Ha Jeung-Hoi, Xu Yikang, Sekhon Harsimranjit, Wilkens Stephan, Ren Dacheng, Loh Stewart N
Department of Biochemistry and Molecular Biology, State University of New York Upstate Medical University, Syracuse, NY 13210.
Department of Biomedical and Chemical Engineering, Syracuse University, Syracuse, NY 13244.
bioRxiv. 2023 Jul 13:2023.07.13.548788. doi: 10.1101/2023.07.13.548788.
Aggregation of leukocyte cell-derived chemotaxin 2 (LECT2) causes ALECT2, a systemic amyloidosis that affects the kidney and liver. Homozygosity of the I40V LECT2 mutation is believed to be necessary but not sufficient for the disease. Previous studies established that LECT2 fibrillogenesis is greatly accelerated by loss of its single bound zinc ion and stirring or shaking. These forms of agitation are often used to facilitate protein aggregation, but they create heterogeneous shear conditions, including air-liquid interfaces that denature proteins, that are not present in the body. Here, we determined the extent to which a more physiological form of mechanical stress-shear generated by fluid flow through a network of artery and capillary-sized channels-drives LECT2 fibrillogenesis. To mimic blood flow through the human kidney, where LECT2 and other proteins form amyloid deposits, we developed a microfluidic device consisting of progressively branched channels narrowing from 5 mm to 20 μm in width. Flow shear was particularly pronounced at the branch points and in the smallest capillaries, and this induced LECT2 aggregation much more efficiently than conventional shaking methods. EM images suggested the resulting fibril structures were different in the two conditions. Importantly, results from the microfluidic device showed the first evidence that the I40V mutation accelerated fibril formation and increased both size and density of the aggregates. These findings suggest that kidney-like flow shear, in combination with zinc loss, acts in combination with the I40V mutation to trigger LECT2 amyloidogenesis. These microfluidic devices may be of general use for uncovering the mechanisms by which blood flow induces misfolding and amyloidosis of circulating proteins.
白细胞衍生趋化因子2(LECT2)的聚集会导致ALECT2,这是一种影响肾脏和肝脏的全身性淀粉样变性。I40V LECT2突变的纯合性被认为是该疾病发生的必要条件,但并非充分条件。先前的研究表明,LECT2原纤维形成会因单个结合锌离子的丢失以及搅拌或摇晃而大大加速。这些搅拌形式常用于促进蛋白质聚集,但它们会产生异质性剪切条件,包括使蛋白质变性的气液界面,而这些条件在体内并不存在。在这里,我们确定了一种更接近生理状态的机械应力——流体流经动脉和毛细血管大小通道网络产生的剪切力——在多大程度上驱动LECT2原纤维形成。为了模拟LECT2和其他蛋白质形成淀粉样沉积物的人体肾脏中的血流情况,我们开发了一种微流控装置,该装置由宽度从5毫米逐渐变窄至20微米的逐渐分支的通道组成。流动剪切力在分支点和最小的毛细血管处尤为明显,并且与传统摇晃方法相比,这种剪切力能更有效地诱导LECT2聚集。电子显微镜图像表明,在这两种条件下形成的原纤维结构有所不同。重要的是,微流控装置的结果首次证明I40V突变加速了原纤维形成,并增加了聚集体的大小和密度。这些发现表明,类似肾脏的流动剪切力与锌离子丢失相结合,与I40V突变共同作用引发LECT2淀粉样变性。这些微流控装置可能在揭示血流诱导循环蛋白错误折叠和淀粉样变性的机制方面具有广泛用途。