☆ 4.8 Review

The development of CD8 T-cell exhaustion heterogeneity and the therapeutic potentials in cancer

FRONTIERS IN IMMUNOLOGY (2023)

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Rebalancing TGFβ1/BMP signals in exhausted T cells unlocks responsiveness to immune checkpoint blockade therapy

Abbey A. Saadey et al.

Summary: T cell dysfunctionality hinders the clearance of chronic infections and cancer, and limits their response to immunotherapies. Chronic TGF beta 1 signaling accelerates the dysfunction of CD8(+) T cells through stable epigenetic changes, while boosting BMP signaling and blocking TGF beta 1 preserves effector and memory programs, enhancing immune responses to tumors and synergizing with immune checkpoint blockade responses. Thus, rebalancing TGF beta 1/BMP signals provides a promising approach to unleash dysfunctional CD8(+) T cells and improve T cell immunotherapies.

NATURE IMMUNOLOGY (2023)

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Article Immunology

Hypoxia drives CD39-dependent suppressor function in exhausted T cells to limit antitumor immunity

Paolo D. A. Vignali et al.

Summary: CD8(+) T cells play a crucial role in cancer cell elimination. Exhaustion, a hypofunctional state, can be induced in these cells by factors in the tumor microenvironment (TME). Highly exhausted T (tT(ex)) cells, resistant to checkpoint blockade immunotherapy, resemble CD4(+)Foxp3(+) regulatory T cells and suppress T cell proliferation through CD39-generated immunosuppressive adenosine. Restricting CD39 in endogenous CD8(+) T cells slows tumor progression, improves immunotherapy response, and enhances infiltration of tumor-specific T cells. Induced by tumor hypoxia, CD39 expression on tT(ex) cells can be mitigated to reduce their suppressive effects. Hence, targeting or eliminating tT(ex) cells in the TME could enhance immunotherapy efficacy.

NATURE IMMUNOLOGY (2023)

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Article Immunology

CXCL10 chemokine regulates heterogeneity of the CD8+ T cell response and viral set point during chronic infection

Aleksandra J. Ozga et al.

Summary: The differentiation of CD8(+) T cells in chronic infection is controlled by CXCR3 and CXCL10, which has important therapeutic implications.

IMMUNITY (2022)

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Combination strategies with PD-1/PD-L1 blockade: current advances and future directions

Ming Yi et al.

Summary: Antibodies targeting PD-1/PD-L1 revive immune response against cancer cells, but the low response rate calls for combination therapies. Combining with chemotherapy, radiotherapy, and other treatments can achieve better outcomes, and individualized combination selection is needed to overcome treatment resistance.

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Ton N. Schumacher et al.

Summary: This article discusses the current knowledge on TLSs in cancer, focusing on the drivers of TLS formation, the function and contribution of TLSs to the antitumor immune response, and the potential of TLSs as therapeutic targets in human cancers.

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Tfh-cell-derived interleukin 21 sustains effector CD8+ T cell responses during chronic viral infection

Ryan Zander et al.

Summary: This study found that CD4(+) T cells consist of three distinct subsets during chronic viral infection, and IL-21 derived from Tfh cells is critical for sustaining CD8(+) T cell responses and viral control.

IMMUNITY (2022)

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Human epigenetic and transcriptional T cell differentiation atlas for identifying functional T cell-specific enhancers

Josephine R. Giles et al.

Summary: This study generated an epigenetic and transcriptional atlas of T cell differentiation from healthy humans and applied it to explore disease-specific biology. The study identified molecular regulations of gene expression and chromatin accessibility during T cell differentiation and provided insights into disease biology through three research settings. The study also successfully predicted genome-wide cis-regulatory elements and validated the approach for functional annotation of key effector genes, demonstrating the potential of identifying targets for non-coding cellular engineering.

IMMUNITY (2022)

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Lymphoid tissue residency: A key to understand Tcf-1+PD-1+ T cells

Chaoyu Ma et al.

Summary: This study summarizes recent findings on Tcf-1(+) T cells, focusing on their migratory and resident behavior, as well as the mechanisms underlying their differentiation and maintenance during persistent antigen stimulation.

FRONTIERS IN IMMUNOLOGY (2022)

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MYB orchestrates T cell exhaustion and response to checkpoint inhibition

Carlson Tsui et al.

Summary: This study reveals that CD62L(+) T-PEX cells, maintained by the transcription factor MYB, play a crucial role in maintaining the proliferative potential, multipotency, and repopulation capacity of exhausted T cells during chronic infection, thus contributing to long-term antiviral immunity and responsiveness to immunotherapy.

NATURE (2022)

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Potentiating adoptive cell therapy using synthetic IL-9 receptors

Anusha Kalbasi et al.

Summary: Synthetic receptor signaling has the potential to enhance the functions of adoptively transferred T cells, improving their ability to treat solid tumors. By designing chimeric receptors with an orthogonal IL-2 receptor extracellular domain fused with the intracellular domain of receptors for common gamma-chain cytokines IL-4, IL-7, IL-9, and IL-21, T cells can be activated to elicit corresponding gamma(e) cytokine signals. This activation leads to improved anti-tumor efficacy in challenging mouse models of melanoma and pancreatic cancer.

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cBAF complex components and MYC cooperate early in CD8+ T cell fate

Ao Guo et al.

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Dapl1 controls NFATc2 activation to regulate CD8+ T cell exhaustion and responses in chronic infection and cancer

Lele Zhu et al.

Summary: This study identified Dapl1 as a crucial regulator of CD8(+) T cell immunity, showing that Dapl1 deficiency can lead to functional exhaustion of CD8(+) T cells in chronic infection and cancer.

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Qizhao Huang et al.

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Expansion of T memory stem cells with superior anti-tumor immunity by Urolithin A-induced mitophagy

Dominic Denk et al.

Summary: T memory stem cells (T-SCM) can be expanded by UA and oral administration of UA enhances anti-tumor CD8(+) T cell immunity. The formation of T-SCM cells induced by UA depends on Pink1-mediated mitophagy triggering cytosolic release of Pgam5, which drives Wnt signaling and compensatory mitochondrial biogenesis.

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TGF-β promotes stem-like T cells via enforcing their lymphoid tissue retention

Chaoyu Ma et al.

Summary: This study reveals that TGF-beta promotes lymphoid residency and partially inhibits the effector differentiation of stem-like T cells through controlling the expression of alpha 4 integrins.

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PD-1-cis IL-2R agonism yields better effectors from stem-like CD8+ T cells

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Summary: The study shows that PD1-IL2v can induce the differentiation of stem-like CD8(+) T cells into better effector cells by binding to PD-1, without the need for CD25 binding. PD1-IL2v has superior efficacy compared to PD-1 or PD-L1 blocking antibodies, as it avoids the accumulation of terminally differentiated and exhausted T cells.

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PD-1 combination therapy with IL-2 modifies CD8+ T cell exhaustion program

Masao Hashimoto et al.

Summary: The study showed that combination therapy with PD-1 blockade and IL-2 during chronic lymphocytic choriomeningitis virus infection significantly alters the differentiation program of CD8(+) T cells, resulting in the generation of highly functional effector CD8(+) T cells that mediate viral control, thus providing a new perspective for cancer treatment.

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Divergent clonal differentiation trajectories of T cell exhaustion

Bence Daniel et al.

Summary: In this study, the authors generate a single-cell multiomic atlas of T cell exhaustion in chronic viral infection, revealing molecular programs and clonal differentiation trajectories of exhausted T cell subsets. The results show that T cell receptor signal strength is a driver of clonal fate in T cell exhaustion.

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Shared and distinct biological circuits in effector, memory and exhausted CD8+ T cells revealed by temporal single-cell transcriptomics and epigenetics

Josephine R. Giles et al.

Summary: This study used longitudinal single-cell RNA sequencing and single-cell assay for transposase-accessible chromatin sequencing analyses to uncover new subsets of CD8(+) T cells and explore the epigenetic differences in T-ex cell subsets in different infection states.

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TCF1 in T cell immunity: a broadened frontier

Xudong Zhao et al.

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Memory-like HCV-specific CD8+ T cells retain a molecular scar after cure of chronic HCV infection

Nina Hensel et al.

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IL-2 regulates tumor-reactive CD8+ T cell exhaustion by activating the aryl hydrocarbon receptor

Yuying Liu et al.

Summary: IL-2 acts as an environmental cue to induce CD8(+) T cell exhaustion within tumor microenvironments by activating STAT5, inducing tryptophan hydroxylase 1, and subsequently causing T cell dysfunction.

NATURE IMMUNOLOGY (2021)

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Effector and stem-like memory cell fates are imprinted in distinct lymph node niches directed by CXCR3 ligands

Brigette C. Duckworth et al.

Summary: This study shows that the differentiation fate of T cells is influenced by their location in the lymph node, CXCR3 signaling, and the expression of CXCL9 and CXCL10. Tuning T cell location can promote effector or stem-like memory cell development.

NATURE IMMUNOLOGY (2021)

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Deleting DNMT3A in CAR T cells prevents exhaustion and enhances antitumor activity

Brooke Prinzing et al.

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SCIENCE TRANSLATIONAL MEDICINE (2021)

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LSD1 inhibition sustains T cell invigoration with a durable response to PD-1 blockade

Yi Liu et al.

Summary: Targeting the histone demethylase LSD1 can increase the persistence of exhausted CD8(+) T cells in chronic infections and cancer, improving response to immune checkpoint blockade therapy. This strategy may alleviate T cell exhaustion and enhance the effectiveness of immunotherapy.

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T cell exhaustion-a memory locked behind scars

Amir Yousif et al.

Summary: After clearance of chronic infections, virus-specific CD8(+) T cells regain some memory-related transcriptome features, but their unique open chromatin landscape mostly indicates an exhausted or dysfunctional state, which limits their protective memory potential.

NATURE IMMUNOLOGY (2021)

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Epigenetic scars of CD8+ T cell exhaustion persist after cure of chronic infection in humans

Kathleen B. Yates et al.

Summary: Exhausted CD8(+) T cells exhibit a stable core epigenetic exhaustion signature that is largely irreversible even after the resolution of chronic infection. The epigenetic state of exhaustion persists independent of chronic antigen stimulation and inflammation, suggesting that therapeutic efforts to reverse T cell exhaustion may require increasing the epigenetic plasticity of exhausted T cells.

NATURE IMMUNOLOGY (2021)

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Epigenetic scarring of exhausted T cells hinders memory differentiation upon eliminating chronic antigenic stimulation

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Summary: Exhausted T cells only partially recover memory T cell characteristics upon chronic antigen elimination, with a failure to restore core memory epigenetic circuits, leading to compromised immune responses upon rechallenge.

NATURE IMMUNOLOGY (2021)

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Differentiation of exhausted CD8+ T cells after termination of chronic antigen stimulation stops short of achieving functional T cell memory

Pierre Tonnerre et al.

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Hepatitis C Virus (HCV) Sequence Variation Induces an HCV-Specific T-Cell Phenotype Analogous to Spontaneous Resolution

Victoria Kasprowicz et al.

JOURNAL OF VIROLOGY (2010)

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Article Biochemistry & Molecular Biology

Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF

Michael Quigley et al.

NATURE MEDICINE (2010)

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Article Hematology

Programmed death 1 signaling on chronic myeloid leukemia-specific T cells results in T-cell exhaustion and disease progression

Sabine Mumprecht et al.

BLOOD (2009)

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Article Multidisciplinary Sciences

Selective expansion of a subset of exhausted CD8 T cells by αPD-L1 blockade

Shawn D. Blackburn et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2008)

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Article Medicine, General & Internal

Antigen load and viral sequence diversification determine the functional profile of HIV-1-specific CD8+ T cells

Hendrik Streeck et al.

PLOS MEDICINE (2008)

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Article Immunology

Molecular signature of CD8+ T cell exhaustion during chronic viral infection

E. John Wherry et al.

IMMUNITY (2007)

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Article Multidisciplinary Sciences

Type, density, and location of immune cells within human colorectal tumors predict clinical outcome

Jerom Galon et al.

SCIENCE (2006)

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Article Multidisciplinary Sciences

Restoring function in exhausted CD8 T cells during chronic viral infection

DL Barber et al.

NATURE (2006)

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Article Medicine, Research & Experimental

Reprogramming of antiviral T cells prevents inactivation and restores T cell activity during persistent viral infection

David G. Brooks et al.

JOURNAL OF CLINICAL INVESTIGATION (2006)

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Article Biochemistry & Molecular Biology

CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms

RV Parry et al.

MOLECULAR AND CELLULAR BIOLOGY (2005)

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Article Immunology

SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation

JM Chemnitz et al.

JOURNAL OF IMMUNOLOGY (2004)

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Article Biochemistry & Molecular Biology

Cytokine stimulation of aerobic glycolysis in hematopoietic cells exceeds proliferative demand

DE Bauer et al.

FASEB JOURNAL (2004)

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