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DNA-based digital tension probes reveal integrin forces during early cell adhesion

Author

Listed:
  • Yun Zhang

    (Emory University)

  • Chenghao Ge

    (Georgia Institute of Technology and Emory University)

  • Cheng Zhu

    (Georgia Institute of Technology and Emory University
    Woodruff School of Mechanical Engineering, Georgia Institute of Technology
    Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology)

  • Khalid Salaita

    (Emory University
    Georgia Institute of Technology and Emory University)

Abstract

Mechanical stimuli profoundly alter cell fate, yet the mechanisms underlying mechanotransduction remain obscure because of a lack of methods for molecular force imaging. Here to address this need, we develop a new class of molecular tension probes that function as a switch to generate a 20- to 30-fold increase in fluorescence upon experiencing a threshold piconewton force. The probes employ immobilized DNA hairpins with tunable force response thresholds, ligands and fluorescence reporters. Quantitative imaging reveals that integrin tension is highly dynamic and increases with an increasing integrin density during adhesion formation. Mixtures of fluorophore-encoded probes show integrin mechanical preference for cyclized RGD over linear RGD peptides. Multiplexed probes with variable guanine-cytosine content within their hairpins reveal integrin preference for the more stable probes at the leading tip of growing adhesions near the cell edge. DNA-based tension probes are among the most sensitive optical force reporters to date, overcoming the force and spatial resolution limitations of traction force microscopy.

Suggested Citation

  • Yun Zhang & Chenghao Ge & Cheng Zhu & Khalid Salaita, 2014. "DNA-based digital tension probes reveal integrin forces during early cell adhesion," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms6167
    DOI: 10.1038/ncomms6167
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    Cited by:

    1. Mitchell S. Wang & Yuesong Hu & Elisa E. Sanchez & Xihe Xie & Nathan H. Roy & Miguel Jesus & Benjamin Y. Winer & Elizabeth A. Zale & Weiyang Jin & Chirag Sachar & Joanne H. Lee & Yeonsun Hong & Minsoo, 2022. "Mechanically active integrins target lytic secretion at the immune synapse to facilitate cellular cytotoxicity," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Matthew R. Pawlak & Adam T. Smiley & Maria Paz Ramirez & Marcus D. Kelly & Ghaidan A. Shamsan & Sarah M. Anderson & Branden A. Smeester & David A. Largaespada & David J. Odde & Wendy R. Gordon, 2023. "RAD-TGTs: high-throughput measurement of cellular mechanotype via rupture and delivery of DNA tension probes," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Arventh Velusamy & Radhika Sharma & Sk Aysha Rashid & Hiroaki Ogasawara & Khalid Salaita, 2024. "DNA mechanocapsules for programmable piconewton responsive drug delivery," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Myung Hyun Jo & Jing Li & Valentin Jaumouillé & Yuxin Hao & Jessica Coppola & Jiabin Yan & Clare M. Waterman & Timothy A. Springer & Taekjip Ha, 2022. "Single-molecule characterization of subtype-specific β1 integrin mechanics," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Ehsan Akbari & Melika Shahhosseini & Ariel Robbins & Michael G. Poirier & Jonathan W. Song & Carlos E. Castro, 2022. "Low cost and massively parallel force spectroscopy with fluid loading on a chip," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    6. A. Mills & N. Aissaoui & D. Maurel & J. Elezgaray & F. Morvan & J. J. Vasseur & E. Margeat & R. B. Quast & J. Lai Kee-Him & N. Saint & C. Benistant & A. Nord & F. Pedaci & G. Bellot, 2022. "A modular spring-loaded actuator for mechanical activation of membrane proteins," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    7. Jérôme R D Soiné & Christoph A Brand & Jonathan Stricker & Patrick W Oakes & Margaret L Gardel & Ulrich S Schwarz, 2015. "Model-based Traction Force Microscopy Reveals Differential Tension in Cellular Actin Bundles," PLOS Computational Biology, Public Library of Science, vol. 11(3), pages 1-16, March.

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