Direct Presentation Is Sufficient for an Efficient Anti-Viral CD8 T Cell Response
The extent to which direct- and cross-presentation (DP and CP) contribute to the priming of CD8+ T cell (TCD8+) responses to viruses is unclear mainly because of the difficulty in separating the two processes. Hence, while CP in the absence of DP has been clearly demonstrated, induction of an anti-viral TCD8+ response that excludes CP has never been purposely shown. Using vaccinia virus (VACV), which has been used as the vaccine to rid the world of smallpox and is proposed as a vector for many other vaccines, we show that DP is the main mechanism for the priming of an anti-viral TCD8+ response. These findings provide important insights to our understanding of how one of the most effective anti-viral vaccines induces immunity and should contribute to the development of novel vaccines.
Vyšlo v časopise:
Direct Presentation Is Sufficient for an Efficient Anti-Viral CD8 T Cell Response. PLoS Pathog 6(2): e32767. doi:10.1371/journal.ppat.1000768
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1000768
Souhrn
The extent to which direct- and cross-presentation (DP and CP) contribute to the priming of CD8+ T cell (TCD8+) responses to viruses is unclear mainly because of the difficulty in separating the two processes. Hence, while CP in the absence of DP has been clearly demonstrated, induction of an anti-viral TCD8+ response that excludes CP has never been purposely shown. Using vaccinia virus (VACV), which has been used as the vaccine to rid the world of smallpox and is proposed as a vector for many other vaccines, we show that DP is the main mechanism for the priming of an anti-viral TCD8+ response. These findings provide important insights to our understanding of how one of the most effective anti-viral vaccines induces immunity and should contribute to the development of novel vaccines.
Zdroje
1. LauLL
JamiesonBD
SomasundaramT
AhmedR
1994 Cytotoxic T-cell memory without antigen. Nature 369 648 652
2. WelshRM
SelinLK
Szomolanyi-TsudaE
2004 Immunological memory to viral infections. Annu Rev Immunol 22 711 743
3. FangM
SigalLJ
2005 Antibodies and CD8+ T Cells Are Complementary and Essential for Natural Resistance to a Highly Lethal Cytopathic Virus. J Immunol 175 6829 6836
4. XuR-H
FangM
Klein-SzantoA
SigalLJ
2007 Memory CD8+ T cells are gatekeepers of the lymph node draining the site of viral infection. Proc Natl Acad Sci U S A 104 10992 10997
5. LenzLL
ButzEA
BevanMJ
2000 Requirements for bone marrow-derived antigen-presenting cells in priming cytotoxic T cell responses to intracellular pathogens. J Exp Med 192 1135 1142
6. SigalLJ
CrottyS
AndinoR
RockKL
1999 Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 398 77 80
7. SigalLJ
RockKL
2000 Bone marrow-derived antigen-presenting cells are required for the generation of cytotoxic T lymphocyte responses to viruses and use transporter associated with antigen presentation (TAP)-dependent and - independent pathways of antigen presentation. J Exp Med 192 1143 1150
8. HeathWR
BelzGT
BehrensGM
SmithCM
ForehanSP
2004 Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev 199 9 26
9. RockKL
1996 A new foreign policy: MHC class I molecules monitor the outside world. Immunology Today 17 131 137
10. MeliefCJ
2003 Mini-review: Regulation of cytotoxic T lymphocyte responses by dendritic cells: peaceful coexistence of cross-priming and direct priming? Eur J Immunol 33 2645 2654
11. WilsonNS
BehrensGM
LundieRJ
SmithCM
WaithmanJ
2006 Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat Immunol 7 165 172
12. ZinkernagelRM
2002 On cross-priming of MHC class I-specific CTL: rule or exception? Eur J Immunol 32 2385 2392
13. AmigorenaS
2003 Y in X priming. Nat Immunol 4 1047 1048
14. LizeeG
BashaG
TiongJ
JulienJP
TianM
2003 Control of dendritic cell cross-presentation by the major histocompatibility complex class I cytoplasmic domain. Nat Immunol 4 1065 1073
15. HeathWR
CarboneFR
2001 Cross-presentation in viral immunity and self-tolerance. Nat Rev Immunol 1 126 134
16. SernaA
RamirezMC
SoukhanovaA
SigalLJ
2003 Cutting Edge: Efficient MHC Class I Cross-Presentation during Early Vaccinia Infection Requires the Transfer of Proteasomal Intermediates between Antigen Donor and Presenting Cells. J Immunol 171 5668 5672
17. NorburyCC
BastaS
DonohueKB
TscharkeDC
PrinciottaMF
2004 CD8+ T cell cross-priming via transfer of proteasome substrates. Science 304 1318 1321
18. RestifoNP
BacikI
IrvineKR
YewdellJW
McCabeBJ
1995 Antigen processing in vivo and the elicitation of primary CTL responses. J Immunol 154 4414 4422
19. WherryEJ
PuorroKA
PorgadorA
EisenlohrLC
1999 The induction of virus-specific CTL as a function of increasing epitope expression: responses rise steadily until excessively high levels of epitope are attained. J Immunol 163 3735 3745
20. PorgadorA
YewdellJW
DengY
BenninkJR
GermainRN
1997 Localization, quantitation, and in situ detection of specific peptide- MHC class I complexes using a monoclonal antibody. Immunity 6 715 726
21. PrinciottaMF
FinziD
QianSB
GibbsJ
SchuchmannS
2003 Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18 343 354
22. GilbertPA
McFaddenG
2006 Poxvirus cancer therapy. Recent Pat Antiinfect Drug Discov 1 309 321
23. GherardiMM
EstebanM
2005 Recombinant poxviruses as mucosal vaccine vectors. J Gen Virol 86 2925 2936
24. NorburyCC
MalideD
GibbsJS
BenninkJR
YewdellJW
2002 Visualizing priming of virus-specific CD8+ T cells by infected dendritic cells in vivo. Nat Immunol 3 265 271
25. HickmanHD
TakedaK
SkonCN
MurrayFR
HensleySE
2008 Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat Immunol 9 155 165
26. MaX
SernaA
XuRH
SigalLJ
2009 The amino acid sequences flanking an antigenic determinant can strongly affect MHC class I cross-presentation without altering direct presentation. J Immunol 182 4601 4607
27. KarttunenJ
SandersonS
ShastriN
1992 Detection of rare antigen-presenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens. Proc Natl Acad Sci U S A 89 6020 6024
28. SandersonS
ShastriN
1994 LacZ inducible, antigen/MHC-specific T cell hybrids. Int Immunol 6 369 376
29. HogquistKA
JamesonSC
HeathWR
HowardJL
BevanMJ
1994 T cell receptor antagonist peptides induce positive selection. Cell 76 17 27
30. ClarkeSR
BarndenM
KurtsC
CarboneFR
MillerJF
2000 Characterization of the ovalbumin-specific TCR transgenic line OT-I: MHC elements for positive and negative selection. Immunol Cell Biol 78 110 117
31. KurtsC
KosakaH
CarboneFR
MillerJF
HeathWR
1997 Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells. J Exp Med 186 239 245
32. Nikolic-ZugicJ
BevanMJ
1990 Role of self-peptides in positively selecting the T-cell repertoire. Nature 344 65 67
33. BadovinacVP
HaringJS
HartyJT
2007 Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) T cell response to infection. Immunity 26 827 841
34. TscharkeDC
KarupiahG
ZhouJ
PalmoreT
IrvineKR
2005 Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J Exp Med 201 95 104
35. QuC
NguyenVA
MeradM
RandolphGJ
2009 MHC class I/peptide transfer between dendritic cells overcomes poor cross-presentation by monocyte-derived APCs that engulf dying cells. J Immunol 182 3650 3659
36. DolanBP
GibbsKDJr
Ostrand-RosenbergS
2006 Dendritic cells cross-dressed with peptide MHC class I complexes prime CD8+ T cells. J Immunol 177 6018 6024
37. SollidLM
VaageJT
2006 Cross-dressing T cells go wild. Nat Med 12 611 612
38. SmythLA
HerreraOB
GolshayanD
LombardiG
LechlerRI
2006 A novel pathway of antigen presentation by dendritic and endothelial cells: Implications for allorecognition and infectious diseases. Transplantation 82 S15 18
39. SmythLA
HarkerN
TurnbullW
El-DoueikH
KlavinskisL
2008 The relative efficiency of acquisition of MHC:peptide complexes and cross-presentation depends on dendritic cell type. J Immunol 181 3212 3220
40. ShenL
SigalLJ
BoesM
RockKL
2004 Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 21 155 165
41. LarssonM
FonteneauJF
SomersanS
SandersC
BickhamK
2001 Efficiency of cross presentation of vaccinia virus-derived antigens by human dendritic cells. Eur J Immunol 31 3432 3442
42. RamirezMC
SigalLJ
2002 Macrophages and Dendritic Cells Use the Cytosolic Pathway to Rapidly Cross-Present Antigen from Live, Vaccinia-Infected Cells. J Immunol 169 6733 6742
43. GasteigerG
KastenmullerW
LjapociR
SutterG
DrexlerI
2007 Cross-priming of cytotoxic T cells dictates antigen requisites for modified vaccinia virus Ankara vector vaccines. J Virol 81 11925 11936
44. BastaS
ChenW
BenninkJR
YewdellJW
2002 Inhibitory effects of cytomegalovirus proteins US2 and US11 point to contributions from direct priming and cross-priming in induction of vaccinia virus-specific CD8(+) T cells. J Immunol 168 5403 5408
45. ShenX
WongSB
BuckCB
ZhangJ
SilicianoRF
2002 Direct priming and cross-priming contribute differentially to the induction of CD8+ CTL following exposure to vaccinia virus via different routes. J Immunol 169 4222 4229
46. AckermanAL
GiodiniA
CresswellP
2006 A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 25 607 617
47. JuntT
MosemanEA
IannaconeM
MassbergS
LangPA
2007 Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450 110 114
48. ShastriN
GonzalezF
1993 Endogenous generation and presentation of the ovalbumin peptide/Kb complex to T cells. J Immunol 150 2724 2736
49. EarlPL
CooperN
WyattLS
MossB
CarrollMW
2001 Preparation of cell cultures and vaccinia virus stocks. Curr Protoc Mol Biol Chapter 16 Unit16 16
50. EarlPL
MossB
WyattLS
CarrollMW
2001 Generation of recombinant vaccinia viruses. Curr Protoc Mol Biol Chapter 16 Unit16 17
51. FangM
SigalLJ
2006 Direct CD28 Costimulation Is Required for CD8+ T Cell-Mediated Resistance to an Acute Viral Disease in a Natural Host. J Immunol 177 8027 8036
52. RodenkoB
ToebesM
HadrupSR
van EschWJ
MolenaarAM
2006 Generation of peptide-MHC class I complexes through UV-mediated ligand exchange. Nat Protoc 1 1120 1132
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 2
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Caspase-1 Activation via Rho GTPases: A Common Theme in Mucosal Infections?
- Kaposi's Sarcoma Associated Herpes Virus (KSHV) Induced COX-2: A Key Factor in Latency, Inflammation, Angiogenesis, Cell Survival and Invasion
- IL-1β Processing in Host Defense: Beyond the Inflammasomes
- Reverse Genetics in Predicts ARF Cycling Is Essential for Drug Resistance and Virulence