How Helicobacter pylori infection controls gastric acid secretion

Journal of Gastroenterology

Volumn 47, Issue 6, 2012, Pages 609-618

  Smolka, Adam J ^a   Backert, Steffen ^b  

^a University Family Medicine   (United States)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

ADAM17; Cag pathogenicity island; EGFR; ERK1 2; Gastric adenocarcinoma; HB EGF; Helicobacter pylori; HK ATPase; Hypochlorhydria; Integrin 5 1; Parietal cells; Transcription factor NF jB; Type IV secretion system

Indexed keywords

A DISINTEGRIN AND A METALLOPROTEASE 17; ADAM PROTEIN; BACTERIAL PROTEIN; CAGA PROTEIN; CAGE PROTEIN; CAGL PROTEIN; CAGM PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; HOMODIMER; HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE; HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE ALPHA SUBUNIT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTON PUMP; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; VIRULENCE FACTOR;

ACHLORHYDRIA; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; CYTOTOXIN ASSOCIATED GENE PATHOGENICITY ISLAND; ENZYME ACTIVATION; ENZYME RELEASE; ENZYME REPRESSION; EXPERIMENTAL MODEL; GENE REPRESSION; HELICOBACTER INFECTION; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; INTRACELLULAR SIGNALING; MOLECULAR PATHOLOGY; NONHUMAN; PATHOGENICITY ISLAND; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; REVIEW; STOMACH ACID SECRETION; TRANSCRIPTION TERMINATION; TYPE IV SECRETION SYSTEM;

ACHLORHYDRIA; ANIMALS; DISEASE MODELS, ANIMAL; EVIDENCE-BASED MEDICINE; GASTRIC ACID; H(+)-K(+)-EXCHANGING ATPASE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; PROTON PUMPS; TRANSCRIPTION, GENETIC;

EID: 84865119876     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-012-0592-1     Document Type: Review

References (102)

1. Amieva MR, El-Omar EM. Host-bacterial interactions in Heli-cobacter pylori infection. Gastroenterology. 2008;134:306-23. (Pubitemid 350309334)
2. Atherton JC, Blaser MJ. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest. 2009;119(9):2475-87.
3. Polk DB, Peek RM. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer. 2010;10(6):403-14.
4. Linz B, et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature. 2007;445 (7130):915-8.
5. Dixon MF, et al. Classification and grading of gastritis. The updated Sydney System. International workshop on the histo-pathology of gastritis, Houston 1994. Am J Surg Pathol. 1996;20(10):1161-81.
6. Marshall BJ, et al. Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med J Aust. 1985;142(8):436-9. (Pubitemid 15233564)
7. Morris A, Nicholson G. Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH. Am J Gastroen-terol. 1987;82(3):192-9. (Pubitemid 17047002)
8. Graham DY, et al. Iatrogenic Campylobacter pylori infection is a cause of epidemic achlorhydria. Am J Gastroenterol. 1988;83(9):974-80.
9. Sobala GM, et al. Acute Helicobacter pylori infection: clinical features, local and systemic immune response, gastric mucosal histology, and gastric juice ascorbic acid concentrations. Gut. 1991;32(11):1415-8.
10. Ramsey EJ, et al. Epidemic gastritis with hypochlorhydria. Gastroenterology. 1979;76(6):1449-57. (Pubitemid 9183097)
11. El-Omar EM, et al. Helicobacter pylori infection and chronic gastric acid hyposecretion. Gastroenterology. 1997;113(1):15-24. (Pubitemid 27281753)
12. Harford WV, et al. Acute gastritis with hypochlorhydria: report of 35 cases with long term follow up. Gut. 2000;47(4):467-72.
13. Sonnenberg A, et al. Hypochlorhydrie bei akuter gastritis. Dtsch Med Wochenschr. 1979;104(51):1814-6. (Pubitemid 10172071)
14. Takashima M, et al. Effects of Helicobacter pylori infection on gastric acid secretion and serum gastrin levels in Mongolian gerbils. Gut. 2001;48(6):765-73. (Pubitemid 32476976)
15. Defize J, Goldie J, Hunt RH. Inhibition of acid production by Campylobacter pylori in isolated guinea pig parietal cells. Am J Gastroenterol. 1989;96:A114.
16. Cave DR, Vargas M. Effect of a Campylobacter pylori protein on acid secretion by parietal cells. Lancet. 1989;2(8656):187-9. (Pubitemid 19186998)
17. Hoffman JS, et al. Rabbit and ferret parietal cell inhibition by Helicobacter species. Dig Dis Sci. 1995;40(1):147-52.
18. Chen XG, et al. Ultrastructure of the gastric mucosa harboring Campylobacter-like organisms. Am J Clin Pathol. 1986;86(5): 575-82. (Pubitemid 17181357)
19. Bjorkholm B, et al. Helicobacter pylori entry into human gastric epithelial cells: A potential determinant of virulence, persistence, and treatment failures. Helicobacter. 2000;5(3):148-54.
20. Tagkalidis PP, et al. Selective colonization by Helicobacter pylori of the deep gastric glands and intracellular canaliculi of parietal cells in the setting of chronic proton pump inhibitor use. Eur J Gastroenterol Hepatol. 2002;14(4):453-6. (Pubitemid 34439050)
21. Tricottet V, et al. Campylobacter-like organisms and surface epithelium abnormalities in active, chronic gastritis in humans: an ultrastructural study. Ultrastruct Pathol. 1986;10(2):113-22. (Pubitemid 16037247)
22. Lee A, et al. Role of Helicobacter felis in chronic canine gastritis. Vet Pathol. 1992;29(6):487-94.
23. Fox JG, et al. Role of gastric pH in isolation of Helicobacter mustelae from the feces of ferrets. Gastroenterology. 1993;104(1):86-92. (Pubitemid 23040010)
24. Kobayashi H, et al. The effect of Helicobacter pylori on gastric acid secretion by isolated parietal cells from a guinea pig. Association with production of vacuolating toxin by H. pylori. Scand J Gastroenterol. 1996;31(5):428-33.
25. Jablonowski H, et al. Effects of Helicobacter pylori on hista-mine and carbachol stimulated acid secretion by human parietal cells. Gut. 1994;35(6):755-7. (Pubitemid 24193215)
26. Jablonowski H, et al. Effect of Helicobacter pylori on dibutyryl c-AMP-stimulated acid secretion by human parietal cells. Hep- atogastroenterology. 1994;41(6):546-8.
27. Furuta T, et al. H+/K+-adenosine triphosphatase mRNA in gastric fundic gland mucosa in patients infected with Helico-bacter pylori. Scand J Gastroenterol. 1999;34(4):384-90. (Pubitemid 29232373)
28. Plottel CS, Blaser MJ. Microbiome and malignancy. Cell Host Microbe. 2011;10(4):324-35.
29. Zavros Y, et al. Chronic gastritis in the hypochlorhydric gastrin-deficient mouse progresses to adenocarcinoma. Oncogene. 2005;24(14):2354-66. (Pubitemid 40546694)
30. Spicer Z, et al. Stomachs of mice lacking the gastric H,K-ATPase alpha-subunit have achlorhydria, abnormal parietal cells, and ciliated metaplasia. J Biol Chem. 2000;275(28): 21555-65. (Pubitemid 30481861)
31. Forte JG, et al. Pumps and pathways for gastric HCl secretion. Ann N Y Acad Sci. 1989;574:145-58. (Pubitemid 20122436)
32. Sachs G. The gastric proton pump: the H+,K-ATPase. In: Johnson LR, editor, Physiology of the gastrointestinal tract. New York: Raven; 1987. p. 865-881.
33. Black JA, Forte TM, Forte JG. Structure of oxyntic cell membranes during conditions of rest and secretion of HCl as revealed by freeze-fracture. Anat Rec. 1980;196(2):163-72. (Pubitemid 10155466)
34. Smolka A, Helander HF, Sachs G. Monoclonal antibodies against gastric H+ + K+ATPase. Am J Physiol. 1983;245: 589-96.
35. Soroka CJ, et al. Characterization of membrane and cytoskeletal compartments in cultured parietal cells: immunofluorescence and confocal microscopic examination. Eur J Cell Biol. 1993;60(1):76-87. (Pubitemid 23092665)
36. Roepke TK, et al. The KCNE2 potassium channel ancillary subunit is essential for gastric acid secretion. J Biol Chem. 2006;281(33):23740-7. (Pubitemid 44274149)
37. Song P, et al. KCNQ1 is the luminal K+ recycling channel during stimulation of gastric acid secretion. J Physiol. 2009;587(Pt 15):3955-65.
38. Song P, et al. Kir4.1 channel expression is essential for parietal cell control of acid secretion. J Biol Chem. 2011;286(16): 14120-8.
39. Del Valle J, Sugano K, Yamada T. Progastrin and its glycine-extended posttranslational processing intermediates in human gastrointestinal tissues. Gastroenterology. 1987;92(6):1908-12. (Pubitemid 17072240)
40. Beales I, et al. Effect of Helicobacter pylori products and recombinant cytokines on gastrin release from cultured canine G cells. Gastroenterology. 1997;113(2):465-71. (Pubitemid 27351772)
41. 2+i signaling systems. Am J Physiol. 1992;263(6 Pt 1):G967-72.
42. Seal A, et al. Somatostatin-14 and-28: clearance and potency on gastric function in dogs. Am J Physiol. 1982;243(2):G97-102. (Pubitemid 12053102)
43. Li P, Chang TM, Chey WY. Secretin inhibits gastric acid secretion via a vagal afferent pathway in rats. Am J Physiol Gastrointest Liver Physiol. 1998;275(1):G22-8.
44. Wallace JL, et al. Secretagogue-specific effects of interleukin-1 on gastric acid secretion. Am J Physiol. 1991;261(4 Pt 1):G559-64.
45. Gooz M, et al. Inhibition of human gastric H(+)-K(+)-ATPase alpha-subunit gene expression by Helicobacter pylori. Am J Physiol Gastrointest Liver Physiol. 2000;278(6):G981-91. (Pubitemid 30439178)
46. Mills JC, et al. A molecular profile of the mouse gastric parietal cell with and without exposure to Helicobacter pylori. Proc Natl Acad Sci USA. 2001;98(24):13687-92. (Pubitemid 33115959)
47. Saha A, et al. IL-1beta modulation of H,K-ATPase {alpha}-subunit gene transcription in Helicobacter pylori infection. Am J Physiol Gastrointest Liver Physiol. 2007;292(4):G1055-61. (Pubitemid 46557770)
48. Saha A, et al. Helicobacter pylori-induced H,K-ATPase {alpha}-subunit gene repression is mediated by NF-{kappa}B p50 homodimer promoter binding. Am J Physiol Gastrointest Liver Physiol. 2008;294(3):G795-807. (Pubitemid 351468758)
49. Saha A, et al. The role of Sp1 in IL-1beta and H. pylori-mediated regulation of H,K-ATPase gene transcription. Am J Physiol Gastrointest Liver Physiol. 2008;295(5):G977-86.
50. Saha A, et al. Helicobacter pylori represses proton pump expression and inhibits acid secretion in human gastric mucosa. Gut. 2010;59(7):874-81.
51. Saha A, et al. Helicobacter pylori CagL activates ADAM17 to induce repression of the gastric H,K-ATPase alpha subunit. Gastroenterology. 2010;139(1):239-48.
52. Campbell VW, Yamada T. Acid secretagogue-induced stimulation of gastric parietal cell gene expression. J Biol Chem. 1989;264(19):11381-6. (Pubitemid 19168874)
53. Campbell VW, Yamada T. Effect of omeprazole on gene expression in canine gastric parietal cells. Am J Physiol. 1991;260(3 Pt 1):G434-9.
54. Nishi T, et al. Transcriptional activation of H+/K+-ATPase genes by gastric GATA binding proteins. J Biochem (Tokyo). 1997;121(5):922-9. (Pubitemid 27236911)
55. Tamura S, et al. Gastric DNA-binding proteins recognize upstream sequence motifs of parietal cell-specific genes published erratum appears in Proc Natl Acad Sci USA 1994 May 10;91(10):4609. Proc Natl Acad Sci USA. 1993;90(22):10876-80. (Pubitemid 23347146)
56. Muraoka A, et al. Canine H(+)-K(+)-ATPase alpha-subunit gene promoter: studies with canine parietal cells in primary culture. Am J Physiol. 1996;271(6 Pt 1):G1104-13.
57. Kaise M, et al. Epidermal growth factor induces H+,K+-ATPase alpha-subunit gene expression through an element homologous to the 3 half-site of the c-fos serum response element. J Biol Chem. 1995;270(31):18637-42.
58. Dubois A, et al. Natural gastric infection with Helicobacter pylori in monkeys: A model for spiral bacteria infection in humans. Gastroenterology. 1994;106(6):1405-17. (Pubitemid 24163108)
59. Viala J, et al. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol. 2004;5(11):1166-74. (Pubitemid 39549631)
60. Backert S, Selbach M. Role of type IV secretion in Helicobacter pylori pathogenesis. Cell Microbiol. 2008;10(8):1573-81. (Pubitemid 352006141)
61. Backert S, Clyne M, Tegtmeyer N. Molecular mechanisms of gastric epithelial cell adhesion and injection of CagA by Heli-cobacter pylori. Cell Commun Signal. 2011;9(1):28.
62. Ruoslahti E. RGD and other recognition sequences for integrins. Ann Rev Cell Dev Biol. 1996;12:697-715. (Pubitemid 26422728)
63. Covacci A, Rappuoli R. Tyrosine-phosphorylated bacterial proteins: Trojan horses for the host cell. J Exp Med. 2000;191(4):587-92.
64. Kwok T, et al. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature. 2007;449(7164):862-6. (Pubitemid 47598611)
65. Kim H, Lim JW, Kim KH. Helicobacter pylori-induced expression of interleukin-8 and cyclooxygenase-2 in AGS gastric epithelial cells: mediation by nuclear factor-kappaB. Scand J Gastroenterol. 2001;36(7):706-16. (Pubitemid 32568548)
66. Schlondorff J, Blobel CP. Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J Cell Sci. 1999;112(Pt 21):3603-17.
67. Bridges LC, Bowditch RD. ADAM-integrin interactions: potential integrin regulated ectodomain shedding activity. Curr Pharm Des. 2005;11(7):837-47. (Pubitemid 40331034)
68. Tegtmeyer N, et al. A small fibronectin-mimicking protein from bacteria induces cell spreading and focal adhesion formation. J Biol Chem. 2010;285(30):23515-26.
69. Lichtenberger LM, Delansorne R, Graziani LA. Importance of amino acid uptake and decarboxylation in gastrin release from isolated G cells. Nature. 1982;295(5851):698-700. (Pubitemid 12116146)
70. Zanner R, et al. Intracellular signal transduction during gastrin-induced histamine secretion in rat gastric ECL cells. Am J Physiol Cell Physiol. 2002;282(2):C374-82. (Pubitemid 34663197)
71. Tucker TP, et al. Helicobacter pylori induction of the gastrin promoter through GC-rich DNA elements. Helicobacter. 2010;15(5):438-48.
72. Wiedemann T, et al. Helicobacter pylori CagL dependent induction of gastrin expression via a novel avb5-integrin-inte-grin linked kinase signalling complex. Gut 2012;in press.
73. Mimuro H, et al. Grb2 is a key mediator of Helicobacter pylori CagA protein activities. Mol Cell. 2002;10(4):745-55. (Pubitemid 35335631)
74. Brandt S, et al. NF-kappaB activation and potentiation of pro-inflammatory responses by the Helicobacter pylori CagA protein. Proc Natl Acad Sci USA. 2005;102(26):9300-5. (Pubitemid 40923558)
75. Keates S, et al. cag+ Helicobacter pylori induces transactivation of the epidermal growth factor receptor in AGS gastric epithelial cells. J Biol Chem. 2001;276(51):48127-34.
76. Nozawa Y, et al. Identification of a signaling cascade for interleukin-8 production by Helicobacter pylori in human gastric epithelial cells. Biochem Pharmacol. 2002;64(1):21-30. (Pubitemid 34775172)
77. Hirata Y, et al. Helicobacter pylori CagA protein activates serum response element-driven transcription independently of tyrosine phosphorylation. Gastroenterology. 2002;123(6):1962-71. (Pubitemid 35408320)
78. Suzuki M, et al. Helicobacter pylori CagA phosphorylation-independent function in epithelial proliferation and inflammation. Cell Host Microbe. 2009;5(1):23-34.
79. Lamb A, et al. Helicobacter pylori CagA activates NF-kappaB by targeting TAK1 for TRAF6-mediated Lys 63 ubiquitination. EMBO Rep. 2009;10(11):1242-9.
80. Hirata Y, et al. MyD88 and TNF receptor-associated factor 6 are critical signal transducers in Helicobacter pylori-infected human epithelial cells. J Immunol. 2006;176(6):3796-803. (Pubitemid 43364028)
81. Watanabe T, et al. NOD1 contributes to mouse host defense against Helicobacter pylori via induction of type I IFN and activation of the ISGF3 signaling pathway. J Clin Invest. 2010;120(5):1645-62.
82. Blaser MJ, Atherton JC. Helicobacter pylori persistence: biology and disease. J Clin Invest. 2004;113(3):321-33. (Pubitemid 38544173)
83. Telford JL, et al. Gene structure of the Helicobacter pylori cytotoxin and evidence of its key role in gastric disease. J Exp Med. 1994;179(5):1653-8. (Pubitemid 24129582)
84. Cover TL, Blanke SR. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol. 2005;3(4):320-32. (Pubitemid 40443725)
85. Nakayama M, et al. Helicobacter pylori VacA activates the p38/activating transcription factor 2-mediated signal pathway in AZ-521 cells. J Biol Chem. 2004;279(8):7024-8. (Pubitemid 38248847)
86. Tegtmeyer N, et al. Importance of EGF receptor, HER2/Neu and Erk1/2 kinase signalling for host cell elongation and scattering induced by the Helicobacter pylori CagA protein: antagonistic effects of the vacuolating cytotoxin VacA. Cell Microbiol. 2009;11(3):488-505.
87. Wang F, et al. Helicobacter pylori VacA disrupts apical mem-brane-cytoskeletal interactions in gastric parietal cells. J Biol Chem. 2008;283(39):26714-25.
88. Peek RM Jr, et al. Heightened inflammatory response and cytokine expression in vivo to cagA? Helicobacter pylori strains. Lab Invest. 1995;73(6):760-70. (Pubitemid 26002335)
89. Sharma SA, et al. Interleukin-8 response of gastric epithelial cell lines to Helicobacter pylori stimulation in vitro. Infect Immun. 1995;63(5):1681-7.
90. Yamaoka Y, et al. Helicobacter pylori cagA gene and expression of cytokine messenger RNA in gastric mucosa. Gastroen-terology. 1996;110(6):1744-52. (Pubitemid 26169211)
91. Wolfe MM, Nompleggi DJ. Cytokine inhibition of gastric acid secretion\a little goes a long way. Gastroenterology. 1992;102(6):2177-8.
92. Beales IL, Calam J. Interleukin 1 beta and tumour necrosis factor alpha inhibit acid secretion in cultured rabbit parietal cells by multiple pathways. Gut. 1998;42(2):227-34. (Pubitemid 28212178)
93. Schepp W, et al. Identification and functional importance of IL-1 receptors on rat parietal cells. Am J Physiol. 1998;275(5 Pt 1): G1094-105.
94. Peek RM Jr, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2002;2(1):28-37. (Pubitemid 37328805)
95. El-Omar EM, et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature. 2000;404(6776): 398-402. (Pubitemid 30164342)
96. Keates S, et al. Helicobacter pylori infection activates NF-kappa B in gastric epithelial cells. Gastroenterology. 1997;113(4): 1099-109. (Pubitemid 27418963)
97. Perkins ND. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol. 2007; 8(1):49-62. (Pubitemid 46012014)
98. Hayden MS, Ghosh S. Signaling to NF-{kappa}B. Genes Dev. 2004;18(18):2195-224.
99. Zhang W, Kone BC. NF-kappaB inhibits transcription of the H(+)-K(+)-ATPase alpha(2)-subunit gene: role of histone deacetylases. Am J Physiol Renal Physiol. 2002;283(5): F904-11. (Pubitemid 35192456)
100. Zhong H, et al. The phosphorylation status of nuclear NF-kappaB determines its association with CBP/p300 or HDAC-1. Mol Cell. 2002;9(3):625-36. (Pubitemid 34273792)
101. Blaser MJ. Helicobacter pylori and esophageal disease: wake-up call? Gastroenterology. 2010;139(6):1819-22.
102. Malfertheiner P, et al. Symposium: Helicobacter pylori and clinical risks\focus on gastro-oesophageal reflux disease. Aliment Pharmacol Ther. 2002;16(Suppl 3):1-10. (Pubitemid 34534201)