A Viral Immunoevasin Controls Innate Immunity by Targeting the Prototypical Natural Killer Cell Receptor Family - PubMed (original) (raw)
. 2017 Mar 23;169(1):58-71.e14.
doi: 10.1016/j.cell.2017.03.002.
Richard Berry 2, Mir Munir A Rahim 3, Johanna J Reichel 4, Branka Popović 4, Miho Tanaka 1, Zhihui Fu 5, Gautham R Balaji 2, Timothy N H Lau 1, Megan M Tu 3, Christina L Kirkham 1, Ahmad Bakur Mahmoud 6, Aruz Mesci 1, Astrid Krmpotić 4, David S J Allan 1, Andrew P Makrigiannis 7, Stipan Jonjić 8, Jamie Rossjohn 9, James R Carlyle 10
Affiliations
- PMID: 28340350
- DOI: 10.1016/j.cell.2017.03.002
Free article
A Viral Immunoevasin Controls Innate Immunity by Targeting the Prototypical Natural Killer Cell Receptor Family
Oscar A Aguilar et al. Cell. 2017.
Free article
Abstract
Natural killer (NK) cells play a key role in innate immunity by detecting alterations in self and non-self ligands via paired NK cell receptors (NKRs). Despite identification of numerous NKR-ligand interactions, physiological ligands for the prototypical NK1.1 orphan receptor remain elusive. Here, we identify a viral ligand for the inhibitory and activating NKR-P1 (NK1.1) receptors. This murine cytomegalovirus (MCMV)-encoded protein, m12, restrains NK cell effector function by directly engaging the inhibitory NKR-P1B receptor. However, m12 also interacts with the activating NKR-P1A/C receptors to counterbalance m12 decoy function. Structural analyses reveal that m12 sequesters a large NKR-P1 surface area via a "polar claw" mechanism. Polymorphisms in, and ablation of, the viral m12 protein and host NKR-P1B/C alleles impact NK cell responses in vivo. Thus, we identify the long-sought foreign ligand for this key immunoregulatory NKR family and reveal how it controls the evolutionary balance of immune recognition during host-pathogen interplay.
Keywords: NK1.1 ligand; Natural killer cell; host-pathogen interactions; murine cytomegalovirus; viral immune evasion.
Copyright © 2017 Elsevier Inc. All rights reserved.
Similar articles
- Mouse Cytomegalovirus m153 Protein Stabilizes Expression of the Inhibitory NKR-P1B Ligand Clr-b.
Aguilar OA, Sampaio IS, Rahim MMA, Samaniego JD, Tilahun ME, Krishnamoorthy M, Popović B, Babić M, Krmpotić A, Treanor B, Margulies DH, Allan DSJ, Makrigiannis AP, Jonjić S, Carlyle JR. Aguilar OA, et al. J Virol. 2019 Dec 12;94(1):e01220-19. doi: 10.1128/JVI.01220-19. Print 2019 Dec 12. J Virol. 2019. PMID: 31597762 Free PMC article. - Expansion and Protection by a Virus-Specific NK Cell Subset Lacking Expression of the Inhibitory NKR-P1B Receptor during Murine Cytomegalovirus Infection.
Rahim MM, Wight A, Mahmoud AB, Aguilar OA, Lee SH, Vidal SM, Carlyle JR, Makrigiannis AP. Rahim MM, et al. J Immunol. 2016 Sep 15;197(6):2325-37. doi: 10.4049/jimmunol.1600776. Epub 2016 Aug 10. J Immunol. 2016. PMID: 27511735 - Interferon-Dependent Induction of Clr-b during Mouse Cytomegalovirus Infection Protects Bystander Cells from Natural Killer Cells via NKR-P1B-Mediated Inhibition.
Kirkham CL, Aguilar OA, Yu T, Tanaka M, Mesci A, Chu KL, Fine JH, Mossman KL, Bremner R, Allan DSJ, Carlyle JR. Kirkham CL, et al. J Innate Immun. 2017;9(4):343-358. doi: 10.1159/000454926. Epub 2017 Mar 14. J Innate Immun. 2017. PMID: 28288457 Free PMC article. - Viral Evasion of Natural Killer Cell Activation.
Ma Y, Li X, Kuang E. Ma Y, et al. Viruses. 2016 Apr 12;8(4):95. doi: 10.3390/v8040095. Viruses. 2016. PMID: 27077876 Free PMC article. Review. - Physiologic functions of activating natural killer (NK) complex-encoded receptors on NK cells.
Ryan JC, Naper C, Hayashi S, Daws MR. Ryan JC, et al. Immunol Rev. 2001 Jun;181:126-37. doi: 10.1034/j.1600-065x.2001.1810110.x. Immunol Rev. 2001. PMID: 11513134 Review.
Cited by
- Alveolar macrophage metabolic programming via a C-type lectin receptor protects against lipo-toxicity and cell death.
Scur M, Mahmoud AB, Dey S, Abdalbarri F, Stylianides I, Medina-Luna D, Gamage GS, Woblistin A, Wilson ANM, Zein HS, Stueck A, Wight A, Aguilar OA, Di Cara F, Parsons BD, Rahim MMA, Carlyle JR, Makrigiannis AP. Scur M, et al. Nat Commun. 2022 Nov 25;13(1):7272. doi: 10.1038/s41467-022-34935-w. Nat Commun. 2022. PMID: 36433992 Free PMC article. - NK Cell Memory to Cytomegalovirus: Implications for Vaccine Development.
Forrest C, Gomes A, Reeves M, Male V. Forrest C, et al. Vaccines (Basel). 2020 Jul 20;8(3):394. doi: 10.3390/vaccines8030394. Vaccines (Basel). 2020. PMID: 32698362 Free PMC article. Review. - Mouse cytomegalovirus-experienced ILC1s acquire a memory response dependent on the viral glycoprotein m12.
Weizman OE, Song E, Adams NM, Hildreth AD, Riggan L, Krishna C, Aguilar OA, Leslie CS, Carlyle JR, Sun JC, O'Sullivan TE. Weizman OE, et al. Nat Immunol. 2019 Aug;20(8):1004-1011. doi: 10.1038/s41590-019-0430-1. Epub 2019 Jul 1. Nat Immunol. 2019. PMID: 31263280 Free PMC article. - Mutually assured destruction: the cold war between viruses and natural killer cells.
Ali A, Gyurova IE, Waggoner SN. Ali A, et al. Curr Opin Virol. 2019 Feb;34:130-139. doi: 10.1016/j.coviro.2019.02.005. Epub 2019 Mar 13. Curr Opin Virol. 2019. PMID: 30877885 Free PMC article. Review. - The complex of MCMV proteins and MHC class I evades NK cell control and drives the evolution of virus-specific activating Ly49 receptors.
Železnjak J, Lisnić VJ, Popović B, Lisnić B, Babić M, Halenius A, L'Hernault A, Roviš TL, Hengel H, Erhard F, Redwood AJ, Vidal SM, Dölken L, Krmpotić A, Jonjić S. Železnjak J, et al. J Exp Med. 2019 Aug 5;216(8):1809-1827. doi: 10.1084/jem.20182213. Epub 2019 May 29. J Exp Med. 2019. PMID: 31142589 Free PMC article.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases
Miscellaneous