Division of Thoracic Surgery, Toronto General Hospital, University Health Network, Toronto, ON M5G 2C4, Canada.
Graduate Department of Pharmaceutical Sciences, Leslie Dan Faculty of Pharmacy, University of Toronto, Toronto, ON M5S 3M2, Canada.
Int J Oncol. 2018 Nov;53(5):2034-2046. doi: 10.3892/ijo.2018.4555. Epub 2018 Sep 7.
Photodynamic therapy (PDT) following lung-sparing extended pleurectomy for malignant pleural mesothelioma (MPM) has been investigated as a potential means to kill residual microscopic cells. High expression levels of folate receptor 1 (FOLR1) have been reported in MPM; therefore, targeting FOLR1 has been considered a novel potential strategy. The present study developed FOLR1‑targeting porphyrin-lipid nanoparticles (folate-porphysomes, FP) for the treatment of PDT. Furthermore, inhibition of activated epidermal growth factor (EGFR)-associated survival pathways enhance PDT efficacy. In the present study, these approaches were combined; FP-based PDT was used together with an EGFR-tyrosine kinase inhibitor (EGFR-TKI). The frequency of FOLR1 and EGFR expression in MPM was analyzed using tissue microarrays. Confocal microscopy and a cell viability assay were performed to confirm the specificity of FOLR1‑targeting cellular uptake and photocytotoxicity in vitro. In vivo fluorescence activation and therapeutic efficacy were subsequently examined. The effects of EGFR-TKI were also assessed in vitro. The in vivo combined antitumor effect of EGFR-TKI and FP-PDT was then evaluated. The results revealed that FOLR1 and EGFR were expressed in 79 and 89% of MPM samples, respectively. In addition, intracellular uptake of FP corresponded well with FOLR1 expression. When MPM cells were incubated with FP and then irradiated at 671 nm, there was significant in vitro cell death, which was inhibited in the presence of free folic acid, thus suggesting the specificity of FPs. FOLR1 targeting resulted in disassembly of the porphysomes and subsequent fluorescence activation in intrathoracic disseminated MPM tumors, as demonstrated by ex vivo tissue imaging. FP-PDT resulted in significant cellular damage and apoptosis in vivo. Furthermore, the combination of pretreatment with EGFR-TKI and FP-PDT induced a marked improvement of treatment responses. In conclusion, FP-based PDT induced selective destruction of MPM cells based on FOLR1 targeting, and pretreatment with EGFR-TKI further enhanced the therapeutic response.
光动力疗法 (PDT) 是一种通过将药物和激光联合应用于肿瘤组织以治疗癌症的方法。在这项研究中,我们开发了一种基于叶酸受体 1 (FOLR1) 的光敏剂脂质体纳米颗粒 (folate-porphysomes, FP),并研究了其在恶性胸膜间皮瘤 (MPM) 中的治疗效果。FOLR1 在 MPM 中高表达,因此靶向 FOLR1 被认为是一种新的潜在策略。此外,抑制激活的表皮生长因子 (EGFR) 相关的生存途径可以增强 PDT 的疗效。在这项研究中,我们将这两种方法结合起来,使用基于 FP 的 PDT 联合 EGFR 酪氨酸激酶抑制剂 (EGFR-TKI)。我们使用组织微阵列分析了 MPM 中 FOLR1 和 EGFR 的表达频率。通过共聚焦显微镜和细胞活力测定证实了 FOLR1 靶向细胞摄取和体外光毒性的特异性。随后在体内检测了荧光激活和治疗效果。还在体外评估了 EGFR-TKI 的作用。然后评估了 EGFR-TKI 和 FP-PDT 联合的体内抗肿瘤效果。结果表明,FOLR1 和 EGFR 在 79%和 89%的 MPM 样本中表达。此外,FP 的细胞内摄取与 FOLR1 的表达密切相关。当 MPM 细胞与 FP 孵育后在 671nm 下照射时,会导致显著的体外细胞死亡,而游离叶酸的存在会抑制这种死亡,这表明 FP 的特异性。FOLR1 靶向导致在胸内播散性 MPM 肿瘤中 porphysomes 的解体和随后的荧光激活,通过离体组织成像进行了验证。FP-PDT 导致体内细胞损伤和凋亡。此外,EGFR-TKI 预处理与 FP-PDT 的联合应用可显著改善治疗反应。总之,基于 FOLR1 靶向的 FP-PDT 诱导了 MPM 细胞的选择性破坏,而 EGFR-TKI 的预处理进一步增强了治疗反应。