GM-CSF augmented the photothermal immunotherapeutic outcome of self-driving gold nanoparticles against a mouse CT-26 colon tumor model

Biomaterials Research - Tập 27 - Trang 1-17 - 2023
Jie Dai1, Jianmei Li1, Yuqin Zhang1, Qian Wen1, Yun Lu1, Yu Fan1, Fancai Zeng2, Zhiyong Qian3, Yan Zhang4, Shaozhi Fu1,5
1Department of Oncology, The Affiliated Hospital of Southwest Medical University, Luzhou, P. R. China
2Laboratory of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Southwest Medical University, Luzhou, P.R. China
3State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Collaborative Innovation Center for Biotherapy, Sichuan University, Chengdu, P.R. China
4Department of Oncology, the Affiliated Traditional Chinese Medicine Hospital of Southwest Medical University, Luzhou, P.R. China
5Nuclear Medicine and Molecular Imaging Key Laboratory of Sichuan Province, Luzhou, P.R. China

Tóm tắt

Hypoxia is a frequent characteristic observed in solid tumors and is strongly associated with tumor metastasis, angiogenesis, and drug resistance. While the vasculature of hypoxic tumor tissues poses obstacles to the efficient administration of conventional drugs, it may prove advantageous in sustaining hyperthermia. Photothermal therapy (PTT) offers a promising treatment strategy that utilizes the activation of photosensitizers to produce heat, thus facilitating the selective ablation of tumor tissues. To enhance the accumulation of photothermal agents in tumor tissue and improve the effectiveness of PTT, we developed a self-propelled hybrid called Bif@PAu-NPs. This hybrid consists of polydopamine (PDA)-coated gold nanoparticles (Au-NPs) loaded onto the anaerobic Bifidobacterium infantis (Bif). The Bif@PAu-NPs actively aggregated at the tumor site because the ability of Bif can target hypoxic regions, and PAu-NPs achieved precise PTT due to their high photothermal conversion efficiency (η = 67.8%). The tumor tissues were ablated by PTT, resulting in the release of antigens through immunogenic cell death (ICD), which stimulates an immune response. The inclusion of GM-CSF enhanced the immune response by recruiting dendritic cells and initiating long-term anti-tumor immunity. The Bif@PAu-NPs hybrid effectively suppressed the growth of both primary tumors and re-challenged tumors. The utilization Bif@PAu-NPs in conjunction with GM-SCF exhibits great potential as a photothermal-immunotherapeutic strategy for precisely treating solid tumors. In this study, the bacterial Bif@PAu-NPs biohybrid is exploited the self-driving ability of anaerobic Bifidobacterium infantis to deliver polydopamine-modified gold nanoparticles to hypoxic region of tumor. Under irradiation with 808 nm NIR laser, the hybrid exerts precise photothermal therapy to stimulate the immune response, which is further enhanced by GM-CSF, leading to recruitment of dendritic cells and initiation of a long-term anti-tumor immunity remember to prevent tumor recurrence.

Tài liệu tham khảo

Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and Mortality Worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49. Gotwals P, Cameron S, Cipolletta D, et al. Prospects for combining targeted and conventional cancer therapy with immunotherapy. Nat Rev Cancer [Internet]. 2017;17:286–301. Ramakrishnan R, Gabrilovich DI. Novel mechanism of synergistic effects of conventional chemotherapy and immune therapy of cancer. Cancer Immunol Immunother. 2013;62:405–10. Zhu JY, Zheng DW, Zhang MK, et al. Preferential Cancer Cell Self-Recognition and Tumor Self-Targeting by Coating Nanoparticles with Homotypic Cancer cell membranes. Nano Lett. 2016;16:5895–901. Hangauer MJ, Viswanathan VS, Ryan MJ, et al. Drug-tolerant persister cancer cells are vulnerable to GPX4 inhibition. Nat [Internet]. 2017;551:247–50. Smith TT, Moffett HF, Stephan SB, et al. Biopolymers codelivering engineered T cells and STING agonists can eliminate heterogeneous tumors. J Clin Invest. 2017;127:2176–91. Sun H, Zhang Y, Zhong Z. Reduction-sensitive polymeric nanomedicines: an emerging multifunctional platform for targeted cancer therapy. Adv Drug Deliv Rev [Internet]. 2018;132:16–32. Liu Z, Jiang W, Nam J, et al. Immunomodulating Nanomedicine for Cancer Therapy. Nano Lett. 2018;18:6655–9. Goldberg MS. Improving cancer immunotherapy through nanotechnology. Nat Rev Cancer [Internet]. 2019;19:587–602. Vines JB, Yoon JH, Ryu NE, et al. Gold nanoparticles for photothermal cancer therapy. Front Chem. 2019;7:1–16. Tay ZW, Chandrasekharan P, Chiu-Lam A, et al. Magnetic particle imaging-guided heating in vivo using Gradient Fields for arbitrary localization of magnetic hyperthermia therapy. ACS Nano. 2018;12:3699–713. Galluzzi L, Vitale I, Aaronson SA, et al. Molecular mechanisms of cell death: recommendations of the nomenclature Committee on Cell Death 2018. Cell Death Differ. 2018;25:486–541. Krysko DV, Garg AD, Kaczmarek A, et al. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer [Internet]. 2012;12:860–75. Lu J, Liu X, Liao YP, Wang X, et al. Breast Cancer chemo-immunotherapy through liposomal delivery of an immunogenic cell death stimulus plus interference in the IDO-1 pathway. ACS Nano. 2018;12:11041–61. Zhou C, Zhang L, Sun T, et al. Activatable NIR-II Plasmonic Nanotheranostics for efficient photoacoustic imaging and Photothermal Cancer Therapy. Adv Mater. 2021;33:1–11. Li JJ, Hartono D, Ong CN, et al. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials [Internet]. 2010;31:5996–6003. Dreyer DR, Miller DJ, Freeman BD, et al. Elucidating the structure of poly(dopamine). Langmuir. 2012;28:6428–35. Lee H, Dellatore SM, Miller WM, et al. Mussel-inspired surface chemistry for multifunctional coatings. Science. 2007;318(5849):426–30. Tian Y, Younis MR, Zhao Y, et al. Precision Delivery of Dual Immune inhibitors loaded Nanomodulator to reverse Immune suppression for Combinational Photothermal-Immunotherapy. Small. 2023;2206441:1–14. Chen W, Qin M, Chen X, et al. Combining photothermal therapy and immunotherapy against melanoma by polydopamine-coated Al2O3 nanoparticles. Theranostics. 2018;8:2229–41. Liu Y, Ai K, Lu L. Polydopamine and its derivative materials: synthesis and promising applications in energy, environmental, and biomedical fields. Chem Rev. 2014;114:5057–115. D’Ischia M, Napolitano A, Ball V, et al. Polydopamine and eumelanin: from structure-property relationships to a unified tailoring strategy. Acc Chem Res. 2014;47:3541–50. Ku SH, Ryu J, Hong SK, et al. General functionalization route for cell adhesion on non-wetting surfaces. Biomaterials [Internet]. 2010;31:2535–41. Hafner D, Ziegler L, Ichwan M, et al. Mussel-inspired polymer carpets: direct photografting of polymer brushes on polydopamine nanosheets for controlled cell adhesion. Adv Mater. 2016;28:1489–94. Cheng W, Zeng X, Chen H, et al. Versatile polydopamine platforms: synthesis and promising applications for Surface Modification and Advanced Nanomedicine. ACS Nano. 2019;13:8537–65. Corbet C, Feron O. Tumour acidosis: from the passenger to the driver’s seat. Nat Rev Cancer. 2017;17:577–93. Singleton DC, Macann A, Wilson WR. Therapeutic targeting of the hypoxic tumour microenvironment. Nat Rev Clin Oncol [Internet]. 2021;18:751–72. Zheng DW, Chen Y, Li ZH, et al. Optically-controlled bacterial metabolite for cancer therapy. Nat Commun. 2018;9:1–12. Deng X, Yang W, Shao Z, et al. Genetically modified bacteria for targeted phototherapy of tumor. Biomaterials [Internet]. 2021;272:120809. Yi X, Zhou H, Chao Y, et al. Bacteria-triggered tumor-specific thrombosis to enable potent photothermal immunotherapy of cancer. Sci Adv. 2020;6:1–12. Liu L, He H, Luo Z, et al. In situ photocatalyzed oxygen generation with photosynthetic Bacteria to Enable Robust Immunogenic Photodynamic Therapy in Triple-Negative breast Cancer. Adv Funct Mater. 2020;30:1–14. Lu D, Wang L, Wang L, et al. Probiotic Engineering and targeted Sonoimmuno-Therapy augmented by STING agonist. Adv Sci. 2022;9:1–12. Xiao S, Shi H, Zhang Y, et al. Bacteria-driven hypoxia targeting delivery of chemotherapeutic drug proving outcome of breast cancer. J Nanobiotechnol [Internet]. 2022;20:1–17. Wang C, Shen Y, Ma Y. Bifidobacterium infantis-mediated herpes simplex Virus-TK/Ganciclovir treatment inhibits Cancer Metastasis in Mouse Model. Int J Mol Sci. 2023;24:11721. Zhang H, Wang Y, Li M, et al. A self-guidance biological hybrid drug delivery system driven by anaerobes to inhibit the proliferation and metastasis of colon cancer. Asian J Pharm Sci [Internet]. 2022;17:892–907. Zhou H, He Z, Wang C, et al. Intravenous administration is an effective and safe route for cancer gene therapy using the bifidobacterium-mediated recombinant HSV-1 thymidine kinase and ganciclovir. Int J Mol Sci. 2016;17:1–18. Wang K, Xiang Y, Pan W, et al. Dual-targeted photothermal agents for enhanced cancer therapy. Chem Sci. 2020;11:8055–72. Wang H, Chang J, Shi M, et al. A dual-targeted Organic Photothermal Agent for enhanced Photothermal Therapy. Angew Chemie - Int Ed. 2019;58:1057–61. Castro F, Pinto ML, Pereira CL et al. Chitosan/γ-PGA nanoparticles-based immunotherapy as adjuvant to radiotherapy in breast cancer. Biomaterials. 2020;257:120218. Min Y, Roche KC, Tian S, et al. Antigen-capturing nanoparticles improve the abscopal effect and cancer immunotherapy. Nat Nanotechnol. 2017;12(9):877–82. Fu Q, Li Z, Ye J, et al. Magnetic targeted near-infrared II PA/MR imaging guided photothermal therapy to trigger cancer immunotherapy. Theranostics. 2020;10:4997–5010. Wang J, Chang Y, Luo H, et al. Designing immunogenic nanotherapeutics for photothermal-triggered immunotherapy involving reprogramming immunosuppression and activating systemic antitumor responses. Biomaterials [Internet]. 2020;255:120153. Liu T, Zhu M, Chang X, et al. Tumor-specific photothermal-therapy-assisted immunomodulation via multiresponsive adjuvant nanoparticles. Adv Mater. 2023;35(18):e2300086. Dougan M, Dranoff G, Dougan SK, GM-CSF. IL-3, and IL-5 family of cytokines: regulators of inflammation. Immun [Internet]. 2019;50:796–811. Yan WL, Wu CC, Shen KY, et al. Activation of GM-CSF and TLR2 signaling synergistically enhances antigen-specific antitumor immunity and modulates the tumor microenvironment. J Immunother Cancer. 2021;9:1–15. Lazarus HM, Ragsdale CE, Gale RP, et al. Sargramostim (rhu GM-CSF) as Cancer Therapy (systematic review) and an Immunomodulator. A drug before its time? Front Immunol. 2021;12:1–20. Mashima H, Zhang R, Kobayashi T, et al. Generation of GM-CSF-producing antigen-presenting cells that induce a cytotoxic T cell-mediated antitumor response. Oncoimmunology [Internet]. 2020;9:1–16. Turkevich J, Stevenson PC, Hillier J. A study of the nucleation and growth processes in the synthesis of colloidal gold. Discuss Faraday Soc. 1951;11:55–75. Xiong W, Peng L, Chen H, et al. Surface modification of MPEG-b-PCL-based nanoparticles via oxidative self-polymerization of dopamine for malignant melanoma therapy. Int J Nanomedicine. 2015;10:2985–96. Chang M, Hou Z, Jin D, et al. Colorectal tumor microenvironment-activated bio-decomposable and metabolizable Cu2O@CaCO3 nanocomposites for synergistic oncotherapy. Adv Mater. 2020;32(43):e2004647. Aftab S, Shah A, Nadhman A, et al. Nanomedicine: an effective tool in cancer therapy. Int J Pharm [Internet]. 2018;540:132–49. Liu Y, Ashton JR, Moding EJ, et al. A plasmonic gold nanostar theranostic probe for in vivo tumor imaging and photothermal therapy. Theranostics. 2015;5:946–60. Wilson WR, Hay MP. Targeting hypoxia in cancer therapy. Nat Rev Cancer [Internet]. 2011;11:393–410. Chen W, Wang Y, Qin M, et al. Bacteria-Driven Hypoxia Targeting for Combined Biotherapy and Photothermal Therapy. ACS Nano. 2018;12:5995–6005. Li Y, Leng Q, Zhang Y et al. Anaerobic bacteria mediated ‘smart missile’ targeting tumor hypoxic area enhances the therapeutic outcome of lung cancer. Chem Eng J. 2022;438:135566. Fan JX, Peng MY, Wang H, et al. Engineered bacterial bioreactor for tumor therapy via fenton-like reaction with localized H2O2 generation. Adv Mater. 2019;31:1–8. Zhang W, Liu J, Li X, et al. Precise chemodynamic therapy of Cancer by Trifunctional Bacterium-Based nanozymes. ACS Nano. 2021;15:19321–33. Kuo WS, Wu CM, Yang ZS et al. Biocompatible bacteria@Au composites for application in the photothermal destruction of cancer cells. Chem Commun. 2008;37:4430–2. Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313:1960–4. Wang M, Chang M, Zheng P, et al. A noble AuPtAg-GOx nanozyme for synergistic Tumor Immunotherapy Induced by Starvation Therapy-Augmented mild Photothermal Therapy. Adv Sci. 2022;9:1–10.