Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2004 May 22;271(1543):1065–1072. doi: 10.1098/rspb.2004.2674

Evolution of the human ABO polymorphism by two complementary selective pressures.

Robert M Seymour 1, Martin J Allan 1, Andrew Pomiankowski 1, Kenth Gustafsson 1
PMCID: PMC1691687  PMID: 15293861

Abstract

The best-known example of terminal-glycan variation is the ABO histo-blood group polymorphism in humans. We model two selective forces acting on histo-blood group antigens that may account for this polymorphism. The first is generated by the invasion of opportunistic bacterial or other pathogens that interact with the epithelial-mucosal surfaces. The bacteria adapt to the microenvironments of common host phenotypes and so create frequency-dependent selection for rarer host alleles. The second is generated by intracellular viruses, and accounts for the observed differentials between the ABO-phenotype frequencies. It is thought that viruses acquire histo-blood group structures as part of their envelope from their previous host. The presence of host antigens on the viral envelope causes differential transmission of the virus between host types owing to the asymmetric action of ABO natural antibodies. Our model simulations show that these two forces acting together can account for the major features of the ABO polymorphism in humans.

Full Text

The Full Text of this article is available as a PDF (397.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aho K., Pyhälä R., Visakorpi R. ABO associated genetic determinant in H1N1 influenza. Tissue Antigens. 1980 Oct;16(4):310–313. doi: 10.1111/j.1399-0039.1980.tb00311.x. [DOI] [PubMed] [Google Scholar]
  2. Appelmelk B. J., Shiberu B., Trinks C., Tapsi N., Zheng P. Y., Verboom T., Maaskant J., Hokke C. H., Schiphorst W. E., Blanchard D. Phase variation in Helicobacter pylori lipopolysaccharide. Infect Immun. 1998 Jan;66(1):70–76. doi: 10.1128/iai.66.1.70-76.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arendrup M., Hansen J. E., Clausen H., Nielsen C., Mathiesen L. R., Nielsen J. O. Antibody to histo-blood group A antigen neutralizes HIV produced by lymphocytes from blood group A donors but not from blood group B or O donors. AIDS. 1991 Apr;5(4):441–444. doi: 10.1097/00002030-199104000-00014. [DOI] [PubMed] [Google Scholar]
  4. Balanzino L. E., Barra J. L., Monferran C. G., Cumar F. A. Differential interaction of Escherichia coli heat-labile toxin and cholera toxin with pig intestinal brush border glycoproteins depending on their ABH and related blood group antigenic determinants. Infect Immun. 1994 Apr;62(4):1460–1464. doi: 10.1128/iai.62.4.1460-1464.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berger S. A., Young N. A., Edberg S. C. Relationship between infectious diseases and human blood type. Eur J Clin Microbiol Infect Dis. 1989 Aug;8(8):681–689. doi: 10.1007/BF01963752. [DOI] [PubMed] [Google Scholar]
  6. Björkholm B., Lundin A., Sillén A., Guillemin K., Salama N., Rubio C., Gordon J. I., Falk P., Engstrand L. Comparison of genetic divergence and fitness between two subclones of Helicobacter pylori. Infect Immun. 2001 Dec;69(12):7832–7838. doi: 10.1128/IAI.69.12.7832-7838.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blackwell C. Caroline, Dundas Stephanie, James Valerie S., Mackenzie Doris A. C., Braun Jan M., Alkout Abdulhamid M., Todd W. T. Andrew, Elton Robert A., Weir Donald M. Blood group and susceptibility to disease caused by Escherichia coli O157. J Infect Dis. 2002 Jan 8;185(3):393–396. doi: 10.1086/338343. [DOI] [PubMed] [Google Scholar]
  8. Fischer C., Jock B., Vogel F. Interplay between humans and infective agents: a population genetic study. Hum Genet. 1998 Apr;102(4):415–422. doi: 10.1007/s004390050714. [DOI] [PubMed] [Google Scholar]
  9. Gagneux P., Varki A. Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology. 1999 Aug;9(8):747–755. doi: 10.1093/glycob/9.8.747. [DOI] [PubMed] [Google Scholar]
  10. Glass R. I., Holmgren J., Haley C. E., Khan M. R., Svennerholm A. M., Stoll B. J., Belayet Hossain K. M., Black R. E., Yunus M., Barua D. Predisposition for cholera of individuals with O blood group. Possible evolutionary significance. Am J Epidemiol. 1985 Jun;121(6):791–796. doi: 10.1093/oxfordjournals.aje.a114050. [DOI] [PubMed] [Google Scholar]
  11. Henry S. M. Molecular diversity in the biosynthesis of GI tract glycoconjugates. A blood-group-related chart of microorganism receptors. Transfus Clin Biol. 2001 Jun;8(3):226–230. doi: 10.1016/s1246-7820(01)00112-4. [DOI] [PubMed] [Google Scholar]
  12. Henry S., Oriol R., Samuelsson B. Lewis histo-blood group system and associated secretory phenotypes. Vox Sang. 1995;69(3):166–182. doi: 10.1111/j.1423-0410.1995.tb02591.x. [DOI] [PubMed] [Google Scholar]
  13. Hutson Anne M., Atmar Robert L., Marcus Donald M., Estes Mary K. Norwalk virus-like particle hemagglutination by binding to h histo-blood group antigens. J Virol. 2003 Jan;77(1):405–415. doi: 10.1128/JVI.77.1.405-415.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Karlsson K. A. Meaning and therapeutic potential of microbial recognition of host glycoconjugates. Mol Microbiol. 1998 Jul;29(1):1–11. doi: 10.1046/j.1365-2958.1998.00854.x. [DOI] [PubMed] [Google Scholar]
  15. Lindesmith Lisa, Moe Christine, Marionneau Severine, Ruvoen Nathalie, Jiang Xi, Lindblad Lauren, Stewart Paul, LePendu Jacques, Baric Ralph. Human susceptibility and resistance to Norwalk virus infection. Nat Med. 2003 Apr 14;9(5):548–553. doi: 10.1038/nm860. [DOI] [PubMed] [Google Scholar]
  16. Marionneau S., Cailleau-Thomas A., Rocher J., Le Moullac-Vaidye B., Ruvoën N., Clément M., Le Pendu J. ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie. 2001 Jul;83(7):565–573. doi: 10.1016/s0300-9084(01)01321-9. [DOI] [PubMed] [Google Scholar]
  17. Moran A. P., Prendergast M. M., Appelmelk B. J. Molecular mimicry of host structures by bacterial lipopolysaccharides and its contribution to disease. FEMS Immunol Med Microbiol. 1996 Dec 1;16(2):105–115. doi: 10.1111/j.1574-695X.1996.tb00127.x. [DOI] [PubMed] [Google Scholar]
  18. Mourant A. E. Recent advances in the study of associations between infection and genetic markers. FEMS Microbiol Immunol. 1989 Jun;1(6-7):317–319. doi: 10.1111/j.1574-6968.1989.tb02416.x. [DOI] [PubMed] [Google Scholar]
  19. Naikhin A. N., Katorgina L. G., Tsaritsyna I. M., Kim T. N., Reznik V. N., Trusov N. V., Denisov G. M. Pokazateli kollektivnogo immuniteta k grippu v zavisimosti ot gruppi krovi i pola obsleduemogo naseleniia. Vopr Virusol. 1989 Jul-Aug;34(4):419–423. [PubMed] [Google Scholar]
  20. Oriol R., Candelier J. J., Taniguchi S., Balanzino L., Peters L., Niekrasz M., Hammer C., Cooper D. K. Major carbohydrate epitopes in tissues of domestic and African wild animals of potential interest for xenotransplantation research. Xenotransplantation. 1999 May;6(2):79–89. doi: 10.1034/j.1399-3089.1999.00008.x. [DOI] [PubMed] [Google Scholar]
  21. Pfennig K. S. Evolution of pathogen virulence: the role of variation in host phenotype. Proc Biol Sci. 2001 Apr 7;268(1468):755–760. doi: 10.1098/rspb.2000.1582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Preece Andrew F., Strahan Karen M., Devitt James, Yamamoto Fumi-ichiro, Gustafsson Kenth. Expression of ABO or related antigenic carbohydrates on viral envelopes leads to neutralization in the presence of serum containing specific natural antibodies and complement. Blood. 2002 Apr 1;99(7):2477–2482. doi: 10.1182/blood.v99.7.2477. [DOI] [PubMed] [Google Scholar]
  23. Prizont R., Reed W. P. Differences in blood group B-specific mucinase activity between virulent and avirulent Shigella flexneri 2a strains. Microb Pathog. 1991 Aug;11(2):129–135. doi: 10.1016/0882-4010(91)90006-v. [DOI] [PubMed] [Google Scholar]
  24. Rad Roland, Gerhard Markus, Lang Roland, Schöniger Martin, Rösch Thomas, Schepp Wolfgang, Becker Ingrid, Wagner Hermann, Prinz Christian. The Helicobacter pylori blood group antigen-binding adhesin facilitates bacterial colonization and augments a nonspecific immune response. J Immunol. 2002 Mar 15;168(6):3033–3041. doi: 10.4049/jimmunol.168.6.3033. [DOI] [PubMed] [Google Scholar]
  25. Ravn V., Dabelsteen E. Tissue distribution of histo-blood group antigens. APMIS. 2000 Jan;108(1):1–28. doi: 10.1034/j.1600-0463.2000.d01-1.x. [DOI] [PubMed] [Google Scholar]
  26. SPRINGER G. F. Influenza virus vaccine and blood group A-like substances. Transfusion. 1963 May-Jun;3:233–236. doi: 10.1111/j.1537-2995.1963.tb04633.x. [DOI] [PubMed] [Google Scholar]
  27. SPRINGER G. F., SCHUSTER R. BLUTGRUPPEN A-AEHNLICHE FORSSMAN-ANTIGENE IN HUEHNEREI GEZUECHTETEN MYXOVIREN: IHRE MOEGLICHE PATHOGENETISCHE BEDEUTUNG IN IMPFSTOFFEN. Klin Wochenschr. 1964 Aug 15;42:821–823. doi: 10.1007/BF01479140. [DOI] [PubMed] [Google Scholar]
  28. Sinha A. K., Bhattacharya S. K., Sen D., Dutta P., Dutta D., Bhattacharya M. K., Pal S. C. Blood group and shigellosis. J Assoc Physicians India. 1991 Jun;39(6):452–453. [PubMed] [Google Scholar]
  29. Springer G. F., Horton R. E. Blood group isoantibody stimulation in man by feeding blood group-active bacteria. J Clin Invest. 1969 Jul;48(7):1280–1291. doi: 10.1172/JCI106094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Swerdlow D. L., Mintz E. D., Rodriguez M., Tejada E., Ocampo C., Espejo L., Barrett T. J., Petzelt J., Bean N. H., Seminario L. Severe life-threatening cholera associated with blood group O in Peru: implications for the Latin American epidemic. J Infect Dis. 1994 Aug;170(2):468–472. doi: 10.1093/infdis/170.2.468. [DOI] [PubMed] [Google Scholar]
  31. Takeuchi Y., Liong S. H., Bieniasz P. D., Jäger U., Porter C. D., Friedman T., McClure M. O., Weiss R. A. Sensitization of rhabdo-, lenti-, and spumaviruses to human serum by galactosyl(alpha1-3)galactosylation. J Virol. 1997 Aug;71(8):6174–6178. doi: 10.1128/jvi.71.8.6174-6178.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Takeuchi Y., Porter C. D., Strahan K. M., Preece A. F., Gustafsson K., Cosset F. L., Weiss R. A., Collins M. K. Sensitization of cells and retroviruses to human serum by (alpha 1-3) galactosyltransferase. Nature. 1996 Jan 4;379(6560):85–88. doi: 10.1038/379085a0. [DOI] [PubMed] [Google Scholar]
  33. Yamamoto F., Clausen H., White T., Marken J., Hakomori S. Molecular genetic basis of the histo-blood group ABO system. Nature. 1990 May 17;345(6272):229–233. doi: 10.1038/345229a0. [DOI] [PubMed] [Google Scholar]
  34. Zweibaum A., Bouhou E. Studies of digestive groups. I. The A alloantigen-alloantibody system in rabbits. Transplantation. 1973 Mar;15(3):291–293. [PubMed] [Google Scholar]
  35. Zweibaum A., Oriol R., Feingold N., Dussaulx E., Rousset M., Chevalier G. Studies on canine secretory alloantigens (CSA). Tissue Antigens. 1974;4(2):115–129. doi: 10.1111/j.1399-0039.1974.tb00232.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES