Understanding human γδ T cell biology toward a better management of cytomegalovirus infection.
Journal
Immunological reviews
ISSN: 1600-065X
Titre abrégé: Immunol Rev
Pays: England
ID NLM: 7702118
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
08
08
2020
revised:
04
09
2020
accepted:
04
09
2020
pubmed:
23
10
2020
medline:
26
10
2021
entrez:
22
10
2020
Statut:
ppublish
Résumé
Cytomegalovirus (CMV) infection is responsible for significant morbidity and mortality in immunocompromised patients, namely solid organ and hematopoietic cell transplant recipients, and can induce congenital infection in neonates. There is currently an unmet need for new management and treatment strategies. Establishment of an anti-CMV immune response is critical in order to control CMV infection. The two main human T cells involved in HCMV-specific response are αβ and non-Vγ9Vδ2 T cells that belong to γδ T cell compartment. CMV-induced non-Vγ9Vδ2 T cells harbor a specific clonal expansion and a phenotypic signature, and display effector functions against CMV. So far, only two main molecular mechanisms underlying CMV sensing have been identified. Non-Vγ9Vδ2 T cells can be activated either by stress-induced surface expression of the γδT cell receptor (TCR) ligand annexin A2, or by a multimolecular stress signature composed of the γδTCR ligand endothelial protein C receptor and co-stimulatory signals such as the ICAM-1-LFA-1 axis. All this basic knowledge can be harnessed to improve the clinical management of CMV infection in at-risk patients. In particular, non-Vγ9Vδ2 T cell monitoring could help better stratify the risk of infection and move forward a personalized medicine. Moreover, recent advances in cell therapy protocols open the way for a non-Vγ9Vδ2 T cell therapy in immunocompromised patients.
Substances chimiques
Receptors, Antigen, T-Cell, gamma-delta
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
264-288Informations de copyright
© 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Zuhair M, Smit GSA, Wallis G, et al. Estimation of the worldwide seroprevalence of cytomegalovirus: A systematic review and meta-analysis. Rev Med Virol 2019;29:e2034.
Ljungman P, Boeckh M, Hirsch HH, et al. Definitions of cytomegalovirus infection and disease in transplant patients for use in clinical trials. Clin Infect Dis. 2017;64:87-91.
Humar A, Lebranchu Y, Vincenti F, et al. The efficacy and safety of 200 days valganciclovir cytomegalovirus prophylaxis in high-risk kidney transplant recipients. Am J Transplant. 2010;10:1228-1237.
Witzke O, Hauser IA, Bartels M, et al. Valganciclovir prophylaxis versus preemptive therapy in cytomegalovirus-positive renal allograft recipients: 1-year results of a randomized clinical trial. Transplantation. 2012;93:61-68.
Kotton CN, Kumar D, Caliendo AM, et al. The third international consensus guidelines on the management of cytomegalovirus in solid-organ transplantation. Transplantation. 2018;102:900-931.
Niederwieser D, Baldomero H, Atsuta Y, et al. One and half million hematopoietic stem cell transplants (HSCT). Dissemination, trends and potential to improve activity by telemedicine from the worldwide network for blood and marrow transplantation (WBMT). Blood. 2019;423-432.
Ljungman P, Hakki M, Boeckh M. Cytomegalovirus in hematopoietic stem cell transplant recipients. Hematol Oncol Clin North Am. 2011;25:151-169.
Ljungman P, de la Camara R, Robin C, et al. Guidelines for the management of cytomegalovirus infection in patients with haematological malignancies and after stem cell transplantation from the 2017 European Conference on Infections in Leukaemia (ECIL 7). Lancet Infect Dis. 2019;19:e260-e272.
Teira P, Battiwalla M, Ramanathan M, et al. Early cytomegalovirus reactivation remains associated with increased transplant-related mortality in the current era: a CIBMTR analysis. Blood. 2016;127:2427-2438.
Port AD, Orlin A, Kiss S, et al. Cytomegalovirus retinitis: a review. J Ocul Pharmacol Ther. 2017;33:224-234.
Leruez-Ville M, Foulon I, Pass R, et al. Cytomegalovirus infection during pregnancy: state of the science. Am J Obstet Gynecol 2020;223(3):330-349.
Andronaco DW. Congenital cytomegalovirus and hearing loss. J Obstet Gynecol Neonatal Nurs. 2020;49(3):293-304.
Dollard SC, Grosse SD, Ross DS. New estimates of the prevalence of neurological and sensory sequelae and mortality associated with congenital cytomegalovirus infection. Rev Med Virol. 2007;17(5):355-363.
Berry R, Watson GM, Jonjic S, et al. Modulation of innate and adaptive immunity by cytomegaloviruses. Nat Rev Immunol. 2020;20:113-127.
Compton T, Nowlin DM, Cooper NR. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology. 1993;193:834-841.
Farrell HE, Stevenson PG. Cytomegalovirus host entry and spread. J Gen Virol. 2019;100(4):545-553.
Crough T, Khanna R. Immunobiology of human cytomegalovirus: from bench to bedside. Clin Microbiol Rev. 2009;22(1):76-98.
Gerna G, Sarasini A, Genini E, et al. Prediction of endothelial cell tropism of human cytomegalovirus strains. J Clin Virol. 2006;35:470-473.
Sinclair J, Sissons P. Latent and persistent infections of monocytes and macrophages. Intervirology. 1996;39:293-301.
Reeves MB, MacAry PA, Lehner PJ, et al. Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers. Proc Natl Acad Sci USA. 2005;102:4140-4145.
Hahn G, Jores R, Mocarski ES. Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells. Proc Natl Acad Sci USA. 1998;95:3937-3942.
Mendelson M, Monard S, Sissons P, et al. Detection of endogenous human cytomegalovirus in CD34+ bone marrow progenitors. J Gen Virol. 1996;77(Pt 12):3099-3102.
Elder E, Sinclair J. HCMV latency: what regulates the regulators? Med Microbiol Immunol. 2019;208(3-4):431-438.
Zhang Z, Qiu L, Yan S, et al. A clinically relevant murine model unmasks a "two-hit" mechanism for reactivation and dissemination of cytomegalovirus after kidney transplant. Am J Transplant. 2019;19:2421-2433.
Soderberg-Naucler C, Fish KN, Nelson JA. Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors. Cell. 1997;91:119-126.
Marshall GS, Rabalais GP, Stout GG, et al. Antibodies to recombinant-derived glycoprotein B after natural human cytomegalovirus infection correlate with neutralizing activity. J Infect Dis. 1992;165:381-384.
Britt WJ, Vugler L, Butfiloski EJ, et al. Cell surface expression of human cytomegalovirus (HCMV) gp55-116 (gB): use of HCMV-recombinant vaccinia virus-infected cells in analysis of the human neutralizing antibody response. J Virol. 1990;64:1079-1085.
Rasmussen L, Matkin C, Spaete R, et al. Antibody response to human cytomegalovirus glycoproteins gB and gH after natural infection in humans. J Infect Dis. 1991;164:835-842.
Jonjić S, Pavić I, Polić B, et al. Antibodies are not essential for the resolution of primary cytomegalovirus infection but limit dissemination of recurrent virus. J Exp Med. 1994;179:1713-1717.
Polić B, Hengel H, Krmpotić A, et al. Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J Exp Med. 1998;188(6):1047-1054.
Bonaros NE, Kocher A, Dunkler D, et al. Comparison of combined prophylaxis of cytomegalovirus hyperimmune globulin plus ganciclovir versus cytomegalovirus hyperimmune globulin alone in high-risk heart transplant recipients. Transplantation. 2004;77:890-897.
Khairallah C, Netzer S, Villacreces A, et al. γδ T cells confer protection against murine cytomegalovirus (MCMV). PLoS Pathog. 2015;11(3):e1004702.
Kumar D, Mian M, Singer L, et al. An interventional study using cell-mediated immunity to personalize therapy for cytomegalovirus infection after transplantation. Am J Transplant. 2017;17:2468-2473.
Kaminski H, Garrigue I, Couzi L, et al. Surveillance of gammadelta T Cells predicts cytomegalovirus infection resolution in kidney transplants. J Am Soc Nephrol 2016;27:637-645.
Adams NM, Grassmann S, Sun JC. Clonal expansion of innate and adaptive lymphocytes. Nat Rev Immunol. 2020. https://doi.org/10.1038/s41577-020-0307-4
Pitard V, Roumanes D, Lafarge X, et al. Long-term expansion of effector/memory Vdelta2-gammadelta T cells is a specific blood signature of CMV infection. Blood. 2008;112:1317-1324.
Bukowski JF, Warner JF, Dennert G, et al. Adoptive transfer studies demonstrating the antiviral effect of natural killer cells in vivo. J Exp Med. 1985;161:40-52.
Mace EM, Orange JS. Emerging insights into human health and NK cell biology from the study of NK cell deficiencies. Immunol Rev. 2019;287(1):202-225.
Venema H, Van Den Berg AP, Van Zanten C, et al. Natural killer cell responses in renal transplant patients with cytomegalovirus infection. J Med Virol. 1994;42:188-192.
Tomasec P, Braud VM, Rickards C, et al. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science. 2000;287:1031.
Stern M, Elsässer H, Hönger G, et al. The number of activating KIR genes inversely correlates with the rate of CMV infection/reactivation in kidney transplant recipients. Am J Transplant. 2008;8:1312-1317.
Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457:557-561.
Gumá Mónica, Angulo A, Vilches C, et al. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood. 2004;104:3664-3671.
Gumá Mónica, Budt M, Sáez A, et al. Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood. 2006;107:3624-3631.
Hammer Q, Rückert T, Borst EM, et al. Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells. Nat Immunol. 2018;19(5):453-463.
Quinnan GV, Manischewitz JE. The role of natural killer cells and antibody-dependent cell-mediated cytotoxicity during murine cytomegalovirus infection. J Exp Med. 1979;150:1549-1554.
Lang P, Griesinger A, Hamprecht K, et al. Antiviral activity against CMV-infected fibroblasts in pediatric patients transplanted with CD34+-selected allografts from alternative donors. Hum Immunol. 2004;65(5):423-431.
Sylwester AW, Mitchell BL, Edgar JB, et al. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med. 2005;202(5):673-685.
Gamadia LE, Remmerswaal EB, Weel JF, et al. Primary immune responses to human CMV: a critical role for IFN-gamma-producing CD4+ T cells in protection against CMV disease. Blood. 2003;101:2686-2692.
Gamadia LE, van Leeuwen EMM, Remmerswaal EBM, et al. The size and phenotype of virus-specific T cell populations is determined by repetitive antigenic stimulation and environmental cytokines. J Immunol. 2004;172:6107-6114.
Appay V, Dunbar PR, Callan M, et al. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat Med. 2002;8(4):379-385.
Klenerman P, Oxenius A. T cell responses to cytomegalovirus. Nat Rev Immunol. 2016;16:367-377.
Gamadia LE, Rentenaar RJ, Baars PA, et al. Differentiation of cytomegalovirus-specific CD8(+) T cells in healthy and immunosuppressed virus carriers. Blood. 2001;98:754-761.
Kuijpers TW, Vossen MT, Gent MR, et al. Frequencies of circulating cytolytic, CD45RA+CD27-, CD8+ T lymphocytes depend on infection with CMV. J Immunol. 1950;2003(170):4342-4348.
Hamann D, Baars PA, Rep MHG, et al. Phenotypic and functional separation of memory and effector human CD8+ T cells. J Exp Med. 1997;186:1407-1418.
Sallusto F, Lenig D, Förster R, et al. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401:708-712.
van Stijn A, Rowshani AT, Yong SL, et al. Human cytomegalovirus infection induces a rapid and sustained change in the expression of NK cell receptors on CD8+ T cells. J Immunol. 1950;2008(180):4550-4560.
Snyder CM, Cho KS, Bonnett EL, et al. Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity. 2008;29:650-659.
Babel N, Brestrich G, Gondek LP, et al. Clonotype analysis of cytomegalovirus-specific cytotoxic T lymphocytes. J Am Soc Nephrol. 2009;20:344-352.
Miconnet I, Marrau A, Farina A, et al. Large TCR diversity of virus-specific CD8 T cells provides the mechanistic basis for massive TCR renewal after antigen exposure. J Immunol. 1950;2011(186):7039-7049.
Wang GC, Dash P, McCullers JA, et al. T cell receptor αβ diversity inversely correlates with pathogen-specific antibody levels in human cytomegalovirus infection. Sci Transl Med 2012;4:128ra142.
Bunde T, Kirchner A, Hoffmeister B, et al. Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J Exp Med 2005;201(7):1031-1036.
Jarque M, Crespo E, Melilli E, et al. Cellular immunity to predict the risk of cytomegalovirus infection in kidney transplantation: a prospective, interventional, multicenter clinical trial. Clin Infect Dis. 2020. https://doi.org/10.1093/cid/ciz1209
Cobbold M, Khan N, Pourgheysari B, et al. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J Exp Med. 2005;202:379-386.
Ştefan G, Stancu S, Căpuşă C, et al. Catheter-related infections in chronic hemodialysis: a clinical and economic perspective. Int Urol Nephrol. 2013;45:817-823.
Rentenaar RJ, Gamadia LE, van derHoek N, et al. Development of virus-specific CD4(+) T cells during primary cytomegalovirus infection. J Clin Invest. 2000;105:541-548.
van Leeuwen EM, Remmerswaal EB, Vossen MT, et al. Emergence of a CD4+CD28- granzyme B+, cytomegalovirus-specific T cell subset after recovery of primary cytomegalovirus infection. J Immunol. 1950;2004(173):1834-1841.
Casazza JP, Betts MR, Price DA, et al. Acquisition of direct antiviral effector functions by CMV-specific CD4+ T lymphocytes with cellular maturation. J Exp Med. 2006;203(13):2865-2877.
Davignon JL, Castanié P, Yorke JA, et al. Anti-human cytomegalovirus activity of cytokines produced by CD4+ T-cell clones specifically activated by IE1 peptides in vitro. J Virol. 1996;70(4):2162-2169.
Vermijlen D, Brouwer M, Donner C, et al. Human cytomegalovirus elicits fetal gammadelta T cell responses in utero. J Exp Med 2010;207:807-821.
Kaminski H, Ménard C, El Hayani B, et al. Characterization of a unique γδ T cell subset as a specific marker of CMV infection severity. J Infect Dis 2020. https://doi.org/10.1093/infdis/jiaa400
Davey MS, Willcox CR, Hunter S, et al. The human Vdelta2(+) T-cell compartment comprises distinct innate-like Vgamma9(+) and adaptive Vgamma9(-) subsets. Nat Commun 2018;9:1760.
Howard J, Loizon S, Tyler CJ, et al. The antigen-presenting potential of Vγ9Vδ2 T cells during plasmodium falciparum blood-stage infection. J Infect Dis. 2017;215(10):1569-1579.
Scalise F, Gerli R, Castellucci G, et al. Lymphocytes bearing the gamma delta T-cell receptor in acute toxoplasmosis. Immunology. 1992;76:668-670.
Lu J, Aggarwal R, Kanji S, et al. Human ovarian tumor cells escape γδ T cell recognition partly by down regulating surface expression of MICA and limiting cell cycle related molecules. PLoS One. 2011;6:e23348.
Mariani S, Muraro M, Pantaleoni F, et al. Effector gammadelta T cells and tumor cells as immune targets of zoledronic acid in multiple myeloma. Leukemia. 2005;19:664-670.
Dechanet J, Merville P, Berge F, et al. Major expansion of gammadelta T lymphocytes following cytomegalovirus infection in kidney allograft recipients. J Infect Dis 1999;179:1-8.
Dechanet J, Merville P, Lim A, et al. Implication of gammadelta T cells in the human immune response to cytomegalovirus. J Clin Investig. 1999;103:1437-1449.
Davey MS, Willcox CR, Joyce SP, et al. Clonal selection in the human Vdelta1 T cell repertoire indicates gammadelta TCR-dependent adaptive immune surveillance. Nat Commun 2017;8:14760.
Roux A, Mourin G, Larsen M, et al. Differential impact of age and cytomegalovirus infection on the γδ T cell compartment. J Immunol. 2013;191(3):1300-1306.
Ehl S, Schwarz K, Enders A, et al. A variant of SCID with specific immune responses and predominance of gamma delta T cells. J Clin Investig 2005;115:3140-3148.
de Villartay JP, Lim A, Al-Mousa H, et al. A novel immunodeficiency associated with hypomorphic RAG1 mutations and CMV infection. J Clin Investig. 2005;115:3291-3299.
Knight A, Madrigal AJ, Grace S, et al. The role of Vdelta2-negative gammadelta T cells during cytomegalovirus reactivation in recipients of allogeneic stem cell transplantation. Blood. 2010;116:2164-2172.
Puig-Pey I, Bohne F, Benítez C, et al. Characterization of γδ T cell subsets in organ transplantation. Transpl Int. 2010;23:1045-1055.
Scheper W, van Dorp S, Kersting S, et al. γδT cells elicited by CMV reactivation after allo-SCT cross-recognize CMV and leukemia. Leukemia. 2013;27:1328-1338.
van der Heiden M, Björkander S, Rahman Qazi K, et al. Characterization of the γδ T-cell compartment during infancy reveals clear differences between the early neonatal period and 2 years of age. Immunol Cell Biol. 2020;98(1):79-87.
Rovito R, Korndewal MJ, van Zelm MC, et al. T and B cell markers in dried blood spots of neonates with congenital cytomegalovirus infection: B cell numbers at birth are associated with long-term outcomes. J Immunol. 2017;198(1):102-109.
Tieppo P, Papadopoulou M, Gatti D, et al. The human fetal thymus generates invariant effector γδ T cells. J Exp Med. 2020;217(3):jem.20190580.
Gaballa A, Arruda LCM, Rådestad E, et al. CD8(+) γδ T cells are more frequent in CMV seropositive bone marrow grafts and display phenotype of an adaptive immune response. Stem Cells Int 2019;2019:6348060.
Ravens S, Schultze-Florey C, Raha S, et al. Human γδ T cells are quickly reconstituted after stem-cell transplantation and show adaptive clonal expansion in response to viral infection. Nat Immunol 2017;18:393-401.
Prinz I, Thamm K, Port M, et al. Donor Vδ1+ γδ T cells expand after allogeneic hematopoietic stem cell transplantation and show reactivity against CMV-infected cells but not against progressing B-CLL. Exp Hematol Oncol. 2013;2:14.
Kim JM, Kwon CHD, Joh JW, et al. Comparative peripheral blood T cells analysis between adult deceased donor liver transplantation (DDLT) and living donor liver transplantation (LDLT). Annals of Transplantation. 2017;22:475-483.
Shi X-L, de Mare-Bredemeijer ELD, Tapirdamaz Ö, et al. CMV primary infection is associated with donor-specific T cell hyporesponsiveness and fewer late acute rejections after liver transplantation. Am J Transplant. 2015;15:2431-2442.
Gilroy RK, Coccia PF, Talmadge JE, et al. Donor immune reconstitution after liver-small bowel transplantation for multiple intestinal atresia with immunodeficiency. Blood. 2004;103:1171-1174.
Couzi L, Lafarge X, Pitard V, et al. Gamma-delta T cell expansion is closely associated with cytomegalovirus infection in all solid organ transplant recipients. Transpl Int. 2011;24:e40-e42.
Hunter S, Willcox CR, Davey MS, et al. Human liver infiltrating γδ T cells are composed of clonally expanded circulating and tissue-resident populations. J Hepatol. 2018;69(3):654-665.
Khairallah C, Dechanet-Merville J, Capone M. gammadelta T cell-mediated immunity to cytomegalovirus infection. Front Immunol 2017;8:105.
Pistillo M, Bigley AB, Spielmann G, et al. The effects of age and viral serology on γδ T-cell numbers and exercise responsiveness in humans. Cell Immunol. 2013;284(1-2):91-97.
Fujishima N, Hirokawa M, Fujishima M, et al. Skewed T cell receptor repertoire of Vdelta1(+) gammadelta T lymphocytes after human allogeneic haematopoietic stem cell transplantation and the potential role for Epstein-Barr virus-infected B cells in clonal restriction. Clin Exp Immunol 2007;149:70-79.
Orsini DLM, Res PCM, Laar JM, et al. A subset of V delta 1+ T cells proliferates in response to Epstein-Barr virus-transformed B cell lines in vitro. Scand J Immunol. 1993;38:335-340.
Orsini DL, van Gils M, Kooy YM, et al. Functional and molecular characterization of B cell-responsive V delta 1+ gamma delta T cells. Eur J Immunol. 1994;24:3199-3204.
De Paoli P, Gennari D, Martelli P, et al. Gamma delta T cell receptor-bearing lymphocytes during Epstein-Barr virus infection. J Infect Dis 1990;161:1013-1016.
Djaoud Z, Guethlein LA, Horowitz A, et al. Two alternate strategies for innate immunity to Epstein-Barr virus: One using NK cells and the other NK cells and γδ T cells. J Exp Med 2017;214:1827-1841.
Lafarge X, Pitard V, Ravet S, et al. Expression of MHC class I receptors confers functional intraclonal heterogeneity to a reactive expansion of gammadelta T cells. Eur J Immunol. 2005;35:1896-1905.
Couzi L, Pitard V, Netzer S, et al. Common features of gammadelta T cells and CD8(+) alphabeta T cells responding to human cytomegalovirus infection in kidney transplant recipients. J Infect Dis 2009;200:1415-1424.
Appay V, van Lier RAW, Sallusto F, et al. Phenotype and function of human T lymphocyte subsets: Consensus and issues. Cytometry A. 2008;73A:975-983.
Davey MS, Willcox CR, Baker AT, et al. Recasting human Vdelta1 lymphocytes in an adaptive role. Trends Immunol 2018;39:446-459.
Roux A, Mourin G, Larsen M, et al. Differential impact of age and cytomegalovirus infection on the gammadelta T cell compartment. J Immunol. 2013;191:1300-1306.
Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: A common denominator approach to cancer therapy. Cancer Cell. 2015;27(4):450-461.
Huard B, Gaulard P, Faure F, et al. Cellular expression and tissue distribution of the human LAG-3-encoded protein, an MHC class II ligand. Immunogenetics. 1994;39:213-217.
Sánchez-Fueyo A, Tian J, Picarella D, et al. Tim-3 inhibits T helper type 1-mediated auto- and alloimmune responses and promotes immunological tolerance. Nat Immunol. 2003;4(11):1093-1101.
De Libero G. Control of gammadelta T cells by NK receptors. Microbes Infect. 1999;1:263-267.
Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331:44-49.
Lee S, Affandi JS, Irish AB, et al. Cytomegalovirus infection alters phenotypes of different γδ T-cell subsets in renal transplant recipients with long-term stable graft function. J Med Virol. 2017;89:1442-1452.
Couzi L, Helou S, Bachelet T, et al. High incidence of anticytomegalovirus drug resistance among D+R- kidney transplant recipients receiving preemptive therapy. Am J Transplant. 2012;12:202-209.
Pizzolato G, Kaminski H, Tosolini M, et al. Single-cell RNA sequencing unveils the shared and the distinct cytotoxic hallmarks of human TCRVδ1 and TCRVδ2 γδ T lymphocytes. Proc Natl Acad Sci USA. 2019;116:11906-11915.
Kallemeijn MJ, Boots AMH, van der Klift MY, et al. Ageing and latent CMV infection impact on maturation, differentiation and exhaustion profiles of T-cell receptor gammadelta T-cells. Sci Rep. 2017;7:5509.
Wistuba-Hamprecht K, Haehnel K, Janssen N, et al. pist. Immunity & ageing: I & A. 2015;12:25.
Wistuba-Hamprecht K, Frasca D, Blomberg B, et al. Age-associated alterations in γδ T-cells are present predominantly in individuals infected with Cytomegalovirus. Immun Ageing. 2013;10:26.
Alejenef A, Pachnio A, Halawi M, et al. Cytomegalovirus drives Vδ2neg γδ T cell inflation in many healthy virus carriers with increasing age. Clin Exp Immunol. 2014;176:418-428.
Wistuba-Hamprecht K, Haehnel K, Janssen N, et al. Peripheral blood T-cell signatures from high-resolution immune phenotyping of γδ and αβ T-cells in younger and older subjects in the Berlin Aging Study II. Immun Ageing. 2015;12:25.
Andreu-Ballester JC, García-Ballesteros C, Benet-Campos C, et al. Values for αβ and γδ T-lymphocytes and CD4+, CD8+, and CD56+ subsets in healthy adult subjects: assessment by age and gender. Cytometry B Clin Cytom. 2012;82:238-244.
Chidrawar S, Khan N, Wei W, et al. Cytomegalovirus-seropositivity has a profound influence on the magnitude of major lymphoid subsets within healthy individuals. Clin Exp Immunol. 2009;155:423-432.
Couzi L, Pitard V, Sicard X, et al. Antibody-dependent anti-cytomegalovirus activity of human γδ T cells expressing CD16 (FcγRIIIa). Blood. 2012;119:1418-1427.
Guerville F, Daburon S, Marlin R, et al. TCR-dependent sensitization of human γδ T cells to non-myeloid IL-18 in cytomegalovirus and tumor stress surveillance. Oncoimmunology. 2015;4:e1003011.
Halary F, Pitard V, Dlubek D, et al. Shared reactivity of V{delta}2(neg) gamma}{delta T cells against cytomegalovirus-infected cells and tumor intestinal epithelial cells. J Exp Med. 2005;201:1567-1578.
Willcox CR, Pitard V, Netzer S, et al. Cytomegalovirus and tumor stress surveillance by binding of a human γδ T cell antigen receptor to endothelial protein C receptor. Nat Immunol. 2012;13:872-879.
Jackson SE, Sedikides GX, Mason GM, et al. Human cytomegalovirus (HCMV)-Specific CD4(+) T cells are polyfunctional and can respond to HCMV-infected dendritic cells in vitro. J Virol. 2017;91:e02128-16.
Jackson SE, Mason GM, Okecha G, et al. Diverse specificities, phenotypes, and antiviral activities of cytomegalovirus-specific CD8+ T cells. J Virol. 2014;88:10894-10908.
Chen KC, Stanton RJ, Banat JJ, et al. Leukocyte immunoglobulin-like receptor 1-expressing human natural killer cell subsets differentially recognize isolates of human cytomegalovirus through the viral major histocompatibility complex class I homolog UL18. J Virol. 2016;90:3123-3137.
Marlin R, Pappalardo A, Kaminski H, et al. Sensing of cell stress by human gammadelta TCR-dependent recognition of annexin A2. Proc Natl Acad Sci USA. 2017;114:3163-3168.
Benveniste PM, Roy S, Nakatsugawa M, et al. Generation and molecular recognition of melanoma-associated antigen-specific human γδ T cells. Sci Immunol. 2018;3(30):eaav4036.
Halenius A, Gerke C, Hengel H. Classical and non-classical MHC I molecule manipulation by human cytomegalovirus: so many targets-but how many arrows in the quiver? Cell Mol Immunol. 2015;12:139-153.
Karunakaran MM, Willcox CR, Salim M, et al. Butyrophilin-2A1 Directly Binds Germline-Encoded Regions of the Vγ9Vδ2 TCR and Is Essential for Phosphoantigen Sensing. Immunity. 2020;52(487-498):e486.
Rigau M, Ostrouska S, Fulford TS, et al. Butyrophilin 2A1 is essential for phosphoantigen reactivity by γδ T cells. Science. 2020;367(6478):eaay5516.
Uldrich AP, Le Nours J, Pellicci DG, et al. CD1d-lipid antigen recognition by the γδ TCR. Nat Immunol. 2013;14:1137-1145.
Luoma AM, Castro CD, Mayassi T, et al. Crystal structure of Vδ1 T cell receptor in complex with CD1d-sulfatide shows MHC-like recognition of a self-lipid by human γδ T cells. Immunity. 2013;39:1032-1042.
Spada FM, Grant EP, Peters PJ, et al. Self-recognition of CD1 by gamma/delta T cells: implications for innate immunity. J Exp Med. 2000;191:937-948.
Roy S, Ly D, Castro CD, et al. Molecular analysis of lipid-reactive Vδ1 γδ T cells identified by CD1c tetramers. J Immunol. 1950;2016(196):1933-1942.
Le Nours J, Gherardin NA, Ramarathinam SH, et al. A class of γδ T cell receptors recognize the underside of the antigen-presenting molecule MR1. Science. 2019;366:1522-1527.
Vermijlen D, Gatti D, Kouzeli A, et al. γδ T cell responses: How many ligands will it take till we know? Semin Cell Dev Biol. 2018;84:75-86.
Bruder J, Siewert K, Obermeier B, et al. Target specificity of an autoreactive pathogenic human γδ-T cell receptor in myositis. J Biol Chem. 2012;287:20986-20995.
Zeng X, Wei YL, Huang J, et al. γδ T cells recognize a microbial encoded B cell antigen to initiate a rapid antigen-specific interleukin-17 response. Immunity. 2012;37:524-534.
McSharry BP, Samer C, McWilliam HEG, et al. Virus-mediated suppression of the antigen presentation molecule MR1. Cell Rep. 2020;30:2948-2962.
Willcox CR, Vantourout P, Salim M, et al. Butyrophilin-like 3 directly binds a human Vγ4(+) T cell receptor using a modality distinct from clonally-restricted antigen. Immunity. 2019;51:813-825.e814.
Costa-Garcia M, Vera A, Moraru M, et al. Antibody-mediated response of NKG2Cbright NK cells against human cytomegalovirus. J Immunol. 1950;2015(194):2715-2724.
Wu Z, Sinzger C, Reichel JJ, et al. Natural killer cells can inhibit the transmission of human cytomegalovirus in cell culture by using mechanisms from innate and adaptive immune responses. J Virol. 2015;89:2906-2917.
Walling BL, Kim M. LFA-1 in T Cell Migration and Differentiation. Front Immunol. 2018;9:952.
Chan G, Bivins-Smith ER, Smith MS, et al. Transcriptome analysis reveals human cytomegalovirus reprograms monocyte differentiation toward an M1 macrophage. J Immunol. 1950;2008(181):698-711.
Ito M, Watanabe M, Ihara T, et al. Increased expression of adhesion molecules (CD54, CD29 and CD44) on fibroblasts infected with cytomegalovirus. Microbiol Immunol. 1995;39:129-133.
Shahgasempour S, Woodroffe SB, Garnett HM. Alterations in the expression of ELAM-1, ICAM-1 and VCAM-1 after in vitro infection of endothelial cells with a clinical isolate of human cytomegalovirus. Microbiol Immunol. 1997;41:121-129.
Warren AP, Owens CN, Borysiewicz LK, et al. Down-regulation of integrin alpha 1/beta 1 expression and association with cell rounding in human cytomegalovirus-infected fibroblasts. J Gen Virol. 1994;75(Pt 12):3319-3325.
Watanabe M, Ito M, Kamiya H, et al. Adherence of peripheral blood leukocytes to cytomegalovirus-infected fibroblasts. Microbiol Immunol. 1996;40:519-523.
Waldman WJ, Knight DA, Huang EH. An in vitro model of T cell activation by autologous cytomegalovirus (CMV)-infected human adult endothelial cells: contribution of CMV-enhanced endothelial ICAM-1. J Immunol. 1950;1998(160):3143-3151.
Leong CC, Chapman TL, Bjorkman PJ, et al. Modulation of natural killer cell cytotoxicity in human cytomegalovirus infection: the role of endogenous class I major histocompatibility complex and a viral class I homolog. J Exp Med. 1998;187:1681-1687.
Srour EF, Leemhuis T, Jenski L, et al. Cytolytic activity of human natural killer cell subpopulations isolated by four-color immunofluorescence flow cytometric cell sorting. Cytometry. 1990;11:442-446.
Hayday A, Theodoridis E, Ramsburg E, et al. Intraepithelial lymphocytes: exploring the Third Way in immunology. Nat Immunol. 2001;2:997-1003.
Bucy RP, Chen CL, Cooper MD. Tissue localization and CD8 accessory molecule expression of T gamma delta cells in humans. J Immunol. 1950;1989(142):3045-3049.
Deusch K, Lüling F, Reich K, et al. A major fraction of human intraepithelial lymphocytes simultaneously expresses the gamma/delta T cell receptor, the CD8 accessory molecule and preferentially uses the V delta 1 gene segment. Eur J Immunol. 1991;21:1053-1059.
Kierkels GJJ, Scheper W, Meringa AD, et al. Identification of a tumor-specific allo-HLA-restricted γδTCR. Blood Adv. 2019;3:2870-2882.
Almeida AR, Correia DV, Fernandes-Platzgummer A, et al. Delta One T Cells for Immunotherapy of Chronic Lymphocytic Leukemia: Clinical-Grade Expansion/Differentiation and Preclinical Proof of Concept. Clin Cancer Res. 2016;22:5795-5804.
Simões AE, Di Lorenzo B, Silva-Santos B. Molecular Determinants of Target Cell Recognition by Human γδ T Cells. Front Immunol. 2018;9:929.
Ribeiro ST, Ribot JC, Silva-Santos B. Five Layers of Receptor Signaling in γδ T-Cell Differentiation and Activation. Front Immunol. 2015;6:15.
Fausther-Bovendo H, Wauquier N, Cherfils-Vicini J, et al. NKG2C is a major triggering receptor involved in the V[delta]1 T cell-mediated cytotoxicity against HIV-infected CD4 T cells. AIDS. 2008;22:217-226.
Hudspeth K, Fogli M, Correia DV, et al. Engagement of NKp30 on Vδ1 T cells induces the production of CCL3, CCL4, and CCL5 and suppresses HIV-1 replication. Blood. 2012;119:4013-4016.
Vantourout P, Hayday A. Six-of-the-best: unique contributions of γδ T cells to immunology. Nat Rev Immunol. 2013;13:88-100.
Rölle A, Mousavi-Jazi M, Eriksson M, et al. Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: up-regulation of UL16-binding protein (ULBP)1 and ULBP2 is counteracted by the viral UL16 protein. J Immunol. 2003;171(2):902-908.
Dunn C, Chalupny NJ, Sutherland CL, et al. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med. 2003;197:1427-1439.
Chalupny NJ, Rein-Weston A, Dosch S, et al. Down-regulation of the NKG2D ligand MICA by the human cytomegalovirus glycoprotein UL142. Biochem Biophys Res Comm. 2006;346:175-181.
Fielding CA, Aicheler R, Stanton RJ, et al. Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLoS Pathog. 2014;10:e1004058.
Nachmani D, Lankry D, Wolf DG, et al. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol. 2010;11:806-813.
Goodier MR, Jonjić S, Riley EM, et al. CMV and natural killer cells: shaping the response to vaccination. Eur J Immunol. 2018;48:50-65.
Romo N, Magri G, Muntasell A, et al. Natural killer cell-mediated response to human cytomegalovirus-infected macrophages is modulated by their functional polarization. J Leukoc Biol. 2011;90:717-726.
Bayer C, Varani S, Wang L, et al. Human cytomegalovirus infection of M1 and M2 macrophages triggers inflammation and autologous T-cell proliferation. J Virol. 2013;87:67-79.
Renneson J, Dutta B, Goriely S, et al. IL-12 and type I IFN response of neonatal myeloid DC to human CMV infection. Eur J Immunol. 2009;39:2789-2799.
Lafarge X, Merville P, Cazin MC, et al. Cytomegalovirus infection in transplant recipients resolves when circulating gammadelta T lymphocytes expand, suggesting a protective antiviral role. J Infect Dis. 2001;184:533-541.
Nicholson E, Peggs KS. Cytomegalovirus-specific T-cell therapies: current status and future prospects. Immunotherapy. 2015;7:135-146.
Gaballa A, Stikvoort A, Önfelt B, et al. T-cell frequencies of CD8(+) γδ and CD27(+) γδ cells in the stem cell graft predict the outcome after allogeneic hematopoietic cell transplantation. Bone Marrow Transplant. 2019;54:1562-1574.
Houghtelin A, Bollard CM. Virus-Specific T Cells for the Immunocompromised Patient. Front Immunol. 2017;8:1272.
Brestrich G, Zwinger S, Fischer A, et al. Adoptive T-cell therapy of a lung transplanted patient with severe CMV disease and resistance to antiviral therapy. Am J Transplant. 2009;9:1679-1684.
Holmes-Liew C-L, Holmes M, Beagley L, et al. Adoptive T-cell immunotherapy for ganciclovir-resistant CMV disease after lung transplantation. Clin Transl Immunology. 2015;4:e35.
Pierucci P, Malouf M, Glanville AR, et al. Novel autologous T-cell therapy for drug-resistant cytomegalovirus disease after lung transplantation. J Heart Lung Transplant. 2016;35:685-687.
Macesic N, Langsford D, Nicholls K, et al. Adoptive T cell immunotherapy for treatment of ganciclovir-resistant cytomegalovirus disease in a renal transplant recipient. Am J Transplant. 2015;15:827-832.
Smith C, Corvino D, Beagley L, et al. T cell repertoire remodeling following post-transplant T cell therapy coincides with clinical response. J Clin Investig. 2019;129:5020-5032.
Smith C, Beagley L, Rehan S, et al. Autologous adoptive T-cell therapy for recurrent or drug-resistant cytomegalovirus complications in solid organ transplant recipients: a single-arm open-label phase I clinical trial. Clin Infect Dis. 2019;68:632-640.
Feuchtinger T, Opherk K, Bethge WA, et al. Adoptive transfer of pp65-specific T cells for the treatment of chemorefractory cytomegalovirus disease or reactivation after haploidentical and matched unrelated stem cell transplantation. Blood. 2010;116:4360-4367.
Peggs KS, Thomson K, Samuel E, et al. Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stem cell transplantation. Clin Infect Dis. 2011;52:49-57.
Scheinberg P, Melenhorst JJ, Brenchley JM, et al. The transfer of adaptive immunity to CMV during hematopoietic stem cell transplantation is dependent on the specificity and phenotype of CMV-specific T cells in the donor. Blood. 2009;114:5071-5080.
Stevens CE, Carrier C, Carpenter C, et al. HLA mismatch direction in cord blood transplantation: impact on outcome and implications for cord blood unit selection. Blood. 2011;118:3969-3978.
Hanley PJ, Cruz CR, Savoldo B, et al. Functionally active virus-specific T cells that target CMV, adenovirus, and EBV can be expanded from naive T-cell populations in cord blood and will target a range of viral epitopes. Blood. 2009;114:1958-1967.
Hanley PJ, Melenhorst JJ, Nikiforow S, et al. CMV-specific T cells generated from naïve T cells recognize atypical epitopes and may be protective in vivo. Sci Transl Med. 2015;7:285ra263.
Jedema I, van de Meent M, Pots J, et al. Successful generation of primary virus-specific and anti-tumor T-cell responses from the naive donor T-cell repertoire is determined by the balance between antigen-specific precursor T cells and regulatory T cells. Haematologica. 2011;96:1204-1212.
Gatault P, Al-Hajj S, Noble J, et al. CMV-infected kidney grafts drive the expansion of blood-borne CMV-specific T cells restricted by shared class I HLA molecules via presentation on donor cells. Am J Transplant. 2018;18:1904-1913.
Gatault P, Halimi JM, Forconi C, et al. CMV infection in the donor and increased kidney graft loss: impact of full HLA-I mismatch and posttransplantation CD8(+) cell reduction. Am J Transplant. 2013;13:2119-2129.
Shabir S, Kaul B, Pachnio A, et al. Impaired direct priming of CD8 T cells by donor-derived cytomegalovirus following kidney transplantation. J Am Soc Nephrol. 2013;24:1698-1708.
Schmitt A, Tonn T, Busch DH, et al. Adoptive transfer and selective reconstitution of streptamer-selected cytomegalovirus-specific CD8+ T cells leads to virus clearance in patients after allogeneic peripheral blood stem cell transplantation. Transfusion. 2011;51:591-599.
Peggs KS, Verfuerth S, Pizzey A, et al. Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet. 2003;362:1375-1377.
Suessmuth Y, Mukherjee R, Watkins B, et al. CMV reactivation drives posttransplant T-cell reconstitution and results in defects in the underlying TCRβ repertoire. Blood. 2015;125:3835-3850.
Schilbach K, Frommer K, Meier S, et al. Immune response of human propagated gammadelta-T-cells to neuroblastoma recommend the Vdelta1+ subset for gammadelta-T-cell-based immunotherapy. J Immunother. 1997;2008(31):896-905.
Correia DV, Fogli M, Hudspeth K, et al. Differentiation of human peripheral blood Vδ1+ T cells expressing the natural cytotoxicity receptor NKp30 for recognition of lymphoid leukemia cells. Blood. 2011;118:992-1001.
Siegers GM, Dhamko H, Wang X-H, et al. Human Vδ1 γδ T cells expanded from peripheral blood exhibit specific cytotoxicity against B-cell chronic lymphocytic leukemia-derived cells. Cytotherapy. 2011;13:753-764.
Knight A, Mackinnon S, Lowdell MW. Human Vdelta1 gamma-delta T cells exert potent specific cytotoxicity against primary multiple myeloma cells. Cytotherapy. 2012;14:1110-1118.
Wu D, Wu P, Wu X, et al. Ex vivo expanded human circulating Vδ1 γδT cells exhibit favorable therapeutic potential for colon cancer. Oncoimmunology. 2015;4:e992749.
Lopez RD, Xu S, Guo B, et al. CD2-mediated IL-12-dependent signals render human gamma delta-T cells resistant to mitogen-induced apoptosis, permitting the large-scale ex vivo expansion of functionally distinct lymphocytes: implications for the development of adoptive immunotherapy strategies. Blood. 2000;96:3827-3837.
Knight A, Arnouk H, Britt W, et al. CMV-independent lysis of glioblastoma by ex vivo expanded/activated Vδ1+ γδ T cells. PLoS One. 2013;8:e68729.
Deniger DC, Maiti SN, Mi T, et al. Activating and propagating polyclonal gamma delta T cells with broad specificity for malignancies. Clin Cancer Res. 2014;20:5708-5719.
Fisher JP, Yan M, Heuijerjans J, et al. Neuroblastoma killing properties of Vδ2 and Vδ2-negative γδT cells following expansion by artificial antigen-presenting cells. Clin Cancer Res. 2014;20:5720-5732.
Di Lorenzo B, Simões AE, Caiado F, et al. Broad cytotoxic targeting of acute myeloid leukemia by polyclonal delta one T cells. Cancer Immunol Res. 2019;7:552-558.
Couzi L, Pitard V, Moreau JF, et al. Direct and indirect effects of cytomegalovirus-induced γδ T Cells after Kidney Transplantation. Front Immunol. 2015;6:3.
Couzi L, Levaillant Y, Jamai A, et al. Cytomegalovirus-induced gammadelta T cells associate with reduced cancer risk after kidney transplantation. J Am Soc Nephrol. 2010;21:181-188.
Lamb LS Jr, Henslee-Downey PJ, Parrish RS, et al. Increased frequency of TCR gamma delta + T cells in disease-free survivors following T cell-depleted, partially mismatched, related donor bone marrow transplantation for leukemia. J Hematother. 1996;5:503-509.
Godder KT, Henslee-Downey PJ, Mehta J, et al. Long term disease-free survival in acute leukemia patients recovering with increased gammadelta T cells after partially mismatched related donor bone marrow transplantation. Bone Marrow Transplant. 2007;39:751-757.
Khoury JA, Storch GA, Bohl DL, et al. Prophylactic versus preemptive oral valganciclovir for the management of cytomegalovirus infection in adult renal transplant recipients. Am J Transplant. 2006;6:2134-2143.
Reischig T, Hribova P, Jindra P, et al. Long-term outcomes of pre-emptive valganciclovir compared with valacyclovir prophylaxis for prevention of cytomegalovirus in renal transplantation. J Am Soc Nephrol. 2012;23:1588-1597.
Åsberg A, Humar A, Rollag H, et al. Oral valganciclovir is noninferior to intravenous ganciclovir for the treatment of cytomegalovirus disease in solid organ transplant recipients. Am J Transplant. 2007;7:2106-2113.
Åsberg A, Jardine AG, Bignamini AA, et al. Effects of the intensity of immunosuppressive therapy on outcome of treatment for CMV disease in organ transplant recipients. Am J Transplant. 2010;10:1881-1888.
Manuel O, Husain S, Kumar D, et al. Assessment of cytomegalovirus-specific cell-mediated immunity for the prediction of cytomegalovirus disease in high-risk solid-organ transplant recipients: a multicenter cohort study. Clin Infect Dis. 2013;56:817-824.
Jarque M, Melilli E, Crespo E, et al. CMV-specific cell-mediated immunity at 3-month prophylaxis withdrawal discriminates D+/R+ kidney transplants at risk of late-onset CMV infection regardless the type of induction therapy. Transplantation. 2018;102:e472-e480.
Kumar D, Chin-Hong P, Kayler L, et al. A prospective multicenter observational study of cell-mediated immunity as a predictor for cytomegalovirus infection in kidney transplant recipients. Am J Transplant. 2019;19:2505-2516.
Lúcia M, Crespo E, Melilli E, et al. Preformed frequencies of cytomegalovirus (CMV)-specific memory T and B cells identify protected CMV-sensitized individuals among seronegative kidney transplant recipients. Clin Infect Dis. 2014;59:1537-1545.
Kaminski H, Jarque M, Halfon M, et al. Different impact of rATG induction on CMV infection risk in D+R- and R+ KTRs. J Infect Dis. 2019;220:761-771.
Lisboa LF, Kumar D, Wilson LE, et al. Clinical utility of cytomegalovirus cell-mediated immunity in transplant recipients with cytomegalovirus viremia. Transplantation. 2012;93:195-200.
Chemaly RF, El Haddad L, Winston DJ, et al. Cytomegalovirus (CMV) cell-mediated immunity and CMV infection after allogeneic hematopoietic cell transplantation: the REACT study. Clin Infect Dis. 2020. https://doi.org/10.1093/cid/ciz1210
Yong MK, Cameron PU, Slavin M, et al. Identifying cytomegalovirus complications using the quantiferon-CMV assay after allogeneic hematopoietic stem cell transplantation. J Infect Dis. 2017;215:1684-1694.
Nesher L, Shah DP, Ariza-Heredia EJ, et al. Utility of the enzyme-linked immunospot interferon-γ-release assay to predict the risk of cytomegalovirus infection in hematopoietic cell transplant recipients. J Infect Dis. 2016;213:1701-1707.
Barron MA, Gao D, Springer KL, et al. Relationship of reconstituted adaptive and innate cytomegalovirus (CMV)-specific immune responses with CMV viremia in hematopoietic stem cell transplant recipients. Clin Infect Dis. 2009;49:1777-1783.
El Haddad L, Ariza-Heredia E, Shah DP, et al. The ability of a cytomegalovirus ELISPOT assay to predict outcome of low-level CMV reactivation in hematopoietic cell transplant recipients. J Infect Dis. 2019;219:898-907.
Giménez E, Solano C, Piñana JL, et al. Failure of cytomegalovirus-specific CD8+ T cell levels at viral DNAemia onset to predict the eventual need for preemptive antiviral therapy in allogeneic hematopoietic stem cell transplant recipients. J Infect Dis. 2019;219:1510-1512.
Vivier E, Tomasello E, Baratin M, et al. Functions of natural killer cells. Nat Immunol. 2008;9:503-510.
Lopez-Vergès S, Milush JM, Schwartz BS, et al. Expansion of a unique CD57⁺NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci USA. 2011;108:14725-14732.
Foley B, Cooley S, Verneris MR, et al. Human cytomegalovirus (CMV)-induced memory-like NKG2C(+) NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J Immunol. 2012;189:5082-5088.
Foley B, Cooley S, Verneris MR, et al. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood. 2012;119:2665-2674.
Béziat V, Dalgard O, Asselah T, et al. CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur J Immunol. 2012;42:447-457.
Cichocki F, Taras E, Chiuppesi F, et al. Adaptive NK cell reconstitution is associated with better clinical outcomes. JCI Insight. 2019;4:e125553.
Cao K, Marin D, Sekine T, et al. Donor NKG2C copy number: an independent predictor for CMV reactivation after double cord blood transplantation. Front Immunol. 2018;9:2444.
Giménez E, Solano C, Amat P, et al. Enumeration of NKG2C+ natural killer cells early following allogeneic stem cell transplant recipients does not allow prediction of the occurrence of cytomegalovirus DNAemia. J Med Virol. 2015;87:1601-1607.
Ataya M, Redondo-Pachón D, Llinàs-Mallol L, et al. Pretransplant adaptive NKG2C+ NK cells protect against cytomegalovirus infection in kidney transplant recipients. Am J Transplant. 2020;20:663-676.
Kaminski H, Couzi L, Garrigue I, et al. Easier control of late-onset cytomegalovirus disease following universal prophylaxis through an early antiviral immune response in donor-positive, recipient-negative kidney transplants. Am J Transplant. 2016;16:2384-2394.