Instituto de Física, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-972, Brazil; Centro Nacional de Biologia Estrutural e Bioimagem (CENABIO), Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-902, Brazil.
Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-902, Brazil.
Exp Cell Res. 2020 Dec 15;397(2):112370. doi: 10.1016/j.yexcr.2020.112370. Epub 2020 Nov 11.
The mechanical properties of erythrocytes have been investigated by different techniques. However, there are few reports on how the viscoelasticity of these cells varies during malaria disease. Here, we quantitatively map the viscoelastic properties of Plasmodium falciparum-parasitized human erythrocytes. We apply new methodologies based on optical tweezers to measure the viscoelastic properties and defocusing microscopy to measure the erythrocyte height profile, the overall cell volume, and its form factor, a crucial parameter to convert the complex elastic constant into complex shear modulus. The storage and loss shear moduli are obtained for each stage of parasite maturation inside red blood cells, while the former increase, the latter decrease. Employing a soft glassy rheology model, we obtain the power-law exponent for the storage and loss shear moduli, characterizing the soft glassy features of red blood cells in each parasite maturation stage. Ring forms present a liquid-like behavior, with a slightly lower power-law exponent than healthy erythrocytes, whereas trophozoite and schizont stages exhibit increasingly solid-like behaviors. Finally, the surface elastic shear moduli, low-frequency surface viscosities, and shape recovery relaxation times all increase not only in a stage-dependent manner but also when compared to healthy red blood cells. Overall, the results call attention to the soft glassy characteristics of Plasmodium falciparum-parasitized erythrocyte membrane and may provide a basis for future studies to better understand malaria disease from a mechanobiological perspective.
已经有许多技术研究了红细胞的力学特性。然而,关于这些细胞在疟疾期间的粘弹性如何变化的报道却很少。在这里,我们定量绘制了恶性疟原虫寄生的人红细胞的粘弹性特性。我们应用了基于光学镊子的新方法来测量粘弹性特性,以及离焦显微镜来测量红细胞高度轮廓、总细胞体积及其形态因子,这是将复杂弹性常数转换为复杂剪切模量的关键参数。我们获得了每个红细胞内寄生虫成熟阶段的储能和损耗剪切模量,前者增加,后者减少。利用软玻璃状流变学模型,我们获得了储能和损耗剪切模量的幂律指数,这一指数描述了各寄生虫成熟阶段红细胞的软玻璃状特征。环状形态表现出类液态行为,其幂律指数略低于健康红细胞,而滋养体和裂殖体阶段表现出越来越明显的类固态行为。最后,表面弹性剪切模量、低频表面黏度和形状恢复松弛时间不仅在依赖于阶段的方式上增加,而且与健康红细胞相比也增加。总的来说,这些结果引起了人们对恶性疟原虫寄生的红细胞膜的软玻璃状特征的关注,并且可能为未来的研究提供了一个基础,以便从机械生物学的角度更好地理解疟疾。