Nanomaterial-Based Tumor Photothermal Immunotherapy

Figures & data

Figure 1 (A) Schematic illustration of nanoparticle-based PTT. Reproduced from Riley RS, Day ES. Gold nanoparticle-mediated photothermal therapy: applications and opportunities for multimodal cancer treatment. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2017;9(4):1449. Copyright 2017, John Wiley and Sons.⁸⁸ (B) Four major photothermal agents for PTT, including gold nanoparticles, carbon nanomaterials, semiconductor nanomaterials and organic NIR dyes.Reprouduced from Kim H, Beack S, Han S, et al. Multifunctional photonic nanomaterials for diagnostic, therapeutic, and theranostic applications. Adv Mater. 2018;30(10):1701460.Copyright 2018, John Wiley and Sons.⁹⁷

Figure 2 (A) Mechanism of apoptosis after NIR laser-irradiation. Reproduced with permission from Pérez-Hernández M, Del Pino P, Mitchell SG, et al. Dissecting the molecular mechanism of apoptosis during photothermal therapyusing gold nanoprisms. ACS Nano. 2015;9(1):52–61.¹¹⁶ Copyright 2015, American Chemical Society. (B) Schematic illustration of HSP70 inhibitor optimized PTT. Reproduced with permission  from Ali MRK, Ali HR, Rankin CR, et al. Targeting heat shock protein70 using gold nanorods enhances cancer cell apoptosis in lowdose plasmonic photothermal therapy. Biomaterials. 2016;102:1–8. .¹²⁸ Copyright 2016, Elsevier.

Figure 3 The Cells in the Tumor Microenvironment. Reproduced with permission from Hanahan D, Weinberg RA. Hallmarks of cancer: the nextgeneration. Cell. 2011;144(5):646–674.¹⁴⁰ Copyright 2011, Elsevier.

Figure 4 Characteristics of immunogenic cell death (ICD). Reproduced with permission from Duan X, Chan C, LinW. Nanoparticle-mediated immunogenic celldeath enables and potentiates cancer immunotherapy. Angew ChemInt Ed Engl. 2019;58(3):670–680.¹⁶³ Copyright 2019, John Wiley and Sons.

Figure 5 PTT generates ICD when an optimal thermal dose is administered to tumors. Reproduced with permission from Sweeney EE, Cano-Mejia J, Fernandes R. Photothermal therapy generatesa thermal window of immunogenic cell death in neuroblastoma. Small. 2018;14(20):1800678..¹⁶⁴ Copyright 2018, John Wiley and Sons.

Figure 6 Schematics diagram of combined photothermal and immunotherapy using chitosan-coated hollow copper sulfide nanoparticles. Reproduced with permission from Guo L, Yan DD, Yang D, et al. Combinatorial photothermal andimmuno cancer therapy using chitosan-coated hollow coppersulfide nanoparticles. ACS Nano. 2014;8(6):5670–5681.¹⁷¹ Copyright 2014, American Chemical Society.

Table 1 Photothermal Nanomaterials Combined with Immunoadjuvants for Photothermal Immunotherapy

Photothermal Nanoparticles	Immunoadjuvants	Effector Cells	Cytokines	Tumors	References
GNR	CpG	–	TNF-α, IL-6	Murine hepatocellular carcinoma cell H22	[^Citation188]
GNR-DNA hydrogels	CpG	–	TNF-α, IL-6, IL-12p40, IFN-γ	Murine T lymphoma cell EG7-OVA	[^Citation168]
Ovalbumin assembled gold nanorods (OVA-GNR)	CpG	DCs, CD8^+ T cells	IL-6, IL-12, IL-1β	Murine breast cancer cell 4T1	[^Citation189]
Bovine serum albumin coated gold nanorods (BSA-GNRs)	R837	DCs, CD8^+ T cells	TNF-α, IL-6, IL-12	Murine melanoma cell B16-F10	[^Citation166]
GNR-PEI	CpG	DCs, CD8+ T cells, CD4+ T cells	–	Murine breast cancer cell 4T1	[^Citation190]
Gold nanoshell	CpG	DCs, CD8^+ T cells, CD4^+ T cells	IL-2, IL-6, IFN-γ	Murine gastric cancer cell MFC	[^Citation167]
NIR heptamethine cyanine dye IR-7 loaded liposomes (IR-7-lipo)	CpG	DCs, CD8^+ T cells, CD4^+ T cells	TNF-α, IL-6, IL-12	Murine colon cancer cell CT26	[^Citation174]
IR820-hydrogel	CpG	DCs, CD8^+ T cells	TNF-α, IL-2, IFN-γ	Murine melanoma cell B16	[^Citation175]
IR820 thermosensitive liposomes (IR820-TSL)	R837	DCs	TNF-α, IL-12p70, IFN- γ	Murine gastric cancer cell MFC	[^Citation191]
Single-walled carbon nanotube (SWNTs)	Glycated Chitosan (GC)	–	DAMPs	Murine breast cancer cell EMT6	[^Citation169]
Graphene oxide sheets conjugated with PEI and PEG (GO-PEG-PEI)	CpG	–	TNF-α, IL-6	Murine colon cancer cell CT26	[^Citation170]
Mitochondria-Targeted Nanographene	CpG	–	TNF-α, IL-6, IL-12, INF-γ	Murine breast cancer cell EMT6	[^Citation192]
Polydopamine coated graphene quantum dots (GQD-PDA)	CpG	DCs, CD8^+ T cells, CD4^+ T cells	TNF-α, IL-6	Murine breast cancer cell EMT6	[^Citation193]
Chitosan-coated hollow CuS nanoparticles (HCuSNPs-Chitosan)	CpG	DCs, CD8^+ T cells, NK cells	IL-2, IFN-γ	Murine breast cancer cell EMT6	[^Citation171]
MoS2 nanosheets	CpG	DCs	TNF-α, IL-6	Murine breast cancer cell 4T1	[^Citation194]
Lipopolysaccharide coated copper sulfide nanoparticles (LPS-CuS)	Lipopolysaccharide (LPS)	DCs	TNF-α, IL-6, IL-12p40, IFN-γ	Murine colon cancer cell CT26	[^Citation172]
Polydopamine coated Al2O3 nanoparticles (PDA-Al2O3)	CpG	DCs	TNF-α, IFN-γ	Murine melanoma cell B16-F10	[^Citation195]
Folic acid coated polydopamine nanoparticles (FA-PDA)	R837	DCs	TNF-α, IL-12p40	Murine hepatocellular carcinoma cell H22	[^Citation196]
Prussian blue nanoparticles (PBNPs)	CpG	DCs, CD8^+ T cells	–	Murine neuroblastoma cell Neuro2a	[^Citation197]

Figure 7 Schematic diagram of nanoparticle-based PTT together with anti-CTLA-4. Reproduced with permission from Wang C, Xu L, Liang C, et al. Immunological responses triggeredby photothermal therapy with carbon nanotubes in combination with anti-CTLA-4 therapy to inhibit cancermetastasis. Adv Mater. 2014;26(48):8154–8162..¹⁸⁰ Copyright 2014, John Wiley and Sons.

Figure 8 Schematic diagram of nanoparticle-based PTT together with anti-PD-L1. Reproduced from Liu Y, Maccarini P, Palmer GM, et al. Synergistic immuno photothermal nanotherapy (SYMPHONY) for the treatment of unre-sectable and metastatic cancers. Sci Rep. 2017;7(1):8606. Creative Commons license and disclaimer available from: (http://creativecommons.org/licenses/by/4.0/legalcode„http://creativecommons.org/licenses/by/4.0/legalcode).¹⁸²

Table 2 Photothermal Nanomaterials Combined with Immune Checkpoint Inhibitors for Photothermal Immunotherapy

Photothermal Nanoparticles	Checkpoint Blockade	Effector Cells	Cytokines	Tumors	References
Gold nanostar (GNS)	Anti-PD-L1	CD8^+ T cells, CD4^+ T cells, B cells	–	Murine bladder cancer cells MB49	[^Citation182]
Hollow gold nanoshell (HAuNS)	Anti-PD-1	CD8^+ T cells, CD4^+ T cells	TNF-α, IL-2, IFN-γ	Murine breast cancer cell 4T1, murine colon cancer cell CT26	[^Citation198]
Au@Pt nanoparticles	Anti-PD-L1	CD8^+ T cells, CD4^+ T cells	TNF-α, IL-6, IL-12p70, IFN-γ	Murine breast cancer cell 4T1	[^Citation199]
IR780 micelles	IDO	CD8^+ T cells, CD4^+ T cells	–	Murine breast cancer cell 4T1	[^Citation200]
ICG Hydrogel	Anti-PD-L1	DCs, CD8^+ T cells	TNF-α, IL-6, IFN-γ	Murine breast cancer cell 4T1	[^Citation201]
NIR dyes IR820	Anti-PD-L1	CD8^+ T cells, CD4^+ T cells	TNF-α, IL-6, IL-12p70, IFN-γ	Murine breast cancer cell 4T1	[^Citation183]
IRDye800CW	Anti-PD-L1	CD8^+ T cells	TNF-α, IL-2, IL-4, IL-6, IL-1β, IFN- γ	Murine breast cancer cell 4T1	[^Citation202]
Single-walled nanotubes (SWNTs)	Anti-CTLA-4	DCs, CD8^+ T cells, CD4^+ T cells, CD20^+ T cells	TNF-α, IL-6, IL-12, IL-1β	Murine breast cancer cell 4T1, murine melanoma cell B16	[^Citation180]
Black phosphorus quantum dots (BPQDs)	Anti-PD-1	DCs, CD8^+ T cells, CD4^+ T cells	TNF-α, IFN-γ	Murine breast cancer cell 4T1, murine melanoma cell B16F10	[^Citation203]
Red blood cell membranes coated black phosphorus quantum dot nanovesicles (BPQD-RMNVs)	Anti-PD-1	DCs, CD8^+ T cells, CD4^+ T cells	TNF-α, IFN-γ	Murine breast cancer cell 4T1	[^Citation204]
Prussian blue nanoparticle (PBNP)	Anti-CTLA-4	CD8^+ T cells, CD4^+ T cells	–	Murine neuroblastoma cell Neuro2a	[^Citation181]
Hollow gold nanoshells (HAuNS)	Anti-PD-1	DCs, CD8^+ T cells	TNF-α, IL-2, IL-12p70, IFN-γ	Murine breast cancer cell 4T1, murine colon cancer cell CT26	[^Citation205]
Reduced graphene oxide (rGO)-based nanosheets	Anti-PD-L1 and IDO	DCs, CD45^+ leukocytes, CD8^+ T cells, CD4^+ T cells, NK cells	IFN-γ	Murine colon cancer cell CT26	[^Citation206]
Single-walled carbon nanotube (SWNT)	Anti-CTLA-4 and glycated chitosan (GC)	DCs, CD8^+ T cells	IFN-γ	Murine breast cancer cell 4T1	[^Citation185]
Fe3O4-R837 spherical superparticles(SPs)SPs	Anti-PD-L1 and R837	DCs, CD8^+ T cells, CD4^+ T cells, NK cells, B cells	TNF-α, IL-6, IFN-γ	Murine breast cancer cell 4T1	[^Citation207]
PLGA-ICG-R837	Anti-CTLA-4 and R837	DCs, CD8^+ T cells	TNF-α, IL-6, IL-12p70, IFN-γ	Murine breast cancer cell 4T1, murine colon cancer cell CT26	[^Citation184]
PEG modified PDA loaded with carbon dots (PDA-PEG-CD)	Anti-PD-L1 and R848	CD8^+ T cells	TNF-α, IFN-γ	Murine breast cancer cell 4T1	[^Citation208]

Figure 9 Schematic diagram of PTT with immunoadjuvant nanoparticles together with anti-CTLA-4. Reproduced with permissionfrom Chen Q, Xu L, Liang C, et al. Photothermal therapy withimmune-adjuvant nanoparticles together with checkpoint blockadefor effective cancer immunotherapy. Nat Commun. 2016;7(1):13193. Creative Commons license and disclaimer available from: (http://creativecommons.org/licenses/by/4.0/legalcode„http://creativecommons.org/licenses/by/4.0/legalcode).¹⁸⁴

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