Massively parallel pyrosequencing highlights minority variants in the HIV-1 env quasispecies deriving from lymphomonocyte sub-populations

Retrovirology

Volumn 6, Issue , 2009, Pages

  Rozera, Gabriella ^a   Abbate, Isabella ^a   Bruselles, Alessandro ^a   Vlassi, Crhysoula ^a   D'Offizi, Gianpiero ^a   Narciso, Pasquale ^a   Chillemi, Giovanni ^b   Prosperi, Mattia ^a   Ippolito, Giuseppe ^a   Capobianchi, Maria R ^a  

^a NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^b CASPUR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; GLYCOPROTEIN GP 120; PROTEINASE INHIBITOR; RITONAVIR; RNA DIRECTED DNA POLYMERASE INHIBITOR; VASOPRESSIN V3 RECEPTOR; VIRUS ENVELOPE PROTEIN;

ADULT; AMINO ACID SEQUENCE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE AMPLIFICATION; GENETIC ALGORITHM; GENETIC HETEROGENEITY; GENETIC VARIABILITY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; MONOCYTE; PHYLOGENY; POLYMERASE CHAIN REACTION; PYROSEQUENCING; T LYMPHOCYTE; VIRION; VIRUS LOAD; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETIC POLYMORPHISM; GENETICS; ISOLATION AND PURIFICATION; LYMPHOCYTE; METHODOLOGY; MIDDLE AGED; PLASMA; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; CLUSTER ANALYSIS; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; LYMPHOCYTES; MALE; MIDDLE AGED; MONOCYTES; PHYLOGENY; PLASMA; POLYMORPHISM, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 63549147504     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-6-15     Document Type: Article

References (41)

1. Fisher AG Ensoli B Looney D Rose A Gallo RC Saag MS Shaw GM Hahn BH Wong-Staal F Biologically diverse molecular variants within a single HIV-1 isolate Nature 1988, 334:444-447 10.1038/334444a0 2841608
2. Coffin JM HIV population dynamics in vivo: Implications for genetic variation, pathogenesis, and therapy Science 1995, 267:483-489 10.1126/ science.7824947 7824947
3. Hwang SS Boyle TJ Lyerly HK Cullen BR Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1 Science 1991, 253:71-74 10.1126/science.1905842 1905842
4. Troyer RM Collins KR Abraha A Fraundorf E Moore DM Krizan RW Toossi Z Colebunders RL Jensen MA Mullins JI Vanham G Arts EJ Changes in Human Immunodeficiency Virus Type 1 Fitness and Genetic Diversity during Disease Progression J Virol 2005, 79:9006-9018 1168764 15994794 10.1128/ JVI.79.14.9006-9018.2005
5. Nowak P Karlsson AC Naver L Bohlin AB Piasek A Sönnerborg A The selection and evolution of viral quasispecies in HIV-1 infected children HIV Med 2002, 3:1-11 10.1046/j.1464-2662.2001.00097.x 12059945
6. Poss M Rodrigo AG Gosink JJ Learn GH De Vange Panteleef D Martin HL Bwayo J Kreiss JK Overbaugh J Evolution of Envelope Sequences from the Genital Tract and Peripheral Blood of Women Infected with Clade A Human Immunodeficiency Virus Type 1 J Virol 1998, 72:8240-8251 110179 9733867
7. Haggerty S Stevenson M Predominance of distinct viral genotypes in brain and lymph node compartments of HIV-1-infected individuals Viral Immunol 1991, 4:123-131 1684709
8. Hughes ES Bell JE Simmonds P Investigation of the dynamics of the spread of human immunodeficiency virus to brain and other tissues by evolutionary analysis of sequences from the 17 gag and env genes J Virol 1997, 71:1272-1280 191182 8995651
9. Epstein LG Kuiken C Blumberg BM Hartman S Sharer LR Clement M Goudsmit J HIV-1 V3 domain variation in brain and spleen of children with AIDS: tissue-specific evolution within host-determined quasispecies Virology 1991, 180:583-590 10.1016/0042-6822(91)90072-J 1989385
10. Zhu T Muthui D Holte S Nickle D Feng F Brodie S Hwangbo Y Mullins JI Corey L Evidence for human immunodeficiency virus type 1 replication in vivo in CD14(+) monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy J Virol 2002, 76:707-716 136806 11752161 10.1128/JVI.76.2.707-716.2002
11. Fulcher JA Hwangbo Y Zioni R Nickle D Lin X Heath L Mullins JI Corey L Zhu T Compartmentalization of Human Immunodeficiency Virus Type 1 between Blood Monocytes and CD4+T Cells during Infection J Virol 2004, 78:7883-7893 446117 15254161 10.1128/JVI.78.15.7883-7893.2004
12. Chun TW Davey RT Ostrowski M Shawn Justement J Engel D Mullins JI Fauci AS Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy Nat Med 2000, 6:736-737 10.1038/77481 10888912
13. Imamichi H Crandall KA Natarajan V Jiang MK Dewar RL Berg S Gaddam A Bosche M Metcalf JA Davey RT Clifford Lane H Human immunodeficiency virus type 1 quasi species that rebound after discontinuation of highly active antiretroviral therapy are similar to the viral quasispecies present before initiation of therapy J Infect Dis 2001, 183:36-50 10.1086/317641 11106537
14. Llewellyn N Zioni R Zhu H Andrus T Xu Y Corey L Zhu T Continued evolution of HIV-1 circulating in blood monocytes with antiretroviral therapy: Genetics analysis of HIV-1 in monocytes and CD4+ T cells of patients with discontinued therapy J Leukoc Biol 2006, 80:1118-26 10.1189/jlb.0306144 17056765
15. Lambotte O Chaix ML Gubler B Nasreddine N Wallon C Goujard C Rouzioux C Taoufik Y Delfraissy JF The lymphocyte HIV reservoirs in patients on long-term HAART is a memory of virus evolution AIDS 2004, 18:1147-58 10.1097/00002030-200405210-00008 15166530
16. Delobel P Sandres-Sauné K Cazabat M L'Faqihi FE Aquilina C Obadia M Pasquier C Marchou B Massip P Izopet J Persistence of distinct HIV-1 populations in blood monocytes and naive and memory CD4 T cells during prolonged suppressive HAART AIDS 2005, 19:1739-50 10.1097/ 01.aids.0000183125.93958.26 16227781
17. Capobianchi MR Fais S Castilletti C Gentile M Ameglio F Dianzani F A simple and reliable method to detect cell membrane proteins on infectious human immunodeficiency virus type 1 particles J Infect Dis 1994, 169:886-9 7907644
18. Saarloos M Sullivan BL Czerniewski MA Parameswar KD Spear GT Detection of HLA-DR associated with monocytotropic, primary, and plasma isolates of human immunodeficiency virus type 1 J Virol 1997, 71:1640-1643 191223 8995692
19. Lawn SD Roberts BD Griffin GE Folks TM Butera ST Cellular Compartments of Human Immunodeficiency Virus Type 1 Replication In Vivo: Determination by Presence of Virion-Associated Host Proteins and Impact of Opportunistic Infection J Virol 2000, 74:139-145 111522 10590100 10.1128/JVI.74.21.10256-10259.2000
20. Abbate I Dianzani F Turriziani O Antonelli G D'Offizi G Galati V Pierdominici M Pandolfi F Capobianchi MR Changes in host cell molecules acquired by circulating HIV-1 in patients treated with HAART AIDS 2001, 15:11-16 10.1097/00002030-200101050-00004 11192851
21. Abbate I Cappiello G Longo R Ursitti A Spanò A Calcaterra S Dianzani F Antinori A Capobianchi MR Cell membrane proteins and quasispecies compartmentalization of CSF and plasma HIV-1 from aids patients with neurological disorders Infect Genet Evol 2005, 5:247-53 10.1016/j.meegid.2004.08.006 15737916
22. Toossi Z Mayana-Kizza H Lawn SD Hirsch CS Lupo LD Butera ST Dinamic Variation in the Cellular Origin of HIV Type 1 during Treatment of Tuberculosis in Dually Infected Subjects AIDS Research and Human Retroviruses 2007, 23:93-100 10.1089/aid.2006.0050
23. Wang C Mitsuya Y Gharizadeh B Ronaghi M Shafer RW Characterization of mutation spectra with ultra-deep pyrosequencing: Application to HIV-1 drug resistance Genome Res 2007, 17:1195-201 1933516 17600086 10.1101/ gr.6468307
24. Hoffmann C Minkah N Leipzig J Wang G Arens MQ Tebas P Bushman FD DNA bar coding and pyrosequencing to identify rare HIV drug resistance mutations Nucl Acids Res 2007, 35:e91 1934997 17576693 10.1093/nar/gkm435
25. Mitsuya Y Varghese V Wang C Liu TF Holmes SP Jayakumar P Gharizadeh B Ronaghi M Klein D Fessel WJ Shafer RW Minority HIV-1 Variants in Antiretroviral Naive Persons with Reverse Transcriptase Codon 215 Revertant Mutations J Virol 2008, 82:10747-55 10.1128/JVI.01827-07 18715933
26. Margulies M Egholm M Altman WE Attiya S Bader JS Bemben LA Berka J Braverman MS Chen YJ Chen Z Dewell SB Du L Fierro JM Gomes XV Brian C Godwin BC He W Helgesen S Ho CH Irzyk GP Jando SC Alenquer MLI Jarvie TP Jirage KB Kim JB Knight JR Lanza JR Leamon JH Lefkowitz SM Lei M Jing Li J Lohman KL Lu H Makhijani VB McDade KE McKenna MP Eugene W Myers Ew Nickerson E Nobile JR Plant R Puc BP Ronan MT Roth GT Sarkis GJ Simons JF Simpson JW Srinivasan M Tartaro KR Tomasz A Vogt KA Volkmer GA Shally H Wang SH Wang Y Weiner MP Yu P Begley RF Rothberg JM Genome sequencing in microfabricated high-density picolitre reactors Nature 2005, 437:376-80 1464427 16056220
27. Rice P Longden I Bleasby A EMBOSS: The European Molecular Biology Open Software Suite Trends Genet 2000, 16:276-7 10.1016/S0168-9525(00)02024-2 10827456
28. Edgar RC MUSCLE: A multiple sequence alignment method with reduced time and space complexity BMC Bioinformatics 2004, 19:5-113 15318951 517706
29. Huse SM Huber JA Morrison HG Sogin ML Welch DM Accuracy and quality of massively parallel DNA pyrosequencing Genome Biol 2007, 8:R143 2323236 17659080 10.1186/gb-2007-8-7-r143
30. Jensen MA Li FS van't Wout AB Nickle DC Shriner D He HX McLaughlin S Shankarappa R Margolick JB Mullins JI Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of HIV-1 env V3 loop sequences J Virol 2003, 77:13376-13388 296044 14645592 10.1128/JVI.77.24.13376-13388.2003
31. Garbuglia AR Calcaterra S D'Offizi G Topino S Narciso P Lillo F Girardi E Capobianchi MR HIV-1 DNA burden dynamics in CD4 T cells and monocytes in patients undergoing a transient therapy interruption J Med Virol 2004, 74:373-81 10.1002/jmv.20188 15368526
32. Fais S Capobianchi MR Abbate I Castilletti C Gentile M Cordiali Fei P Ameglio F Dianzani F Unidirectional budding of HIV-1 at the site of cell-to-cell contact is associated with co-polarization of intercellular adhesion molecules and HIV-1 viral matrix protein AIDS 1995, 9:329-335 10.1097/00002030-199509040-00003 7794538
33. Joos B Fischer M Kuster H Pillai SK Wong JK Böni J Hirschel B Weber R Trkola A Günthard HF Swiss HIV Cohort Study HIV rebounds from latently infected cells, rather than from continuing low-level replication Proc Natl Acad Sci USA 2008, 105:16725-16730 10.1073/ pnas.0804192105 18936487
34. Lehmann C Daumer M Boussaad I Sing T Beerenwinkel N Lengauer T Schmeisser N Wyen C Fätkenheuer G Kaiser R Stable coreceptor usage of HIV in patients with ongoing treatment failure on HAART J Clin Virol 2006, 37:300-4 10.1016/j.jcv.2006.08.008 17005445
35. Kupfer B Sing T Schuffer P Hall R Kurz R McKeown A Schneweis KE Eberl W Oldenburg J Brackmann HH Rockstroh JK Spengler U Daumer MP Kaiser R Lengauer MB Fifteen years of env C2V3C3 evolution in six individuals infected clonally with human immunodeficiency virus type 1 J Med Virol 2007, 79:1629-39 10.1002/jmv.20976 17854039
36. Jayakumar P Berger I Autschbach F Weinstein M Funke B Verdin E Goldsmith MA Keppler OT Tissue Resident Macrophages Are Productively Infected Ex Vivo by Primary X4 Isolates of Human Immunodeficiency Virus Type 1 J Virol 2005, 79:5220-5226 1069582 15795306 10.1128/JVI.79.8.5220-5226.2005
37. Chen S Tuttle DL Oshier JT Knot HJ Streit WJ Goodenow MM Harrison JK Transforming growth factor-β1 increases CXCR4 expression, stromal-derived factor-1α-stimulated signalling and human immunodeficiency virus-1 entry in human monocyte-derived macrophages Immunology 2005, 114:565-574 1782104 15804293 10.1111/ j.1365-2567.2004.02110.x
38. De Mendoza C Rodriguez C Garcìa F Eiros JM Ruìz L Caballero E Aguilera A Leiva P Colomina J Gutierrez F Del Romero J Aguero J Soriano V on behalf of the Spanish HIV Seroconverter Study Group Prevalence of X4 tropic viruses in patients recently infected with HIV-1 and lack of association with transmission of drug resistance J Antimicrobiol Chemotherapy 2007, 59:698-704 10.1093/jac/dkm012
39. Repik A Richards KH Clapham PR The promise of CCR5 antagonists as new therapies for HIV-1 Curr Opin Investig Drugs 2007, 8:130-9 17328229
40. Bushman FD Hoffmann C Ronen K Malani N Minkah N Rose HM Tebas P Wang GP Massively parallel pyrosequencing in HIV research AIDS 2008, 22:1411-1415 10.1097/QAD.0b013e3282fc972e 18614863
41. Bailey JR Sedaghat AR Kieffer T Brennan T Lee PK Wind-Rotolo M Haggerty CM Kamireddi AR Liu Y Lee J Persaud D Gallant JE Cofrancesco J Jr Quinn TC Wilke CO Ray SC Siliciano JD Nettles RE Siliciano RF Residual Human Immunodeficiency Virus Type 1 viremia in some patients on antiretroviral therapy is dominated by a small number of invariant clones rarely found in circulating CD4+ T cells J Virol 2006, 80:6441-6457 1488985 16775332 10.1128/JVI.00591-06