Department of Pharmaceutical Analysis, China Pharmaceutical University, Nanjing, 211198, China.
Department of Natural Medicinal Chemistry, China Pharmaceutical University, Nanjing, 211198, China.
Cancer Immunol Immunother. 2023 Sep;72(9):3079-3095. doi: 10.1007/s00262-023-03479-3. Epub 2023 Jun 23.
Photodynamic therapy (PDT) is an emerging clinical treatment that is expected to become an important adjuvant strategy for the immunotherapeutic cancer treatment. Recently, numerous works have reported combination strategies. However, clinical data showed that the anti-tumor immune response of PDT was not lasting though existing. The immune activation effect will eventually turn to immunosuppressive effect and get aggravated at the late stage post-PDT. So far, the mechanism is still unclear, which limits the design of specific correction strategies and further development of PDT. Several lines of evidence suggest a role for TGF-β1 in the immunosuppression associated with PDT. Herein, this study systematically illustrated the dynamic changes of immune states post-PDT within the tumor microenvironment. The results clearly demonstrated that high-light-dose PDT, as a therapeutic dose, induced early immune activation followed by late immunosuppression, which was mediated by the activated TGF-β1 upregulation. Then, the mechanism of PDT-induced TGF-β1 accumulation and immunosuppression was elucidated, including the ROS/TGF-β1/MMP-9 positive feedback loop and CD44-mediated local amplification, which was further confirmed by spatial transcriptomics, as well as by the extensive immune inhibitory effect of local high concentration of TGF-β1. Finally, a TGF-β blockade treatment strategy was presented as a promising combinational strategy to reverse high-light-dose PDT-associated immunosuppression. The results of this study provide new insights for the biology mechanism and smart improvement approaches to enhance tumor photodynamic immunotherapy.
光动力疗法(PDT)是一种新兴的临床治疗方法,有望成为癌症免疫治疗的重要辅助策略。最近,许多研究都报道了联合策略。然而,临床数据表明,尽管 PDT 现有的抗肿瘤免疫反应并不持久。PDT 后,免疫激活效应最终会转变为免疫抑制效应,并在后期加重。迄今为止,其机制尚不清楚,这限制了特定矫正策略的设计和 PDT 的进一步发展。有几条证据表明 TGF-β1 在与 PDT 相关的免疫抑制中起作用。在此,本研究系统地阐述了 PDT 后肿瘤微环境中免疫状态的动态变化。结果清楚地表明,高光剂量 PDT 作为治疗剂量,诱导早期免疫激活,随后是晚期免疫抑制,这是由激活的 TGF-β1 上调介导的。然后,阐明了 PDT 诱导 TGF-β1 积累和免疫抑制的机制,包括 ROS/TGF-β1/MMP-9 正反馈环和 CD44 介导的局部放大,这进一步通过空间转录组学以及局部 TGF-β1 高浓度的广泛免疫抑制作用得到证实。最后,提出了 TGF-β 阻断治疗策略作为一种有前途的联合策略,以逆转高光剂量 PDT 相关的免疫抑制。本研究的结果为增强肿瘤光动力免疫治疗的生物学机制和智能改进方法提供了新的见解。