The Role of Mechanical Tension in Neurons
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The Role of Mechanical Tension in Neurons Jagannathan Rajagopalan, Alireza Tofangchi, M. Taher A. Saif Department of Mechanical Science and Engineering, University of Illinois at Urbana-Champaign
ABSTRACT We used high resolution micromechanical force sensors to study the in vivo mechanical response of embryonic Drosophila neurons. Our experiments show that Drosophila axons have a rest tension of a few nN and respond to mechanical forces in a manner characteristic of viscoelastic solids. In response to fast externally applied stretch they show a linear forcedeformation response and when the applied stretch is held constant the force in the axons relaxes to a steady state value over time. More importantly, when the tension in the axons is suddenly reduced by releasing the external force the neurons actively restore the tension, sometimes close to their resting value. Along with the recent findings of Siechen et al (Proc. Natl. Acad. Sci. USA 106, 12611 (2009)) showing a link between mechanical tension and synaptic plasticity, our observation of active tension regulation in neurons suggest an important role for mechanical forces in the functioning of neurons in vivo.
INTRODUCTION The influence of mechanical forces/microenvironment on various cell processes such as motility, growth and differentiation has become increasingly clear over the last two decades [1, 2]. In particular, neurons have been shown to respond to a variety of mechanical inputs. For example, in vitro experiments on different neuronal cells have revealed that new axons can be initiated by externally applied tension [3, 4] and that existing axons grow when tension that exceeds a threshold is applied [5, 6]. Experiments have also shown that a buildup of mechanical tension in a developing axonal branch stabilizes it and causes the retraction of other axon branches and collaterals [7]. A recent experimental study by Siechen et al [8] on live Drosophila embryos has revealed an important new facet of the role of mechanical tension in neurons. These experiments show that mechanical tension is necessary for accumulation of neurotransmitter vesicles in the pre-synaptic terminal of Drosophila motor neurons. Furthermore, an increase in tension enhances the accumulation of the vesicles. This connection between tension and vesicle accumulation suggests that neurons are likely to regulate their tension in vivo. To test this hypothesis, we studied the in vivo mechanical response of Drosophila axons using high resolution micromechanical force sensors. Our experiments reveal the overall mechanical behavior of axons and provide direct evidence that neurons regulate their tension in response to mechanical perturbations.
EXPERIMENTAL DETAILS Transgenic Drosophila (ELAV-GAP/ GFP) embryos expressing green fluorescent protein (GFP) in neuronal membranes were used for the experiments. Flies were transferred from fly stock into a culture container sealed with grape jelly-coated petri dish and maintained under controlled temperature ( 25 C) and humidity ( ~60%
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