Cellular and Molecular Life Sciences

, Volume 69, Issue 3, pp 357–371 | Cite as

Acoustic sensors as a biophysical tool for probing cell attachment and cell/surface interactions

  • Michael Saitakis
  • Electra Gizeli
Multi-author review


Acoustic biosensors offer the possibility to analyse cell attachment and spreading. This is due to the offered speed of detection, the real-time non-invasive approach and their high sensitivity not only to mass coupling, but also to viscoelastic changes occurring close to the sensor surface. Quartz crystal microbalance (QCM) and surface acoustic wave (Love-wave) systems have been used to monitor the adhesion of animal cells to various surfaces and record the behaviour of cell layers under various conditions. The sensors detect cells mostly via their sensitivity in viscoelasticity and mechanical properties. Particularly, the QCM sensor detects cytoskeletal rearrangements caused by specific drugs affecting either actin microfilaments or microtubules. The Love-wave sensor directly measures cell/substrate bonds via acoustic damping and provides 2D kinetic and affinity parameters. Other studies have applied the QCM sensor as a diagnostic tool for leukaemia and, potentially, for chemotherapeutic agents. Acoustic sensors have also been used in the evaluation of the cytocompatibility of artificial surfaces and, in general, they have the potential to become powerful tools for even more diverse cellular analysis.


Quartz crystal microbalance Surface acoustic wave Love wave Cell adhesion Cell/substrate interactions Cytoskeleton Two-dimensional affinity 



Quartz crystal microbalance


Surface acoustic wave


Extracellular matrix


Human leukocyte antigen



The authors would like to thank Dr. A. Tsortos for helpful discussions and for critically reading the manuscript. ELKE-University of Crete is acknowledged for financial support (research grant K.A. 2732).


  1. 1.
    Gumbiner BM (1996) Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84(3):345–357PubMedCrossRefGoogle Scholar
  2. 2.
    Alon R, Hammer DA, Springer TA (1995) Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 374(6522):539–542PubMedCrossRefGoogle Scholar
  3. 3.
    Berg EL, Goldstein LA, Jutila MA, Nakache M, Picker LJ, Streeter PR, Wu NW, Zhou D, Butcher EC (1989) Homing receptors and vascular addressins: cell adhesion molecules that direct lymphocyte traffic. Immunol Rev 108:5–18PubMedCrossRefGoogle Scholar
  4. 4.
    Chen S, Springer TA (2001) Selectin receptor-ligand bonds: formation limited by shear rate and dissociation governed by the Bell model. Proc Natl Acad Sci USA 98(3):950–955PubMedCrossRefGoogle Scholar
  5. 5.
    Juliano RL (1987) Membrane receptors for extracellular matrix macromolecules: relationship to cell adhesion and tumor metastasis. Biochim Biophys Acta 907(3):261–278PubMedGoogle Scholar
  6. 6.
    Huppa JB, Davis MM (2003) T-cell-antigen recognition and the immunological synapse. Nat Rev Immunol 3(12):973–983PubMedCrossRefGoogle Scholar
  7. 7.
    Springer TA (1990) Adhesion receptors of the immune system. Nature 346(6283):425–434PubMedCrossRefGoogle Scholar
  8. 8.
    van der Merwe PA, Davis SJ (2003) Molecular interactions mediating T cell antigen recognition. Annu Rev Immunol 21:659–684PubMedCrossRefGoogle Scholar
  9. 9.
    Abraham VC, Taylor DL, Haskins JR (2004) High content screening applied to large-scale cell biology. Trends Biotechnol 22(1):15–22PubMedCrossRefGoogle Scholar
  10. 10.
    Taylor DL, Woo ES, Giuliano KA (2001) Real-time molecular and cellular analysis: the new frontier of drug discovery. Curr Opin Biotechnol 12(1):75–81PubMedCrossRefGoogle Scholar
  11. 11.
    Ballantine DS, White RM, Martin SJ, Ricco AJ, Zellers ET, Frye GC, Wohltjen H (1997) Acoustic wave sensors. Academic Press, San DiegoGoogle Scholar
  12. 12.
    Gizeli E, Lowe CR (2002) Biomolecular sensors. Taylor & Francis Inc., LondonGoogle Scholar
  13. 13.
    Cooper MA, Singleton VT (2007) A survey of the 2001 to 2005 quartz crystal microbalance biosensor literature: applications of acoustic physics to the analysis of biomolecular interactions. J Mol Recognit 20(3):154–184PubMedCrossRefGoogle Scholar
  14. 14.
    Cooper MA, Whalen C (2005) Profiling molecular interactions using label-free acoustic screening. Drug Discov Today Technol 2(3):241–245CrossRefGoogle Scholar
  15. 15.
    Fang Y, Ferrie AM, Fontaine NH, Yuen PK (2005) Characteristics of dynamic mass redistribution of epidermal growth factor receptor signaling in living cells measured with label-free optical biosensors. Anal Chem 77(17):5720–5725PubMedCrossRefGoogle Scholar
  16. 16.
    Fang Y, Ferrie AM, Fontaine NH, Mauro J, Balakrishnan J (2006) Resonant waveguide grating biosensor for living cell sensing. Biophys J 91(5):1925–1940PubMedCrossRefGoogle Scholar
  17. 17.
    Yanase Y, Suzuki H, Tsutsui T, Hiragun T, Kameyoshi Y, Hide M (2007) The SPR signal in living cells reflects changes other than the area of adhesion and the formation of cell constructions. Biosens Bioelectron 22(6):1081–1086PubMedCrossRefGoogle Scholar
  18. 18.
    Endo T, Yamamura S, Kerman K, Tamiya E (2008) Label-free cell-based assay using localized surface plasmon resonance biosensor. Anal Chim Acta 614(2):182–189PubMedCrossRefGoogle Scholar
  19. 19.
    Rodahl M, Hook F, Krozer A, Brzezinski P, Kasemo B (1995) Quartz-crystal microbalance setup for frequency and Q-factor measurements in gaseous and liquid environments. Rev Sci Instrum 66(7):3924–3930CrossRefGoogle Scholar
  20. 20.
    Marx KA (2007) The quartz crystal microbalance and the electrochemical QCM: applications to studies of thin polymer films, electron transfer systems, biological macromolecules, biosensors, and cells. In: Steinem C, Janshoff A (eds) Piezoelectric sensors. Springer, Berlin, pp 371–424CrossRefGoogle Scholar
  21. 21.
    Gronewold TM (2007) Surface acoustic wave sensors in the bioanalytical field: recent trends and challenges. Anal Chim Acta 603(2):119–128PubMedCrossRefGoogle Scholar
  22. 22.
    Gizeli E (2002) Acoustic transducers. In: Gizeli E, Lowe CR (eds) Biomolecular sensors. Taylor & Francis Inc, LondonGoogle Scholar
  23. 23.
    Gizeli E, Bender F, Rasmusson A, Saha K, Josse F, Cernosek R (2003) Sensitivity of the acoustic waveguide biosensor to protein binding as a function of the waveguide properties. Biosens Bioelectron 18(11):1399–1406PubMedCrossRefGoogle Scholar
  24. 24.
    Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110(6):673–687PubMedCrossRefGoogle Scholar
  25. 25.
    Doherty GJ, McMahon HT (2008) Mediation, modulation, and consequences of membrane-cytoskeleton interactions. Annu Rev Biophys 37:65–95PubMedCrossRefGoogle Scholar
  26. 26.
    Bray JJ, Fernyhough P, Bamburg JR, Bray D (1992) Actin depolymerizing factor is a component of slow axonal transport. J Neurochem 58(6):2081–2087PubMedCrossRefGoogle Scholar
  27. 27.
    Gryte DM, Ward MD, Hu WS (1993) Real-time measurement of anchorage-dependent cell-adhesion using a quartz crystal microbalance. Biotechnol Progr 9(1):105–108CrossRefGoogle Scholar
  28. 28.
    Redepenning J, Schlesinger TK, Mechalke EJ, Puleo DA, Bizios R (1993) Osteoblast attachment monitored with a quartz-crystal microbalance. Anal Chem 65(23):3378–3381PubMedCrossRefGoogle Scholar
  29. 29.
    Wegener J, Janshoff A, Galla HJ (1998) Cell adhesion monitoring using a quartz crystal microbalance: comparative analysis of different mammalian cell lines. Eur Biophys J 28(1):26–37CrossRefGoogle Scholar
  30. 30.
    Wegener J, Seebach J, Janshoff A, Galla HJ (2000) Analysis of the composite response of shear wave resonators to the attachment of mammalian cells. Biophys J 78(6):2821–2833PubMedCrossRefGoogle Scholar
  31. 31.
    Lord MS, Modin C, Foss M, Duch M, Simmons A, Pedersen FS, Milthorpe BK, Besenbacher F (2006) Monitoring cell adhesion on tantalum and oxidised polystyrene using a quartz crystal microbalance with dissipation. Biomaterials 27(26):4529–4537PubMedCrossRefGoogle Scholar
  32. 32.
    Modin C, Stranne AL, Foss M, Duch M, Justesen J, Chevallier J, Andersen LK, Hemmersam AG, Pedersen FS, Besenbacher F (2006) QCM-D studies of attachment and differential spreading of pre-osteoblastic cells on Ta and Cr surfaces. Biomaterials 27(8):1346–1354PubMedCrossRefGoogle Scholar
  33. 33.
    Sauerbrey G (1959) Verwendung von Schwingquartzen zur Wagung dunner Schichten und zur microwagung. Z Phys 155:206–222CrossRefGoogle Scholar
  34. 34.
    Janshoff A, Wegener J, Sieber M, Galla HJ (1996) Double-mode impedance analysis of epithelial cell monolayers cultured on shear wave resonators. Eur Biophys J 25(2):93–103PubMedCrossRefGoogle Scholar
  35. 35.
    Zhou T, Marx KA, Warren M, Schulze H, Braunhut SJ (2000) The quartz crystal microbalance as a continuous monitoring tool for the study of endothelial cell surface attachment and growth. Biotechnol Prog 16(2):268–277PubMedCrossRefGoogle Scholar
  36. 36.
    Fohlerova Z, Skladal P, Turanek J (2007) Adhesion of eukaryotic cell lines on the gold surface modified with extracellular matrix proteins monitored by the piezoelectric sensor. Biosens Bioelectron 22(9–10):1896–1901PubMedCrossRefGoogle Scholar
  37. 37.
    Li F, Wang JH, Wang QM (2008) Thickness shear mode acoustic wave sensors for characterizing the viscoelastic properties of cell monolayer. Sensor Actuat B Chem 128:399–406CrossRefGoogle Scholar
  38. 38.
    Dubin-Thaler BJ, Giannone G, Dobereiner HG, Sheetz MP (2004) Nanometer analysis of cell spreading on matrix-coated surfaces reveals two distinct cell states and STEPs. Biophys J 86(3):1794–1806PubMedCrossRefGoogle Scholar
  39. 39.
    Reinhart-King CA, Dembo M, Hammer DA (2005) The dynamics and mechanics of endothelial cell spreading. Biophys J 89(1):676–689PubMedCrossRefGoogle Scholar
  40. 40.
    Cuvelier D, Thery M, Chu YS, Dufour S, Thiery JP, Bornens M, Nassoy P, Mahadevan L (2007) The universal dynamics of cell spreading. Curr Biol 17(8):694–699PubMedCrossRefGoogle Scholar
  41. 41.
    Saitakis M, Dellaporta A, Gizeli E (2008) Measurement of two-dimensional binding constants between cell-bound major histocompatibility complex and immobilized antibodies with an acoustic biosensor. Biophys J 95(10):4963–4971PubMedCrossRefGoogle Scholar
  42. 42.
    Galli Marxer C, Collaud Coen M, Greber T, Greber UF, Schlapbach L (2003) Cell spreading on quartz crystal microbalance elicits positive frequency shifts indicative of viscosity changes. Anal Bioanal Chem 377(3):578–586PubMedCrossRefGoogle Scholar
  43. 43.
    Braunhut SJ, McIntosh D, Vorotnikova E, Zhou T, Marx KA (2005) Detection of apoptosis and drug resistance of human breast cancer cells to taxane treatments using quartz crystal microbalance biosensor technology. Assay Drug Dev Techn 3(1):77–88CrossRefGoogle Scholar
  44. 44.
    Li J, Thielemann C, Reuning U, Johannsmann D (2005) Monitoring of integrin-mediated adhesion of human ovarian cancer cells to model protein surfaces by quartz crystal resonators: evaluation in the impedance analysis mode. Biosens Bioelectron 20(7):1333–1340PubMedCrossRefGoogle Scholar
  45. 45.
    Heitmann V, Wegener J (2007) Monitoring cell adhesion by piezoresonators: impact of increasing oscillation amplitudes. Anal Chem 79(9):3392–3400PubMedCrossRefGoogle Scholar
  46. 46.
    Reiss B, Janshoff A, Steinem C, Seebach J, Wegener J (2003) Adhesion kinetics of functionalized vesicles and mammalian cells: a comparative study. Langmuir 19(5):1816–1823CrossRefGoogle Scholar
  47. 47.
    Fredriksson C, Kihlman S, Rodahl M, Kasemo B (1998) The piezoelectric quartz crystal mass and dissipation sensor: a means of studying cell adhesion. Langmuir 14(2):248–251CrossRefGoogle Scholar
  48. 48.
    Tan L, Xie Q, Jia X, Guo M, Zhang Y, Tang H, Yao S (2009) Dynamic measurement of the surface stress induced by the attachment and growth of cells on Au electrode with a quartz crystal microbalance. Biosens Bioelectron 24(6):1603–1609PubMedCrossRefGoogle Scholar
  49. 49.
    Saitakis M, Tsortos A, Gizeli E (2010) Probing the interaction of a membrane receptor with a surface-attached ligand using whole cells on acoustic biosensors. Biosens Bioelectron 25(7):1688–1693PubMedCrossRefGoogle Scholar
  50. 50.
    Tsortos A, Papadakis G, Gizeli E (2008) Shear acoustic wave biosensor for detecting DNA intrinsic viscosity and conformation: a study with QCM-D. Biosens Bioelectron 24(4):836–841CrossRefGoogle Scholar
  51. 51.
    Papadakis G, Tsortos A, Gizeli E (2010) Acoustic characterization of nanoswitch structures: application to the DNA holliday junction. Nano Lett 10(12):5093–5097CrossRefGoogle Scholar
  52. 52.
    Melzak K, Tsortos A, Gizeli E (2009) Use of acoustic sensors to probe the mechanical properties of liposomes. Methods Enzymol 465:21–41PubMedCrossRefGoogle Scholar
  53. 53.
    Li F, Wang JH, Wang QM (2007) Monitoring cell adhesion by using thickness shear mode acoustic wave sensors. Biosens Bioelectron 23(1):42–50PubMedCrossRefGoogle Scholar
  54. 54.
    Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105(4):1473–1478PubMedCrossRefGoogle Scholar
  55. 55.
    Coue M, Brenner SL, Spector I, Korn ED (1987) Inhibition of actin polymerization by latrunculin A. FEBS Lett 213(2):316–318PubMedCrossRefGoogle Scholar
  56. 56.
    Nakano MY, Boucke K, Suomalainen M, Stidwill RP, Greber UF (2000) The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. J Virol 74(15):7085–7095PubMedCrossRefGoogle Scholar
  57. 57.
    Hoebeke J, Van Nijen G, De Brabander M (1976) Interaction of oncodazole (R 17934), a new antitumoral drug, with rat brain tubulin. Biochem Biophys Res Commun 69(2):319–324PubMedCrossRefGoogle Scholar
  58. 58.
    Schiff PB, Fant J, Horwitz SB (1979) Promotion of microtubule assembly in vitro by taxol. Nature 277(5698):665–667PubMedCrossRefGoogle Scholar
  59. 59.
    Marx KA, Zhou T, Montrone A, Schulze H, Braunhut SJ (2001) A quartz crystal microbalance cell biosensor: detection of microtubule alterations in living cells at nM nocodazole concentrations. Biosens Bioelectron 16(9–12):773–782PubMedCrossRefGoogle Scholar
  60. 60.
    Marx KA, Zhou T, Montrone A, McIntosh D, Braunhut SJ (2007) A comparative study of the cytoskeleton binding drugs nocodazole and taxol with a mammalian cell quartz crystal microbalance biosensor: different dynamic responses and energy dissipation effects. Anal Biochem 361(1):77–92PubMedCrossRefGoogle Scholar
  61. 61.
    Cans AS, Hook F, Shupliakov O, Ewing AG, Eriksson PS, Brodin L, Orwar O (2001) Measurement of the dynamics of exocytosis and vesicle retrieval at cell populations using a quartz crystal microbalance. Anal Chem 73(24):5805–5811PubMedCrossRefGoogle Scholar
  62. 62.
    Elsom J, Lethem MI, Rees GD, Hunter AC (2008) Novel quartz crystal microbalance based biosensor for detection of oral epithelial cell-microparticle interaction in real-time. Biosens Bioelectron 23(8):1259–1265PubMedCrossRefGoogle Scholar
  63. 63.
    Tan L, Jia X, Jiang XF, Zhang YY, Tang H, Yao SZ, Xie QJ (2008) Real-time monitoring of the cell agglutination process with a quartz crystal microbalance. Anal Biochem 383(1):130–136PubMedCrossRefGoogle Scholar
  64. 64.
    Kang HW, Muramatsu H (2009) Monitoring of cultured cell activity by the quartz crystal and the micro CCD camera under chemical stressors. Biosens Bioelectron 24(5):1318–1323PubMedCrossRefGoogle Scholar
  65. 65.
    Hong S, Ergezen E, Lec R, Barbee KA (2006) Real-time analysis of cell-surface adhesive interactions using thickness shear mode resonator. Biomaterials 27(34):5813–5820PubMedCrossRefGoogle Scholar
  66. 66.
    Ergezen E, Hong S, Barbee KA, Lec R (2007) Real time monitoring of the effects of Heparan Sulfate Proteoglycan (HSPG) and surface charge on the cell adhesion process using thickness shear mode (TSM) sensor. Biosens Bioelectron 22(9–10):2256–2260PubMedCrossRefGoogle Scholar
  67. 67.
    Heitmann V, Reiss B, Wegener J (2007) The quartz crystal microbalance in cell biology: basics and applications. In: Steinem C, Janshoff A (eds) Piezoelectric sensors. Springer, Berlin, pp 303–338CrossRefGoogle Scholar
  68. 68.
    Marx KA, Zhou T, Montrone A, McIntosh D, Braunhut SJ (2005) Quartz crystal microbalance biosensor study of endothelial cells and their extracellular matrix following cell removal: evidence for transient cellular stress and viscoelastic changes during detachment and the elastic behavior of the pure matrix. Anal Biochem 343(1):23–34PubMedCrossRefGoogle Scholar
  69. 69.
    Dustin ML, Bromley SK, Davis MM, Zhu C (2001) Identification of self through two-dimensional chemistry and synapses. Annu Rev Cell Dev Biol 17:133–157PubMedCrossRefGoogle Scholar
  70. 70.
    Shaw AS, Dustin ML (1997) Making the T cell receptor go the distance: a topological view of T cell activation. Immunity 6(4):361–369PubMedCrossRefGoogle Scholar
  71. 71.
    Saitakis M, Gizeli E (2011) Quantification of the effect of glycocalyx condition on membrane receptor interactions using an acoustic wave sensor. Eur Biophys J 40(2):209–215PubMedCrossRefGoogle Scholar
  72. 72.
    Wang H, Zeng H, Liu Z, Yang Y, Deng T, Shen G, Yu R (2004) Immunophenotyping of acute leukemia using an integrated piezoelectric immunosensor array. Anal Chem 76(8):2203–2209PubMedCrossRefGoogle Scholar
  73. 73.
    Wang H, Zeng H, Shen G, Yu R (2006) Immunophenotyping of acute leukemias using a quartz crystal microbalance and monoclonal antibody-coated magnetic microspheres. Anal Chem 78(8):2571–2578PubMedCrossRefGoogle Scholar
  74. 74.
    Zeng H, Wang H, Chen F, Xin H, Wang G, Xiao L, Song K, Wu D, He Q, Shen G (2006) Development of quartz-crystal-microbalance-based immunosensor array for clinical immunophenotyping of acute leukemias. Anal Biochem 351(1):69–76PubMedCrossRefGoogle Scholar
  75. 75.
    Pan YL, Guo ML, Nie Z, Huang Y, Pan CF, Zeng K, Zhang Y, Yao SZ (2010) Selective collection and detection of leukemia cells on a magnet-quartz crystal microbalance system using aptamer-conjugated magnetic beads. Biosens Bioelectron 25(7):1609–1614PubMedCrossRefGoogle Scholar
  76. 76.
    Wei XL, Mo ZH, Li B, Wei JM (2007) Disruption of HepG2 cell adhesion by gold nanoparticle and Paclitaxel disclosed by in situ QCM measurement. Colloid Surface B 59(1):100–104CrossRefGoogle Scholar
  77. 77.
    Tan L, Jia XE, Jiang XF, Zhang YY, Tang H, Yao SZ, Xie QJ (2009) In vitro study on the individual and synergistic cytotoxicity of adriamycin and selenium nanoparticles against Bel7402 cells with a quartz crystal microbalance. Biosens Bioelectron 24(7):2268–2272PubMedCrossRefGoogle Scholar
  78. 78.
    Zhou YP, Jia XE, Tan L, Xie QJ, Lei LH, Yao SZ (2010) Magnetically enhanced cytotoxicity of paramagnetic selenium-ferroferric oxide nanocomposites on human osteoblast-like MG-63 cells. Biosens Bioelectron 25(5):1116–1121PubMedCrossRefGoogle Scholar
  79. 79.
    Lee YJ, Park SJ, Lee WK, Ko JS, Kim HM (2003) MG63 osteoblastic cell adhesion to the hydrophobic surface precoated with recombinant osteopontin fragments. Biomaterials 24(6):1059–1066PubMedCrossRefGoogle Scholar
  80. 80.
    Jensen T, Dolatshahi-Pirouz A, Foss M, Baas J, Lovmand J, Duch M, Pedersen FS, Kassem M, Bunger C, Soballe K, Besenbacher F (2010) Interaction of human mesenchymal stem cells with osteopontin coated hydroxyapatite surfaces. Colloid Surface B 75(1):186–193CrossRefGoogle Scholar
  81. 81.
    Lakard S, Herlem G, Valles-Villareal N, Michel G, Propper A, Gharbi T, Fahys B (2005) Culture of neural cells on polymers coated surfaces for biosensor applications. Biosens Bioelectron 20(10):1946–1954PubMedCrossRefGoogle Scholar
  82. 82.
    Guo M, Chen J, Zhang Y, Chen K, Pan C, Yao S (2008) Enhanced adhesion/spreading and proliferation of mammalian cells on electropolymerized porphyrin film for biosensing applications. Biosens Bioelectron 23(6):865–871PubMedCrossRefGoogle Scholar
  83. 83.
    Saravia V, Toca-Herrera JL (2009) Substrate influence on cell shape and cell mechanics: HepG2 cells spread on positively charged surfaces. Microsc Res Tech 72(12):957–964PubMedCrossRefGoogle Scholar
  84. 84.
    Satriano C, Messina GM, Marino C, Aiello I, Conte E, La Mendola D, Distefano DA, D’ Alessandro F, Pappalardo G, Impellizzeri G (2010) Surface immobilization of fibronectin-derived PHSRN peptide on functionalized polymer films–effects on fibroblast spreading. J Colloid Interface Sci 341(2):232–239PubMedCrossRefGoogle Scholar
  85. 85.
    Keller CA, Kasemo B (1998) Surface specific kinetics of lipid vesicle adsorption measured with a quartz crystal microbalance. Biophys J 75(3):1397–1402PubMedCrossRefGoogle Scholar
  86. 86.
    Andersson AS, Glasmastar K, Sutherland D, Lidberg U, Kasemo B (2003) Cell adhesion on supported lipid bilayers. J Biomed Mater Res A 64A(4):622–629CrossRefGoogle Scholar
  87. 87.
    Svedhem S, Dahlborg D, Ekeroth J, Kelly J, Hook F, Gold J (2003) In situ peptide-modified supported lipid bilayers for controlled cell attachment. Langmuir 19(17):6730–6736CrossRefGoogle Scholar
  88. 88.
    Li PCH, Wang WJ, Parameswaran M (2003) An acoustic wave sensor incorporated with a microfluidic chip for analyzing muscle cell contraction. Analyst 128(3):225–231PubMedCrossRefGoogle Scholar
  89. 89.
    Li M, Cui T, Mills DK, Lvov YM, McShane MJ (2005) Comparison of selective attachment and growth of smooth muscle cells on gelatin- and fibronectin-coated micropatterns. J Nanosci Nanotechno 5(11):1809–1815CrossRefGoogle Scholar
  90. 90.
    Wang XM, Ellis JS, Kan CD, Li RK, Thompson M (2008) Surface immobilisation and properties of smooth muscle cells monitored by on-line acoustic wave detector. Analyst 133(1):85–92PubMedCrossRefGoogle Scholar
  91. 91.
    Khraiche ML, Zhou A, Muthuswamy J (2005) Acoustic sensor for monitoring adhesion of Neuro-2A cells in real-time. J Neurosci Methods 144(1):1–10PubMedCrossRefGoogle Scholar
  92. 92.
    Cheung S, Fick LJ, Belsham DD, Thompson M (2010) Depolarization of surface-attached hypothalamic mouse neurons studied by acoustic wave (thickness shear mode) detector. Analyst 135(2):289–295PubMedCrossRefGoogle Scholar
  93. 93.
    Sapper A, Wegener J, Janshoff A (2006) Cell motility probed by noise analysis of thickness shear mode resonators. Anal Chem 78(14):5184–5191PubMedCrossRefGoogle Scholar
  94. 94.
    Tarantola M, Marel AK, Sunnick E, Adam H, Wegener J, Janshoff A (2010) Dynamics of human cancer cell lines monitored by electrical and acoustic fluctuation analysis. Integr Biol 2(2–3):139–150CrossRefGoogle Scholar
  95. 95.
    Wegener J, Janshoff A, Steinem C (2001) The quartz crystal microbalance as a novel means to study cell–substrate interactions in situ. Cell Biochem Biophys 34(1):121–151PubMedCrossRefGoogle Scholar
  96. 96.
    Filler TJ, Peuker ET (2000) Reflection contrast microscopy (RCM): a forgotten technique? J Pathol 190(5):635–638PubMedCrossRefGoogle Scholar
  97. 97.
    Dustin ML, Ferguson LM, Chan PY, Springer TA, Golan DE (1996) Visualization of CD2 interaction with LFA-3 and determination of the two-dimensional dissociation constant for adhesion receptors in a contact area. J Cell Biol 132(3):465–474PubMedCrossRefGoogle Scholar
  98. 98.
    Dustin ML, Golan DE, Zhu DM, Miller JM, Meier W, Davies EA, van der Merwe PA (1997) Low affinity interaction of human or rat T cell adhesion molecule CD2 with its ligand aligns adhering membranes to achieve high physiological affinity. J Biol Chem 272(49):30889–30898PubMedCrossRefGoogle Scholar
  99. 99.
    Zhu DM, Dustin ML, Cairo CW, Golan DE (2007) Analysis of two-dimensional dissociation constant of laterally mobile cell adhesion molecules. Biophys J 92(3):1022–1034PubMedCrossRefGoogle Scholar
  100. 100.
    Huppa JB, Axmann M, Mortelmaier MA, Lillemeier BF, Newell EW, Brameshuber M, Klein LO, Schutz GJ, Davis MM (2010) TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 463(7283):963–967PubMedCrossRefGoogle Scholar
  101. 101.
    Chesla SE, Selvaraj P, Zhu C (1998) Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys J 75(3):1553–1572PubMedCrossRefGoogle Scholar
  102. 102.
    Huang J, Zarnitsyna VI, Liu B, Edwards LJ, Jiang N, Evavold BD, Zhu C (2010) The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464(7290):932–936PubMedCrossRefGoogle Scholar
  103. 103.
    Tolentino TP, Wu J, Zarnitsyna VI, Fang Y, Dustin ML, Zhu C (2008) Measuring diffusion and binding kinetics by contact area FRAP. Biophys J 95(2):920–930PubMedCrossRefGoogle Scholar
  104. 104.
    Wu J, Fang Y, Zarnitsyna VI, Tolentino TP, Dustin ML, Zhu C (2008) A coupled diffusion-kinetics model for analysis of contact-area FRAP experiment. Biophys J 95(2):910–919PubMedCrossRefGoogle Scholar
  105. 105.
    El-Ali J, Sorger PK, Jensen KF (2006) Cells on chips. Nature 442(7101):403–411PubMedCrossRefGoogle Scholar
  106. 106.
    Mitsakakis K, Tserepi A, Gizeli E (2008) Integration of microfluidics with a love wave sensor for the fabrication of a multisample analytical microdevice. J Microelectromech S 17(4):1010–1019CrossRefGoogle Scholar
  107. 107.
    Bender F, Roach P, Tsortos A, Papadakis G, Newton MI, McHale G, Gizeli E (2009) Development of a combined surface plasmon resonance/surface acoustic wave device for the characterization of biomolecules. Meas Sci Technol 20Google Scholar
  108. 108.
    Urbanski JP, Thies W, Rhodes C, Amarasinghe S, Thorsen T (2006) Digital microfluidics using soft lithography. Lab Chip 6(1):96–104PubMedCrossRefGoogle Scholar

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© Springer Basel AG 2011

Authors and Affiliations

  1. 1.Department of BiologyUniversity of CreteHeraklion-CreteGreece
  2. 2.Institute of Molecular Biology and BiotechnologyFORTHHeraklion-CreteGreece

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