Discovery and characterization of distinct simian pegiviruses in three wild African old world monkey species

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Sibley, Samuel D ^a   Lauck, Michael ^b   Bailey, Adam L ^b   Hyeroba, David ^c   Tumukunde, Alex ^c   Weny, Geoffrey ^c   Chapman, Colin A ^c,d   O'Connor, David H ^b,e   Goldberg, Tony L ^a,c,e   Friedrich, Thomas C ^a,e  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c MAKERERE UNIVERSITY   (Uganda)

^d MCGILL UNIVERSITY   (Canada)

^e UNIVERSITY OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' UNTRANSLATED REGION; ARTICLE; CERCOPITHECIDAE; CERCOPITHECUS ASCANIUS; FLAVIVIRUS; GENE FUNCTION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC VARIABILITY; MONOPHYLY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PAPIO ANUBIS; PHYLOGENY; PROCOLOBUS TEPHROSCELES; SIMIAN PEGIVIRUS; UGANDA; VIRUS DETECTION; VIRUS LOAD; VIRUS STRAIN; ANIMAL; CERCOPITHECUS; COLOBUS; FLAVIVIRIDAE; GENETICS; ISOLATION AND PURIFICATION; MONKEY DISEASE; VIROLOGY; VIRUS GENOME;

ANIMALS; CERCOPITHECUS; COLOBUS; FLAVIVIRIDAE; GENOME, VIRAL; MONKEY DISEASES; PAPIO ANUBIS; PHYLOGENY;

EID: 84903388741     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098569     Document Type: Article

References (98)

1. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, et al. (1989) Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244: 359-362. (Pubitemid 19117877)
2. Simons JN, Leary TP, Dawson GJ, Pilot-Matias TJ, Muerhoff AS, et al. (1995) Isolation of novel virus-like sequences associated with human hepatitis. Nat Med 1: 564-569.
3. Stapleton JT, Foung S, Muerhoff AS, Bukh J, Simmonds P (2011) The GB viruses: a review and proposed classification of GBV-A, GBV-C (HGV), and GBV-D in genus Pegivirus within the family Flaviviridae. J Gen Virol 92: 233-246.
4. Stapleton JT, Bukh J, Muerhoff AS, Foung S, Simmonds P (2012) Assignment of human, simian and bat pegiviruses (previously described as GBV-A, GBV-C, and GBV-D) as members of a new Genus (Pegivirus) within the Flaviviridae. Available: http://talk.ictvonline.org/files/ictv-official- taxonomy-updates-since-the-8th- report/m/vertebrate-official/4486.aspx. Accessed 15 July 2013.
5. Stapleton JT (2003) GB virus type C/Hepatitis G virus. Semin Liver Dis 23: 137-148.
6. Schaluder GG, Dawson GJ, Simons JN, Pilot-Matias TJ, Gutierrez RA, et al. (1995) Molecular and serologic analysis in the transmission of the GB hepatitis agents. J Med Virol 46: 81-90.
7. Bukh J, Apgar CL (1997) Five new or recently discovered (GBV-A) virus species are indigenous to New World monkeys and may constitute a separate genus of the Flaviviridae. Virology 229: 429-436.
8. Adams NJ, Prescott LE, Jarvis LM, Lewis JC, McClure MO, et al. (1998) Detection in chimpanzees of a novel flavivirus related to GB virus-C/hepatitis G virus. J Gen Virol 79: 1871-1877. (Pubitemid 28391174)
9. Birkenmeyer LG, Desai SM, Muerhoff AS, Leary TP, Simons JN, et al. (1998) Isolation of a GB virus-related genome from a chimpanzee. J Med Virol 56: 44-51. (Pubitemid 28380429)
10. Chandriani S, Skewes-Cox P, Zhong W, Ganem DE, Divers TJ, et al. (2013) Identification of a previously undescribed divergent virus from the Flaviviridae family in an outbreak of equine serum hepatitis. Proc Natl Acad Sci. 110: E1407-E1415.
11. Kapoor A, Simmonds P, Cullen JM, Scheel T, Medina JL, et al. (2013) Identification of a pegivirus (GBV-like virus) that infects horses. J Virol. 87: 7185-7190.
12. Quan P-L, Firth C, Conte JM, Williams SH, Zambrana-Torrelio CM, et al. (2013) Bats are a major natural reservoir for hepaciviruses and pegiviruses. Proc Natl Acad Sci. 110: 8194-8199.
13. Epstein JH, Quan P-L, Briese T, Street C, Jabado O, et al. (2010) Identification of GBV-D, a Novel GB-like Flavivirus from Old World Frugivorous Bats (Pteropus giganteus) in Bangladesh. PLoS Pathog 6: e1000972. doi:10.1371/journal.ppat.1000972.
14. Kapoor A, Simmonds P, Scheel TKH, Hjelle B, Cullen JM, et al. (2013) Identification of Rodent Homologs of Hepatitis C Virus and Pegiviruses. mBio 4: e00216-13.
15. Drexler JF, Corman VM, Müller MA, Lukashev AN, Gmyl A, et al. (2013) Evidence for Novel Hepaciviruses in Rodents. PLoS Pathog 9: e1003438. doi:10.1371/journal.ppat.1003438.
16. Muerhoff AS, Leary TP, Sathar MA, Dawson GJ, Desai SM (2005) African origin of GB virus C determined by phylogenetic analysis of a complete genotype 5 genome from South Africa. J Gen Virol 86: 1729-1735. (Pubitemid 40766885)
17. Hitzler WE, Runkel S (2004) Prevalence, persistence and liver enzyme levels of HGV RNA-positive blood donors determined by large-scale screening and transmission by blood components. Clin Lab 50: 25-31. (Pubitemid 38268392)
18. Bhattarai N, Stapleton JT (2012) GB virus C: the good boy virus? Trends Microbiol 20: 124-130.
19. Mohr EL, Stapleton JT (2009) GB virus type C interactions with HIV: the role of envelope glycoproteins. J Viral Hepat 16: 757-768.
20. Giret MTM, Miraglia JL, Sucupira MCA, Nishiya A, Levi JE, et al. (2011) Prevalence, Incidence Density, and Genotype Distribution of GB Virus C Infection in a Cohort of Recently HIV-1-Infected Subjects in Sao Paulo, Brazil. PLoS ONE 6: e18407. doi:10.1371/journal.pone.0018407.
21. Rey D, Vidinic-Moularde J, Meyer P, Schmitt C, Fritsch S, et al. (2000) High prevalence of GB virus C/hepatitis G virus RNA and antibodies in patients infected with human immunodeficiency virus type 1. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol 19: 721-724.
22. Schwarze-Zander C, Blackard JT, Zheng H, Addo MM, Lin W, et al. (2006) GB virus C (GBV-C) infection in hepatitis C virus (HCV)/HIV-coinfected patients receiving HCV treatment: importance of the GBV-C genotype. J Infect Dis 194: 410-419. (Pubitemid 44162651)
23. Bhanich Supapol W, Remis RS, Raboud J, Millson M, Tappero J, et al. (2011) Prevalence and correlates of GB virus C infection in HIV-infected and HIV-uninfected pregnant women in Bangkok, Thailand. J Med Virol 83: 33-44.
24. Charrel RN, De Micco P, de Lamballerie X (1999) Phylogenetic analysis of GB viruses A and C: evidence for cospeciation between virus isolates and their primate hosts. J Gen Virol 80: 2329-2335. (Pubitemid 29408358)
25. Romano CM, Zanotto PM de A, Holmes EC (2008) Bayesian coalescent analysis reveals a high rate of molecular evolution in GB virus C. J Mol Evol 66: 292-297.
26. Pavesi A (2001) Origin and evolution of GBV-C/hepatitis G virus and relationships with ancient human migrations. J Mol Evol 53: 104-113.
27. Bhattarai N, McLinden JH, Xiang J, Landay AL, Chivero ET, et al. (2013) GB Virus C Particles Inhibit T Cell Activation via Envelope E2 Protein-Mediated Inhibition of TCR Signaling. J Immunol Baltim Md 1950 190: 6351-6359.
28. Goldberg TL, Paige SB, Chapman CA (2012) The Kibale EcoHealth Project: exploring connections among human health, animal health, and landscape dynamics in western Uganda. In: Aguirre AA, Ostfeld RS, Daszak P (ed.), New directions in conservation medicine: Applied cases of ecological health. Oxford; New York: Oxford University Press. 452-465.
29. Lauck M, Hyeroba D, Tumukunde A, Weny G, Lank SM, et al. (2011) Novel, divergent simian hemorrhagic fever viruses in a wild Ugandan red colobus monkey discovered using direct pyrosequencing. PloS One 6: e19056. doi:10.1371/journal. pone.0019056.
30. Goldberg TL, Chapman CA, Cameron K, Saj T, Karesh WB, et al. (2008) Serologic evidence for novel poxvirus in endangered red Colobus monkeys, Western Uganda. Emerg Infect Dis 14: 801-803. (Pubitemid 351838647)
31. Salyer SJ, Gillespie TR, Rwego IB, Chapman CA, Goldberg TL (2012) Epidemiology and Molecular Relationships of Cryptosporidium spp. in People, Primates, and Livestock from Western Uganda. PLoS Negl Trop Dis 6: e1597. doi:10.1371/journal.pntd.0001597.
32. Johnston AR, Gillespie TR, Rwego IB, McLachlan TLT, Kent AD, et al. (2010) Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Negl Trop Dis 4: e683. doi:10.1371/journal.pntd.0000683.
33. Thurber MI, Ghai RR, Hyeroba D, Weny G, Tumukunde A, et al. (2013) Co-infection and cross-species transmission of divergent Hepatocystis lineages in a wild African primate community. Int J Parasitol 43: 613-619. doi:10.1016/j.ijpara.2013.03.002.
34. Goldberg TL, Gillespie TR, Rwego IB, Estoff EL, Chapman CA (2008) Forest Fragmentation as Cause of Bacterial Transmission among Nonhuman Primates, Humans, and Livestock, Uganda. Emerg Infect Dis 14: 1375-1382. doi:10.3201/eid1409.071196.
35. Mohr EL, Murthy KK, McLinden JH, Xiang J, Stapleton JT (2011) The natural history of non-human GB virus C in captive chimpanzees. J Gen Virol 92: 91-100.
36. Simons JN, Desai SM, Schultz DE, Lemon SM, Mushahwar IK (1996) Translation initiation in GB viruses A and C: evidence for internal ribosome entry and implications for genome organization. J Virol 70: 6126-6135. (Pubitemid 26266829)
37. Thurner C, Witwer C, Hofacker IL, Stadler PF (2004) Conserved RNA secondary structures in Flaviviridae genomes. J Gen Virol 85: 1113-1124. (Pubitemid 38659775)
38. Bernhart SH, Hofacker IL, Will S, Gruber AR, Stadler PF (2008) RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinformatics 9: 474.
39. Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL (2008) The Vienna RNA Websuite. Nucleic Acids Res 36: W70-W74.
40. Chang K-S, Luo G (2006) The polypyrimidine tract-binding protein (PTB) is required for efficient replication of hepatitis C virus (HCV) RNA. Virus Res 115: 1-8. (Pubitemid 41772475)
41. Yanagi M, St Claire M, Emerson SU, Purcell RH, Bukh J (1999) In vivo analysis of the 3′ untranslated region of the hepatitis C virus after in vitro mutagenesis of an infectious cDNA clone. Proc Natl Acad Sci. 96: 2291-2295. (Pubitemid 29117907)
42. Wang L, Jeng K-S, Lai MMC (2011) Poly(C)-binding protein 2 interacts with sequences required for viral replication in the hepatitis C virus (HCV) 5′ untranslated region and directs HCV RNA replication through circularizing the viral genome. J Virol 85: 7954-7964.
43. Holcik M, Liebhaber SA (1997) Four highly stable eukaryotic mRNAs assemble 3′ untranslated region RNA-protein complexes sharing cis and trans components. Proc Natl Acad Sci 94: 2410-2414.
44. Cuceanu NM, Tuplin A, Simmonds P (2001) Evolutionarily conserved RNA secondary structures in coding and non-coding sequences at the 39 end of the hepatitis G virus/GB-virus C genome. J Gen Virol 82: 713-722. (Pubitemid 32280028)
45. Mandl CW, Heinz FX, Puchhammer-Stóckl E, Kunz C (1991) Sequencing the termini of capped viral RNA by 5′-3′ ligation and PCR. BioTechniques 10: 484-486.
46. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
47. Reynolds SM, Kall L, Riffle ME, Bilmes JA, Noble WS (2008) Transmembrane Topology and Signal Peptide Prediction Using Dynamic Bayesian Networks. PLoS Comput Biol 4. e1000213. doi:10.1371/journal.pcbi.1000213.
48. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
49. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, et al. (2005) Protein Identification and Analysis Tools on the ExPASy Server. In: Walker JM (ed.), The Proteomics Protocols Handbook. Totowa, NJ: Humana Press. 571-607.
50. Erker JC, Desai SM, Leary TP, Chalmers ML, Montes CC, et al. (1998) Genomic analysis of two GB virus A variants isolated from captive monkeys. J Gen Virol 79: 41-45. (Pubitemid 28039297)
51. Welbourn S, Pause A (2006) HCV NS2/3 Protease. Available: http://www.ncbi.nlm.nih.gov/books/NBK1622/. Accessed 2013 Mar 14.
52. Lin C (2006) HCV NS3-4A Serine Protease. Available: http://www.ncbi.nlm. nih.gov/books/NBK1623/. Accessed 2013 Mar 14.
53. Belyaev AS, Chong S, Novikov A, Kongpachith A, Masiarz FR, et al. (1998) Hepatitis G Virus Encodes Protease Activities Which Can Effect Processing of the Virus Putative Nonstructural Proteins. J Virol 72: 868-872. (Pubitemid 28048915)
54. Lee YJ, Kang H, Rho S-H, Eom SH, Park WJ (2001) Assessment of Substrate Specificity of Hepatitis G Virus NS3 Protease by a Genetic Method. Biochem Biophys Res Commun 286: 171-175. (Pubitemid 32917665)
55. George SL, Varmaz D, Tavis JE, Chowdhury A (2012) The GB Virus C (GBV-C) NS3 Serine Protease Inhibits HIV-1 Replication in a CD4+ T Lymphocyte Cell Line without Decreasing HIV Receptor Expression. PLoS ONE 7: e30653. doi:10.1371/journal.pone.0030653.
56. Koonin EV, Dolja VV (1993) Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28: 375-430. (Pubitemid 23294324)
57. Koonin EV (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J Gen Virol 72: 2197-2206.
58. Tellinghuisen TL, Paulson MS, Rice CM (2006) The NS5A Protein of Bovine Viral Diarrhea Virus Contains an Essential Zinc-Binding Site Similar to That of the Hepatitis C Virus NS5A Protein. J Virol 80: 7450-7458. (Pubitemid 44092567)
59. Feuerstein S, Solyom Z, Aladag A, Favier A, Schwarten M, et al. (2012) Transient structure and SH3 interaction sites in an intrinsically disordered fragment of the hepatitis C virus protein NS5A. J Mol Biol 420: 310-323.
60. Gupta G, Qin H, Song J (2012) Intrinsically Unstructured Domain 3 of Hepatitis C Virus NS5A Forms a "Fuzzy Complex" with VAPB-MSP Domain Which Carries ALS-Causing Mutations. PLoS ONE 7: e39261. doi:10.1371/journal. pone.0039261.
61. Lauck M, Sibley SD, Lara J, Purdy MA, Khudyakov Y, et al. (2013) A novel hepacivirus with an unusually long and intrinsically disordered NS5A protein in a wild Old World primate. J. Virol. 87: 8971-8981.
62. Dosztányi Z, Csizmok V, Tompa P, Simon I (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21: 3433-3434. (Pubitemid 41222453)
63. Dosztányi Z, Mészáros B, Simon I (2009) ANCHOR: web server for predicting protein binding regions in disordered proteins. Bioinforma Oxf Engl 25: 2745-2746.
64. Mészáros B, Simon I, Dosztányi Z (2009) Prediction of Protein Binding Regions in Disordered Proteins. PLoS Comput Biol 5: e1000376. doi:10.1371/journal.pcbi.1000376.
65. Dinkel H, Michael S, Weatheritt RJ, Davey NE, Van Roey K, et al. (2012) ELM-the database of eukaryotic linear motifs. Nucleic Acids Res 40: D242-251.
66. Bouwmeester T, Bauch A, Ruffner H, Angrand P-O, Bergamini G, et al. (2004) A physical and functional map of the human TNF-α/NF-κB signal transduction pathway. Nat Cell Biol 6: 97-105. (Pubitemid 38425708)
67. Takeuchi M, Rothe M, Goeddel DV (1996) Anatomy of TRAF2 distinct domains for nuclear factor-κB activation and association with tumor necrosis factor signaling proteins. J Biol Chem 271: 19935-19942.
68. Takahashi K, Hijikata M, Hino K, Mishiro S (1997) Entire polyprotein-ORF sequences of Japanese GBV-C/HGV isolates: implications for new genotypes. Hepatol Res 8: 139-148. (Pubitemid 27382069)
69. Lyons S, Kapoor A, Sharp C, Schneider BS, Wolfe ND, et al. (2012) Nonprimate Hepaciviruses in Domestic Horses, United Kingdom. Emerg Infect Dis 18: 1976-1982.
70. Burbelo PD, Dubovi EJ, Simmonds P, Medina JL, Henriquez JA, et al. (2012) Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J Virol 86: 6171-6178.
71. Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, et al. (2011) A Molecular Phylogeny of Living Primates. PLoS Genet 7: e1001342. doi:10.1371/journal.pgen.1001342.
72. Leary TP, Desai SM, Yamaguchi J, Chalmers ML, Schlauder GG, et al. (1996) Species-specific variants of GB virus A in captive monkeys. J Virol 70: 9028-9030. (Pubitemid 26378492)
73. Leary TP, Desai SM, Erker JC, Mushahwar IK (1997) The sequence and genomic organization of a GB virus A variant isolated from captive tamarins. J Gen Virol 78: 2307-2313. (Pubitemid 27387045)
74. Pybus OG, Gray RR (2013) Virology: The virus whose family expanded. Nature 498: 310-311.
75. Ghai R, Sibley SD, Lauck M, Dinis J, Bailey AL, et al. (2013) Deep sequencing identifies two genotypes and high viral genetic diversity of human pegivirus (GB virus C) among rural Ugandan patients. J Gen Virol. 94: 2670-2678.
76. Lauck M, Alvarado-Mora MV, Becker EA, Bhattacharya D, Striker R, et al. (2012) Analysis of Hepatitis C Virus Intra-Host Diversity Across The Coding Region by Ultra-Deep Pyrosequencing. J Virol. 86: 3952-3960.
77. Plumptre AJ, Davenport TRB, Behangana M, Kityo R, Eilu G, et al. (2007) The biodiversity of the Albertine Rift. Biol Conserv 134: 178-194. (Pubitemid 44816316)
78. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, et al. (2008) Global trends in emerging infectious diseases. Nature 451: 990-993. (Pubitemid 351301726)
79. Goldberg TL, Sintasath DM, Chapman CA, Cameron KM, Karesh WB, et al. (2009) Coinfection of Ugandan red colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) with novel, divergent delta-, lenti-, and spumaretroviruses. J Virol 83: 11318-11329.
80. Bukh J, Kim JP, Govindarajan S, Apgar CL, Foung SK, et al. (1998) Experimental infection of chimpanzees with hepatitis G virus and genetic analysis of the virus. J Infect Dis 177: 855-862. (Pubitemid 28155136)
81. Kryazhimskiy S, Plotkin JB (2008) The Population Genetics of dN/dS. PLoS Genet 4: e1000304. doi:10.1371/journal.pgen.1000304.
82. Parreira R, Branco C, Piedade J, Esteves A (2012) GB virus C (GBV-C) evolutionary patterns revealed by analyses of reference genomes, E2 and NS5B sequences amplified from viral strains circulating in the Lisbon area (Portugal). Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 12: 86-93.
83. Tillmann HL, Heiken H, Knapik-Botor A, Heringlake S, Ockenga J, et al. (2001) Infection with GB virus C and reduced mortality among HIV-infected patients. N Engl J Med 345: 715-724.
84. Heringlake S, Ockenga J, Tillmann HL, Trautwein C, Meissner D, et al. (1998) GB virus C/hepatitis G virus infection: a favorable prognostic factor in human immunodeficiency virus-infected patients? J Infect Dis 177: 1723-1726. (Pubitemid 28243603)
85. Cheng Y, Zhang W, Li J, Li B a, Zhao J m, et al. (2000) Serological and histological findings in infection and transmission of GBV-C/HGV to macaques. J Med Virol 60: 28-33.
86. Ren H, Zhu F-L, Cao M-M, Wen X-Y, Zhao P, et al. (2005) Hepatitis G virus genomic RNA is pathogenic to Macaca mulatta. World J Gastroenterol WJG 11: 970-975. (Pubitemid 40347747)
87. Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM (2011) Host Phylogeny Determines Viral Persistence and Replication in Novel Hosts. PLoS Pathog 7: e1002260. doi:10.1371/journal.ppat.1002260.
88. Zhang M, Gaschen B, Blay W, Foley B, Haigwood N, et al. (2004) Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14: 1229-1246. (Pubitemid 39585357)
89. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564-577. (Pubitemid 47171631)
90. Abascal F, Zardoya R, Telford MJ (2010) TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. Available: http://nar.oxfordjournals.org/content/early/2010/04/30/nar.gkq291. Accessed 17 July 2013.
91. Xia X (2013) DAMBE5: A comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol. 38: W7-W13.
92. Guindon S, Gascuel O (2003) A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood. Syst Biol 52: 696-704. (Pubitemid 37365050)
93. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28: 2731-2739.
94. Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinforma Oxf Engl 26: 2455-2457.
95. Martin DP, Lemey P, Lott M, Moulton V, Posada D, et al. (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26: 2462-2463.
96. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, et al. (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73: 152-160. (Pubitemid 28565356)
97. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426. (Pubitemid 16010523)
98. Korber B (2000) HIV Signature and Sequence Variation Analysis. In: Rodrigo AG, Learn GH. (eds.), Computational Analysis of HIV Molecular Sequences. Dordrecht, Netherlands: Kluwer Academic Publishers. 55-72.