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Experimental study of the difference in deformation between normal and pathological, renal and bladder, cells induced by acoustic radiation force

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Abstract

Previous studies have shown that alterations in the mechanical properties of cells may be associated with the onset and progression of some forms of pathology. In this paper, an experimental study of two types of cells, renal (cancer) and bladder (cancer) cells, is described which used acoustic radiation force (ARF) generated by a high-frequency ultrasound focusing transducer and performed on the operating platform of an inverted light microscope. Comparing images of cancer cells with those of normal cells of the same kind, we find that the cancer cells are more prone to deform than normal cells of the same kind under the same ARF. In addition, cancer cells with higher malignancy are more deformable than those with lower malignancy. This means that the deformability of cells may be used to distinguish diseased cells from normal ones, and more aggressive cells from less aggressive ones, which may provide a more rapid and accurate method for clinical diagnosis of urological disease in the future.

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References

  1. Ashkin A, Dziedzic JM, Bjorkholm JE (1986) Observation of a single-beam gradient force optical trap for dielectric particles. Opt Lett 11: 288–290. https://doi.org/10.1364/OL.11.000288

  2. Bausch AR, Moller W, Sackmann E (1999) Measurement of local viscoelasticity and forces in living cells by magnetic tweezers. Biophys J 76:573–579. https://doi.org/10.1016/S0006-3495(99)77225-5

  3. Binnig G, Quate CF, Gerber C (1986) Atomic force microscope. Phys Rev Lett 56: 930–933. https://doi.org/10.1002/9780471729259.mc02c02s8

  4. Brodaczewska KK, Szczylik C, Fiedorowicz M, Porta C, Czarneck AM (2016) Choosing the right cell line for renal cell cancer research. Mol Cancer 15(83):1–15. https://doi.org/10.1186/s12943-016-0565-8

  5. Chahine NO, Blanchette C, Thomas CB (2013) Effect of age and cytoskeletal elements on the indentation-dependent mechanical properties of chondrocytes. PLoS ONE 8(E61651):1–14. https://doi.org/10.1371/journal.pone.0061651

  6. Chen JB, Zhang M, Zhang XL (2018) Glucocorticoid-inducible kinase 2 promotes bladder cancer cell proliferation, migration and invasion by enhancing beta-catenin/c-myc signaling pathway. J Cancer 9: 774–4782. https://doi.org/10.7150/jca.25811

  7. Dao M, Lim CT (2013) Mechanics of the human red blood cell deformed by optical tweezers. J Mech Phys Solinds 51:2259–2280. https://doi.org/10.1016/j.jmps.2003.09.019

  8. Darling EM, Zauscher S, Guilak F (2006) Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthr Cartil 14:571–579. https://doi.org/10.1016/j.joca.2005.12.003

  9. Drury JL, Dembo M (1999) Hydrodynamics of micropipette aspiration. Biophys J 76:110–128. https://doi.org/10.1016/S0006-3495(99)77183-3

  10. Evans EA (1973) A new material concept for the red cell membrane. Biophys J 13:926–940. https://doi.org/10.1016/S0006-3495(73)86035-7

  11. Evans EA, Hochmuth RM (1976) Membrane viscoelasticity. Biophys J 16:1–11. https://doi.org/10.1016/S0006-3495(76)85658-5

  12. Henon S (1999) A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys J 76:1145–1151. https://doi.org/10.1016/S0006-3495(99)77279-6

  13. Hochmuth RM (2000) Micropipette aspiration of living cells. J Biomech 33:15–22. https://doi.org/10.1016/S0021-9290(99)00175-X

  14. Horimizu M, Kawase T, Tanaka T (2013) Biomechanical evaluation by AFM of cultured human cell-multilayered periosteal sheets. Micron 48:1–10. https://doi.org/10.1016/j.micron.2013.02.001

  15. Hu S, Tan Y, Sun D (2013) Cell Manipulation with Robot-Aided Optical Tweezers Technology. In: Guo Y. (eds) Selected Topics in Micro/Nano-robotics for Biomedical Applications. Springer, New York, NY, pp 159–174. https://doi.org/10.1007/978-1-4419-8411-1_9

  16. Hwang JY, Lee C, Lam KH (2014) Cell Membrane Deformation Induced by a Fibronectin-Coated Polystyrene Microbead in a 200-MHz Acoustic Trap. IEEE Trans Ultrason. Ferroelectr Freq Control 61: 399–406. https://doi.org/10.1109/TUFFC.2014.2925

  17. Hwang JY, Kim J, Park JM (2016) Cell Deformation by single-beam acoustic trapping: a promising tool for measurements of cell mechanics. Sci Rep 6(27238):1–8. https://doi.org/10.1038/srep27238

  18. Jauffred L, Callisen TH, Oddershede LB (2007) Visco-elastic membrane tethers extracted from Escherichia coli by optical tweezers. Biophys J 93:4068–4075. https://doi.org/10.1529/biophysj.107.103861

  19. Kim H (2003) Quantification of cell adhesion force with AFM: distribution of vitronectin receptors on a living MC3T3-EI cell. Ultramicroscopy 97:359–363. https://doi.org/10.1016/s0304-3991(03)00061-5

  20. Lam KH, Li Y, Li Y, Lim HG, Zhou Q, Shung KK (2016) Multifunctional single beam acoustic tweezer for noninvasive cell/organism manipulation and tissue imaging. Sci Rep 6:37554. https://doi.org/10.1038/srep37554

  21. Lekka M, Laidler P, Gil D, Lekki J, Stachura Z, Hrynkiewicz AZ (1999) Elasticity of normal and cancerous human bladder cells studied by scanning force microscopy. Eur Biophys J 28:312–316. https://doi.org/10.1007/s002490050213

  22. Li QS, Lee GYH, Ong CN, Lim CT (2008) AFM indentation study of breast cancer cells. Biochem Bioph Res Co 374:609–613. https://doi.org/10.1016/j.bbrc.2008.07.078

  23. Lim CT, Dao M, Suresh S (2004) Large deformation of living cells using laser traps. Acta Mater 52:1837–1845. https://doi.org/10.1016/j.actamat.2003.12.028

  24. Lim CT, Zhou EH, Li A (2006) Experimental techniques for single cell and single molecule biomechanics. Mat Sci Eng C 26:1278–1288. https://doi.org/10.1016/j.msec.2005.08.022

  25. Liu HC, Gang EJ, Kim HN, Lim HG, Jung H, Chen R, Kim YM (2018) Characterizing deformability of drug resistant patient-derived acute lymphoblastic leukemia (ALL) cells using acoustic tweezers. Sci Rep 8(15708):1–10. https://doi.org/10.1038/s41598-018-34024-3

  26. Puig-de-Morales-Marinkovic M, Turner KT, Butler JP (2007) Viscoelasticity of the human red blood cells. Am J Physiol-Cell Ph 293: C597-C605. https://doi.org/10.1152/ajpcell.00562.2006

  27. Siegel RL, Miller KD, Jemal A (2016) Cancer statistics, 2016. CA Cancer J Clin 66:7–30. https://doi.org/10.3322/caac.21332

  28. Sleep J (1999) Elasticity of the red cell membrance and its relation to hemolytic disorders: an optical tweezers study. Biophys J 77:3085–3095. https://doi.org/10.1016/S0006-3495(99)77139-0

  29. Sundvik M, Nieminen HJ, Salmi A, Panula P, Hæggström E (2015) Effects of acoustic levitation on the development of zebrafish, Danio rerio, embryos. Sci Rep 5:13596. https://doi.org/10.1038/srep13596

  30. Tan Y, Sun D (2010) Mechanical characterization of human red blood cells under different osmotic conditions by robotic manipulation with optical tweezers. IEEE Trans Biomed Eng 57:1816–1825. https://doi.org/10.1109/TBME.2010.2042448

  31. Tan SCM, Pan WX, Ma G (2008) Viscoelastic behavior of human mesenchymal stem cells. BMC Cell Biol 9:40–46. https://doi.org/10.1186/1471-2121-9-40

  32. Tan Y, Sun D, Huang W (2010) Characterizing mechanical properties of biological cells by microinjection. IEEE T Nanobiosci 9:171–180. https://doi.org/10.1109/TNB.2010.2050598

  33. Tan Y, Sun D, Cheng SH, Han S, Li RA (2011) Robotic cell manipulation with optical tweezers for biomechanical characterization. IEEE Int Conf Robot Autom. https://doi.org/10.1109/ICRA.2011.5979577

  34. Titushkin L, Cho M (2006) Distinct membrane mechanical properties of human mesenchymal stem cells determined using laser optical tweezers. Biophys J 90:2582–2591. https://doi.org/10.1529/biophysj.105.073775

  35. Trickey WR, Lee GM, Guilak F (2000) Viscoelastic properties of chondrocytes from normal and osteoarthritic human cartilage. J Orthop Res 18:891–898. https://doi.org/10.1002/jor.1100180607

  36. Wang N, Ingber DE (1995) Probing transmembrane mechanical coupling and cytomechanics using magnetic twisting cytometry. Biochem cell Biol 73:327–335. https://doi.org/10.1139/o95-041

  37. Williams RD, Elliott AY, Stein N, Fraley EE (1976) In vitro cultivation of human renal cell cancer. I Establishment of Cell in Culture. Vitro 12:623–627. https://doi.org/10.1007/bf02797460

  38. Zhang X, Chen A (2004) Atomic force microscopy measurement of leukocyte-endothelial interaction. Am J Physiol-Heart C 286:H359–H367. https://doi.org/10.1152/ajpheart.00491.2003

  39. Zhong J, Chen Y, Liao X (2016) Testis expressed 19 is a novel cancer-testis antigen expressed in bladder cancer. Tumor Biol 37:7757–7765. https://doi.org/10.1007/s13277-015-4567-8

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Acknowledgements

This work was supported by National key R & D program (No. 2016YFF0203000), State Key Program of National Natural Science of China (No. 11834008), the National Natural Science Foundation of China (No. 11774167), State Key Laboratory of Acoustics, Chinese Academy of Science (No. SKLA201809), Key Laboratory of Underwater Acoustic Environment, Chinese Academy of Sciences (No. SSHJ-KFKT-1701), and AQSIQ technology R&D program (No. 2017QK125).

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Correspondence to Xiaozhou Liu.

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Wang, H., Qiao, Y., Liu, J. et al. Experimental study of the difference in deformation between normal and pathological, renal and bladder, cells induced by acoustic radiation force. Eur Biophys J (2020). https://doi.org/10.1007/s00249-020-01422-3

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Keywords

  • Acoustic radiation force
  • Deformability of cells
  • Ultrasound focusing transducer
  • Renal cells
  • Bladder cells