Kearns Jeffrey D, Wassmann Paul, Olgac Ufuk, Fichter Marie, Christen Brigitte, Rubic-Schneider Tina, Koepke Stephan, Cochin de Billy Benjamin, Ledieu David, Andre Cedric, Hawtin Stuart, Fischer Benoit, Moretti Francesca, Hug Christian, Bepperling Alexander, Brannetti Barbara, Mendez-Garcia Celia, Littlewood-Evans Amanda, Clemens Andreas, Grosskreutz Cynthia L, Mehan Pawan, Schmouder Robert L, Sasseville Vito, Brees Dominique, Karle Anette C
Novartis Institutes for BioMedical Research, Cambridge, MA 02139, USA.
Novartis Institutes for BioMedical Research, Basel CH-4056, Switzerland.
Sci Transl Med. 2023 Feb;15(681):eabq5068. doi: 10.1126/scitranslmed.abq5068. Epub 2023 Feb 1.
Immunogenicity against intravitreally administered brolucizumab has been previously described and associated with cases of severe intraocular inflammation, including retinal vasculitis/retinal vascular occlusion (RV/RO). The presence of antidrug antibodies (ADAs) in these patients led to the initial hypothesis that immune complexes could be key mediators. Although the formation of ADAs and immune complexes may be a prerequisite, other factors likely contribute to some patients having RV/RO, whereas the vast majority do not. To identify and characterize the mechanistic drivers underlying the immunogenicity of brolucizumab and the consequence of subsequent ADA-induced immune complex formation, a translational approach was performed to bridge physicochemical characterization, structural modeling, sequence analysis, immunological assays, and a quantitative systems pharmacology model that mimics physiological conditions within the eye. This approach revealed that multiple factors contributed to the increased immunogenic potential of brolucizumab, including a linear epitope shared with bacteria, non-natural surfaces due to the single-chain variable fragment format, and non-native drug species that may form over prolonged time in the eye. Consideration of intraocular drug pharmacology and disease state in a quantitative systems pharmacology model suggested that immune complexes could form at immunologically relevant concentrations modulated by dose intensity. Assays using circulating immune cells from treated patients or treatment-naïve healthy volunteers revealed the capacity of immune complexes to trigger cellular responses such as enhanced antigen presentation, platelet aggregation, endothelial cell activation, and cytokine release. Together, these studies informed a mechanistic understanding of the clinically observed immunogenicity of brolucizumab and associated cases of RV/RO.
玻璃体内注射布罗珠单抗的免疫原性此前已有描述,且与严重眼内炎症病例相关,包括视网膜血管炎/视网膜血管阻塞(RV/RO)。这些患者体内抗药抗体(ADA)的存在引发了最初的假设,即免疫复合物可能是关键介质。尽管ADA和免疫复合物的形成可能是一个先决条件,但其他因素可能导致一些患者发生RV/RO,而绝大多数患者则不会。为了识别和表征布罗珠单抗免疫原性的机制驱动因素以及随后ADA诱导的免疫复合物形成的后果,采用了一种转化方法,将物理化学表征、结构建模、序列分析、免疫测定以及模拟眼内生理条件的定量系统药理学模型联系起来。该方法表明,多种因素导致布罗珠单抗免疫原性增加,包括与细菌共有的线性表位、单链可变片段形式导致的非天然表面以及可能在眼内长时间形成的非天然药物种类。在定量系统药理学模型中考虑眼内药物药理学和疾病状态表明,免疫复合物可在由剂量强度调节的免疫相关浓度下形成。使用治疗患者或未接受过治疗的健康志愿者的循环免疫细胞进行的测定显示,免疫复合物有能力触发细胞反应,如增强抗原呈递、血小板聚集、内皮细胞活化和细胞因子释放。这些研究共同为临床上观察到的布罗珠单抗免疫原性及相关RV/RO病例提供了机制理解。