Ten years after the first Helicobacter pylori genome: Comparative and functional genomics provide new insights in the variability and adaptability of a persistent pathogen

FEMS Immunology and Medical Microbiology

Volumn 50, Issue 2, 2007, Pages 165-176

  De Reuse, Hilde ^a   Bereswill, Stefan ^b  

^a INSTITUT PASTEUR   (France)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Diversity; DNA arrays; Evolution; Gastric pathologies; Transcriptome

Indexed keywords

ACIDITY; BACTERIAL STRAIN; COEVOLUTION; CONFERENCE PAPER; DISEASE COURSE; EVOLUTIONARY ADAPTATION; FUNCTIONAL GENOMICS; GASTROENTEROLOGY; GENE EXPRESSION; GENE IDENTIFICATION; GENE SEQUENCE; GENE TRANSFER; GENETIC VARIABILITY; GENOMICS; GROWTH CURVE; HELICOBACTER PYLORI; IMMUNE RESPONSE; MOLECULAR BIOLOGY; NONHUMAN; PATHOGENESIS; POINT MUTATION; PRIORITY JOURNAL; TRANSCRIPTOMICS; VIRULENCE;

ADAPTATION, PHYSIOLOGICAL; GENOME, BACTERIAL; GENOMICS; HELICOBACTER PYLORI; VARIATION (GENETICS); VIRULENCE;

EID: 34250354686     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2007.00244.x     Document Type: Conference Paper

References (90)

1. Allan E, Clayton CL, McLaren A et al 2001) Characterization of low-pH responses of Helicobacter pylori using genomic DNA arrays. Microbiology 147 : 2285 2292.
2. Alm RA, Ling LSL, Moir DT et al 1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397 : 176 180.
3. Ang S, Lee CZ, Peck K et al 2001) Acid-induced expression in Helicobacter pylori: study in genomic scale by microarray. Infect Immun 69 : 1679 1686.
4. Atherton JC, Cao P, Peek RM et al 1995) Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. J Biol Chem 270 : 17771 17777.
5. Baar C, Eppinger M, Raddatz G et al 2003) Complete genome sequence and analysis of Wolinella succinogenes. Proc Natl Acad Sci USA 100 : 11690 11695.
6. Bang IS, Audia JP, Park YK Foster JW (2002) Autoregulation of the ompR response regulator by acid shock and control of the Salmonella enterica acid tolerance response. Mol Microbiol 44 : 1235 1250.
7. Beier D Frank R (2000) Molecular characterization of two-component systems of Helicobacter pylori. J Bacteriol 182 : 2068 2076.
8. Bereswill S, Waidner U, Odenbreit S et al 1998) Structural, functional and mutational analysis of the pfr gene encoding a ferritin from Helicobacter pylori. Microbiology 144 : 2505 2516.
9. Bereswill S, Schönenberger R, Thies C et al 2000a) New approaches for genotyping of Helicobacter pylori based on amplification of polymorphisms in intergenic DNA regions and at the insertion site of the cag pathogenicity island. Med Microbiol Immunol 189 : 105 113.
10. Bereswill S, Greiner S, van Vliet AHM et al 2000b) Regulation of ferritin-mediated cytoplasmic iron storage by the ferric uptake regulator homolog (Fur) of Helicobacter pylori. J Bacteriol 182 : 5948 5953.
11. Bijlsma JJE, Waidner B, Van Vliet AHM et al 2002) The Helicobacter pylori homologue of the ferric uptake regulator is involved in acid resistance. Infect Immun 70 : 606 611.
12. Bizzozero G (1893) Ueber die schlauchfoermigen Druesen des Magendarmkanals und die Beziehungen ihres Epithels zu dem Oberflaechenepithel der Schleimhaut. Arch Mikr Anat 42 : 82.
13. Blaser MJ (1994) Helicobacter pylori phenotypes associated with peptic ulceration. Scand J Gastroenterol 205 : 1 5.
14. Boneca IG, De Reuse H, Epinat JC et al 2003) A revised annotation and comparative analysis of Helicobacter pylori genomes. Nucleic Acids Res 31 : 1704 1714.
15. Bury-Moné S, Thiberge JM, Contreras M et al 2004) Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori. Mol Microbiol 53 : 623 638.
16. 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.
17. Colland F, Rain JC, Gounon P et al 2001) Identification of the Helicobacter pylori anti-σ28 factor. Mol Microbiol 41 : 477 487.
18. Contreras M, Thiberge JM, Mandrand-Berthelot MA Labigne A (2003) Characterization of the roles of NikR, a nickel-responsive pleiotropic autoregulator of Helicobacter pylori. Mol Microbiol 49 : 947 963.
19. Cooke CL, Huff JL Solnick JV (2005) The role of genome diversity and immune evasion in persistent infection with Helicobacter pylori. FEMS Immunol Med Microbiol 45 : 11 23.
20. Covacci A Rappuoli R (1998) Helicobacter pylori molecular evolution of a bacterial quasi-species. Curr Opin Microbiol 1 : 96 102.
21. Covacci A, Telford JL, Del Giudice G et al 1999) Helicobacter pylori virulence and genetic geography. Science 284 : 1328 1333.
22. Danielli A, Roncarati D, Delany I et al 2006) In vivo dissection of the Helicobacter pylori Fur regulatory circuit by genome-wide location analysis. J Bacteriol 188 : 4654 4662.
23. Delany I, Spohn G, Pacheco ABF et al 2002) Autoregulation of Helicobacter pylori Fur revealed by functional analysis of the iron-binding site. Mol Microbiol 46 : 1107 1122.
24. Delany I, Ieva R, Soragni A et al 2005) In vitro analysis of protein-operator interactions of the NikR and Fur metal-responsive regulators of coregulated genes in Helicobacter pylori. J Bacteriol 187 : 7703 7715.
25. De Pina K, Desjardin V, Mandrand-Berthelot MA et al 1999) Isolation and characterization of the nikR gene encoding a nickel-responsive regulator in Escherichia coli. J Bacteriol 181 : 670 674.
26. de Vries N, van Vliet AHM Kusters JG (2001) Gene regulation. Helicobacter pylori: Physiology and Genetics (Mobley HLT, Mendz GL Hazell SL, eds), pp. 321 334. ASM Press, Washington, DC.
27. Dietz P, Gerlach G Beier D (2002) Identification of target genes regulated by the two-component system HP166-HP165 of Helicobacter pylori. J Bacteriol 184 : 350 362.
28. Eppinger M, Baar C, Raddatz G et al 2004) Comparative analysis of four Campylobacterales. Nat Rev Microbiol 2 : 872 885.
29. Eppinger M, Baar C, Linz B et al 2006) Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet 2 : e120.
30. Ernst FD, Bereswill S, Waidner B et al 2005a) Transcriptional profiling of Helicobacter pylori Fur- and iron-regulated gene expression. Microbiology 151 : 533 546.
31. Ernst FD, Homuth G, Stoof J et al 2005b) Iron-responsive regulation of the Helicobacter pylori iron-cofactored superoxide dismutase SodB is mediated by Fur. J Bacteriol 187 : 3687 3692.
32. Ernst FD, Kuipers EJ, Heijens A et al 2005c) The nickel-responsive regulator NikR controls activation and repression of gene transcription in Helicobacter pylori. Infect Immun 73 : 7252 7258.
33. Falush D, Kraft C, Taylor NS et al 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 USA 98 : 15056 15061.
34. Falush D, Wirth T, Linz B et al 2003a) Traces of human migrations in Helicobacter pylori populations. Science 299 : 1582 1585.
35. Falush D, Stephens M Pritchard JK (2003b) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164 : 1567 1587.
36. Forsyth MH, Cao P, Garcia PP et al 2002) Genome-wide transcriptional profiling in a histidine kinase mutant of Helicobacter pylori identifies members of a regulon. J Bacteriol 184 : 4630 4635.
37. 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.
38. Garcia-Vallve S, Janssen PJ Ouzounis CA (2002) Genetic variation between Helicobacter pylori strains: gene acquisition or loss? Trends Microbiol 10 : 445 447.
39. Gressmann H, Linz B, Ghai R, Pleissner KP et al 2005) Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet 1 : e43.
40. Gupta RS (2006) Molecular signatures (unique proteins and conserved indels) that are specific for the epsilon proteobacteria (Campylobacterales). BMC Genomics 7 : 167.
41. Hofreuter D Haas R (2002) Characterization of two cryptic Helicobacter pylori plasmids: a putative source for horizontal gene transfer and gene shuffling. J Bacteriol 184 : 2755 2766.
42. Israel DA, Salama N, Krishna U et al 2001) Helicobacter pylori genetic diversity within the gastric niche of a single human host. Proc Natl Acad Sci USA 98 : 14625 14630.
43. Janssen PJ, Audit B Ouzounis CA (2001) Strain-specific genes of Helicobacter pylori: distribution, function and dynamics. Nucleic Acids Res 29 : 4395 4404.
44. Jiang Q, Hiratsuka K Taylor DE (1996) Variability of gene order in different Helicobacter pylori strains contributes to genome diversity. Mol Microbiol 20 : 833 842.
45. Josenhans C, Niehus E, Amersbach S et al 2002) Functional characterization of the antagonist flagellar late regulators FliA and FlgM of Helicobacter pylori and their effects on the H. pylori transcriptome. Mol Microbiol 43 : 307 322.
46. Jungblut PR, Bumann D, Haas G et al 2000) Comparative proteome analysis of Helicobacter pylori. Mol Microbiol 36 : 710 725.
47. Karnholz A, Hoefler C, Odenbreit S et al 2006) Functional and topological characterization of novel components of the comB DNA transformation competence system in Helicobacter pylori. J Bacteriol 188 : 882 893.
48. Kim N, Marcus EA, Wen Y et al 2004) Genes of Helicobacter pylori regulated by attachment to AGS cells. Infect Immun 72 : 2358 2368.
49. Konjetzny GE (1923) Chronische Gastritis und Duodenitis als Ursache des Magenduodenalgeschwuers. Beitraege zur pathologischen Anatomie und allgemeinen Pathologie 71 : 595 618.
50. Kraft C, Stack A, Josenhans C et al 2006) Genomic changes during chronic Helicobacter pylori infection. J Bacteriol 188 : 249 254.
51. Kusters JG, van Vliet AH Kuipers EJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19 : 449 490.
52. Linz B, Balloux F, Moodley Y et al 2007) An African origin for the intimate association between humans and Helicobacter pylori. Nature 445 : 915 918.
53. Loh JT Cover TL (2006) Requirement of histidine kinases HP0165 and HP1364 for acid resistance in Helicobacter pylori. Infect Immun 74 : 3052 3059.
54. Maamar H Dubnau D (2005) Bistability in the Bacillus subtilis K-state (competence) system requires a positive feedback loop. Mol Microbiol 56 : 615 624.
55. Marais A, Mendz GL, Hazell SL Megraud F (1999) Metabolism and genetics of Helicobacter pylori: the genome era. Microbiol Mol Biol Rev 63 : 642 674.
56. Marshall BJ Warren JR (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1 : 1311 1315.
57. Marshall BJ, Armstrong JA, McGechie DB et al 1985) Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med J Aust 142 : 436 439.
58. Merrell DS, Goodrich ML, Otto G et al 2003a) pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect Immun 71 : 3529 3539.
59. Merrell DS, Thompson LJ, Kim CC et al 2003b) Growth phase-dependent response of Helicobacter pylori to iron starvation. Infect Immun 71 : 6510 6525.
60. Niehaus E, Gressmann H, Ye F et al 2004) Genome-wide analysis of transcriptional hierarchy and feedback regulation in the flagellar system of Helicobacter pylori. Mol Microbiol 52 : 947 961.
61. Oh JD, Kling-Backhed H, Giannakis M et al 2006) The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc Natl Acad Sci USA 103 : 9999 10004.
62. Panthel K, Dietz P, Haas R Beier D (2003) Two-component systems of Helicobacter pylori contribute to virulence in a mouse model infection model. Infect Immun 71 : 5381 5385.
63. Parkhill J, Wren BW, Mungall K et al 2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403 : 665 668.
64. Pflock M, Dietz P, Shaer J Beier D (2004) Genetic evidence for histidine kinase HP165 being an acid sensor of Helicobacter pylori. FEMS Microbiol Lett 234 : 51 61.
65. Pflock M, Kennard S, Delany I et al 2005) Acid-induced activation of the urease promoters is mediated directly by the ArsRS two-component system of Helicobacter pylori. Infect Immun 73 : 6437 6445.
66. Pflock M, Finsterer N, Joseph B et al 2006a) Characterization of the ArsRS regulon of Helicobacter pylori, involved in acid adaptation. J Bacteriol 188 : 3449 3462.
67. Pflock M, Kennard S, Finsterer N Beier D (2006b) Acid-responsive gene regulation in the human pathogen Helicobacter pylori. J Biotechnol 126 : 52 60.
68. Salama N, Guillemin K, McDaniel TK et al 2000) A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc Natl Acad Sci USA 97 : 14668 14673.
69. Salaun L, Linz B, Suerbaum S Saunders NJ (2004) The diversity within an expanded and redefined repertoire of phase-variable genes in Helicobacter pylori. Microbiology 150 : 817 830.
70. Saunders NJ, Boonmee P, Peden JF Jarvis SA (2005) Inter-species horizontal transfer resulting in core-genome and niche-adaptive variation within Helicobacter pylori. BMC Genomics 6 : 9.
71. Schreiber S, Konradt M, Groll C et al 2004) The spatial orientation of Helicobacter pylori in the gastric mucus. Proc Natl Acad Sci USA 101 : 5024 5029.
72. Skouloubris S, Labigne A De Reuse H (1997) Identification and characterization of an aliphatic amidase in Helicobacter pylori. Mol Microbiol 25 : 989 998.
73. Skouloubris S, Labigne A De Reuse H (2001) The AmiE aliphatic amidase and AmiF formamidase of Helicobacter pylori: natural evolution of two enzyme paralogs. Mol Microbiol 40 : 596 609.
74. Solnick JV, Hansen LM, Salama NR et al 2004) Modification of Helicobacter pylori outer membrane protein expression during experimental infection of rhesus macaques. Proc Natl Acad Sci USA 101 : 2106 2111.
75. Sommi P, Ricci V, Fiocca R et al 1996) Significance of ammonia in the genesis of gastric epithelial lesions induced by Helicobacter pylori: an in vitro study with different bacterial strains and urea concentrations. Digestion 57 : 299 304.
76. Stingl K De Reuse H (2005) Staying alive overdosed: how does Helicobacter pylori control urease activity? Int J Med Microbiol 295 : 307 315.
77. Suerbaum S Achtman M (2004) Helicobacter pylori recombination, population structure and human migrations. Int J Med Microbiol 294 : 133 139.
78. Suerbaum S Michetti P (2002) Helicobacter pylori infection. N Engl J Med 347 : 1175 1186.
79. Suerbaum S, Smith JM, Bapumia K et al 1998) Free recombination within Helicobacter pylori. Proc Natl Acad Sci USA 95 : 12619 12624.
80. Suerbaum S, Josenhans C, Sterzenbach T et al 2004) The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc Natl Acad Sci USA 100 : 7901 7906.
81. Thompson L, Merrell DS, Neilan BA et al 2003) Gene expression profiling of Helicobacter pylori reveals a growth-phase-dependent switch in virulence gene expression. Infect Immun 71 : 2643 2655.
82. Tomb JF, White O, Kerlavage AR, Clayton RA et al 1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388 : 539 547.
83. van Vliet AH, Kuipers EJ, Stoof J et al 2004a) Acid-responsive gene induction of ammonia-producing enzymes in Helicobacter pylori is mediated via a metal-responsive repressor cascade. Infect Immun 72 : 766 773.
84. van Vliet AHM, Bereswill S Kusters JG (2001) Ion metabolism and transport. Helicobacter pylori: Physiology and genetics (Mobley HL, Mendz GL Hazell SL, ed), pp. 193 206. ASM Press, Washington, DC.
85. van Vliet AHM, Stoof J, Poppelaars SW et al 2003) Differential regulation of amidase- and formamidase-mediated ammonia production by the Helicobacter pylori Fur repressor. J Biol Chem 278 : 9052 9057.
86. van Vliet AHM, Ernst FD Kusters JG (2004b) NikR-mediated regulation of Helicobacter pylori acid adaptation. Trends Microbiol 12 : 489 494.
87. Waidner B, Melchers K, Stähler FN et al 2005) The Helicobacter pylori CrdRS two-component regulation system (HP1364/HP1365) is required for copper-mediated induction of the copper resistance determinant CrdA. J Bacteriol 187 : 4683 4688.
88. Wen Y, Marcus EA, Matrubutham U et al 2003) Acid-adaptive genes of Helicobacter pylori. Infect Immun 71 : 5921 5939.
89. Wen Y, Feng J, Scott DR et al 2006) Involvement of the HP0165-HP0166 two-component system in expression of some acidic-pH-upregulated genes of Helicobacter pylori. J Bacteriol 188 : 1750 1761.
90. Wirth T, Wang X, Linz B et al 2004) Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh. Proc Natl Acad Sci USA 101 : 4746 4751.