Stimuli-responsive nanodelivery systems for amplifying immunogenic cell death in cancer immunotherapy
Wenhao Xu
Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, China
Shanghai Genitourinary Cancer Institute, Shanghai, China
Search for more papers by this authorWangrui Liu
Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Search for more papers by this authorJianfeng Yang
Department of Surgery, ShangNan Branch of Longhua Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai, China
Search for more papers by this authorJiahe Lu
Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, China
Shanghai Genitourinary Cancer Institute, Shanghai, China
School of Cellular and Molecular Medicine, University of Bristol, Bristol, UK
Search for more papers by this authorCorresponding Author
Hailiang Zhang
Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, China
Shanghai Genitourinary Cancer Institute, Shanghai, China
Correspondence
Dingwei Ye and Hailiang Zhang, Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai 200032, China.
Email: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Dingwei Ye
Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, China
Shanghai Genitourinary Cancer Institute, Shanghai, China
Correspondence
Dingwei Ye and Hailiang Zhang, Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai 200032, China.
Email: [email protected]; [email protected]
Search for more papers by this authorWenhao Xu
Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, China
Shanghai Genitourinary Cancer Institute, Shanghai, China
Search for more papers by this authorWangrui Liu
Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
Search for more papers by this authorJianfeng Yang
Department of Surgery, ShangNan Branch of Longhua Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai, China
Search for more papers by this authorJiahe Lu
Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, China
Shanghai Genitourinary Cancer Institute, Shanghai, China
School of Cellular and Molecular Medicine, University of Bristol, Bristol, UK
Search for more papers by this authorCorresponding Author
Hailiang Zhang
Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, China
Shanghai Genitourinary Cancer Institute, Shanghai, China
Correspondence
Dingwei Ye and Hailiang Zhang, Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai 200032, China.
Email: [email protected]; [email protected]
Search for more papers by this authorCorresponding Author
Dingwei Ye
Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai, China
Shanghai Genitourinary Cancer Institute, Shanghai, China
Correspondence
Dingwei Ye and Hailiang Zhang, Department of Urology, Fudan University Shanghai Cancer Center, Fudan University, Shanghai 200032, China.
Email: [email protected]; [email protected]
Search for more papers by this authorWenhao Xu, Wangrui Liu and Jianfeng Yang have contributed equally to this work and share first authorship.
This article is part of a series of reviews covering Mechanisms of programmed cell death appearing in Volume 321 of Immunological Reviews.
Summary
Immunogenic cell death (ICD) is a special pattern of tumor cell death, enabling to elicit tumor-specific immune response via the release of damage-associated molecular patterns and tumor-associated antigens in the tumor microenvironment. ICD-induced immunotherapy holds the promise for completely eliminating tumors and long-term protective antitumor immune response. Increasing ICD inducers have been discovered for boosting antitumor immunity via evoking ICD. Nonetheless, the utilization of ICD inducers remains insufficient owing to serious toxic reactions, low localization efficiency within the tumor microenvironmental niche, etc. For overcoming such limitations, stimuli-responsive multifunctional nanoparticles or nanocomposites with ICD inducers have been developed for improving immunotherapeutic efficiency via lowering toxicity, which represent a prospective scheme for fostering the utilization of ICD inducers in immunotherapy. This review outlines the advances in near-infrared (NIR)-, pH-, redox-, pH- and redox-, or NIR- and tumor microenvironment-responsive nanodelivery systems for ICD induction. Furthermore, we discuss their clinical translational potential. The progress of stimuli-responsive nanoparticles in clinical settings depends upon the development of biologically safer drugs tailored to patient needs. Moreover, an in-depth comprehending of ICD biomarkers, immunosuppressive microenvironment, and ICD inducers may accelerate the advance in smarter multifunctional nanodelivery systems to further amplify ICD.
CONFLICT OF INTEREST STATEMENT
The authors declare that there are no conflicts of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
REFERENCES
- 1Galluzzi L, Bravo-San Pedro JM, Vitale I, et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 2015; 22(1): 58-73.
- 2Maekawa T, Kashkar H, Coll NS. Dying in self-defence: a comparative overview of immunogenic cell death signalling in animals and plants. Cell Death Differ. 2023; 30(2): 258-268.
- 3Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013; 31: 51-72.
- 4Galluzzi L, Vitale I, Warren S, et al. Consensus guidelines for the definition, detection and interpretation of immunogenic cell death. J Immunother Cancer. 2020; 8(1):e000337.
- 5Mok TSK, Wu YL, Kudaba I, et al. Pembrolizumab versus chemotherapy for previously untreated, PD-L1-expressing, locally advanced or metastatic non-small-cell lung cancer (KEYNOTE-042): a randomised, open-label, controlled, phase 3 trial. Lancet. 2019; 393(10183): 1819-1830.
- 6D'Angelo SP, Melchiori L, Merchant MS, et al. Antitumor activity associated with prolonged persistence of adoptively transferred NY-ESO-1 (c259)T cells in synovial sarcoma. Cancer Discov. 2018; 8(8): 944-957.
- 7Benjamin R, Graham C, Yallop D, et al. Genome-edited, donor-derived allogeneic anti-CD19 chimeric antigen receptor T cells in paediatric and adult B-cell acute lymphoblastic leukaemia: results of two phase 1 studies. Lancet. 2020; 396(10266): 1885-1894.
- 8Li Z, Lai X, Fu S, et al. Immunogenic cell death activates the tumor immune microenvironment to boost the immunotherapy efficiency. Adv Sci (Weinh). 2022; 9(22):e2201734.
- 9Nikolos F, Hayashi K, Hoi XP, et al. Cell death-induced immunogenicity enhances chemoimmunotherapeutic response by converting immune-excluded into T-cell inflamed bladder tumors. Nat Commun. 2022; 13(1): 1487.
- 10Lu Z, Liu D, Wei P, Yi T. Activated aggregation strategies to construct size-increasing nanoparticles for cancer therapy. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2023; 15(2):e1848.
- 11Phan HT, Lauzon D, Vallée-Bélisle A, Angioletti-Uberti S, Leblond Chain J, Giasson S. Bimodal brush-functionalized nanoparticles selective to receptor surface density. Proc Natl Acad Sci USA. 2023; 120(3):e2208377120.
- 12Nguyen NTT, Nguyen TTT, Nguyen DTC, Tran TV. Green synthesis of ZnFe(2)O(4) nanoparticles using plant extracts and their applications: a review. Sci Total Environ. 2023; 872:162212.
- 13Kroemer G, Galassi C, Zitvogel L, Galluzzi L. Immunogenic cell stress and death. Nat Immunol. 2022; 23(4): 487-500.
- 14Marin I, Boix O, Garcia-Garijo A, et al. Cellular senescence is immunogenic and promotes antitumor immunity. Cancer Discov. 2023; 13(2): 410-431.
- 15Meng Q, Ding B, Ma P, Lin J. Interrelation between programmed cell death and immunogenic cell death: Take antitumor nanodrug as an example. Small Methods. 2023; 7:e2201406.
- 16Ding F, Li F, Tang D, et al. Restoration of the immunogenicity of tumor cells for enhanced cancer therapy via nanoparticle-mediated copper chaperone inhibition. Angew Chem Int Ed Engl. 2022; 61(31):e202203546.
- 17Fucikova J, Spisek R, Kroemer G, Galluzzi L. Calreticulin and cancer. Cell Res. 2021; 31(1): 5-16.
- 18Li W, Yang J, Luo L, et al. Targeting photodynamic and photothermal therapy to the endoplasmic reticulum enhances immunogenic cancer cell death. Nat Commun. 2019; 10(1): 3349.
- 19von Roemeling CA, Wang Y, Qie Y, et al. Therapeutic modulation of phagocytosis in glioblastoma can activate both innate and adaptive antitumour immunity. Nat Commun. 2020; 11(1): 1508.
- 20Galluzzi L, Buqué A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol. 2017; 17(2): 97-111.
- 21Hayashi K, Nikolos F, Lee YC, et al. Tipping the immunostimulatory and inhibitory DAMP balance to harness immunogenic cell death. Nat Commun. 2020; 11(1): 6299.
- 22Chabanon RM, Rouanne M, Lord CJ, Soria JC, Pasero P, Postel-Vinay S. Targeting the DNA damage response in immuno-oncology: developments and opportunities. Nat Rev Cancer. 2021; 21(11): 701-717.
- 23Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer. 2012; 12(12): 860-875.
- 24Chauhan D, Vande Walle L, Lamkanfi M. Therapeutic modulation of inflammasome pathways. Immunol Rev. 2020; 297(1): 123-138.
- 25Lau TS, Chan LKY, Man GCW, et al. Paclitaxel induces immunogenic cell death in ovarian cancer via TLR4/IKK2/SNARE-dependent exocytosis. Cancer Immunol Res. 2020; 8(8): 1099-1111.
- 26Mandula JK, Chang S, Mohamed E, et al. Ablation of the endoplasmic reticulum stress kinase PERK induces paraptosis and type I interferon to promote anti-tumor T cell responses. Cancer Cell. 2022; 40(10): 1145-1160.e1149.
- 27Limagne E, Nuttin L, Thibaudin M, et al. MEK inhibition overcomes chemoimmunotherapy resistance by inducing CXCL10 in cancer cells. Cancer Cell. 2022; 40(2): 136-152.e112.
- 28Arai H, Xiao Y, Loupakis F, et al. Immunogenic cell death pathway polymorphisms for predicting oxaliplatin efficacy in metastatic colorectal cancer. J Immunother Cancer. 2020; 8(2):e001714.
- 29Zhou F, Feng B, Yu H, et al. Tumor microenvironment-activatable prodrug vesicles for Nanoenabled cancer chemoimmunotherapy combining immunogenic cell death induction and CD47 blockade. Adv Mater. 2019; 31(14):e1805888.
- 30Ma X, Yang S, Zhang T, et al. Bioresponsive immune-booster-based prodrug nanogel for cancer immunotherapy. Acta Pharm Sin B. 2022; 12(1): 451-466.
- 31Hetz C, Zhang K, Kaufman RJ. Mechanisms, regulation and functions of the unfolded protein response. Nat Rev Mol Cell Biol. 2020; 21(8): 421-438.
- 32Blanchet FP, Piguet V. Immunoamphisomes in dendritic cells amplify TLR signaling and enhance exogenous antigen presentation on MHC-II. Autophagy. 2010; 6(6): 816-818.
- 33Tang T, Huang X, Zhang G, et al. Oncolytic peptide LTX-315 induces anti-pancreatic cancer immunity by targeting the ATP11B-PD-L1 axis. J Immunother Cancer. 2022; 10(3):e004129.
- 34Zhou H, Sauvat A, Gomes-da-Silva LC, et al. The oncolytic compound LTX-401 targets the Golgi apparatus. Cell Death Differ. 2016; 23(12): 2031-2041.
- 35Niu X, Chen L, Li Y, Hu Z, He F. Ferroptosis, necroptosis, and pyroptosis in the tumor microenvironment: perspectives for immunotherapy of SCLC. Semin Cancer Biol. 2022; 86(Pt 3): 273-285.
- 36Wu J, Waxman DJ. Immunogenic chemotherapy: dose and schedule dependence and combination with immunotherapy. Cancer Lett. 2018; 419: 210-221.
- 37Fucikova J, Kepp O, Kasikova L, et al. Detection of immunogenic cell death and its relevance for cancer therapy. Cell Death Dis. 2020; 11(11): 1013.
- 38Del Re DP, Amgalan D, Linkermann A, Liu Q, Kitsis RN. Fundamental mechanisms of regulated cell death and implications for heart disease. Physiol Rev. 2019; 99(4): 1765-1817.
- 39Aaes TL, Vandenabeele P. The intrinsic immunogenic properties of cancer cell lines, immunogenic cell death, and how these influence host antitumor immune responses. Cell Death Differ. 2021; 28(3): 843-860.
- 40Yan J, Wan P, Choksi S, Liu ZG. Necroptosis and tumor progression. Trends Cancer. 2022; 8(1): 21-27.
- 41Tang R, Xu J, Zhang B, et al. Ferroptosis, necroptosis, and pyroptosis in anticancer immunity. J Hematol Oncol. 2020; 13(1): 110.
- 42Tan Y, Chen Q, Li X, et al. Pyroptosis: a new paradigm of cell death for fighting against cancer. J Exp Clin Cancer Res. 2021; 40(1): 153.
- 43Hänggi K, Ruffell B. Cell death, therapeutics, and the immune response in cancer. Trends Cancer. 2023; 9: 381-396.
- 44Zheng M, Kanneganti TD. The regulation of the ZBP1-NLRP3 inflammasome and its implications in pyroptosis, apoptosis, and necroptosis (PANoptosis). Immunol Rev. 2020; 297(1): 26-38.
- 45Alptekin A, Parvin M, Chowdhury HI, Rashid MH, Arbab AS. Engineered exosomes for studies in tumor immunology. Immunol Rev. 2022; 312(1): 76-102.
- 46Xu X, Li Y, Li H, et al. Smart nanovehicles based on pH-triggered disassembly of supramolecular peptide-amphiphiles for efficient intracellular drug delivery. Small. 2014; 10(6): 1133-1140.
- 47Boedtkjer E, Pedersen SF. The acidic tumor microenvironment as a driver of cancer. Annu Rev Physiol. 2020; 82: 103-126.
- 48Li Y, Yuan R, Luo Y, et al. A hierarchical structured fiber device remodeling the acidic tumor microenvironment for enhanced cancer immunotherapy. Adv Mater. 2023; 35:e2300216.
- 49Tu K, Deng H, Kong L, et al. Reshaping tumor immune microenvironment through acidity-responsive nanoparticles featured with CRISPR/Cas9-mediated programmed death-ligand 1 attenuation and chemotherapeutics-induced immunogenic cell death. ACS Appl Mater Interfaces. 2020; 12(14): 16018-16030.
- 50Dorand RD, Nthale J, Myers JT, et al. Cdk5 disruption attenuates tumor PD-L1 expression and promotes antitumor immunity. Science. 2016; 353(6297): 399-403.
- 51Zhang X, Lu Y, Jia D, et al. Acidic microenvironment responsive polymeric MOF-based nanoparticles induce immunogenic cell death for combined cancer therapy. J Nanobiotechnology. 2021; 19(1): 455.
- 52Jiang M, Chen W, Yu W, et al. Sequentially pH-responsive drug-delivery Nanosystem for tumor immunogenic cell death and cooperating with immune checkpoint blockade for efficient cancer chemoimmunotherapy. ACS Appl Mater Interfaces. 2021; 13(37): 43963-43974.
- 53Zhang Y, Guo C, Liu L, et al. ZnO-based multifunctional nanocomposites to inhibit progression and metastasis of melanoma by eliciting antitumor immunity via immunogenic cell death. Theranostics. 2020; 10(24): 11197-11214.
- 54Yao D, Wang Y, Bian K, Zhang B, Wang D. A self-cascaded unimolecular prodrug for pH-responsive chemotherapy and tumor-detained photodynamic-immunotherapy of triple-negative breast cancer. Biomaterials. 2023; 292:121920.
- 55Yu X, Han N, Dong Z, et al. Combined chemo-Immuno-photothermal therapy for effective cancer treatment via an all-in-one and one-for-all nanoplatform. ACS Appl Mater Interfaces. 2022; 14(38): 42988-43009.
- 56Wang R, Xu X, Li D, et al. Smart pH-responsive polyhydralazine/bortezomib nanoparticles for remodeling tumor microenvironment and enhancing chemotherapy. Biomaterials. 2022; 288:121737.
- 57Qiu W, Liang M, Gao Y, et al. Polyamino acid calcified nanohybrids induce immunogenic cell death for augmented chemotherapy and chemo-photodynamic synergistic therapy. Theranostics. 2021; 11(19): 9652-9666.
- 58Lei Y, Tang L, Chen Q, et al. Disulfiram ameliorates nonalcoholic steatohepatitis by modulating the gut microbiota and bile acid metabolism. Nat Commun. 2022; 13(1): 6862.
- 59Li Q, Chao Y, Liu B, et al. Disulfiram loaded calcium phosphate nanoparticles for enhanced cancer immunotherapy. Biomaterials. 2022; 291:121880.
- 60Chen M, Huang Z, Xia M, et al. Glutathione-responsive copper-disulfiram nanoparticles for enhanced tumor chemotherapy. J Control Release. 2022; 341: 351-363.
- 61Abu-Serie MM, Abdelfattah EZA. Anti-metastatic breast cancer potential of novel nanocomplexes of diethyldithiocarbamate and green chemically synthesized iron oxide nanoparticles. Int J Pharm. 2022; 627:122208.
- 62Kelley KC, Grossman KF, Brittain-Blankenship M, et al. A phase 1 dose-escalation study of disulfiram and copper gluconate in patients with advanced solid tumors involving the liver using S-glutathionylation as a biomarker. BMC Cancer. 2021; 21(1): 510.
- 63Huang J, Chaudhary R, Cohen AL, et al. A multicenter phase II study of temozolomide plus disulfiram and copper for recurrent temozolomide-resistant glioblastoma. J Neurooncol. 2019; 142(3): 537-544.
- 64Huang J, Campian JL, Gujar AD, et al. Final results of a phase I dose-escalation, dose-expansion study of adding disulfiram with or without copper to adjuvant temozolomide for newly diagnosed glioblastoma. J Neurooncol. 2018; 138(1): 105-111.
- 65Wesch D, Kabelitz D, Oberg HH. Tumor resistance mechanisms and their consequences on γδ T cell activation. Immunol Rev. 2020; 298(1): 84-98.
- 66Long GV, Dummer R, Hamid O, et al. Epacadostat plus pembrolizumab versus placebo plus pembrolizumab in patients with unresectable or metastatic melanoma (ECHO-301/KEYNOTE-252): a phase 3, randomised, double-blind study. Lancet Oncol. 2019; 20(8): 1083-1097.
- 67Sadik A, Somarribas Patterson LF, Öztürk S, et al. IL4I1 is a metabolic immune checkpoint that activates the AHR and promotes tumor progression. Cell. 2020; 182(5): 1252-1270.e1234.
- 68Hanurry EY, Birhan YS, Darge HF, et al. PAMAM dendritic nanoparticle-incorporated hydrogel to enhance the immunogenic cell death and immune response of Immunochemotherapy. ACS Biomater Sci Eng. 2022; 8(6): 2403-2418.
- 69Zhu Y, Yang Z, Dong Z, et al. CaCO(3)-assisted preparation of pH-responsive immune-modulating nanoparticles for augmented chemo-immunotherapy. Nanomicro Lett. 2020; 13(1): 29.
- 70Yang W, Zhang F, Deng H, et al. Smart nanovesicle-mediated immunogenic cell death through tumor microenvironment modulation for effective photodynamic immunotherapy. ACS Nano. 2020; 14(1): 620-631.
- 71Mei KC, Liao YP, Jiang J, et al. Liposomal delivery of mitoxantrone and a cholesteryl Indoximod prodrug provides effective chemo-immunotherapy in multiple solid tumors. ACS Nano. 2020; 14(10): 13343-13366.
- 72Zhu H, Bengsch F, Svoronos N, et al. BET bromodomain inhibition promotes anti-tumor immunity by suppressing PD-L1 expression. Cell Rep. 2016; 16(11): 2829-2837.
- 73Li W, Gupta SK, Han W, et al. Targeting MYC activity in double-hit lymphoma with MYC and BCL2 and/or BCL6 rearrangements with epigenetic bromodomain inhibitors. J Hematol Oncol. 2019; 12(1): 73.
- 74Gu J, Zhao G, Yu J, et al. Injectable pH-responsive hydrogel for combinatorial chemoimmunotherapy tailored to the tumor microenvironment. J Nanobiotechnology. 2022; 20(1): 372.
- 75Huang SW, Wang ST, Chang SH, et al. Imiquimod exerts antitumor effects by inducing immunogenic cell death and is enhanced by the glycolytic inhibitor 2-Deoxyglucose. J Invest Dermatol. 2020; 140(9): 1771-1783.e1776.
- 76Yue J, Mei Q, Wang P, Miao P, Dong WF, Li L. Light-triggered multifunctional nanoplatform for efficient cancer photo-immunotherapy. J Nanobiotechnology. 2022; 20(1): 181.
- 77Lambing S, Tan YP, Vasileiadou P, et al. RIG-I immunotherapy overcomes radioresistance in p53-positive malignant melanoma. J Mol Cell Biol. 2023;mjad001.
- 78Thoresen D, Wang W, Galls D, Guo R, Xu L, Pyle AM. The molecular mechanism of RIG-I activation and signaling. Immunol Rev. 2021; 304(1): 154-168.
- 79Hornung V, Ellegast J, Kim S, et al. 5′-triphosphate RNA is the ligand for RIG-I. Science. 2006; 314(5801): 994-997.
- 80Jacobson ME, Wang-Bishop L, Becker KW, Wilson JT. Delivery of 5′-triphosphate RNA with endosomolytic nanoparticles potently activates RIG-I to improve cancer immunotherapy. Biomater Sci. 2019; 7(2): 547-559.
- 81Gunassekaran GR, Poongkavithai Vadevoo SM, Baek MC, Lee B. M1 macrophage exosomes engineered to foster M1 polarization and target the IL-4 receptor inhibit tumor growth by reprogramming tumor-associated macrophages into M1-like macrophages. Biomaterials. 2021; 278:121137.
- 82Kamerkar S, Leng C, Burenkova O, et al. Exosome-mediated genetic reprogramming of tumor-associated macrophages by exoASO-STAT6 leads to potent monotherapy antitumor activity. Sci Adv. 2022; 8:eabj7002.
- 83Larson C, Oronsky B, Carter CA, et al. TGF-beta: a master immune regulator. Expert Opin Ther Targets. 2020; 24(5): 427-438.
- 84Xiao H, Guo Y, Li B, et al. M2-like tumor-associated macrophage-targeted codelivery of STAT6 inhibitor and IKKβ siRNA induces M2-to-M1 repolarization for cancer immunotherapy with low immune side effects. ACS Cent Sci. 2020; 6(7): 1208-1222.
- 85Jaynes JM, Sable R, Ronzetti M, et al. Mannose receptor (CD206) activation in tumor-associated macrophages enhances adaptive and innate antitumor immune responses. Sci Transl Med. 2020; 12(530):eaax6337.
- 86Du T, Wang Y, Luan Z, Zhao C, Yang K. Tumor-associated macrophage membrane-camouflaged pH-responsive polymeric micelles for combined cancer chemotherapy-sensitized immunotherapy. Int J Pharm. 2022; 624:121911.
- 87Zhu Y, Yang J, Xu D, et al. Disruption of tumour-associated macrophage trafficking by the osteopontin-induced colony-stimulating factor-1 signalling sensitises hepatocellular carcinoma to anti-PD-L1 blockade. Gut. 2019; 68(9): 1653-1666.
- 88Zhu M, Bai L, Liu X, et al. Silence of a dependence receptor CSF1R in colorectal cancer cells activates tumor-associated macrophages. J Immunother Cancer. 2022; 10(12):e005610.
- 89Quail DF, Bowman RL, Akkari L, et al. The tumor microenvironment underlies acquired resistance to CSF-1R inhibition in gliomas. Science. 2016; 352(6288):aad3018.
- 90Park K, Ahn JW, Kim JH, Kim JW. Tumor-associated macrophage-targeted photodynamic cancer therapy using a dextran sulfate-based nano-photosensitizer. Int J Biol Macromol. 2022; 218: 384-393.
- 91Sun X, Zhang J, Zhao X, et al. Binary regulation of the tumor microenvironment by a pH-responsive reversible shielding nanoplatform for improved tumor chemo-immunotherapy. Acta Biomater. 2022; 138: 505-517.
- 92Romani P, Nirchio N, Arboit M, et al. Mitochondrial fission links ECM mechanotransduction to metabolic redox homeostasis and metastatic chemotherapy resistance. Nat Cell Biol. 2022; 24(2): 168-180.
- 93Zhu B, Qu F, Bi D, Geng R, Chen S, Zhu J. Monolayer LDH nanosheets with ultrahigh ICG loading for phototherapy and Ca(2+)-induced mitochondrial membrane potential damage to Co-enhance cancer immunotherapy. ACS Appl Mater Interfaces. 2023; 15: 9135-9149.
- 94Bao D, Zhao J, Zhou X, et al. Mitochondrial fission-induced mtDNA stress promotes tumor-associated macrophage infiltration and HCC progression. Oncogene. 2019; 38(25): 5007-5020.
- 95Jiang Y, Krantz S, Qin X, et al. Caveolin-1 controls mitochondrial damage and ROS production by regulating fission – fusion dynamics and mitophagy. Redox Biol. 2022; 52:102304.
- 96Gao Z, Li Y, Wang F, et al. Mitochondrial dynamics controls anti-tumour innate immunity by regulating CHIP-IRF1 axis stability. Nat Commun. 2017; 8(1): 1805.
- 97Li S, Han S, Zhang Q, et al. FUNDC2 promotes liver tumorigenesis by inhibiting MFN1-mediated mitochondrial fusion. Nat Commun. 2022; 13(1): 3486.
- 98Zhao M, Li J, Liu J, et al. Charge-switchable nanoparticles enhance cancer immunotherapy based on mitochondrial dynamic regulation and immunogenic cell death induction. J Control Release. 2021; 335: 320-332.
- 99Sun Y, Lyu B, Yang C, et al. An enzyme-responsive and transformable PD-L1 blocking peptide-photosensitizer conjugate enables efficient photothermal immunotherapy for breast cancer. Bioact Mater. 2023; 22: 47-59.
- 100Barve A, Jain A, Liu H, Zhao Z, Cheng K. Enzyme-responsive polymeric micelles of cabazitaxel for prostate cancer targeted therapy. Acta Biomater. 2020; 113: 501-511.
- 101Liu Y, Xie J, Zhao X, Zhang Y, Zhong Z, Deng C. A polymeric IDO inhibitor based on poly(ethylene glycol)-b-poly(L-tyrosine-co-1-methyl-D-tryptophan) enables facile trident cancer immunotherapy. Biomater Sci. 2022; 10(19): 5731-5743.
- 102Sameiyan E, Bagheri E, Dehghani S, et al. Aptamer-based ATP-responsive delivery systems for cancer diagnosis and treatment. Acta Biomater. 2021; 123: 110-122.
- 103You Z, Chi H. Lipid metabolism in dendritic cell biology. Immunol Rev. 2023.
- 104Oresta B, Pozzi C, Braga D, et al. Mitochondrial metabolic reprogramming controls the induction of immunogenic cell death and efficacy of chemotherapy in bladder cancer. Sci Transl Med. 2021; 13(575):eaba6110.
- 105Yu M, Zeng W, Ouyang Y, et al. ATP-exhausted nanocomplexes for intratumoral metabolic intervention and photoimmunotherapy. Biomaterials. 2022; 284:121503.
- 106Jiang W, Chen L, Guo X, et al. Combating multidrug resistance and metastasis of breast cancer by endoplasmic reticulum stress and cell-nucleus penetration enhanced immunochemotherapy. Theranostics. 2022; 12(6): 2987-3006.
- 107Sun L, Shen F, Tian L, et al. ATP-responsive smart hydrogel releasing immune adjuvant synchronized with repeated chemotherapy or radiotherapy to boost antitumor immunity. Adv Mater. 2021; 33(18):e2007910.
- 108Zhong W, Zhang X, Duan X, et al. Redox-responsive self-assembled polymeric nanoprodrug for delivery of gemcitabine in B-cell lymphoma therapy. Acta Biomater. 2022; 144: 67-80.
- 109Wan J, Zhang X, Li Z, et al. Oxidative stress amplifiers as immunogenic cell death Nanoinducers disrupting mitochondrial redox homeostasis for cancer immunotherapy. Adv Healthc Mater. 2022; 12:e2202710.
- 110Li D, Zhang R, Liu G, Kang Y, Wu J. Redox-responsive self-assembled nanoparticles for cancer therapy. Adv Healthc Mater. 2020; 9(20):e2000605.
- 111He M, Wang M, Xu T, et al. Reactive oxygen species-powered cancer immunotherapy: current status and challenges. J Control Release. 2023; 356: 623-648.
- 112Yan P, Luo Y, Li X, et al. A redox-responsive Nanovaccine combined with A2A receptor antagonist for cancer immunotherapy. Adv Healthc Mater. 2021; 10(21):e2101222.
- 113Jeon J, Yoon B, Dey A, et al. Self-immolative polymer-based immunogenic cell death inducer for regulation of redox homeostasis. Biomaterials. 2023; 295:122064.
- 114Song J, Cheng M, Xie Y, Li K, Zang X. Efficient tumor synergistic chemoimmunotherapy by self-augmented ROS-responsive immunomodulatory polymeric nanodrug. J Nanobiotechnology. 2023; 21(1): 93.
- 115Jin F, Qi J, Zhu M, et al. NIR-triggered sequentially responsive nanocarriers amplified Cascade synergistic effect of chemo-photodynamic therapy with inspired antitumor immunity. ACS Appl Mater Interfaces. 2020; 12(29): 32372-32387.
- 116Zhang Y, Du X, Liu S, et al. NIR-triggerable ROS-responsive cluster-bomb-like nanoplatform for enhanced tumor penetration, phototherapy efficiency and antitumor immunity. Biomaterials. 2021; 278:121135.
- 117Chen X, Ling X, Xia J, et al. Mature dendritic cell-derived dendrosomes swallow oxaliplatin-loaded nanoparticles to boost immunogenic chemotherapy and tumor antigen-specific immunotherapy. Bioact Mater. 2022; 15: 15-28.
- 118Lu Y, Gong Y, Zhu X, Dong X, Zhu D, Ma G. Design of Light-Activated Nanoplatform through boosting “eat me” signals for improved CD47-blocking immunotherapy. Adv Healthc Mater. 2022; 11(10):e2102712.
- 119Gong Y, Chen M, Tan Y, et al. Injectable reactive oxygen species-responsive SN38 prodrug scaffold with checkpoint inhibitors for combined chemoimmunotherapy. ACS Appl Mater Interfaces. 2020; 12(45): 50248-50259.
- 120Mao C, Yeh S, Fu J, et al. Delivery of an ectonucleotidase inhibitor with ROS-responsive nanoparticles overcomes adenosine-mediated cancer immunosuppression. Sci Transl Med. 2022; 14(648):eabh1261.
- 121Wang Y, Zhu L, Wang Y, et al. Ultrasensitive GSH-responsive ditelluride-containing poly(ether-urethane) nanoparticles for controlled drug release. ACS Appl Mater Interfaces. 2016; 8(51): 35106-35113.
- 122Wu W, Chen M, Luo T, et al. ROS and GSH-responsive S-nitrosoglutathione functionalized polymeric nanoparticles to overcome multidrug resistance in cancer. Acta Biomater. 2020; 103: 259-271.
- 123Hu J, Liang M, Ye M, et al. Reduction-triggered polycyclodextrin supramolecular nanocage induces immunogenic cell death for improved chemotherapy. Carbohydr Polym. 2023; 301(Pt B):120365.
- 124Guo Y, Fan Y, Wang Z, et al. Chemotherapy mediated by biomimetic polymeric nanoparticles potentiates enhanced tumor immunotherapy via amplification of endoplasmic reticulum stress and mitochondrial dysfunction. Adv Mater. 2022; 34(47):e2206861.
- 125Heffeter P, Atil B, Kryeziu K, et al. The ruthenium compound KP1339 potentiates the anticancer activity of sorafenib in vitro and in vivo. Eur J Cancer. 2013; 49(15): 3366-3375.
- 126Wernitznig D, Kiakos K, Del Favero G, et al. First-in-class ruthenium anticancer drug (KP1339/IT-139) induces an immunogenic cell death signature in colorectal spheroids in vitro. Metallomics. 2019; 11(6): 1044-1048.
- 127Zhang F, Chen F, Yang C, et al. Coordination and redox dual-responsive mesoporous Organosilica nanoparticles amplify immunogenic cell death for cancer chemoimmunotherapy. Small. 2021; 17(26):e2100006.
- 128Antuamwine BB, Bosnjakovic R, Hofmann-Vega F, et al. N1 versus N2 and PMN-MDSC: a critical appraisal of current concepts on tumor-associated neutrophils and new directions for human oncology. Immunol Rev. 2023; 314(1): 250-279.
- 129Li K, Shi H, Zhang B, et al. Myeloid-derived suppressor cells as immunosuppressive regulators and therapeutic targets in cancer. Signal Transduct Target Ther. 2021; 6(1): 362.
- 130Zhao H, Teng D, Yang L, et al. Myeloid-derived itaconate suppresses cytotoxic CD8(+) T cells and promotes tumour growth. Nat Metab. 2022; 4(12): 1660-1673.
- 131Xia C, Li M, Ran G, et al. Redox-responsive nanoassembly restrained myeloid-derived suppressor cells recruitment through autophagy-involved lactate dehydrogenase a silencing for enhanced cancer immunochemotherapy. J Control Release. 2021; 335: 557-574.
- 132Liu X, Li Y, Wang K, et al. GSH-responsive Nanoprodrug to inhibit glycolysis and alleviate immunosuppression for cancer therapy. Nano Lett. 2021; 21(18): 7862-7869.
- 133Huang Z, Wang Y, Yao D, Wu J, Hu Y, Yuan A. Nanoscale coordination polymers induce immunogenic cell death by amplifying radiation therapy mediated oxidative stress. Nat Commun. 2021; 12(1): 145.
- 134Zhao L, Zheng R, Liu L, et al. Self-delivery oxidative stress amplifier for chemotherapy sensitized immunotherapy. Biomaterials. 2021; 275:120970.
- 135Li M, Zhang Y, Zhang X, et al. Degradable multifunctional porphyrin-based porous organic polymer Nanosonosensitizer for tumor-specific sonodynamic, chemo- and immunotherapy. ACS Appl Mater Interfaces. 2022; 14(43): 48489-48501.
- 136Wang Z, Qu S, Gao D, Shao Q, Nie C, Xing C. A strategy of on-demand immune activation for antifungal treatment using near-infrared responsive conjugated polymer nanoparticles. Nano Lett. 2023; 23(1): 326-335.
- 137Tian Y, Younis MR, Tang Y, et al. Dye-loaded mesoporous polydopamine nanoparticles for multimodal tumor theranostics with enhanced immunogenic cell death. J Nanobiotechnology. 2021; 19(1): 365.
- 138Wang-Bishop L, Wehbe M, Shae D, et al. Potent STING activation stimulates immunogenic cell death to enhance antitumor immunity in neuroblastoma. J Immunother Cancer. 2020; 8(1):e000282.
- 139Zhan M, Yu X, Zhao W, et al. Extracellular matrix-degrading STING nanoagonists for mild NIR-II photothermal-augmented chemodynamic-immunotherapy. J Nanobiotechnology. 2022; 20(1): 23.
- 140Sun X, Zhang Y, Li J, et al. Amplifying STING activation by cyclic dinucleotide-manganese particles for local and systemic cancer metalloimmunotherapy. Nat Nanotechnol. 2021; 16(11): 1260-1270.
- 141Li Q, Yang M, Sun X, et al. NIR responsive nanoenzymes via photothermal ablation and hypoxia reversal to potentiate the STING-dependent innate antitumor immunity. Mater Today Bio. 2023; 19:100566.
- 142Ozlu B, Kabay G, Bocek I, et al. Controlled release of doxorubicin from polyethylene glycol functionalized melanin nanoparticles for breast cancer therapy: part I. production and drug release performance of the melanin nanoparticles. Int J Pharm. 2019; 570:118613.
- 143Liu D, Huang H, Zhao B, Guo W. Natural melanin-based nanoparticles with combined chemo/photothermal/photodynamic effect induce immunogenic cell death (ICD) on tumor. Front Bioeng Biotechnol. 2021; 9:635858.
- 144Yasothamani V, Karthikeyan L, Shyamsivappan S, Haldorai Y, Seetha D, Vivek R. Synergistic effect of photothermally targeted NIR-responsive nanomedicine-induced immunogenic cell death for effective triple negative breast cancer therapy. Biomacromolecules. 2021; 22(6): 2472-2490.
- 145Yasothamani V, Vivek R. Targeted NIR-responsive theranostic immuno-nanomedicine combined TLR7 agonist with immune checkpoint blockade for effective cancer photothermal immunotherapy. J Mater Chem B. 2022; 10(33): 6392-6403.
- 146Yang Y, Huang J, Liu M, et al. Emerging sonodynamic therapy-based nanomedicines for cancer immunotherapy. Adv Sci (Weinh). 2023; 10(2):e2204365.
- 147Lee J, Um W, Moon H, et al. Evading doxorubicin-induced systemic immunosuppression using ultrasound-responsive liposomes combined with focused ultrasound. Pharmaceutics. 2022; 14(12):2603.
- 148Ji C, Si J, Xu Y, et al. Mitochondria-targeted and ultrasound-responsive nanoparticles for oxygen and nitric oxide codelivery to reverse immunosuppression and enhance sonodynamic therapy for immune activation. Theranostics. 2021; 11(17): 8587-8604.
- 149Zheng J, Sun Y, Long T, et al. Sonosensitizer nanoplatform-mediated sonodynamic therapy induced immunogenic cell death and tumor immune microenvironment variation. Drug Deliv. 2022; 29(1): 1164-1175.
- 150Wang Y, Wang Z, Chen B, et al. Cooperative self-assembled nanoparticle induces sequential immunogenic cell death and toll-like receptor activation for synergistic chemo-immunotherapy. Nano Lett. 2021; 21(10): 4371-4380.
- 151Li J, Zhou S, Yu J, et al. Low dose shikonin and anthracyclines coloaded liposomes induce robust immunogenetic cell death for synergistic chemo-immunotherapy. J Control Release. 2021; 335: 306-319.
- 152Jia L, Pang M, Fan M, et al. A pH-responsive Pickering Nanoemulsion for specified spatial delivery of immune checkpoint inhibitor and chemotherapy agent to tumors. Theranostics. 2020; 10(22): 9956-9969.
- 153Ding M, Fan Y, Lv Y, et al. A prodrug hydrogel with tumor microenvironment and near-infrared light dual-responsive action for synergistic cancer immunotherapy. Acta Biomater. 2022; 149: 334-346.