Evidence for selection at HIV host susceptibility genes in a West Central African human population

BMC Evolutionary Biology

Volumn 12, Issue 1, 2012, Pages

  Zhao, Kai ^a   Ishida, Yasuko ^a   Oleksyk, Taras K ^b   Winkler, Cheryl A ^c   Roca, Alfred L ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^c SAIC FREDERICK INC   (United States)

Author keywords

Biaka pygmies; HIV dependency factors; Mbuti pygmies; Single nucleotide polymorphisms

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; BIODEGRADATION; GENE EXPRESSION; GENOME; GENOMICS; GENOTYPE; GEOGRAPHICAL REGION; HOMINID; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE SYSTEM; PATHOGENICITY; POPULATION OUTBREAK; SELECTION; VIRUS;

AFRICA;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; PAN; PAN TROGLODYTES; PAN TROGLODYTES TROGLODYTES; SIMIAN IMMUNODEFICIENCY VIRUS;

APOBEC3H PROTEIN, HUMAN; CARRIER PROTEIN; CHEMOKINE RECEPTOR; CUL5 PROTEIN, HUMAN; CULLIN; CXCR6 PROTEIN, HUMAN; DNA BINDING PROTEIN; ESCRT PROTEIN; HLA C ANTIGEN; HYDROLASE; TRANSCRIPTION FACTOR; TRIM5 PROTEIN, HUMAN; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; VIRUS RECEPTOR;

AFRICA; ANIMAL; ARTICLE; CENTRAL AFRICA; DISEASE TRANSMISSION; DNA SEQUENCE; ETHNIC GROUP; ETHNOLOGY; GENETIC PREDISPOSITION; GENETIC SELECTION; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MISSENSE MUTATION; MOLECULAR GENETICS; NEGRO; PAN TROGLODYTES; PHYSIOLOGY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SINGLE NUCLEOTIDE POLYMORPHISM; VIROLOGY;

AFRICA, CENTRAL; AFRICA, WESTERN; AFRICAN CONTINENTAL ANCESTRY GROUP; AMINOHYDROLASES; ANIMALS; CARRIER PROTEINS; CULLIN PROTEINS; DNA-BINDING PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ETHNIC GROUPS; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HIV INFECTIONS; HIV-1; HLA-C ANTIGENS; HOST-PATHOGEN INTERACTIONS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PAN TROGLODYTES; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, CHEMOKINE; RECEPTORS, VIRUS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION FACTORS;

MLCS; MLOWN;

EID: 84870408680     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-12-237     Document Type: Article

References (84)

1. Host genes associated with HIV/AIDS: advances in gene discovery. An P, Winkler CA, Trends Genet 2010 26 119 131 10.1016/j.tig.2010.01.002 20149939
2. Human genes that limit AIDS. O'Brien SJ, Nelson GW, Nat Genet 2004 36 565 574 10.1038/ng1369 15167933 (Pubitemid 38715980)
3. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Dean M, Carrington M, Winkler C, Huttley GA, Smith MW, Allikmets R, Goedert JJ, Buchbinder SP, Vittinghoff E, Gomperts E, et al. Science 1996 273 1856 1862 10.1126/science.273.5283.1856 8791590
4. HLA and HIV-1: Heterozygote advantage and B*35-Cw*04 disadvantage. Carrington M, Science 1999 283 1748 1752 10.1126/science.283.5408. 1748 10073943 (Pubitemid 29143811)
5. KIR-HLA intercourse in HIV disease. Carrington M, Martin MP, Bergen J, Trends Microbiol 2008 16 620 627 10.1016/j.tim.2008.09.002 18976921
6. New class I and II HLA alleles strongly associated with opposite patterns of progression to AIDS. Hendel H, Caillat-Zucman S, Lebuanec H, Carrington M, O'Brien S, Andrieu JM, Schachter F, Zagury D, Rappaport J, Winkler C, et al. J Immunol 1999 162 6942 6946 10352317 (Pubitemid 29309424)
7. Host genetics and HIV-1 viral load set-point in African-Americans. Shrestha S, Aissani B, Song W, Wilson CM, Kaslow RA, Tang J, AIDS 2009 23 673 677 10.1097/QAD.0b013e328325d414 19276793
8. Genome-wide association study implicates PARD3B-based AIDS restriction. Troyer JL, Nelson GW, Lautenberger J, Chinn L, McIntosh C, Johnson RC, Sezgin E, Kessing B, Malasky M, Hendrickson SL, et al. J Infect Dis 2011 203 1491 1502 10.1093/infdis/jir046 21502085
9. Genomewide association study of an AIDS-nonprogression cohort emphasizes the role played by HLA genes (ANRS Genomewide Association Study 02). Limou S, Le Clerc S, Coulonges C, Carpentier W, Dina C, Delaneau O, Labib T, Taing L, Sladek R, Deveau C, et al. J Infect Dis 2009 199 419 426 10.1086/596067 19115949
10. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Konig R, Zhou Y, Elleder D, Diamond TL, Bonamy GM, Irelan JT, Chiang CY, Tu BP, Jesus PDD, Lilley CE, et al. Cell 2008 135 49 60 10.1016/j.cell.2008.07.032 18854154
11. Identification of host proteins required for HIV infection through a functional genomic screen. Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, Xavier RJ, Lieberman J, Elledge SJ, Science 2008 319 921 926 10.1126/science.1152725 18187620 (Pubitemid 351263756)
12. Genome-scale RNAi screen for host factors required for HIV replication. Zhou H, Xu M, Huang Q, Gates AT, Zhang XD, Castle JC, Stec E, Ferrer M, Strulovici B, Hazuda DJ, Espeseth AS, Cell Host Microbe 2008 4 495 504 10.1016/j.chom.2008.10.004 18976975
13. Knockdown screens to knockout HIV-1. Goff SP, Cell 2008 135 417 420 10.1016/j.cell.2008.10.007 18984154
14. The evolution of HIV-1 and the origin of AIDS. Sharp PM, Hahn BH, Philos Trans R Soc Lond B Biol Sci 2010 365 2487 2494 10.1098/rstb.2010.0031 20643738
15. Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Worobey M, Gemmel M, Teuwen DE, Haselkorn T, Kunstman K, Bunce M, Muyembe JJ, Kabongo JM, Kalengayi RM, Marck EV, et al. Nature 2008 455 661 664 10.1038/nature07390 18833279
16. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Keele BF, Van Heuverswyn F, Li Y, Bailes E, Takehisa J, Santiago ML, Bibollet-Ruche F, Chen Y, Wain LV, Liegeois F, et al. Science 2006 313 523 526 10.1126/science.1126531 16728595 (Pubitemid 44148457)
17. High GUD incidence in the early 20 century created a particularly permissive time window for the origin and initial spread of epidemic HIV strains. de Sousa JD, Muller V, Lemey P, Vandamme AM, PLoS One 2010 5 9936 10.1371/journal.pone.0009936 20376191
18. Protective correlates against HIVs may have evolved in human populations in the areas of historic occurrence of primate-to-man transmissions of SIVs ancestral to HIVs: studies in these populations may provide crucial insights for treatment and prevention. Parsyan AE, Med Hypotheses 2005 64 433 437 10.1016/j.mehy.2004.09.018 15617844 (Pubitemid 40022997)
19. Identifying selected regions from heterozygosity and divergence using a light-coverage genomic dataset from two human populations. Oleksyk TK, Zhao K, Vega FMDL, Gilbert DA, O'Brien SJ, Smith MW, PLoS One 2008 3 1712 10.1371/journal.pone.0001712 18320033 (Pubitemid 351903001)
20. Genome-wide scans for footprints of natural selection. Oleksyk TK, Smith MW, O'Brien SJ, Phil Trans Roy Soc Lond B Biol Sci 2010 365 185 205 10.1098/rstb.2009.0219
21. Evolutionary strategies of human T-cell lymphotropic virus type II. Vandamme A-M, Bertazzoni U, Salemi M, Gene 2000 261 171 180 10.1016/S0378- 1119(00)00473-X 11164048 (Pubitemid 32103534)
22. HTLV-2B strains, similar to those found in several Amerindian tribes, are endemic in central African Bakola Pygmies. Mauclère P, Afonso PV, Meertens L, Plancoulaine S, Calattini S, Froment A, Van Beveren M, de Thé G, Quintana-Murci L, Mahieux R, Gessain A, J Infect Dis 2011 203 1316 1323 10.1093/infdis/jir031 21459818
23. HTLV-1 but not HTLV-2 found in pygmies from Central African Republic. Gessain A, Hervé V, Jeannel D, Garin B, Mathiot C, J AIDS 1993 6 1373
24. New strain of human T lymphotropic virus (HTLV) type 3 in a pygmy from Cameroon with peculiar HTLV serologic results. Calattini S, Betsem E, Bassot S, Chevalier SA, Mahieux R, Froment A, Gessain A, J Infect Dis 2009 199 561 564 10.1086/596206 19099485
25. Naturally acquired simian retrovirus infections in central African hunters. Wolfe ND, Switzer WM, Carr JK, Bhullar VB, Shanmugam V, Tamoufe U, Prosser AT, Torimiro JN, Wright A, Mpoudi-Ngole E, et al. Lancet 2004 363 932 937 10.1016/S0140-6736(04)15787-5 15043960 (Pubitemid 38388326)
26. Lineage-specific expansions of retroviral insertions within the genomes of African great apes but not humans and orangutans. Yohn CT, Jiang Z, McGrath SD, Hayden KE, Khaitovich P, Johnson ME, Eichler MY, McPherson JD, Zhao S, Pääbo S, Eichler EE, PLoS Biol 2005 3 110 10.1371/journal.pbio.0030110 15737067 (Pubitemid 40721153)
27. Restriction of an extinct retrovirus by the human TRIM5alpha antiviral protein. Kaiser SM, Malik HS, Emerman M, Science 2007 316 1756 1758 10.1126/science.1140579 17588933 (Pubitemid 46988552)
28. Worldwide human relationships inferred from genome-wide patterns of variation. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, Ramachandran S, Cann HM, Barsh GS, Feldman M, Cavalli-Sforza LL, Myers RM, Science 2008 319 1100 1104 10.1126/science.1153717 18292342 (Pubitemid 351300793)
29. Inferring the demographic history of African farmers and pygmy hunter-gatherers using a multilocus resequencing data set. Patin E, Laval G, Barreiro LB, Salas A, Semino O, Santachiara-Benerecetti S, Kidd KK, Kidd JR, Van Der Veen L, Hombert JM, et al. PLoS Genet 2009 5 1000448 10.1371/journal.pgen. 1000448 19360089
30. Insights into the demographic history of African pygmies from complete mitochondrial genomes. Batini C, Lopes J, Behar DM, Calafell F, Jorde LB, van der Veen L, Quintana-Murci L, Spedini G, Destro-Bisol G, Comas D, Mol Biol Evol 2011 28 1099 1110 10.1093/molbev/msq294 21041797
31. Cavalli-Sforza LL, African Pygmies Orlando: Academic Press 1986
32. Forest people: The role of African rainforests in human evolution and dispersal. Mercader J, Evol Anthropol 2002 11 117 124 10.1002/evan.10022 (Pubitemid 37239459)
33. Origins and genetic diversity of pygmy hunter-gatherers from Western Central Africa. Verdu P, Austerlitz F, Estoup A, Vitalis R, Georges M, Thery S, Froment A, Bomin SL, Gessain A, Hombert J, et al. Curr Biol 2009 19 312 318 10.1016/j.cub.2008.12.049 19200724
34. Phillipson DW, African Archaeology Cambridge, UK: Cambridge University Press 3 2005
35. The analysis of variation of mtDNA hypervariable region 1 suggests that Eastern and Western Pygmies diverged before the Bantu expansion. Destro-Bisol G, Coia V, Boschi I, Verginelli F, Caglia A, Pascali V, Spedini G, Calafell F, Am Nat 2004 163 212 226 10.1086/381405 14970923 (Pubitemid 38335218)
36. Polymorphisms of CUL5 are associated with CD4+ T cell loss in HIV-1 infected individuals. An P, Duggal P, Wang LH, O'Brien SJ, Donfield S, Goedert JJ, Phair J, Buchbinder S, Kirk GD, Winkler CA, PLoS Genet 2007 3 19 10.1371/journal.pgen.0030019 17257057 (Pubitemid 46168839)
37. The Human Genome Diversity Project: past, present and future. Cavalli-Sforza LL, Nat Rev Genet 2005 6 333 340 15803201 (Pubitemid 40469052)
38. Common genetic variation and the control of HIV-1 in humans. Fellay J, Ge D, Shianna KV, Colombo S, Ledergerber B, Cirulli ET, Urban TJ, Zhang K, Gumbs CE, Smith JP, et al. PLoS Genet 2009 5 1000791 10.1371/journal.pgen.1000791 20041166
39. Effects of human TRIM5-alpha polymorphisms on antiretroviral function and susceptibility to human immunodeficiency virus infection. Javanbakht H, An P, Gold B, Petersen DC, O'Huigin C, Nelson GW, O'Brien SJ, Kirk GD, Detels R, Buchbinder S, et al. Virology 2006 354 15 27 10.1016/j.virol.2006.06.031 16887163 (Pubitemid 44468115)
40. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, Diaz-Griffero F, Anderson DJ, Sundquist WI, Sodroski J, Proc Natl Acad Sci U S A 2006 103 5514 5519 10.1073/pnas.0509996103 16540544
41. Genomewide association study for determinants of HIV-1 acquisition and viral set point in HIV-1 serodiscordant couples with quantified virus exposure. Lingappa JR, Petrovski S, Kahle E, Fellay J, Shianna K, McElrath MJ, Thomas KK, Baeten JM, Celum C, Wald A, et al. PLoS One 2011 6 28632 10.1371/journal.pone. 0028632 22174851
42. Host determinants of HIV-1 control in African Americans. Pelak K, Goldstein DB, Walley NM, Fellay J, Ge D, Shianna KV, Gumbs C, Gao X, Maia JM, Cronin KD, et al. J Infect Dis 2010 201 1141 1149 10.1086/651382 20205591
43. Common human genetic variants and HIV-1 susceptibility: a genome-wide survey in a homogeneous African population. Petrovski S, Fellay J, Shianna KV, Carpenetti N, Kumwenda J, Kamanga G, Kamwendo DD, Letvin NL, McMichael AJ, Haynes BF, et al. AIDS 2011 25 513 518 10.1097/QAD.0b013e328343817b 21160409
44. Genome-wide association study identifies single nucleotide polymorphism in DYRK1A associated with replication of HIV-1 in monocyte-derived macrophages. Bol SM, Moerland PD, Limou S, van Remmerden Y, Coulonges C, van Manen D, Herbeck JT, Fellay J, Sieberer M, Sietzema JG, et al. PLoS One 2011 6 17190 10.1371/journal.pone.0017190 21364930
45. Genomewide association study of a rapid progression cohort identifies new susceptibility alleles for AIDS (ANRS Genomewide Association Study 03). Le Clerc S, Limou S, Coulonges C, Carpentier W, Dina C, Taing L, Delaneau O, Labib T, Sladek R, Deveau C, et al. J Infect Dis 2009 200 1194 1201 10.1086/605892 19754311
46. APOBEC3G genetic variants and their influence on the progression to AIDS. An P, Bleiber G, Duggal P, Nelson G, May M, Mangeat B, Alobwede I, Trono D, Vlahov D, Donfield S, et al. J Virol 2004 78 11070 11076 10.1128/JVI.78.20. 11070-11076.2004 15452227 (Pubitemid 39299647)
47. Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H. Harari A, Ooms M, Mulder LCF, Simon V, J Virol 2009 83 295 303 10.1128/JVI.01665-08 18945781
48. Genetic influence of CXCR6 chemokine receptor alleles on PCP-mediated AIDS progression among African Americans. Duggal P, An P, Beaty TH, Strathdee SA, Farzadegan H, Markham RB, Johnson L, O'Brien SJ, Vlahov D, Winkler CA, Genes Immun 2003 4 245 250 10.1038/sj.gene.6363950 12761559 (Pubitemid 39562122)
49. Positive natural selection in the human lineage. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A, Mikkelsen TS, Altshuler D, Lander ES, Science 2006 312 1614 1620 10.1126/science.1124309 16778047 (Pubitemid 43902654)
50. Signals of recent positive selection in a worldwide sample of human populations. Pickrell JK, Coop G, Novembre J, Kudaravalli S, Li JZ, Absher D, Srinivasan BS, Barsh GS, Myers RM, Feldman MW, Pritchard JK, Genome Res 2009 19 5 826 837 10.1101/gr.087577.108 19307593
51. Genetic variation and recent positive selection in worldwide human populations: evidence from nearly 1 million SNPs. Lopez Herraez D, Bauchet M, Tang K, Theunert C, Pugach I, Li J, Nandineni MR, Gross A, Scholz M, Stoneking M, PLoS One 2009 4 7888 10.1371/journal.pone.0007888 19924308
52. Consistent effects of TSG101 genetic variability on multiple outcomes of exposure to human immunodeficiency virus type 1. Bashirova AA, Bleiber G, Qi Y, Hutcheson H, Yamashita T, Johnson RC, Cheng J, Alter G, Goedert JJ, Buchbinder S, et al. J Virol 2006 80 6757 6763 10.1128/JVI.00094-06 16809281 (Pubitemid 44025175)
53. Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Smith MW, Science 1997 277 959 965 10.1126/science.277.5328.959 9252328 (Pubitemid 27366682)
54. True HIV-1 infection in a pygmy. Gonzalez JP, Georges-Courbot MC, Martin PM, Mathiot CC, Salaun D, Georges AJ, Lancet 1987 1 1499 2885497 (Pubitemid 17080626)
55. HIV type 1 infection in Pygmy hunter gatherers is from contact with Bantu rather than from nonhuman primates. Ndembi N, Habakkuk Y, Takehisa J, Takemura T, Kobayashi E, Ngansop C, Songok E, Miura T, Ido E, Hayami M, et al. AIDS Res Hum Retroviruses 2003 19 435 439 10.1089/088922203765551773 12816089 (Pubitemid 36629962)
56. Update on HIV/SIV infections in Cameroon. Zekeng L, Philos Trans R Soc Lond B Biol Sci 2001 356 799 10.1098/rstb.2001.0858 11405923 (Pubitemid 32614653)
57. The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Gonzalez E, Kulkarni H, Bolivar H, Mangano A, Sanchez R, Catano G, Nibbs RJ, Freedman BI, Quinones MP, Bamshad MJ, et al. Science 2005 307 1434 1440 10.1126/science.1101160 15637236 (Pubitemid 40321934)
58. Analysis of west African hunters for foamy virus infections. Goepfert PA, Ritter GD Jr, Peng X, Gbakima AA, Zhang Y, Mulligan MJ, AIDS Res Hum Retroviruses 1996 12 1725 1730 10.1089/aid.1996.12.1725 8959250 (Pubitemid 26424052)
59. Coinfection with HIV-1 and simian foamy virus in West Central Africans. Switzer WM, Garcia AD, Yang C, Wright A, Kalish ML, Folks TM, Heneine W, J Infect Dis 2008 197 1389 1393 10.1086/587493 18444796 (Pubitemid 351706462)
60. Exposure to nonhuman primates in rural Cameroon. Wolfe ND, Prosser TA, Carr JK, Tamoufe U, Mpoudi-Ngole E, Torimiro JN, LeBreton M, McCutchan FE, Birx DL, Burke DS, Emerg Infect Dis 2004 10 2094 2099 10.3201/eid1012.040062 15663844 (Pubitemid 39587331)
61. APOBEC proteins and intrinsic resistance to HIV-1 infection. Malim MH, Philos Trans R Soc Lond B Biol Sci 2009 364 675 687 10.1098/rstb.2008.0185 19038776
62. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. Song B, Javanbakht H, Perron M, Park DH, Stremlau M, Sodroski J, J Virol 2005 79 3930 10.1128/JVI.79.7.3930-3937.2005 15767395 (Pubitemid 40388333)
63. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Pertel T, Hausmann S, Morger D, Züger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, et al. Nature 2011 472 361 365 10.1038/nature09976 21512573
64. A rare null allele potentially encoding a dominant-negative TRIM5alpha protein in Baka pygmies. Torimiro JN, Javanbakht H, Diaz-Griffero F, Kim J, Carr JK, Carrington M, Sawitzke J, Burke DS, Wolfe ND, Dean M, Sodroski J, Virology 2009 391 140 147 10.1016/j.virol.2009.05.038 19577266
65. A whole-genome association study of major determinants for host control of HIV-1. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, Weale M, Zhang K, Gumbs C, Castagna A, Cossarizza A, et al. Science 2007 317 944 947 10.1126/science.1143767 17641165 (Pubitemid 47301321)
66. Race-specific HIV-1 disease-modifying effects associated with CCR5 haplotypes. Gonzalez E, Bamshad M, Sato N, Mummidi S, Dhanda R, Catano G, Cabrera S, McBride M, Cao XH, Merrill G, et al. Proc Natl Acad Sci U S A 1999 96 12004 10.1073/pnas.96.21.12004 10518566 (Pubitemid 29502848)
67. Role of CCL3L1-CCR5 genotypes in the epidemic spread of HIV-1 and evaluation of vaccine efficacy. Kulkarni H, Marconi VC, Agan BK, McArthur C, Crawford G, Clark RA, Dolan MJ, Ahuja SK, PLoS One 2008 3 3671 10.1371/journal.pone.0003671 18989363
68. The spread and effect of HIV-1 infection in sub-Saharan Africa. Buve A, Bishikwabo-Nsarhaza K, Mutangadura G, Lancet 2002 359 2011 2017 10.1016/S0140-6736(02)08823-2 12076570 (Pubitemid 34663721)
69. Linkage disequilibrium in human populations. Lonjou C, Zhang W, Collins A, Tapper WJ, Elahi E, Maniatis N, Morton NE, Proc Natl Acad Sci U S A 2003 100 6069 6074 10.1073/pnas.1031521100 12721363 (Pubitemid 36576932)
70. Standardized subsets of the HGDP-CEPH Human Genome Diversity Cell Line Panel, accounting for atypical and duplicated samples and pairs of close relatives. Rosenberg NA, Ann Hum Genet 2006 70 841 847 10.1111/j.1469-1809.2006. 00285.x 17044859 (Pubitemid 44530648)
71. A second generation human haplotype map of over 3.1 million SNPs. Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, Gibbs RA, Belmont JW, Boudreau A, Hardenbol P, Leal SM, et al. Nature 2007 449 851 861 10.1038/nature06258 17943122 (Pubitemid 47598626)
72. Human immunodeficiency virus type 1, human protein interaction database at NCBI. Fu W, Sanders-Beer BE, Katz KS, Maglott DR, Pruitt KD, Ptak RG, Nucleic Acids Res 2009 37 417 D422 10.1093/nar/gkn708 18927109
73. The UCSC Genome Browser database: update 2011. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, Cline MS, Goldman M, Barber GP, Clawson H, Coelho A, et al. Nucleic Acids Res 2010 39 876 D882 20959295
74. Genotype, haplotype and copy-number variation in worldwide human populations. Jakobsson M, Scholz SW, Scheet P, Gibbs JR, VanLiere JM, Fung H-C, Szpiech ZA, Degnan JH, Wang K, Guerreiro R, et al. Nature 2008 451 998 1003 10.1038/nature06742 18288195 (Pubitemid 351301742)
75. R: A language and environment for statistical computing. http://www.R-project.org/
76. CCR2 chemokine receptor and AIDS progression. Smith M, Carrington M, Winkler C, Lomb D, Nat Med 1997 3 1052 1053 9334699 (Pubitemid 27444420)
77. A zinc-binding region in Vif binds Cul5 and determines cullin selection. Mehle A, Thomas ER, Rajendran KS, Gabuzda D, J Biol Chem 2006 281 17259 17265 10.1074/jbc.M602413200 16636053
78. Structure and functional interactions of the Tsg101 UEV domain. Pornillos O, Alam SL, Rich RL, Myszka DG, Davis DR, Sundquist WI, EMBO J 2002 21 2397 2406 10.1093/emboj/21.10.2397 12006492 (Pubitemid 34546712)
79. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, et al. Cell 2001 107 55 65 10.1016/S0092-8674(01)00506-2 11595185 (Pubitemid 32972037)
80. Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Donaghy H, Pozniak A, Gazzard B, Qazi N, Gilmour J, Gotch F, Patterson S, Blood 2001 98 2574 2576 10.1182/blood.V98.8.2574 11588058
81. Synergistic increases in intracellular Ca2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 Tat. El-Hage N, Gurwell JA, Singh IN, Knapp PE, Nath A, Hauser KF, Glia 2005 50 91 106 10.1002/glia.20148 15630704 (Pubitemid 40695264)
82. Primer3 on the WWW for general users and for biologist programmers. Rozen S, Skaletsky H, Methods Mol Biol 2000 132 365 386 10547847
83. Distinguishing forest and savanna African elephants using short nuclear DNA sequences. Ishida Y, Demeke Y, van Coeverden de Groot PJ, Georgiadis NJ, Leggett KE, Fox VE, Roca AL, J Hered 2011 102 610 616 10.1093/jhered/esr073 21775678
84. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, Kel OV, Ignatieva EV, Ananko EA, Podkolodnaya OA, Kolpakov FA, et al. Nucleic Acids Res 1998 26 362 367 10.1093/nar/26.1.362 9399875 (Pubitemid 28295292)