bims-spamet Biomed News
on Spatial metabolomics of T cells
Issue of 2026–07–05
nine papers selected by
Peio Azcoaga, Katholieke Universiteit te Leuven



  1. Proc Natl Acad Sci U S A. 2026 Jul 07. 123(27): e2602385123
      Although A2AR is a key immunoregulatory receptor that suppresses CD8+ T cell activation in response to elevated extracellular adenosine in inflamed or hypoxic microenvironments, its role in CD8+ T cell differentiation and cell-fate decisions during chronic viral infection and cancer remains poorly understood. Using A2AR-eGFP reporter mice, we show that A2AR expression is rapidly induced by TCR stimulation and persists under chronic antigen exposure and hypoxia, with sustained expression strongly associated with terminal exhaustion via the canonical Gαs-cAMP-PKA pathway. Paradoxically, A2AR loss does not alleviate exhaustion but instead accelerates differentiation toward the terminally exhausted state. Single-cell multiomics profiling revealed that A2AR deficiency activates CD122 (IL-2Rβ)-dependent signaling, driving T cell exhaustion. Genetic deletion of CD122 in A2AR-deficient CD8+ T cells reduced terminal exhaustion, identifying CD122 signaling as a key mediator of A2AR loss-driven exhaustion. Intriguingly, both sustained A2AR expression and A2AR loss converge to promote T cell exhaustion differentiation through distinct mechanisms. These findings uncover a paradoxical role of A2AR in shaping CD8+ T cell fate choices during chronic infection and cancer.
    Keywords:  A2AR; CD8(+) T cell differentiation; exhaustion; immunotherapy
    DOI:  https://doi.org/10.1073/pnas.2602385123
  2. J Immunother Cancer. 2026 Jun 29. pii: e003100corr1. [Epub ahead of print]14(6):
      
    DOI:  https://doi.org/10.1136/jitc-2021-003100corr1
  3. iScience. 2026 Jul 17. 29(7): 116411
      miR-139 acts as a tumor suppressor in breast cancer cells, yet its role within the tumor immune microenvironment (TIME) remains unclear. This study explores the dual functions of miR-139 in both tumor and immune cells, particularly its effect on CD8+ T cell function and chemokine-mediated immune recruitment. Bioinformatics analysis using TCGA and GEO data identified miR-139 as differentially expressed in breast cancer. Using samples from 32 patients, we detected elevated miR-139 levels in tumor-infiltrating CD8+ T cells compared with adjacent normal tissues. Further experiments confirmed that miR-139 directly targets CD28, leading to its downregulation. Concurrently, increased expression of exhaustion markers PD-1 and TIGIT was observed. Moreover, tumors with high miR-139 expression showed upregulation of T-cell-recruiting chemokines CX3CL1, CXCL12, and CXCL14. These results demonstrate that miR-139 promotes CD8+ T cell exhaustion via suppression of CD28 and facilitates chemokine-mediated T cell recruitment, highlighting its immunosuppressive role in breast cancer.
    Keywords:  Cancer; Cell biology; Immunology
    DOI:  https://doi.org/10.1016/j.isci.2026.116411
  4. Med. 2026 Jul 02. pii: S2666-6340(26)00217-5. [Epub ahead of print] 101214
       BACKGROUND: Head and neck squamous cell carcinoma (HNSCC) exhibits substantial biological heterogeneity that is not fully explained by human papillomavirus (HPV) status. The spatial organization of tumor, immune, and stromal cell populations and its relationship to clinical outcome remain incompletely understood.
    METHODS: We performed single-cell spatial transcriptomic and proteomic profiling of 44 primary HNSCC tumors, generating a spatial atlas of 19,471,501 cells across whole-slide tissue sections. Spatial niches and ecosystem states were identified through integrated computational analyses and evaluated for associations with tumor programs, clinicopathologic features, and patient outcomes.
    FINDINGS: HPV-negative tumors were enriched for fibroblast-rich, immune-poor niches associated with epithelial-mesenchymal transition and hypometabolic tumor programs, whereas HPV-positive tumors displayed more diverse immune, stromal, and vascular niche combinations and were enriched for immunogenic ecosystem states. Approximately 20% of HPV-positive tumors exhibited fibroblast-rich ecosystem architectures resembling HPV-negative disease and were associated with less favorable outcomes than other HPV-positive tumors of similar stage. In patient-derived co-culture models, extracellular matrix-associated fibroblasts were associated with epithelial-mesenchymal transition (EMT)-like tumor states, CD8+ T cell dysfunction, and chemotherapy resistance-associated phenotypes.
    CONCLUSIONS: Spatial ecosystem architecture is associated with clinically relevant heterogeneity beyond conventional HPV-based classification. Fibroblast-rich, immune-poor ecosystem states characterize a high-risk subset of HPV-positive tumors and may provide a framework for improved biological classification and risk stratification in HNSCC.
    FUNDING: This work was supported by the National Institutes of Health (R01CA291607 and R21CA267527-01) and the Feldstein Medical Foundation.
    Keywords:  Translation to patients; head and neck squamous cell carcinoma; human papillomavirus; microenvironmental niches; spatial proteomics; spatial transcriptomics; tumor ecosystem; tumor microenvironment
    DOI:  https://doi.org/10.1016/j.medj.2026.101214
  5. Front Immunol. 2026 ;17 1874242
       Introduction: Osteoporosis weakens the skeleton by lowering bone mass and damaging bone microarchitecture. A growing body of evidence points to disruptions in osteoimmune homeostasis as a key driver of this disease. In particular, apoptosis of bone cells and immune cells appears to be a critical contributing mechanism. Within the bone marrow, CD8+ T cells display a surprising functional duality: whether they protect bone or promote its loss depends heavily on local signals. Under healthy conditions or after mechanical loading, activated CD8+ T cells help maintain bone mass. They do so mainly by secreting interferon‑γ (IFN‑γ), which blocks osteoclast formation through interference with NF‑κB and MAPK signaling. However, this protective role is not fixed. Pathological cues such as estrogen deficiency can flip CD8+ T cells into a bone‑destroying phenotype. For example, when estrogen drops, muscle‑derived IL‑33 decreases. That drop prompts bone marrow CD8+ T cells to release large amounts of CCL5. CCL5 then binds to CCR3 on osteoclast precursors and activates the ERK pathway, thereby accelerating bone loss in postmenopausal osteoporosis. Aging and chronic inflammation add another layer of complexity. They drive the accumulation of senescent CD28- CD8+ T cells. These aged cells no longer produce enough IFN‑γ to protect bone; instead, they adopt a senescence‑associated secretory phenotype (SASP) that suppresses osteoblast differentiation and reduces mesenchymal stromal cell viability. Moreover, apoptosis of osteoblasts and osteocytes-triggered by TNF‑α, IFN‑γ, or glucocorticoids-worsens bone loss. New findings suggest that CD8+ T cells may fuel this apoptotic process through Fas/FasL interactions and the granzyme/perforin pathway. This review brings together these context‑dependent mechanisms. We place special emphasis on how hormonal shifts, metabolic changes, and inflammatory mediators converge to decide whether CD8+ T cells support skeletal integrity or drive bone resorption.
    Methods: We performed a narrative review of recent studies on CD8+ T cells in osteoporosis. We searched PubMed and Web of Science using keywords such as "osteoporosis", "osteoimmunology", "CD8+ T cells", "IFN‑γ", "CCL5", "cellular senescence", "SASP", "Fas/FasL", and "granzyme". From the retrieved articles, we selected original research (including in vitro co‑culture systems, animal models, and clinical samples) and relevant reviews. We then extracted and integrated key mechanistic evidence regarding the dual functionality of CD8+ T cells and its regulatory pathways.
    Results: CD8+ T cells have two opposing functions. Under healthy conditions or mechanical loading, activated CD8+ T cells secrete IFN‑γ, which inhibits osteoclast formation by interfering with NF‑κB and MAPK signaling, thus maintaining bone mass. In contrast, when estrogen is deficient, reduced muscle‑derived IL‑33 causes bone marrow CD8+ T cells to release large amounts of CCL5. CCL5 binds to CCR3 on osteoclast precursors and activates the ERK pathway, accelerating bone loss. Aging and chronic inflammation shift the balance. Aging and chronic inflammation lead to the accumulation of senescent CD28- CD8+ T cells. These cells no longer produce sufficient protective IFN‑γ. Instead, they exhibit a senescence‑associated secretory phenotype (SASP) that suppresses osteoblast differentiation and reduces mesenchymal stromal cell viability. CD8+ T cells may promote bone cell apoptosis through multiple pathways. TNF‑α, IFN‑γ, or glucocorticoids can trigger apoptosis of osteoblasts and osteocytes. Newer evidence suggests that CD8+ T cells amplify this process via Fas/FasL interactions and the granzyme/perforin pathway. Two newly identified CD8+ T cell‑derived molecules deserve attention. Granzyme K protects against bone loss, whereas CCL5 promotes bone loss. These two molecules offer fresh opportunities for biomarkers and therapies.
    Discussion: Our synthesis shows that CD8+ T cells act as a double‑edged sword in osteoporosis: their functional switch depends on the integration of hormonal, metabolic, and inflammatory signals. Under normal conditions or after mechanical loading, the anti‑osteoclastogenic effect of IFN‑γ dominates. But when estrogen levels fall, the IL‑33/CCL5/CCR3/ERK axis becomes activated, turning CD8+ T cells toward a bone‑resorbing phenotype. During aging, the buildup of CD28⁻ CD8+ T cells and their SASP further weakens bone formation and worsens bone cell death through apoptotic pathways. These observations point to a more precise therapeutic strategy. Instead of broadly modulating T cells, one could specifically target pathogenic pathways-for example, by interfering with the IL 33/ST2/CCL5 cascade or by clearing immune senescent CD28⁻ subsets. Such approaches might help restore osteoimmune balance. Two recently discovered CD8+ T cell derived molecules, granzyme K and CCL5, are particularly interesting because they respectively protect against and promote bone loss. They could serve as novel biomarkers or even therapeutic targets. Future studies should examine the cell type specific regulation of these pathways in vivo and test the safety and efficacy of targeted interventions.
    Keywords:  CD8+ T cells; cellular senescence; immunotherapy; interferon-γ; osteoimmunology; osteoporosis
    DOI:  https://doi.org/10.3389/fimmu.2026.1874242
  6. Acta Pharm Sin B. 2026 Jun;16(6): 3892-3906
      The immunosuppressive tumor microenvironment (TME) profoundly limits the therapeutic efficacy of CD8+ T cells in solid tumors. While cytokine therapies have shown promise in reactivating CD8+ T cells, they fail to address the common suppressive environmental attributes (e.g., acidosis and Mg2+ deficiency) of solid tumors. Here, we report an innovative CD8+ T cell dual-functional modulator, interleukin-12-tethered nano-aluminum adjuvant (IL12@NAM), which counteracts the acidic TME to relieve acidosis and concurrently releases Mg2+ and IL12. Locally released Mg2+ and IL12 synergize in T cell infiltration and activation by promoting the phosphorylation of focal adhesion kinase and extracellular signal-regulated kinase 1/2, and enhance CD8+ T cell activation and functions via the Ca2+-nuclear factor of activated T cells 2 pathway. Furthermore, dual-functional IL12@NAM mitigates CD8+ T cell exhaustion by reducing PD1 and LAG3 expression and effectively increases the differentiation towards T helper 1 cells while decreasing regulatory T cells, creating a more favorable immune network for enhanced CD8+ T cell-mediated anti-tumor immunity. As a result, IL12@NAM has demonstrated potent therapeutic efficacy against advanced melanoma and breast cancer, and remarkably empowered adoptive T therapy of solid tumors. This study provides a paradigm for empowering cytotoxic T cells by reactivating and creating a sustainable immunoresponsive environment, offering a potential adjuvant strategy to enhance solid tumor therapy.
    Keywords:  Acidosis alleviation; Cytotoxic T cell activation; Cytotoxic T cell immune exhaustion; Cytotoxic T cell infiltration; Interleukin-12 tumor therapy; Mg2+ supplementation; Nano-aluminum adjuvants; Tumor microenvironment
    DOI:  https://doi.org/10.1016/j.apsb.2025.10.021
  7. Front Immunol. 2026 ;17 1839684
       Introduction: The efficacy of oncolytic adenoviruses in colorectal cancer models is constrained by a treatment-induced limitation: the high-dose, repetitive administration required for sustained oncolysis promotes chronic antigen exposure and tumor microenvironmental stress, driving CD8+ T cells into a state of exhaustion.
    Methods: To mitigate this, we constructed an oncolytic adenovirus, ADV-PTD4-D3, engineered for intratumoral expression of a peptide inhibitor of CDK4/6. This local strategy aims to retain immunomodulatory potential while minimizing systemic exposure. In syngeneic murine models, ADV-PTD4-D3 demonstrated improved tumor control and the ability to induce robust, antigen-specific immunological memory, with its therapeutic effect being primarily dependent on CD8+ T cells. Notably, it also exhibited potent antitumor activity in a humanized xenograft model and showed no evidence of significant off-target toxicity in immunocompetent hosts.
    Results: The mechanism involves a signaling axis where viral-mediated CDK4/6 inhibition reduces retinoblastoma (Rb) protein phosphorylation. This decrease relieves Rb-mediated sequestration of the NF-kB p65 subunit, allowing p65 nuclear translocation and transcriptional upregulation of the T-cell chemoattractant CCL5, a factor linked to favorable patient prognosis. Thus, ADV-PTD4-D3 promotes a T-cell-inflamed microenvironment by providing a sustained chemotactic signal CCL5 for CD8+ T cell recruitment. Furthermore, this treatment strategy successfully reverses the functional exhaustion of infiltrating CD8+ T cells, thereby addressing two major barriers to effective therapy: inadequate infiltration and functional exhaustion. By modifying the tumor microenvironment in this way, the armed virus addresses two factors that limit T-cell-based immunotherapies: inadequate infiltration and functional exhaustion. Correspondingly, ADV-PTD4-D3 treatment improved the antitumor response to both PD-1 blockade and CAR-T cell therapy in combination studies.
    Discussion: These findings suggest that engineering oncolytic viruses to locally modulate pathways involved in T cell exhaustion represents a viable and translatable strategy for enhancing antitumor immunity.
    Keywords:  CD8; T cell; colorectal cancer; immunity; tumor
    DOI:  https://doi.org/10.3389/fimmu.2026.1839684
  8. Med Oncol. 2026 Jul 01. pii: 208. [Epub ahead of print]43(8):
      The tumor microenvironment (TME) limits durable antitumor immunity by impairing CD8+ T cell responses. Memory like CD8+ T cells are important for long-term immune control but are often restricted in the TME. Dendritic cells (DCs) are key regulators of T cell fate. Previous studies have shown that SHP1 in DCs fosters an immunosuppressive microenvironment and facilitates tumor immune escape. T cell factor-1 (TCF-1), encoded by Tcf7 gene, is required for central memory CD8+ T cell (TCM) formation and is closely linked to canonical Wnt/β-catenin signaling. However, whether SHP1 in DCs regulates TCF-1 expression and TCM formation remains unclear. To investigate the role of DC intrinsic SHP1 in T cell immunity, SHP1 deficient DC2.4 cells and primary bone marrow derived dendritic cells (BMDCs) were co-cultured with OT-1 T cells to assess proliferation, TCM formation, cytotoxic activity, and TCF-1 expression. A DC-specific SHP1 knockout mice model was used to evaluate antitumor immunity in vivo, and Tcf7 or Ctnnb1 silencing was used to probe the TCF-1/Wnt/β-catenin axis. SHP1 downregulation in DCs markedly enhanced CD8+ T cell proliferation, promoted the generation of CD62L+ CD44+ central memory T cells, and potentiated B16-F10-OVA tumor cell killing, accompanied by increased TCF-1 expression in OT-1 T cells. In DC-specific SHP1 knockout mice, EO771 tumor growth was suppressed with concurrent increases in intratumoral IFN-γ+ and TCF-1+ CD8+ T cell frequencies. Mechanistically, we found that DC SHP1 regulates TCM formation via TCF-1, as silencing Tcf7 in OT-1 T cells abrogated this effect. SHP1-deficient DCs activated Wnt/β-catenin signaling in CD8+ T cells, as shown by increased active β-catenin, total β-catenin, c-Myc and Cyclin D1, and a reduced phospho β-catenin/total β-catenin ratio. Critically, Ctnnb1 silencing in T cells abrogated the enhanced proliferation, TCM formation, and cytotoxic activity induced by SHP1-deficient DCs. DC-intrinsic SHP1 restrains central memory CD8+ T cell formation via the TCF-1/Wnt/β-catenin axis.
    Keywords:  Dendritic cells; SHP-1; TCF-1; TCM; Wnt/β-catenin
    DOI:  https://doi.org/10.1007/s12032-026-03329-z
  9. Gut. 2026 Jul 02. pii: gutjnl-2026-338277. [Epub ahead of print]
       BACKGROUND: The application of the novel KRASG12D inhibitor in pancreatic ductal adenocarcinoma (PDAC) is currently hindered by adaptive resistance. Metabolic reprogramming is a hallmark of KRASG12D signalling, yet the mechanisms linking these alterations to immunosuppression and low therapeutic response are poorly defined.
    OBJECTIVE: To identify the key regulatory nodes connecting KRASG12D-driven metabolic adaptations to tumour microenvironment and develop a mechanistic-based combinatorial strategy.
    DESIGN: We integrated whole-exome sequencing, untargeted metabolomics and single-cell RNA sequencing of human PDAC specimens to analyse the metabolic-immune landscape. We evaluated therapeutic efficacy using the autochthonous mouse and patient-derived xenograft models.
    RESULTS: We found that KRASG12D enhanced cholesterol metabolism and promoted CD8+ T cell exhaustion, whereas KRASG12D inhibition or cholesterol synthesis blockade induced compensatory ULK1-associated autophagy. Cotargeting cholesterol metabolism and autophagy potentiated the antitumour efficacy of the KRASG12D inhibitor MRTX1133 and alleviated CD8+ T cell exhaustion. Mechanistically, KRASG12D transcriptionally upregulated USP20 via EGR1, which simultaneously deubiquitinated and stabilised 3-hydroxy-3-methylglutaryl-CoA reductase and ULK1, thereby orchestrating cholesterol metabolism and autophagy-associated survival. Genetic depletion or pharmacological inhibition of USP20 with GSK2643943A suppressed these pathways and restored CD8+ T cell function, improving responses to MRTX1133 and anti-programmed cell death protein-1 (anti-PD-1). In preclinical PDAC models, triple therapy with GSK2643943A, MRTX1133 and anti-PD-1 elicited a robust therapeutic response and induced significant tumour regression.
    CONCLUSION: USP20 acts as a critical metabolic checkpoint that orchestrates CD8+ T cell exhaustion and therapeutic response. Targeting the USP20-cholesterol-autophagy axis represents a promising strategy to reverse immune suppression and unlock the full potential of KRASG12D inhibitors in PDAC.
    Keywords:  IMMUNE RESPONSE; MOLECULAR TARGETED THERAPY; PANCREATIC CANCER
    DOI:  https://doi.org/10.1136/gutjnl-2026-338277