Helicobacter pylori adaptation in vivo in response to a high-salt diet

Infection and Immunity

Volumn 83, Issue 12, 2015, Pages 4871-4883

  Loh, John T ^a   Gaddy, Jennifer A ^a,b   Scott Algood, Holly M ^a,b   Gaudieri, Silvana ^a,c,d   Mallal, Simon ^a,d   Cover, Timothy L ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d MURDOCH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; GENE MUTATION; GENE SEQUENCE; HELICOBACTER PYLORI; HIGH SODIUM INTAKE; HUMAN; HUMAN TISSUE; IN VIVO STUDY; MERIONES UNGUICULATUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEOMICS; SEQUENCE ANALYSIS; ANIMAL; BACTERIAL GENOME; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GERBIL; HELICOBACTER INFECTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PATHOLOGY; PHARMACOLOGY; SALT INTAKE; STOMACH MUCOSA;

BACTERIAL PROTEIN; FERRIC UPTAKE REGULATING PROTEINS, BACTERIAL; IRON; PROTEOME; REPRESSOR PROTEIN; SALT INTAKE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; GASTRIC MUCOSA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; GERBILLINAE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; IRON; MOLECULAR SEQUENCE DATA; MUTATION; OXIDATIVE STRESS; PROTEOME; REPRESSOR PROTEINS; SODIUM CHLORIDE, DIETARY;

EID: 84949666035     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00918-15     Document Type: Article

References (61)

1. Atherton JC, Blaser MJ. 2009. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest 119:2475-2487. http://dx.doi.org/10.1172/JCI38605.
2. Cover TL, Blaser MJ. 2009. Helicobacter pylori in health and disease. Gastroenterology 136:1863-1873. http://dx.doi.org/10.1053/j.gastro.2009.01.073.
3. Blaser MJ, Berg DE. 2001. Helicobacter pylori genetic diversity and risk of human disease. J Clin Invest 107:767-773. http://dx.doi.org/10.1172/JCI12672.
4. Suerbaum S, Josenhans C. 2007. Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat Rev Microbiol 5:441-452. http://dx.doi.org/10.1038/nrmicro1658.
5. Falush D, Kraft C, Taylor NS, Correa P, Fox JG, Achtman M, Suerbaum S. 2001. Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci U S A 98:15056-15061. http://dx.doi.org/10.1073/pnas.251396098.
6. Linz B, Windsor HM, McGraw JJ, Hansen LM, Gajewski JP, Tomsho LP, Hake CM, Solnick JV, Schuster SC, Marshall BJ. 2014. A mutation burst during the acute phase of Helicobacter pylori infection in humans and rhesus macaques. Nat Commun 5:4165.
7. Amieva MR, El-Omar EM. 2008. Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134:306-323. http://dx.doi.org/10.1053/j.gastro.2007.11.009.
8. Fox JG, Wang TC. 2007. Inflammation, atrophy, and gastric cancer. J Clin Invest 117:60-69. http://dx.doi.org/10.1172/JCI30111.
9. Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, Stemmermann GN, Nomura A. 1995. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55:2111-2115.
10. Hatakeyama M. 2014. Helicobacter pylori CagA and gastric cancer: a paradigm for hit-and-run carcinogenesis. Cell Host Microbe 15:306-316. http://dx.doi.org/10.1016/j.chom.2014.02.008.
11. Fischer W, Puls J, Buhrdorf R, Gebert B, Odenbreit S, Haas R. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol Microbiol 42:1337-1348.
12. 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 270:17771-11777.
13. Figueiredo C, Machado JC, Pharoah P, Seruca R, Sousa S, Carvalho R, Capelinha AF, Quint W, Caldas C, van Doorn LJ, Carneiro F, Sobrinho-Simoes M. 2002. Helicobacter pylori and interleukin 1 genotyping: an opportunity to identify high-risk individuals for gastric carcinoma. J Natl Cancer Inst 94:1680-1687. http://dx.doi.org/10.1093/jnci/94.22.1680.
14. Cover TL, Peek RM, Jr. 2013. Diet, microbial virulence, and Helicobacter pylori-induced gastric cancer. Gut Microbes 4:482-493. http://dx.doi.org/10.4161/gmic.26262.
15. Lee SA, Kang D, Shim KN, Choe JW, Hong WS, Choi H. 2003. Effect of diet and Helicobacter pylori infection to the risk of early gastric cancer. J Epidemiol 13:162-168. http://dx.doi.org/10.2188/jea.13.162.
16. Tsugane S. 2005. Salt, salted food intake, and risk of gastric cancer: epidemiologic evidence. Cancer Sci 96:1-6. http://dx.doi.org/10.1111/j.1349-7006.2005.00006.x.
17. Tsugane S, Sasazuki S. 2007. Diet and the risk of gastric cancer: review of epidemiological evidence. Gastric Cancer 10:75-83. http://dx.doi.org/10.1007/s10120-007-0420-0.
18. Bergin IL, Sheppard BJ, Fox JG. 2003. Helicobacter pylori infection and high dietary salt independently induce atrophic gastritis and intestinal metaplasia in commercially available outbred Mongolian gerbils. Dig Dis Sci 48:475-485. http://dx.doi.org/10.1023/A:1022524313355.
19. Fox JG, Dangler CA, Taylor NS, King A, Koh TJ, Wang TC. 1999. High-salt diet induces gastric epithelial hyperplasia and parietal cell loss, and enhances Helicobacter pylori colonization in C57BL/6 mice. Cancer Res 59:4823-4828.
20. Gamboa-Dominguez A, Ubbelohde T, Saqui-Salces M, Romano-Mazzoti L, Cervantes M, Dominguez-Fonseca C, de la Luz Estreber M, Ruiz-Palacios GM. 2007. Salt and stress synergize Helicobacter pyloriinduced gastric lesions, cell proliferation, and p21 expression in Mongolian gerbils. Dig Dis Sci 52:1517-1526. http://dx.doi.org/10.1007/s10620-006-9524-3.
21. Kato S, Tsukamoto T, Mizoshita T, Tanaka H, Kumagai T, Ota H, Katsuyama T, Asaka M, Tatematsu M. 2006. High salt diets dosedependently promote gastric chemical carcinogenesis in Helicobacter pylori-infected Mongolian gerbils associated with a shift in mucin production from glandular to surface mucous cells. Int J Cancer 119:1558-1566. http://dx.doi.org/10.1002/ijc.21810.
22. Gaddy JA, Radin JN, Loh JT, Zhang F, Washington MK, Peek RM, Jr, Algood HM, Cover TL. 2013. High dietary salt intake exacerbates Helicobacter pylori-induced gastric carcinogenesis. Infect Immun 81:2258-2267. http://dx.doi.org/10.1128/IAI.01271-12.
23. Gancz H, Jones KR, Merrell DS. 2008. Sodium chloride affects Helicobacter pylori growth and gene expression. J Bacteriol 190:4100-4105. http://dx.doi.org/10.1128/JB.01728-07.
24. Loh JT, Friedman DB, Piazuelo MB, Bravo LE, Wilson KT, Peek RM, Jr, Correa P, Cover TL. 2012. Analysis of Helicobacter pylori cagA promoter elements required for salt-induced upregulation of CagA expression. Infect Immun 80:3094-3106. http://dx.doi.org/10.1128/IAI.00232-12.
25. Loh JT, Torres VJ, Cover TL. 2007. Regulation of Helicobacter pylori cagA expression in response to salt. Cancer Res 67:4709-4715. http://dx.doi.org/10.1158/0008-5472.CAN-06-4746.
26. Voss BJ, Loh JT, Hill S, Rose KL, McDonald HW, Cover TL. 24 June 2015. Alteration of the Helicobacter pylori membrane proteome in response to changes in environmental salt concentration. Proteomics Clin Appl http://dx.doi.org/10.1002/prca.201400176.
27. 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 102:10646-10651. http://dx.doi.org/10.1073/pnas.0504927102.
28. Israel DA, Salama N, Arnold CN, Moss SF, Ando T, Wirth HP, Tham KT, Camorlinga M, Blaser MJ, Falkow S, Peek RM, Jr. 2001. Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses. J Clin Invest 107:611-620. http://dx.doi.org/10.1172/JCI11450.
29. Voss BJ, Gaddy JA, McDonald WH, Cover TL. 2014. Analysis of surfaceexposed outer membrane proteins in Helicobacter pylori. J Bacteriol 196: 2455-2471. http://dx.doi.org/10.1128/JB.01768-14.
30. MacCoss MJ, McDonald WH, Saraf A, Sadygov R, Clark JM, Tasto JJ, Gould KL, Wolters D, Washburn M, Weiss A, Clark JI, Yates JR, III. 2002. Shotgun identification of protein modifications from protein complexes and lens tissue. Proc Natl Acad Sci U S A 99:7900-7905. http://dx.doi.org/10.1073/pnas.122231399.
31. Shaffer CL, Gaddy JA, Loh JT, Johnson EM, Hill S, Hennig EE, McClain MS, McDonald WH, Cover TL. 2011. Helicobacter pylori exploits a unique repertoire of type IV secretion system components for pilus assembly at the bacteria-host cell interface. PLoS Pathog 7:e1002237. http://dx.doi.org/10.1371/journal.ppat.1002237.
32. Farnbacher M, Jahns T, Willrodt D, Daniel R, Haas R, Goesmann A, Kurtz S, Rieder G. 2010. Sequencing, annotation, and comparative genome analysis of the gerbil-adapted Helicobacter pylori strain B8. BMC Genomics 11:335. http://dx.doi.org/10.1186/1471-2164-11-335.
33. Barrozo RM, Cooke CL, Hansen LM, Lam AM, Gaddy JA, Johnson EM, Cariaga TA, Suarez G, Peek RM, Jr, Cover TL, Solnick JV. 2013. Functional plasticity in the type IV secretion system of Helicobacter pylori. PLoS Pathog 9:e1003189. http://dx.doi.org/10.1371/journal.ppat.1003189.
34. Styer CM, Hansen LM, Cooke CL, Gundersen AM, Choi SS, Berg DE, Benghezal M, Marshall BJ, Peek RM, Jr, Boren T, Solnick JV. 2010. Expression of the BabA adhesin during experimental infection with Helicobacter pylori. Infect Immun 78:1593-1600. http://dx.doi.org/10.1128/IAI.01297-09.
35. Johnson EM, Gaddy JA, Voss BJ, Hennig EE, Cover TL. 2014. Genes required for assembly of pili associated with the Helicobacter pylori cag type IV secretion system. Infect Immun 82:3457-3470. http://dx.doi.org/10.1128/IAI.01640-14.
36. Waidner B, Greiner S, Odenbreit S, Kavermann H, Velayudhan J, Stahler F, Guhl J, Bisse E, van Vliet AH, Andrews SC, Kusters JG, Kelly DJ, Haas R, Kist M, Bereswill S. 2002. Essential role of ferritin Pfr in Helicobacter pylori iron metabolism and gastric colonization. Infect Immun 70:3923-3929. http://dx.doi.org/10.1128/IAI.70.7.3923-3929.2002.
37. Odenbreit S, Wieland B, Haas R. 1996. Cloning and genetic characterization of Helicobacter pylori catalase and construction of a catalasedeficient mutant strain. J Bacteriol 178:6960-6967.
38. Carrizo-Chávez MA, Cruz-Castaneda A, Olivares-Trejo Jde J. 2012. The frpB1 gene of Helicobacter pylori is regulated by iron and encodes a membrane protein capable of binding haem and haemoglobin. FEBS Lett 586: 875-879. http://dx.doi.org/10.1016/j.febslet.2012.02.015.
39. Delany I, Pacheco AB, Spohn G, Rappuoli R, Scarlato V. 2001. Irondependent transcription of the frpB gene of Helicobacter pylori is controlled by the Fur repressor protein. J Bacteriol 183:4932-4937. http://dx.doi.org/10.1128/JB.183.16.4932-4937.2001.
40. Tsugawa H, Suzuki H, Matsuzaki J, Hirata K, Hibi T. 2012. FecA1, a bacterial iron transporter, determines the survival of Helicobacter pylori in the stomach. Free Radic Biol Med 52:1003-1010. http://dx.doi.org/10.1016/j.freeradbiomed.2011.12.011.
41. Grubman A, Phillips A, Thibonnier M, Kaparakis-Liaskos M, Johnson C, Thiberge JM, Radcliff FJ, Ecobichon C, Labigne A, de Reuse H, Mendz GL, Ferrero RL. 2010. Vitamin B6 is required for full motility and virulence in Helicobacter pylori. mBio 1:e00112-10. http://dx.doi.org/10.1128/mBio.00112-10.
42. Asim M, Chikara SK, Ghosh A, Vudathala S, Romero-Gallo J, Krishna US, Wilson KT, Israel DA, Peek RM, Jr, Chaturvedi R. 2015. Draft genome sequence of gerbil-adapted carcinogenic Helicobacter pylori strain 7.13. Genome Announc 3:e00641-15. http://dx.doi.org/10.1128/genomeA.00641-15.
43. Danielli A, Romagnoli S, Roncarati D, Costantino L, Delany I, Scarlato V. 2009. Growth phase and metal-dependent transcriptional regulation of the fecA genes in Helicobacter pylori. J Bacteriol 191:3717-3725. http://dx.doi.org/10.1128/JB.01741-08.
44. Baldwin DN, Shepherd B, Kraemer P, Hall MK, Sycuro LK, Pinto-Santini DM, Salama NR. 2007. Identification of Helicobacter pylori genes that contribute to stomach colonization. Infect Immun 75:1005-1016. http://dx.doi.org/10.1128/IAI.01176-06.
45. Ernst FD, Bereswill S, Waidner B, Stoof J, Mader U, Kusters JG, Kuipers EJ, Kist M, van Vliet AH, Homuth G. 2005. Transcriptional profiling of Helicobacter pylori Fur-and iron-regulated gene expression. Microbiology 151:533-546. http://dx.doi.org/10.1099/mic.0.27404-0.
46. Gancz H, Censini S, Merrell DS. 2006. Iron and pH homeostasis intersect at the level of Fur regulation in the gastric pathogen Helicobacter pylori. Infect Immun 74:602-614. http://dx.doi.org/10.1128/IAI.74.1.602-614.2006.
47. Agriesti F, Roncarati D, Musiani F, Del Campo C, Iurlaro M, Sparla F, Ciurli S, Danielli A, Scarlato V. 2014. FeON-FeOFF: the Helicobacter pylori Fur regulator commutates iron-responsive transcription by discriminative readout of opposed DNA grooves. Nucleic Acids Res 42: 3138-3151. http://dx.doi.org/10.1093/nar/gkt1258.
48. Danielli A, Roncarati D, Delany I, Chiarini V, Rappuoli R, Scarlato V. 2006. In vivo dissection of the Helicobacter pylori Fur regulatory circuit by genome-wide location analysis. J Bacteriol 188:4654-4662. http://dx.doi.org/10.1128/JB.00120-06.
49. Gancz H, Merrell DS. 2011. The Helicobacter pylori ferric uptake regulator (Fur) is essential for growth under sodium chloride stress. J Microbiol 49:294-298. http://dx.doi.org/10.1007/s12275-011-0396-7.
50. Carpenter BM, Gancz H, Gonzalez-Nieves RP, West AL, Whitmire JM, Michel SL, Merrell DS. 2009. A single nucleotide change affects furdependent regulation of sodB in Helicobacter pylori. PLoS One 4:e5369. http://dx.doi.org/10.1371/journal.pone.0005369.
51. Cooksley C, Jenks PJ, Green A, Cockayne A, Logan RP, Hardie KR. 2003. NapA protects Helicobacter pylori from oxidative stress damage, and its production is influenced by the ferric uptake regulator. J Med Microbiol 52:461-469. http://dx.doi.org/10.1099/jmm.0.05070-0.
52. Ernst FD, Homuth G, Stoof J, Mader U, Waidner B, Kuipers EJ, Kist M, Kusters JG, Bereswill S, van Vliet AH. 2005. Iron-responsive regulation of the Helicobacter pylori iron-cofactored superoxide dismutase SodB is mediated by Fur. J Bacteriol 187:3687-3692. http://dx.doi.org/10.1128/JB.187.11.3687-3692.2005.
53. Seyler RW, Jr, Olson JW, Maier RJ. 2001. Superoxide dismutasedeficient mutants of Helicobacter pylori are hypersensitive to oxidative stress and defective in host colonization. Infect Immun 69:4034-4040. http://dx.doi.org/10.1128/IAI.69.6.4034-4040.2001.
54. Wang G, Alamuri P, Maier RJ. 2006. The diverse antioxidant systems of Helicobacter pylori. Mol Microbiol 61:847-860. http://dx.doi.org/10.1111/j.1365-2958.2006.05302.x.
55. Dian C, Vitale S, Leonard GA, Bahlawane C, Fauquant C, Leduc D, Muller C, de Reuse H, Michaud-Soret I, Terradot L. 2011. The structure of the Helicobacter pylori ferric uptake regulator Fur reveals three functional metal binding sites. Mol Microbiol 79:1260-1275. http://dx.doi.org/10.1111/j.1365-2958.2010.07517.x.
56. Gilbreath JJ, Pich OQ, Benoit SL, Besold AN, Cha JH, Maier RJ, Michel SL, Maynard EL, Merrell DS. 2013. Random and site-specific mutagenesis of the Helicobacter pylori ferric uptake regulator provides insight into Fur structure-function relationships. Mol Microbiol 89:304-323. http://dx.doi.org/10.1111/mmi.12278.
57. Blanchard TG, Czinn SJ, Correa P, Nakazawa T, Keelan M, Morningstar L, Santana-Cruz I, Maroo A, McCracken C, Shefchek K, Daugherty S, Song Y, Fraser CM, Fricke WF. 2013. Genome sequences of 65 Helicobacter pylori strains isolated from asymptomatic individuals and patients with gastric cancer, peptic ulcer disease, or gastritis. Pathog Dis 68:39-43. http://dx.doi.org/10.1111/2049-632X.12045.
58. Miles S, Piazuelo MB, Semino-Mora C, Washington MK, Dubois A, Peek RM, Jr, Correa P, Merrell DS. 2010. Detailed in vivo analysis of the role of Helicobacter pylori Fur in colonization and disease. Infect Immun 78:3073-3082. http://dx.doi.org/10.1128/IAI.00190-10.
59. den Besten HM, Mols M, Moezelaar R, Zwietering MH, Abee T. 2009. Phenotypic and transcriptomic analyses of mildly and severely saltstressed Bacillus cereus ATCC 14579 cells. Appl Environ Microbiol 75: 4111-4119. http://dx.doi.org/10.1128/AEM.02891-08.
60. Höper D, Bernhardt J, Hecker M. 2006. Salt stress adaptation of Bacillus subtilis: a physiological proteomics approach. Proteomics 6:1550-1562. http://dx.doi.org/10.1002/pmic.200500197.
61. Hoffmann T, Schutz A, Brosius M, Volker A, Volker U, Bremer E. 2002. High-salinity-induced iron limitation in Bacillus subtilis. J Bacteriol 184: 718-727. http://dx.doi.org/10.1128/JB.184.3.718-727.2002.