A biomimetic nanoplatform for customized photothermal therapy of HNSCC evaluated on patient-derived xenograft models

Abstract

Cancer cell membrane (CCM) derived nanotechnology functionalizes nanoparticles (NPs) to recognize homologous cells, exhibiting translational potential in accurate tumor therapy. However, these nanoplatforms are majorly generated from fixed cell lines and are typically evaluated in cell line-derived subcutaneous-xenografts (CDX), ignoring the tumor heterogeneity and differentiation from inter- and intra- individuals and microenvironments between heterotopic- and orthotopic-tumors, limiting the therapeutic efficiency of such nanoplatforms. Herein, various biomimetic nanoplatforms (CCM-modified gold@Carbon, i.e., Au@C-CCM) were fabricated by coating CCMs of head and neck squamous cell carcinoma (HNSCC) cell lines and patient-derived cells on the surface of Au@C NP. The generated Au@C-CCMs were evaluated on corresponding CDX, tongue orthotopic xenograft (TOX), immune-competent primary and distant tumor models, and patient-derived xenograft (PDX) models. The Au@C-CCM generates a photothermal conversion efficiency up to 44.2% for primary HNSCC therapy and induced immunotherapy to inhibit metastasis via photothermal therapy-induced immunogenic cell death. The homologous CCM endowed the nanoplatforms with optimal targeting properties for the highest therapeutic efficiency, far above those with mismatched CCMs, resulting in distinct tumor ablation and tumor growth inhibition in all four models. This work reinforces the feasibility of biomimetic NPs combining modular designed CMs and functional cores for customized treatment of HNSCC, can be further extended to other malignant tumors therapy.

References

[1.] Ju Y, . Nanostructured particles assembled from natural building blocks for advanced therapies. Chem. Soc. Rev., 2022, 51: 4287-4336.

[2.] Guo X, . Mito-Bomb: targeting mitochondria for cancer therapy. Adv. Mater., 2021, 33: e2007778.

[3.] Huang X, . Right Cu_2-xS@MnS core-shell nanoparticles as a photo/HO-responsive platform for effective cancer theranostics. Adv. Sci., 2019, 6: 1901461.

[4.] Cramer JD, Burtness B, Le QT, Ferris RL. The changing therapeutic landscape of head and neck cancer. Nat. Rev. Clin. Oncol., 2019, 16: 669-683.

[5.] Kaidar-Person O, Gil Z, Billan S. Precision medicine in head and neck cancer. Drug Resist. Updat., 2018, 40: 13-16.

[6.] Lai X, . Light-triggered efficient sequential drug delivery of biomimetic nanosystem for multimodal Chemo-, antiangiogenic, and anti-MDSC therapy in melanoma. Adv. Mater., 2022, 34: e2106682.

[7.] Xu X, . Fabrication of methylene blue-loaded ovalbumin/polypyrrole nanoparticles for enhanced phototherapy-triggered antitumour immune activation. J. Nanobiotechnology, 2022, 20

[8.] Lu L, . Polymer chimera of stapled oncolytic peptide coupled with anti-PD-L1 peptide boosts immunotherapy of colorectal cancer. Theranostics, 2022, 12: 3456-3473.

[9.] Kadria-Vili Y, . GdO-mesoporous silica/gold nanoshells: a potential dual/contrast agent for MRI-guided localized near-IR photothermal therapy. Proc. Natl Acad. Sci. USA, 2022, 119: e2123527119.

[10.] Liang S, Liao G, Zhu W, Zhang L. Manganese-based hollow nanoplatforms for MR imaging-guided cancer therapies. Biomater. Res., 2022, 26

[11.] Li X, Lovell JF, Yoon J, Chen X. Clinical development and potential of photothermal and photodynamic therapies for cancer. Nat. Rev. Clin. Oncol., 2020, 17: 657-674.

[12.] Zhang Y, . Photoelectrochemical immunosensor for the sensitive detection of neuron-specific enolase based on the effect of Z-scheme WO/NiCoO nanoarrays p-n heterojunction. Biosens. Bioelectron., 2022, 213: 114452.

[13.] Zhang F, . Cu₂O induced Au nanochains for highly sensitive dual-mode detection of hydrogen sulfide. J. Hazard Mater., 2022, 436: 129144.

[14.] Shao H, . Efficient radiative enhancement in perovskite light-emitting devices through involving a novel sandwich localized surface plasmon structure. Small Methods, 2022, 6: e2200163.

[15.] Wang Y, . In situ investigation of ultrafast dynamics of hot electron-driven photocatalysis in plasmon-resonant grating structures. J. Am. Chem. Soc., 2022, 144: 3517-3526.

[16.] Camargo FVA, . Visualizing ultrafast electron transfer processes in semiconductor-metal hybrid nanoparticles: toward excitonic-plasmonic light harvesting. Nano Lett., 2021, 21: 1461-1468.

[17.] Jia J, . Fine-tuning the homometallic interface of Au-on-Au nanorods and their photothermal therapy in the NIR-II window. Angew. Chem. Int. Ed. Engl., 2020, 59: 14443-14448.

[18.] Rastinehad AR, . Gold nanoshell-localized photothermal ablation of prostate tumors in a clinical pilot device study. Proc. Natl Acad. Sci. USA, 2019, 116: 18590-18596.

[19.] Cameron SJ, Sheng J, Hosseinian F, Willmore WG. Nanoparticle effects on stress response pathways and nanoparticle-protein interactions. Int. J. Mol. Sci., 2022, 23: 7962.

[20.] Dagogo-Jack I, Shaw AT. Tumour heterogeneity and resistance to cancer therapies. Nat. Rev. Clin. Oncol., 2018, 15: 81-94.

[21.] Shi J, Kantoff PW, Wooster R, Farokhzad OC. Cancer nanomedicine: progress, challenges and opportunities. Nat. Rev. Cancer, 2017, 17: 20-37.

[22.] Ouyang B, . The dose threshold for nanoparticle tumour delivery. Nat. Mater., 2020, 19: 1362-1371.

[23.] Paul A, . Cell adhesion molecule KIRREL1 is a feedback regulator of Hippo signaling recruiting SAV1 to cell-cell contact sites. Nat. Commun., 2022, 13

[24.] Chen Z, . Cancer cell membrane-biomimetic nanoparticles for homologous-targeting dual-modal imaging and photothermal therapy. ACS Nano, 2016, 10: 10049-10057.

[25.] Rao L, . Cancer cell membrane-coated upconversion nanoprobes for highly specific tumor imaging. Adv. Mater., 2016, 28: 3460-3466.

[26.] Guo Y, Cao X, Zhang S. Au-Fe₃O₄ nanoagent coated cell membrane for targeted delivery and enhanced chem/photo therapy. Chem. Commun., 2021, 57: 10504-10507.

[27.] Wang R, . Biomimetic upconversion nanoparticles and gold nanoparticles for novel simultaneous dual-modal imaging-guided photothermal therapy of cancer. Cancers, 2020, 12: 3136.

[28.] Zhang D, . Cell membrane coated smart two-dimensional supraparticle for in vivo homotypic cancer targeting and enhanced combinational theranostics. Nanotheranostics, 2021, 5: 275-287.

[29.] Smolina M, Goormaghtigh E. FTIR imaging of the 3D extracellular matrix used to grow colonies of breast cancer cell lines. Analyst, 2016, 141: 620-629.

[30.] Yang D, . Assembly of Au plasmonic photothermal agent and iron oxide nanoparticles on ultrathin black phosphorus for targeted photothermal and photodynamic cancer therapy. Adv. Funct. Mater., 2017, 27: 1700371.

[31.] Shanmugam V, Selvakumar S, Yeh CS. Near-infrared light-responsive nanomaterials in cancer therapeutics. Chem. Soc. Rev., 2014, 43: 6254-6287.

[32.] Nozdriukhin D, . Rapid volumetric optoacoustic tracking of individual microparticles in vivo enabled by a NIR-absorbing gold-carbon shell. ACS Appl. Mater. Interfaces, 2021, 13: 48423-48432.

[33.] Nozdriukhin D, . Gold nanoparticle-carbon nanotube multilayers on silica microspheres: optoacoustic-Raman enhancement and potential biomedical applications. Mater. Sci. Eng. C. Mater. Biol. Appl., 2021, 120: 111736.

[34.] Proctor DM, Relman DA. The landscape ecology and microbiota of the human nose, mouth, and throat. Cell Host Microbe, 2017, 21: 421-432.

[35.] Hoffman RM. Orthotopic is orthodox: why are orthotopic-transplant metastatic models different from all other models?. J. Cell Biochem., 1994, 56: 1-3.

[36.] Lofgren J, . Analgesics promote welfare and sustain tumour growth in orthotopic 4T1 and B16 mouse cancer models. Lab Anim., 2018, 52: 351-364.

[37.] Ozasa R, Ohno J, Iwahashi T, Taniguchi K. Tumor-induced lymphangiogenesis in cervical lymph nodes in oral melanoma-bearing mice. J. Exp. Clin. Cancer Res., 2012, 31: 83.

[38.] Ferdinandus, . Modulation of local cellular activities using a photothermal dye-based subcellular-sized heat spot. ACS Nano, 2022, 16: 9004-9018.

[39.] Lee NP, . Tumor xenograft animal models for esophageal squamous cell carcinoma. J. Biomed. Sci., 2018, 25: 66.

[40.] Decaudin D. Primary human tumor xenografted models (‘tumorgrafts’) for good management of patients with cancer. Anticancer Drugs, 2011, 22: 827-841.

[41.] Stewart EL, . Clinical utility of patient-derived xenografts to determine biomarkers of prognosis and map resistance pathways in EGFR-mutant lung adenocarcinoma. J. Clin. Oncol., 2015, 33: 2472-2480.

[42.] Hidalgo M, . Patient-derived xenograft models: an emerging platform for translational cancer research. Cancer Disco., 2014, 4: 998-1013.

[43.] Lopez-Mendez TB, . Cell microencapsulation technologies for sustained drug delivery: latest advances in efficacy and biosafety. J. Control. Release, 2021, 335: 619-636.

[44.] Garcia S, Trinh CT. Modular design: implementing proven engineering principles in biotechnology. Biotechnol. Adv., 2019, 37: 107403.

[45.] Chen J, . Furin-instructed intracellular gold nanoparticle aggregation for tumor photothermal therapy. Adv. Funct. Mater., 2020, 30: 2001566.

[46.] Ogarev VA, Rudoi VM, Dement’eva OV. Gold nanoparticles: synthesis, optical properties, and application. Inorg. Mater. Appl. Res., 2018, 9: 134-140.

[47.] Dreaden EC, . Beating cancer in multiple ways using nanogold. Chem. Soc. Rev., 2011, 40: 3391-3404.

[48.] Wang Y, . Comparison study of gold nanohexapods, nanorods, and nanocages for photothermal cancer treatment. ACS Nano, 2013, 7: 2068-2077.

[49.] Yu N, . Dopant-dependent crystallization and photothermal effect of Sb-doped SnO₂ nanoparticles as stable theranostic nanoagents for tumor ablation. Nanoscale, 2018, 10: 2542-2554.

[50.] Schmidt RM, . Quantifying radiosensitization of PSMA-targeted gold nanoparticles on prostate cancer cells at megavoltage radiation energies by Monte Carlo simulation and local effect model. Pharmaceutics, 2022, 14: 2205.

[51.] Fang RH, Gao W, Zhang L. Targeting drugs to tumours using cell membrane-coated nanoparticles. Nat. Rev. Clin. Oncol., 2022

[52.] Glinsky VV, . Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium. Cancer Res., 2003, 63: 3805-3811.

[53.] Hu CM, . Nanoparticle biointerfacing by platelet membrane cloaking. Nature, 2015, 526: 118-121.

[54.] Yu B, . Reassembly of (89) ZR-labeled Cancer Cell Membranes Into Multicompartment Membrane-derived Liposomes for PET-trackable tumor-targeted theranostics. Adv. Mater., 2018, 30: e1704934.

[55.] Fang RH, . Cancer cell membrane-coated nanoparticles for anticancer vaccination and drug delivery. Nano Lett., 2014, 14: 2181-2188.

[56.] Wu Y, . Stapled wasp venom-derived oncolytic peptides with side chains induce rapid membrane lysis and prolonged immune responses in melanoma. J. Med. Chem., 2021, 64: 5802-5815.

[57.] Gu Z, . Pharmacogenomic landscape of head and neck squamous cell carcinoma informs precision oncology therapy. Sci. Transl. Med., 2022, 14: eabo5987.

[58.] Liu X, . Conditional reprogramming and long-term expansion of normal and tumor cells from human biospecimens. Nat. Protoc., 2017, 12: 439-451.

[59.] Han Y, . Repurposing ponatinib as a potent agent against KIT mutant melanomas. Theranostics, 2019, 9: 1952-1964.

[60.] Morvan VL, . Cytochrome P450 1B1 polymorphism drives cancer cell stemness and patient outcome in head-and-neck carcinoma. Brit. J. Cancer, 2020, 123: 772-784.

[61.] Yao Y, . Clinical utility of PDX cohorts to reveal biomarkers of intrinsic resistance and clonal architecture changes underlying acquired resistance to cetuximab in HNSCC. Signal Transduct. Target Ther., 2022, 7: 73.

[62.] Ruan S, . Integrin β4-targeted cancer immunotherapies inhibit tumor growth and decrease metastasis. Cancer Res., 2020, 80: 771-783.

[63.] Choi J, . Visible-light-triggered prodrug nanoparticles combine chemotherapy and photodynamic therapy to potentiate checkpoint blockade cancer immunotherapy. ACS Nano, 2021

[64.] Zhang Y, . Plasmonic modulation of gold nanotheranostics for targeted NIR-II photothermal-augmented immunotherapy. Nano Today, 2020, 35: 100987.

[65.] Wicker CA, . Glutaminase inhibition with telaglenastat (CB-839) improves treatment response in combination with ionizing radiation in head and neck squamous cell carcinoma models. Cancer Lett., 2021, 502: 180-188.

[66.] Sano D, . Disruptive TP53 mutation is associated with aggressive disease characteristics in an orthotopic murine model of oral tongue cancer. Clin. Cancer Res., 2011, 17: 6658-6670.

Funding

National Natural Science Foundation of China (National Science Foundation of China)(81872199, 82002853); Key Program of National Natural Science Foundation of China (82030085)； “Shuguang Program” supported by Shanghai Education Development Foundation and Shanghai Municipal Education Commission (19SG13); Innovative Research Team of High-level Local Universities in Shanghai (SHSMU-ZLCX20212300, SSMU-ZLCX20180500)