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

Abstract Background 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 ad...

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Main Authors: Jie Dai, Jianmei Li, Yuqin Zhang, Qian Wen, Yun Lu, Yu Fan, Fancai Zeng, Zhiyong Qian, Yan Zhang, Shaozhi Fu
Format: Article
Language:English
Published: American Association for the Advancement of Science (AAAS) 2023-10-01
Series:Biomaterials Research
Subjects:
Online Access:https://doi.org/10.1186/s40824-023-00430-6
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author Jie Dai
Jianmei Li
Yuqin Zhang
Qian Wen
Yun Lu
Yu Fan
Fancai Zeng
Zhiyong Qian
Yan Zhang
Shaozhi Fu
author_facet Jie Dai
Jianmei Li
Yuqin Zhang
Qian Wen
Yun Lu
Yu Fan
Fancai Zeng
Zhiyong Qian
Yan Zhang
Shaozhi Fu
author_sort Jie Dai
collection DOAJ
description Abstract Background 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. Method 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). Results 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. Conclusion 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. Graphical Abstract 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.
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spelling doaj.art-e65594f1c0334251a0b0739c64838dc92024-04-03T03:25:26ZengAmerican Association for the Advancement of Science (AAAS)Biomaterials Research2055-71242023-10-0127111710.1186/s40824-023-00430-6GM-CSF augmented the photothermal immunotherapeutic outcome of self-driving gold nanoparticles against a mouse CT-26 colon tumor modelJie Dai0Jianmei Li1Yuqin Zhang2Qian Wen3Yun Lu4Yu Fan5Fancai Zeng6Zhiyong Qian7Yan Zhang8Shaozhi Fu9Department of Oncology, the Affiliated Hospital of Southwest Medical UniversityDepartment of Oncology, the Affiliated Hospital of Southwest Medical UniversityDepartment of Oncology, the Affiliated Hospital of Southwest Medical UniversityDepartment of Oncology, the Affiliated Hospital of Southwest Medical UniversityDepartment of Oncology, the Affiliated Hospital of Southwest Medical UniversityDepartment of Oncology, the Affiliated Hospital of Southwest Medical UniversityLaboratory of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Southwest Medical UniversityState Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Collaborative Innovation Center for Biotherapy, Sichuan UniversityDepartment of Oncology, the Affiliated Traditional Chinese Medicine Hospital of Southwest Medical UniversityDepartment of Oncology, the Affiliated Hospital of Southwest Medical UniversityAbstract Background 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. Method 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). Results 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. Conclusion 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. Graphical Abstract 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.https://doi.org/10.1186/s40824-023-00430-6Gold nanoparticelsGM-CSFAnaerobic bacteriaPhotothermal therapyImmunotherapyColorectal cancer
spellingShingle Jie Dai
Jianmei Li
Yuqin Zhang
Qian Wen
Yun Lu
Yu Fan
Fancai Zeng
Zhiyong Qian
Yan Zhang
Shaozhi Fu
GM-CSF augmented the photothermal immunotherapeutic outcome of self-driving gold nanoparticles against a mouse CT-26 colon tumor model
Biomaterials Research
Gold nanoparticels
GM-CSF
Anaerobic bacteria
Photothermal therapy
Immunotherapy
Colorectal cancer
title GM-CSF augmented the photothermal immunotherapeutic outcome of self-driving gold nanoparticles against a mouse CT-26 colon tumor model
title_full GM-CSF augmented the photothermal immunotherapeutic outcome of self-driving gold nanoparticles against a mouse CT-26 colon tumor model
title_fullStr GM-CSF augmented the photothermal immunotherapeutic outcome of self-driving gold nanoparticles against a mouse CT-26 colon tumor model
title_full_unstemmed GM-CSF augmented the photothermal immunotherapeutic outcome of self-driving gold nanoparticles against a mouse CT-26 colon tumor model
title_short GM-CSF augmented the photothermal immunotherapeutic outcome of self-driving gold nanoparticles against a mouse CT-26 colon tumor model
title_sort gm csf augmented the photothermal immunotherapeutic outcome of self driving gold nanoparticles against a mouse ct 26 colon tumor model
topic Gold nanoparticels
GM-CSF
Anaerobic bacteria
Photothermal therapy
Immunotherapy
Colorectal cancer
url https://doi.org/10.1186/s40824-023-00430-6
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