A photon-driven micromotor can direct nerve fibre growth

Journal name:
Nature Photonics
Volume:
6,
Pages:
62–67
Year published:
DOI:
doi:10.1038/nphoton.2011.287
Received
Accepted
Published online

Abstract

Axonal path-finding is important in the development of the nervous system, nerve repair and nerve regeneration. The behaviour of the growth cone at the tip of the growing axon determines the direction of axonal growth and migration. We have developed an optical-based system to control the direction of growth of individual axons (nerve fibres) using laser-driven spinning birefringent spheres. One or two optical traps position birefringent beads adjacent to growth cones of cultured goldfish retinal ganglion cell axons. Circularly polarized light with angular momentum causes the trapped bead to spin. This creates a localized microfluidic flow generating an estimated 0.17 pN shear force against the growth cone that turns in response to the shear. The direction of axonal growth can be precisely manipulated by changing the rotation direction and position of this optically driven micromotor. A physical model estimating the shear force density on the axon is described.

At a glance

Figures

  1. Time-lapse images when a vaterite particle is rotated anticlockwise and positioned to the left of the axon defined by the growth direction of the axon (dashed arrow 1).
    Figure 1: Time-lapse images when a vaterite particle is rotated anticlockwise and positioned to the left of the axon defined by the growth direction of the axon (dashed arrow 1).

    a, Before the trapped vaterite particle was moved near the axon. b, The vaterite particle was moved to the left of the axon and rotated anticlockwise at ~1 Hz. c, After 340 s, the axonal growth cone had already turned to a new direction following rotation of the vaterite particle. d, After 540 s, the axon was growing at a 30° angle to the previous direction. Scale bar, 10 µm.

  2. Time-lapse images when a vaterite particle is rotated clockwise and positioned to the left of the axon defined by the axon growth direction (dashed arrow 1).
    Figure 2: Time-lapse images when a vaterite particle is rotated clockwise and positioned to the left of the axon defined by the axon growth direction (dashed arrow 1).

    a, Before the trapped vaterite particle was moved near the axon. b, The vaterite particle was moved to the left of the axon and rotated clockwise at ~1 Hz. c, After 300 s of particle rotation, the axonal growth cone has already turned to a new direction. d, After 610 s, the axon was growing at an angle of 27° from the original direction. Scale bar, 10 µm.

  3. Prolonged time-lapse images: changing the position and rotation direction of a vaterite particle to control the axonal growth direction.
    Figure 3: Prolonged time-lapse images: changing the position and rotation direction of a vaterite particle to control the axonal growth direction.

    a, Before the trapped vaterite particle was moved near the axon. b, The vaterite particle was moved to the right of the axon and rotated clockwise at ~1 Hz. c, After 520 s, the axonal growth cone had turned and was growing in a new direction influenced by the rotating vaterite particle. d, After 26 min, the axon was growing at an angle of 29° to the original growth direction. The vaterite particle was then placed to the left of the axon and the rotation direction of the particle was changed from clockwise to anticlockwise. e, By 38 min, the axonal growth cone had turned to a new direction influenced by the rotation of the vaterite particle. f, At 53 min, the axon was growing at an angle of 44° to the original direction. Scale bar, 10 µm.

  4. Two vaterite particles were trapped and rotated in opposite directions.
    Figure 4: Two vaterite particles were trapped and rotated in opposite directions.

    a, Before the trapped vaterite particles were moved near the axon. b, The vaterite particles were moved near the axon and rotated in the directions indicated by the curved arrows at ~1 Hz. c, After 120 s, the axonal growth cone had turned to a new direction following the microfluidic flows generated by the rotation of the vaterite particles. d, After 290 s, the axon was growing at an angle of 35° to the previous growth direction and was growing between the two spinning beads. Scale bar, 10 µm.

  5. Plot of the shear force per unit area calculated using the proposed model.
    Figure 5: Plot of the shear force per unit area calculated using the proposed model.

    a, Line plot of the shear force per unit area as a function of horizontal distance. b, Quiver plot overlapped with Fig. 1c.

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Author information

Affiliations

  1. Beckman Laser Institute and Medical Clinic, University of California at Irvine, Irvine, California 92617, USA

    • Tao Wu,
    • Samarendra Mohanty &
    • Michael W. Berns
  2. Quantum Science Laboratory, School of Mathematics and Physics, The University of Queensland, Brisbane, Queensland 4072, Australia

    • Timo A. Nieminen &
    • Halina Rubinsztein-Dunlop
  3. Department of Developmental and Cell Biology, University of California at Irvine, Irvine, California 92617, USA

    • Jill Miotke,
    • Ronald L. Meyer &
    • Michael W. Berns
  4. Department of Biomedical Engineering, University of California at Irvine, Irvine, California 92617, USA

    • Michael W. Berns
  5. Present address: Department of Physics, University of Texas at Arlington, Arlington, Texas 76019, USA

    • Samarendra Mohanty

Contributions

T.W. performed all the experiments reported in this paper. S.M. performed seminal experiments that led to the studies reported here. T.A.N. and H.R.-D. developed the physical approximation model. J.M. prepared the goldfish retinal explant cultures. T.W., T.A.N., R.L.M., H.R.-D. and M.W.B. analysed the data. T.W., T.A.N., J.M., R.L.M., H.R.-D. and M.W.B. wrote the paper.

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The authors declare no competing financial interests.

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