Cell dynamic adhesion and elastic properties probed with cylindrical atomic force microscopy cantilever tips†
Félix Rico
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
Search for more papers by this authorPere Roca-Cusachs
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
Search for more papers by this authorRaimon Sunyer
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
Search for more papers by this authorRamon Farré
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
CIBER Enfermedades Respiratorias, Spain
Search for more papers by this authorCorresponding Author
Daniel Navajas
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
CIBER Enfermedades Respiratorias, Spain
Institut de Bioenginyeria de Catalunya (IBEC), Barcelona, Spain
Professor of Physiology.
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona, Casanova 143, Barcelona 08036, Spain.Search for more papers by this authorFélix Rico
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
Search for more papers by this authorPere Roca-Cusachs
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
Search for more papers by this authorRaimon Sunyer
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
Search for more papers by this authorRamon Farré
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
CIBER Enfermedades Respiratorias, Spain
Search for more papers by this authorCorresponding Author
Daniel Navajas
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona-IDIBAPS, Barcelona, Spain
CIBER Enfermedades Respiratorias, Spain
Institut de Bioenginyeria de Catalunya (IBEC), Barcelona, Spain
Professor of Physiology.
Unitat de Biofísica i Bioenginyeria, Facultat de Medicina, Universitat de Barcelona, Casanova 143, Barcelona 08036, Spain.Search for more papers by this authorPaper presented as part of a special issue of papers from the ‘AFM BioMed conference, Barcelona 2007’.
Abstract
Cell adhesion is required for essential biological functions such as migration, tissue formation and wound healing, and it is mediated by individual molecules that bind specifically to ligands on other cells or on the extracellular matrix. Atomic force microscopy (AFM) has been successfully used to measure cell adhesion at both single molecule and whole cell levels. However, the measurement of inherent cell adhesion properties requires a constant cell–probe contact area during indentation, a requirement which is not fulfilled in common pyramidal or spherical AFM tips. We developed a procedure using focused ion beam (FIB) technology by which we modified silicon pyramidal AFM cantilever tips to obtain flat-ended cylindrical tips with a constant and known area of contact. The tips were validated on elastic gels and living cells. Cylindrical tips showed a fairly linear force–indentation behaviour on both gels and cells for indentations >200 nm. Cylindrical tips coated with ligands were used to quantify inherent dynamic cell adhesion and elastic properties. Force, work of adhesion and elasticity showed a marked dynamic response. In contrast, the deformation applied to the cells before rupture was fairly constant within the probed dynamic range. Taken together, these results suggest that the dynamic adhesion strength is counterbalanced by the dynamic elastic response to keep a constant cell deformation regardless of the applied pulling rate. Copyright © 2007 John Wiley & Sons, Ltd.
REFERENCES
- Alcaraz J, Buscemi L, Puig-de-Morales M, Colchero J, Baro A, Navajas D. 2002. Correction of microrheological measurements of soft samples with atomic force microscopy for the hydrodynamic drag on the cantilever. Langmuir 18: 716–721.
- Alcaraz J, Buscemi L, Grabulosa M, Trepat X, Fabry B, Farre R, Navajas D. 2003. Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophys. J. 84: 2071–2079.
- Bell GI. 1978. Models for Specific adhesion of cells to cells. Science 200: 618–627.
- Benoit M, Gaub HE. 2002. Measuring cell adhesion forces with atomic force microscope at the molecular level. Cells Tissues Organs 172: 174–189.
- Boal D. 2002. Mechanics of the Cell. Cambridge University Press: New York.
- Boulbitch A. 2003. Enforced unbinding of biomembranes whose mutual adhesion is mediated by a specific interaction. Eur. Biophys. J. Biophy. 31: 637–642.
- Bursac P, Lenormand G, Fabry B, Oliver M, Weitz DA, Viasnoff V, Butler JP, Fredberg JJ. 2005. Cytoskeletal remodelling and slow dynamics in the living cell. Nat. Mater. 4: 557–561.
- Butt HJ, Jaschke M. 1995. Calculation of thermal noise in atomic force microscopy. Nanotechnology 6: 1–7.
- Cuvelier D, Derenyi I, Bassereau P, Nassoy P. 2005. Coalescence of membrane tethers: experiments, theory, and applications. Biophys. J. 88: 2714–2726.
- Desprat N, Richert A, Simeon J, Asnacios A. 2005. Creep function of a single living cell. Biophys. J. 88: 2224–2233.
- Evans E. 2001. Probing the relation between force—Lifetime—and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30: 105–128.
- Evans E, Ritchie K. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72: 1541–1555.
- Fabry B, Maksym GN, Butler J, Glogauer M, Navajas D, Fredberg JJ. 2001. Scaling the microrheology of living cells. Phys. Rev. Lett. 87: 148102–148105.
- Fernandez P, Pullarkat PA, Ott A. 2006. A master relation defines the nonlinear viscoelasticity of single fibroblasts. Biophys. J. 90: 3796–3805.
- Ganz A, Lambert M, Saez A, Silberzan P, Buguin A, Mege RM, Ladoux B. 2006. Traction forces exerted through N-cadherin contacts. Biol. Cell 98: 721–730.
- Hodges AR, Bussmann KM, Hoh JH. 2001. Improved atomic force microscope cantilever performance by ion beam modification. Rev. Sci. Instr. 72: 3880–3883.
- Horwitz AF. 1997. Integrins and health. Sci. Amer. 276: 68–75.
- Hutter JL, Bechhoefer J. 1993. Calibration of atomic-force microscope tips. Rev. Sci. Instr. 64: 1868–1873.
- Hyonchol K, Arakawa H, Osada T, Ikai A. 2002. Quantification of fibronectin and cell surface interactions by AFM. Colloid Surf. B—Biointerfaces 25: 33–43.
-
Johnson KL.
1985.
Contact Mechanics.
Cambridge University Press: Cambridge.
10.1017/CBO9781139171731 Google Scholar
- Kim H, Arakawa H, Osada T, Ikai A. 2003. Quantification of cell adhesion force with AFM: distribution of vitronectin receptors on a living MC3T3-E1 cell. Ultramicroscopy 97: 359–363.
- Kokkoli E, Ochsenhirt SE, Tirrell M. 2004. Collective and single-molecule interactions of alpha(5)beta(1) integrins. Langmuir 20: 2397–2404.
- Lee I, Marchant RE. 2000. Force measurements on platelet surfaces with high spatial resolution under physiological conditions. Colloid Surf. B—Biointerfaces 19: 357–365.
- Lehenkari PP, Horton MA. 1999. Single integrin molecule adhesion forces in intact cells measured by atomic force microscopy. Biochem. Biophys. Res. Commun. 259: 645–650.
- Leporatti S, Gerth A, Kohler G, Kohlstrunk B, Hauschildt S, Donath E. 2006. Elasticity and adhesion of resting and lipopolysaccharide-stimulated macrophages. FEBS Lett. 580: 450–454.
- Mahaffy RE, Shih CK, MacKintosh FC, Kas J. 2000. Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys. Rev. Lett. 85: 880–883.
- Maksym GN, Fabry B, Butler JP, Navajas D, Tschumperlin DJ, Laporte JD, Fredberg JJ. 2000. Mechanical properties of cultured human airway smooth muscle cells from 0.05 to 0.4 Hz. J. Appl. Physiol. 89: 1619–1632.
- Mathur AB, Collinsworth AM, Reichert WM, Kraus WE, Truskey GA. 2001. Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J. Biomech. 34: 1545–1553.
- Obataya F, Nakamura C, Han SW, Nakamura N, Miyake J. 2005a. Mechanical sensing of the penetration of various nanoneedles into a living cell using atomic force microscopy. Biosens. Bioelectron. 20: 1652–1655.
- Obataya I, Nakamura C, Han S, Nakamura N, Miyake J. 2005b. Nanoscale operation of a living cell using an atomic force microscope with a nanoneedle. Nano Lett. 5: 27–30.
- Pierrat S, Brochard-Wyart F, Nassoy P. 2004. Enforced detachment of red blood cells adhering to surfaces: statics and dynamics. Biophys. J. 87: 2855–2869.
- Prechtel K, Bausch AR, Marchi-Artzner V, Kantlehner M, Kessler H, Merkel R. 2002. Dynamic force spectroscopy to probe adhesion strength of living cells. Phys. Rev. Lett. 89: 028101.
- Ratto TV, Rudd RE, Langry KC, Balhorn RL, McElfresh MW. 2006. Nonlinearly additive forces in multivalent ligand binding to a single protein revealed with force spectroscopy. Langmuir 22: 1749–1757.
- Rico F, Roca-Cusachs P, Gavara N, Farre R, Rotger M, Navajas D. 2005. Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips. Phys. Rev. E 72. 021914
- Roca-Cusachs P, Almendros I, Sunyer R, Gavara N, Farre R, Navajas D. 2006. Rheology of passive and adhesion-activated neutrophils probed by atomic force microscopy. Biophys. J. 91: 3508–3518.
- Sader JE, Larson I, Mulvaney P, White L. 1995. Method for the calibration of atomic force microscope cantilevers. Rev. Sci. Instr. 66: 3789–3798.
- Seifert U. 2000. Rupture of multiple parallel molecular bonds under dynamic loading. Phys. Rev. Lett. 84: 2750–2753.
- Seifert U. 2002. Dynamic strength of adhesion molecules: role of rebinding and self-consistent rates. Europhys. Lett. 58: 792–798.
- Smith BA, Tolloczko B, Martin JG, Grutter P. 2005. Probing the viscoelastic behavior of cultured airway smooth muscle cells with atomic force microscopy: stiffening induced by contractile agonist. Biophys. J. 88: 2994–3007.
- Springer TA. 1990. Adhesion receptors of the immune-system. Nature 346: 425–434.
- Stamenovic D, Wang N. 2000. Invited review: engineering approaches to cytoskeletal mechanics. J. Appl. Physiol. 89: 2085–2090.
- Sulchek TA, Friddle RW, Langry K, Lau EY, Albrecht H, Ratto TV, DeNardo SJ, Colvin ME, Noy A. 2005. Dynamic force spectroscopy of parallel individual mucin1-antibody bonds. Proc. Natl. Acad. Sci. USA. 102: 16638–16643.
- Sun M, Graham JS, Hegedus B, Marga F, Zhang Y, Forgacs G, Grandbois M. 2005. Multiple membrane tethers probed by atomic force microscopy. Biophys. J. 89: 4320–4329.
- Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS. 2003. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl. Acad. Sci. USA 100: 1484–1489.
- Tees DFJ, Woodward JT, Hammer DA. 2001. Reliability theory for receptor–ligand bond dissociation. J. Chem. Phys. 114: 7483–7496.
- Trache A, Trzeciakowski JP, Gardiner LA, Sun Z, Muthuchamy M, Guo M, Yuan SY, Meininger GA. 2005. Histamine effects on endothelial cell fibronectin interaction studied by atomic force microscopy. Biophys. J.
- Trepat X, Grabulosa M, Puig F, Maksym GN, Navajas D, Farre R. 2004. Viscoelasticity of human alveolar epithelial cells subjected to stretch. Amer. J. Physiol.-Lung Cell. Mol. Physiol.
- Trepat X, Grabulosa M, Buscemi L, Rico F, Farre R, Navajas D. 2005. Thrombin and histamine induce stiffening of alveolar epithelial cells. J. Appl. Physiol. 98: 1567–1574.
- Tseng AA. 2004. Recent developments in micromilling using focused ion beam technology. J. Micromechanic. Microengineer. 14: R15–R34.
- Williams PM. 2003. Analytical descriptions of dynamic force spectroscopy: behaviour of multiple connections. Anal. Chim. Acta 479: 107–115.
- Wojcikiewicz EP, Zhang X, Chen A, Moy VT. 2003. Contributions of molecular binding events and cellular compliance to the modulation of leukocyte adhesion. J. Cell Sci. 116: 2531–2539.
- Yang FQ, Li JCM. 2001. Adhesion of a rigid punch to an incompressible elastic film. Langmuir 17: 6524–6529.
- Zhang XH, Moy VT. 2003. Cooperative adhesion of ligand-receptor bonds. Biophys. Chem. 104: 271–278.
- Zhang XH, Wojcikiewicz E, Moy VT. 2002. Force spectroscopy of the leukocyte function-associated antigen-1/intercellular adhesion molecule-1 interaction. Biophys. J. 83: 2270–2279.
- Zhang XH, Chen A, De Leon D, Li H, Noiri E, Moy VT, Goligorsky MS. 2004a. Atomic force microscopy measurement of leukocyte-endothelial interaction. Amer. J. Physiol.—Heart Circ. Phy. 286: H359–H367.
- Zhang XH, Craig SE, Kirby H, Humphries MJ, Moy VT. 2004b. Molecular basis for the dynamic strength of the integrin alpha(4)beta(1)/VCAM-1 interaction. Biophys. J. 87: 3470–3478.
- Zhang X, Wojcikiewicz EP, Moy VT. 2006. Dynamic adhesion of T lymphocytes to endothelial cells revealed by atomic force microscopy. Exp. Biol. Med. (Maywood) 231: 1306–1312.