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Article: Complete response to PD-1 blockade following EBV-specific T-cell therapy in metastatic nasopharyngeal carcinoma.

Smith, Corey / McGrath, Margaret / Neller, Michelle A / Matthews, Katherine K / Crooks, Pauline / Le Texier, Laetitia / Panizza, Benedict / Porceddu, Sandro / Khanna, Rajiv

NPJ precision oncology

2021 Volume 5, Issue 1, Page(s) 24

Abstract: Nasopharyngeal carcinoma (NPC) is an Epstein-Barr virus (EBV)-associated heterogeneous disease and is characterized by peritumoral immune infiltrate. Adoptive T-cell therapy (ACT) has emerged as a potential therapeutic strategy for NPC. However, the ... ...

Abstract	Nasopharyngeal carcinoma (NPC) is an Epstein-Barr virus (EBV)-associated heterogeneous disease and is characterized by peritumoral immune infiltrate. Adoptive T-cell therapy (ACT) has emerged as a potential therapeutic strategy for NPC. However, the tumor microenvironment remains a major roadblock for the successful implementation of ACT in clinical settings. Expression of checkpoint molecules by malignant cells can inhibit the effector function of adoptively transferred EBV-specific T cells. Here we present a novel case report of a patient with metastatic NPC who was successfully treated with a combination of EBV-specific ACT and programmed cell death-1 blockade therapy. Following combination immunotherapy, the patient showed complete resolution of metastatic disease with no evidence of disease relapse for 22 months. Follow-up immunological analysis revealed dramatic restructuring of the global T-cell repertoire that was coincident with the clinical response. This case report provides an important platform for translating these findings to a larger cohort of NPC patients.
Language	English
Publishing date	2021-03-19
Publishing country	England
Document type	Journal Article
ISSN	2397-768X
ISSN	2397-768X
DOI	10.1038/s41698-021-00162-7
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Article ; Online: SARS-CoV-2-specific T cells generated for adoptive immunotherapy are capable of recognizing multiple SARS-CoV-2 variants.

Panikkar, Archana / Lineburg, Katie E / Raju, Jyothy / Chew, Keng Yih / Ambalathingal, George R / Rehan, Sweera / Swaminathan, Srividhya / Crooks, Pauline / Le Texier, Laetitia / Beagley, Leone / Best, Shannon / Solomon, Matthew / Matthews, Katherine K / Srihari, Sriganesh / Neller, Michelle A / Short, Kirsty R / Khanna, Rajiv / Smith, Corey

PLoS pathogens

2022 Volume 18, Issue 2, Page(s) e1010339

Abstract: Adoptive T-cell immunotherapy has provided promising results in the treatment of viral complications in humans, particularly in the context of immunocompromised patients who have exhausted all other clinical options. The capacity to expand T cells from ... ...

Abstract	Adoptive T-cell immunotherapy has provided promising results in the treatment of viral complications in humans, particularly in the context of immunocompromised patients who have exhausted all other clinical options. The capacity to expand T cells from healthy immune individuals is providing a new approach to anti-viral immunotherapy, offering rapid off-the-shelf treatment with tailor-made human leukocyte antigen (HLA)-matched T cells. While most of this research has focused on the treatment of latent viral infections, emerging evidence that SARS-CoV-2-specific T cells play an important role in protection against COVID-19 suggests that the transfer of HLA-matched allogeneic off-the-shelf virus-specific T cells could provide a treatment option for patients with active COVID-19 or at risk of developing COVID-19. We initially screened 60 convalescent individuals and based on HLA typing and T-cell response profile, 12 individuals were selected for the development of a SARS-CoV-2-specific T-cell bank. We demonstrate that these T cells are specific for up to four SARS-CoV-2 antigens presented by a broad range of both HLA class I and class II alleles. These T cells show consistent functional and phenotypic properties, display cytotoxic potential against HLA-matched targets and can recognize HLA-matched cells infected with different SARS-CoV-2 variants. These observations demonstrate a robust approach for the production of SARS-CoV-2-specific T cells and provide the impetus for the development of a T-cell repository for clinical assessment.
MeSH term(s)	Adult ; Epitopes, T-Lymphocyte ; Female ; HEK293 Cells ; HLA Antigens/immunology ; Humans ; Immunophenotyping ; Immunotherapy, Adoptive ; Male ; Middle Aged ; SARS-CoV-2/immunology ; T-Lymphocytes/immunology ; Young Adult
Chemical Substances	Epitopes, T-Lymphocyte ; HLA Antigens
Language	English
Publishing date	2022-02-14
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1010339
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Article: Impact of pre-therapy glioblastoma multiforme microenvironment on clinical response to autologous CMV-specific T-cell therapy.

Walker, David G / Shakya, Reshma / Morrison, Beth / Neller, Michelle A / Matthews, Katherine K / Nicholls, John / Smith, Corey / Khanna, Rajiv

Clinical & translational immunology

2019 Volume 8, Issue 11, Page(s) e01088

Abstract: Objectives: Clinical response to antibody-based immunotherapies targeting checkpoint inhibitors is critically dependent on the tumor immune microenvironment (TIME). However, the precise impact of the TIME on adoptive cellular immunotherapy remains ... ...

Abstract	Objectives: Clinical response to antibody-based immunotherapies targeting checkpoint inhibitors is critically dependent on the tumor immune microenvironment (TIME). However, the precise impact of the TIME on adoptive cellular immunotherapy remains unexplored. Here we have conducted a long-term follow-up analysis of patients with recurrent glioblastoma multiforme (GBM) who were treated with autologous CMV-specific T-cell therapy to delineate the potential impact of the TIME on their clinical response. Methods: Multiplexed immunohistochemical analysis of CD3, PD-L1 and Sox-2 in GBM tissue biopsies obtained before autologous T-cell therapy was carried out and correlated with long-term survival of GBM patients adoptively treated with T-cell therapy. Results: Tumor microenvironment analyses revealed that the pre-treatment cellular composition of the tumor tissue may influence the subsequent response to adoptive T-cell therapy. GBM patients who showed prolonged overall survival following T-cell therapy had a significantly lower number of tumor-infiltrating CD3 Conclusion: We hypothesise that lack of PD-L1-mediated immunosuppression in the TIME may allow efficient immune control following adoptive T-cell therapy. Future studies combining anti-PD-L1 or genetically modified T cells with PD-1 receptor knockdown could be considered to improve clinical responses in patients who have high PD-L1 expression in their tumors.
Language	English
Publishing date	2019-11-05
Publishing country	Australia
Document type	Journal Article
ZDB-ID	2694482-0
ISSN	2050-0068
ISSN	2050-0068
DOI	10.1002/cti2.1088
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Article: Rapid detection of SARS-CoV-2-specific memory T-cell immunity in recovered COVID-19 cases.

Lineburg, Katie E / Srihari, Sriganesh / Altaf, Mohammed / Swaminathan, Srividhya / Panikkar, Archana / Raju, Jyothy / Crooks, Pauline / Ambalathingal, George R / Martins, Jose Paulo / Matthews, Katherine K / Neller, Michelle A / Khanna, Rajiv / Smith, Corey

Clinical & translational immunology

2020 Volume 9, Issue 12, Page(s) e1219

Abstract: Objectives: There is emerging evidence that SARS-CoV-2-specific memory T-cell responses are likely to provide critical long-term protection against COVID-19. Strategies to rapidly assess T-cell responses are therefore likely to be important for ... ...

Abstract	Objectives: There is emerging evidence that SARS-CoV-2-specific memory T-cell responses are likely to provide critical long-term protection against COVID-19. Strategies to rapidly assess T-cell responses are therefore likely to be important for assessing immunity in the global population. Methods: Here, we have developed a rapid immune-monitoring strategy to assess virus-specific memory T-cell responses in the peripheral blood of COVID-19 convalescent individuals. We validated SARS-CoV-2-specific memory T-cell responses detected in whole blood using Results: T-cell immunity characterised by the production of IFN-γ and IL-2 could be consistently detected in the whole blood of recovered participants. T cells predominantly recognised structural SARS-CoV-2 proteins. Conclusion: These observations provide a timely monitoring approach for identifying SARS-CoV-2 cellular immunity and may serve as a diagnostic for the stratification of risk in immunocompromised and other at-risk individuals.
Language	English
Publishing date	2020-12-07
Publishing country	Australia
Document type	Journal Article
ZDB-ID	2694482-0
ISSN	2050-0068
ISSN	2050-0068
DOI	10.1002/cti2.1219
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Article ; Online: Pretransplant Cytomegalovirus-Specific Cellular Immunity and Risk of Viral Reactivation Following Lung Transplantation: A Prospective Cohort Study.

Altaf, Mohammed / Lineburg, Katie E / Crooks, Pauline / Rehan, Sweera / Matthews, Katherine K / Neller, Michelle A / Ambalathingal, George R / Sinha, Debottam / Grant, Michelle / Hopkins, Peter M A / Chambers, Daniel / Khanna, Rajiv / Smith, Corey

The Journal of infectious diseases

2020 Volume 224, Issue 2, Page(s) 312–317

Abstract: Cytomegalovirus (CMV) remains a significant burden in lung transplant recipients. Deficiencies in T-cell immunity posttransplant increase the risk of CMV-associated complications. However, it is not clear if underlying poor pretransplant immunity ... ...

Abstract	Cytomegalovirus (CMV) remains a significant burden in lung transplant recipients. Deficiencies in T-cell immunity posttransplant increase the risk of CMV-associated complications. However, it is not clear if underlying poor pretransplant immunity increases risk. To assess this, we recruited 39 prospective lung transplant patients and performed QuantiFERON-CMV on their peripheral blood. More than a third of prospective CMV-seropositive transplant recipients were CMV non-immune reactive (CMV-NIR) pretransplant. CMV-NIR status was associated with a significantly higher incidence of CMV reactivation posttransplant, demonstrating that dysfunctional CMV immunity in prospective lung transplant recipients is associated with an increased risk of viral reactivation posttransplant.
MeSH term(s)	Cytomegalovirus Infections/epidemiology ; Cytomegalovirus Infections/immunology ; Humans ; Immunity, Cellular ; Latent Infection/virology ; Lung Transplantation/adverse effects ; Prospective Studies
Language	English
Publishing date	2020-12-03
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3019-3
ISSN	1537-6613 ; 0022-1899
ISSN (online)	1537-6613
ISSN	0022-1899
DOI	10.1093/infdis/jiaa750
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Article ; Online: T cell repertoire remodeling following post-transplant T cell therapy coincides with clinical response.

Smith, Corey / Corvino, Dillon / Beagley, Leone / Rehan, Sweera / Neller, Michelle A / Crooks, Pauline / Matthews, Katherine K / Solomon, Matthew / Le Texier, Laetitia / Campbell, Scott / Francis, Ross S / Chambers, Daniel / Khanna, Rajiv

The Journal of clinical investigation

2019 Volume 129, Issue 11, Page(s) 5020–5032

Abstract: BACKGROUNDImpaired T cell immunity in transplant recipients is associated with infection-related morbidity and mortality. We recently reported the successful use of adoptive T cell therapy (ACT) against drug-resistant/recurrent cytomegalovirus in solid- ... ...

Abstract	BACKGROUNDImpaired T cell immunity in transplant recipients is associated with infection-related morbidity and mortality. We recently reported the successful use of adoptive T cell therapy (ACT) against drug-resistant/recurrent cytomegalovirus in solid-organ transplant recipients.METHODSIn the present study, we used high-throughput T cell receptor Vβ sequencing and T cell functional profiling to delineate the impact of ACT on T cell repertoire remodeling in the context of pretherapy immunity and ACT products.RESULTSThese analyses indicated that a clinical response was coincident with significant changes in the T cell receptor Vβ landscape after therapy. This restructuring was associated with the emergence of effector memory T cells in responding patients, while nonresponders displayed dramatic pretherapy T cell expansions with minimal change following ACT. Furthermore, immune reconstitution included both adoptively transferred clonotypes and endogenous clonotypes not detected in the ACT products.CONCLUSIONThese observations demonstrate that immune control following ACT requires significant repertoire remodeling, which may be impaired in nonresponders because of the preexisting immune environment. Immunological interventions that can modulate this environment may improve clinical outcomes.TRIAL REGISTRATIONAustralian New Zealand Clinical Trial Registry, ACTRN12613000981729.FUNDINGThis study was supported by funding from the National Health and Medical Research Council, Australia (APP1132519 and APP1062074).
MeSH term(s)	Adoptive Transfer ; Adult ; Cytomegalovirus/immunology ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/pathology ; Cytomegalovirus Infections/therapy ; Drug Resistance, Viral/immunology ; Female ; Humans ; Male ; Organ Transplantation ; Receptors, Antigen, T-Cell, alpha-beta/immunology ; T-Lymphocytes/immunology ; T-Lymphocytes/pathology ; T-Lymphocytes/transplantation
Chemical Substances	Receptors, Antigen, T-Cell, alpha-beta
Language	English
Publishing date	2019-08-15
Publishing country	United States
Document type	Clinical Trial, Phase I ; Journal Article ; Multicenter Study ; Research Support, Non-U.S. Gov't
ZDB-ID	3067-3
ISSN	1558-8238 ; 0021-9738
ISSN (online)	1558-8238
ISSN	0021-9738
DOI	10.1172/JCI128323
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Article ; Online: Autologous CMV-specific T cells are a safe adjuvant immunotherapy for primary glioblastoma multiforme.

Smith, Corey / Lineburg, Katie E / Martins, J Paulo / Ambalathingal, George R / Neller, Michelle A / Morrison, Beth / Matthews, Katherine K / Rehan, Sweera / Crooks, Pauline / Panikkar, Archana / Beagley, Leone / Le Texier, Laetitia / Srihari, Sriganesh / Walker, David / Khanna, Rajiv

The Journal of clinical investigation

2020 Volume 130, Issue 11, Page(s) 6041–6053

Abstract: BACKGROUNDThe recent failure of checkpoint-blockade therapies for glioblastoma multiforme (GBM) in late-phase clinical trials has directed interest toward adoptive cellular therapies (ACTs). In this open-label, first-in-human trial, we have assessed the ... ...

Abstract	BACKGROUNDThe recent failure of checkpoint-blockade therapies for glioblastoma multiforme (GBM) in late-phase clinical trials has directed interest toward adoptive cellular therapies (ACTs). In this open-label, first-in-human trial, we have assessed the safety and therapeutic potential of cytomegalovirus-specific (CMV-specific) ACT in an adjuvant setting for patients with primary GBM, with an ultimate goal to prevent or delay recurrence and prolong overall survival.METHODSTwenty-eight patients with primary GBM were recruited to this prospective study, 25 of whom were treated with in vitro-expanded autologous CMV-specific T cells. Participants were monitored for safety, progression-free survival, overall survival (OS), and immune reconstitution.RESULTSNo participants showed evidence of ACT-related toxicities. Of 25 evaluable participants, 10 were alive at the completion of follow-up, while 5 were disease free. Reconstitution of CMV-specific T cell immunity was evident and CMV-specific ACT may trigger a bystander effect leading to additional T cell responses to nonviral tumor-associated antigens through epitope spreading. Long-term follow-up of participants treated before recurrence showed significantly improved OS when compared with those who progressed before ACT (median 23 months, range 7-65 vs. median 14 months, range 5-19; P = 0.018). Gene expression analysis of the ACT products indicated that a favorable T cell gene signature was associated with improved long-term survival.CONCLUSIONData presented in this study demonstrate that CMV-specific ACT can be safely used as an adjuvant therapy for primary GBM and, if offered before recurrence, this therapy may improve OS of GBM patients.TRIAL REGISTRATIONanzctr.org.au: ACTRN12615000656538.FUNDINGPhilanthropic funding and the National Health and Medical Research Council (Australia).
MeSH term(s)	Adult ; Blood Transfusion, Autologous ; Cytomegalovirus/immunology ; Disease-Free Survival ; Female ; Follow-Up Studies ; Glioblastoma/immunology ; Glioblastoma/mortality ; Glioblastoma/therapy ; Humans ; Lymphocyte Transfusion ; Male ; Middle Aged ; Prospective Studies ; Survival Rate ; T-Lymphocytes/immunology
Language	English
Publishing date	2020-08-04
Publishing country	United States
Document type	Clinical Trial ; Journal Article ; Multicenter Study ; Research Support, Non-U.S. Gov't
ZDB-ID	3067-3
ISSN	1558-8238 ; 0021-9738
ISSN (online)	1558-8238
ISSN	0021-9738
DOI	10.1172/JCI138649
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Article ; Online: Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function.

Thomas, Sharyn / Mohammed, Fiyaz / Reijmers, Rogier M / Woolston, Annemarie / Stauss, Theresa / Kennedy, Alan / Stirling, David / Holler, Angelika / Green, Louisa / Jones, David / Matthews, Katherine K / Price, David A / Chain, Benjamin M / Heemskerk, Mirjam H M / Morris, Emma C / Willcox, Benjamin E / Stauss, Hans J

Nature communications

2019 Volume 10, Issue 1, Page(s) 4451

Abstract: TCR-gene-transfer is an efficient strategy to produce therapeutic T cells of defined antigen specificity. However, there are substantial variations in the cell surface expression levels of human TCRs, which can impair the function of engineered T cells. ... ...

Abstract	TCR-gene-transfer is an efficient strategy to produce therapeutic T cells of defined antigen specificity. However, there are substantial variations in the cell surface expression levels of human TCRs, which can impair the function of engineered T cells. Here we demonstrate that substitutions of 3 amino acid residues in the framework of the TCR variable domains consistently increase the expression of human TCRs on the surface of engineered T cells.The modified TCRs mediate enhanced T cell proliferation, cytokine production and cytotoxicity, while reducing the peptide concentration required for triggering effector function up to 3000-fold. Adoptive transfer experiments in mice show that modified TCRs control tumor growth more efficiently than wild-type TCRs. Our data indicate that simple variable domain modifications at a distance from the antigen-binding loops lead to increased TCR expression and improved effector function. This finding provides a generic platform to optimize the efficacy of TCR gene therapy in humans.
MeSH term(s)	Animals ; Antigens/immunology ; Antigens, CD/metabolism ; Antigens, Differentiation, T-Lymphocyte/metabolism ; Cell Engineering ; Cell Line, Tumor ; Cell Proliferation ; Cytokines/metabolism ; Gene Expression ; Genes, T-Cell Receptor/genetics ; Genes, T-Cell Receptor/immunology ; Genetic Therapy ; Humans ; Lectins, C-Type/metabolism ; Lymphocyte Activation ; Male ; Mice ; Mice, Inbred NOD ; Mice, SCID ; Models, Molecular ; Protein Domains ; Protein Engineering ; Receptors, Antigen, T-Cell/chemistry ; Receptors, Antigen, T-Cell/genetics ; Receptors, Antigen, T-Cell/immunology ; Receptors, Antigen, T-Cell/metabolism ; T-Lymphocytes/immunology ; T-Lymphocytes/metabolism
Chemical Substances	Antigens ; Antigens, CD ; Antigens, Differentiation, T-Lymphocyte ; CD69 antigen ; Cytokines ; Lectins, C-Type ; Receptors, Antigen, T-Cell
Language	English
Publishing date	2019-10-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-019-12441-w
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Article ; Online: Epstein-Barr virus-specific T cell therapy for progressive multiple sclerosis.

JCI insight

2020 Volume 5, Issue 20

Language	English
Publishing date	2020-10-15
Publishing country	United States
Document type	Journal Article ; Published Erratum
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.144624
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Article ; Online: Activation-Induced Killer Cell Immunoglobulin-like Receptor 3DL2 Binding to HLA-B27 Licenses Pathogenic T Cell Differentiation in Spondyloarthritis.

Ridley, Anna / Hatano, Hiroko / Wong-Baeza, Isabel / Shaw, Jacqueline / Matthews, Katherine K / Al-Mossawi, Hussein / Ladell, Kristin / Price, David A / Bowness, Paul / Kollnberger, Simon

Arthritis & rheumatology (Hoboken, N.J.)

2016 Volume 68, Issue 4, Page(s) 901–914

Abstract: Objective: In the spondyloarthritides (SpA), increased numbers of CD4+ T cells express killer cell immunoglobulin-like receptor 3DL2 (KIR-3DL2). The aim of this study was to determine the factors that induce KIR-3DL2 expression, and to characterize the ... ...

Abstract	Objective: In the spondyloarthritides (SpA), increased numbers of CD4+ T cells express killer cell immunoglobulin-like receptor 3DL2 (KIR-3DL2). The aim of this study was to determine the factors that induce KIR-3DL2 expression, and to characterize the relationship between HLA-B27 and the phenotype and function of KIR-3DL2-expressing CD4+ T cells in SpA. Methods: In total, 34 B27+ patients with SpA, 28 age- and sex-matched healthy controls (20 B27- and 8 B27+), and 9 patients with rheumatoid arthritis were studied. KIR-3DL2 expression and other phenotypic characteristics of peripheral blood and synovial fluid CD4+ T cells were studied by flow cytometry, quantitative polymerase chain reaction, and Western blotting. T cell receptor clonality was determined by template-switch anchored reverse transcription-polymerase chain reaction and sequencing analysis. Cytokines were measured by enzyme-linked immunosorbent assay. Results: Cellular activation induced KIR-3DL2 expression on both naive and effector CD4+ T cells. KIR-3DL2 binding to B27+ cells promoted expression of KIR-3DL2, the Th17-specific transcription factor retinoic acid receptor-related orphan nuclear receptor γt, and the antiapoptotic factor B cell lymphoma 2. KIR-3DL2+CD4+ T cells in patients with ankylosing spondylitis were oligoclonal and enriched for markers of T cell activation and for the gut homing receptor CCR9. In the presence of B27+ antigen-presenting cells, KIR-3DL2+CD4+ T cells produced less interleukin-2 (IL-2) but more IL-17. This effect was blocked by HC10, an antibody that inhibits the binding of KIR-3DL2 to B27 heavy chains. Conclusion: KIR-3DL2 binding to HLA-B27 licenses Th17 cell differentiation in SpA. These findings raise the therapeutic potential of targeting HLA-B27-KIR-3DL2 interactions for the treatment of B27+ patients with SpA.
MeSH term(s)	Adult ; Aged ; Arthritis, Psoriatic/immunology ; Arthritis, Reactive/immunology ; Arthritis, Rheumatoid/immunology ; Blotting, Western ; CD4-Positive T-Lymphocytes/immunology ; Case-Control Studies ; Cell Differentiation/immunology ; Cytokines/immunology ; Enzyme-Linked Immunosorbent Assay ; Female ; Flow Cytometry ; HLA-B27 Antigen/immunology ; HLA-B27 Antigen/metabolism ; Humans ; Male ; Middle Aged ; Receptors, Antigen, T-Cell/genetics ; Receptors, KIR3DL2/immunology ; Receptors, KIR3DL2/metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; Spondylarthropathies/immunology ; Spondylitis, Ankylosing/immunology ; T-Lymphocytes/immunology ; Th17 Cells/immunology ; Transcriptome ; Young Adult
Chemical Substances	Cytokines ; HLA-B27 Antigen ; KIR3DL2 protein, human ; Receptors, Antigen, T-Cell ; Receptors, KIR3DL2
Language	English
Publishing date	2016-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2756371-6
ISSN	2326-5205 ; 2326-5191
ISSN (online)	2326-5205
ISSN	2326-5191
DOI	10.1002/art.39515
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