HIV and Mature Dendritic Cells: Trojan Exosomes Riding the Trojan Horse?
Exosomes are secreted cellular vesicles that can induce specific CD4+ T cell responses in vivo when they interact with competent antigen-presenting cells like mature dendritic cells (mDCs). The Trojan exosome hypothesis proposes that retroviruses can take advantage of the cell-encoded intercellular vesicle traffic and exosome exchange pathway, moving between cells in the absence of fusion events in search of adequate target cells. Here, we discuss recent data supporting this hypothesis, which further explains how DCs can capture and internalize retroviruses like HIV-1 in the absence of fusion events, leading to the productive infection of interacting CD4+ T cells and contributing to viral spread through a mechanism known as trans-infection. We suggest that HIV-1 can exploit an exosome antigen-dissemination pathway intrinsic to mDCs, allowing viral internalization and final trans-infection of CD4+ T cells. In contrast to previous reports that focus on the ability of immature DCs to capture HIV in the mucosa, this review emphasizes the outstanding role that mature DCs could have promoting trans-infection in the lymph node, underscoring a new potential viral dissemination pathway.
Vyšlo v časopise:
HIV and Mature Dendritic Cells: Trojan Exosomes Riding the Trojan Horse?. PLoS Pathog 6(3): e32767. doi:10.1371/journal.ppat.1000740
Kategorie:
Review
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000740
Souhrn
Exosomes are secreted cellular vesicles that can induce specific CD4+ T cell responses in vivo when they interact with competent antigen-presenting cells like mature dendritic cells (mDCs). The Trojan exosome hypothesis proposes that retroviruses can take advantage of the cell-encoded intercellular vesicle traffic and exosome exchange pathway, moving between cells in the absence of fusion events in search of adequate target cells. Here, we discuss recent data supporting this hypothesis, which further explains how DCs can capture and internalize retroviruses like HIV-1 in the absence of fusion events, leading to the productive infection of interacting CD4+ T cells and contributing to viral spread through a mechanism known as trans-infection. We suggest that HIV-1 can exploit an exosome antigen-dissemination pathway intrinsic to mDCs, allowing viral internalization and final trans-infection of CD4+ T cells. In contrast to previous reports that focus on the ability of immature DCs to capture HIV in the mucosa, this review emphasizes the outstanding role that mature DCs could have promoting trans-infection in the lymph node, underscoring a new potential viral dissemination pathway.
Zdroje
1. SteinmanRM
1991 The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9 271 296
2. SteinmanRM
BanchereauJ
2007 Taking dendritic cells into medicine. Nature 449 419 426
3. CameronPU
FreudenthalPS
BarkerJM
GezelterS
InabaK
1992 Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 257 383 387
4. McIlroyD
AutranB
CheynierR
Wain-HobsonS
ClauvelJP
1995 Infection frequency of dendritic cells and CD4+ T lymphocytes in spleens of human immunodeficiency virus-positive patients. J Virol 69 4737 4745
5. GeijtenbeekTB
KwonDS
TorensmaR
van VlietSJ
van DuijnhovenGC
2000 DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100 587 597
6. BlauveltA
AsadaH
SavilleMW
Klaus-KovtunV
AltmanDJ
1997 Productive infection of dendritic cells by HIV-1 and their ability to capture virus are mediated through separate pathways. J Clin Invest 100 2043 2053
7. van KooykY
GeijtenbeekTB
2003 DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol 3 697 709
8. CurtisBM
ScharnowskeS
WatsonAJ
1992 Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc Natl Acad Sci U S A 89 8356 8360
9. KwonDS
GregorioG
BittonN
HendricksonWA
LittmanDR
2002 DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16 135 144
10. FigdorCG
van KooykY
AdemaGJ
2002 C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol 2 77 84
11. EngeringA
GeijtenbeekTB
van VlietSJ
WijersM
van LiemptE
2002 The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol 168 2118 2126
12. MorisA
PajotA
BlanchetF
Guivel-BenhassineF
SalcedoM
2006 Dendritic cells and HIV-specific CD4+ T cells: HIV antigen presentation, T-cell activation, and viral transfer. Blood 108 1643 1651
13. BuseyneF
Le GallS
BoccaccioC
AbastadoJP
LifsonJD
2001 MHC-I-restricted presentation of HIV-1 virion antigens without viral replication. Nat Med 7 344 349
14. MorisA
NobileC
BuseyneF
PorrotF
AbastadoJP
2004 DC-SIGN promotes exogenous MHC-I-restricted HIV-1 antigen presentation. Blood 103 2648 2654
15. TurvilleSG
SantosJJ
FrankI
CameronPU
WilkinsonJ
2004 Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 103 2170 2179
16. NobileC
PetitC
MorisA
SkrabalK
AbastadoJP
2005 Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J Virol 79 5386 5399
17. Izquierdo-UserosN
BlancoJ
ErkiziaI
Fernandez-FiguerasMT
BorrasFE
2007 Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission. J Virol 81 7559 7570
18. BurleighL
LozachPY
SchifferC
StaropoliI
PezoV
2006 Infection of dendritic cells (DCs), not DC-SIGN-mediated internalization of human immunodeficiency virus, is required for long-term transfer of virus to T cells. J Virol 80 2949 2957
19. SandersRW
de JongEC
BaldwinCE
SchuitemakerJH
KapsenbergML
2002 Differential transmission of human immunodeficiency virus type 1 by distinct subsets of effector dendritic cells. J Virol 76 7812 7821
20. McDonaldD
WuL
BohksSM
KewalRamaniVN
UnutmazD
2003 Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300 1295 1297
21. WangJH
JanasAM
OlsonWJ
WuL
2007 Functionally distinct transmission of human immunodeficiency virus type 1 mediated by immature and mature dendritic cells. J Virol 81 8933 8943
22. WuL
KewalramaniVN
2006 Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 6 859 868
23. Granelli-PipernoA
DelgadoE
FinkelV
PaxtonW
SteinmanRM
1998 Immature dendritic cells selectively replicate macrophagetropic (M-tropic) human immunodeficiency virus type 1, while mature cells efficiently transmit both M- and T-tropic virus to T cells. J Virol 72 2733 2737
24. CavroisM
NeidlemanJ
KreisbergJF
FenardD
CallebautC
2006 Human immunodeficiency virus fusion to dendritic cells declines as cells mature. J Virol 80 1992 1999
25. FrankI
PiatakMJr
StoesselH
RomaniN
BonnyayD
2002 Infectious and whole inactivated simian immunodeficiency viruses interact similarly with primate dendritic cells (DCs): differential intracellular fate of virions in mature and immature DCs. J Virol 76 2936 2951
26. MellmanI
SteinmanRM
2001 Dendritic cells: specialized and regulated antigen processing machines. Cell 106 255 258
27. VilladangosJA
SchnorrerP
2007 Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat Rev Immunol 7 543 555
28. CavroisM
NeidlemanJ
KreisbergJF
GreeneWC
2007 In vitro derived dendritic cells trans-infect CD4 T cells primarily with surface-bound HIV-1 virions. PLoS Pathog 3 e4 doi:10.1371/journal.ppat.0030004
29. YuHJ
ReuterMA
McDonaldD
2008 HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells. PLoS Pathog 4 e1000134 doi:10.1371/journal.ppat.1000134
30. BanchereauJ
SteinmanRM
1998 Dendritic cells and the control of immunity. Nature 392 245 252
31. MoserM
MurphyKM
2000 Dendritic cell regulation of TH1-TH2 development. Nat Immunol 1 199 205
32. DouekDC
BrenchleyJM
BettsMR
AmbrozakDR
HillBJ
2002 HIV preferentially infects HIV-specific CD4+ T cells. Nature 417 95 98
33. MillerMJ
SafrinaO
ParkerI
CahalanMD
2004 Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J Exp Med 200 847 856
34. PerelsonAS
NeumannAU
MarkowitzM
LeonardJM
HoDD
1996 HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271 1582 1586
35. GummuluruS
KewalRamaniVN
EmermanM
2002 Dendritic cell-mediated viral transfer to T cells is required for human immunodeficiency virus type 1 persistence in the face of rapid cell turnover. J Virol 76 10692 10701
36. HogueIB
BajariaSH
FallertBA
QinS
ReinhartTA
2008 The dual role of dendritic cells in the immune response to human immunodeficiency virus type 1 infection. J Gen Virol 89 2228 2239
37. BrenchleyJM
PriceDA
SchackerTW
AsherTE
SilvestriG
2006 Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12 1365 1371
38. BarronMA
BlyveisN
PalmerBE
MaWhinneyS
WilsonCC
2003 Influence of plasma viremia on defects in number and immunophenotype of blood dendritic cell subsets in human immunodeficiency virus 1-infected individuals. J Infect Dis 187 26 37
39. FahrbachKM
BarrySM
AyehunieS
LamoreS
KlausnerM
2007 Activated CD34-derived Langerhans cells mediate transinfection with human immunodeficiency virus. J Virol 81 6858 6868
40. ShattockRJ
MooreJP
2003 Inhibiting sexual transmission of HIV-1 infection. Nat Rev Microbiol 1 25 34
41. HIV Vaccine Trials Network 2008 Step study results. Available: http://www.hvtn.org/science/step_buch.html. Accessed 26 February 2010
42. PerreauM
PantaleoG
KremerEJ
2008 Activation of a dendritic cell-T cell axis by Ad5 immune complexes creates an improved environment for replication of HIV in T cells. J Exp Med 205 2717 25
43. SavinaA
JancicC
HuguesS
GuermonprezP
VargasP
2006 NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126 205 218
44. TurvilleSG
ArthosJ
DonaldKM
LynchG
NaifH
2001 HIV gp120 receptors on human dendritic cells. Blood 98 2482 2488
45. TurvilleSG
CameronPU
HandleyA
LinG
PohlmannS
2002 Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 3 975 983
46. WuL
BashirovaAA
MartinTD
VillamideL
MehlhopE
2002 Rhesus macaque dendritic cells efficiently transmit primate lentiviruses independently of DC-SIGN. Proc Natl Acad Sci U S A 99 1568 1573
47. GummuluruS
RogelM
StamatatosL
EmermanM
2003 Binding of human immunodeficiency virus type 1 to immature dendritic cells can occur independently of DC-SIGN and mannose binding C-type lectin receptors via a cholesterol-dependent pathway. J Virol 77 12865 12874
48. TrumpfhellerC
ParkCG
FinkeJ
SteinmanRM
Granelli-PipernoA
2003 Cell type-dependent retention and transmission of HIV-1 by DC-SIGN. Int Immunol 15 289 298
49. HuQ
FrankI
WilliamsV
SantosJJ
WattsP
2004 Blockade of attachment and fusion receptors inhibits HIV-1 infection of human cervical tissue. J Exp Med 199 1065 1075
50. Granelli-PipernoA
PritskerA
PackM
ShimeliovichI
ArrighiJF
2005 Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. J Immunol 175 4265 4273
51. BoggianoC
ManelN
LittmanDR
2007 Dendritic cell-mediated trans-enhancement of human immunodeficiency virus type 1 infectivity is independent of DC-SIGN. J Virol 81 2519 2523
52. Magerus-ChatinetA
YuH
GarciaS
DuclouxE
TerrisB
2007 Galactosyl ceramide expressed on dendritic cells can mediate HIV-1 transfer from monocyte derived dendritic cells to autologous T cells. Virology 362 67 74
53. LambertAA
GilbertC
RichardM
BeaulieuAD
TremblayMJ
2008 The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to trans- and cis-infection pathways. Blood 112 1299 307
54. MoronVG
RuedaP
SedlikC
LeclercC
2003 In vivo, dendritic cells can cross-present virus-like particles using an endosome-to-cytosol pathway. J Immunol 171 2242 2250
55. BuonaguroL
TorneselloML
TagliamonteM
GalloRC
WangLX
2006 Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J Virol 80 9134 9143
56. InabaK
TurleyS
YamaideF
IyodaT
MahnkeK
1998 Efficient presentation of phagocytosed cellular fragments on the major histocompatibility complex class II products of dendritic cells. J Exp Med 188 2163 2173
57. TheryC
RegnaultA
GarinJ
WolfersJ
ZitvogelL
1999 Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol 147 599 610
58. TheryC
ZitvogelL
AmigorenaS
2002 Exosomes: composition, biogenesis and function. Nat Rev Immunol 2 569 579
59. ZitvogelL
RegnaultA
LozierA
WolfersJ
FlamentC
1998 Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 4 594 600
60. WolfersJ
LozierA
RaposoG
RegnaultA
TheryC
2001 Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7 297 303
61. TheryC
DubanL
SeguraE
VeronP
LantzO
2002 Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 3 1156 1162
62. GouldSJ
BoothAM
HildrethJE
2003 The Trojan exosome hypothesis. Proc Natl Acad Sci U S A 100 10592 10597
63. Izquierdo-UserosN
Naranjo-GomezM
ArcherJ
HatchSC
ErkiziaI
2009 Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosome-dissemination pathway. Blood 113 2732 2741
64. GarciaE
PionM
Pelchen-MatthewsA
CollinsonL
ArrighiJF
2005 HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 6 488 501
65. GarciaE
NikolicDS
PiguetV
2008 HIV-1 replication in dendritic cells occurs through a tetraspanin-containing compartment enriched in AP-3. Traffic 9 200 214
66. BoothAM
FangY
FallonJK
YangJM
HildrethJE
2006 Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol 172 923 935
67. FangY
WuN
GanX
YanW
MorrellJC
2007 Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol 5 e158 doi:10.1371/journal.pbio.0050158
68. NguyenDH
HildrethJE
2000 Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J Virol 74 3264 3272
69. WubboltsR
LeckieRS
VeenhuizenPT
SchwarzmannG
MobiusW
2003 Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 278 10963 10972
70. KrishnamoorthyL
BessJWJr
PrestonAB
NagashimaK
MahalLK
2009 HIV-1 and microvesicles from T cells share a common glycome, arguing for a common origin. Nat Chem Biol 5 244 250
71. ChazalN
GerlierD
2003 Virus entry, assembly, budding, and membrane rafts. Microbiol Mol Biol Rev 67 226 237
72. WileyRD
GummuluruS
2006 Immature dendritic cell-derived exosomes can mediate HIV-1 trans infection. Proc Natl Acad Sci U S A 103 738 743
73. BruggerB
GlassB
HaberkantP
LeibrechtI
WielandFT
2006 The HIV lipidome: a raft with an unusual composition. Proc Natl Acad Sci U S A 103 2641 2646
74. SakamotoH
OkamotoK
AokiM
KatoH
KatsumeA
2005 Host sphingolipid biosynthesis as a target for hepatitis C virus therapy. Nat Chem Biol 1 333 337
75. HatchSC
ArcherJ
GummuluruS
2009 Glycosphingolipid composition of human immunodeficiency virus type 1 (HIV-1) particles is a crucial determinant for dendritic cell-mediated HIV-1 trans-infection. J Virol 83 3496 3506
76. AndrieuJM
LuW
2007 A dendritic cell-based vaccine for treating HIV infection: background and preliminary results. J Intern Med 261 123 131
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 3
- 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
- Kaposi's Sarcoma-Associated Herpesvirus ORF57 Protein Binds and Protects a Nuclear Noncoding RNA from Cellular RNA Decay Pathways
- Endocytosis of the Anthrax Toxin Is Mediated by Clathrin, Actin and Unconventional Adaptors
- Perforin and IL-2 Upregulation Define Qualitative Differences among Highly Functional Virus-Specific Human CD8 T Cells
- Inhibition of Macrophage Migration Inhibitory Factor Ameliorates Ocular -Induced Keratitis