Department of Experimental Pathology and Medicine, Mayo Clinic, Rochester, MN, USA.
Department of Obstetrics and Gynecology, Peking University Third Hospital, Beijing, China.
Oncogene. 2023 Sep;42(37):2725-2736. doi: 10.1038/s41388-023-02785-5. Epub 2023 Aug 7.
PG545 (Pixatimod) is a highly sulfated small molecule known for its ability to inhibit heparanase and disrupt signaling mediated by heparan-binding-growth factors (HB-GF). Previous studies indicated that PG545 inhibits growth factor-mediated signaling in ovarian cancer (OC) to enhance response to chemotherapy. Here we investigated the previously unidentified mechanisms by which PG545 induces DNA damage in OC cells and found that PG545 induces DNA single- and double-strand breaks, reduces RAD51 expression in an autophagy-dependent manner and inhibits homologous recombination repair (HRR). These changes accompanied the ability of PG545 to inhibit endocytosis of the heparan-sulfate proteoglycan interacting DNA repair protein, DEK, leading to DEK sequestration in the tumor microenvironment (TME) and loss of nuclear DEK needed for HRR. As a result, PG545 synergized with poly (ADP-ribose) polymerase inhibitors (PARPis) in OC cell lines in vitro and in 55% of primary cultures of patient-derived ascites samples ex vivo. Moreover, PG545/PARPi synergy was observed in OC cells exhibiting either de novo or acquired resistance to PARPi monotherapy. PG545 in combination with rucaparib also generated increased DNA damage, increased antitumor effects and increased survival of mice bearing HRR proficient OVCAR5 xenografts compared to monotherapy treatment in vivo. Synergistic antitumor activity of the PG545/rucaparib combination was likewise observed in an immunocompetent syngeneic ID8F3 OC model. Collectively, these results suggest that targeting DEK-HSPG interactions in the TME through the use of PG545 may be a novel method of inhibiting DNA repair and sensitizing cells to PARPis.
PG545(皮沙替莫德)是一种高度硫酸化的小分子,以抑制硫酸乙酰肝素酶和破坏肝素结合生长因子(HB-GF)介导的信号转导而闻名。先前的研究表明,PG545 抑制卵巢癌(OC)中生长因子介导的信号转导,以增强对化疗的反应。在这里,我们研究了 PG545 诱导 OC 细胞中 DNA 损伤的先前未知机制,并发现 PG545 诱导 DNA 单链和双链断裂,以自噬依赖性方式降低 RAD51 表达,并抑制同源重组修复(HRR)。这些变化伴随着 PG545 抑制肝素硫酸蛋白聚糖相互作用的 DNA 修复蛋白 DEK 内吞作用的能力,导致 DEK 在肿瘤微环境(TME)中被隔离,以及核 DEK 丢失,核 DEK 是 HRR 所必需的。结果,PG545 在体外 OC 细胞系中和 55%的患者来源腹水样本的原代培养物中与聚(ADP-核糖)聚合酶抑制剂(PARPi)协同作用。此外,在对 PARPi 单药治疗具有新发或获得性耐药的 OC 细胞中观察到 PG545/PARPi 协同作用。PG545 与鲁卡帕尼联合使用也在 HRR 功能正常的 OVCAR5 异种移植小鼠体内产生了增加的 DNA 损伤、增加的抗肿瘤作用和增加的生存,与单药治疗相比。在免疫功能正常的同基因 ID8F3 OC 模型中,同样观察到 PG545/rucaparib 联合的协同抗肿瘤活性。总之,这些结果表明,通过使用 PG545 靶向 TME 中的 DEK-HSPG 相互作用可能是抑制 DNA 修复和使细胞对 PARPi 敏感的新方法。