Siposova Katarina, Petrenko Viktor I, Garcarova Ivana, Sedlakova Dagmar, Almásy László, Kyzyma Olena A, Kriechbaum Manfred, Musatov Andrey
Department of Biophysics, Institute of Experimental Physics, Slovak Academy of Sciences, Kosice, Slovakia.
BCMaterials-Basque Center for Materials, Applications and Nanostructures, Leioa, Spain.
Front Mol Biosci. 2022 Aug 19;9:955282. doi: 10.3389/fmolb.2022.955282. eCollection 2022.
The amyloidogenic self-assembly of many peptides and proteins largely depends on external conditions. Among amyloid-prone proteins, insulin attracts attention because of its physiological and therapeutic importance. In the present work, the amyloid aggregation of insulin is studied in the presence of cholesterol-based detergent, Chobimalt. The strategy to elucidate the Chobimalt-induced effect on insulin fibrillogenesis is based on performing the concentration- and time-dependent analysis using a combination of different experimental techniques, such as ThT fluorescence assay, CD, AFM, SANS, and SAXS. While at the lowest Chobimalt concentration (0.1 µM; insulin to Chobimalt molar ratio of 1:0.004) the formation of insulin fibrils was not affected, the gradual increase of Chobimalt concentration (up to 100 µM; molar ratio of 1:4) led to a significant increase in ThT fluorescence, and the maximal ThT fluorescence was 3-4-fold higher than the control insulin fibril's ThT fluorescence intensity. Kinetic studies confirm the dose-dependent experimental results. Depending on the concentration of Chobimalt, either (i) no effect is observed, or (ii) significantly, ∼10-times prolonged lag-phases accompanied by the substantial, ∼ 3-fold higher relative ThT fluorescence intensities at the steady-state phase are recorded. In addition, at certain concentrations of Chobimalt, changes in the elongation-phase are noticed. An increase in the Chobimalt concentrations also triggers the formation of insulin fibrils with sharply altered morphological appearance. The fibrils appear to be more flexible and wavy-like with a tendency to form circles. SANS and SAXS data also revealed the morphology changes of amyloid fibrils in the presence of Chobimalt. Amyloid aggregation requires the formation of unfolded intermediates, which subsequently generate amyloidogenic nuclei. We hypothesize that the different morphology of the formed insulin fibrils is the result of the gradual binding of Chobimalt to different binding sites on unfolded insulin. A similar explanation and the existence of such binding sites with different binding energies was shown previously for the nonionic detergent. Thus, the data also emphasize the importance of a protein partially-unfolded state which undergoes the process of fibrils formation; i.e., certain experimental conditions or the presence of additives may dramatically change not only kinetics but also the morphology of fibrillar aggregates.
许多肽和蛋白质的淀粉样蛋白生成性自组装在很大程度上取决于外部条件。在易形成淀粉样蛋白的蛋白质中,胰岛素因其生理和治疗重要性而备受关注。在本研究中,研究了在基于胆固醇的去污剂Chobimalt存在下胰岛素的淀粉样聚集。阐明Chobimalt对胰岛素纤维形成诱导作用的策略是基于使用不同实验技术(如硫黄素T荧光测定、圆二色性、原子力显微镜、小角中子散射和小角X射线散射)的组合进行浓度和时间依赖性分析。虽然在最低Chobimalt浓度(0.1 μM;胰岛素与Chobimalt的摩尔比为1:0.004)下胰岛素纤维的形成未受影响,但Chobimalt浓度的逐渐增加(高达100 μM;摩尔比为1:4)导致硫黄素T荧光显著增加,且最大硫黄素T荧光比对照胰岛素纤维的硫黄素T荧光强度高3 - 4倍。动力学研究证实了剂量依赖性实验结果。根据Chobimalt的浓度,要么(i)未观察到影响,要么(ii)显著观察到,伴随稳态阶段相对硫黄素T荧光强度大幅提高约3倍,延迟期延长约10倍。此外,在特定Chobimalt浓度下,观察到延伸阶段的变化。Chobimalt浓度的增加还引发了形态外观急剧改变的胰岛素纤维的形成。这些纤维似乎更具柔韧性且呈波浪状,有形成圆圈的趋势。小角中子散射和小角X射线散射数据也揭示了在Chobimalt存在下淀粉样纤维的形态变化。淀粉样聚集需要形成未折叠中间体,随后产生淀粉样生成核。我们假设所形成的胰岛素纤维的不同形态是Chobimalt逐渐与未折叠胰岛素上不同结合位点结合的结果。先前针对非离子去污剂已显示了类似的解释以及具有不同结合能的此类结合位点的存在。因此,这些数据也强调了经历纤维形成过程的蛋白质部分未折叠状态的重要性;即,某些实验条件或添加剂的存在不仅可能显著改变动力学,还可能改变纤维状聚集体的形态。