Genital Tract Sequestration of SIV following Acute Infection
We characterized the evolution of simian immunodeficiency virus (SIV) in the male genital tract by examining blood- and semen-associated virus from experimentally and sham vaccinated rhesus monkeys during primary infection. At the time of peak virus replication, SIV sequences were intermixed between the blood and semen supporting a scenario of high-level virus “spillover” into the male genital tract. However, at the time of virus set point, compartmentalization was apparent in 4 of 7 evaluated monkeys, likely as a consequence of restricted virus gene flow between anatomic compartments after the resolution of primary viremia. These findings suggest that SIV replication in the male genital tract evolves to compartmentalization after peak viremia resolves.
Vyšlo v časopise:
Genital Tract Sequestration of SIV following Acute Infection. PLoS Pathog 7(2): e32767. doi:10.1371/journal.ppat.1001293
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001293
Souhrn
We characterized the evolution of simian immunodeficiency virus (SIV) in the male genital tract by examining blood- and semen-associated virus from experimentally and sham vaccinated rhesus monkeys during primary infection. At the time of peak virus replication, SIV sequences were intermixed between the blood and semen supporting a scenario of high-level virus “spillover” into the male genital tract. However, at the time of virus set point, compartmentalization was apparent in 4 of 7 evaluated monkeys, likely as a consequence of restricted virus gene flow between anatomic compartments after the resolution of primary viremia. These findings suggest that SIV replication in the male genital tract evolves to compartmentalization after peak viremia resolves.
Zdroje
1. PilcherCD
ShugarsDC
FiscusSA
MillerWC
MenezesP
2001 HIV in body fluids during primary HIV infection: implications for pathogenesis, treatment and public health. Aids 15 837 845
2. PilcherH
2004 Snapshot of a pandemic. Nature 430 134 135
3. PilcherCD
EronJJJr
VemazzaPL
BattegayM
HarrT
2001 Sexual transmission during the incubation period of primary HIV infection. Jama 286 1713 1714
4. QuinnTC
WawerMJ
SewankamboN
SerwaddaD
LiC
2000 Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 342 921 929
5. GrayRH
WawerMJ
BrookmeyerR
SewankamboNK
SerwaddaD
2001 Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 357 1149 1153
6. WhitneyJB
LuedemannC
HraberP
RaoSS
MascolaJR
2009 T cell vaccination reduces SIV in semen. J Virol 83 20 10840 3
7. PilcherCD
TienHC
EronJJJr
VernazzaPL
LeuSY
2004 Brief but efficient: acute HIV infection and the sexual transmission of HIV. J Infect Dis 189 1785 1792
8. CoffinJM
1995 HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267 483 489
9. NowakM
1990 HIV mutation rate. Nature 347 522
10. KemalKS
FoleyB
BurgerH
AnastosK
MinkoffH
2003 HIV-1 in genital tract and plasma of women: compartmentalization of viral sequences, coreceptor usage, and glycosylation. Proc Natl Acad Sci U S A 100 12972 12977
11. EronJJ
VernazzaPL
JohnstonDM
Seillier-MoiseiwitschF
AlcornTM
1998 Resistance of HIV-1 to antiretroviral agents in blood and seminal plasma: implications for transmission. Aids 12 F181 189
12. GuptaP
LerouxC
PattersonBK
KingsleyL
RinaldoC
2000 Human immunodeficiency virus type 1 shedding pattern in semen correlates with the compartmentalization of viral Quasi species between blood and semen. J Infect Dis 182 79 87
13. PolesMA
ElliottJ
VingerhoetsJ
MichielsL
ScholliersA
2001 Despite high concordance, distinct mutational and phenotypic drug resistance profiles in human immunodeficiency virus type 1 RNA are observed in gastrointestinal mucosal biopsy specimens and peripheral blood mononuclear cells compared with plasma. J Infect Dis 183 143 148
14. KiesslingAA
FitzgeraldLM
ZhangD
ChhayH
BrettlerD
1998 Human immunodeficiency virus in semen arises from a genetically distinct virus reservoir. AIDS Res Hum Retroviruses 14 Suppl 1 S33 41
15. ByrnRA
ZhangD
EyreR
McGowanK
KiesslingAA
1997 HIV-1 in semen: an isolated virus reservoir. Lancet 350 1141
16. PhilpottS
BurgerH
TsoukasC
FoleyB
AnastosK
2005 Human immunodeficiency virus type 1 genomic RNA sequences in the female genital tract and blood: compartmentalization and intrapatient recombination. J Virol 79 353 363
17. DelwartEL
MullinsJI
GuptaP
LearnGHJr
HolodniyM
1998 Human immunodeficiency virus type 1 populations in blood and semen. J Virol 72 617 623
18. DiemK
NickleDC
MotoshigeA
FoxA
RossS
2008 Male genital tract compartmentalization of human immunodeficiency virus type 1 (HIV). AIDS Res Hum Retroviruses 24 561 571
19. ParanjpeS
CraigoJ
PattersonB
DingM
BarrosoP
2002 Subcompartmentalization of HIV-1 quasispecies between seminal cells and seminal plasma indicates their origin in distinct genital tissues. AIDS Res Hum Retroviruses 18 1271 1280
20. Shehu-XhilagaM
de KretserD
Dejucq-RainsfordN
HedgerM
2005 Standing in the way of eradication: HIV-1 infection and treatment in the male genital tract. Curr HIV Res 3 345 359
21. RouletV
SatieAP
RuffaultA
Le TortorecA
DenisH
2006 Susceptibility of human testis to human immunodeficiency virus-1 infection in situ and in vitro. Am J Pathol 169 2094 2103
22. RouletV
DenisH
StaubC
Le TortorecA
DelaleuB
2006 Human testis in organotypic culture: application for basic or clinical research. Hum Reprod 21 1564 1575
23. Le TortorecA
SatieAP
DenisH
Rioux-LeclercqN
HavardL
2008 Human prostate supports more efficient replication of HIV-1 R5 than X4 strains ex vivo. Retrovirology 5 119
24. Le TortorecA
Le GrandR
DenisH
SatieAP
ManniouiK
2008 Infection of semen-producing organs by SIV during the acute and chronic stages of the disease. PLoS One 3 e1792
25. Le TortorecA
DenisH
SatieAP
PatardJJ
RuffaultA
2008 Antiviral responses of human Leydig cells to mumps virus infection or poly I:C stimulation. Hum Reprod 23 2095 2103
26. Le TortorecA
Dejucq-RainsfordN
2009 HIV infection of the male genital tract - consequences for sexual transmission and reproduction. Int J Androl 33 e98 e108
27. Le TortorecA
Dejucq-RainsfordN
2007 [The male genital tract: A host for HIV]. Gynecol Obstet Fertil 35 1245 1250
28. Dejucq-RainsfordN
JegouB
2004 Viruses in semen and male genital tissues–consequences for the reproductive system and therapeutic perspectives. Curr Pharm Des 10 557 575
29. MillerCJ
VogelP
AlexanderNJ
DandekarS
HendrickxAG
1994 Pathology and localization of simian immunodeficiency virus in the reproductive tract of chronically infected male rhesus macaques. Lab Invest 70 255 262
30. ByrnRA
KiesslingAA
1998 Analysis of human immunodeficiency virus in semen: indications of a genetically distinct virus reservoir. J Reprod Immunol 41 161 176
31. GhosnJ
ChaixML
PeytavinG
ReyE
BressonJL
2004 Penetration of enfuvirtide, tenofovir, efavirenz, and protease inhibitors in the genital tract of HIV-1-infected men. Aids 18 1958 1961
32. KroodsmaKL
KozalMJ
HamedKA
WintersMA
MeriganTC
1994 Detection of drug resistance mutations in the human immunodeficiency virus type 1 (HIV-1) pol gene: differences in semen and blood HIV-1 RNA and proviral DNA. J Infect Dis 170 1292 1295
33. SmithDM
WongJK
ShaoH
HightowerGK
MaiSH
2007 Long-term persistence of transmitted HIV drug resistance in male genital tract secretions: implications for secondary transmission. J Infect Dis 196 356 360
34. PingLH
CohenMS
HoffmanI
VernazzaP
Seillier-MoiseiwitschF
2000 Effects of genital tract inflammation on human immunodeficiency virus type 1 V3 populations in blood and semen. J Virol 74 8946 8952
35. ZhuT
WangN
CarrA
NamDS
Moor-JankowskiR
1996 Genetic characterization of human immunodeficiency virus type 1 in blood and genital secretions: evidence for viral compartmentalization and selection during sexual transmission. J Virol 70 3098 3107
36. PilcherCD
JoakiG
HoffmanIF
MartinsonFE
MapanjeC
2007 Amplified transmission of HIV-1: comparison of HIV-1 concentrations in semen and blood during acute and chronic infection. Aids 21 1723 1730
37. PilcherCD
PriceMA
HoffmanIF
GalvinS
MartinsonFE
2004 Frequent detection of acute primary HIV infection in men in Malawi. Aids 18 517 524
38. TindallB
EvansL
CunninghamP
McQueenP
HurrenL
1992 Identification of HIV-1 in semen following primary HIV-1 infection. Aids 6 949 952
39. RitolaK
PilcherCD
FiscusSA
HoffmanNG
NelsonJA
2004 Multiple V1/V2 env variants are frequently present during primary infection with human immunodeficiency virus type 1. J Virol 78 11208 11218
40. ZhangL
RoweL
HeT
ChungC
YuJ
2002 Compartmentalization of surface envelope glycoprotein of human immunodeficiency virus type 1 during acute and chronic infection. J Virol 76 9465 9473
41. NunnariG
OteroM
DornadulaG
VanellaM
ZhangH
2002 Residual HIV-1 disease in seminal cells of HIV-1-infected men on suppressive HAART: latency without on-going cellular infections. Aids 16 39 45
42. KalichmanSC
Di BertoG
EatonL
2008 Human immunodeficiency virus viral load in blood plasma and semen: review and implications of empirical findings. Sex Transm Dis 35 55 60
43. ZarateS
PondSL
ShapshakP
FrostSD
2007 Comparative study of methods for detecting sequence compartmentalization in human immunodeficiency virus type 1. J Virol 81 6643 6651
44. WhitneyJB
LuedemannC
HraberP
RaoSS
MascolaJR
2009 T-cell vaccination reduces simian immunodeficiency virus levels in semen. J Virol 83 10840 10843
45. KeeleBF
LiH
LearnGH
HraberP
GiorgiEE
2009 Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J Exp Med 206 1117 1134
46. ZhangM
GaschenB
BlayW
FoleyB
HaigwoodN
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
47. Kosakovsky PondSL
FrostSD
2005 Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22 1208 1222
48. Kosakovsky PondSL
PosadaD
GravenorMB
WoelkCH
FrostSD
2006 GARD: a genetic algorithm for recombination detection. Bioinformatics 22 3096 3098
49. PillaiSK
GoodB
PondSK
WongJK
StrainMC
2005 Semen-specific genetic characteristics of human immunodeficiency virus type 1 env. J Virol 79 1734 1742
50. ButlerDM
DelportW
Kosakovsky PondSL
LakdawalaMK
ChengPM
2010 The origins of sexually transmitted HIV among men who have sex with men. Sci Transl Med 2 18re11
51. BhattacharyaT
DanielsM
HeckermanD
FoleyB
FrahmN
2007 Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 315 1583 1586
52. SlatkinM
MaddisonWP
1990 Detecting isolation by distance using phylogenies of genes. Genetics 126 249 260
53. PondSL
FrostSD
MuseSV
2005 HyPhy: hypothesis testing using phylogenies. Bioinformatics 21 676 679
54. BullME
LearnGH
McElhoneS
HittiJ
LockhartD
2009 Monotypic human immunodeficiency virus type 1 genotypes across the uterine cervix and in blood suggest proliferation of cells with provirus. J Virol 83 6020 6028
55. BullM
LearnG
GenowatiI
McKernanJ
HittiJ
2009 Compartmentalization of HIV-1 within the female genital tract is due to monotypic and low-diversity variants not distinct viral populations. PLoS One 4 e7122
56. Kosakovsky PondSL
PosadaD
GravenorMB
WoelkCH
FrostSD
2006 Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23 1891 1901
57. Salazar-GonzalezJF
SalazarMG
KeeleBF
LearnGH
GiorgiEE
2009 Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 206 1273 1289
58. KeeleBF
GiorgiEE
Salazar-GonzalezJF
DeckerJM
PhamKT
2008 Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105 7552 7557
59. PalmerS
KearneyM
MaldarelliF
HalvasEK
BixbyCJ
2005 Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J Clin Microbiol 43 406 413
60. Salazar-GonzalezJF
BailesE
PhamKT
SalazarMG
GuffeyMB
2008 Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82 3952 3970
61. LiuSLRA
ShankarappaR
LearnGH
HsuL
DavidovO
1996 HIV quasispecies and resampling. Science 273 415 416
62. ZhuJ
HladikF
WoodwardA
KlockA
PengT
2009 Persistence of HIV-1 receptor-positive cells after HSV-2 reactivation is a potential mechanism for increased HIV-1 acquisition. Nat Med 15 886 892
63. CelumC
WaldA
LingappaJR
MagaretAS
WangRS
2010 Acyclovir and transmission of HIV-1 from persons infected with HIV-1 and HSV-2. N Engl J Med 362 427 439
64. RiegG
ButlerDM
SmithDM
DaarES
2010 Seminal plasma HIV levels in men with asymptomatic sexually transmitted infections. Int J STD AIDS 21 207 208
65. CohenMS
HoffmanIF
RoyceRA
KazembeP
DyerJR
1997 Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. AIDSCAP Malawi Research Group. Lancet 349 1868 1873
66. HaalandRE
HawkinsPA
Salazar-GonzalezJ
JohnsonA
TichacekA
2009 Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog 5 e1000274
67. DerdeynCA
DeckerJM
Bibollet-RucheF
MokiliJL
MuldoonM
2004 Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303 2019 2022
68. HarrisonRM
1980 Semen parameters in Macaca mulatta: ejaculates from random and selected monkeys. J Med Primatol 9 265 273
69. ClineAN
BessJW
PiatakMJr
LifsonJD
2005 Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J Med Primatol 34 303 312
70. WhitneyJB
LuedemannC
BaoS
MiuraA
RaoSS
2009 Monitoring HIV vaccine trial participants for primary infection: studies in the SIV/macaque model. Aids 23 1453 1460
71. DouekDC
BrenchleyJM
BettsMR
AmbrozakDR
HillBJ
2002 HIV preferentially infects HIV-specific CD4+ T cells. Nature 417 95 98
72. MattapallilJJ
DouekDC
HillB
NishimuraY
MartinM
2005 Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434 1093 1097
73. LearnGHJr
KorberBT
FoleyB
HahnBH
WolinskySM
1996 Maintaining the integrity of human immunodeficiency virus sequence databases. J Virol 70 5720 5730
74. GilbertPB
RossiniAJ
ShankarappaR
2005 Two-sample tests for comparing intra-individual genetic sequence diversity between populations. Biometrics 61 106 117
75. ParadisE
ClaudeJ
StrimmerK
2004 APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20 289 290
76. GascuelO
1997 BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14 685 695
77. GuindonS
GascuelO
2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 696 704
78. KulkarniSS
LapedesA
TangH
GnanakaranS
DanielsMG
2009 Highly complex neutralization determinants on a monophyletic lineage of newly transmitted subtype C HIV-1 Env clones from India. Virology 385 505 520
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 2
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Genetic Mapping Identifies Novel Highly Protective Antigens for an Apicomplexan Parasite
- Type I Interferon Signaling Regulates Ly6C Monocytes and Neutrophils during Acute Viral Pneumonia in Mice
- Infections in Cells: Transcriptomic Characterization of a Novel Host-Symbiont Interaction
- The ESCRT-0 Component HRS is Required for HIV-1 Vpu-Mediated BST-2/Tetherin Down-Regulation