Cytomegalovirus-specific T cells restricted for shared and donor human leukocyte antigens differentially impact on cytomegalovirus reactivation risk after allogeneic hematopoietic stem cell transplantation
After allogeneic hematopoietic stem cell transplantation (HSCT), the emergence of circulating cytomegalovirus (CMV)- specific T cells correlates with protection from CMV reactivation, an important risk factor for non-relapse mortality. However, functional assays measuring CMV-specific cells are time...
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| Veröffentlicht in: | Haematologica (Roma) Jg. 108; H. 6; S. 1530 - 1543 |
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Italy
Fondazione Ferrata Storti
01.06.2023
Ferrata Storti Foundation |
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| ISSN: | 0390-6078, 1592-8721, 1592-8721 |
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| Abstract | After allogeneic hematopoietic stem cell transplantation (HSCT), the emergence of circulating cytomegalovirus (CMV)- specific T cells correlates with protection from CMV reactivation, an important risk factor for non-relapse mortality. However, functional assays measuring CMV-specific cells are time-consuming and often inaccurate at early time-points. We report the results of a prospective single-center, non-interventional study that identified the enumeration of Dextramerpositive CMV-specific lymphocytes as a reliable and early predictor of viral reactivation. We longitudinally monitored 75 consecutive patients for 1 year after allogeneic HSCT (n=630 samples). The presence of ≥0.5 CMV-specific CD8+ cells/mL at day +45 was an independent protective factor from subsequent clinically relevant reactivation in univariate (P<0.01) and multivariate (P<0.05) analyses. Dextramer quantification correlated with functional assays measuring interferon-γ production, and allowed earlier identification of high-risk patients. In mismatched transplants, the comparative analysis of lymphocytes restricted by shared, donor- and host-specific HLA revealed the dominant role of thymic-independent CMV-specific reconstitution. Shared and donor-restricted CMV-specific T cells reconstituted with similar kinetics in recipients of CMV-seropositive donors, while donor-restricted T-cell reconstitution from CMV-seronegative grafts was impaired, indicating that in primary immunological responses the emergence of viral-specific T cells is largely sustained by antigen encounter on host infected cells rather than by cross-priming/presentation by non-infected donor-derived antigen-presenting cells. Multiparametric flow cytometry and high-dimensional analysis showed that shared-restricted CMV-specific lymphocytes display a more differentiated phenotype and increased persistence than donor-restricted counterparts. In this study, monitoring CMV-specific cells by Dextramer assay after allogeneic HSCT shed light on mechanisms of immune reconstitution and enabled risk stratification of patients, which could improve the clinical management of post-transplant CMV reactivations. |
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| AbstractList | After allogeneic hematopoietic stem cell transplantation (HSCT), the emergence of circulating cytomegalovirus (CMV)- specific T cells correlates with protection from CMV reactivation, an important risk factor for non-relapse mortality. However, functional assays measuring CMV-specific cells are time-consuming and often inaccurate at early time-points. We report the results of a prospective single-center, non-interventional study that identified the enumeration of Dextramerpositive CMV-specific lymphocytes as a reliable and early predictor of viral reactivation. We longitudinally monitored 75 consecutive patients for 1 year after allogeneic HSCT (n=630 samples). The presence of ≥0.5 CMV-specific CD8+ cells/mL at day +45 was an independent protective factor from subsequent clinically relevant reactivation in univariate (P<0.01) and multivariate (P<0.05) analyses. Dextramer quantification correlated with functional assays measuring interferon-γ production, and allowed earlier identification of high-risk patients. In mismatched transplants, the comparative analysis of lymphocytes restricted by shared, donor- and host-specific HLA revealed the dominant role of thymic-independent CMV-specific reconstitution. Shared and donor-restricted CMV-specific T cells reconstituted with similar kinetics in recipients of CMV-seropositive donors, while donor-restricted T-cell reconstitution from CMV-seronegative grafts was impaired, indicating that in primary immunological responses the emergence of viral-specific T cells is largely sustained by antigen encounter on host infected cells rather than by cross-priming/presentation by non-infected donor-derived antigen-presenting cells. Multiparametric flow cytometry and high-dimensional analysis showed that shared-restricted CMV-specific lymphocytes display a more differentiated phenotype and increased persistence than donor-restricted counterparts. In this study, monitoring CMV-specific cells by Dextramer assay after allogeneic HSCT shed light on mechanisms of immune reconstitution and enabled risk stratification of patients, which could improve the clinical management of post-transplant CMV reactivations.After allogeneic hematopoietic stem cell transplantation (HSCT), the emergence of circulating cytomegalovirus (CMV)- specific T cells correlates with protection from CMV reactivation, an important risk factor for non-relapse mortality. However, functional assays measuring CMV-specific cells are time-consuming and often inaccurate at early time-points. We report the results of a prospective single-center, non-interventional study that identified the enumeration of Dextramerpositive CMV-specific lymphocytes as a reliable and early predictor of viral reactivation. We longitudinally monitored 75 consecutive patients for 1 year after allogeneic HSCT (n=630 samples). The presence of ≥0.5 CMV-specific CD8+ cells/mL at day +45 was an independent protective factor from subsequent clinically relevant reactivation in univariate (P<0.01) and multivariate (P<0.05) analyses. Dextramer quantification correlated with functional assays measuring interferon-γ production, and allowed earlier identification of high-risk patients. In mismatched transplants, the comparative analysis of lymphocytes restricted by shared, donor- and host-specific HLA revealed the dominant role of thymic-independent CMV-specific reconstitution. Shared and donor-restricted CMV-specific T cells reconstituted with similar kinetics in recipients of CMV-seropositive donors, while donor-restricted T-cell reconstitution from CMV-seronegative grafts was impaired, indicating that in primary immunological responses the emergence of viral-specific T cells is largely sustained by antigen encounter on host infected cells rather than by cross-priming/presentation by non-infected donor-derived antigen-presenting cells. Multiparametric flow cytometry and high-dimensional analysis showed that shared-restricted CMV-specific lymphocytes display a more differentiated phenotype and increased persistence than donor-restricted counterparts. In this study, monitoring CMV-specific cells by Dextramer assay after allogeneic HSCT shed light on mechanisms of immune reconstitution and enabled risk stratification of patients, which could improve the clinical management of post-transplant CMV reactivations. After allogeneic hematopoietic stem cell transplantation (HSCT), the emergence of circulating cytomegalovirus (CMV)-specific T cells correlates with protection from CMV reactivation, an important risk factor for non-relapse mortality. However, functional assays measuring CMV-specific cells are time-consuming and often inaccurate at early time-points. We report the results of a prospective single-center, non-interventional study that identified the enumeration of Dextramer-positive CMV-specific lymphocytes as a reliable and early predictor of viral reactivation. We longitudinally monitored 75 consecutive patients for 1 year after allogeneic HSCT (n=630 samples). The presence of ≥0.5 CMV-specific CD8+ cells/mL at day +45 was an independent protective factor from subsequent clinically relevant reactivation in univariate (P<0.01) and multivariate (P<0.05) analyses. Dextramer quantification correlated with functional assays measuring interferon-γ production, and allowed earlier identification of high-risk patients. In mismatched transplants, the comparative analysis of lymphocytes restricted by shared, donor- and host-specific HLA revealed the dominant role of thymic-independent CMV-specific reconstitution. Shared and donor-restricted CMV-specific T cells reconstituted with similar kinetics in recipients of CMV-seropositive donors, while donor-restricted T-cell reconstitution from CMV-seronegative grafts was impaired, indicating that in primary immunological responses the emergence of viral-specific T cells is largely sustained by antigen encounter on host infected cells rather than by cross-priming/presentation by non-infected donor-derived antigen-presenting cells. Multiparametric flow cytometry and high-dimensional analysis showed that shared-restricted CMV-specific lymphocytes display a more differentiated phenotype and increased persistence than donor-restricted counterparts. In this study, monitoring CMV-specific cells by Dextramer assay after allogeneic HSCT shed light on mechanisms of immune reconstitution and enabled risk stratification of patients, which could improve the clinical management of post-transplant CMV reactivations. After allogeneic hematopoietic stem cell transplantation (HSCT), the emergence of circulating cytomegalovirus (CMV)- specific T cells correlates with protection from CMV reactivation, an important risk factor for non-relapse mortality. However, functional assays measuring CMV-specific cells are time-consuming and often inaccurate at early time-points. We report the results of a prospective single-center, non-interventional study that identified the enumeration of Dextramerpositive CMV-specific lymphocytes as a reliable and early predictor of viral reactivation. We longitudinally monitored 75 consecutive patients for 1 year after allogeneic HSCT (n=630 samples). The presence of ≥0.5 CMV-specific CD8+ cells/mL at day +45 was an independent protective factor from subsequent clinically relevant reactivation in univariate (P<0.01) and multivariate (P<0.05) analyses. Dextramer quantification correlated with functional assays measuring interferon-γ production, and allowed earlier identification of high-risk patients. In mismatched transplants, the comparative analysis of lymphocytes restricted by shared, donor- and host-specific HLA revealed the dominant role of thymic-independent CMV-specific reconstitution. Shared and donor-restricted CMV-specific T cells reconstituted with similar kinetics in recipients of CMV-seropositive donors, while donor-restricted T-cell reconstitution from CMV-seronegative grafts was impaired, indicating that in primary immunological responses the emergence of viral-specific T cells is largely sustained by antigen encounter on host infected cells rather than by cross-priming/presentation by non-infected donor-derived antigen-presenting cells. Multiparametric flow cytometry and high-dimensional analysis showed that shared-restricted CMV-specific lymphocytes display a more differentiated phenotype and increased persistence than donor-restricted counterparts. In this study, monitoring CMV-specific cells by Dextramer assay after allogeneic HSCT shed light on mechanisms of immune reconstitution and enabled risk stratification of patients, which could improve the clinical management of post-transplant CMV reactivations. |
| Author | Oliveira, Giacomo Ciceri, Fabio Bernardi, Massimo Lupo-Stanghellini, Maria T. Abbati, Danilo Oltolini, Chiara Clerici, Daniela Farina, Francesca Greco, Raffaella Tassi, Elena Bonini, Chiara Beretta, Valeria Noviello, Maddalena Manfredi, Francesco Corti, Consuelo Dvir, Roee Peccatori, Jacopo Ruggiero, Eliana Clementi, Massimo Serio, Francesca Lorentino, Francesca Xue, Elisabetta Vago, Luca Brix, Liselotte Doglio, Matteo Giglio, Fabio Valtolina, Veronica Campodonico, Edoardo De Simone, Pantaleo Racca, Sara |
| AuthorAffiliation | 2 Cell Therapy Immunomonitoring Laboratory (MITiCi) , Division of Immunology, Transplantation and Infectious Diseases, Ospedale San Raffaele Scientific Institute , Milan, Italy 5 Infectious Disease Unit , Ospedale San Raffaele Scientific Institute , Milan, Italy 3 Unit of Hematology and Bone Marrow Transplantation, Ospedale San Raffaele Scientific Institute , Milan, Italy 4 Laboratory of Clinical Microbiology and Virology, Ospedale San Raffaele Scientific Institute , Milan, Italy 6 Unit of Immunogenetics, Leukemia Genomics and Immunobiology, Division of Immunology, Transplantation and Infectious Diseases, Ospedale San Raffaele Scientific Institute , Milan, Italy 7 Università Vita-Salute San Raffaele, Milan, Italy 1 Experimental Hematology Unit , Division of Immunology, Transplantation and Infectious Diseases, Ospedale San Raffaele Scientific Institute , Milan, Italy 8 Immudex ApS, Virum, Denmark |
| AuthorAffiliation_xml | – name: 4 Laboratory of Clinical Microbiology and Virology, Ospedale San Raffaele Scientific Institute , Milan, Italy – name: 6 Unit of Immunogenetics, Leukemia Genomics and Immunobiology, Division of Immunology, Transplantation and Infectious Diseases, Ospedale San Raffaele Scientific Institute , Milan, Italy – name: 8 Immudex ApS, Virum, Denmark – name: 3 Unit of Hematology and Bone Marrow Transplantation, Ospedale San Raffaele Scientific Institute , Milan, Italy – name: 1 Experimental Hematology Unit , Division of Immunology, Transplantation and Infectious Diseases, Ospedale San Raffaele Scientific Institute , Milan, Italy – name: 2 Cell Therapy Immunomonitoring Laboratory (MITiCi) , Division of Immunology, Transplantation and Infectious Diseases, Ospedale San Raffaele Scientific Institute , Milan, Italy – name: 7 Università Vita-Salute San Raffaele, Milan, Italy – name: 5 Infectious Disease Unit , Ospedale San Raffaele Scientific Institute , Milan, Italy |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36200418$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1080/17474086.2017.1318054 10.1093/ofid/ofw107 10.1007/978-3-540-77349-8_4 10.1038/s41409-018-0167-8 10.1093/infdis/jix357 10.1016/j.jtct.2021.03.003 10.1016/j.jinf.2016.04.033 10.1016/j.jcv.2018.01.002 10.1016/j.bbmt.2018.12.070 10.1016/j.hoc.2010.11.011 10.1371/journal.pone.0074744 10.1182/blood.V97.5.1232 10.1128/JVI.02128-16 10.1126/scitranslmed.aac8265 10.1182/blood.2020009362 10.1182/blood.2020009396 10.1371/journal.pone.0213739 10.1371/journal.pone.0106044 10.1111/ajt.16450 10.3324/haematol.2019.229252 10.1056/NEJMoa1706640 10.1016/j.bbmt.2015.04.025 10.1097/MOH.0b013e328353bc7d 10.1182/blood.V83.7.1971.1971 10.1093/cid/ciz490 10.1016/S1473-3099(19)30107-0 10.1093/cid/ciw668 10.1093/cid/ciz1210 10.1182/blood-2010-03-273508 10.1007/s12026-009-8139-0 10.1093/infdis/jiy592 10.1182/blood-2016-06-723205 10.1038/sj.bmt.1705825 10.1007/s00277-015-2446-4 10.1038/s41577-020-00457-z 10.1002/cyto.b.21196 10.1182/bloodadvances.2021004362 10.1084/jem.20051787 10.1182/bloodadvances.2020003418 10.1002/eji.202049103 10.1111/ajt.12049 10.1182/blood-2009-12-234096 10.1038/bmt.2015.132 10.1093/infdis/jix192 10.1172/JCI129965 10.1016/j.bbmt.2020.01.013 10.1038/s41409-021-01227-8 10.1016/j.jcv.2016.08.290 10.4049/jimmunol.177.2.777 10.1016/j.immuni.2008.07.017 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Disclosures ET and MN designed the study, conducted laboratory experiments, analyzed and interpreted data and wrote the paper; PDS designed the study, conducted laboratory experiments, and analyzed and interpreted data; MTLS, FS, EC, DC, FG, FL, EX, FF, CO, CC and MB provided clinical data and samples and participated in the data interpretation; MD performed statistical analyses; DA and FM participated in the high dimensional analysis of flow cytometry data; VB and VV participated in the laboratory experiments; GO participated in the design of the study; SR, RD and MC performed the QuantiFERON-CMV, and analyzed and interpreted the results; ER and LV participated in the discussion and interpretation of data; LB participated in the study design and reviewed the paper; FC and JP designed and supervised the study; RG and CB designed and supervised the study and wrote the paper. Contributions CB has received research support from Intellia Therapeutics and is a member of advisory boards or a consultant or speaker for Molmed, Intellia, TxCell, Novartis, GSK, Allogene, Kite/Gilead, Miltenyi, Kiadis, QuellTX, and Janssen. RG discloses honoraria for speaking at educational events supported by Biotest, Medac, Pfizer and Magenta. The datasets generated for this study are available on request to the corresponding author. Data-sharing statement |
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| References | 48308 48307 48306 48305 48304 48303 48268 48302 48269 48301 48309 48266 48300 48267 48291 48292 48290 48299 48297 48298 48295 48296 48293 48294 48280 48281 48288 48289 48286 48287 48284 48285 48282 48283 48315 48314 48279 48313 48312 48270 48277 48311 48278 48310 48275 48276 48273 48274 48271 48272 36453111 - Haematologica. 2023 Jun 01;108(6):1461-1462 |
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| Snippet | After allogeneic hematopoietic stem cell transplantation (HSCT), the emergence of circulating cytomegalovirus (CMV)- specific T cells correlates with... After allogeneic hematopoietic stem cell transplantation (HSCT), the emergence of circulating cytomegalovirus (CMV)-specific T cells correlates with protection... |
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| SubjectTerms | CD8-Positive T-Lymphocytes Cell Therapy & Immunotherapy Cytomegalovirus - physiology Cytomegalovirus Infections - etiology Hematopoietic Stem Cell Transplantation - adverse effects Hematopoietic Stem Cell Transplantation - methods HLA Antigens Humans Prospective Studies T-Lymphocytes Transplantation, Homologous |
| Title | Cytomegalovirus-specific T cells restricted for shared and donor human leukocyte antigens differentially impact on cytomegalovirus reactivation risk after allogeneic hematopoietic stem cell transplantation |
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