Jing Rui, Si Shuai, Zhu Siyu, Tang Xiaoying, Jiang Zhenqi
School of Medical Technology, Beijing Institute of Technology, Beijing 100081, China.
Biomater Sci. 2025 Sep 5. doi: 10.1039/d5bm01193k.
Cancer immunotherapy has transformed oncological treatment paradigms, yet tumor resistance and immune evasion continue to limit therapeutic efficacy. Mitochondria-targeting organic sensitizers (MTOSs) represent an emerging class of therapeutic agents that exploit mitochondrial dysfunction as a convergent node for tumor elimination and immune activation. As central regulators of cellular metabolism, apoptotic signaling, and immune cell function, mitochondria serve as critical determinants of tumor progression and the immunological landscape within the tumor microenvironment (TME). This comprehensive review synthesizes the latest advances (2023-2025) in MTOS-mediated cancer immunotherapy, systematically examining the capacity of MTOSs to induce diverse forms of regulated cell death and orchestrate antitumor immune responses. MTOSs demonstrate remarkable versatility in triggering mitochondria-dependent apoptosis, immunogenic cell death (ICD), necroptosis, pyroptosis, ferroptosis, and autophagic cell death through strategic disruption of mitochondrial homeostasis. These sensitizers modulate key mitochondrial functions including membrane potential dynamics, reactive oxygen species (ROS) generation, electron transport chain integrity, and calcium homeostasis, thereby releasing damage-associated molecular patterns (DAMPs) that potently activate both innate and adaptive immunity. Current MTOS platforms encompass small-molecule sensitizers, polymeric nanocarriers, metal-organic complexes, and biomimetic systems, each offering distinct advantages in mitochondrial targeting and therapeutic efficacy. Clinical translation faces significant challenges including variable mitochondrial targeting efficiency due to transmembrane transport limitations and TME pH fluctuations, systemic toxicity risks from nonspecific metal ion release in metal-organic complexes, insufficient long-term biocompatibility evaluation, and the predominant reliance on simplified tumor models that inadequately reflect clinical heterogeneity and complex spatiotemporal dynamics of mitochondrial damage-immune remodeling interactions. Future research directions emphasize the multidisciplinary integration of synthetic biology, nanotechnology, and computational approaches to engineer next-generation intelligent sensitizer platforms with enhanced TME-adaptive capabilities, enabling precise mitochondrial intervention and immune modulation for improved cancer immunotherapy outcomes.
癌症免疫疗法已经改变了肿瘤治疗模式,但肿瘤耐药性和免疫逃逸仍然限制着治疗效果。线粒体靶向有机敏化剂(MTOSs)是一类新兴的治疗药物,它们利用线粒体功能障碍作为肿瘤消除和免疫激活的汇聚节点。作为细胞代谢、凋亡信号传导和免疫细胞功能的核心调节因子,线粒体是肿瘤进展和肿瘤微环境(TME)内免疫格局的关键决定因素。这篇综述综合了MTOS介导的癌症免疫疗法的最新进展(2023-2025年),系统地研究了MTOSs诱导多种形式的程序性细胞死亡并协调抗肿瘤免疫反应的能力。MTOSs通过对线粒体稳态的策略性破坏,在触发线粒体依赖性凋亡、免疫原性细胞死亡(ICD)、坏死性凋亡、焦亡、铁死亡和自噬性细胞死亡方面表现出显著的多功能性。这些敏化剂调节关键的线粒体功能,包括膜电位动态、活性氧(ROS)生成、电子传递链完整性和钙稳态,从而释放损伤相关分子模式(DAMPs),有力地激活先天免疫和适应性免疫。目前的MTOS平台包括小分子敏化剂、聚合物纳米载体、金属有机复合物和仿生系统,每种平台在靶向线粒体和治疗效果方面都有独特的优势。临床转化面临重大挑战,包括由于跨膜运输限制和TME pH波动导致的线粒体靶向效率可变、金属有机复合物中非特异性金属离子释放带来的全身毒性风险、长期生物相容性评估不足,以及主要依赖于不能充分反映临床异质性和线粒体损伤-免疫重塑相互作用复杂时空动态的简化肿瘤模型。未来的研究方向强调合成生物学、纳米技术和计算方法的多学科整合,以设计具有增强TME适应性能力的下一代智能敏化剂平台,实现精确的线粒体干预和免疫调节,从而改善癌症免疫治疗效果。