Table of Contents
International Journal of Evolutionary Biology
Volume 2013, Article ID 204240, 6 pages
http://dx.doi.org/10.1155/2013/204240
Review Article

Pathogen-Driven Selection in the Human Genome

Bioinformatics, Scientific Institute IRCCS E. Medea, 23842 Bosisio Parini (LC), Italy

Received 14 December 2012; Accepted 31 January 2013

Academic Editor: Stephane Boissinot

Copyright © 2013 Rachele Cagliani and Manuela Sironi. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. D. White, B. Asfaw, D. DeGusta et al., “Pleistocene Homo sapiens from Middle Awash, Ethiopia,” Nature, vol. 423, no. 6941, pp. 742–747, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. N. D. Wolfe, C. P. Dunavan, and J. Diamond, “Origins of major human infectious diseases,” Nature, vol. 447, no. 7142, pp. 279–283, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. A. P. Dobson and E. R. Carper, “Infectious diseases and human population history,” BioScience, vol. 46, no. 2, pp. 115–126, 1996. View at Google Scholar · View at Scopus
  4. J. Diamond, Guns, Germs, and Steel: The Fates of Human Society, Norton, New York, NY, USA, 1997, Edited by S. Jones, R. Martin, and D. Pilbeam.
  5. W. H. McNeill, Plagues and People, Anchor, Garden City, NY, USA, 1976.
  6. K. N. Harper, M. K. Zuckerman, M. L. Harper, J. D. Kingston, and G. J. Armelagos, “The origin and antiquity of syphilis revisited: an appraisal of Old World pre-Columbian evidence for treponemal infection,” American Journal of Physical Anthropology, vol. 146, supplement 53, pp. 99–133, 2011. View at Google Scholar
  7. J. B. S. Haldane, The Causes of Evolution, 1932.
  8. K. Dronamraju, Selected Genetic Papers of J.B.S. Haldane, 1990.
  9. M. Fumagalli, M. Sironi, U. Pozzoli, A. Ferrer-Admettla, L. Pattini, and R. Nielsen, “Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution,” PLOS Genetics, vol. 7, no. 11, Article ID e1002355, 2011. View at Google Scholar
  10. B. C. Verrelli, J. H. McDonald, G. Argyropoulos et al., “Evidence for balancing selection from nucleotide sequence analyses of human G6PD,” American Journal of Human Genetics, vol. 71, no. 5, pp. 1112–1128, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. M. T. Hamblin, E. E. Thompson, and A. Di Rienzo, “Complex signatures of natural selection at the Duffy blood group locus,” American Journal of Human Genetics, vol. 70, no. 2, pp. 369–383, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. D. P. Kwiatkowski, “How malaria has affected the human genome and what human genetics can teach us about malaria,” American Journal of Human Genetics, vol. 77, no. 2, pp. 171–192, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. A. G. Maier, M. T. Duraisingh, J. C. Reeder et al., “Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations,” Nature Medicine, vol. 9, no. 1, pp. 87–92, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. B. K. L. Sim, C. E. Chitnis, C. K. Wasniowska, T. J. Hadley, and L. H. Miller, “Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum,” Science, vol. 264, no. 5167, pp. 1941–1944, 1994. View at Google Scholar · View at Scopus
  15. J. A. Wilder, E. K. Hewett, and M. E. Gansner, “Molecular evolution of gypc: evidence for recent structural innovation and positive selection in humans,” Molecular Biology and Evolution, vol. 26, no. 12, pp. 2679–2687, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Baum, R. H. Ward, and D. J. Conway, “Natural selection on the erythrocyte surface,” Molecular Biology and Evolution, vol. 19, no. 3, pp. 223–229, 2002. View at Google Scholar · View at Scopus
  17. U. Pozzoli, M. Fumagalli, R. Cagliani et al., “The role of protozoa-driven selection in shaping human genetic variability,” Trends in Genetics, vol. 26, no. 3, pp. 95–99, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. O. O. Blumenfeld and S. K. Patnaik, “Allelic genes of blood group antigens: a source of human mutations and cSNPs documented in the blood droup antigen gene mutation database,” Human Mutation, vol. 23, no. 1, pp. 8–16, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. J. B. S. Haldane, “Disease and evolution. Symposium sui fattori ecologici e genetici della speciazione negli animali,” in Selected Genetic Papers of J. B. S. Haldane, pp. 325–334, Garland, New York, NY, USA, 1949. View at Google Scholar
  20. L. Hirschfeld and H. Hirschfeld, “Serological differences between the blood of different races. The result of researches on the macedonian front,” The Lancet, vol. 194, no. 5016, pp. 675–679, 1919. View at Google Scholar · View at Scopus
  21. N. Saitou and F. I. Yamamoto, “Evolution of primate ABO blood group genes and their homologous genes,” Molecular Biology and Evolution, vol. 14, no. 4, pp. 399–411, 1997. View at Google Scholar · View at Scopus
  22. F. Calafell, F. Roubinet, A. Ramírez-Soriano, N. Saitou, J. Bertranpetit, and A. Blancher, “Evolutionary dynamics of the human ABO gene,” Human Genetics, vol. 124, no. 2, pp. 123–135, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Segurel, E. E. Thompson, T. Flutre et al., “The ABO blood group is a trans-species polymorphism in primates,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, pp. 18493–218498, 2012. View at Publisher · View at Google Scholar
  24. A. Ferrer-Admetlla, M. Sikora, H. Laayouni et al., “A natural history of FUT2 polymorphism in humans,” Molecular Biology and Evolution, vol. 26, no. 9, pp. 1993–2003, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. A. E. Fry, M. J. Griffiths, S. Auburn et al., “Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria,” Human Molecular Genetics, vol. 17, no. 4, pp. 567–576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. J. A. Rowe, I. G. Handel, M. A. Thera et al., “Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 44, pp. 17471–17476, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Lindesmith, C. Moe, S. Marionneau et al., “Human susceptibility and resistance to Norwalk virus infection,” Nature Medicine, vol. 9, no. 5, pp. 548–553, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. G. M. Ruiz-Palacios, L. E. Cervantes, P. Ramos, B. Chavez-Munguia, and D. S. Newburg, “Campylobacter jejuni binds intestinal H(O) antigen (Fucα1, 2Galβ1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection,” Journal of Biological Chemistry, vol. 278, no. 16, pp. 14112–14120, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Boren, P. Falk, K. A. Roth, G. Larson, and S. Normark, “Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens,” Science, vol. 262, no. 5141, pp. 1892–1895, 1993. View at Google Scholar · View at Scopus
  30. J. B. Harris, A. I. Khan, R. C. LaRocque et al., “Blood group, immunity, and risk of infection with Vibrio cholerae in an area of endemicity,” Infection and Immunity, vol. 73, no. 11, pp. 7422–7427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Aspholm-Hurtig, G. Dailide, M. Lahmann et al., “Functional adaptation of BabA the H. pylori ABO blood group antigen binding adhesin,” Science, vol. 305, no. 5683, pp. 519–522, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Imberty and A. Varrot, “Microbial recognition of human cell surface glycoconjugates,” Current Opinion in Structural Biology, vol. 18, no. 5, pp. 567–576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Fumagalli, U. Pozzoli, R. Cagliani et al., “Genome-wide identification of susceptibility alleles for viral infections through a population genetics approach,” PLoS Genetics, vol. 6, no. 2, Article ID e1000849, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. J. M. Rojek, C. F. Spiropoulou, K. P. Campbell, and S. Kunz, “Old world and clade C new world arenaviruses mimic the molecular mechanism of receptor recognition used by α-dystroglycan's host-derived ligands,” Journal of Virology, vol. 81, no. 11, pp. 5685–5695, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Kunz, J. M. Rojek, M. Kanagawa et al., “Posttranslational modification of α-dystroglycan, the cellular receptor for arenaviruses, by the glycosyltransferase LARGE is critical for virus binding,” Journal of Virology, vol. 79, no. 22, pp. 14282–14296, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. P. C. Sabeti, P. Varilly, B. Fry et al., “Genome-wide detection and characterization of positive selection in human populations,” Nature, vol. 449, no. 7164, pp. 913–918, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. K. G. Andersen, I. Shylakhter, S. Tabrizi, S. R. Grossman, C. T. Happi, and P. C. Sabeti, “Genome-wide scans provide evidence for positive selection of genes implicated in Lassa fever,” Philosophical Transactions of the Royal Society, vol. 367, pp. 868–877, 2012. View at Google Scholar
  38. M. Yawata, N. Yawata, M. Draghi, A. M. Little, F. Partheniou, and P. Parham, “Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function,” Journal of Experimental Medicine, vol. 203, no. 3, pp. 633–645, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Uhrberg, N. M. Valiante, B. P. Shum et al., “Human diversity in killer cell inhibitory receptor genes,” Immunity, vol. 7, no. 6, pp. 753–763, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. A. L. Hughes and M. Nei, “Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 3, pp. 958–962, 1989. View at Google Scholar · View at Scopus
  41. A. L. Hughes and M. Nei, “Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection,” Nature, vol. 335, no. 6186, pp. 167–170, 1988. View at Google Scholar · View at Scopus
  42. M. Dean, M. Carrington, and S. J. O'Brien, “Balanced polymorphism selected by genetic versus infectious human disease,” Annual Review of Genomics and Human Genetics, vol. 3, pp. 263–292, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Takahata and M. Nei, “Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci,” Genetics, vol. 124, no. 4, pp. 967–978, 1990. View at Google Scholar · View at Scopus
  44. Y. Satta, C. O'Huigin, N. Takahata, and J. Klein, “Intensity of natural selection at the major histocompatibility complex loci,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 15, pp. 7184–7188, 1994. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Takahata, Y. Satta, and J. Klein, “Polymorphism and balancing selection at major histocompatibility complex loci,” Genetics, vol. 130, no. 4, pp. 925–938, 1992. View at Google Scholar · View at Scopus
  46. M. M. Miretti, E. C. Walsh, X. Ke et al., “A high-resolution linkage-disequilibrium map of the human major histocompatibility complex and first generation of tag single-nucleotide polymorphisms,” American Journal of Human Genetics, vol. 76, no. 4, pp. 634–646, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. W. E. Mayer, M. Jonker, D. Klein, P. Ivanyi, G. van Seventer, and J. Klein, “Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution,” The EMBO Journal, vol. 7, no. 9, pp. 2765–2774, 1988. View at Google Scholar · View at Scopus
  48. F. J. Ayala, “The myth of Eve: molecular biology and human origins,” Science, vol. 270, no. 5244, pp. 1930–1936, 1995. View at Google Scholar · View at Scopus
  49. F. Prugnolle, A. Manica, M. Charpentier, J. F. Guégan, V. Guernier, and F. Balloux, “Pathogen-driven selection and worldwide HLA class I diversity,” Current Biology, vol. 15, no. 11, pp. 1022–1027, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Chaix, C. Cao, and P. Donnelly, “Is mate choice in humans MHC-dependent?” PLoS Genetics, vol. 4, no. 9, Article ID e1000184, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Derti, C. Cenik, P. Kraft, and F. P. Roth, “Absence of evidence for MHC-dependent mate selection within HapMap populations,” PLoS Genetics, vol. 6, no. 4, Article ID e1000925, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Saveanu, O. Carroll, V. Lindo et al., “Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum,” Nature Immunology, vol. 6, no. 7, pp. 689–697, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. A. M. Andrés, M. Y. Dennis, W. W. Kretzschmar et al., “Balancing selection maintains a form of ERAP2 that undergoes nonsense-mediated decay and affects antigen presentation,” PLoS Genetics, vol. 6, no. 10, p. e1001157, 2010. View at Google Scholar · View at Scopus
  54. R. Cagliani, S. Riva, M. Biasin et al., “Genetic diversity at endoplasmic reticulum aminopeptidases is maintained by balancing selection and is associated with natural resistance to HIV-1 infection,” Human Molecular Genetics, vol. 19, no. 23, pp. 4705–4714, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Kim, S. Lee, J. Shin et al., “Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1,” Nature Immunology, vol. 12, pp. 984–991, 2011. View at Publisher · View at Google Scholar
  56. A. L. Brass, I. C. Huang, Y. Benita et al., “The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile Virus, and Dengue Virus,” Cell, vol. 139, no. 7, pp. 1243–1254, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. A. R. Everitt, S. Clare, T. Pertel et al., “IFITM3 restricts the morbidity and mortality associated with influenza,” Nature, vol. 484, no. 7395, pp. 519–523, 2012. View at Google Scholar
  58. P. C. Sabeti, S. F. Schaffner, B. Fry et al., “Positive natural selection in the human lineage,” Science, vol. 312, no. 5780, pp. 1614–1620, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. B. F. Voight, S. Kudaravalli, X. Wen, and J. K. Pritchard, “A map of recent positive selection in the human genome,” PLoS Biology, vol. 4, no. 3, p. e72, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. S. H. Williamson, M. J. Hubisz, A. G. Clark, B. A. Payseur, C. D. Bustamante, and R. Nielsen, “Localizing recent adaptive evolution in the human genome,” PLoS Genetics, vol. 3, no. 6, p. e90, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. L. B. Barreiro, G. Laval, H. Quach, E. Patin, and L. Quintana-Murci, “Natural selection has driven population differentiation in modern humans,” Nature Genetics, vol. 40, no. 3, pp. 340–345, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Tang, K. R. Thornton, and M. Stoneking, “A new approach for using genome scans to detect recent positive selection in the human genome,” PLoS Biology, vol. 5, no. 7, p. e171, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. A. M. Andrés, M. J. Hubisz, A. Indap et al., “Targets of balancing selection in the human genome,” Molecular Biology and Evolution, vol. 26, no. 12, pp. 2755–2764, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. E. Vasseur, M. Boniotto, E. Patin et al., “The evolutionary landscape of cytosolic microbial sensors in humans,” The American Journal of Human Genetics, vol. 91, pp. 27–37, 2012. View at Google Scholar
  65. W. H. Witola, E. Mui, A. Hargrave et al., “NALP1 influences susceptibility to human congenital toxoplasmosis, proinflammatory cytokine response, and fate of Toxoplasma gondii-infected monocytic cells,” Infection and Immunity, vol. 79, no. 2, pp. 756–766, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Swanberg, O. Lidman, L. Padyukov et al., “MHC2TA is associated with differential MHC molecule expression and susceptibility to rheumatoid arthritis, multiple sclerosis and myocardial infarction,” Nature Genetics, vol. 37, no. 5, pp. 486–494, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. L. Jostins, S. Ripke, R. K. Weersma et al., “Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease,” Nature, vol. 491, pp. 119–124, 2012. View at Publisher · View at Google Scholar