Brain Barriers Research Center, Department of Pharmaceutics, College of Pharmacy, University of Minnesota, Minneapolis, Minnesota (S.T., W.Z., M.K., A.S.M., W.F.E.); Department of Radiation Oncology, Mayo Clinic, Rochester, Minnesota (D.M.B., S.D., S.K.G., J.N.S.); and Department of Therapeutic Radiology, Yale School of Medicine, New Haven, Connecticut (R.S.B.).
Brain Barriers Research Center, Department of Pharmaceutics, College of Pharmacy, University of Minnesota, Minneapolis, Minnesota (S.T., W.Z., M.K., A.S.M., W.F.E.); Department of Radiation Oncology, Mayo Clinic, Rochester, Minnesota (D.M.B., S.D., S.K.G., J.N.S.); and Department of Therapeutic Radiology, Yale School of Medicine, New Haven, Connecticut (R.S.B.)
J Pharmacol Exp Ther. 2021 Dec;379(3):343-357. doi: 10.1124/jpet.121.000845. Epub 2021 Sep 23.
The effective treatment of brain tumors is a considerable challenge in part because of the presence of the blood-brain barrier (BBB) that limits drug delivery. Glioblastoma multiforme (GBM) is an aggressive and infiltrative primary brain tumor with an extremely poor prognosis after standard-of-care therapy with surgery, radiotherapy (RT), and chemotherapy. DNA damage response (DDR) pathways play a critical role in DNA repair in cancer cells, and inhibition of these pathways can potentially augment RT and chemotherapy tumor cell toxicity. The ataxia telangiectasia and Rad3-related protein (ATR) kinase is a key regulator of the DDR network and is potently and selectively inhibited by the ATR inhibitor berzosertib. Although in vitro studies demonstrate a synergistic effect of berzosertib in combination with temozolomide, in vivo efficacy studies have yet to recapitulate this observation using intracranial tumor models. In the current study, we demonstrate that delivery of berzosertib to the brain is restricted by efflux at the BBB. Berzosertib has a high binding affinity to brain tissue compared with plasma, thereby leading to low free drug concentrations in the brain. Berzosertib distribution is heterogenous within the tumor, wherein concentrations are substantially lower in normal brain and invasive tumor rim (wherein the BBB is intact) when compared with those in the tumor core (wherein the BBB is leaky). These results demonstrate that high tissue binding and limited and heterogenous brain distribution of berzosertib may be important factors that influence the efficacy of berzosertib therapy in GBM. SIGNIFICANCE STATEMENT: This study examined the brain delivery and efficacy of berzosertib in patient-derived xenograft models of glioblastoma multiforme (GBM). Berzosertib is actively effluxed at the blood-brain barrier and is highly bound to brain tissue, leading to low free drug concentrations in the brain. Berzosertib is heterogeneously distributed into different regions of the brain and tumor and, in this study, was not efficacious in vivo when combined with temozolomide. These factors inform the future clinical utility of berzosertib for GBM.
脑肿瘤的有效治疗是一个相当大的挑战,部分原因是血脑屏障(BBB)的存在限制了药物输送。多形性胶质母细胞瘤(GBM)是一种侵袭性和浸润性的原发性脑肿瘤,在接受手术、放疗(RT)和化疗的标准治疗后,预后极差。DNA 损伤反应(DDR)途径在癌细胞的 DNA 修复中起着关键作用,抑制这些途径可能会增强 RT 和化疗的肿瘤细胞毒性。共济失调毛细血管扩张症和 Rad3 相关蛋白(ATR)激酶是 DDR 网络的关键调节剂,ATR 抑制剂伯佐替布可强效且选择性地抑制其活性。尽管体外研究表明伯佐替布与替莫唑胺联合具有协同作用,但在使用颅内肿瘤模型的体内疗效研究中尚未重现这一观察结果。在本研究中,我们证明了伯佐替布递送至大脑受到 BBB 外排的限制。与血浆相比,伯佐替布与脑组织具有高亲和力,从而导致大脑中的游离药物浓度较低。伯佐替布在肿瘤内的分布不均匀,与肿瘤核心(BBB 渗漏)相比,正常脑和侵袭性肿瘤边缘(BBB 完整)中的浓度要低得多。这些结果表明,高组织结合以及伯佐替布在脑内的有限和不均匀分布可能是影响伯佐替布治疗 GBM 疗效的重要因素。
本研究检查了伯佐替布在多形性胶质母细胞瘤(GBM)患者来源异种移植模型中的脑内递送和疗效。伯佐替布在血脑屏障处被主动外排,并且与脑组织高度结合,导致大脑中的游离药物浓度较低。伯佐替布在脑内的不同区域和肿瘤中分布不均匀,在本研究中,当与替莫唑胺联合使用时,在体内没有疗效。这些因素影响了伯佐替布在 GBM 中的临床应用。