Fc-engineered large molecules targeting blood-brain barrier transferrin receptor and CD98hc have distinct central nervous system and peripheral biodistribution compared to standard antibodies

bioRxiv Pub Date : 2024-07-16 DOI:10.1101/2024.07.11.602993
Nathalie Khoury, Michelle E Pizzo, Claire B Discenza, David Joy, David Tatarakis, Mihail I. Todorov, Moritz Negwer, Connie Ha, G. L. de Melo, Lily Sarrafha, Matthew J. Simon, Darren Chan, Roni Chau, Kylie S Chew, Johann Chow, Allisa Clemens, Yaneth Robles-Colmenares, Jason C Dugas, Joseph Duque, Doris Kaltenecker, Holly Kane, A. Leung, Edwin I Lozano, Arash Moshkforoush, E. Roche, T. Sandmann, Mabel Tong, Kaitlin Xa, Yinhan Zhou, Joseph W. Lewcock, Ali Ertürk, Robert G Thorne, Meredith E K Calvert, Y. J. Y. Zuchero
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Abstract

The blood-brain barrier (BBB) poses a significant challenge drug delivery to the brain. BBB-crossing molecules are emerging as a new class of therapeutics with significant potential for central nervous system (CNS) indications. In particular, transferrin receptor (TfR)- and CD98 heavy chain (CD98hc)-targeting molecules have been demonstrated to cross the BBB for enhanced brain delivery. Previously, we reported TfR and CD98hc antibody transport vehicles (ATVTfR and ATVCD98hc) that utilize these BBB receptors to improve CNS drug delivery1,2. Here, we provide a comprehensive and unbiased biodistribution characterization of ATVTfR and ATVCD98hc compared to a standard IgG at a multiscale level, ranging from whole-body to brain region- and cell type-targeting specificity. Mouse whole-body tissue clearing revealed distinct organ localization for each molecule. In the CNS, ATVTfR and ATVCD98hc not only achieves enhanced brain delivery but importantly, much broader parenchymal distribution in contrast to the severely limited distribution observed with a standard antibody that was not able to be improved even at very high dose levels. Using cell sorting and single-cell RNA sequencing of mouse brain, we revealed that standard IgG predominantly localizes to perivascular and leptomeningeal cells and reaches the CNS by entering the CSF, rather than crossing the BBB. In contrast, ATVTfR and ATVCD98hc enables broad parenchymal cell-specific distribution via transcytosis through brain endothelial cells (BECs) along the neurovasculature. Finally, we extended the translational relevance of our findings by revealing enhanced and broad brain and spinal cord biodistribution of ATVTfR compared to standard IgG in cynomolgus monkey. Taken together, this multiscale analysis reveals in-depth biodistribution differences between ATVTfR, ATVCD98hc, and standard IgG. These results may better inform platform selection for specific therapeutic targets of interest, optimally matching platforms to desired CNS target engagement, peripheral organ exposures, and predict or potentially reduce off-target effects.
与标准抗体相比,针对血脑屏障转铁蛋白受体和 CD98hc 的 Fc 工程大分子具有独特的中枢神经系统和外周生物分布特性
血脑屏障(BBB)对向大脑输送药物构成了巨大挑战。BBB穿越分子正在成为一类新的治疗药物,在中枢神经系统(CNS)适应症方面具有巨大潜力。特别是,转铁蛋白受体(TfR)和 CD98 重链(CD98hc)靶向分子已被证明可以穿过 BBB,增强脑部给药。此前,我们曾报道过利用这些 BBB 受体改善中枢神经系统药物递送的 TfR 和 CD98hc 抗体运输载体(ATVTfR 和 ATVCD98hc)1,2。在此,我们提供了 ATVTfR 和 ATVCD98hc 与标准 IgG 相比在多尺度水平上全面、无偏见的生物分布特性,包括从全身到脑区和细胞类型的靶向特异性。小鼠全身组织清除显示了每种分子不同的器官定位。在中枢神经系统中,ATVTfR 和 ATVCD98hc 不仅增强了脑输送能力,更重要的是,它们的实质组织分布更为广泛,而标准抗体的分布则非常有限,即使在非常高的剂量水平下也无法改善。通过对小鼠大脑进行细胞分选和单细胞 RNA 测序,我们发现标准 IgG 主要定位于血管周围细胞和脑膜细胞,通过进入 CSF 而不是穿过 BBB 到达中枢神经系统。与此相反,ATVTfR 和 ATVCD98hc 通过沿神经血管的脑内皮细胞(BECs)的转胞作用,实现了广泛的实质细胞特异性分布。最后,我们通过揭示与标准 IgG 相比,ATVTfR 在犬科猴脑和脊髓的生物分布增强且广泛,从而扩展了我们研究结果的转化相关性。总之,这种多尺度分析揭示了 ATVTfR、ATVCD98hc 和标准 IgG 之间深入的生物分布差异。这些结果可以更好地为感兴趣的特定治疗靶点提供平台选择信息,使平台与所需的中枢神经系统靶点参与、外周器官暴露相匹配,并预测或潜在地减少脱靶效应。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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