Preferential Cell Death of CD8+ Effector Memory (CCR7−CD45RA−) T Cells by Hydrogen Peroxide-Induced Oxidative Stress

Takahashi, Akihiro; Hanson, Mikael G V; Norell, Håkan R; Havelka, Aleksandra Mandic; Kono, Koji; Malmberg, Karl-Johan; Kiessling, Rolf V R

doi:10.4049/jimmunol.174.10.6080

Cited by 101Cell death mechanisms and regulationT-cell and B-cell ImmunologyRedox biology and oxidative stress

Preferential Cell Death of CD8+ Effector Memory (CCR7−CD45RA−) T Cells by Hydrogen Peroxide-Induced Oxidative Stress

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Takahashi, Akihiro, Hanson, Mikael G V, Norell, Håkan R, Havelka, Aleksandra Mandic, Kono, Koji, Malmberg, Karl-Johan, Kiessling, Rolf V R·2005·The Journal of Immunology

DOI 10.4049/jimmunol.174.10.6080

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Abstract

T cells are used in many cell-based cancer treatments. However, oxidative stress that is induced during various chronic inflammatory conditions, such as cancer, can impair the immune system and have detrimental effects on T cell function. In this study, we have investigated the sensitivity of different human T cell subsets to H2O2-induced oxidative stress. We showed that central memory (CD45RA−CCR7+) and effector memory (CD45RA−CCR7−) T cells are more sensitive to H2O2 as compared with naive (CD45RA+CCR7+) T cells. Furthermore, the study showed that CD8+ effector memory T cells are more sensitive to low levels of H2O2 (5 μM) compared with other types of T cells investigated. H2O2-exposed CD45RO+ T cells showed mitochondrial depolarization prior to caspase 3 activity. Moreover, the pan-caspase inhibitor z-Val-Ala-Asp(OMe)-fluoromethylketone rescued cells from death. These experiments suggest that H2O2-induced cell death of CD45RO+ T cells acts via the mitochondrial pathway and that caspase involvement is needed. This study suggests that oxidative stress in cancer patients can be disadvantageous for T cell-based adoptive cell transfer therapies, since effector memory T cells are the primary phenotype of the cells administered.

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T cells expressing CD57 and KLRG1 are more susceptible to H2O2-induced apoptosis than total lymphocytes and naive phenotype cells in vitro.
“T cells expressing cell-surface proteins associated with differentiation or “senescence” (e.g., CD57 and KLRG1) are more susceptible to H2O2 induced apoptosis than total lymphocytes (Wang and Lin 2010) and cells of a naïve phenotype (e.g., CD45RA + CCR7+) in vitro (Takahashi et al. 2005).”
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Camouflage and sabotage: tumor escape from the immune system
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Amino Acids and Immune Response: A Role for Cysteine, Glutamine, Phenylalanine, Tryptophan and Arginine in T-cell Function and Cancer?
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Redox-signaling transmitted in trans to neighboring cells by melanoma-derived TNF-containing exosomes
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Aging and immunity – Impact of behavioral intervention
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MDSC in Mice and Men: Mechanisms of Immunosuppression in Cancer
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Does Regular Exercise Counter T Cell Immunosenescence Reducing the Risk of Developing Cancer and Promoting Successful Treatment of Malignancies?
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Tumour‐induced immune suppression: role of inflammatory mediators released by myelomonocytic cells
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The Immune Signature of CD8+CCR7+ T Cells in the Peripheral Circulation Associates with Disease Recurrence in Patients with HNSCC
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A candidate anti-HIV reservoir compound, auranofin, exerts a selective ‘anti-memory’ effect by exploiting the baseline oxidative status of lymphocytes
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Cold Physical Plasma Treatment Alters Redox Balance in Human Immune Cells
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Reactive oxygen species associated immunoregulation post influenza virus infection
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Intratumoral Hydrogen Peroxide With Radiation Therapy in Locally Advanced Breast Cancer: Results From a Phase 1 Clinical Trial
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Novel Application of Localized Nanodelivery of Anti–Interleukin-6 Protects Organ Transplant From Ischemia–Reperfusion Injuries
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Reactive oxygen homeostasis – the balance for preventing autoimmunity
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T cells expanded in presence of IL-15 exhibit increased antioxidant capacity and innate effector molecules
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Plasma-Activated Medium Potentiates the Immunogenicity of Tumor Cell Lysates for Dendritic Cell-Based Cancer Vaccines
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Targeting Mitochondrial Bioenergetics as a Therapeutic Strategy for Chronic Lymphocytic Leukemia
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Cold physical plasma selects for specific T helper cell subsets with distinct cells surface markers in a caspase‐dependent and NF‐κB‐independent manner
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Amino Acid Metabolism Related to Immune Tolerance by MDSCs
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Tumor‐dependent down‐regulation of the ζ‐chain in T‐cells is detectable in early breast cancer and correlates with immune cell function
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Relationship Between Redox Status and Cell Fate in Immunity and Autoimmunity
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Mitochondrial superoxide disrupts the metabolic and epigenetic landscape of CD4+ and CD8+ T-lymphocytes
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Targeting amino acid-metabolizing enzymes for cancer immunotherapy
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Decreased IL-7 Responsiveness Is Related to Oxidative Stress in HIV Disease
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Differential sensitivity of naïve and subsets of memory CD4+ and CD8+ T cells to hydrogen peroxide-induced apoptosis
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Interleukin-2 based immunotherapy in patients with metastatic renal cell carcinoma.
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Chapter 6 Oxidative Stress and Lymphocyte Persistence
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Oxidative DNA damage in reconstituting T cells is associated with relapse and inferior survival after allo-SCT
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Changes in naïve and memory T-cells in elite swimmers during a winter training season
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Distinct pro-inflammatory properties of myeloid cell–derived apolipoprotein E2 and E4 in atherosclerosis promotion
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Treatment with Exogenously Added Catalase Alters CD8 T Cell Memory Differentiation and Function
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Immunosenescence in Aging-Related Vascular Dysfunction
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Response of Cytokines and Hydrogen Peroxide to Sporothrix schenckii Exoantigen in Systemic Experimental Infection
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Integrated miRNA/mRNA Counter-Expression Analysis Highlights Oxidative Stress-Related Genes CCR7 and FOXO1 as Blood Markers of Coronary Arterial Disease
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Protein-Bound Polysaccharide K Partially Prevents Apoptosis of Circulating T Cells Induced by Anti-Cancer Drug S-1 in Patients with Gastric Cancer
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The Induction of a Permissive Environment to Promote T Cell Immune Evasion in Acute Myeloid Leukemia: The Metabolic Perspective
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Comparative Expression Profiling of Distinct T Cell Subsets Undergoing Oxidative Stress
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Perspectives and Advances of Nonthermal Plasma Technology in Cancers
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ADSA Foundation Scholar Award: Shakin' off the rust—Oxidative stress and redox status as underlying factors of immune dysfunction in periparturient cows and preweaning calves
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Increased prevalence of tumor-infiltrating regulatory T cells is closely related to their lower sensitivity to H2O2-induced apoptosis in gastric and esophageal cancer
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Exercise Cuts Both Ways with ROS in Remodifying Innate and Adaptive Responses: Rewiring the Redox Mechanism of the Immune System during Exercise
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Cutting edge: Metabolic immune reprogramming, reactive oxygen species, and cancer
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Chronic Plasmodium chabaudi Infection Generates CD4 Memory T Cells with Increased T Cell Receptor Sensitivity but Poor Secondary Expansion and Increased Apoptosis
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Ameliorative effects ofα-lipoic acid on high-fat diet-induced oxidative stress and glucose uptake impairment of T cells
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Systemic activation of NRF2 contributes to the therapeutic efficacy of clinically-approved KRAS-G12C anti-cancer drugs
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Dihydrolipoamide dehydrogenase-Lpd (Rv0462)-specific T cell recall responses are higher in healthy household contacts of TB: a novel immunodominant antigen from M. tuberculosis
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Role of immune cell interactions in alcohol-associated liver diseases
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Decreased inflammatory profile in oral leukoplakia tissue exposed to cold physical plasma ex vivo
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Role of antioxidants in modulating anti-tumor T cell immune resposne
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Association of Nutritional Indices With Adverse Effects and Time-to-Treatment-Failure in Triple Therapy for Lung Cancer
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T cell recall response of two hypothetical proteins (Rv2251 and Rv2721c) from Mycobacterium tuberculosis in healthy household contacts of TB – Possible subunit vaccine candidates
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Reactive oxygen species-related oxidative changes are associated with splenic lymphocyte depletion in Ebola virus infection
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Immunology in Plasma Cancer Treatment
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Tumor-mediated changes in the immune system of cancer patients - a balancing act between suppressors and effectors
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Characterization of extracellular and surface bound adherence proteins of Staphylococcus aureus
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Conventional T Cell Subsets and Their Roles Within the Tumor Microenvironment
Azimnasab-sorkhabi, P., Soltani-asl, M., Ansa-Addo, E. A., & Kfoury, J. R. (2024) · Interdisciplinary cancer research · doi:10.1007/16833_2024_332

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Authors: Takahashi, A., Hanson, M. G. V., Norell, H. R., Havelka, A. M., Kono, K., Malmberg, K.-J., & Kiessling, R. V. R.
Affiliations: Karolinska Institutet (SE)
Department of Oncology and Pathology, Immune and Gene Therapy Laboratory, Cancer Center Karolinska, Karolinska Institutet , Stockholm ,
University of Yamanashi (JP)
Karolinska University Hospital (SE)
Corresponding author: Takahashi, Akihiro
ORCID: Takahashi, Akihiro
Kono, Koji
Malmberg, Karl-Johan
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2005-05
Volume: 174
Issue: 10
Pages: 6080-6087
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.174.10.6080
OpenAlex: W2139536543
Cited by: 101
References: 62
Citations by year: 2026: 2 · 2025: 4 · 2024: 9 · 2023: 3 · 2022: 4 · 2021: 8 · 2020: 5 · 2019: 3 · 2018: 6 · 2017: 3 · 2016: 7 · 2015: 4 · 2014: 5 · 2013: 9 · 2012: 8
FWCI: 1.38
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: European Commission
Cancerfonden
Karolinska Institutet
National Institutes of Health
National Cancer Institute (R01CA102280, CA 102280)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Keywords: hydrogen peroxide, oxidative stress, T cell death, CD8+ effector memory T cells, central memory T cells, naive T cells, mitochondrial depolarization, caspase-3, z-VAD-fmk, adoptive cell transfer, T cell subsets, cancer immunotherapy
MeSH terms: Amino Acid Chloromethyl Ketones, Cells, Cultured, Cytotoxicity, Immunologic, Dose-Response Relationship, Immunologic, Growth Inhibitors, Humans, Hydrogen Peroxide, Immunologic Memory, Intracellular Membranes, Membrane Potentials, Mitochondria, Permeability, T-Lymphocytes, Cytotoxic, Cell Death, Leukocyte Common Antigens, Oxidative Stress, Receptors, Chemokine, Receptors, CCR7, Caspase Inhibitors

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Preferential Cell Death of CD8+ Effector Memory (CCR7−CD45RA−) T Cells by Hydrogen Peroxide-Induced Oxidative Stress

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