Genetic adaptation of the antibacterial human innate immunity network

详细信息    查看全文

• 作者：Ferran Casals (1) (2)
  Martin Sikora (1) (6)
  Hafid Laayouni (1)
  Ludovica Montanucci (1)
  Aura Muntasell (3)
  Ross Lazarus (4)
  Francesc Calafell (1)
  Philip Awadalla (2)
  Mihai G Netea (5)
  Jaume Bertranpetit (1)
  
• 刊名：BMC Evolutionary Biology
• 出版年：2011
• 出版时间：December 2011
• 年：2011
• 卷：11
• 期：1
• 全文大小：2691KB
• 参考文献：1. Andres AM, Hubisz MJ, Indap A, Torgerson DG, Degenhardt JD, Boyko AR, Gutenkunst RN, White TJ, Green ED, Bustamante CD, / et al.: Targets of balancing selection in the human genome. / Mol Biol Evol 2009,26(12):2755鈥?764. CrossRef
  2. Pickrell JK, Coop G, Novembre J, Kudaravalli S, Li JZ, Absher D, Srinivasan BS, Barsh GS, Myers RM, Feldman MW, / et al.: Signals of recent positive selection in a worldwide sample of human populations. / Genome Res 2009,19(5):826鈥?37. CrossRef
  3. Tang K, Thornton KR, Stoneking M: A new approach for using genome scans to detect recent positive selection in the human genome. / PLoS Biol 2007,5(7):e171. CrossRef
  4. Voight BF, Kudaravalli S, Wen X, Pritchard JK: A map of recent positive selection in the human genome. / PLoS Biol 2006,4(3):e72. CrossRef
  5. Wang ET, Kodama G, Baldi P, Moyzis RK: Global landscape of recent inferred Darwinian selection for Homo sapiens. / Proc Natl Acad Sci USA 2006,103(1):135鈥?40. CrossRef
  6. Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, Nielsen R: Localizing recent adaptive evolution in the human genome. / PLoS Genet 2007,3(6):e90. CrossRef
  7. Barreiro LB, Quintana-Murci L: From evolutionary genetics to human immunology: how selection shapes host defence genes. / Nat Rev Genet 2010,11(1):17鈥?0. CrossRef
  8. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A, Mikkelsen TS, Altshuler D, Lander ES: Positive natural selection in the human lineage. / Science 2006,312(5780):1614鈥?620. CrossRef
  9. Barreiro LB, Patin E, Neyrolles O, Cann HM, Gicquel B, Quintana-Murci L: The heritage of pathogen pressures and ancient demography in the human innate-immunity CD209/CD209L region. / Am J Hum Genet 2005,77(5):869鈥?86. CrossRef
  10. Cagliani R, Fumagalli M, Riva S, Pozzoli U, Comi GP, Menozzi G, Bresolin N, Sironi M: The signature of long-standing balancing selection at the human defensin beta-1 promoter. / Genome Biol 2008,9(9):R143. CrossRef
  11. Ferrer-Admetlla A, Bosch E, Sikora M, Marques-Bonet T, Ramirez-Soriano A, Muntasell A, Navarro A, Lazarus R, Calafell F, Bertranpetit J, / et al.: Balancing selection is the main force shaping the evolution of innate immunity genes. / J Immunol 2008,181(2):1315鈥?322.
  12. Fumagalli M, Cagliani R, Pozzoli U, Riva S, Comi GP, Menozzi G, Bresolin N, Sironi M: A population genetics study of the Familial Mediterranean Fever gene: evidence of balancing selection under an overdominance regime. / Genes Immun 2009.
  13. Fumagalli M, Pozzoli U, Cagliani R, Comi GP, Riva S, Clerici M, Bresolin N, Sironi M: Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. / J Exp Med 2009,206(6):1395鈥?408. CrossRef
  14. Cagliani R, Fumagalli M, Biasin M, Piacentini L, Riva S, Pozzoli U, Bonaglia MC, Bresolin N, Clerici M, Sironi M: Long-term balancing selection maintains trans-specific polymorphisms in the human TRIM5 gene. / Hum Genet 2010.
  15. Fumagalli M, Cagliani R, Riva S, Pozzoli U, Biasin M, Piacentini L, Comi GP, Bresolin N, Clerici M, Sironi M: Population genetics of IFIH1: ancient population structure, local selection and implications for susceptibility to type 1 diabetes. / Mol Biol Evol 2010.
  16. Alvarez-Ponce D, Aguade M, Rozas J: Network-level molecular evolutionary analysis of the insulin/TOR signal transduction pathway across 12 Drosophila genomes. / Genome Res 2009,19(2):234鈥?42. CrossRef
  17. Kim PM, Korbel JO, Gerstein MB: Positive selection at the protein network periphery: evaluation in terms of structural constraints and cellular context. / Proc Natl Acad Sci USA 2007,104(51):20274鈥?0279. CrossRef
  18. Fumagalli M, Pozzoli U, Cagliani R, Comi GP, Bresolin N, Clerici M, Sironi M: Genome-wide identification of susceptibility alleles for viral infections through a population genetics approach. / PLoS Genet 2010,6(2):e1000849. CrossRef
  19. Pozzoli U, Fumagalli M, Cagliani R, Comi GP, Bresolin N, Clerici M, Sironi M: The role of protozoa-driven selection in shaping human genetic variability. / Trends Genet 2010,26(3):95鈥?9. CrossRef
  20. Lazarus R, Vercelli D, Palmer LJ, Klimecki WJ, Silverman EK, Richter B, Riva A, Ramoni M, Martinez FD, Weiss ST, / et al.: Single nucleotide polymorphisms in innate immunity genes: abundant variation and potential role in complex human disease. / Immunol Rev 2002, 190:9鈥?5. CrossRef
  21. Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. / Nucleic Acids Res 1994,22(22):4673鈥?680. CrossRef
  22. Tajima F: Evolutionary relationship of DNA sequences in finite populations. / Genetics 1983,105(2):437鈥?60.
  23. Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. / Genetics 1989,123(3):585鈥?95.
  24. Fu YX, Li WH: Statistical tests of neutrality of mutations. / Genetics 1993,133(3):693鈥?09.
  25. Zeng K, Fu YX, Shi S, Wu CI: Statistical tests for detecting positive selection by utilizing high-frequency variants. / Genetics 2006,174(3):1431鈥?439. CrossRef
  26. Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. / Bioinformatics 2009,25(11):1451鈥?452. CrossRef
  27. Ramos-Onsins SE, Puerma E, Balana-Alcaide D, Salguero D, Aguade M: Multilocus analysis of variation using a large empirical data set: phenylpropanoid pathway genes in Arabidopsis thaliana. / Mol Ecol 2008,17(5):1211鈥?223. CrossRef
  28. Schaffner SF, Foo C, Gabriel S, Reich D, Daly MJ, Altshuler D: Calibrating a coalescent simulation of human genome sequence variation. / Genome Res 2005,15(11):1576鈥?583. CrossRef
  29. Gao J, Ade AS, Tarcea VG, Weymouth TE, Mirel BR, Jagadish HV, States DJ: Integrating and annotating the interactome using the MiMI plugin for cytoscape. / Bioinformatics 2009,25(1):137鈥?38. CrossRef
  30. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T: Cytoscape: a software environment for integrated models of biomolecular interaction networks. / Genome Res 2003,13(11):2498鈥?504. CrossRef
  31. Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M: Computing topological parameters of biological networks. / Bioinformatics 2008,24(2):282鈥?84. CrossRef
  32. Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW: Evolutionary rate in the protein interaction network. / Science 2002,296(5568):750鈥?52. CrossRef
  33. Csete M, Doyle J: Bow ties, metabolism and disease. / Trends Biotechnol 2004,22(9):446鈥?50. CrossRef
  34. Ma H, Zeng AP: Reconstruction of metabolic networks from genome data and analysis of their global structure for various organisms. / Bioinformatics 2003,19(2):270鈥?77. CrossRef
  35. Ma HW, Zeng AP: The connectivity structure, giant strong component and centrality of metabolic networks. / Bioinformatics 2003,19(11):1423鈥?430. CrossRef
  36. Oda K, Kitano H: A comprehensive map of the toll-like receptor signaling network. / Mol Syst Biol 2006, 2:2006 0015. CrossRef
  37. Zhai W, Nielsen R, Slatkin M: An investigation of the statistical power of neutrality tests based on comparative and population genetic data. / Mol Biol Evol 2009,26(2):273鈥?83. CrossRef
  38. Barreiro LB, Ben-Ali M, Quach H, Laval G, Patin E, Pickrell JK, Bouchier C, Tichit M, Neyrolles O, Gicquel B, / et al.: Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. / PLoS Genet 2009,5(7):e1000562. CrossRef
  39. Carlson CS, Thomas DJ, Eberle MA, Swanson JE, Livingston RJ, Rieder MJ, Nickerson DA: Genomic regions exhibiting positive selection identified from dense genotype data. / Genome Res 2005,15(11):1553鈥?565. CrossRef
  40. Enard D, Depaulis F, Roest Crollius H: Human and non-human primate genomes share hotspots of positive selection. / PLoS Genet 2010,6(2):e1000840. CrossRef
  41. Andres AM, Dennis MY, Kretzschmar WW, Cannons JL, Lee-Lin SQ, Hurle B, Schwartzberg PL, Williamson SH, Bustamante CD, Nielsen R, / et al.: Balancing selection maintains a form of ERAP2 that undergoes nonsense-mediated decay and affects antigen presentation. / PLoS Genet 2010,6(10):e1001157. CrossRef
  42. Cagliani R, Riva S, Biasin M, Fumagalli M, Pozzoli U, Lo Caputo S, Mazzotta F, Piacentini L, Bresolin N, Clerici M, / et al.: Genetic diversity at endoplasmic reticulum aminopeptidases is maintained by balancing selection and is associated with natural resistance to HIV-1 infection. / Hum Mol Genet 2010,19(23):4705鈥?714. CrossRef
  43. Calafell F, Roubinet F, Ramirez-Soriano A, Saitou N, Bertranpetit J, Blancher A: Evolutionary dynamics of the human ABO gene. / Hum Genet 2008,124(2):123鈥?35. CrossRef
  44. Ferrer-Admetlla A, Sikora M, Laayouni H, Esteve A, Roubinet F, Blancher A, Calafell F, Bertranpetit J, Casals F: A natural history of FUT2 polymorphism in humans. / Mol Biol Evol 2009,26(9):1993鈥?003. CrossRef
  45. Fumagalli M, Cagliani R, Pozzoli U, Riva S, Comi GP, Menozzi G, Bresolin N, Sironi M: Widespread balancing selection and pathogen-driven selection at blood group antigen genes. / Genome Res 2008.
  46. Dinarello CA: Immunological and inflammatory functions of the interleukin-1 family. / Annu Rev Immunol 2009, 27:519鈥?50. CrossRef
  47. Mukherjee S, Sarkar-Roy N, Wagener DK, Majumder PP: Signatures of natural selection are not uniform across genes of innate immune system, but purifying selection is the dominant signature. / Proc Natl Acad Sci USA 2009,106(17):7073鈥?078. CrossRef
  48. Akira S, Uematsu S, Takeuchi O: Pathogen recognition and innate immunity. / Cell 2006,124(4):783鈥?01. CrossRef
  49. Krieg AM: CpG motifs in bacterial DNA and their immune effects. / Annu Rev Immunol 2002, 20:709鈥?60. CrossRef
  50. Kitano H: Biological robustness. / Nat Rev Genet 2004,5(11):826鈥?37. CrossRef
  
• 作者单位：Ferran Casals (1) (2)
  Martin Sikora (1) (6)
  Hafid Laayouni (1)
  Ludovica Montanucci (1)
  Aura Muntasell (3)
  Ross Lazarus (4)
  Francesc Calafell (1)
  Philip Awadalla (2)
  Mihai G Netea (5)
  Jaume Bertranpetit (1)
  
  1. Institute of Evolutionary Biology (UPF-CSIC), CEXS - UPF - PRBB, Barcelona, Catalonia, Spain
  2. Centre de Recherche, CHU Sainte-Justine, Universit茅 de Montr茅al, Montr茅al, Qu茅bec, H3T 1C5, Canada
  6. Department of Genetics, Stanford University School of Medicine, Stanford, USA
  3. Unitat d鈥橧mmunologia, IMIM-Hospital del Mar, Barcelona, Catalonia, Spain
  4. Channing Laboratory, Department of Medicine, Brigham and Women鈥檚 Hospital, Harvard Medical School, Boston, MA, 02115, USA
  5. Department of Medicine, Radboud University Nijmegen Medical Center, 6500 HB, Nijmegen, The Netherlands
  

文摘

Background Pathogens have represented an important selective force during the adaptation of modern human populations to changing social and other environmental conditions. The evolution of the immune system has therefore been influenced by these pressures. Genomic scans have revealed that immune system is one of the functions enriched with genes under adaptive selection. Results Here, we describe how the innate immune system has responded to these challenges, through the analysis of resequencing data for 132 innate immunity genes in two human populations. Results are interpreted in the context of the functional and interaction networks defined by these genes. Nucleotide diversity is lower in the adaptors and modulators functional classes, and is negatively correlated with the centrality of the proteins within the interaction network. We also produced a list of candidate genes under positive or balancing selection in each population detected by neutrality tests and showed that some functional classes are preferential targets for selection. Conclusions We found evidence that the role of each gene in the network conditions the capacity to evolve or their evolvability: genes at the core of the network are more constrained, while adaptation mostly occurred at particular positions at the network edges. Interestingly, the functional classes containing most of the genes with signatures of balancing selection are involved in autoinflammatory and autoimmune diseases, suggesting a counterbalance between the beneficial and deleterious effects of the immune response.