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Magnetic Tweezers Optimized to Exert High Forces Over Extended Distances from the Magnet in Multicellular Systems L

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Magnetic Tweezers Optimized to Exert High Forces Over Extended Distances from the Magnet in Multicellular Systems L Magnetic tweezers optimized to exert high forces over extended distances from the magnet in multicellular systems L. Selvaggi, L. Pasakarnis, D. Brunner, and C. M. Aegerter Citation: Review of Scientific Instruments 89, 045106 (2018); doi: 10.1063/1.5010788 View online: https://doi.org/10.1063/1.5010788 View Table of Contents: http://aip.scitation.org/toc/rsi/89/4 Published by the American Institute of Physics REVIEW OF SCIENTIFIC INSTRUMENTS 89, 045106 (2018) Magnetic tweezers optimized to exert high forces over extended distances from the magnet in multicellular systems L. Selvaggi,1,2,a) L. Pasakarnis,2 D. Brunner,2 and C. M. Aegerter1,2 1Department of Physics, University of Zurich UZH, Zurich, Switzerland 2Institute of Molecular Life Science IMLS, Zurich, Switzerland (Received 26 October 2017; accepted 26 March 2018; published online 11 April 2018) Magnetic tweezers are mainly divided into two classes depending on the ability of applying torque or forces to the magnetic probe. We focused on the second category and designed a device composed by a single electromagnet equipped with a core having a special asymmetric profile to exert forces as large as 230 pN–2.8 µm Dynabeads at distances in excess of 100 µm from the magnetic tip. Compared to existing solutions our magnetic tweezers overcome important limitations, opening new experimental paths for the study of a wide range of materials in a variety of biophysical research settings. We discuss the benefits and drawbacks of different magnet core characteristics, which led us to design the current core profile. To demonstrate the usefulness of our magnetic tweezers, we determined the microrheological properties inside embryos of Drosophila melanogaster during the syncytial stage. Measurements in different locations along the dorsal-ventral axis of the embryos showed little variation, with a slight increase in cytoplasm viscosity at the periphery of the embryos. The mean cytoplasm viscosity we obtain by active force exertion inside the embryos is comparable to that determined passively using high-speed video microrheology. Published by AIP Publishing. https://doi.org/10.1063/1.5010788 INTRODUCTION two electromagnets to guarantee constant forces over the area of interest;13 the constraint in employing long working dis- The study of microrheological properties of living organ- tance objectives;9,17 and the restriction in getting high forces isms is often limited due to the disruptive nature of the corre- at long distances from the electromagnet,9 even producing spondingly necessary mechanical manipulation. However, by high power.17 The necessarily short distance between bead and using minimally invasive methods such as magnetic tweezers magnet, imposed by the fact that pN forces can be obtained (MT), it is possible to locally determine cytoplasmic viscoelas- only close to the magnetic tip, makes present setups incompat- ticity inside embryos. Magnetic tweezers apply an external ible with closed chamber design for live cell imaging and also magnetic field to generate a force on superparamagnetic beads. limit the distance over which the sample can be investigated. MT are a robust force spectroscopy technique employed in Moreover, for bead-core distances of only few micrometers, a several fields to manipulate single molecules,1 as magnetic sophisticated feedback force control is necessary to ensure an probes inside live cells,2 to investigate mechanical properties accurate constant force control. The bead movement towards of biological macromolecules3–7 and cancer cells,8 to measure the magnet leads to a steeply increasing force. For bead-core biopolymer and single cell microrheology,9–12 and to study distances of more than 50 µm, the nonlinearity of the force- intracellular applications13 and structure-mechanics relation- distance relationship is instead little pronounced. Motivated ship in biopolymer network,14 as well as force-regulated pro- by the need to learn more about the microrheology proper- cesses in developing embryos.15–17 The large presence of ties of early Drosophila embryos to understand how a robust magnetic tweezers found in the literature demonstrates the and reproducible syncytial development occurs, we designed usefulness of the method that compared to other powerful MT that overcame the existing limitations and were optimized techniques, like optical tweezers and atomic force microscopy, to exert high constant forces (hundreds of pN) over extended presents several advantages. These include no photo-damage, region (>100 µm) from the magnetic tip to explore unimpeded more selectivity in trapping the probe, employment of force the entire inside of fly embryos. Although other setups based as large as hundreds of pN, and the capability of decoupling on permanent magnets7,12 exert forces in the same range of the imaging from the force paths, which allows the use of our MT, the asset of being able to switch the field and hence any objective lens independently of its numerical aperture. the force on and off easily makes our system more useful for Although MT have become a popular biophysical tool also the type of investigations we envisage in live embryos. A fly thanks to their versatility in applying both torques and forces, embryo is about 250 µm in width and 500 µm in length. There- there are still several limitations in existing solutions. The fore, our MT setup is not limited in applying forces at the main drawbacks include the limitation of the time response periphery of the embryo; rather it is able to exert conspicu- of the system and the introduction of mechanical noise by ous forces also in the middle of the embryo, at a distance of moving permanent magnets;14 the constraint of using at least about 120 µm from the magnetic tip. Magnetic beads have been injected inside embryos and used as probes for the surrounding a)Author to whom correspondence should be addressed: [email protected] environment. Viscoelastic properties of the environment of the 0034-6748/2018/89(4)/045106/6/$30.00 89, 045106-1 Published by AIP Publishing. 045106-2 Selvaggi et al. Rev. Sci. Instrum. 89, 045106 (2018) FIG. 1. (a) Picture of the experimen- tal setup. Inset: The magnetic tip sitting on a coverslide used for experiments in fly embryos. (b) Sketch of the mag- netic tweezers setup equipped with a single electromagnet used to measure the viscoelastic properties of the cyto- plasm of Drosophila embryos during early development. beads have been evaluated from the analysis of the recorded cylindrical core with a tapered tip; see Fig. 1(b). This design trajectory of the particles. allows easy replacement of cores by simply sliding them into the electromagnet. The magnitude of the force produced by the electromagnet (EM) is proportional to the current intensity SETUP DESIGN flowing in the coil up to the saturation of the core material. Our MT device consists of a single electromagnet, Our power supply can provide currents ranging from 0.1 to mounted on a homemade inverted microscope, Fig. 1(a), and 5 A to the coil. To guarantee reasonably high forces, while having the following features: minimizing heating of the core, we used a current value of 3.5 A for experiments in Drosophila embryos. Using a ferro- 1. Capability of applying large static constant forces of hun- magnetic core inside the coil, a magnetic flux density gradient dreds of pN on micron-sized beads at distance in excess of 1100 T/m is achieved in the vicinity of the sample, which of 100 µm from the magnetic tip; then exerts a force of 220 pN on 2.8 µm magnetic beads present 2. generation of horizontal forces, exerted perpendicularly inside the embryos. As the coil resistance is 5.3 Ω, we have to to the biological sample; dissipate about 65 W. An increase in temperature due to large 3. use of any objective lens, from immersion up to long currents negatively affects the magnetic properties of the core, working distance; decreases the amplitude and the gradient of the magnetic field, 4. use of open chambers compatible for live cells imaging; and transfers heat to the biological sample affecting the exper- 5. optimization of the cooling system to use coil currents imental results. Therefore, to dissipate heat, we implemented larger than 3 A. nine 1 mm thick black aluminum fins in the electromagnet To assure all the listed requirements, we mainly focused design. Fins sprout directly from the aluminum shell, are on three specifications: coil parameters, cooling system layout, 1 mm in thickness, and spaced by 2 mm. A fan placed in and magnetic core profile. front of the electromagnet is used to cool down these fins. In We performed bright field microscopy by using a small this way, each fin is able to dissipate about 5 W, while supply- working distance objective (Olympus, 60×, 1.42 NA, oil- ing 3.5 A to the coil. Under these conditions, we measured a ◦ immersion, PlanApo N) for force calibration and a long temperature increase of 2.5 C every 15 min next to the mag- working distance objective (Olympus 20×) for measure- netic tip. Since the time scale of our experiments was less than ments inside embryos. A 20× objective for microrheology a minute, the influence of temperature on the experimental investigation inside embryos provides a large field of view outcome could be neglected. (275 µm × 206 µm) that allows controlling the behavior of the overall embryo during the application of the magnetic force. The objective was mounted on a three-axis translational stage MAGNETIC CORE PROFILE to set the relative position between the objective and sample. In order to apply forces in the centre of the embryo at a In order to place one embryo at a time in proximity of the distance larger than 100 µm from the magnetic tip, we com- magnetic tip, the position of the sample relative to the magnet pared the magnetic behavior of our tweezers by changing tip was adjusted by a further three-axis micromanipulator.
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