Evolutionary insights into host-pathogen interactions from mammalian sequence data

Nature Reviews Genetics

Volumn 16, Issue 4, 2015, Pages 224-236

  Sironi, Manuela ^a   Cagliani, Rachele ^a   Forni, Diego ^a   Clerici, Mario ^b,c  

^a SCIENTIFIC INSTITUTE   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G;

ADAPTIVE IMMUNITY; AMINO ACID SUBSTITUTION; ANTIGEN PRESENTATION; ENZYME SPECIFICITY; FREQUENCY DEPENDENT SELECTION; GENE FREQUENCY; GENETIC VARIABILITY; GENOTYPE; HIGH THROUGHPUT SEQUENCING; HOST PATHOGEN INTERACTION; HOST RANGE; HOUSEKEEPING GENE; HUMAN; INFECTION SENSITIVITY; INNATE IMMUNITY; LEPTOSPIROSIS; MAMMAL; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; RNA INTERFERENCE; SELECTIVE SWEEP; SPECIES COMPARISON; SPECIES DIVERSITY; T LYMPHOCYTE ACTIVATION; AMINO ACID SEQUENCE; ANIMAL; DNA SEQUENCE; EVOLUTION; GENETICS; GENOMICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; GENETIC VARIATION; GENOMICS; HOST-PATHOGEN INTERACTIONS; HUMANS; MAMMALS; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84924953319     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3905     Document Type: Review

References (108)

1. Fumagalli M., et al. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet. 7, e1002355 (2011
2. Van Valen L. A new evolutionary law. Evol. Theory 1, 1-30 (1973
3. Brockhurst M. A., et al. Running with the Red Queen: the role of biotic conflicts in evolution. Proc. Biol. Sci. http://dx.doi.org/10.1098/rspb.2014.1382 (2014
4. Haldane J. B. S. The Causes of Evolution (Longmans Green & Co,1932
5. Samson J. E., Magadan A. H., Sabri M. & Moineau S. Revenge of the phages: defeating bacterial defences. Nature Rev. Microbiol. 11, 675-687 (2013
6. Karasov T. L., Horton M. W. & Bergelson J. Genomic variability as a driver of plant-pathogen coevolution?. Curr. Opin. Plant Biol. 18, 24-30 (2014
7. Gray J. C. & Cutter A. D. Mainstreaming Caenorhabditis elegans in experimental evolution. Proc. Biol. Sci. 281, 20133055 (2014
8. Keebaugh E. S. & Schlenke T. A. Insights from natural host-parasite interactions: the Drosophila model. Dev. Comp. Immunol. 42, 111-123 (2014
9. Barreiro L. B. & Quintana-Murci L. From evolutionary genetics to human immunology: how selection shapes host defence genes. Nature Rev. Genet. 11, 17-30 (2010
10. Quintana-Murci L. & Clark A. G. Population genetic tools for dissecting innate immunity in humans. Nature Rev. Immunol. 13, 280-293 (2013
11. Siddle K. J. & Quintana-Murci L. The Red Queen's long race: human adaptation to pathogen pressure. Curr. Opin. Genet. Dev. 29, 31-38 (2014
12. Fumagalli M. & Sironi M. Human genome variability natural selection and infectious diseases. Curr. Opin. Immunol. 30, 9-16 (2014
13. Karlsson E. K., Kwiatkowski D. P. & Sabeti P. C. Natural selection and infectious disease in human populations. Nature Rev. Genet. 15, 379-393 (2014
14. Benton M. J. The Red Queen and the Court Jester: species diversity and the role of biotic and abiotic factors through time. Science 323, 728-732 (2009
15. Venditti C., Meade A. & Pagel M. Phylogenies reveal new interpretation of speciation and the Red Queen. Nature 463, 349-352 (2010
16. Decaestecker E., et al. Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature 450, 870-873 (2007
17. Luijckx P., Fienberg H., Duneau D. & Ebert D. A matching-allele model explains host resistance to parasites. Curr. Biol. 23, 1085-1088 (2013
18. Paterson S., et al. Antagonistic coevolution accelerates molecular evolution. Nature 464, 275-278 (2010
19. Woolhouse M. E., Webster J. P., Domingo E., Charlesworth B. & Levin B. R. Biological and biomedical implications of the co evolution of pathogens and their hosts. Nature Genet. 32, 569-577 (2002
20. Jones K. E., et al. Global trends in emerging infectious diseases. Nature 451, 990-993 (2008
21. Sharp P. M. & Hahn B. H. Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1, a006841 (2011
22. Stremlau M., et al. The cytoplasmic body component TRIM5a restricts HIV 1 infection in Old World monkeys. Nature 427, 848-853 (2004
23. Sawyer S. L., Wu, L. I., Emerman M. & Malik H. S. Positive selection of primate TRIM5a identifies a critical species-specific retroviral restriction domain. Proc. Natl Acad. Sci. USA 102, 2832-2837 (2005
24. Kaiser S. M., Malik H. S. & Emerman M. Restriction of an extinct retrovirus by the human TRIM5a antiviral protein. Science 316, 1756-1758 (2007
25. Meyerson N. R., et al. Positive selection of primate genes that promote HIV 1 replication. Virology 454-455, 291-298 (2014
26. Schaller T., et al. HIV 1 capsid-cyclophilin interactions determine nuclear import pathway integration targeting and replication efficiency. PLoS Pathog. 7, e1002439 (2011
27. Bean A. G., et al. Studying immunity to zoonotic diseases in the natural host - keeping it real. Nature Rev. Immunol. 13, 851-861 (2013
28. Dietrich M., et al. Diversification of an emerging pathogen in a biodiversity hotspot: Leptospira in endemic small mammals of Madagascar. Mol. Ecol. 23, 2783-2796 (2014
29. Kosiol C., et al. Patterns of positive selection in six mammalian genomes. PLoS Genet. 4, e1000144 (2008
30. Seim I., et al. Genome analysis reveals insights into physiology and longevity of the Brandt's bat Myotis brandtii. Nature Commun. 4, 2212 (2013
31. Shaughnessy J., et al. Molecular characterization of the interaction between sialylated Neisseria gonorrhoeae and factor H. J. Biol. Chem. 286, 22235-22242 (2011
32. Hajjar A. M., et al. Humanized TLR4/MD 2 mice reveal LPS recognition differentially impacts susceptibility to Yersinia pestis and Salmonella enterica. PLoS Pathog. 8, e1002963 (2012
33. Raetz C. R., Reynolds C. M., Trent M. S. & Bishop R. E. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76, 295-329 (2007
34. Ohto U., Fukase K., Miyake K. & Shimizu T. Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD 2. Proc. Natl Acad. Sci. USA 109, 7421-7426 (2012
35. Areal H., Abrantes J. & Esteves P. J. Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. BMC Evol. Biol. 11, 368 (2011
36. Wang L. F., Walker P. J. & Poon L. L. Mass extinctions biodiversity and mitochondrial function: are bats 'special' as reservoirs for emerging viruses?. Curr. Opin. Virol. 1, 649-657 (2011
37. Zhang G., et al. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339, 456-460 (2013
38. Demogines A., Farzan M. & Sawyer S. L. Evidence for ACE2 utilizing coronaviruses (CoVs) related to severe acute respiratory syndrome CoV in bats. J. Virol. 86, 6350-6353 (2012
39. Kuo L., Godeke G. J., Raamsman M. J., Masters P. S. & Rottier P. J. Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. J. Virol. 74, 1393-1406 (2000
40. Guan Y., et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302, 276-278 (2003
41. Lau S. K., et al. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl Acad. Sci. USA 102, 14040-14045 (2005
42. Ge, X. Y., et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503, 535-538 (2013
43. Cotten M., et al. Full-genome deep sequencing and phylogenetic analysis of novel human betacoronavirus. Emerg. Infect. Dis. 19, 736-742B (2013
44. Raj V. S., et al. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495, 251-254 (2013
45. van Doremalen N., et al. Host species restriction of Middle East respiratory syndrome coronavirus through its receptor dipeptidyl peptidase 4. J. Virol. 88, 9220-9232 (2014
46. Cui J., Eden J. S., Holmes E. C. & Wang L. F. Adaptive evolution of bat dipeptidyl peptidase 4 (dpp4): implications for the origin and emergence of Middle East respiratory syndrome coronavirus. Virol. J. 10, 304 (2013
47. Lu, G., et al. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 500, 227-231 (2013
48. Wlasiuk G. & Nachman M. W. Adaptation and constraint at Toll-like receptors in primates. Mol. Biol. Evol. 27, 2172-2186 (2010
49. Fornuskova A., et al. Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (MURINAE). BMC Evol. Biol. 13, 194 (2013
50. Werling D., Jann O. C., Offord V., Glass E. J. & Coffey T. J. Variation matters: TLR structure and species-specific pathogen recognition. Trends Immunol. 30, 124-130 (2009
51. Brunette R. L., et al. Extensive evolutionary and functional diversity among mammalian AIM2 like receptors. J. Exp. Med. 209, 1969-1983 (2012
52. Cagliani R., et al. Ancient and recent selective pressures shaped genetic diversity at AIM2 like nucleic acid sensors. Genome Biol. Evol. 6, 830-845 (2014
53. Cagliani R., et al. RIG I like receptors evolved adaptively in mammals with parallel evolution at LGP2 and RIG I. J. Mol. Biol. 426, 1351-1365 (2014
54. Tenthorey J. L., Kofoed E. M., Daugherty M. D., Malik H. S. & Vance R. E. Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes. Mol. Cell 54, 17-29 (2014
55. Daugherty M. D. & Malik H. S. Rules of engagement: molecular insights from host-virus arms races. Annu. Rev. Genet. 46, 677-700 (2012
56. Duggal N. K. & Emerman M. Evolutionary conflicts between viruses and restriction factors shape immunity. Nature Rev. Immunol. 12, 687-695 (2012
57. Sawyer S. L. & Elde N. C. A cross-species view on viruses. Curr. Opin. Virol. 2, 561-568 (2012
58. Best S., Le Tissier P., Towers G. & Stoye J. P. Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382, 826-829 (1996
59. Aswad A. & Katzourakis A. Paleovirology and virally derived immunity. Trends Ecol. Evol. 27, 627-636 (2012
60. Yap M. W., Colbeck E., Ellis S. A. & Stoye J. P. Evolution of the retroviral restriction gene Fv1: inhibition of non-MLV retroviruses. PLoS Pathog. 10, e1003968 (2014
61. Mitchell P. S., et al. Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12, 598-604 (2012
62. Goujon C., et al. Human MX2 is an interferon-induced post-entry inhibitor of HIV 1 infection. Nature 502, 559-562 (2013
63. Sironi M., et al. Evolutionary analysis identifies an MX2 haplotype associated with natural resistance to HIV 1 infection. Mol. Biol. Evol. 31, 2402-2414 (2014
64. Khan N., Gowthaman U., Pahari S. & Agrewala J. N. Manipulation of costimulatory molecules by intracellular pathogens: veni vidi vici. PLoS Pathog. 8, e1002676 (2012
65. Hansen T. H. & Bouvier M. MHC class I antigen presentation: learning from viral evasion strategies. Nature Rev. Immunol. 9, 503-513 (2009
66. Forni D., et al. An evolutionary analysis of antigen processing and presentation across different timescales reveals pervasive selection. PLoS Genet. 10, e1004189 (2014
67. Forni D., et al. A 175 million year history of T cell regulatory molecules reveals widespread selection with adaptive evolution of disease alleles. Immunity 38, 1129-1141 (2013
68. Kajikawa M., et al. The intertransmembrane region of Kaposi's sarcoma-associated herpesvirus modulator of immune recognition 2 contributes to B7 2 downregulation. J. Virol. 86, 5288-5296 (2012
69. Chaudhry A., et al. The Nef protein of HIV 1 induces loss of cell surface costimulatory molecules CD80 and CD86 in APCs. J. Immunol. 175, 4566-4574 (2005
70. Short J. J., Vasu C., Holterman M. J., Curiel D. T. & Pereboev A. Members of adenovirus species B utilize CD80 and CD86 as cellular attachment receptors. Virus Res. 122, 144-153 (2006
71. Feinberg H., et al. Structural basis for langerin recognition of diverse pathogen and mammalian glycans through a single binding site. J. Mol. Biol. 405, 1027-1039 (2011
72. Horst D., Geerdink R. J., Gram A. M., Stoppelenburg A. J. & Ressing M. E. Hiding lipid presentation: viral interference with CD1d restricted invariant natural killer T (iNKT) cell activation. Viruses 4, 2379-2399 (2012
73. Liu J., et al. A threonine-based targeting signal in the human CD1d cytoplasmic tail controls its functional expression. J. Immunol. 184, 4973-4981 (2010
74. Machado L. R., et al. Evolutionary history of copy-number-variable locus for the low-affinity Fcγ receptor: mutation rate autoimmune disease and the legacy of helminth infection. Am. J. Hum. Genet. 90, 973-985 (2012
75. Engelmann B. & Massberg S. Thrombosis as an intravascular effector of innate immunity. Nature Rev. Immunol. 13, 34-45 (2013
76. Demogines A., Abraham J., Choe H., Farzan M. & Sawyer S. L. Dual host-virus arms races shape an essential housekeeping protein. PLoS Biol. 11, e1001571 (2013
77. Kaelber J. T., et al. Evolutionary reconstructions of the transferrin receptor of caniforms supports canine parvovirus being a re emerged and not a novel pathogen in dogs. PLoS Pathog. 8, e1002666 (2012
78. Barber M. F. & Elde N. C. Nutritional immunity. Escape from bacterial iron piracy through rapid evolution of transferrin. Science 346, 1362-1366 (2014
79. Al Daghri N. M., et al. Mammalian NPC1 genes may undergo positive selection and human polymorphisms associate with type 2 diabetes. BMC Med. 10, 140 (2012
80. Krishnan A., et al. Niemann-Pick C1 (NPC1)/NPC1 like1 chimeras define sequences critical for NPC1's function as a flovirus entry receptor. Viruses 4, 2471-2484 (2012
81. Ng, M., et al. Cell entry by a novel European filovirus requires host endosomal cysteine proteases and Niemann-Pick C1. Virology 468-470, 637-646 (2014
82. Shoemaker C. J., et al. Multiple cationic amphiphiles induce a Niemann-Pick C phenotype and inhibit Ebola virus entry and infection. PLoS ONE 8, e56265 (2013
83. Lee K., et al. Inhibition of ebola virus infection: identification of Niemann-Pick C1 as the target by optimization of a chemical probe. ACS Med. Chem. Lett. 4, 239-243 (2013
84. Cote M., et al. Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 477, 344-348 (2011
85. Cagliani R., et al. Evolutionary analysis of the contact system indicates that kininogen evolved adaptively in mammals and in human populations. Mol. Biol. Evol. 30, 1397-1408 (2013
86. Rallapalli P. M., Orengo C. A., Studer R. A. & Perkins S. J. Positive selection during the evolution of the blood coagulation factors in the context of their disease-causing mutations. Mol. Biol. Evol. 31, 3040-3056 (2014
87. Imamura T., et al. Induction of vascular leakage through release of bradykinin and a novel kinin by cysteine proteinases from Staphylococcus aureus. J. Exp. Med. 201, 1669-1676 (2005
88. Pichlmair A., et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 487, 486-490 (2012
89. Karlas A., et al. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463, 818-822 (2010
90. Smith J. D., McManus K. F. & Fraser H. B. A novel test for selection on cis-regulatory elements reveals positive and negative selection acting on mammalian transcriptional enhancers. Mol. Biol. Evol. 30, 2509-2518 (2013
91. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007
92. Anisimova M., Bielawski J. P. & Yang Z. Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol. Biol. Evol. 19, 950-958 (2002
93. Yang Z., Wong W. S. & Nielsen R. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22, 1107-1118 (2005
94. Murrell B., et al. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8, e1002764 (2012
95. Markova-Raina P. & Petrov D. High sensitivity to aligner and high rate of false positives in the estimates of positive selection in the 12 Drosophila genomes. Genome Res. 21, 863-874 (2011
96. Blackburne B. P. & Whelan S. Class of multiple sequence alignment algorithm affects genomic analysis. Mol. Biol. Evol. 30, 642-653 (2013
97. Schneider A., et al. Estimates of positive Darwinian selection are inflated by errors in sequencing annotation and alignment. Genome Biol. Evol. 1, 114-118 (2009
98. Jordan G. & Goldman N. The effects of alignment error and alignment filtering on the sitewise detection of positive selection. Mol. Biol. Evol. 29, 1125-1139 (2012
99. Anisimova M., Nielsen R. & Yang Z. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164, 1229-1236 (2003
100. Zhang J., Nielsen R. & Yang Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22, 2472-2479 (2005
101. Fletcher W. & Yang Z. The effect of insertions deletions and alignment errors on the branch-site test of positive selection. Mol. Biol. Evol. 27, 2257-2267 (2010
102. Anisimova M. & Yang Z. Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites. Mol. Biol. Evol. 24, 1219-1228 (2007
103. Kosakovsky Pond S. L., et al. A random effects branch-site model for detecting episodic diversifying selection. Mol. Biol. Evol. 28, 3033-3043 (2011
104. Guindon S., Rodrigo A. G., Dyer K. A. & Huelsenbeck J. P. Modeling the site-specific variation of selection patterns along lineages. Proc. Natl Acad. Sci. USA 101, 12957-12962 (2004
105. Lu, A. & Guindon S. Performance of standard and stochastic branch-site models for detecting positive selection among coding sequences. Mol. Biol. Evol. 31, 484-495 (2014
106. Yang Z. & dos Reis M. Statistical properties of the branch-site test of positive selection. Mol. Biol. Evol. 28, 1217-1228 (2011
107. Neefjes J., Jongsma M. L., Paul P. & Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nature Rev. Immunol. 11, 823-836 (2011
108. Barral D. C. & Brenner M. B. CD1 antigen presentation: how it works. Nature Rev. Immunol. 7, 929-941 (2007