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Therapeutic reprogramming of tumour-associated macrophages in pancreatic cancer using a cytotoxic CCR2-targeted nanotheranostic.

Molecular cancer 2026 Vol.25(1)

Somani VK, Zhang X, Chen TH, Bulle A, Bansod S, Li L, Geng Y, Kang LI, Heo GS, Luehmann H, Zhang Y, Saeed MA, Lavine KJ, DeNardo DG, Pachynski RK, Liu Y, Lim KH

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[BACKGROUND] Pancreatic ductal adenocarcinoma (PDAC) exhibits a profoundly immunosuppressive tumour microenvironment (TME) dominated by inflammatory monocytes (IMs) and tumour-associated macrophages (

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APA Somani VK, Zhang X, et al. (2026). Therapeutic reprogramming of tumour-associated macrophages in pancreatic cancer using a cytotoxic CCR2-targeted nanotheranostic.. Molecular cancer, 25(1). https://doi.org/10.1186/s12943-026-02597-7
MLA Somani VK, et al.. "Therapeutic reprogramming of tumour-associated macrophages in pancreatic cancer using a cytotoxic CCR2-targeted nanotheranostic.." Molecular cancer, vol. 25, no. 1, 2026.
PMID 41654815

Abstract

[BACKGROUND] Pancreatic ductal adenocarcinoma (PDAC) exhibits a profoundly immunosuppressive tumour microenvironment (TME) dominated by inflammatory monocytes (IMs) and tumour-associated macrophages (TAMs), which restrict adaptive immunity and drive resistance to immune checkpoint blockade (ICB). Recruitment of CCR2⁺ IMs by tumour-derived CCL2 is a central mechanism underlying TAM accumulation. Conventional gemcitabine (GEM) and small-molecule CCR2 inhibitors provide limited benefit due to poor intratumoural delivery, transient target engagement, and compensatory myeloid recruitment.

[METHODS] We engineered a CCR2-targeted nanotheranostic by conjugating a CCR2-binding peptide (ECL1i) and GEM onto ultrasmall copper nanoclusters (CuNCs-ECL1i-GEM; C-E-G). Therapeutic efficacy and immune remodelling were evaluated using orthotopic subcutaneous and the autochthonous PDAC mouse models model, using scRNAseq, flow cytometry, multiplex immunohistochemistry, and in vitro functional assays.

[RESULTS] C-E-G exhibited robust tumour accumulation and selectively eliminated CCR2⁺ TAMs without systemic myelotoxicity, while durably reprogramming residual macrophages. Mechanistically, C-E-G induced the emergence of an immunostimulatory CCRL2⁺ TAM subset through true macrophage repolarization rather than monocyte replacement. CCRL2⁺ TAMs accumulated intratumoural chemerin, upregulated antigen-presentation and co-stimulatory programs, and were essential for CD8⁺ T-cell recruitment and activation. Genetic and orthotopic studies confirmed their CCR2-independent origin and requirement for tumour control. C-E-G remodelled the TME toward a lymphocyte-permissive inflammatory state and synergized with ICB to induce complete tumour regression and prolong survival in KPPC mice.

[CONCLUSIONS] CCR2-targeted cytotoxic nanotherapy eliminates immunosuppressive CCR2 + TAMs, reprograms the macrophage landscape including CCRL2⁺ TAMs, and unlocks durable anti-tumour immunity in PDAC, supporting translational development of this strategy.

[SUPPLEMENTARY INFORMATION] The online version contains supplementary material available at 10.1186/s12943-026-02597-7.

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