acad Sci U S A 111(4):1455–1460. doi:10.1073/pnas.1318093111

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotloff KL, Sztein MB, Wasserman SS, Losonsky GA, DiLorenzo SC, Walker RI (2001) Safety and immunogenicity of oral inactivated whole-cell Helicobacter pylori vaccine with adjuvant among volunteers with or without subclinical infection. Infect Immun 69(6):3581–3590

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Krakowka S, Eaton KA, Rings DM, Morgan DR (1991) Gastritis induced by Helicobacter pylori in gnotobiotic piglets. Rev Infect Dis 13(Suppl 8):S681–S685

    CrossRef  PubMed  Google Scholar 

  • Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, Misselwitz R, Berger J, Sewald N, Konig W, Backert S (2007) Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449(7164):862–866. doi:10.1038/nature06187

    CrossRef  CAS  PubMed  Google Scholar 

  • Li LF, Chan RL, Lu L, Shen J, Zhang L, Wu WK, Wang L, Hu T, Li MX, Cho CH (2014) Cigarette smoking and gastrointestinal diseases: the causal relationship and underlying molecular mechanisms (review). Int J Mol Med 34(2):372–380. doi:10.3892/ijmm.2014.1786

    CAS  PubMed  Google Scholar 

  • Lind J, Backert S, Pfleiderer K, Berg DE, Yamaoka Y, Sticht H, Tegtmeyer N (2014) Systematic analysis of phosphotyrosine antibodies recognizing single phosphorylated EPIYA-motifs in CagA of Western-type Helicobacter pylori strains. PLoS ONE 9(5):e96488. doi:10.1371/journal.pone.0096488

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Lind J, Backert S, Hoffmann R, Eichler J, Yamaoka Y, Perez-Perez GI, Torres J, Sticht H, Tegtmeyer N (2016) Systematic analysis of phosphotyrosine antibodies recognizing single phosphorylated EPIYA-motifs in CagA of East Asian-type Helicobacter pylori strains. BMC Microbiol 16(1):201. doi:10.1186/s12866-016-0820-6

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Liu T, Peng L, Yu P, Zhao Y, Shi Y, Mao X, Chen W, Cheng P, Wang T, Chen N, Zhang J, Liu X, Li N, Guo G, Tong W, Zhuang Y, Zou Q (2012) Increased circulating Th22 and Th17 cells are associated with tumor progression and patient survival in human gastric cancer. J Clin Immunol 32(6):1332–1339. doi:10.1007/s10875-012-9718-8

    CrossRef  PubMed  CAS  Google Scholar 

  • Loh JT, Gaddy JA, Algood HM, Gaudieri S, Mallal S, Cover TL (2015) Helicobacter pylori adaptation in vivo in response to a high-salt diet. Infect Immun 83(12):4871–4883. doi:10.1128/IAI.00918-15

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu H, Hsu PI, Graham DY, Yamaoka Y (2005) Duodenal ulcer promoting gene of Helicobacter pylori. Gastroenterology 128(4):833–848

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu H, Wu JY, Beswick EJ, Ohno T, Odenbreit S, Haas R, Reyes VE, Kita M, Graham DY, Yamaoka Y (2007) Functional and intracellular signaling differences associated with the Helicobacter pylori AlpAB adhesin from Western and East Asian strains. J Biol Chem 282(9):6242–6254. doi:10.1074/jbc.M611178200

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Luther J, Owyang SY, Takeuchi T, Cole TS, Zhang M, Liu M, Erb-Downward J, Rubenstein JH, Chen CC, Pierzchala AV, Paul JA, Kao JY (2011) Helicobacter pylori DNA decreases pro-inflammatory cytokine production by dendritic cells and attenuates dextran sodium sulphate-induced colitis. Gut 60(11):1479–1486. doi:10.1136/gut.2010.220087

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Macarthur M, Hold GL, El-Omar EM (2004) Inflammation and cancer II. Role of chronic inflammation and cytokine gene polymorphisms in the pathogenesis of gastrointestinal malignancy. Am J Physiol Gastrointest Liver Physiol 286(4):G515–G520

    Google Scholar 

  • Mahdavi J, Sonden B, Hurtig M, Olfat FO, Forsberg L, Roche N, Angstrom J, Larsson T, Teneberg S, Karlsson KA, Altraja S, Wadstrom T, Kersulyte D, Berg DE, Dubois A, Petersson C, Magnusson KE, Norberg T, Lindh F, Lundskog BB, Arnqvist A, Hammarstrom L, Boren T (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297(5581):573–578. doi:10.1126/science.1069076

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Malfertheiner P (2011) The intriguing relationship of Helicobacter pylori infection and acid secretion in peptic ulcer disease and gastric cancer. Dig Dis 29(5):459–464. doi:10.1159/000332213

    CrossRef  CAS  PubMed  Google Scholar 

  • Malfertheiner P, Fry LC, Monkemuller K (2006) Can gastric cancer be prevented by Helicobacter pylori eradication? Best Pract Res Clin Gastroenterol 20(4):709–719. doi:10.1016/j.bpg.2006.04.005

    CrossRef  PubMed  Google Scholar 

  • 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, European Helicobacter Study G (2012) Management of Helicobacter pylori infection—the Maastricht IV/Florence consensus report. Gut 61(5):646–664. doi:10.1136/gutjnl-2012-302084

  • Marshall BJ, Warren JR (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1(8390):1311–1315

    CrossRef  CAS  PubMed  Google Scholar 

  • Michetti P, Kreiss C, Kotloff KL, Porta N, Blanco JL, Bachmann D, Herranz M, Saldinger PF, Corthesy-Theulaz I, Losonsky G, Nichols R, Simon J, Stolte M, Ackerman S, Monath TP, Blum AL (1999) Oral immunization with urease and Escherichia coli heat-labile enterotoxin is safe and immunogenic in Helicobacter pylori-infected adults. Gastroenterology 116(4):804–812

    CrossRef  CAS  PubMed  Google Scholar 

  • Mueller D, Tegtmeyer N, Brandt S, Yamaoka Y, De Poire E, Sgouras D, Wessler S, Torres J, Smolka A, Backert S (2012) c-Src and c-Abl kinases control hierarchic phosphorylation and function of the CagA effector protein in Western and East Asian Helicobacter pylori strains. J Clin Invest 122(4):1553–1566. doi:10.1172/jci61143

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Munari F, Fassan M, Capitani N, Codolo G, Vila-Caballer M, Pizzi M, Rugge M, Della Bella C, Troilo A, D’Elios S, Baldari CT, D’Elios MM, de Bernard M (2014) Cytokine BAFF released by Helicobacter pylori-infected macrophages triggers the Th17 response in human chronic gastritis. J Immunol 193(11):5584–5594. doi:10.4049/jimmunol.1302865

    CrossRef  CAS  PubMed  Google Scholar 

  • Na HK, Woo JH (2014) Helicobacter pylori induces hypermethylation of CpG islands through upregulation of DNA methyltransferase: possible involvement of reactive oxygen/nitrogen species. J Cancer Prevent 19(4):259–264. doi:10.15430/JCP.2014.19.4.259

    CrossRef  Google Scholar 

  • Nagy P, Johansson S, Molloy-Bland M (2016) Systematic review of time trends in the prevalence of Helicobacter pylori infection in China and the USA. Gut Pathog 8:8

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Nakayama M, Hisatsune J, Yamasaki E, Nishi Y, Wada A, Kurazono H, Sap J, Yahiro K, Moss J, Hirayama T (2006) Clustering of Helicobacter pylori VacA in lipid rafts, mediated by its receptor, receptor-like protein tyrosine phosphatase beta, is required for intoxication in AZ-521 Cells. Infection and Immunity 74 (12):6571–6580. doi:10.1128/IAI.00356-06

  • Odenbreit S, Kavermann H, Puls J, Haas R (2002) CagA tyrosine phosphorylation and interleukin-8 induction by Helicobacter pylori are independent from alpAB, HopZ and bab group outer membrane proteins. Int J Med Microbiol 292(3–4):257–266

    CrossRef  CAS  PubMed  Google Scholar 

  • Oertli M, Sundquist M, Hitzler I, Engler DB, Arnold IC, Reuter S, Maxeiner J, Hansson M, Taube C, Quiding-Jarbrink M, Muller A (2012) DC-derived IL-18 drives Treg differentiation, murine Helicobacter pylori-specific immune tolerance, and asthma protection. J Clin Invest 122(3):1082–1096. doi:10.1172/JCI61029 61029 [pii]

  • Oertli M, Noben M, Engler DB, Semper RP, Reuter S, Maxeiner J, Gerhard M, Taube C, Muller A (2013) Helicobacter pylori gamma-glutamyl transpeptidase and vacuolating cytotoxin promote gastric persistence and immune tolerance. Proc Natl Acad Sci U S A 110(8):3047–3052. doi:10.1073/pnas.1211248110

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Oldani A, Cormont M, Hofman V, Chiozzi V, Oregioni O, Canonici A, Sciullo A, Sommi P, Fabbri A, Ricci V, Boquet P (2009) Helicobacter pylori counteracts the apoptotic action of its VacA toxin by injecting the CagA protein into gastric epithelial cells. PLoS Pathogens 5(10):e1000603. doi:10.1371/journal.ppat.1000603

  • Ordonez-Mena JM, Schottker B, Mons U, Jenab M, Freisling H, Bueno-de-Mesquita B, O’Doherty MG, Scott A, Kee F, Stricker BH, Hofman A, de Keyser CE, Ruiter R, Soderberg S, Jousilahti P, Kuulasmaa K, Freedman ND, Wilsgaard T, de Groot LC, Kampman E, Hakansson N, Orsini N, Wolk A, Nilsson LM, Tjonneland A, Pajak A, Malyutina S, Kubinova R, Tamosiunas A, Bobak M, Katsoulis M, Orfanos P, Boffetta P, Trichopoulou A, Brenner H, Consortium on H, Ageing: Network of Cohorts in E, the United S (2016) Quantification of the smoking-associated cancer risk with rate advancement periods: meta-analysis of individual participant data from cohorts of the CHANCES consortium. BMC Med 14(1):62. doi:10.1186/s12916-016-0607-5

  • Patel SR, Smith K, Letley DP, Cook KW, Memon AA, Ingram RJ, Staples E, Backert S, Zaitoun AM, Atherton JC, Robinson K (2013) Helicobacter pylori downregulates expression of human beta-defensin 1 in the gastric mucosa in a type IV secretion-dependent fashion. Cell Microbiol 15(12):2080–2092. doi:10.1111/cmi.12174

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Pflock M, Kennard S, Delany I, Scarlato V, Beier D (2005) Acid-induced activation of the urease promoters is mediated directly by the ArsRS two-component system of Helicobacter pylori. Infect Immun 73(10):6437–6445. doi:10.1128/IAI.73.10.6437-6445.2005

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Pflock M, Finsterer N, Joseph B, Mollenkopf H, Meyer TF, Beier D (2006) Characterization of the ArsRS regulon of Helicobacter pylori, involved in acid adaptation. J Bacteriol 188(10):3449–3462. doi:10.1128/JB.188.10.3449-3462.2006

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Plummer M, Franceschi S, Vignat J, Forman D, de Martel C (2015) Global burden of gastric cancer attributable to Helicobacter pylori. Int J Cancer 136(2):487–490. doi:10.1002/ijc.28999

    CrossRef  CAS  PubMed  Google Scholar 

  • Quiding-Jarbrink M, Raghavan S, Sundquist M (2010) Enhanced M1 macrophage polarization in human Helicobacter pylori-associated atrophic gastritis and in vaccinated mice. PLoS ONE 5(11):e15018. doi:10.1371/journal.pone.0015018

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramarao N, Gray-Owen SD, Meyer TF (2000) Helicobacter pylori induces but survives the extracellular release of oxygen radicals from professional phagocytes using its catalase activity. Mol Microbiol 38(1):103–113

    CrossRef  CAS  PubMed  Google Scholar 

  • Ramis IB, Vianna JS, Goncalves CV, von Groll A, Dellagostin OA, da Silva PE (2015) Polymorphisms of the IL-6, IL-8 and IL-10 genes and the risk of gastric pathology in patients infected with Helicobacter pylori. J Microbiol Immunol Infect = Wei mian yu gan ran za zhi. doi:10.1016/j.jmii.2015.03.002

  • Rhead JL, Letley DP, Mohammadi M, Hussein N, Mohagheghi MA, Eshagh Hosseini M, Atherton JC (2007) A new Helicobacter pylori vacuolating cytotoxin determinant, the intermediate region, is associated with gastric cancer. Gastroenterology 133(3):926–936

    CrossRef  CAS  PubMed  Google Scholar 

  • Rizzuti D, Ang M, Sokollik C, Wu T, Abdullah M, Greenfield L, Fattouh R, Reardon C, Tang M, Diao J, Schindler C, Cattral M, Jones NL (2015) Helicobacter pylori inhibits dendritic cell maturation via interleukin-10-mediated activation of the signal transducer and activator of transcription 3 pathway. J Innate Immun 7(2):199–211. doi:10.1159/000368232

    CrossRef  CAS  PubMed  Google Scholar 

  • Robinson K (2015) Helicobacter pylori-mediated protection against extra-gastric immune and inflammatory disorders: the evidence and controversies. Diseases 3(2):34–55. doi:10.3390/diseases3020034

    CrossRef  Google Scholar 

  • Robinson K, Kenefeck R, Pidgeon EL, Shakib S, Patel S, Polson RJ, Zaitoun AM, Atherton JC (2008) Helicobacter pylori-induced peptic ulcer disease is associated with inadequate regulatory T cell responses. Gut 57(10):1375–1385

    CrossRef  CAS  PubMed  Google Scholar 

  • Rossez Y, Gosset P, Boneca IG, Magalhaes A, Ecobichon C, Reis CA, Cieniewski-Bernard C, Joncquel Chevalier Curt M, Leonard R, Maes E, Sperandio B, Slomianny C, Sansonetti PJ, Michalski JC, Robbe-Masselot C (2014) The lacdiNAc-specific adhesin LabA mediates adhesion of Helicobacter pylori to human gastric mucosa. J Infect Dis 210(8):1286–1295. doi:10.1093/infdis/jiu239

    CrossRef  CAS  PubMed  Google Scholar 

  • 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 (2004) Therapeutic vaccination against Helicobacter pylori in the beagle dog experimental model: safety, immunogenicity, and efficacy. Infect Immun 72(6):3252–3259

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Salama NR, Hartung ML, Muller A (2013) Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat Rev Microbiol 11(6):385–399. doi:10.1038/nrmicro3016

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Schreiber S, Bucker R, Groll C, Azevedo-Vethacke M, Garten D, Scheid P, Friedrich S, Gatermann S, Josenhans C, Suerbaum S (2005) Rapid loss of motility of Helicobacter pylori in the gastric lumen in vivo. Infect Immun 73(3):1584–1589. doi:10.1128/IAI.73.3.1584-1589.2005

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinnett CG, Letley DP, Narayanan GL, Patel SR, Hussein NR, Zaitoun AM, Robinson K, Atherton JC (2016) Helicobacter pylori vacA transcription is genetically-determined and stratifies the level of human gastric inflammation and atrophy. J Clin Pathol. doi:10.1136/jclinpath-2016-203641

  • Smyk DS, Koutsoumpas AL, Mytilinaiou MG, Rigopoulou EI, Sakkas LI, Bogdanos DP (2014) Helicobacter pylori and autoimmune disease: cause or bystander. World J Gastroenterol 20(3):613–629. doi:10.3748/wjg.v20.i3.613

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Solnick JV, Canfield DR, Hansen LM, Torabian SZ (2000) Immunization with recombinant Helicobacter pylori urease in specific-pathogen-free rhesus monkeys (Macaca mulatta). Infect Immun 68(5):2560–2565

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, Haruma K, Asaka M, Uemura N, Malfertheiner P, faculty members of Kyoto Global Consensus C (2015) Kyoto global consensus report on Helicobacter pylori gastritis. Gut 64(9):1353–1367. doi:10.1136/gutjnl-2015-309252

  • Sutton P, Danon SJ, Walker M, Thompson LJ, Wilson J, Kosaka T, Lee A (2001) Post-immunisation gastritis and Helicobacter infection in the mouse: a long term study. Gut 49(4):467–473

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Tabassam FH, Graham DY, Yamaoka Y (2008) OipA plays a role in Helicobacter pylori-induced focal adhesion kinase activation and cytoskeletal re-organization. Cell Microbiol 10(4):1008–1020. doi:10.1111/j.1462-5822.2007.01104.x

    CrossRef  CAS  PubMed  Google Scholar 

  • Tan S, Noto JM, Romero-Gallo J, Peek RM, Jr, Amieva MR (2011) Helicobacter pylori perturbs iron trafficking in the epithelium to grow on the cell surface. PLoS Pathogens 7(5):e1002050. doi:10.1371/journal.ppat.1002050

  • Tegtmeyer N, Wessler S, Backert S (2011) Role of the cag-pathogenicity island encoded type IV secretion system in Helicobacter pylori pathogenesis. FEBS J 278(8):1190–1202. doi:10.1111/j.1742-4658.2011.08035.x

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Terebiznik MR, Raju D, Vazquez CL, Torbricki K, Kulkarni R, Blanke SR, Yoshimori T, Colombo MI, Jones NL (2009) Effect of Helicobacter pylori’s vacuolating cytotoxin on the autophagy pathway in gastric epithelial cells. Autophagy 5(3):370–379

    CrossRef  CAS  PubMed  Google Scholar 

  • Tsutsumi R, Takahashi A, Azuma T, Higashi H, Hatakeyama M (2006) Focal adhesion kinase is a substrate and downstream effector of SHP-2 complexed with Helicobacter pylori CagA. Molecular and Cellular Biology 26(1):261–276. doi:10.1128/MCB.26.1.261-276.2006

  • Tummuru MK, Cover TL, Blaser MJ (1994) Mutation of the cytotoxin-associated cagA gene does not affect the vacuolating cytotoxin activity of Helicobacter pylori. Infect Immun 62(6):2609–2613

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ubukata H, Nagata H, Tabuchi T, Konishi S, Kasuga T, Tabuchi T (2011) Why is the coexistence of gastric cancer and duodenal ulcer rare? Examination of factors related to both gastric cancer and duodenal ulcer. Gastric Cancer (Official Journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association) 14(1):4–12. doi:10.1007/s10120-011-0005-9

    Google Scholar 

  • Vanaja SK, Rathinam VA, Fitzgerald KA (2015) Mechanisms of inflammasome activation: recent advances and novel insights. Trends Cell Biol 25(5):308–315. doi:10.1016/j.tcb.2014.12.009

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, Moran AP, Athman R, Memet S, Huerre MR, Coyle AJ, DiStefano PS, Sansonetti PJ, Labigne A, Bertin J, Philpott DJ, Ferrero RL (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5(11):1166–1174

    CrossRef  CAS  PubMed  Google Scholar 

  • Walduck A, Andersen LP, Raghavan S (2015) Inflammation, immunity, and vaccines for Helicobacter pylori infection. Helicobacter 20(Suppl 1):17–25. doi:10.1111/hel.12252

    CrossRef  PubMed  Google Scholar 

  • Weeks DL, Eskandari S, Scott DR, Sachs G (2000) A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287(5452):482–485

    CrossRef  CAS  PubMed  Google Scholar 

  • Wen Y, Feng J, Scott DR, Marcus EA, Sachs G (2007) The HP0165-HP0166 two-component system (ArsRS) regulates acid-induced expression of HP1186 alpha-carbonic anhydrase in Helicobacter pylori by activating the pH-dependent promoter. J Bacteriol 189(6):2426–2434. doi:10.1128/JB.01492-06

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • White JR, Winter JA, Robinson K (2015) Differential inflammatory response to Helicobacter pylori infection: etiology and clinical outcomes. J Inflamm Res 8:137–147. doi:10.2147/JIR.S64888

    PubMed  PubMed Central  Google Scholar 

  • Wu CY, Wu MS, Kuo KN, Wang CB, Chen YJ, Lin JT (2010) Effective reduction of gastric cancer risk with regular use of nonsteroidal anti-inflammatory drugs in Helicobacter pylori-infected patients. J Clin Oncol (Official Journal of the American Society of Clinical Oncology) 28(18):2952–2957. doi:10.1200/JCO.2009.26.0695

    CrossRef  CAS  Google Scholar 

  • Yamaoka Y, Graham DY (2014) Helicobacter pylori virulence and cancer pathogenesis. Future Oncol 10(8):1487–1500. doi:10.2217/fon.14.29

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaoka Y, Ojo O, Fujimoto S, Odenbreit S, Haas R, Gutierrez O, El-Zimaity HM, Reddy R, Arnqvist A, Graham DY (2006) Helicobacter pylori outer membrane proteins and gastroduodenal disease. Gut 55(6):775–781

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoyama K, Higashi H, Ishikawa S, Fujii Y, Kondo S, Kato H, Azuma T, Wada A, Hirayama T, Aburatani H, Hatakeyama M (2005) Functional antagonism between Helicobacter pylori CagA and vacuolating toxin VacA in control of the NFAT signaling pathway in gastric epithelial cells. Proceedings of the National Academy of Sciences of the United States of America 102(27):9661–9666. doi: 10.1073/pnas.0502529102

  • Yu J, Leung WK, Go MY, Chan MC, To KF, Ng EK, Chan FK, Ling TK, Chung SC, Sung JJ (2002) Relationship between Helicobacter pylori babA2 status with gastric epithelial cell turnover and premalignant gastric lesions. Gut 51(4):480–484

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Yun CH, Lundgren A, Azem J, Sjoling A, Holmgren J, Svennerholm AM, Lundin BS (2005) Natural killer cells and Helicobacter pylori infection: bacterial antigens and interleukin-12 act synergistically to induce gamma interferon production. Infect Immun 73(3):1482–1490

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng M, Mao XH, Li JX, Tong WD, Wang B, Zhang YJ, Guo G, Zhao ZJ, Li L, Wu DL, Lu DS, Tan ZM, Liang HY, Wu C, Li DH, Luo P, Zeng H, Zhang WJ, Zhang JY, Guo BT, Zhu FC, Zou QM (2015) Efficacy, safety, and immunogenicity of an oral recombinant Helicobacter pylori vaccine in children in China: a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 386(10002):1457–1464. doi:10.1016/S0140-6736(15)60310-5

    CrossRef  CAS  PubMed  Google Scholar 

  • Zhou Y, Toh ML, Zrioual S, Miossec P (2007) IL-17A versus IL-17F induced intracellular signal transduction pathways and modulation by IL-17RA and IL-17RC RNA interference in AGS gastric adenocarcinoma cells. Cytokine 38(3):157–164. doi:10.1016/j.cyto.2007.06.002

    CrossRef  CAS  PubMed  Google Scholar 

  • Zucca E, Bertoni F (2016) The spectrum of MALT lymphoma at different sites: biological and therapeutic relevance. Blood 127(17):2082–2092. doi:10.1182/blood-2015-12-624304

    CrossRef  CAS  PubMed  Google Scholar 

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Acknowledgements

Our research was supported by the National Institute for Health Research (NIHR), through the Biomedical Research Unit in Gastrointestinal and Liver Diseases at Nottingham University Hospitals NHS Trust and the University of Nottingham. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR, or the Department of Health.

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  1. NIHR Biomedical Research Unit in Gastrointestinal and Liver Diseases at Nottingham University Hospitals NHS Trust and the Nottingham Digestive Diseases Centre, Queen’s Medical Centre, University of Nottingham, Nottingham, NG7 2UH, UK

    Karen Robinson, Darren P. Letley & Kazuyo Kaneko

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  1. Division of Microbiology, Department of Biology, Friedrich Alexander University Erlangen/Nuremberg, Erlangen, Germany

    Nicole Tegtmeyer

  2. Divisioin of Microbiology, Department of Biology, Friedrich Alexander University Erlangen/Nuremberg, Erlangen, Germany

    Steffen Backert

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Robinson, K., Letley, D.P., Kaneko, K. (2017). The Human Stomach in Health and Disease: Infection Strategies by Helicobacter pylori . In: Tegtmeyer, N., Backert, S. (eds) Molecular Pathogenesis and Signal Transduction by Helicobacter pylori. Current Topics in Microbiology and Immunology, vol 400. Springer, Cham. https://doi.org/10.1007/978-3-319-50520-6_1

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