Unconventional Repertoire Profile Is Imprinted during Acute Chikungunya Infection for Natural Killer Cells Polarization toward Cytotoxicity
Chikungunya virus (CHIKV) is a worldwide emerging pathogen. In humans it causes a syndrome characterized by high fever, polyarthritis, and in some cases lethal encephalitis. Growing evidence indicates that the innate immune response plays a role in controlling CHIKV infection. We show here that CHIKV induces major but transient modifications in NK-cell phenotype and function soon after the onset of acute infection. We report a transient clonal expansion of NK cells that coexpress CD94/NKG2C and inhibitory receptors for HLA-C1 alleles and are correlated with the viral load. Functional tests reveal cytolytic capacity driven by NK cells in the absence of exogenous signals and severely impaired IFN-γ production. Collectively these data provide insight into the role of this unique subset of NK cells in controlling CHIKV infection by subset-specific expansion in response to acute infection, followed by a contraction phase after viral clearance.
Vyšlo v časopise:
Unconventional Repertoire Profile Is Imprinted during Acute Chikungunya Infection for Natural Killer Cells Polarization toward Cytotoxicity. PLoS Pathog 7(9): e32767. doi:10.1371/journal.ppat.1002268
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002268
Souhrn
Chikungunya virus (CHIKV) is a worldwide emerging pathogen. In humans it causes a syndrome characterized by high fever, polyarthritis, and in some cases lethal encephalitis. Growing evidence indicates that the innate immune response plays a role in controlling CHIKV infection. We show here that CHIKV induces major but transient modifications in NK-cell phenotype and function soon after the onset of acute infection. We report a transient clonal expansion of NK cells that coexpress CD94/NKG2C and inhibitory receptors for HLA-C1 alleles and are correlated with the viral load. Functional tests reveal cytolytic capacity driven by NK cells in the absence of exogenous signals and severely impaired IFN-γ production. Collectively these data provide insight into the role of this unique subset of NK cells in controlling CHIKV infection by subset-specific expansion in response to acute infection, followed by a contraction phase after viral clearance.
Zdroje
1. WeaverSCBarrettAD 2004 Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol 2 789 801
2. SchwartzOAlbertML 2010 Biology and pathogenesis of chikungunya virus. Nature Rev Microbiol 8 491 500
3. PialouxGGaüzèreBAJauréguiberrySStrobelM 2007 Chikungunya, an epidemic arbovirosis. Lancet Infect Dis 7 319 327
4. SourisseauMSchilteCCasartelliNTrouilletCGuivel-Benhassine F etal 2007 Characterization of reemerging chikungunya virus. PLoS Pathog 3 e89
5. de LamballerieXLeroyECharrelRNTtsetsarkinKHiggsS 2008 Chikungunya virus adapts to tiger mosquito via evolutionary convergence: a sign of things to come? J Virol 5 33
6. RezzaGLNicolettiRAngeliniRRomiACFinarelliM 2007 Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370 1840 1846
7. LeroyEMNkogheDOllomoBNze-NkogueCBecquartP 2009 Concurrent chikungunya and dengue virus infections during simultaneous outbreaks, Gabon, 2007. Emerg Infect Dis 15 591 593
8. GérardinPBarauGMichaultABintnerMRandrianaivoH 2008 Multidisciplinary prospective study of mother-to-child chikungunya virus infections on the island of La Réunion. PLoS Med 5 e60
9. SissokoDMoendandzeAMalvyDGiryCEzzedineK 2008 Seroprevalence and risk factors of chikungunya virus infection in Mayotte, Indian Ocean, 2005-2006: a population-based survey. PLoS One 3 e3066
10. LabadieKLarcherTJoubertCManniouiADelacheB 2010 Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages. J Clin Invest 120 894 906
11. NgLFChowASunYJKwekDJLimPL 2009 IL-1beta, IL-6, and RANTES as biomarkers of Chikungunya severity. PLoS One 4 e4261
12. SchilteCCoudercTChretienFSourisseauMGangneuxM 2010 Type I IFN controls chikungunya virus via its action on non hematopoietic cells. J Exp Med 207 429 442
13. NewmanKCRileyEM 2007 Whatever turns you on: accessory-cell-dependent activation of NK cells by pathogens. Nat Rev Immunol 7 279 291
14. WauquierNBecquartPNkgheDPadillaCNdjoyi-MbiguinoA 2011 Strong innate immunity and T CD8 cell responses characterize the acute phase of mild chikungunya virus infection in humans. J Infec Dis 204 115 123
15. BrycesonYTLongEO 2009 Line of attack NK cell specificity and integration of signals. Curr Opin Immunol 20 344 352
16. LanierLL 2008 Evolutionary struggles between NK cells and viruses. Nat Rev Immunol 8 259 268
17. VivierETomaselloEBaratinMWalzerTUgoliniS 2008 Functions of natural killer cells. Nat Immunol 9 503 510
18. YokoyamaWM 2008 Mistaken notions about natural killer cells. Nat Immunol 9 481 485
19. LanierLL 2005 NK cell recognition. Annu Rev Immunol 23 225 274
20. LeeS-HBironCA 2010 Here today – not gone tomorrow: roles for activating receptors in sustaining NK cells during viral infections. Eur J Immunol 40 923 932
21. AaskovJGDalglishDA 1981 Regulation in vitro of human natural killer (NK) cell activity. Med Microbiol Immunol 170 109 116
22. AlsharifiMLobigsMSimonMMKerstenAMüllerK 2006 NK cell-mediated immunopathology during an acute viral infection of the CNS. Eur J Immunol 36 887 896
23. HoarauJJJaffar BandjeeMCKrejbich TrototPDasTLi-Pat-YuenG 2010 Persistent chronic inflammation and infection by Chikungunya arthritogenic alphavirus in spite of a robust host immune response. J Immunol 184 5914 5927
24. AzeredoELDe Oliveira-PintoLMZagneSMCerqueiraDINogueiraRM 2006 NK cells, displaying early activation, cytotoxicity and adhesion molecules, are associated with mild dengue disease. Clin Exp Immunol 143 345 356
25. HershkovitzORosentalBRosenbergLANavarro-SanchezMEJivovS 2009 NKp44 receptor mediates interaction of the envelope glycoproteins from the West Nile and dengue viruses with NK cells. J Immunol 183 2610 2621
26. KingNJKessonAM 2003 Interaction of flaviviruses with cells of the vertebrate host and decoy of the immune response. Immunol Cell Biol 81 207 216
27. López-BotetMBellónT 1999 Natural killer cell activation and inhibition by receptors for MHC class I. Curr Opin Immunol 11 301 307
28. PoliAMichelTThérésineMAndrèsEHentgesF 2009 CD56bright natural killer (NK) cells: an important NK cell subset. Immunology 126 458 465
29. CooperMAColonnaMYokoyamaWM 2009 Hidden talents of natural killers: NK cells in innate and adaptive immunity. EMBO Rep 10 1103 1110
30. MavilioDBenjaminJDaucherMLombardoGKottililS 2003 Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc Natl Acad Sci U S A 100 15011 15016
31. GumáMAnguloAVilchesCGómez-LozanoNMalatsN 2004 Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104 3664 3671
32. MavilioDLombardoGBenjaminJKimDFollmanD 2005 Characterization of CD56-/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc Natl Acad Sci USA 102 2886 2891
33. AzzoniLPapasavvasEChehimiJKostmanJRMounzerKOndercinJ 2002 Sustained impairment of IFN-gamma secretion in suppressed HIV-infected patients despite mature NK cell recovery: evidence for a defective reconstitution of innate immunity. J Immunol 168 5764 5770
34. DunnCPeppaDKhannaPNebbiaGJonesM 2009 Temporal analysis of early immune responses in patients with acute hepatitis B virus infection. Gastroenterology 137 1289 1300
35. RomagnaniCJuelkeKFalcoMMorandiBD'AgostinoA 2007 CD56brightCD16- killer Ig-like receptor- NK cells display longer telomeres and acquire features of CD56dim NK cells upon activation. J Immunol 178 4947 4955
36. BéziatVDescoursBParizotCDebréPVieillardV 2010 NK cell terminal differentiation: correlated stepwise decrease of NKG2A and acquisition of KIRs. PLoS One 5 e11966
37. BjörkströmNKRiesePHeutsFAnderssonSFauriatC 2010 Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 116 3853 3864
38. Le Garff-TavernierMBéziatVDecocqJSiguretVGandjbakhchF 2010 Human NK cells display major phenotypic and functional changes over the life span. Aging Cell 9 527 535
39. BjörkströmNKLindgrenTStoltzMFauriatCBraunM 2011 Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med 208 13 21
40. MelaCMBurtonCTImamiNNelsonMSteelA 2005 Switch from inhibitory to activating NKG2 receptor expression in HIV-1 infection: lack of reversion with highly active antiretroviral therapy. AIDS 19 1761 1769
41. Fausther-BovendoHWauquierNCherfils-ViciniJCremerIDebréP 2008 NKG2C is a major triggering receptor involved in the V[delta]1 T cell-mediated cytotoxicity against HIV-infected CD4 T cells. AIDS 22 217 226
42. OlivieroBVarchettaSPaudiceEMicheloneGZaramellaM 2009 Natural killer cell functional dichotomy in chronic hepatitis B and chronic hepatitis C virus infections. Gastroenterology 137 1151 1160
43. DokunAOKimSSmithHRKangHSChuDT 2001 Specific and nonspecific NK cell activation during virus infection. Nat Immunol 2 951 956
44. RobbinsSHTessmerMSMikayamaTBrossayL 2004 Expansion and contraction of the NK cell compartment in response to murine cytomegalovirus infection. J Immunol 173 259 266
45. SunJCBeilkeJNLanierLL 2009 Adaptive immune features of natural killer cells. Nature 457 557 561
46. SunJCBeilkeJNLanierLL 2010 Immune Memory redefined : characterizing the longevity of natural killer cells. Immunol Rev 236 83 94
47. GumáMCabreraCErkiziaIBofillMClotetB 2006 Human cytomegalovirus infection is associated with increased proportions of NK cells that express the CD94/NKG2C receptor in aviremic HIV-1-positive patients. J Infect Dis 194 38 41
48. CannonMJSchmidDSHydeTB 2010 Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 20 202 213
49. BéziatVHervierBAchourABoutolleauDMarfain-KokaA 2011 Human NKG2A overrides NKG2C effector functions to prevent autoreactivity of NK cells. Blood 117 4394 4396
50. KuijpersTWBaarsPADantinCvan den BurgMvan LierRA 2008 Human NK cells can control CMV infection in the absence of T cells. Blood 112 914 915
51. PastorinoBBessaudMGrandadamMMurriSTolouHJ 2005 Development of a TaqMan RT-PCR assay without RNA extraction step for the detection and quantification of African Chikungunya viruses. J Virol Methods 124 65 71
52. SturnAQuackenbushJTrajanoskiZ 2002 Genesis: Cluster analysis of microarray data. Bioinformatics 18 207 208
53. PagèsFBergerACamusMSanchez-CaboFCostesA 2005 Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353 2654 2666
54. VieillardVFausther-BovendoHSamriA Debré P and French Asymptomatiques à Long Terme (ALT) ANRS-CO15 Study Group 2010 Specific phenotypic and functional features of natural killer cells from HIV-infected long-term nonprogressors and HIV controllers. J Acquir Immune Defic Syndr 53 564 573
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 9
- 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
- Hostile Takeover by : Reorganization of Parasite and Host Cell Membranes during Liver Stage Egress
- HTLV-1 Propels Thymic Human T Cell Development in “Human Immune System” Rag2 gamma c Mice
- Exploiting and Subverting Tor Signaling in the Pathogenesis of Fungi, Parasites, and Viruses
- A Viral Ubiquitin Ligase Has Substrate Preferential SUMO Targeted Ubiquitin Ligase Activity that Counteracts Intrinsic Antiviral Defence