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Precision nanomedicine: navigating the tumor microenvironment for enhanced cancer immunotherapy and targeted drug delivery

Sabit, Hussein, Pawlik, Timothy M., Radwan, Faisal, Abdel-Hakeem, Mohamed, Abdel-Ghany, Shaimaa, Wadan, Al-Hassan Soliman, Elzawahri, Mokhtar, El-Hashash, Ahmed, Arneth, Borros·2025·Molecular Cancer
DOI 10.1186/s12943-025-02357-zPMC PMC12131435
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Fig. 1 Various regulated cell death mechanisms—ferroptosis (1), cuproptosis (2), and necroptosis (3)—influence the tumor microenvironment (TME) by shaping immune cell populations and modulating tumor progression. 1) Ferroptosis, characterized by iron-dependent lipid peroxidation and requiring GPX4 for protection, triggers the release of danger-associated molecular patterns (DAMPs). These signals promote dendritic cell (DC) maturation, enhance antigen presentation, and support cytotoxic T lymphocyte (CTL) responses while also affecting macrophage polarization (M1 vs. M2). 2) Cuproptosis, a copper-induced cell death mechanism dependent on ASAH2, can activate the cGAS–STING pathway and stimulate the production of pro-inflammatory cytokines (e.g., IFN-γ, IL-2). This may boost natural killer (NK) cell and T-cell activity but can also recruit immunosuppressive cells (e.g., regulatory T cells [Tregs], myeloid-derived suppressor cells [MDSCs]) and promote a tolerogenic TME under certain conditions. 3) Necroptosis, driven by the RIPK1/RIPK3/MLKL signaling axis, results in cell membrane rupture and additional DAMP release. While this can elicit strong innate and adaptive immune responses—such as NK cell activation and T-cell priming—it may also foster chronic inflammation that supports tumor growth. These distinct death pathways collectively reshape the TME and influence therapeutic outcomes, including responses to immunotherapy. The figure is created with BioRender
Fig. 1 Various regulated cell death mechanisms—ferroptosis (1), cuproptosis (2), and necroptosis (3)—influence the tumor microenvironment (TME) by shaping immune cell populations and modulating tumor progression. 1) Ferroptosis, characterized by iron-dependent lipid peroxidation and requiring GPX4 for protection, triggers the release of danger-associated molecular patterns (DAMPs). These signals promote dendritic cell (DC) maturation, enhance antigen presentation, and support cytotoxic T lymphocyte (CTL) responses while also affecting macrophage polarization (M1 vs. M2). 2) Cuproptosis, a copper-induced cell death mechanism dependent on ASAH2, can activate the cGAS–STING pathway and stimulate the production of pro-inflammatory cytokines (e.g., IFN-γ, IL-2). This may boost natural killer (NK) cell and T-cell activity but can also recruit immunosuppressive cells (e.g., regulatory T cells [Tregs], myeloid-derived suppressor cells [MDSCs]) and promote a tolerogenic TME under certain conditions. 3) Necroptosis, driven by the RIPK1/RIPK3/MLKL signaling axis, results in cell membrane rupture and additional DAMP release. While this can elicit strong innate and adaptive immune responses—such as NK cell activation and T-cell priming—it may also foster chronic inflammation that supports tumor growth. These distinct death pathways collectively reshape the TME and influence therapeutic outcomes, including responses to immunotherapy. The figure is created with BioRenderCC BY-NC-ND · PubMed Central
Fig. 2 The process of normal fibroblasts transforming into CAFs can be described as follows: a Growth Factor and cytokine stimulation. Growth factors and cytokines—including transforming growth factor-beta 1 (TGF-β1), osteopontin (OPN), and IL-1β—bind to their receptors on NFs. This binding trigger downstream effectors such as microRNAs (miRNAs) and CD44, which then regulate CAF-specific gene expression via the TGF-β/Smads and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) pathways. b Exosome-Mediated Transformation: Exosomes released by cancer cells, carrying cargos like miRNAs and long non-coding RNAs (lncRNAs), convert NFs into CAFs. They do so by activating several signaling cascades, including TGF-β/Smads, Janus kinase/signal transducers and activators of transcription (JAK/STAT), NF-κB, and mitogen-activated protein kinase (MAPK) pathways. c Metabolic Reprogramming: The conversion is also driven by a reprogramming of glucose metabolism. The hypoxia-inducible factor-1α (HIF-1α) signaling pathway promotes glycolysis during this transformation. d Homeostasis disruption: Shifts in cellular homeostasis trigger a self-sustaining conversion by modulating the activation of cytoskeletal proteins and altering the cell’s secretory phenotype through the JAK/STAT and p53 pathways. Additional regulatory elements in this conversion process include factors such as Fli-1 leukemia integration 1, transcription factor 12 (TCF12), suppressor of cytokine signaling (1SOCS1), β−1,4-galactosyltransferases III (B4GALT3), insulin-like growth factor 2 receptor (IGF2R), lysophosphatidic acid (LPA), voltage-dependent anion channel (VDAC), Yes-associated protein 1 (YAP1), TEA domain transcription factor-1 (TEAD1), stromal cell-derived factor-1 (SDF-1), epiregulin (EREG), and reactive oxygen species (ROS). The figure is created with BioRender
Fig. 2 The process of normal fibroblasts transforming into CAFs can be described as follows: a Growth Factor and cytokine stimulation. Growth factors and cytokines—including transforming growth factor-beta 1 (TGF-β1), osteopontin (OPN), and IL-1β—bind to their receptors on NFs. This binding trigger downstream effectors such as microRNAs (miRNAs) and CD44, which then regulate CAF-specific gene expression via the TGF-β/Smads and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) pathways. b Exosome-Mediated Transformation: Exosomes released by cancer cells, carrying cargos like miRNAs and long non-coding RNAs (lncRNAs), convert NFs into CAFs. They do so by activating several signaling cascades, including TGF-β/Smads, Janus kinase/signal transducers and activators of transcription (JAK/STAT), NF-κB, and mitogen-activated protein kinase (MAPK) pathways. c Metabolic Reprogramming: The conversion is also driven by a reprogramming of glucose metabolism. The hypoxia-inducible factor-1α (HIF-1α) signaling pathway promotes glycolysis during this transformation. d Homeostasis disruption: Shifts in cellular homeostasis trigger a self-sustaining conversion by modulating the activation of cytoskeletal proteins and altering the cell’s secretory phenotype through the JAK/STAT and p53 pathways. Additional regulatory elements in this conversion process include factors such as Fli-1 leukemia integration 1, transcription factor 12 (TCF12), suppressor of cytokine signaling (1SOCS1), β−1,4-galactosyltransferases III (B4GALT3), insulin-like growth factor 2 receptor (IGF2R), lysophosphatidic acid (LPA), voltage-dependent anion channel (VDAC), Yes-associated protein 1 (YAP1), TEA domain transcription factor-1 (TEAD1), stromal cell-derived factor-1 (SDF-1), epiregulin (EREG), and reactive oxygen species (ROS). The figure is created with BioRenderCC BY-NC-ND · PubMed Central
Fig. 3 The image illustrates the immunological process following vaccine administration, showing cellular and molecular interactions that generate protective immunity. On the left, a schematic human figure displays an injection site where the vaccine is administered. The right side details the immune cascade: vaccine antigens and adjuvants containing danger signals are recognized by PRR on dendritic cells, which become activated and traffic to lymph nodes. These dendritic cells process and present antigens via MHC class II to CD4 + T cells, which recognize the antigen-MHC complex through their TCR. Meanwhile, soluble vaccine antigens can directly bind to BCR on B cells. The activated CD4 + T cells help B cells, stimulating their proliferation, maturation of antibody response, and differentiation into plasma cells that produce antibodies. The bottom portion shows how dendritic cells also present antigens via MHC class I to CD8 + T cells, which differentiate into CD8 + effector T cells and CD8 + memory T cells. The final stage depicts the migration of long-lived plasma cells to the bone marrow, where they continue antibody production for extended periods, establishing durable immunity. The figure is created with BioRender
Fig. 3 The image illustrates the immunological process following vaccine administration, showing cellular and molecular interactions that generate protective immunity. On the left, a schematic human figure displays an injection site where the vaccine is administered. The right side details the immune cascade: vaccine antigens and adjuvants containing danger signals are recognized by PRR on dendritic cells, which become activated and traffic to lymph nodes. These dendritic cells process and present antigens via MHC class II to CD4 + T cells, which recognize the antigen-MHC complex through their TCR. Meanwhile, soluble vaccine antigens can directly bind to BCR on B cells. The activated CD4 + T cells help B cells, stimulating their proliferation, maturation of antibody response, and differentiation into plasma cells that produce antibodies. The bottom portion shows how dendritic cells also present antigens via MHC class I to CD8 + T cells, which differentiate into CD8 + effector T cells and CD8 + memory T cells. The final stage depicts the migration of long-lived plasma cells to the bone marrow, where they continue antibody production for extended periods, establishing durable immunity. The figure is created with BioRenderCC BY-NC-ND · PubMed Central
Fig. 4 The integrated approach to cancer immunotherapy using nanoparticle-mediated strategies combined with checkpoint inhibitors. On the left, a schematic cancer patient is shown receiving an injection. The right side details the complex tumor microenvironment containing multiple cell types: cancer cells (pink), T lymphocytes (green), natural killer cells (purple), myeloid-derived suppressor cells (light blue), dendritic cells (light blue with projections), cancer-associated fibroblasts (gray), red blood cells, and pericytes (yellow). The top panel shows the mechanism of nanoparticle-mediated immunotherapy: functionalized nanoparticles trigger immunogenic cell death in cancer cells and CAFs, leading to dendritic cell maturation and subsequent T cell activation. The middle-left panel illustrates the T cell-tumor cell interaction, with T cell receptors recognizing tumor antigens. The tumor microenvironment depicts blood vessels supplying the tumor mass. The combination therapy approach is highlighted, showing how nanoparticle-mediated immunotherapy works synergistically with checkpoint inhibitors (represented by blocking symbols) to enhance anti-tumor immune responses. A legend on the far right identifies all cell types and therapeutic components, providing a comprehensive view of how these advanced immunotherapeutic strategies interact within the tumor microenvironment to combat cancer. The figure is created with BioRender
Fig. 4 The integrated approach to cancer immunotherapy using nanoparticle-mediated strategies combined with checkpoint inhibitors. On the left, a schematic cancer patient is shown receiving an injection. The right side details the complex tumor microenvironment containing multiple cell types: cancer cells (pink), T lymphocytes (green), natural killer cells (purple), myeloid-derived suppressor cells (light blue), dendritic cells (light blue with projections), cancer-associated fibroblasts (gray), red blood cells, and pericytes (yellow). The top panel shows the mechanism of nanoparticle-mediated immunotherapy: functionalized nanoparticles trigger immunogenic cell death in cancer cells and CAFs, leading to dendritic cell maturation and subsequent T cell activation. The middle-left panel illustrates the T cell-tumor cell interaction, with T cell receptors recognizing tumor antigens. The tumor microenvironment depicts blood vessels supplying the tumor mass. The combination therapy approach is highlighted, showing how nanoparticle-mediated immunotherapy works synergistically with checkpoint inhibitors (represented by blocking symbols) to enhance anti-tumor immune responses. A legend on the far right identifies all cell types and therapeutic components, providing a comprehensive view of how these advanced immunotherapeutic strategies interact within the tumor microenvironment to combat cancer. The figure is created with BioRenderCC BY-NC-ND · PubMed Central
Fig. 5 A schematic representation of nanoparticles targeting cancer stem cells. On the left, differentiated tumor cells and cancer stem cells are depicted within a tumor mass. The nanoparticle conjugated with a chemotherapeutic agent specifically designed to target the CSC marker is shown on the right. The nanoparticle structure consists of a linker chain connecting the chemotherapeutic agent to the targeting antibody, which binds to the cancer stem cell's CSC marker, ensuring targeted treatment delivery. The figure is created with BioRender
Fig. 5 A schematic representation of nanoparticles targeting cancer stem cells. On the left, differentiated tumor cells and cancer stem cells are depicted within a tumor mass. The nanoparticle conjugated with a chemotherapeutic agent specifically designed to target the CSC marker is shown on the right. The nanoparticle structure consists of a linker chain connecting the chemotherapeutic agent to the targeting antibody, which binds to the cancer stem cell's CSC marker, ensuring targeted treatment delivery. The figure is created with BioRenderCC BY-NC-ND · PubMed Central
Fig. 6 Nanotechnology approaches for cancer diagnosis and treatment use nanostructures like liposomes, polymers, micelles, and dendrimers to deliver drugs with active or passive targeting mechanisms. Cancer can be diagnosed using nanotechnology through microfluidic chips, biomarker detection, nanoscale probes, and quantum dots. Treatment options include light-activated gene silencing, RNA-based nanotherapies, strategies to overcome drug resistance, and nanoparticle-delivered CRISPR/Cas9 systems. The figure is created with BioRender
Fig. 6 Nanotechnology approaches for cancer diagnosis and treatment use nanostructures like liposomes, polymers, micelles, and dendrimers to deliver drugs with active or passive targeting mechanisms. Cancer can be diagnosed using nanotechnology through microfluidic chips, biomarker detection, nanoscale probes, and quantum dots. Treatment options include light-activated gene silencing, RNA-based nanotherapies, strategies to overcome drug resistance, and nanoparticle-delivered CRISPR/Cas9 systems. The figure is created with BioRenderCC BY-NC-ND · PubMed Central
Fig. 7 The application of nanomedicine in cancer therapy, showing various nanoparticle delivery systems and their mechanisms of action. At the top, different nanocarriers are displayed: mesoporous NPs, CNTs, gold NPs, liposomes, quantum dots, and polymeric micelles, each with unique structural characteristics. On the left side, a schematic cancer patient is shown receiving an injection of these nanoparticles. The right portion details the mechanism of targeted cancer therapy at the cellular level, featuring normal cells in blue and cancer cells in red with darker nuclei. The process is illustrated in three sequential steps shown in magnified circles: 1) nanocarrier active targeting, where functionalized nanoparticles specifically recognize and bind to cancer cell receptors; 2) receptor-mediated endocytosis, showing the internalization of the nanocarrier into the cancer cell; and 3) cancer cell apoptosis, depicting the death and fragmentation of cancer cells following treatment. A"Stimulation"arrow indicates the activation of the therapeutic effect after nanoparticle administration, showing how these nanomaterials can selectively target and destroy cancer cells while potentially sparing normal tissue. The figure is created with BioRender
Fig. 7 The application of nanomedicine in cancer therapy, showing various nanoparticle delivery systems and their mechanisms of action. At the top, different nanocarriers are displayed: mesoporous NPs, CNTs, gold NPs, liposomes, quantum dots, and polymeric micelles, each with unique structural characteristics. On the left side, a schematic cancer patient is shown receiving an injection of these nanoparticles. The right portion details the mechanism of targeted cancer therapy at the cellular level, featuring normal cells in blue and cancer cells in red with darker nuclei. The process is illustrated in three sequential steps shown in magnified circles: 1) nanocarrier active targeting, where functionalized nanoparticles specifically recognize and bind to cancer cell receptors; 2) receptor-mediated endocytosis, showing the internalization of the nanocarrier into the cancer cell; and 3) cancer cell apoptosis, depicting the death and fragmentation of cancer cells following treatment. A"Stimulation"arrow indicates the activation of the therapeutic effect after nanoparticle administration, showing how these nanomaterials can selectively target and destroy cancer cells while potentially sparing normal tissue. The figure is created with BioRenderCC BY-NC-ND · PubMed Central
Fig. 8 The intricate signaling interactions between cancer-associated fibroblasts (CAFs) and cancer cells, highlighting key pathways involved in tumor progression, proliferation, migration, and metastasis. The PI3 K/AKT/mTOR and ERK signaling cascades are prominently depicted, showing their roles in cellular proliferation, stemness, and invasion. PIP2-PIP3 conversion by PI3 K and its regulation by PTEN influence downstream mTOR activation, facilitating tumor growth and CAF transformation. Additionally, cancer-derived factors such as CXCL12, IL-32, and POSTN promote EMT and metastatic potential through JNK, p38, and ERK1/2 signaling. The interplay between CAF-secreted factors and cancer cells fosters an immunosuppressive and tumor-promoting microenvironment. This schematic underscores the importance of targeting CAF-cancer cell crosstalk to develop effective therapeutic interventions. The figure is created with BioRender
Fig. 8 The intricate signaling interactions between cancer-associated fibroblasts (CAFs) and cancer cells, highlighting key pathways involved in tumor progression, proliferation, migration, and metastasis. The PI3 K/AKT/mTOR and ERK signaling cascades are prominently depicted, showing their roles in cellular proliferation, stemness, and invasion. PIP2-PIP3 conversion by PI3 K and its regulation by PTEN influence downstream mTOR activation, facilitating tumor growth and CAF transformation. Additionally, cancer-derived factors such as CXCL12, IL-32, and POSTN promote EMT and metastatic potential through JNK, p38, and ERK1/2 signaling. The interplay between CAF-secreted factors and cancer cells fosters an immunosuppressive and tumor-promoting microenvironment. This schematic underscores the importance of targeting CAF-cancer cell crosstalk to develop effective therapeutic interventions. The figure is created with BioRenderCC BY-NC-ND · PubMed Central

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Metadata

Authors
Sabit, H., Pawlik, T. M., Radwan, F., Abdel-Hakeem, M., Abdel-Ghany, S., Wadan, A.-H. S., Elzawahri, M., El-Hashash, A., & Arneth, B.
Venue
Molecular Cancer
Publisher
Springer Science and Business Media LLC
Published
2025-06-03
Volume
24
Issue
1
ISSN
1476-4598
DOI
10.1186/s12943-025-02357-z
PMC
PMC12131435
Cited by
239
References
4
Language
en
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