Abstract
Mechanical properties such as force generation are fundamental for neuronal motility, development and regeneration. We used optical tweezers to compare the force exerted by growth cones (GCs) of neurons from the Peripheral Nervous System (PNS), such as Dorsal Root Ganglia (DRG) neurons, and from the Central Nervous System (CNS) such as hippocampal neurons. Developing GCs from dissociated DRG and hippocampal neurons were obtained from P1-P2 and P10-P12 rats. Comparing their morphology, we observed that the area of GCs of hippocampal neurons was 8-10 µm2 and did not vary between P1-P2 and P10-P12 rats, but GCs of DRG neurons were larger and their area increased from P1-P2 to P10-P12 by 2-4 times. The force exerted by DRG filopodia was in the order of 1-2 pN and never exceeded 5 pN, while hippocampal filopodia exerted a larger force, often in the order of 5 pN. Hippocampal and DRG lamellipodia exerted lateral forces up to 20 pN, but lamellipodia of DRG neurons could exert a vertical force larger than that of hippocampal neurons. Force-velocity relationships (Fv) in both types of neurons had the same qualitative behaviour, consistent with a common autocatalytic model of force generation. These results indicate that molecular mechanisms of force generation of GC from CNS and PNS neurons are similar but the amplitude of generated force is influenced by their cytoskeletal properties.
Highlights
Neuronal motility is at the basis of several major functions, such as neuronal development, memory, repair and cell migration [1]
Dorsal Root Ganglia neurons (DRG) neurons that we previously investigated were obtained from P10-P12 rats and it is possible that neurons isolated from rats at different developmental stages exert a force with a different strength
Silica beads with a diameter of 1 μm were trapped with an infrared (IR) optical tweezer in front of growth cones (GCs) and it was possible to measure the force exerted by neuronal filopodia and lamellipodia with sub pN sensitivity at 10 kHz resolution
Summary
Neuronal motility is at the basis of several major functions, such as neuronal development, memory, repair and cell migration [1]. Filopodia tips can move at a velocity that can reach 0.8-1 μm/s [7,8,9] and their motility is at the basis of the efficient formation of neural networks. Mathematical modeling provides a way to link known molecular events to force generation processes. A key outcome of these models is represented by the force – velocity (Fv) relationships, describing how the force (F) exerted by the actin filament network is related to the velocity (v) of their growing ends. Several other mathematical models have been developed [16] providing a link between measured forces and underlying molecular events. By using optical tweezers [17,18], we previously measured the force exerted by lamellipodia and filopodia from developing GCs of isolated Dorsal Root Ganglia neurons (DRG) [19]. The force exerted by filopodia was in the order of 1-2 pN and never exceeded 5 pN, while lamellipodia exerted large forces up to 20 pN
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