In vivo sequence variation in HopZ, a phase-variable outer membrane protein of helicobacter pylori

Infection and Immunity

Volumn 80, Issue 12, 2012, Pages 4364-4373

  Kennemann, Lynn ^a   Brenneke, Birgit ^a   Andres, Sönke ^b,c   Engstrand, Lars ^b,c   Meyer, Thomas F ^d   Aebischer, Toni ^d   Josenhans, Christine ^a   Suerbaum, Sebastian ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

^d MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HOPZ PROTEIN; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATROPHIC GASTRITIS; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM ISOLATE; CONTROLLED STUDY; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURIFYING SELECTION;

ACUTE DISEASE; AFRICA; AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; CHRONIC DISEASE; GASTRITIS, ATROPHIC; GENETIC VARIATION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMAN MIGRATION; HUMANS; MUTATION; PHYLOGENY;

EID: 84870821322     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00977-12     Document Type: Article

References (62)

1. Aebischer T, et al. 2008. Correlation of T cell response and bacterial clearance in human volunteers challenged with Helicobacter pylori revealed by randomised controlled vaccination with Ty21a-based Salmonella vaccines. Gut 57:1065-1072.
2. Alm RA, et al. 2000. Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect. Immun. 68:4155-4168.
3. Alm, RA, et al. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176-180.
4. Aro P, et al. 2004. Valid symptom reporting at upper endoscopy in a random sample of the Swedish adult general population: the Kalixanda study. Scand. J. Gastroenterol. 39:1280-1288.
5. Aspholm-Hurtig M, et al. 2004. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305:519-522.
6. Behrens W, Bonig T, Suerbaum S, Josenhans C. 2012. Genome sequence of Helicobacter pylori hpEurope strain N6. J. Bacteriol. 194:3725-3726.
7. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
8. Borén T, Falk P, Roth KA, Larson G, Normark S. 1993. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262:1892-1895.
9. Censini S, et al. 1996. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. U. S. A. 93:14648-14653.
10. Chattopadhyay S, et al. 2004. Multiplex PCR assay for rapid detection and genotyping of Helicobacter pylori directly from biopsy specimens. J. Clin. Microbiol. 42:2821-2824.
11. Colbeck JC, Hansen LM, Fong JM, Solnick JV. 2006. Genotypic profile of the outer membrane proteins BabA and BabB in clinical isolates of Helicobacter pylori. Infect. Immun. 74:4375-4378.
12. Correa P, et al. 2000. Chemoprevention of gastric dysplasia: randomized trial of antioxidant supplements and anti-Helicobacter pylori therapy. J. Natl. Cancer Inst. 92:1881-1888.
13. Cover TL, Blanke SR. 2005. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat. Rev. Microbiol. 3:320-332.
14. Dossumbekova A, et al. 2006. Helicobacter pylori HopH (OipA) and bacterial pathogenicity: genetic and functional genomic analysis of hopH gene polymorphisms. J. Infect. Dis. 194:1346-1355.
15. Falk P, et al. 1993. An in vitro adherence assay reveals that Helicobacter pylori exhibits cell lineage-specific tropism in the human gastric epithelium. Proc. Natl. Acad. Sci. U. S. A. 90:2035-2039.
16. Falush D, Stephens M, Pritchard JK. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567-1587.
17. Falush D, et al. 2003. Traces of human migrations in Helicobacter pylori populations. Science 299:1582-1585.
18. Ferrero RL, Cussac V, Courcoux P, Labigne A. 1992. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J. Bacteriol. 174:4212-4217.
19. Gerhard M, et al. 1999. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc. Natl. Acad. Sci. U. S. A. 96:12778-12783.
20. Giannakis M, et al. 2009. Response of gastric epithelial progenitors to Helicobacter pylori isolates obtained from Swedish patients with chronic atrophic gastritis. J. Biol. Chem. 284:30383-30394.
21. Graham DY, Alpert LC, Smith JL, Yoshimura HH. 1988. Iatrogenic Campylobacter pylori infection is a cause of epidemic achlorhydria. Am. J. Gastroenterol. 83:974-980.
22. Graham DY, et al. 2004. Challenge model for Helicobacter pylori infection in human volunteers. Gut 53:1235-1243.
23. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
24. Hennig EE, Allen JM, Cover TL. 2006. Multiple chromosomal loci for the babA gene in Helicobacter pylori. Infect. Immun. 74:3046-3051.
25. Ilver D, et al. 1998. Helicobacter pylori adhesin binding fucosylated histoblood group antigens revealed by retagging. Science 279:373-377.
26. Ilver D, Barone S, Mercati D, Lupetti P, Telford JL. 2004. Helicobacter pylori toxin VacA is transferred to host cells via a novel contact-dependent mechanism. Cell. Microbiol. 6:167-174.
27. Ishijima N, et al. 2011. BabA-mediated adherence is a potentiator of the Helicobacter pylori type IV secretion system activity. J. Biol. Chem. 286: 25256-25264.
28. Karlsson A, Ryberg A, Nosouhi DM, Borch K, Monstein HJ. 2012. Variation in number of cagA EPIYA-C phosphorylation motifs between cultured Helicobacter pylori and biopsy strain DNA. Infect. Genet. Evol. 12:175-179.
29. Kavermann H, et al. 2003. Identification and characterization of Helicobacter pylori genes essential for gastric colonization. J. Exp. Med. 197:813-822.
30. Kawai M, et al. 2011. Evolution in an oncogenic bacterial species with extreme genome plasticity: Helicobacter pylori East Asian genomes. BMC Microbiol. 11:104. doi:10.1186/1471-2180-11-104.
31. Kennemann L, et al. 2011. Helicobacter pylori genome evolution during human infection. Proc. Natl. Acad. Sci. U. S. A. 108:5033-5038.
32. Kersulyte D, et al. 2010. Helicobacter pylori from Peruvian Amerindians: traces of human migrations in strains from remote Amazon, and genome sequence of an Amerind strain. PLoS One 5:e15076. doi:10.1371/ journal.pone.0015076.
33. Kraft C, et al. 2006. Genomic changes during chronic Helicobacter pylori infection. J. Bacteriol. 188:249-254.
34. Labigne-Roussel A, Courcoux P, Tompkins L. 1988. Gene disruption and replacement as a feasible approach for mutagenesis of Campylobacter jejuni. J. Bacteriol. 170:1704-1708.
35. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
36. Linden SK, et al. 2009. MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy. PLoS Pathog. 5:e1000617. doi:10.1371/journal.ppat.1000617.
37. Linz B, et al. 2007. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445:915-918.
38. Mahdavi J, et al. 2002. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297:573-578.
39. Marshall BJ, Armstrong JA, McGechie DB, Glancy RJ. 1985. Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med. J. Aust. 142:436-439.
40. Meinke A, et al. 2009. Composition of the ANTIGENome of Helicobacter pylori defined by human serum antibodies. Vaccine 27:3251-3259.
41. Merrell DS, Goodrich ML, Otto G, Tompkins LS, Falkow S. 2003. pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect. Immun. 71:3529-3539.
42. Moodley Y, et al. 2012. Age of the association between Helicobacter pylori and man. PLoS Pathog. 8:e1002693. doi:10.1371/journal.ppat. 1002693.
43. Moodley Y, et al. 2009. The peopling of the Pacific from a bacterial perspective. Science 323:527-530.
44. Morris A, Nicholson G. 1987. Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH. Am. J. Gastroenterol. 82:192-199.
45. Morris AJ, Ali MR, Nicholson GI, Perez-Perez GI, Blaser MJ. 1991. Long-term follow-up of voluntary ingestion of Helicobacter pylori. Ann. Intern. Med. 114:662-663.
46. Odenbreit S, Till M, Hofreuter D, Faller G, Haas R. 1999. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 31: 1537-1548.
47. Olbermann P, et al. 2010. A global overview of the genetic and functional diversity in the Helicobacter pylori cag pathogenicity island. PLoS Genet. 6:e1001069. doi:10.1371/journal.pgen.1001069.
48. Peck B, Ortkamp M, Diehl KD, Hundt E, Knapp B. 1999. Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucleic Acids Res. 27:3325-3333.
49. Ramsey EJ, et al. 1979. Epidemic gastritis with hypochlorhydria. Gastroenterology 76:1449-1457.
50. Schmitz A, Josenhans C, Suerbaum S. 1997. Cloning and characterization of the Helicobacter pylori flbA gene, which codes for a membrane protein involved in coordinated expression of flagellar genes. J. Bacteriol. 179:987-997.
51. Schwarz S, et al. 2008. Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog. 4:e1000180. doi:10.1371/journal.ppat.1000180.
52. Solnick JV, Hansen LM, Salama NR, Boonjakuakul JK, Syvanen M. 2004. Modification of Helicobacter pylori outer membrane protein expression during experimental infection of rhesus macaques. Proc. Natl. Acad. Sci. U. S. A. 101:2106-2111.
53. Sterzenbach T, et al. 2008. The role of the Helicobacter hepaticus flagellar sigma factor FliA in gene regulation and murine colonization. J. Bacteriol. 190:6398-6408.
54. Storskrubb T, et al. 2005. A negative Helicobacter pylori serology test is more reliable for exclusion of premalignant gastric conditions than a negative test for current H. pylori infection: a report on histology and H. pylori detection in the general adult population. Scand. J. Gastroenterol. 40:302-311.
55. Suerbaum S, Michetti P. 2002. Helicobacter pylori infection. N. Engl. J. Med. 347:1175-1186.
56. Taylor NS, et al. 1995. Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J. Clin. Microbiol. 33:918-923.
57. Tomb JF, et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
58. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76:4350-4354.
59. Yamaoka Y. 2008. Roles of the plasticity regions of Helicobacter pylori in gastroduodenal pathogenesis. J. Med. Microbiol. 57:545-553.
60. Yamaoka Y, et al. 2002. Helicobacter pylori infection in mice: role of outer membrane proteins in colonization and inflammation. Gastroenterology 123:1992-2004.
61. Yamaoka Y, et al. 2004. Role of interferon-stimulated responsive element- like element in interleukin-8 promoter in Helicobacter pylori infection. Gastroenterology 126:1030-1043.
62. Yanisch-Perron C, Vieira J, Messing J. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.