Publication date: 25th July 2016
FRET-based molecular tension sensors are well-suited to answer questions regarding the molecular mechanisms mediating mechanosensitive phenomena, which are poorly understood and important in many aspects of development, physiology and pathology. However, the limited force sensitivity of a given sensor, typically in the range of several piconewtons, has prevented the general applicability of this approach. Here, we develop a method enabling the rational design of sensors with optimal force-sensitivities for a variety of applications. We evaluate a variety of the common features of these sensors, including the specific fluorescent proteins used as a FRET pair as well as the composition and length of the extensible elements that enable tension sensing. Rational design was made possible through the development of a first-principles, predictive model of the behavior of the extensible elements, regarding them as unstructured poly-peptides. Based on model predictions, we designed and created a suite of tension sensors with sensitivities ranging from 2-35 pN. Furthermore, we evaluated the performance of these sensors in the context of vinculin mechanobiology. These improved biosensors reveal asymmetric loading of vinculin within individual integrin-mediated adhesions, exhibiting a 300% improvement in performance. Additionally, the comparison of multiple vinculin-based tension sensors with distinct force-extension characteristics allows analysis of whether molecular forces or extensions are the critical determinant for mechanotransduction. Surprisingly, we observe that the various sensors report distinct forces, but similar extensions, suggesting the existence of an extension-based control mechanism in vinculin-based mechanotransduction. Also, we utilize the model to create a guide for the construction of new sensors. Specifically, we make predictions of the behavior for over 1000 distinct tension sensors, which are comprised of various extensible domains of different lengths and/or stiffnesses as well as differing FRET-pairs. This resource should enable the rational design of additional tension sensors suitable for a wide range of studies in mechanobiology.
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