T cell regeneration after immunological injury

Velardi, Enrico; Tsai, Jennifer J.; van den Brink, Marcel R. M.

doi:10.1038/s41577-020-00457-z

Cited by 222T-cell and B-cell ImmunologyHematopoietic Stem Cell TransplantationImmunotherapy and Immune Responses

T cell regeneration after immunological injury

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Velardi, Enrico, Tsai, Jennifer J., van den Brink, Marcel R. M.·2021·Nature Reviews Immunology

DOI 10.1038/s41577-020-00457-zPMC PMC7583557

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Abstract

Following periods of haematopoietic cell stress, such as after chemotherapy, radiotherapy, infection and transplantation, patient outcomes are linked to the degree of immune reconstitution, specifically of T cells. Delayed or defective recovery of the T cell pool has significant clinical consequences, including prolonged immunosuppression, poor vaccine responses and increased risks of infections and malignancies. Thus, strategies that restore thymic function and enhance T cell reconstitution can provide considerable benefit to individuals whose immune system has been decimated in various settings. In this Review, we focus on the causes and consequences of impaired adaptive immunity and discuss therapeutic strategies that can recover immune function, with a particular emphasis on approaches that can promote a diverse repertoire of T cells through de novo T cell formation.

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Mass Cytometry and Topological Data Analysis Reveal Immune Parameters Associated with Complications after Allogeneic Stem Cell Transplantation
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Humoral Immune Reconstitution Kinetics after Allogeneic Hematopoietic Stem Cell Transplantation in Children: A Maturation Block of IgM Memory B Cells May Lead to Impaired Antibody Immune Reconstitution
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Insulin-like growth factor-I enhances lymphoid and myeloid reconstitution after allogeneic bone marrow transplantation12
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IL-12 Facilitates Both the Recovery of Endogenous Hematopoiesis and the Engraftment of Stem Cells after Ionizing Radiation
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Early recovery of T-cell function predicts improved survival after T-cell depleted allogeneic transplant
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Administration of RANKL boosts thymic regeneration upon bone marrow transplantation
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Sex Steroid Ablation Enhances Immune Reconstitution Following Cytotoxic Antineoplastic Therapy in Young Mice
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Sex Steroid Ablation Enhances Hematopoietic Recovery following Cytotoxic Antineoplastic Therapy in Aged Mice
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Low dose aerosol infection of mice with virulent type A Francisella tularensis induces severe thymus atrophy and CD4+CD8+ thymocyte depletion
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Immune memory and aging: an infinite or finite resource?
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Hallmarks of T cell aging
Mittelbrunn, M., & Kroemer, G. (2021) · Nature Immunology · doi:10.1038/s41590-021-00927-z · Cited by 702 · see citing works
Immunosenescence: signaling pathways, diseases and therapeutic targets
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Dysregulation of Systemic Immunity in Aging and Dementia
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Age-related epithelial defects limit thymic function and regeneration
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Tissue-specific immunity for a changing world
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Glioblastoma vaccines: past, present, and opportunities
Xiong, Z., Raphael, I., Olin, M. R., Okada, H., Li, X., & Kohanbash, G. (2024) · EBioMedicine · doi:10.1016/j.ebiom.2023.104963 · Cited by 90 · see citing works
Tcf1–CTCF cooperativity shapes genomic architecture to promote CD8+ T cell homeostasis
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Impact of SARS-CoV-2 in Hematopoietic Stem Cell Transplantation and Chimeric Antigen Receptor T Cell Therapy Recipients
Mushtaq, M. U., Shahzad, M., Chaudhary, S. G., Luder, M., Ahmed, N., Abdelhakim, H., Bansal, R., Balusu, R., DeJarnette, S., Divine, C. L., et al. (2021) · Transplantation and Cellular Therapy · doi:10.1016/j.jtct.2021.07.005 · Cited by 57 · see citing works
Antigen presentation for central tolerance induction
Klein, L., & Petrozziello, E. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-01076-8 · Cited by 56 · see citing works
Immune landscape after allo-HSCT: TIGIT- and CD161-expressing CD4 T cells are associated with subsequent leukemia relapse
Gournay, V., Vallet, N., Peux, V., Vera, K., Bordenave, J., Lambert, M., Corneau, A., Michonneau, D., de Latour, R. P., Caillat‐Zucman, S., et al. (2022) · Blood · doi:10.1182/blood.2022015522 · Cited by 55 · see citing works
Immune Reconstitution After Allogeneic Haematopoietic Cell Transplantation: From Observational Studies to Targeted Interventions
Yanir, A. D., Schulz, A., Lawitschka, Á., Nierkens, S., & Eyrich, M. K. (2022) · Frontiers in Pediatrics · doi:10.3389/fped.2021.786017 · Cited by 53 · see citing works
Impact of COVID‐19 in hematopoietic stem cell transplant recipients: A systematic review and meta‐analysis
Shahzad, M., Chaudhary, S. G., Zafar, M. U., Hassan, M. A., Hussain, A., Ali, F., Anwar, I., Ahmed, M., Ahmed, N., Khurana, S., et al. (2022) · Transplant Infectious Disease · doi:10.1111/tid.13792 · Cited by 44 · see citing works
Immunosenescence and Aging: Neuroinflammation Is a Prominent Feature of Alzheimer’s Disease and Is a Likely Contributor to Neurodegenerative Disease Pathogenesis
Bowirrat, A. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12111817 · Cited by 45 · see citing works
Effects of Chemotherapy Agents on Circulating Leukocyte Populations: Potential Implications for the Success of CAR-T Cell Therapies
Truong, N. T., Gargett, T., Brown, M. P., & Ebert, L. M. (2021) · Cancers · doi:10.3390/cancers13092225 · Cited by 45 · see citing works
60 Years Young: The Evolving Role of Allogeneic Hematopoietic Stem Cell Transplantation in Cancer Immunotherapy
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The Safety of Bridging Radiation with Anti-BCMA CAR T-Cell Therapy for Multiple Myeloma
Manjunath, S. H., Cohen, A. D., Lacey, S. F., Suhoski, M. M., Garfall, A. L., Melenhorst, J. J., Maxwell, R., Arscott, W. T., Maity, A. M., Jones, J., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-21-0308 · Cited by 42 · see citing works
SARS-CoV-2 infection of thymus induces loss of function that correlates with disease severity
Rosichini, M., Bordoni, V., Silvestris, D. A., Mariotti, D., Matusali, G., Cardinale, A., Zambruno, G., Condorelli, A. G., Flamini, S., Genah, S., et al. (2023) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2023.01.022 · Cited by 39 · see citing works
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Hematopoietic Stem Cells and Their Niche in Bone Marrow
Kwon, M., Kim, B. S., Yoon, S., Oh, S., & Lee, D. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25136837 · Cited by 40 · see citing works
Recent Advancements in Regenerative Approaches for Thymus Rejuvenation
Sharma, H., & Moroni, L. (2021) · Advanced Science · doi:10.1002/advs.202100543 · Cited by 39 · see citing works
Graft-versus-host disease: a disorder of tissue regeneration and repair
Chakraverty, R. K., & Teshima, T. (2021) · Blood · doi:10.1182/blood.2021011867 · Cited by 38 · see citing works
Endogenous thymic regeneration: restoring T cell production following injury
Granadier, D., Acenas, D. D., II, & Dudakov, J. A. (2025) · Nature reviews. Immunology · doi:10.1038/s41577-024-01119-0 · Cited by 40 · see citing works
Oleic acid availability impacts thymocyte preprogramming and subsequent peripheral Treg cell differentiation
Lin, L., Hu, M., Li, Q., Du, L., Lin, L., Xue, Y., Zheng, F., Wang, F., Liu, K., Wang, Y., et al. (2023) · Nature Immunology · doi:10.1038/s41590-023-01672-1 · Cited by 36 · see citing works
Immunosenescence as a convergence pathway in neurodegeneration
Mohapatra, L., Mishra, D. K., Tripathi, A. S., & Parida, S. K. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110521 · Cited by 36 · see citing works
Proton and Carbon Ion Radiation Therapy Decreased Severe Lymphopenia by Reducing Thoracic Vertebra and Aortic Doses in Non-Small Cell Lung Cancer Versus Intensity Modulated Radiation Therapy
Li, Y., Fan, X., Yu, Q., Zhai, H., Mo, M., Sun, J., Mi, J., Lu, R., Mao, J., Chen, J., et al. (2022) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2022.12.030 · Cited by 34 · see citing works
Thymic Function and T-Cell Receptor Repertoire Diversity: Implications for Patient Response to Checkpoint Blockade Immunotherapy
Cardinale, A., Luca, C. D. D., Locatelli, F., & Velardi, E. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.752042 · Cited by 36 · see citing works
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Activation of the zinc-sensing receptor GPR39 promotes T-cell reconstitution after hematopoietic cell transplant in mice
Iovino, L., Cooper, K., DeRoos, P. C., Kinsella, S. M., Evandy, C., Ugrai, T. M., Mazziotta, F., Ensbey, K. S., Granadier, D. W., Hopwo, K. S., et al. (2022) · Blood · doi:10.1182/blood.2021013950 · Cited by 34 · see citing works
Radio-induced lymphopenia in the era of anti-cancer immunotherapy
de Kermenguy, F., Meziani, L., Mondini, M., Clémenson, C., Morel, D., Deutsch, É., & Robert, C. (2023) · International review of cytology · doi:10.1016/bs.ircmb.2023.03.002 · Cited by 34 · see citing works
Targeting Chronic Myeloid Leukemia Stem/Progenitor Cells Using Venetoclax-Loaded Immunoliposome
Houshmand, M., Garello, F., Stefanìa, R., Gaidano, V., Cignetti, A., Spinelli, M., Fava, C., Zarif, M. N., Galimberti, S., Pungolino, E. M., et al. (2021) · Cancers · doi:10.3390/cancers13061311 · Cited by 33 · see citing works
T cell aging and Alzheimer’s disease
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Primary and secondary defects of the thymus
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TRIB2 safeguards naive T cell homeostasis during aging
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Cyclosporine A-resistant CAR-T cells mediate antitumour immunity in the presence of allogeneic cells
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Recirculating regulatory T cells mediate thymic regeneration through amphiregulin following damage
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Blasts in context: the impact of the immune environment on acute myeloid leukemia prognosis and treatment
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Ablation of FAS confers allogeneic CD3– CAR T cells with resistance to rejection by T cells and natural killer cells
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CD4+ T-Cell Senescence in Neurodegenerative Disease: Pathogenesis and Potential Therapeutic Targets
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The Use and Duration of Preintubation Respiratory Support Is Associated With Increased Mortality in Immunocompromised Children With Acute Respiratory Failure*
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Naive T Cells in Graft Versus Host Disease and Graft Versus Leukemia: Innocent or Guilty?
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Obesity-induced thymic involution and cancer risk
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RANKL treatment restores thymic function and improves T cell–mediated immune responses in aged mice
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Immune Reconstitution in the Aging Host: Opportunities for Mechanism-Based Therapy in Allogeneic Hematopoietic Cell Transplantation
Lin, R. J., Elias, H. K., & van den Brink, M. R. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.674093 · Cited by 22 · see citing works
Triple-negative breast cancer modifies the systemic immune landscape and alters neutrophil functionality
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Disruption of thymic central tolerance by infection with murine roseolovirus induces autoimmune gastritis
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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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Kidney Disease as a Driver of Immunosenescence
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HLA haploidentical HSCT: from immune imbalance to a platform for immune homeostasis restoration
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Attenuation of apoptotic cell detection triggers thymic regeneration after damage
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Association Between Lymphopenia and Survival Outcomes in Esophageal Carcinoma Patients Receiving Combined Immunotherapy and Chemoradiotherapy
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An Unconventional View of T Cell Reconstitution After Allogeneic Hematopoietic Cell Transplantation
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Multifunctional hydrogel encapsulated with baicalin for full-layer regeneration of drug-resistant bacteria-infected wounds after radiotherapy
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Understanding the impact of radiation-induced lymphopenia: Preclinical and clinical research perspectives
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Compassionate use of recombinant human IL‐7‐hyFc as a salvage treatment for restoring lymphopenia in patients with recurrent glioblastoma
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Nuclear fragile X mental retardation-interacting protein 1-mediated ribophagy protects T lymphocytes against apoptosis in sepsis
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NK- and T-cell repertoire is established early after allogeneic HSCT and is imprinted by CMV reactivation
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Diagnosis and treatment for the early stage of cytomegalovirus infection during hematopoietic stem cell transplantation
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The potential role of the thymus in immunotherapies for acute myeloid leukemia
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Age-related thymic involution: Mechanistic insights and rejuvenating approaches to restore immune function
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MAIT cells numbers and frequencies in patients with acute myeloid leukemia at diagnosis: association with cytogenetic profile and gene mutations
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Protein O-GlcNAcylation in multiple immune cells and its therapeutic potential
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N-acetyltransferase 10 is implicated in the pathogenesis of cycling T cell-mediated autoimmune and inflammatory disorders in mice
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Thymus Reconstitution in Young and Aged Mice Is Facilitated by In Vitro-Generated Progenitor T Cells
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Single-cell clonal tracking of persistent T-cells in allogeneic hematopoietic stem cell transplantation
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Distinct Immune Homeostasis Remodeling Patterns after HLA‐Matched and Haploidentical Transplantation
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Dynamics of Immune Reconstitution and Impact on Outcomes across CAR-T Cell Products in Large B-cell Lymphoma
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Damage-induced IL-18 stimulates thymic NK cells limiting endogenous tissue regeneration
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How Effective are Nanotechnology-Based Therapeutics to Treat Autoimmune Diseases
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European flow cytometry quality assurance guidelines for the diagnosis of primary immune deficiencies and assessment of immune reconstitution following B cell depletion therapies and transplantation
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Mechanisms and strategies of immunosenescence effects on non-small cell lung cancer (NSCLC) treatment: A comprehensive analysis and future directions
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Somatic TP53 mutations are preleukemic events in acute lymphoblastic leukemia
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Sustained lymphocyte decreases after treatment for early breast cancer
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Respiratory Viral Infections in Recipients of Cellular Therapies: A Review of Incidence, Outcomes, Treatment, and Prevention
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GSH-activatable camptothecin prodrug-loaded gold nanostars coated with hyaluronic acid for targeted breast cancer therapy via multiple radiosensitization strategies
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Pelvic bone marrow dose-volume predictors of late lymphopenia following pelvic lymph node radiation therapy for prostate cancer
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Systemic immunostimulation induces glucocorticoid-mediated thymic involution succeeded by rebound hyperplasia which is impaired in aged recipients
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Drug and Chemical Allergy: A Role for a Specific Naive T-Cell Repertoire?
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SARS‐CoV‐2‐specific T cells are generated in less than half of allogeneic HSCT recipients failing to seroconvert after COVID‐19 vaccination
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A road map for uniform, comprehensive long-term follow-up after curative therapy for sickle cell disease
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The contribution of the intestinal microbiome to immune recovery after HCT
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Circulating biomarkers in perioperative management of cancer patients
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Graft-versus-host disease prophylaxis shapes T cell biology and immune reconstitution after hematopoietic cell transplantPreprint
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Premature thymic functional senescence is a hallmark of childhood acute lymphoblastic leukemia survivorship
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Preclinical development of an mRNA-based multiepitope immunotherapeutic for glioblastoma
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“Since cytore-ductive therapy significantly impairs the immune system [37], the potential to induce strong CD8 + T-cell responses is particularly relevant for an antigen-based immunotherapeutic for GBM, where chemotherapy and radiotherapy remain the standard of care, and induced T cells must cross…”
Burning Down the House: Thymic Repair and Regeneration After Acute Damage
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The CXCR4-CXCL12 axis promotes T cell reconstitution via efficient hematopoietic immigration
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Real clinical outcomes of nivolumab plus ipilimumab for renal cell carcinoma in patients over 75 years old
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Targeting the adaptive immune continuum in atherosclerosis and post-MI injury
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Reparative immunological consequences of stem cell transplantation as a cellular therapy for refractory Crohn’s disease
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Advanced Medical Countermeasures and Devices for Use During a Radiological or Nuclear Emergency
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Structure-Activity relationship of 1-(Furan-2ylmethyl)Pyrrolidine-Based Stimulation-2 (ST2) inhibitors for treating graft versus host disease
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Dynamic surveillance of lymphocyte subsets in patients with non-small cell lung cancer during chemotherapy or combination immunotherapy for early prediction of efficacy
Zhen, S., Wang, W., Qin, G., Lu, T., Li, Y., & Zhang, Y. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1316778 · Cited by 8 · see citing works
Comparative analysis of reduced toxicity conditioning regimens between fludarabine plus melphalan and fludarabine plus busulfex in adult patients with acute lymphoblastic leukemia
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Deciphering bone marrow engraftment after allogeneic stem cell transplantation in humans using single-cell analyses
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Immunity and Genetics at the Revolving Doors of Diagnostics in Primary Immunodeficiencies
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Signaling Crosstalks Drive Generation and Regeneration of the Thymus
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A spatial atlas of human gastrointestinal acute GVHD reveals epithelial and immune dynamics underlying disease pathophysiology
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Curcumin enhances GSDME-mediated pyroptosis to potentiate PD-1/PD-L1 immune checkpoint blockade in colorectal cancer
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Fish Collagen Peptides Enhance Thymopoietic Gene Expression, Cell Proliferation, Thymocyte Adherence, and Cytoprotection in Thymic Epithelial Cells via Activation of the Nuclear Factor-κB Pathway, Leading to Thymus Regeneration after Cyclophosphamide-Induced Injury
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Revealing the effect of X-ray or proton brain irradiation on systemic inflammation and leukocyte subpopulation interplay in rodents
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Human pegivirus-1 replication influences NK cell reconstitution after allogeneic haematopoietic stem cell transplantation
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Strategies to enhance T-cell reconstitution in immunocompromised patients
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When the Damage Is Done: Injury and Repair in Thymus Function
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Lucarelli, B., Merli, P., Bertaina, V., & Locatelli, F. (2015) · Expert Review of Clinical Immunology · doi:10.1586/1744666x.2016.1123091 · Cited by 23 · see citing works

Authors: Velardi, E., Tsai, J. J., & van den Brink, M. R. M.
Affiliations: Bambino Gesù Children's Hospital (IT)
State University of New York (US)
Corresponding author: Velardi, Enrico
ORCID: Velardi, Enrico
Tsai, Jennifer J.
van den Brink, Marcel R. M.
Venue: Nature Reviews Immunology
Publisher: Springer Science and Business Media LLC
Published: 2020-10-23
Volume: 21
Issue: 5
Pages: 277-291
ISSN: 1474-1733 (ISSN-L)
1474-1741
DOI: 10.1038/s41577-020-00457-z
PMC: PMC7583557
OpenAlex: W3094124272
Cited by: 222
References: 282
Citations by year: 2026: 41 · 2025: 46 · 2024: 44 · 2023: 38 · 2022: 29 · 2021: 24
FWCI: 2.22
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature reviews. Immunology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Memorial Sloan-Kettering Cancer Center (P01-CA023766, CA008748, P30 CA008748)
Society of Memorial Sloan Kettering (P30-CA008748)
Parker Institute for Cancer Immunotherapy
Seres Therapeutics
Ministero della Salute
Associazione Italiana per la Ricerca sul Cancro
National Institutes of Health (1r01hl147584-01a1, 7r01ca228308-07)
National Institute on Aging (P01AG052359)
National Heart, Lung, and Blood Institute (HL123340, R01‐HL147584, R01HL123340, CA008748, R01HL125571)
National Cancer Institute (P01CA023766, R01‐CA228308, CA008748, R01CA228358, P30CA008748)
National Institute of Allergy and Infectious Diseases (AI124275, U01AI124275)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: T cell reconstitution, immune reconstitution, thymic function, T cell depletion, chemotherapy, radiotherapy, transplantation, infection, adaptive immunity, T cell diversity, immunosuppression, vaccine response
MeSH terms: Immunosenescence, Animals, B-Lymphocytes, Graft vs Host Disease, Humans, Immunotherapy, Lymphopenia, Regeneration, Stress, Physiological, T-Lymphocytes, Hematopoietic Stem Cell Transplantation, Models, Immunological, Adaptive Immunity, Cellular Microenvironment

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