A changing gastric environment leads to adaptation of lipopolysaccharide variants in Helicobacter pylori populations during colonization

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Skoglund, Anna ^a,b   Bäckhed, Helene Kling ^a,b   Nilsson, Christina ^a,b,c   Björkholm, Britta ^b   Normark, Staffan ^a,b   Engstrand, Lars ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; EPITOPE; LIPOPOLYSACCHARIDE; PRIMER DNA;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATROPHIC GASTRITIS; BACTERIAL COLONIZATION; BACTERIUM ISOLATE; BLOOD GROUP LEWIS SYSTEM; CHRONIC GASTRITIS; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN TISSUE; IN VITRO STUDY; INFLAMMATION; MOUSE; NONHUMAN; PHENOTYPE; STOMACH ADENOCARCINOMA; STOMACH PH; ANIMAL; CASE CONTROL STUDY; CHEMISTRY; METABOLISM; MIDDLE AGED; PH;

HELICOBACTER PYLORI; MUS;

AGED; ANIMALS; CASE-CONTROL STUDIES; DISEASE PROGRESSION; DNA PRIMERS; EPITOPES; HELICOBACTER PYLORI; HUMANS; HYDROGEN-ION CONCENTRATION; INFLAMMATION; LEWIS BLOOD-GROUP SYSTEM; LIPOPOLYSACCHARIDES; MICE; MIDDLE AGED; PHENOTYPE;

EID: 67649968030     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005885     Document Type: Article

References (44)

1. Suerbaum S, Michetti P (2002) Helicobacter pylori infection. N Engl J Med 347: 1175-1186.
2. Correa P (2005) New strategies for the prevention of gastric cancer: Helicobacter pylori and genetic susceptibility. J Surg Oncol 90: 134-138. discussion 138.
3. Censini S, Lange C, Xiang Z, Crabtree JE, Ghiara P, 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.
4. Crabtree JE, Covacci A, Farmery SM, Xiang Z, Tompkins DS, et al. (1995) Helicobacter pylori induced interleukin-8 expression in gastric epithelial cells is associated with CagA positive phenotype. J Clin Pathol 48: 41-45.
5. Cover TL, Blanke SR (2005) Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol 3: 320-332.
6. Appelmelk BJ, Martin SL, Monteiro MA, Clayton CA, McColm AA, et al. (1999) Phase variation in Helicobacter pylori lipopolysaccharide due to changes in the lengths of poly(C) tracts in α3-fucosyltransferase genes. Infect Immun 67: 5361-5366.
7. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
8. Appelmelk BJ, Shiberu B, Trinks C, Tapsi N, Zheng PY, et al. (1998) Phase variation in Helicobacter pylori lipopolysaccharide. Infect Immun 66: 70-76.
9. Wang G, Ge Z, Rasko DA, Taylor DE (2000) Lewis antigens in Helicobacter pylori: biosynthesis and phase variation. Mol Microbiol 36: 1187-1196.
10. Lerouge I, Vanderleyden J (2002) O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol Rev 26: 17-47.
11. Moran AP (2008) Relevance of fucosylation and Lewis antigen expression in the bacterial gastroduodenal pathogen Helicobacter pylori. Carbohydr Res 343: 1952-1965.
12. Bergman MP, Engering A, Smits HH, van Vliet SJ, van Bodegraven AA, et al. (2004) Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J Exp Med 200: 979-990.
13. Heneghan MA, McCarthy CF, Moran AP (2000) Relationship of blood group determinants on Helicobacter pylori lipopolysaccharide with host lewis phenotype and inflammatory response. Infect Immun 68: 937-941.
14. Simoons-Smit IM, Appelmelk BJ, Verboom T, Negrini R, Penner JL, et al. (1996) Typing of Helicobacter pylori with monoclonal antibodies against Lewis antigens in lipopolysaccharide. J Clin Microbiol 34: 2196-2200.
15. Wirth HP, Yang M, Karita M, Blaser MJ (1996) Expression of the human cell surface glycoconjugates Lewis x and Lewis y by Helicobacter pylori isolates is related to cagA status. Infect Immun 64: 4598-4605.
16. Marshall DG, Hynes SO, Coleman DC, O'Morain CA, Smyth CJ, et al. (1999) Lack of a relationship between Lewis antigen expression and cagA, CagA, vacA and VacA status of Irish Helicobacter pylori isolates. FEMS Immunol Med Microbiol 24: 79-90.
17. Monteiro MA, Chan KH, Rasko DA, Taylor DE, Zheng PY, et al. (1998) Simultaneous expression of type 1 and type 2 Lewis blood group antigens by Helicobacter pylori lipopolysaccharides. Molecular mimicry between H. pylori lipopolysaccharides and human gastric epithelial cell surface glycoforms. J Biol Chem 273: 11533-11543.
18. Monteiro MA, Appelmelk BJ, Rasko DA, Moran AP, Hynes SO, et al. (2000) Lipopolysaccharide structures of Helicobacter pylori genomic strains 26695 and J99, mouse model H. pylori Sydney strain, H. pylori P466 carrying sialyl Lewis X, and H. pylori UA915 expressing Lewis B classification of H. pylori lipopolysaccharides into glycotype families. Eur J Biochem 267: 305-320.
19. Monteiro MA, Zheng P, Ho B, Yokota S, Amano K, et al. (2000) Expression of histo-blood group antigens by lipopolysaccharides of Helicobacter pylori strains from Asian hosts: the propensity to express type 1 blood-group antigens. Glycobiology 10: 701-713.
20. Ma B, Simala-Grant JL, Taylor DE (2006) Fucosylation in prokaryotes and eukaryotes. Glycobiology 16: 158R-184R.
21. Wang G, Rasko DA, Sherburne R, Taylor DE (1999) Molecular genetic basis for the variable expression of Lewis Y antigen in Helicobacter pylori: analysis of the α(1,2) fucosyltransferase gene. Mol Microbiol 31: 1265-1274.
22. Nilsson C, Skoglund A, Moran AP, Annuk H, Engstrand L, et al. (2006) An enzymatic ruler modulates Lewis antigen glycosylation of Helicobacter pylori LPS during persistent infection. Proc Natl Acad Sci U S A 103: 2863-2868.
23. Nilsson C, Skoglund A, Moran AP, Annuk H, Engstrand L, et al. (2008) Lipopolysaccharide diversity evolving in Helicobacter pylori communities through genetic modifications in fucosyltransferases. PLoS ONE 3: e3811.
24. Moran AP, Prendergast MM, Appelmelk BJ (1996) Molecular mimicry of host structures by bacterial lipopolysaccharides and its contribution to disease. FEMS Immunol Med Microbiol 16: 105-115.
25. Moran AP, Knirel YA, Senchenkova SN, Widmalm G, Hynes SO, et al. (2002) Phenotypic variation in molecular mimicry between Helicobacter pylori lipopolysaccharides and human gastric epithelial cell surface glycoforms. Acid-induced phase variation in Lewis(x) and Lewis(y) expression by H. pylori lipopolysaccharides. J Biol Chem 277: 5785-5795.
26. Keenan JI, Davis KA, Beaugie CR, McGovern JJ, Moran AP (2008) Alterations in Helicobacter pylori outer membrane and outer membrane vesicle-associated lipopolysaccharides under iron-limiting growth conditions. Innate Immun 14: 279-290.
27. Oh JD, Karam SM, Gordon JI (2005) Intracellular Helicobacter pylori in gastric epithelial progenitors. Proc Natl Acad Sci U S A 102: 5186-5191.
28. Broutet N, Moran A, Hynes S, Sakarovitch C, Megraud F (2002) Lewis antigen expression and other pathogenic factors in the presence of atrophic chronic gastritis in a European population. J Infect Dis 185: 503-512.
29. Björkholm B, Lundin A, Sillen A, Guillemin K, Salama N, et al. (2001) Comparison of genetic divergence and fitness between two subclones of Helicobacter pylori. Infect Immun 69: 7832-7838.
30. Kersulyte D, Chalkauskas H, Berg DE (1999) Emergence of recombinant strains of Helicobacter pylori during human infection. Mol Microbiol 31: 31-43.
31. Rasko DA, Keelan M, Wilson TJ, Taylor DE (2001) Lewis antigen expression by Helicobacter pylori. J Infect Dis 184: 315-321.
32. Syder AJ, Guruge JL, Li Q, Hu Y, Oleksiewicz CM, et al. (1999) Helicobacter pylori attaches to NeuAcα2,3Galβ1,4 glycoconjugates produced in the stomach of transgenic mice lacking parietal cells. Mol Cell 3: 263-274.
33. Wirth HP, Yang M, Sanabria-Valentin E, Berg DE, Dubois A, et al. (2006) Host Lewis phenotype-dependent Helicobacter pylori Lewis antigen expression in rhesus monkeys. FASEB J 20: 1534-1536.
34. Wirth HP, Yang M, Peek RM Jr., Tham KT, Blaser MJ (1997) Helicobacter pylori Lewis expression is related to the host Lewis phenotype. Gastroenterology 113: 1091-1098.
35. Taylor DE, Rasko DA, Sherburne R, Ho C, Jewell LD (1998) Lack of correlation between Lewis antigen expression by Helicobacter pylori and gastric epithelial cells in infected patients. Gastroenterology 115: 1113-1122.
36. Rasko DA, Wilson TJ, Zopf D, Taylor DE (2000) Lewis antigen expression and stability in Helicobacter pylori isolated from serial gastric biopsies. J Infect Dis 181: 1089-1095.
37. Kuipers EJ, Israel DA, Kusters JG, Gerrits MM, Weel J, et al. (2000) Quasispecies development of Helicobacter pylori observed in paired isolates obtained years apart from the same host. J Infect Dis 181: 273-282.
38. Vimr ER, Kalivoda KA, Deszo EL, Steenbergen SM (2004) Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68: 132-153.
39. Guerry P, Szymanski CM, Prendergast MM, Hickey TE, Ewing CP, et al. (2002) Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect Immun 70: 787-793.
40. McGowan CC, Necheva A, Thompson SA, Cover TL, Blaser MJ (1998) Acid-induced expression of an LPS-associated gene in Helicobacter pylori. Mol Microbiol 30: 19-31.
41. Oh JD, Kling-Bäckhed H, Giannakis M, Xu J, Fulton RS, et al. (2006) The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc Natl Acad Sci U S A 103: 9999-10004.
42. Enroth H, Kraaz W, Engstrand L, Nyren O, Rohan T (2000) Helicobacter pylori strain types and risk of gastric cancer: a case-control study. Cancer Epidemiol Biomarkers Prev 9: 981-985.
43. Aro P, Storskrubb T, Ronkainen J, Bolling-Sternevald E, Engstrand L, et al. (2006) Peptic ulcer disease in a general adult population: the Kalixanda study: a random population-based study. Am J Epidemiol 163: 1025-1034.
44. Storskrubb T, Aro P, Ronkainen J, Vieth M, Stolte M, 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.