1. CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, National Center for Nanoscience and Technology (NCNST), Beijing 100190, China 2. The Cancer Hospital of the University of Chinese Academy of Sciences (Zhejiang Cancer Hospital), Institute of Basic Medicine and Cancer (IBMC), Chinese Academy of Sciences, Hangzhou 310022, China 3. Beijing Key Laboratory of Molecular Pharmaceutics and New Drug Delivery Systems, School of Pharmaceutical Sciences, Peking University, Beijing 100191, China
Compared to conventional hyperthermia that is limited by low selectivity and severe side effects, nano-enabled hyperthermia yields great potentials to tackle these limitations for cancer treatment. Another major advance is the observation of immunological responses associated with nano-enabled hyperthermia, which introduces a new avenue, allowing a potential paradigm shift from the acutely effective and cytotoxicity-centric response to the next-phase discovery, i.e., long-lasting and/or systemic anti-tumor immunity. This perspective first discusses the temperature-gradient and the spatially-structured immunological landscape in solid tumors receiving nano-enabled hyperthermia. This includes the discussion about underlying mechanism such as immunogenic cell death, which initiates a profound immunological chain reaction. In order to propagate the immune activation as a viable therapeutic principle, we further discussed the tumor type-specific complexity in the immunological tumor microenvironment, including the creative design of nano-enabled combination therapy to synergize with nano-enabled hyperthermia.
Chitosan-coated hollow CuS NPs with immunoadjuvants oligodeoxynucleotides containing the cytosine-guanine (CpG) motifs
EMT6 breast cancer
i.t. (intratumorally injection)
The HCuSNPs-CpG-mediated photothermal immunotherapy elicits more effective systemic immune responses than immunotherapy or PTT alone, resulting in combined anticancer effects against primary treated as well as distant untreated tumors
[29]
NIR PTT
PEGylated SWNTs
4T1 breast cancer
i.t.
The PEGylated SWNTs mediated photothermal tumor destruction could release tumor-associated antigens and act as an immunological adjuvant to greatly promote maturation of DCs and production of anti-tumor cytokines. The combination of SWNT-based PTT with antiCTLA-4 therapy could modulate the adaptive immune responses especially cellular immunity for the treatment of metastatic cancer
[30]
NIR PTT
PEG and polyethylenimine (PEI) dual-polymer-functionalized GO (GO-PEG-PEI) carrying CpG
CT26 colon cancer
i.t.
The GO-PEG-PEI mediated photothermal effect enhanced immunostimulation responses of CpG, owing to the photothermally induced local heating that accelerated intracellular trafficking of nanovectors
[31]
NIR PTT
Poly(lactic-co-glycolic) acid (PLGA) NPs encapsulating NIR photothermal agent indocyanine green (ICG) and toll-like-receptor-7 agonist imiquimod (R837)
The photothermal ablation of primary tumours using PLGA-ICG-R837 NPs, generated tumour-associated antigens, which in the presence of R837-containing NPs as the adjuvant showed vaccine-like functions. In combination with anti-CTLA4, the generated immunological responses was able to attack remaining tumour cells in mice to inhibit metastasis. This strategy offered a strong immunological memory effect, which provided protection against tumour rechallenging post elimination of their initial tumours
[32]
NIR PTT
PEG coated plasmonic gold nanostar (GNS)
MB49 bladder cancer
i.t., i.v.
The GNS-mediated PTT combined with anti-PD-L1 were able to achieve complete eradication of primary treated tumors and distant untreated tumors in some mice with effective long-lasting immunity against MB49 cancer cells rechallenge
[33]
NIR PTT
Polydopamine-coated spiky AuNPs (SGNP@PDA)
CT26 colorectal cancer; TC-1 head and neck squamous cell carcinoma
i.t.
SGNP@PDA PTT combined with a sub-therapeutic chemo dose of doxorubicin (DOX), elicits robust anti-tumor responses in both cellular (CD8+ T and NK cells) and humoral compartments. Chemo-PTT eliminates residual tumor cells from locally treated tumors and exerts an abscopal effect against untreated, distant tumors, and also exhibits long-term resistance against tumor rechallenge due to the establishment of immunological memory
[34]
NIR PTT
MDSC membrane-coated iron oxide MNP (MNP@MDSC)
B16-F10 melanoma
i.v.
MNPs@MDSC mediated PTT effects enhanced antitumor response by inducing ICD, reprogramming the tumor infiltrating macrophages, and reducing the tumor’s metabolic activity
IR820-hydrogel mediated PTT induced tumor antigens release for enhancing the immunotherapy effect. CpG NPs serve as adjuvant to improve the immune stimulation. The combined specific antitumor immunity achieved more effective systemic therapeutic effect than PTT or immunotherapy alone
[36]
NIR PTT
Intracellularly generated AuNPs
B16F10 Melanoma 4T1 breast cancer
s.c.
The AuNPs were generated intracellularly and then exocytosed as nanoparticle trapped vesicles with retained original bioinformation. After further introduction to DCs, DCs-derived immunological AuNPs induced HT under NIR irradiation and provoked strong antitumor immune responses, promoting DCs maturation, multiple cytokines secretion, and T cells activation
[37]
Magnetic HT
PEGylated iron NPs (FeNPs)
4T1 breast cancer CT26 colon cancer
i.t.
The combination of FeNP-based MHT with local injection of nanoadjuvant and systemic injection of anti-CTLA4 checkpoint blockade would result in systemic therapeutic responses to inhibit tumor metastasis and a robust immune memory effect to prevent tumor recurrence
[38]
NIR PTT
Mesoporous silica NPs decorated with AuNPs (Au@XL-MSNs) loaded with CpG-ODNs
4T1 breast cancer
i.t.
The photothermal effect of AuNPs enhanced cancer immunotherapy by generating a cancer antigen at the tumor site, which can be processed by tumor-infiltrated DCs and induce antigen-specific adaptive immune response
[39]
NIR(II) PTT
Self-assembly complex of liposome with AuNPs; two-dimensional polypyrrole nanosheets
4T1 breast cancer
i.v.
PTT effect induced by NIR(II) light could trigger ICD more homogeneously and deeper than NIR(I) and red light, and more effective than oxaliplatin in solid tumors. The NIR(II) PTT provoked innate and adaptive immunity led to efficient antitumor and anti-metastasis effects when combined with checkpoint blockade therapy
The CP NPs mediated photothermal effect demonstrated effective activation of proinflammatory immune response, induced antitumor immunity activation and ultimately inhibited tumor growth
[41]
NIR PTT
M NPs coated with cancer cell membrane (M@C NPs)
4T1 breast cancer
i.v.
M@C NPs mediated PTT effects enhanced antitumor immune response by inducing ICD, which led to good therapeutic effect for primary and abscopal tumor when combined with immunoblocking inhibitor
[42]
Tab.1
Fig.1
Fig.2
Fig.3
Fig.4
Fig.5
Fig.6
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