Discovery

Mount Sinai, Memorial Sloan Kettering explore colorectal cancer immune resistance with quadruple checkpoint combo

Researchers at the Icahn School of Medicine at Mount Sinai in New York, with contributions from Memorial Sloan Kettering Cancer Center, report that a four-drug immune checkpoint combination targeting PD-1, LAG-3, CTLA-4, and TREM2 achieved complete tumor clearance in preclinical models of both mismatch repair-deficient and mismatch repair-proficient colorectal cancer, according to a study published May 6, 2026 in Cell Reports Medicine. The findings address one of the most persistent problems in colorectal cancer immunotherapy: the near-complete failure of anti-PD-1 therapy in the majority of patients whose tumors carry intact mismatch repair machinery.

Approved checkpoint inhibitors, including Keytruda (pembrolizumab) and Opdivo (nivolumab), have demonstrated activity in colorectal cancer only within the mismatch repair-deficient subgroup, which accounts for roughly 5% of metastatic cases. The mismatch repair-proficient, microsatellite-stable population — the vast majority of patients — has remained without an effective immunotherapy option. The Mount Sinai study, led by Nina Bhardwaj, set out to define why immune resistance colorectal cancer is so pervasive and whether it could be dismantled through rational combination design.

The team's central finding is that resistance is not a single-pathway problem. Using single-cell RNA sequencing, spatial transcriptomics, TCR clonal diversity profiling, and spectral flow cytometry across multiple murine tumor models and patient-derived tissue, the researchers mapped a convergence of T cell exhaustion, myeloid spatial exclusion, and tumor-intrinsic evasion mechanisms operating simultaneously within the tumor microenvironment.

Mapping the myeloid-T cell axis

A core mechanistic finding concerns TREM2-expressing macrophages. Spatial transcriptomics showed that TREM2-positive macrophages accumulate preferentially in tumor core regions, where they co-localize with exhausted T cells and physically exclude effector lymphocytes from sites of active tumor growth. These macrophages expressed high levels of immunosuppressive mediators including IL-10, TGF-β1, and VEGF-A, and their abundance correlated negatively with T cell infiltration and cytotoxic function across both murine and human datasets.

In the T cell compartment, LAG-3 emerged as the dominant co-inhibitory receptor on tumor-infiltrating CD8-positive T cells in mismatch repair-deficient tumors. Anti-PD-1 therapy alone expanded T cell receptor clonotype diversity and activated CD8-positive cells but triggered compensatory upregulation of LAG-3, TIM-3, and TIGIT, creating redundant suppressive signals that monotherapy could not overcome. Non-responders in reanalyzed human single-cell RNA sequencing datasets from mismatch repair-deficient colorectal cancer patients showed persistent co-expression of TOX, PDCD1, and HAVCR2 — a signature of deep T cell exhaustion — while responders demonstrated expansion of clonally diverse effector populations with upregulated cytotoxic gene signatures.

The spatial data further showed that in animals achieving tumor clearance, the immune architecture reorganized: effector T cells redistributed toward the tumor core while TREM2-positive macrophage density at the tumor-immune interface declined. This architectural shift was absent in non-responders.

The quadruple combination and its results

The study tested more than ten checkpoint blockade combinations per model across CT26, 4T1, B16F10, and MC38 cell lines in both orthotopic and subcutaneous settings, as well as in three-dimensional spheroid cultures. The lead combination — anti-PD-1 plus anti-LAG-3 plus anti-CTLA-4 plus anti-TREM2 — produced complete responses in approximately 100 percent of mismatch repair-deficient CT26 tumors, compared with roughly 40 to 50 percent for anti-PD-1 monotherapy. In mismatch repair-proficient models, where anti-PD-1 alone produced near-zero complete responses, the quadruple combination achieved approximately 73 percent complete response rates.

The combination immunotherapy CRC results were replicated in patient-derived mismatch repair-deficient colorectal cancer spheroids, where the quadruple regimen produced superior tumor killing relative to anti-PD-1 monotherapy, with increased secretion of IFN-γ, TNF-α, and IL-2 confirmed by Luminex cytokine profiling. Depletion of TREM2-positive macrophages in co-culture systems directly enhanced T cell cytotoxicity, providing a mechanistic link between the myeloid targeting component and the observed anti-tumor activity.

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Each element of the combination was assigned a non-redundant biological role. Anti-LAG-3 blocked MHC class II-mediated T cell suppression and enhanced CD4-positive TCF-positive T cell infiltration. Anti-CTLA-4 depleted regulatory T cells and strengthened early T cell priming, which the authors identify as necessary for complete responses in immunologically cold mismatch repair-proficient tumors. Anti-TREM2 reduced the frequency of SPP1-positive immunosuppressive macrophages while preserving and expanding MHC-positive C1Q-positive CXCL9-positive macrophages, a subset associated with antigen presentation and cytotoxic T cell recruitment.

Animals achieving complete tumor clearance were protected against rechallenge, with elevated effector memory CD4-positive and CD8-positive T cells detected in spleens and lymph nodes, indicating the combination established durable immunological memory.

Predicting response and assessing tumor mutational burden

The team applied Random Forest and Gradient Boosting machine learning models to single-cell RNA sequencing data from mismatch repair-deficient colorectal cancer patients, achieving 87.5% accuracy in predicting response to immune checkpoint blockade on an independent validation cohort. The top predictive features were TREM2-positive macrophage frequency as a negative predictor, effector CD8-positive T cell clonal diversity as a positive predictor, and LAG-3 expression on tumor-infiltrating lymphocytes as a negative predictor.

Whole-exome sequencing of MSH2 knockout CT26 lines showed that high tumor mutational burden correlated with greater baseline T cell infiltration and superior checkpoint response. However, the data indicated that tumor mutational burden alone was insufficient to predict response: TREM2-positive macrophage composition provided additive predictive value beyond mutational load. In low tumor mutational burden mismatch repair-proficient tumors, high response rates were achievable only when myeloid targeting via anti-TREM2 was added to T cell-directed checkpoint blockade. Analysis of TCGA colorectal adenocarcinoma and uterine corpus endometrial carcinoma cohorts via CIBERSORT and CRI iAtlas confirmed that high TREM2-positive macrophage infiltration was associated with significantly worse overall survival.

Takeaways

The findings arrive in a field where combination immunotherapy CRC strategies are under active investigation but no approved option exists for the mismatch repair-proficient metastatic population. Agenus is advancing botensilimab, an Fc-enhanced anti-CTLA-4 antibody designed to engage myeloid cells via Fc receptors, combined with balstilimab (anti-PD-1), with early-phase signals of activity in microsatellite-stable colorectal cancer. Innovent Biologics is recruiting patients to a trial of IBI363, a PD-1/IL-2 bispecific fusion protein, with mechanistic profiling of the myeloid and T cell compartments as a primary endpoint. CSF1R inhibitors including cabiralizumab, which deplete tumor-associated macrophages rather than reprogramming them, have produced mixed results in unselected colorectal cancer populations, suggesting that myeloid depletion alone is insufficient and that the composition of the residual myeloid compartment matters.

The Mount Sinai study positions TREM2 macrophage cancer resistance as a correctable node within a broader suppressive network rather than an isolated target, and frames the myeloid compartment as a co-equal partner to T cell checkpoint inhibitors in determining whether anti-tumor immunity can be established. The work remains preclinical, and the authors note that clinical translation of the quadruple combination will require formal toxicity evaluation, particularly given the established adverse event profile of CTLA-4 blockade in humans. No clinical trial testing the exact anti-PD-1, anti-LAG-3, anti-CTLA-4, and anti-TREM2 regimen in colorectal cancer patients has been identified as of publication.


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