Research ArticleAPPLIED SCIENCES AND ENGINEERING

IRONSperm: Sperm-templated soft magnetic microrobots

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Science Advances  08 Jul 2020:
Vol. 6, no. 28, eaba5855
DOI: 10.1126/sciadv.aba5855
  • Fig. 1 Magnetite nanoparticles are attached to the head, midpiece, principal piece, and distal end of the sperm cells.

    (A) The cryo-scanning electron micrograph shows a bovine sperm cell covered with 100-nm iron oxide particles. (B) Sperm head, (C) sperm midpiece, (D) principal piece, and (E) distal end of the sperm cell with attached nanoparticles. (F) The density of the nanoparticles coating is based on the charge equilibrium between the sperm cell and the nanoparticles. Sperm cells and particles display negative and positive zeta potential (V), respectively (1). Nanoparticles (10 and 48 particles) are randomly distributed, and the electric potential is calculated around a sperm cell to indicate the attachment.

  • Fig. 2 Bovine sperm cells are coated with rice grain–shaped maghemite nanoparticles resulting in IRONSperms.

    (A) Microscopic images of different cases of IRONSperm indicate the attachment of the nanoparticles to the organic body. e1(t) and e2(t) are orthonormal vectors of the material frame of IRONSperm, and the shape of its flagellum is characterized by the tangent angle (φ(s, t)) as a function of the arc length s. The magnetic moment of the head is oriented along e1(t) after fabrication. The direction of the magnetic moment is enclosed between the e1(t) and the magnetic field. Magnetic dipole moment of the head, midpiece, principal piece, and distal end are mh, mm, mp, and md, respectively. (B) Time-lapse images depicting the flagellar response of IRONSperm to a uniform magnetic field with periodic component at frequency f. The head rotates with constant precession and induces a helical traveling wave along the flagellum and results in forward swimming speed (v). The blue and red arrows indicate the magnetic field and direction of rotation, respectively. See also movie S1. (C) The distal end of IRONSperm is fixed, and the head aligns with the magnetic field. The deformation is represented by the blue dots and is approximated by an ellipse with minor and major diameters of 50 and 82 μm, respectively. See movie S2 in supporting information for illustration of the flexible bending.

  • Fig. 3 Time-dependent deformation of the flagellum indicates flexibility of IRONSperm as the actuation frequency (f) affects the amplitude of the overall wave pattern.

    Left column, amplitudes; right column, tangent angles. Darker lines indicate the flagellum at later times, and the dashed lines represent the envelope of the motion. (A) Maximum amplitude is 37 μm at f = 3 Hz. (B) Tangent angle (φ) at 3 Hz. (C) Maximum amplitude is 30 μm at f = 5 Hz. (D) φ at 5 Hz. (E) Maximum amplitude is 30 μm at f = 7 Hz. (F) φ at 7 Hz. (G) Maximum amplitude is 23 μm at f = 9 Hz. (H) φ at 9 Hz. (I) Maximum amplitude is 18 μm at f = 11 Hz. (D) φ at 11 Hz.

  • Fig. 4 Swimming speed of IRONSperms is influenced by the actuation frequency (f) and the cone angle of the head (α).

    The deviations between the magnetization of the segments of the IRONSperm also influence the swimming speed. The flagellum deformation and swimming velocity are calculated for E = 1 MPa, Lm = 13 μm, Lp = 40 μm, Ld = 7 μm, rm = 0.5 μm, rp = 0.25 μm, rd = 0.25 μm. mh = 4.65 × 10−12 Am2, mm = 1.2 × 10−12 Am2, mp = 7.8 × 10−12 Am2, md = 1.35 × 10−12 Am2, 2a = 5 μm, and b = 4 μm. (A) f = 1 Hz and αm = 15°. (B) f = 1 Hz and αm = 30°. (C) f = 1 Hz and αm = 45°. (D) f = 1 Hz and αm = 45°. (E) f = 5 Hz and αm = 45°. (F) f = 10 Hz and αm = 45°. (G) Swimming speed (v) is calculated versus the actuation frequency and cone angle. (H) Theoretically predicted and experimentally (n = 15) obtained swimming speeds of IRONSperm increase linearly with the actuation frequency and decrease slowly above the step-out frequency of 8 Hz.

  • Fig. 5 Flagellar propulsion of IRONSperm is achieved under the influence of rotating magnetic fields.

    (A) Magnetic actuation of IRONSperm is achieved using a triaxial Helmholtz coil electromagnetic system. Photo credit: I.S.M. Khalil. (B) IRONSperm is allowed to swim under the influence of a rotating magnetic field at a frequency of 2 Hz. The time-dependent deformation of the flagellum is measured during flagellar propulsion. (C) The head aligns along the rotating field with an amplitude of 20 μm. The amplitude of the distal end is 21.2 μm at t = 0 s and decreases to 7.9 μm at t = 13 s, as indicated by the blue tracking line over a time period of 13 s. The average swimming speed of IRONSperm is 10.8 μm/s. See also movies S3 and S4. (D) The tangent angle of the flagellum is calculated from the measured waveform over one beat cycle. (E) Curvature (k = 8.8 rad/mm), amplitude rise (A = 13.5 rad/mm), and wavelength (λ = 150 μm) are characterized by fitting lines to the zeroth and first Fourier modes of the tangent angle.

  • Fig. 6 Control of IRONSperm is achieved using a triaxial Helmholtz coil electromagnetic system.

    (A) IRONSperm samples are contained in the common centers of the coils and controlled by a homogeneous rotating field with a maximum magnitude of 2 mT on a square trajectory. IRONSperm follows a square trajectory with edge length of 260 μm at an average speed of 7.2 μm/s at an actuation frequency of 4 Hz. See also movie S5. (B) IRONSperm undergoes a U-turn trajectory at an average speed of 12.5 μm/s at an actuation frequency of 6 Hz. The blue circles indicate IRONSperm. See also movies S5 and S6.

  • Fig. 7 Ultrasound images showing efficient localization of a cluster of IRONSperm.

    (A) Clusters of IRONSperm samples are contained inside a polyethylene tube with an inner diameter of 380 μm. The tube is submerged inside a water reservoir above an inverted microscope. Photo credit: I.S.M. Khalil. (B) Visual feedback is obtained by the microscopic images and indicates several clusters that align with the external magnetic field lines (red arrow). (C) Ultrasound scans show a cluster of IRONSperm samples (green arrow) moving with the flowing streams of the medium along one dimension. Parameters: depth = 2 cm, frequency of the ultrasound waves = 16 MHz. See also movie S7.

  • Fig. 8 Drug loading of IRONSperm.

    (A) Fluorescence image of drug-loaded IRONSperms, bright-field overview image of drug-loaded IRONSperms, and merged image. (B) Big field view of drug-loaded IRONSperms (×10 magnification, merged image). (C) Exemplary image of an unloaded IRONSperm showing no fluorescence and a drug-loaded IRONSperm. (D) Spectrophotometry data obtained for different DOX-HCl dilutions (1.25, 0.62, 0.31, 0.16, 0.08, and 0.04 μg/ml), to obtain the corresponding drug concentration present in the IRONSperm sample by linear regression. a.u., arbitrary units. (E) Cumulative release rate by IRONSperms over 72 hours. Error bars correspond to four technical replicates.

Supplementary Materials

  • Supplementary Materials

    IRONSperm: Sperm-templated soft magnetic microrobots

    Veronika Magdanz, Islam S. M. Khalil, Juliane Simmchen, Guilherme P. Furtado, Sumit Mohanty, Johannes Gebauer, Haifeng Xu, Anke Klingner, Azaam Aziz, Mariana Medina-Sánchez, Oliver G. Schmidt, Sarthak Misra

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