Quantifying stiffness and forces of tumor colonies and embryos using a magnetic microrobot.

Journal: Science robotics
Published Date: Jan 25, 2023

Abstract

Stiffness and forces are two fundamental quantities essential to living cells and tissues. However, it has been a challenge to quantify both 3D traction forces and stiffness (or modulus) using the same probe in vivo. Here, we describe an approach that overcomes this challenge by creating a magnetic microrobot probe with controllable functionality. Biocompatible ferromagnetic cobalt-platinum microcrosses were fabricated, and each microcross (about 30 micrometers) was trapped inside an arginine-glycine-apartic acid-conjugated stiff poly(ethylene glycol) (PEG) round microgel (about 50 micrometers) using a microfluidic device. The stiff magnetic microrobot was seeded inside a cell colony and acted as a stiffness probe by rigidly rotating in response to an oscillatory magnetic field. Then, brief episodes of ultraviolet light exposure were applied to dynamically photodegrade and soften the fluorescent nanoparticle-embedded PEG microgel, whose deformation and 3D traction forces were quantified. Using the microrobot probe, we show that malignant tumor-repopulating cell colonies altered their modulus but not traction forces in response to different 3D substrate elasticities. Stiffness and 3D traction forces were measured, and both normal and shear traction force oscillations were observed in zebrafish embryos from blastula to gastrula. Mouse embryos generated larger tensile and compressive traction force oscillations than shear traction force oscillations during blastocyst. The microrobot probe with controllable functionality via magnetic fields could potentially be useful for studying the mechanoregulation of cells, tissues, and embryos.

Authors

  • Erfan Mohagheghian
    Department of Mechanical Science and Engineering, Grainger College of Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
  • Junyu Luo
    National Institute of Biological Sciences, Beijing 102206, China.
  • F Max Yavitt
    Department of Chemical and Biological Engineering, University of Colorado, Boulder, CO 80303, USA.
  • Fuxiang Wei
    Key Laboratory of Molecular Biophysics of the Ministry of Education, Laboratory for Cellular Biomechanics and Regenerative Medicine, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei 430074, China.
  • Parth Bhala
    Department of Mechanical Science and Engineering, Grainger College of Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
  • Kshitij Amar
    Department of Mechanical Science and Engineering, Grainger College of Engineering, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
  • Fazlur Rashid
    Department of Mechanical and Aerospace Engineering, Missouri University of Science and Technology, Rolla, MO, 65401, USA.
  • Yuzheng Wang
    Department of Electrical and Computer Engineering, University of Florida, Gainesville, FL 32611, USA.
  • Xingchen Liu
    Institute of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, China.
  • Chenyang Ji
    Key Laboratory of Molecular Biophysics of the Ministry of Education, Laboratory for Cellular Biomechanics and Regenerative Medicine, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, Hubei 430074, China.
  • Junwei Chen
    School of Health Science and Engineering, University of Shanghai for Science and Technology, Shanghai, China.
  • David P Arnold
    Department of Electrical and Computer Engineering, University of Florida, Gainesville, FL 32611, USA.
  • Zhen Liu
    School of Pharmacy, Fudan University, PR China; Analytical Service Unit, WuXi AppTec (Shanghai) Co., Ltd, Shanghai, 200131, PR China.
  • Kristi S Anseth
    Department of Chemical and Biological Engineering, University of Colorado, Boulder, CO 80303, USA.
  • Ning Wang
    Qilu Hospital of Shandong University Dezhou Hospital, Dezhou, Shandong, China.

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