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The impact of genetic adaptation on chimpanzee subspecies differentiation


Autoři: Joshua M. Schmidt aff001;  Marc de Manuel aff003;  Tomas Marques-Bonet aff003;  Sergi Castellano aff002;  Aida M. Andrés aff001
Působiště autorů: UCL Genetics Institute, Department of Genetics, Evolution and Environment, University College London, London, United Kingdom aff001;  Max Planck Institute for Evolutionary Anthropology, Department of Evolutionary Genetics, Leipzig, Germany aff002;  Institut de Biologia Evolutiva (Consejo Superior de Investigaciones Científicas–Universitat Pompeu Fabra), Barcelona, Spain aff003;  National Centre for Genomic Analysis–Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain aff004;  Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain aff005;  Genetics and Genomic Medicine Programme, Great Ormond Street Institute of Child Health, University College London (UCL), London, United Kingdom aff006;  UCL Genomics, London, United Kingdom aff007
Vyšlo v časopise: The impact of genetic adaptation on chimpanzee subspecies differentiation. PLoS Genet 15(11): e32767. doi:10.1371/journal.pgen.1008485
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008485

Souhrn

Chimpanzees, humans’ closest relatives, are in danger of extinction. Aside from direct human impacts such as hunting and habitat destruction, a key threat is transmissible disease. As humans continue to encroach upon their habitats, which shrink in size and grow in density, the risk of inter-population and cross-species viral transmission increases, a point dramatically made in the reverse with the global HIV/AIDS pandemic. Inhabiting central Africa, the four subspecies of chimpanzees differ in demographic history and geographical range, and are likely differentially adapted to their particular local environments. To quantitatively explore s genetic adaptation, we investigated the genic enrichment for SNPs highly differentiated between chimpanzee subspecies. Previous analyses of such patterns in human populations exhibited limited evidence of adaptation. In contrast, chimpanzees show evidence of recent positive selection, with differences among subspecies. Specifically, we observe strong evidence of recent selection in eastern chimpanzees, with highly differentiated SNPs being uniquely enriched in genic sites in a way that is expected under recent adaptation but not under neutral evolution or background selection. These sites are enriched for genes involved in immune responses to pathogens, and for genes inferred to differentiate the immune response to infection by simian immunodeficiency virus (SIV) in natural vs. non-natural host species. Conversely, central chimpanzees exhibit an enrichment of signatures of positive selection only at cytokine receptors, due to selective sweeps in CCR3, CCR9 and CXCR6 –paralogs of CCR5 and CXCR4, the two major receptors utilized by HIV to enter human cells. Thus, our results suggest that positive selection has contributed to the genetic and phenotypic differentiation of chimpanzee subspecies, and that viruses likely play a predominate role in this differentiation, with SIV being a likely selective agent. Interestingly, our results suggest that SIV has elicited distinctive adaptive responses in these two chimpanzee subspecies.

Klíčová slova:

Human genomics – Chimpanzees – Immune response – Macaque – Monkeys – Natural selection – SIV – Virus effects on host gene expression


Zdroje

1. Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, Lorente-Galdos B, et al. Great ape genetic diversity and population history. Nature. 2013;499(7459):471–5. doi: 10.1038/nature12228 23823723

2. Waterson RH, Lander ES, Wilson RK. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature. 2005;437(7055):69. doi: 10.1038/nature04072 16136131

3. Cagan A, Theunert C, Laayouni H, Santpere G, Pybus M, Casals F, et al. Natural selection in the great apes. Molecular Biology and Evolution. 2016;33(12):3268–83. doi: 10.1093/molbev/msw215 27795229

4. Enard D, Cai L, Gwennap C, Petrov DA. Viruses are a dominant driver of protein adaptation in mammals. Elife. 2016;5. Epub 2016/05/18. doi: 10.7554/eLife.12469 27187613; PubMed Central PMCID: PMC4869911.

5. Sabeti PC, Reich DE, Higgins JM, Levine HZP, Richter DJ, Schaffner SF, et al. Detecting recent positive selection in the human genome from haplotype structure. Nature. 2002;419(6909):832–7. doi: 10.1038/nature01140 12397357

6. Voight BF, Kudaravalli S, Wen X, Pritchard JK. A map of recent positive selection in the human genome. PLoS Biology. 2006;4(3):0446–58. doi: 10.1371/journal.pbio.0040072 16494531

7. Sabeti PC, Varilly P, Fry B, Lohmueller J, Hostetter E, Cotsapas C, et al. Genome-wide detection and characterization of positive selection in human populations. Nature. 2007;449(7164):913–8. doi: 10.1038/nature06250 17943131

8. Yi X, Liang Y, Huerta-Sanchez E, Jin X, Cuo ZXP, Pool JE, et al. Sequencing of 50 human exomes reveals adaptation to high altitude. Science. 2010;329(5987):75–8. doi: 10.1126/science.1190371 20595611

9. Racimo F. Testing for ancient selection using cross-population allele frequency differentiation. Genetics. 2016;202(2):733–50. doi: 10.1534/genetics.115.178095 26596347

10. Coop G, Pickrell JK, Novembre J, Kudaravalli S, Li J, Absher D, et al. The role of geography in human adaptation. PLoS Genetics. 2009;5(6):e1000500-e. doi: 10.1371/journal.pgen.1000500 19503611

11. Key FM, Fu Q, Romagne F, Lachmann M, Andres AM. Human adaptation and population differentiation in the light of ancient genomes. Nature Communications. 2016;7:10775–. doi: 10.1038/ncomms10775 26988143

12. Enard D, Messer PW, Petrov DA. Genome-wide signals of positive selection in human evolution. Genome Research. 2014;24(6):885–95. doi: 10.1101/gr.164822.113 24619126

13. Schrider DR, Kern AD. S/HIC: Robust Identification of Soft and Hard Sweeps Using Machine Learning. PLoS Genet. 2016;12(3):e1005928. Epub 2016/03/16. doi: 10.1371/journal.pgen.1005928 26977894; PubMed Central PMCID: PMC4792382.

14. Pybus M, Luisi P, Dall'Olio GM, Uzkudun M, Laayouni H, Bertranpetit J, Engelken J. Hierarchical boosting: a machine-learning framework to detect and classify hard selective sweeps in human populations. Bioinformatics. 2015 31(24):3946–52. doi: 10.1093/bioinformatics/btv493 26315912

15. Sugden LA, Atkinson EG, Fischer AP, Rong S, Henn BM, Ramachandran S. Localization of adaptive variants in human genomes using averaged one-dependence estimation. Nat Commun. 92018.

16. Schrider DR, Kern AD. Soft Sweeps Are the Dominant Mode of Adaptation in the Human Genome. Mol Biol Evol. 2017;34(8):1863–77. Epub 2017/05/10. doi: 10.1093/molbev/msx154 28482049; PubMed Central PMCID: PMC5850737.

17. Harris RB, Sackman A, Jensen JD. On the unfounded enthusiasm for soft selective sweeps II: Examining recent evidence from humans, flies, and viruses. PLoS Genet. 2018;14(12):e1007859. Epub 2018/12/29. doi: 10.1371/journal.pgen.1007859 30592709; PubMed Central PMCID: PMC6336318.

18. Nam K, Munch K, Mailund T, Nater A, Greminger MP, Krützen M, et al. Evidence that the rate of strong selective sweeps increases with population size in the great apes. Proceedings of the National Academy of Sciences. 2017;114(7):1613–8. doi: 10.1073/pnas.1605660114 28137852

19. Han S, Andres AM, Marques-Bonet T, Kuhlwilm M. Genetic Variation in Pan Species Is Shaped by Demographic History and Harbors Lineage-Specific Functions. Genome Biol Evol. 2019;11(4):1178–91. Epub 2019/03/09. doi: 10.1093/gbe/evz047 30847478; PubMed Central PMCID: PMC6482415.

20. De Manuel M, Kuhlwilm M, Frandsen P, Sousa VC, Desai T, Prado-Martinez J, et al. Chimpanzee genomic diversity reveals ancient admixture with bonobos. Science. 2016;354(6311):477–81. doi: 10.1126/science.aag2602 27789843

21. Humle T, Maisels F, Oates JF, Plumptre A, Williamson EA. Pan troglodytes errata version published in 2018). 2016 http://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T15933A17964454.en.

22. Leendertz FH, Ellerbrok H, Boesch C, Couacy-Hymann E, Mätz-Rensing K, Hakenbeck R, et al. Anthrax kills wild chimpanzees in a tropical rainforest. Nature. 2004;430(6998):451–2. doi: 10.1038/nature02722 15269768

23. Formenty P, Boesch C, Wyers M, Steiner C, Donati F, Dind F, et al. Ebola Virus Outbreak among Wild Chimpanzees Living in a Rain Forest of Cote d'Ivoire. The Journal of Infectious Diseases. 1999;179(s1):S120–S6. doi: 10.1086/514296 9988175

24. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science. 2006;313(5786):523–6. doi: 10.1126/science.1126531 16728595

25. Rudicell RS, Jones JH, Wroblewski EE, Learn GH, Li Y, Robertson JD, et al. Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathogens. 2010;6(9). doi: 10.1371/journal.ppat.1001116 20886099

26. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, et al. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature. 2009;460(7254):515–9. doi: 10.1038/nature08200 19626114

27. Locatelli S, Harrigan RJ, Sesink Clee PR, Mitchell MW, McKean KA, Smith TB, et al. Why are Nigeria-Cameroon chimpanzees (Pan troglodytes ellioti) free of SIVcpz infection? PLoS ONE. 2016;11(8):e0160788-e. doi: 10.1371/journal.pone.0160788 27505066

28. Heuverswyn FV, Li Y, Bailes E, Neel C, Lafay B, Keele BF, et al. Genetic diversity and phylogeographic clustering of SIVcpzPtt in wild chimpanzees in Cameroon. Virology. 2007;368(1):155–71. doi: 10.1016/j.virol.2007.06.018 17651775

29. Hernandez RD, Kelley JL, Elyashiv E, Melton SC, Auton A, McVean G, et al. Classic selective sweeps were rare in recent human evolution. Science. 2011;331(6019):920–4. doi: 10.1126/science.1198878 21330547

30. Keinan A, Reich D. Human population differentiation is strongly correlated with local recombination rate. PLoS Genet. 2010;6(3):e1000886. Epub 2010/04/03. doi: 10.1371/journal.pgen.1000886 20361044; PubMed Central PMCID: PMC2845648.

31. Lohmueller KE, Albrechtsen A, Li Y, Kim SY, Korneliussen T, Vinckenbosch N, et al. Natural selection affects multiple aspects of genetic variation at putatively neutral sites across the human genome. PLoS Genet. 2011;7(10):e1002326. Epub 2011/10/25. doi: 10.1371/journal.pgen.1002326 22022285; PubMed Central PMCID: PMC3192825.

32. Auton A, Fledel-Alon A, Pfeifer S, Venn O, Ségurel L, Street T, et al. A fine-scale chimpanzee genetic map from population sequencing. Science. 2012;336(6078):193–8. doi: 10.1126/science.1216872 22422862

33. Charlesworth B, Morgan MT, Charlesworth D. The Effect of Deleterious Mutations on Neutral Molecular Variation. Genetics. 1993;134(4):1289–303. WOS:A1993LP87300030. 8375663

34. McVicker G, Gordon D, Davis C, Green P. Widespread Genomic Signatures of Natural Selection in Hominid Evolution. Plos Genetics. 2009;5(5). ARTN e100047110.1371/journal.pgen.1000471. WOS:000267083000026.

35. Nordborg M, Charlesworth B, Charlesworth D. The effect of recombination on background selection. Genet Res. 1996;67(2):159–74. Epub 1996/04/01. doi: 10.1017/s0016672300033619 8801188.

36. Hudson RR, Kaplan NL. Deleterious background selection with recombination. Genetics. 1995;141(4):1605–17. Epub 1995/12/01. 8601498; PubMed Central PMCID: PMC1206891.

37. Bataillon T, Duan J, Hvilsom C, Jin X, Li Y, Skov L, et al. Inference of purifying and positive selection in three subspecies of chimpanzees (Pan troglodytes) from exome sequencing. Genome Biology and Evolution. 2015;7(4):1122–32. doi: 10.1093/gbe/evv058 25829516

38. Corbett-Detig RB, Hartl DL, Sackton TB. Natural Selection Constrains Neutral Diversity across A Wide Range of Species. PLoS Biology. 2015;13(4):e1002112-e. doi: 10.1371/journal.pbio.1002112 25859758

39. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, et al. Annotation of functional variation in personal genomes using RegulomeDB. Genome Research. 2012;22(9):1790–7. doi: 10.1101/gr.137323.112 22955989

40. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Research. 2005;15(8):1034–50. doi: 10.1101/gr.3715005 16024819

41. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25(1):25–9. Epub 2000/05/10. doi: 10.1038/75556 10802651; PubMed Central PMCID: PMC3037419.

42. The Gene Ontology C. Expansion of the Gene Ontology knowledgebase and resources. Nucleic Acids Res. 2017;45(D1):D331–D8. Epub 2016/12/03. doi: 10.1093/nar/gkw1108 27899567; PubMed Central PMCID: PMC5210579.

43. Jacquelin B, Petitjean G, Kunkel D, Liovat AS, Jochems SP, Rogers KA, et al. Innate immune responses and rapid control of inflammation in African green monkeys treated or not with interferon-alpha during primary SIVagm infection. PLoS Pathog. 2014;10(7):e1004241. Epub 2014/07/06. doi: 10.1371/journal.ppat.1004241 PubMed Central PMCID: PMC4081777. 24991927

44. Jacquelin B, Mayau V, Targat B, Liovat AS, Kunkel D, Petitjean G, et al. Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest. 2009;119(12):3544–55. Epub 2009/12/05. doi: 10.1172/JCI40093 19959873; PubMed Central PMCID: PMC2786805.

45. Ayache J, Benard M, Ernoult-Lange M, Minshall N, Standart N, Kress M, et al. P-body assembly requires DDX6 repression complexes rather than decay or Ataxin2/2L complexes. Molecular Biology of the Cell. 2015;26(14):2579–95. doi: 10.1091/mbc.E15-03-0136 25995375

46. Nonhoff U, Ralser M, Welzel F, Piccini I, Balzereit D, Yaspo ML, et al. Ataxin-2 Interacts with the DEAD/H-Box RNA Helicase DDX6 and Interferes with P-Bodies and Stress Granules. Mol Biol Cell. 182007. p. 1385–96.

47. Loschi M, Leishman CC, Berardone N, Boccaccio GL. Dynein and kinesin regulate stress-granule and P-body dynamics. J Cell Sci. 1222009. p. 3973–82.

48. Tsai WC, Lloyd RE. Cytoplasmic RNA Granules and Viral Infection. Annu Rev Virol. 2014;1(1):147–70. doi: 10.1146/annurev-virology-031413-085505 26958719; PubMed Central PMCID: PMC4867093.

49. Lloyd RE. Regulation of Stress Granules and P-Bodies During RNA Virus Infection. Wiley Interdiscip Rev RNA. 2013;4(3):317–31. doi: 10.1002/wrna.1162 23554219; PubMed Central PMCID: PMC3652661.

50. Santiago ML, Rodenburg CM, Kamenya S, Bibollet-Ruche F, Gao F, Bailes E, et al. SIVcpz in wild chimpanzees. Science. 2002;295(5554):465–. doi: 10.1126/science.295.5554.465 11799233

51. Santiago ML, Lukasik M, Kamenya S, Li Y, Bibollet-Ruche F, Bailes E, et al. Foci of endemic simian immunodeficiency virus infection in wild-living eastern chimpanzees (Pan troglodytes schweinfurthii). Journal of virology. 2003;77(13):7545–62. doi: 10.1128/JVI.77.13.7545-7562.2003 12805455

52. Nerrienet E, Santiago ML, Foupouapouognigni Y, Bailes E, Mundy NI, Njinku B, et al. Simian Immunodeficiency Virus Infection in Wild-Caught Chimpanzees from Cameroon. Journal of Virology. 2005;79(2):1312–9. doi: 10.1128/JVI.79.2.1312-1319.2005 15613358

53. Boué V, Locatelli S, Boucher F, Ayouba A, Butel C, Esteban A, et al. High rate of simian immunodeficiency virus (SIV) infections in wild chimpanzees in northeastern Gabon. Viruses. 2015;7(9):4997–5015. doi: 10.3390/v7092855 26389939

54. Svardal H, Jasinska AJ, Apetrei C, Coppola G, Huang Y, Schmitt CA, et al. Ancient hybridization and strong adaptation to viruses across African vervet monkey populations. Nature Genetics. 2017;49(12):1705–13. doi: 10.1038/ng.3980 29083404

55. Griffith JW, Sokol CL, Luster AD. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol. 2014;32:659–702. Epub 2014/03/25. doi: 10.1146/annurev-immunol-032713-120145 24655300.

56. Ma W, Bryce PJ, Humbles AA, Laouini D, Yalcindag A, Alenius H, et al. CCR3 is essential for skin eosinophilia and airway hyperresponsiveness in a murine model of allergic skin inflammation. J Clin Invest. 2002;109(5):621–8. Epub 2002/03/06. doi: 10.1172/JCI14097 11877470; PubMed Central PMCID: PMC150891.

57. Uehara S, Grinberg A, Farber JM, Love PE. A role for CCR9 in T lymphocyte development and migration. J Immunol. 2002;168(6):2811–9. Epub 2002/03/09. doi: 10.4049/jimmunol.168.6.2811 11884450.

58. Berger EA. HIV entry and tropism: the chemokine receptor connection. AIDS. 1997;11 Suppl A:S3–16. Epub 1997/01/01. 9451961.

59. Moore JP, Kitchen SG, Pugach P, Zack JA. The CCR5 and CXCR4 coreceptors—central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection. AIDS Res Hum Retroviruses. 2004;20(1):111–26. Epub 2004/03/06. doi: 10.1089/088922204322749567 15000703.

60. Nedellec R, Coetzer M, Shimizu N, Hoshino H, Polonis VR, Morris L, et al. Virus entry via the alternative coreceptors CCR3 and FPRL1 differs by human immunodeficiency virus type 1 subtype. Journal of Viral Entry. 2010;4(1):33–. doi: 10.1128/JVI.00780-09 19553323

61. Gorry PR, Dunfee RL, Mefford ME, Kunstman K, Morgan T, Moore JP, et al. Changes in the V3 region of gp120 contribute to unusually broad coreceptor usage of an HIV-1 isolate from a CCR5 Delta32 heterozygote. Virology. 2007;362(1):163–78. Epub 2007/01/24. doi: 10.1016/j.virol.2006.11.025 17239419; PubMed Central PMCID: PMC1973138.

62. Bron R, Klasse PJ, Wilkinson D, Clapham PR, Pelchen-Matthews A, Power C, et al. Promiscuous use of CC and CXC chemokine receptors in cell-to-cell fusion mediated by a human immunodeficiency virus type 2 envelope protein. J Virol. 1997;71(11):8405–15. Epub 1997/10/29. 9343197; PubMed Central PMCID: PMC192303.

63. Willey SJ, Reeves JD, Hudson R, Miyake K, Dejucq N, Schols D, et al. Identification of a subset of human immunodeficiency virus type 1 (HIV-1), HIV-2, and simian immunodeficiency virus strains able to exploit an alternative coreceptor on untransformed human brain and lymphoid cells. J Virol. 2003;77(11):6138–52. Epub 2003/05/14. doi: 10.1128/JVI.77.11.6138-6152.2003 12743271; PubMed Central PMCID: PMC155019.

64. Elliott STC, Wetzel KS, Francella N, Bryan S, Romero DC, Riddick NE, et al. Dualtropic CXCR6/CCR5 Simian Immunodeficiency Virus (SIV) Infection of Sooty Mangabey Primary Lymphocytes: Distinct Coreceptor Use in Natural versus Pathogenic Hosts of SIV. 2015. doi: 10.1128/JVI.01236-15 26109719

65. Wetzel KS, Yi Y, Elliott STC, Romero D, Jacquelin B, Hahn BH, et al. CXCR6-Mediated Simian Immunodeficiency Virus SIVagmSab Entry into Sabaeus African Green Monkey Lymphocytes Implicates Widespread Use of Non-CCR5 Pathways in Natural Host Infections. J Virol. 912017.

66. Wetzel KS, Yi Y, Yadav A, Bauer AM, Bello EA, Romero DC, et al. Loss of CXCR6 coreceptor usage characterizes pathogenic lentiviruses. PLoS Pathog. 2018;14(4):e1007003. Epub 2018/04/17. doi: 10.1371/journal.ppat.1007003 29659623; PubMed Central PMCID: PMC5919676.

67. Steen A, Thiele S, Guo D, Hansen LS, Frimurer TM, Rosenkilde MM. Biased and Constitutive Signaling in the CC-chemokine Receptor CCR5 by Manipulating the Interface between Transmembrane Helices 6 and 7*. J Biol Chem. 2882013. p. 12511–21.

68. Hermisson J, Pennings PS. Soft sweeps and beyond: understanding the patterns and probabilities of selection footprints under rapid adaptation. Methods in Ecology and Evolution. 2017;8(6):700–16. doi: 10.1111/2041-210x.12808 WOS:000402919100005.

69. Pritchard JK, Pickrell JK, Coop G. The Genetics of Human Adaptation: Hard Sweeps, Soft Sweeps, and Polygenic Adaptation. Current Biology. 2010;20(4):R208–R15. doi: 10.1016/j.cub.2009.11.055 20178769

70. Sadler AJ, Williams BRG. Interferon-inducible antiviral effectors. Nat Rev Immunol. 2008;8(7):559–68. doi: 10.1038/nri2314 18575461; PubMed Central PMCID: PMC2522268.

71. Andrés AM, Dennis MY, Kretzschmar WW, Cannons JL, Lee-Lin SQ, Hurle B, et al. Balancing selection maintains a form of ERAP2 that undergoes nonsense-mediated decay and affects antigen presentation. PLoS Genetics. 2010;6(10):1–13. doi: 10.1371/journal.pgen.1001157 20976248

72. Hearn A, York IA, Rock KL. The Specificity of Trimming of MHC Class I-Presented Peptides in the Endoplasmic Reticulum1. J Immunol. 2009;183(9):5526–36. doi: 10.4049/jimmunol.0803663 19828632; PubMed Central PMCID: PMC2855122.

73. Harris LD, Tabb B, Sodora DL, Paiardini M, Klatt NR, Douek DC, et al. Downregulation of robust acute type I interferon responses distinguishes nonpathogenic simian immunodeficiency virus (SIV) infection of natural hosts from pathogenic SIV infection of rhesus macaques. J Virol. 2010;84(15):7886–91. Epub 2010/05/21. doi: 10.1128/JVI.02612-09 20484518; PubMed Central PMCID: PMC2897601.

74. Rotger M, Dalmau J, Rauch A, McLaren P, Bosinger SE, Martinez R, et al. Comparative transcriptomics of extreme phenotypes of human HIV-1 infection and SIV infection in sooty mangabey and rhesus macaque. Journal of Clinical Investigation. 2011;121(6):2391–400. doi: 10.1172/JCI45235 21555857

75. Utay NS, Douek DC. Interferons and HIV Infection: The Good, the Bad, and the Ugly. Pathog Immun. 2016;1(1):107–16. Epub 2016/08/09. doi: 10.20411/pai.v1i1.125 27500281; PubMed Central PMCID: PMC4972494.

76. Friedman J, Cho WK, Chu CK, Keedy KS, Archin NM, Margolis DM, et al. Epigenetic Silencing of HIV-1 by the Histone H3 Lysine 27 Methyltransferase Enhancer of Zeste 2▿. J Virol. 852011. p. 9078–89.

77. Khan S, Iqbal M, Tariq M, Baig SM, Abbas W. Epigenetic regulation of HIV-1 latency: focus on polycomb group (PcG) proteins. Clinical Epigenetics. 2018;10(1):14–. doi: 10.1186/s13148-018-0441-z 29441145

78. Pickrell JK, Berisa T, Liu JZ, Ségurel L, Tung JY, Hinds DA. Detection and interpretation of shared genetic influences on 42 human traits. Nature Genetics. 2016;48(7):709–17. doi: 10.1038/ng.3570 27182965

79. Browning SR, Browning BL. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet. 2007;81(5):1084–97. Epub 2007/10/10. doi: 10.1086/521987 PubMed Central PMCID: PMC2265661. 17924348

80. Reich D, Thangaraj K, Patterson N, Price AL, Singh L. Reconstructing Indian population history. Nature. 2009;461(7263):489–94. Epub 2009/09/26. doi: 10.1038/nature08365 19779445; PubMed Central PMCID: PMC2842210.

81. Busing FMTA, Meijer E, Leeden RVDJS, Computing. Delete-m Jackknife for Unequal m. 1999;9(1):3–8. doi: 10.1023/a:1008800423698

82. Cheng X, Xu C, DeGiorgio M. Fast and robust detection of ancestral selective sweeps. Mol Ecol. 2017;26(24):6871–91. Epub 2017/11/08. doi: 10.1111/mec.14416 29113018.

83. Racimo F, Berg JJ, Pickrell JK. Detecting polygenic adaptation in admixture graphs. Genetics. 2018;208(4):1565–84. doi: 10.1534/genetics.117.300489 29348143

84. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25. Epub 1987/07/01. doi: 10.1093/oxfordjournals.molbev.a040454 3447015.

85. Bhatia G, Patterson N, Sankararaman S, Price AL. Estimating and interpreting FST: the impact of rare variants. Genome Res. 2013;23(9):1514–21. Epub 2013/07/19. doi: 10.1101/gr.154831.113 23861382; PubMed Central PMCID: PMC3759727.

86. Ewing G, Hermisson J. MSMS: a coalescent simulation program including recombination, demographic structure and selection at a single locus. Bioinformatics. 2010;26(16):2064–5. Epub 2010/07/02. doi: 10.1093/bioinformatics/btq322 20591904; PubMed Central PMCID: PMC2916717.

87. Kofler R, Schlötterer C. Gowinda: Unbiased analysis of gene set enrichment for genome-wide association studies. Bioinformatics. 2012;28(15):2084–5. doi: 10.1093/bioinformatics/bts315 22635606

88. https://commons.wikimedia.org/wiki/File:Blank_Map-Africa.svg

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Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

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