Role of ABO secretor status in mucosal innate immunity and H. pylori infection

PLoS Pathogens

Volumn 4, Issue 1, 2008, Pages 0006-0013

  Lindén, Sara ^a,b,c   Mahdavi, Jafar ^d   Semino Mora, Cristina ^a,b   Olsen, Cara ^a   Carlstedt, Ingemar ^e   Borén, Thomas ^f   Dubois, Andre ^a,b  

^a Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

^b United States Military Cancer Institute   (United States)

^c MATER MEDICAL RESEARCH INSTITUTE   (Australia)

^d QUEEN S MEDICAL CENTRE   (United Kingdom)

^e LUND UNIVERSITY   (Sweden)

^f UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD GROUP ABH ANTIGEN; BLOOD GROUP ANTIGEN; LEWIS A ANTIGEN; LEWIS B ANTIGEN; UNCLASSIFIED DRUG;

ARTICLE; BLOOD GROUP ABO SYSTEM; BLOOD GROUP B; BLOOD GROUP LEWIS SYSTEM; FUCOSYLATION; GASTRITIS; GLYCOSYLATION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOST BACTERIAL INTERACTION; HUMAN; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INFECTION RESISTANCE; INFLAMMATION; INNATE IMMUNITY; INTESTINE EPITHELIUM; MOLECULAR INTERACTION; MOLECULAR MODEL; MONKEY; NONHUMAN; PHENOTYPE; RHESUS MONKEY; SALIVATION; SIALYLATION; STOMACH BIOPSY; STOMACH MUCOSA; ANIMAL; GENETICS; IMMUNOLOGY; MACACA; MUCOSAL IMMUNITY; SECRETIONS;

ANIMALIA; BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI; MACACA MULATTA; PRIMATES;

ABO BLOOD-GROUP SYSTEM; ANIMALS; BODILY SECRETIONS; GASTRIC MUCOSA; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; IMMUNITY, MUCOSAL; IMMUNITY, NATURAL; IMMUNOHISTOCHEMISTRY; LEWIS BLOOD-GROUP SYSTEM; MACACA MULATTA; PHENOTYPE;

EID: 38949194318     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0040002     Document Type: Article

References (49)

1. Boren 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.
2. Mahdavi J, Sonden B, Hurtig M, Olfat FO, Forsberg L, et al. (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297: 573-578.
3. Aspholm-Hurtig M, Dailide G, Lahmann M, Kalia A, Ilver D, et al. (2004) Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305: 519-522.
4. Lindén S, Nordman H, Hedenbro J, Hurtig M, Boren T, et al. (2002) Strain-and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology 123: 1923-1930.
5. Ilver D, Arnqvist A, Ogren J, Frick IM, Kersulyte D, et al. (1998) Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279: 373-377.
6. Gerhard M, Lehn N, Neumayer N, Boren T, Rad R, 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.
7. Prinz C, Schoniger M, Rad R, Becker I, Keiditsch E, et al. (2001) Key importance of the Helicobacter pylori adherence factor blood group antigen binding adhesin during chronic gastric inflammation. Cancer Res 61: 1903-1909.
8. Peek RM, Blaser MJ (2002) Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2: 28-37.
9. Kobayashi M, Mitoma J, Nakamura N, Katsuyama T, Nakayama J, et al. (2004) Induction of peripheral lymph node addressin in human gastric mucosa infected by Helicobacter pylori. Proc Natl Acad Sci U S A 101: 17807-17812.
10. Unemo M, Aspholm-Hurtig M, Ilver D, Bergstrom J, Boren T, et al. (2005) The sialic acid binding SabA adhesin of Helicobacter pylori is essential for nonopsonic activation of human neutrophils. J Biol Chem 280: 15390-15397.
11. Henry S, Oriol R, Samuelsson B (1995) Lewis histo-blood group system and associated secretory phenotypes. Vox Sang 69: 166-182.
12. Clausen H, Hakomori S (1989) ABH and related histo-blood group antigens; immunochemical differences in carrier isotypes and their distribution. Vox Sang 56: 1-20.
13. Kelly RJ, Rouquier S, Giorgi D, Lennon GG, Lowe JB (1995) Sequence and expression of a candidate for the human Secretor blood group alpha(1,2) fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. J Biol Chem 270: 4640-4649.
14. Linden S, Mahdavi J, Hedenbro J, Boren T, Carlstedt I (2004) Effects of pH on Helicobacter pylori binding to human gastric mucins: identification of binding to non-MUC5AC mucins. Biochem J 384: 263-270.
15. Lindén S, Borén T, Dubois A, Carlstedt I (2004) Rhesus monkey gastric mucins: Oligomeric structure, glycoforms and Helicobacter pylori binding. Biochem J 379: 765-775.
16. Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS (2003) Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 278: 14112-14120.
17. Linden S, Mahdavi J, Hedenbro J, Boren T, Carlstedt I (2004) Effects of pH on Helicobacter pylori binding to human gastric mucins: identification of binding to non-MUC5AC mucins. Biochem J 384: 263-270.
18. Newburg DS, Ruiz-Palacios GM, Morrow AL (2005) Human milk glycans protect infants against enteric pathogens. Annu Rev Nutr 25: 37-58.
19. Stapleton AE, Stroud MR, Hakomori SI, Stamm WE (1998) The globoseries glycosphingolipid sialosyl galactosyl globoside is found in urinary tract tissues and is a preferred binding receptor In vitro for uropathogenic Escherichia coli expressing pap-encoded adhesins. Infect Immun 66: 3856-3861.
20. Lomberg H, Jodal U, Leffler H, De MP, Svanborg C (1992) Blood group non-secretors have an increased inflammatory response to urinary tract infection. Scand J Infect Dis 24: 77-83.
21. Aird I, Bentall HH, Mehigan JA, Roberts JA (1954) The blood groups in relation to peptic ulceration and carcinoma of colon, rectum, breast, and bronchus; an association between the ABO groups and peptic ulceration. Br Med J 4883: 315-321.
22. Mentis A, Blackwell CC, Weir DM, Spiliadis C, Dailianas A, et al. (1991) ABO blood group, secretor status and detection of Helicobacter pylori among patients with gastric or duodenal ulcers. Epidemiol Infect 106: 221-229.
23. Heneghan MA, Moran AP, Feeley KM, Egan EL, Goulding J, et al. (1998) Effect of host Lewis and ABO blood group antigen expression on Helicobacter pylori colonisation density and the consequent inflammatory response. FEMS Immunol Med Microbiol 20: 257-266.
24. Marionneau S, Airaud F, Bovin NV, Pendu JL, Ruvoen-Clouet N (2005) Influence of the combined ABO, FUT2, and FUT3 polymorphism on susceptibility to Norwalk virus attachment. J Infect Dis 192: 1071-1077.
25. Dubois A, Fiala N, Heman-Ackah LM, Drazek ES, Tarnawski A, et al. (1994) Natural gastric infection with Helicobacter pylori in monkeys. A model for human infection with spiral bacteria. Gastroenterology 106: 1405-1417.
26. Dubois A, Fiala N, Weichbrod RH, Ward GS, Nix M, et al. (1995) Seroepizootiology of Helicobacter pylori gastric infection in nonhuman primates housed in social environments. J Clinical Microbiol 33: 1492-1495.
27. Apoil PA, Roubinet F, Despiau S, Mollicone R, Oriol R, et al. (2000) Evolution of alpha 2-fucosyltransferase genes in primates: relation between an intronic Alu-Y element and red cell expression of ABH antigens. Mol Biol Evol 17: 337-351.
28. Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, et al. (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316: 222-234.
29. Dubois A, Berg D, Incecik E, Fiala N, Heman Ackah L, et al. (1999) Host specificity of Helicobacter pylori strains and host responses in experimentally challenged nonhuman primates. Gastroenterology 116: 90-96.
30. Aspholm M, Olfat FO, Norden J, Sonden B, Lundberg C, et al. (2006) SabA is the H. pylori hemagglutinin and is polymorphic in binding to sialylated glycans. LoS Pathog 2: e110. doi:10.1371/journal.ppat.0020110
31. Aspholm M, Kalia A, Ruhl S, Schedin S, Arnqvist A, et al. (2006) Helicobacter pylori adhesion to carbohydrates. Methods Enzymol 417: 293-339.
32. Mourant AE, Kopec AC, Domaniewska-Sobczak K (1976) The distribution of the human blood groups and other polymorphisms. London: Oxford University Press.
33. Malekasgar AM (2005) ABO blood group prevalence in spontaneously repeated abortion. Turk J Haematol 21: 181-187.
34. Hernandez RD, Hubisz MJ, Wheeler DA, Smith DG, Ferguson B, et al. (2007) Demographic histories and patterns of linkage disequilibrium in Chinese and Indian rhesus macaques. Science 316: 240-243.
35. Malaivijitnond S, Sae-Low W, Hamada Y (2007) The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand. J Med Primatol 37: 10.1111-1600-0684.
36. Seymour RM, Allan MJ, Pomiankowski A, Gustafsson K (2004) Evolution of the human ABO polymorphism by two complementary selective pressures. Proc Biol Sci 271: 1065-1072.
37. Glass RI, Holmgren J, Haley CE, Khan MR, Svennerholm AM, et al. (1985) Predisposition for cholera of individuals with O blood group. Possible evolutionary significance. Am J Epidemiol 121: 791-796.
38. Saitou N, Yamamoto F (1997) Evolution of primate ABO blood group genes and their homologous genes. Mol Biol Evol 14: 399-411.
39. Landsteiner K (1900) Zur Kenntnis der antifermentativen, lytischen und agglutinierenden Wirkungen des Blutserums und der Lymphe. Zentralblatt Bakteriologie 27: 357-362.
40. Morgan WT, Watkins WM (1969) Genetic and biochemical aspects of human blood-group A, B, H, Lea and Leb specificity. Br Med Bull 25: 30-34.
41. Kabat EA (1973) Immunological studies on the carbohydrate moiety of water-soluble blood group A, B, H, Lea, and Leb substances and their precursor i antigens. Carbohydrates in solution. Adv Chem Ser 117: 334-361.
42. Yamamoto F, Clausen H, White T, Marken J, Hakomori S (1990) Molecular genetic basis of the histo-blood group ABO system. Nature 345: 229-233.
43. Grubb R (1948) Correlation between Lewis blood group and secretor character in man. Nature 162: 728.
44. Smith EL, McKibbin JM, Karlsson KA, Pascher I, Samuelsson BE (1975) Characterization by mass spectrometry of blood group A active glycolipids from human and dog small intestins. Biochemistry 14: 2120-2124.
45. Greenwell P (1997) Blood group antigens: molecules seeking a function? Glycoconj J 14: 159-173.
46. Brown JR, Fuster MM, Whisenant T, Esko JD (2003) Expression patterns of alpha 2,3-sialyltransferases and alpha 1,3-flucosyltransferases determine the mode of sialyl Lewis X inhibition by disaccharide decoys. J Biol Chem 278: 23352-23359.
47. Bry L, Falk PG, Midtvedt T, Gordon JI (1996) A model of host-microbial interactions in an open mammalian ecosystem. Science 273: 1380-1383.
48. Kang W, Rathinavelu S, Samuelson LC, Merchant JL (2005) Interferon gamma induction of gastric mucous neck cell hypertrophy. Lab Invest 85: 702-715.
49. National Research Council (1996) Guide for the care and use of laboratory animals. Washington (D.C.): National Academy Press.