Ancient and recent selective pressures shaped genetic diversity at AIM2-like nucleic acid sensors

Genome Biology and Evolution

Volumn 6, Issue 4, 2014, Pages 830-845

  Cagliani, Rachele ^a   Forni, Diego ^a   Biasin, Mara ^b   Comabella, Manuel ^c   Guerini, Franca R ^d   Riva, Stefania ^a   Pozzoli, Uberto ^a   Agliardi, Cristina ^d   Caputo, Domenico ^d   Malhotra, Sunny ^c   Montalban, Xavier ^c   Bresolin, Nereo ^a,b   Clerici, Mario ^b,d   Sironi, Manuela ^a  

^a SCIENTIFIC INSTITUTE   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^d IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

Author keywords

AIM2 like receptors; IFI16; Long standing balancing selection; Positive selection

Indexed keywords

DNA BINDING PROTEIN;

ANIMAL; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GORILLA; HUMAN; MACACA FASCICULARIS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; ORANG UTAN; PAN TROGLODYTES; PHYLOGENY;

ANIMALS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; COS CELLS; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GORILLA GORILLA; HUMANS; MACACA FASCICULARIS; MOLECULAR SEQUENCE DATA; PAN TROGLODYTES; PHYLOGENY; PONGO PYGMAEUS; SELECTION, GENETIC;

EID: 84901401406     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu066     Document Type: Article

References (78)

1. 1000 Genomes Project Consortium, et al. 2010. Amap of human genome variation from population-scale sequencing. Nature, 467, 1061-1073.
2. Anisimova M, Bielawski JP, Yang Z. 2002. Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol Biol Evol. 19:950-958.
3. Anisimova M, Nielsen R, Yang Z. 2003. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229-1236.
4. Bandelt HJ, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 16:37-48.
5. Barrett JC, Fry B, Maller J, Daly MJ. 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265.
6. Brunette RL, et al. 2012. Extensive evolutionary and functional diversity among mammalian AIM2-like receptors. J Exp Med. 209:1969-1983.
7. Burckstummer T, et al. 2009. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol. 10:266-272.
8. Cagliani R, et al. 2010. Long-term balancing selection maintains transspecific polymorphisms in the human TRIM5 gene. Hum Genet. 128:577-588.
9. Cagliani R, et al. 2011. Balancing selection is common in the extended MHC region but most alleleswith opposite risk profile for autoimmune diseases are neutrally evolving. BMC Evol Biol. 11:171.
10. Cagliani R, et al. 2012. A trans-specific polymorphism in ZC3HAV1 is maintained by long-standing balancing selection and may confer susceptibility to multiple sclerosis. Mol Biol Evol. 29:1599-1613.
11. Cereda M, Sironi M, Cavalleri M, Pozzoli U. 2011. GeCo++: aC++ library for genomic features computation and annotation in the presence of variants. Bioinformatics 27:1313-1315.
12. Charlesworth D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet. 2:e64.
13. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL. 2010. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455-2457.
14. Desmet CJ, Ishii KJ. 2012. Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat Rev Immunol. 12: 479-491.
15. Evans PD, et al. 2005. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science 309:1717-1720.
16. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES. 2009. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458:509-513.
17. Fu YX, Li WH. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
18. Fumagalli M, et al. 2009a.Widespread balancing selection and pathogendriven selection at blood group antigen genes. Genome Res. 19: 199-212.
19. Fumagalli M, et al. 2009b. Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J Exp Med. 206:1395-1408.
20. Fumagalli M, et al. 2010. Population genetics of IFIH1: ancient population structure, local selection and implications for susceptibility to type 1 diabetes. Mol Biol Evol. 27:2555-2566.
21. Fumagalli M, et al. 2011. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet. 7:e1002355.
22. Gabriel SB, et al. 2002. The structure of haplotype blocks in the human genome. Science 296:2225-2229.
23. Garrigan D, Hammer MF. 2006. Reconstructing human origins in the genomic era. Nat Rev Genet. 7:669-680.
24. Glazko GV, Nei M. 2003. Estimation of divergence times formajor lineages of primate species. Mol Biol Evol. 20:424-434.
25. Goudet J. 2005. Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes. 5(1):184-186.
26. Griffiths RC, Tavare S. 1994. Sampling theory for neutral alleles in a varying environment. Philos Trans R Soc Lond B Biol Sci. 344:403-410.
27. Griffiths RC, Tavare S. 1995. Unrooted genealogical tree probabilities in the infinitely-many-sites model. Math Biosci. 127:77-98.
28. Guindon S, Delsuc F, Dufayard JF, Gascuel O. 2009. Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol. 537:113-137.
29. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5:e1000695.
30. Hornung V, et al. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514-518.
31. Jakobsen MR, et al. 2013. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc Natl Acad Sci U S A. 110:E4571-E4580.
32. Jin T, Perry A, Smith P, Jiang J, Xiao TS. 2013. Structure of the absent in melanoma 2 (AIM2) pyrin domain provides insights into the mechanisms of AIM2 autoinhibition and inflammasome assembly. J Biol Chem. 288:13225-13235.
33. Jin T, et al. 2012. Structures of the HIN domain:DNA complexes reveal ligand binding and activationmechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 36:561-571.
34. Johnstone RW, Kershaw MH, Trapani JA. 1998. Isotypic variants of the interferon-inducible transcriptional repressor IFI 16 arise through differential mRNA splicing. Biochemistry 37:11924-11931.
35. Kerur N, et al. 2011. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to kaposi sarcoma-associated herpesvirus infection. Cell Host Microbe. 9:363-375.
36. Kosakovsky Pond SL, Frost SD. 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol. 22:1208-1222.
37. Kosakovsky Pond SL, et al. 2006. Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol. 23: 1891-1901.
38. Kosakovsky Pond SL, et al. 2011. A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol. 28:3033-3043.
39. Kosiol C, et al. 2008. Patterns of positive selection in six mammalian genomes. PLoS Genet. 4:e1000144.
40. Leffler EM, et al. 2013. Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339: 1578-1582.
41. Li JZ, et al. 2008. Worldwide human relationships inferred from genomewide patterns of variation. Science 319:1100-1104.
42. Li T, Diner BA, Chen J, Cristea IM. 2012. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc Natl Acad Sci U S A. 109:10558-10563.
43. Marth GT, Czabarka E, Murvai J, Sherry ST. 2004. The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations. Genetics 166:351-372.
44. Mitchell PS, et al. 2012. Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe. 12:598-604.
45. Murrell B, et al. 2012. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8:e1002764.
46. Nei M, Li WH. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A. 76: 5269-5273.
47. Orzalli MH, DeLuca NA, Knipe DM. 2012. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc Natl Acad Sci U S A. 109:E3008-E3017.
48. Patel MR, Loo YM, Horner SM, Gale M Jr, Malik HS. 2012. Convergent evolution of escape from hepaciviral antagonism in primates. PLoS Biol. 10:e1001282.
49. Pavlicek A, et al. 2004. Evolution of the tumor suppressor BRCA1 locus in primates: implications for cancer predisposition. Hum Mol Genet. 13: 2737-2751.
50. Quintana-Murci L, Clark AG. 2013. Population genetic tools for dissecting innate immunity in humans. Nat Rev Immunol. 13:280-293.
51. Rosenberg NA. 2006. Standardized subsets of the HGDP-CEPH human genome diversity cell line panel, accounting for atypical and duplicated samples and pairs of close relatives. Ann Hum Genet. 70:841-847.
52. Schaffner SF, et al. 2005. Calibrating a coalescent simulation of human genome sequence variation. Genome Res. 15:1576-1583.
53. Schattgen SA, Fitzgerald KA. 2011. The PYHIN protein family as mediators of host defenses. Immunol Rev. 243:109-118.
54. Segurel L, et al. 2012. The ABO blood group is a trans-species polymorphism in primates. Proc Natl Acad Sci U S A. 109: 18493-18498.
55. Sironi M, Clerici M. 2010. The hygiene hypothesis: an evolutionary perspective. Microbes Infect. 12:421-427.
56. Sirota M, Schaub MA, Batzoglou S, Robinson WH, Butte AJ. 2009. Autoimmune disease classification by inverse association with SNP alleles. PLoS Genet. 5:e1000792.
57. Stephens M, Smith N, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 68:978-989.
58. Stephens M, Scheet P. 2005. Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet. 76:449-462.
59. Tajima F. 1989. Statisticalmethod for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
60. Tellier A, Brown JK. 2007. Stability of genetic polymorphism in hostparasite interactions. Proc Biol Sci. 274:809-817.
61. Thomson R, Pritchard JK, Shen P, Oefner PJ, Feldman MW. 2000. Recent common ancestry of human Y chromosomes: evidence from DNA sequence data. Proc Natl Acad Sci U S A. 97:7360-7365.
62. Thornton K. 2003. Libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19:2325-2327.
63. Unterholzner L, et al. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol. 11:997-1004. Vasseur E, et al. 2011.
64. The selective footprints of viral pressures at the human RIG-I-like receptor family. Hum Mol Genet. 20:4462-4474.
65. Veeranki S, Choubey D. 2012. Interferon-inducible p200-family protein IFI16, an innate immune sensor for cytosolic and nuclear doublestranded DNA: regulation of subcellular localization. Mol Immunol. 49:567-571.
66. Voight BF, et al. 2005. Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci U S A. 102:18508-18513.
67. Wang K, et al. 2010. Comparative genetic analysis of inflammatory bowel disease and type 1 diabetes implicates multiple loci with opposite effects. Hum Mol Genet. 19:2059-2067.
68. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7:256-276.
69. Wernersson R, Pedersen AG. 2003. RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 31:3537-3539.
70. Wilson DJ, Hernandez RD, Andolfatto P, Przeworski M. 2011. A population genetics-phylogenetics approach to inferring natural selection in coding sequences. PLoS Genet. 7:e1002395.
71. Wright S. 1950. Genetical structure of populations. Nature 166:247-249.
72. Wright SI, Charlesworth B. 2004. The HKA test revisited: a maximumlikelihood- ratio test of the standard neutral model. Genetics 168: 1071-1076.
73. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
74. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
75. Yang Z, Nielsen R. 1998. Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol. 46:409-418.
76. Yang Z, Wong WS, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22: 1107-1118.
77. Zhang J, Nielsen R, Yang Z. 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol. 22:2472-2479.
78. Zhernakova A, et al. 2011. Meta-analysis of genome-wide association studies in celiac disease and rheumatoid arthritis identifies fourteen non- HLA shared loci. PLoS Genet. 7:e1002004.