Skip to main content
Log in

How Cells Feel Their Environment: A Focus on Early Dynamic Events

  • Published:
Cellular and Molecular Bioengineering Aims and scope Submit manuscript

Abstract

It is now well demonstrated that cell adhesion to a foreign surface strongly influences prominent functions such as survival, proliferation, differentiation, migration, or mediator release. Thus, a current challenge of major practical and theoretical interest is to understand how cells process and integrate environmental cues to determine future behavior. The purpose of this review is to summarize some pieces of information that might serve this task. Three sequential points are discussed. First, selected examples are presented to illustrate the influence of substratum chemistry, topography, and mechanical properties on nearly all aspects of cell behavior observed during the days following adhesion. Second, we review reported evidence that long term cell behavior is highly dependent on the alterations of cell shape and cytoskeletal organization that are often initiated during the minutes to hours following adhesion. Third, we review recently obtained information on cell membrane roughness and dynamics, as well as kinetics and mechanics of molecular interactions. This knowledge is required to understand the influence of substratum structure on cell signaling during the first minute following contact, before the appearance of detectable structural changes. It is suggested that unraveling the earliest phenomena following cell-to-substratum encounter might provide a tractable way of better understanding subsequent events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2

Similar content being viewed by others

References

  1. Allen L. T., E. J. P. Fox, I. Blute, Z. D. Kelly, Y. Rochev, A. K. Keenan, K. A. Dawson, and W. M. Gallagher. Interaction of soft condensed materials with living cells: phenotype/transcriptome correlations for the hydrophobic effect. Proc. Natl. Acad. Sci. (USA) 100:6331–6336, 2003

    Article  Google Scholar 

  2. Bohnet S., R. Ananthakrishnan, A. Mogilner, and J. J. Meister. Weak force stalls protrusion at the leading edge of the lamellipodium. Biophys. J. 90:1810–1820, 2006

    Article  Google Scholar 

  3. Bruinsma R., A. Behrisch, and E. Sackmann. Adhesive switching of membranes: experiment and theory. Phys. Rev. E 61:4253–4267, 2000

    Article  Google Scholar 

  4. Burroughs N. G., Z. Lazic, and P. A. van der Merwe. Ligand detection and discrimination by spatial relocalization: a kinase-phosphatase segregation model of TCR activation. Biophys. J. 91:1619–1629, 2006

    Article  Google Scholar 

  5. Calvacanti-Adam E. A., T. Volberg, A. Micoulet, H. Kessler, B. Geiger, and J. P. Spatz. Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys. J. 92:2964–2974, 2007

    Article  Google Scholar 

  6. Capo C., P. Bongrand, A. M. Benoliel, and R. Depieds. Nonspecific recognition in phagocytosis: ingestion of aldehyde treated erythrocytes by rat peritoneal macrophages. Immunology 36:501–508, 1979

    Google Scholar 

  7. Chen W., E. A. Evans, R. P. McEver, and C. Zhu. Monitoring receptor-ligand interactions between surfaces by thermal fluctuations. Biophys. J. 94:694–701, 2008

    Article  Google Scholar 

  8. Chen C. S., M. Mrksich, S. Huang, G. M. Whitesides, and D. E. Ingber. Geometric control of cell life and death. Science 276:1425–1428, 1997

    Article  Google Scholar 

  9. Choquet D., D. P. Felsenfeld, and M. P. Sheetz. Extracellular matrix rigidity causes strengthening of integrin–cytoskeleton linkages. Cell 88:39–48, 1997

    Article  Google Scholar 

  10. Clark P., P. Connolly, A. S. G. Curtis, J. A. T. Dow, and C. D. W. Wilkinson. Topographical control of cell behaviour: II. Multiple grooved substrata. Development 108:635–644, 1990

    Google Scholar 

  11. Cukierman E., R. Pankov, D. R. Stevens, and K. M. Yamada. Taking cell–matrix adhesions to the third dimension. Science 294:1708–1712, 2001

    Article  Google Scholar 

  12. Curtis A. S. G. The mechanism of adhesion of cells to glass. J. Cell Biol. 20:199–215, 1964

    Article  Google Scholar 

  13. Curtis A. S. G., J. V. Forrester, C. McInnes, and F. Lawrie. Adhesion of cells to polystyrene surfaces. J. Cell Biol. 97:1500–1506, 1983

    Article  Google Scholar 

  14. Curtis A. S. G., N. Gadegaard, M. J. Dalby, M. O. Riehle, C. D. W. Wilkinson, and G. Artchison. Cells react to nanoscale order and symmetry in their surroundings. IEEE Trans. Nanobiosci. 3:61, 2004

    Article  Google Scholar 

  15. Dalby M. J., S. Childs, M. O. Riehle, H. J. H. Johnstone, S. Affrossman, and A. S. G. Curtis. Fibroblast reaction to island topography: changes in cytoskeleton and morphology with time. Biomaterials 24:927–935, 2003

    Article  Google Scholar 

  16. Dalby M. J., S. J. Yarwood, M. O. Riehle, H. J. Johnstone, S. Affrossman, and A. S. Curtis. Increasing fibroblast response to materials using nanotopography: morphological and genetic measurements of cell response to 13-nm-high polymer demixed islands. Exp. Cell Res. 276:1–9, 2002

    Article  Google Scholar 

  17. Döbereiner H. G., B. Dubin-Thaler, G. Giannone, H. S. Xenias, and M. P. Sheetz. Dynamic phase transitions in cell spreading. Phys. Rev. Lett. 93:108105, 2004

    Article  Google Scholar 

  18. Engler A. J., S. Sen, H. L. Sweeney, and D. E. Discher. Matric elasticity directs stem cell lineage specification. Cell 126:677–689, 2006

    Article  Google Scholar 

  19. Evans E., V. Heinrich, A. Leung, and K. Kinoshita. Nano- to microscale dynamics of P-selectin detachment from leukocyte interfaces. I. Membrane separation from the cytoskeleton. Biophys. J. 88:2288–2298, 2005

    Article  Google Scholar 

  20. Forgacs G., S. H. Yook, P. A. Janmey, H. Jeong, C. G. Burd. Role of the cytoskeleton in signaling networks. J. Cell Sci. 117:2769–2775, 2004

    Article  Google Scholar 

  21. Frey M. T., I. Y. Tsai, T. P. Russell, S. K. Hanks, and Y. L. Wang. Cellular responses to substrate topography: role of myosin II and focal adhesion kinase. Biophys. J. 90:3774–3782, 2006

    Article  Google Scholar 

  22. Garcia A. J., and D. Boettiger. Integrin–fibronectin interactions at the cell-material interface: initial integrin binding and signaling. Biomaterials 20:2427–2333, 1999

    Article  Google Scholar 

  23. Giancotti F. G., and E. Ruoslahti. Integrin signaling. Science 285:1028–1032, 1999

    Article  Google Scholar 

  24. Gingell D., I. Todd, and J. Bailey. Topography of cell-glass apposition revealed by total internal reflection fluorescence of volume markers. J. Cell Biol. 100:1334–1338, 1985

    Article  Google Scholar 

  25. Grinnell F., and M. K. Feld. Fibronectin adsorption on hydrophilic and hydrophobic surfaces detected by antibody binding and analyzed during cell adhesion in serum-containing medium. J. Biol. Chem. 257:4888–4893, 1982

    Google Scholar 

  26. Harris A. K., P. Wild, and D. Stopak. Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208:177–179, 1980

    Article  Google Scholar 

  27. Haugh J. M. Membrane-binding/modification model of signaling protein activation and analysis of its control by cell morphology. Biophys. J. 107:L93–L95, 2007

    Article  Google Scholar 

  28. Horoyan M., A. M. Benoliel, C. Capo, and P. Bongrand. Localization of calcium and microfilament changes in mechanically stressed cells. Cell Biophys. 17:243–256, 1990

    Google Scholar 

  29. Janmey P. A. The cytoskeleton and cell signalling: component localization and mechanical coupling. Physiol. Rev. 78:763–781, 1998

    Google Scholar 

  30. Jiang H., and F. Grinnell. Cell–matrix entanglement and mechanical anchorage of fibroblasts in three-dimensional collagen matrices. Mol. Biol. Cell 16:5070–5076, 2005

    Article  Google Scholar 

  31. Jirouskova M., J. K. Jaiswal, and B. S. Coller. Ligand density dramatically affects integrin αIIbβ-mediated platelet signaling and spreading. Blood 109:5260–5269, 2007

    Article  Google Scholar 

  32. Jones G. E., R. Gillett, and T. Partridge. Rapid modification of the morphology of cell contact sites during the aggregation of limpet haemocytes. J. Cell Sci. 22:21–33, 1976

    Google Scholar 

  33. Kostic A., and M. P. Sheetz. Fibronectin rigidity response through Fyn and p130 Cas recruitment to the leading edge. Mol. Biol. Cell 17:2684–2695, 2006

    Article  Google Scholar 

  34. Kung C. A possible unifying principle for mechanosensation. Nature 436:647–654, 2005

    Article  Google Scholar 

  35. Leupin O., R. Zaru, T. Laroche, S. Müller, and S. Valitutti. Exclusion of CD45 from the T-cell receptor signaling area in antigen-stimulated T lymphocytes. Curr. Biol. 10:277–280, 2000

    Article  Google Scholar 

  36. Lo C. M., H. B. Wang, M. Dembo, and Y. L. Wang. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79:144–152, 2000

    Google Scholar 

  37. Luo B. H., C. V. Carman, and T. A. Springer. Structural basis of integrin regulation and signaling. Ann. Rev. Immunol. 25:619–647, 2007

    Article  Google Scholar 

  38. Maheswari G., G. Brown, D. Lauffenburger, A. Wells, and L. G. Griffith. Cell adhesion and motility depend on nanoscale RGD clustering. J. Cell Sci. 113:1677–1686, 2000

    Google Scholar 

  39. Mammoto A., S. Huang, and D. E. Ingber. Filamin links cell shape and cytoskeletal structure to Rho regulation by controlling accumulation of p190RhoGAP in lipid rafts. J. Cell Sci. 120:456–467, 2007

    Article  Google Scholar 

  40. Mao Y., and J. E. Schwarzbauer. Stimulatory effects of a three-dimensional microenvironment on cell-mediated fibronectin fibrillogenesis. J. Cell Sci. 118:4427–4436, 2005

    Article  Google Scholar 

  41. Marshall B. T., K. K. Sarangapani, J. Lou, R. P. McEver, and C. Zhu. Force history dependence of receptor–ligand dissociation. Biophys. J. 88:1458–1466, 2005

    Article  Google Scholar 

  42. Matthews B. D., D. R. Overby, R. Mannix, and D. E. Ingber. Cellular adaptation to mechanical stress: role of integrins, rho, cytoskeletal tension and mechanosensitive ion channels. J. Cell Sci. 119:508–518, 2006

    Article  Google Scholar 

  43. McBeath R., D. M. Pirone, C. M. Nelson, K. Bhadriraju, and C. S. Chen. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6:483–495, 2004

    Article  Google Scholar 

  44. Mossman K. D., G. Campi, J. T. Groves, and M. L. Dustin. Altered TCR signaling from geometrically repatterned immunological synapses. Science 310:1191–1193, 2005

    Article  Google Scholar 

  45. Pankov R., Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K. M. Yamada. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170:793–802, 2005

    Article  Google Scholar 

  46. Patel K. D., M. U. Nollert, and R. P. McEver. P-selectin must extend a sufficient length from the plasma membrane to mediate rolling of neutrophils. J. Cell Biol. 131:1893–1902, 1995

    Article  Google Scholar 

  47. Pennington S. R., B. J. Foster, S. R. Hawley, R. E. Jenkins, O. Zolle, M. R. H. White, C. J. McNamee, P. Sheterline, A. W. M. Simpson. Cell shape-dependent control of Ca2+ influx and cell cycle progression in Swiss 3T3 fibro blasts. J. Biol. Chem. 282:32112–32120, 2007

    Article  Google Scholar 

  48. Pierres A., A. M. Benoliel, and P. Bongrand. Cell fitting to adhesive surfaces: a prerequisite to firm attachment and subsequent events. Eur. Cell Mater. 3:31–45, 2002

    Google Scholar 

  49. Pierres, A., A. M. Benoliel, D. Touchard, and P. Bongrand. How cells tiptoe on adhesive surfaces before sticking. Biophys. J. (in press)

  50. Pierres A., A. Prakasam, D. Touchard, A. M. Benoliel, P. Bongrand, and D. Leckband. Dissecting subsecond cadherin bound states reveals an efficient way for cells to achieve ultrafast probing of their environment. FEBS Lett. 581:1841–1846, 2007

    Article  Google Scholar 

  51. Pierres A., O. Tissot, B. Malissen, and P. Bongrand. Dynamic adhesion of CD8-positive cells to antibody-coated surfaces the initial step is independent of microfilaments and intracellular domains of cell-binding molecules. J. Cell Biol. 125:945–953, 1994

    Article  Google Scholar 

  52. Pierres A., D. Touchard, A. M. Benoliel, and P. Bongrand. Dissecting streptavidin–biotin interaction with a laminar flow chamber. Biophys. J. 82:3214–3223, 2002

    Google Scholar 

  53. Pierres A., J. Vitte, A. M. Benoliel, and P. Bongrand. Dissecting individual ligand–receptor bonds with a laminar flow chamber. Biophys. Rev. Lett. 1:231–257, 2006

    Article  Google Scholar 

  54. Pincet F. and J. Husson. The solution to the streptavidin–biotin paradox: the influence of history on the strength of single molecular bonds. Biophys. J. 89:4374–4381, 2005

    Article  Google Scholar 

  55. Reynwar B. J., G. Illya, V. A. Harmandaris, M. M. Muller, K. Kremer, and M. Deserno. Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447:461–465, 2007

    Article  Google Scholar 

  56. Ridley A. J., M. A. Schwartz, K. Burridge, R. A. Firtel, M. H. Ginsberg, G. Borisy, J. T. Parsons, and A. R. Horwitz. Cell migration: integrating signals from front to back. Science 302:1704–1709, 2003

    Article  Google Scholar 

  57. Riveline D., E. Zamir, N. Q. Balaban, U. S. Schwarz, T. Ishizaki, S. Narumiya, Z. Kam, B. Geiger, and A. D. Bershadsky. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of contacts by an mDia1-dependent and ROC-independent mechanism. J. Cell Biol. 153:1175–1185, 2001

    Article  Google Scholar 

  58. Robert P., A. M. Benoliel, A. Pierres, and P. Bongrand. What is the biological relevance of the specific bond properties revealed by single molecule studies? J. Mol. Recognit. 20:432–447, 2007

    Article  Google Scholar 

  59. Robert P., Limozin L., Benoliel A. M., Pierres A., Bongrand P. Glycocalyx regulation of cell adhesion. In: Principles of Cellular Engineering, edited by M. R. King, Amsterdam: Elsevier, Academic Press, 2006, pp 143–169

    Chapter  Google Scholar 

  60. Runyan R. B., J. Versakovic, and B. D. Shur. Functionally distinct laminin receptors mediate cell adhesion and spreading: the requirement for surface galactosyltransferase in cell spreading. J. Cell Biol. 107:1863–1871, 1988

    Article  Google Scholar 

  61. Sabri S., A. Pierres, A. M. Benoliel, and P. Bongrand. Influence of surface charges on cell adhesion: difference between static and dynamic conditions. Biochem. Cell Biol. 73:411–420, 1995

    Article  Google Scholar 

  62. Seifert U. Rupture of multiple parallel molecular bonds under dynamic loading. Phys. Rev. Lett. 84:2750–2753, 2000

    Article  Google Scholar 

  63. Shao J. Y., H. P. Ting-Beall, and R. M. Hochmuth. Static and dynamic lengths of neutrophil microvilli. Proc. Natl. Acad. Sci. USA 95:6797–6802, 1998

    Article  Google Scholar 

  64. Simson R., E. Wallraff, J. Faix, J. Niewöhner, G. Gerish, and E. Sackmann. Membrane bending modulus and adhesion energy of wild-type and mutant cells of Dictyostelium lacking talin or cortexillins. Biophys. J. 74:514–522, 1998

    Google Scholar 

  65. Soler M., C. Merant, C. Servant, M. Fraterno, C. Allasia, J. C. Lissitzky, P. Bongrand, and C. Foa. Leukosialin (CD43) behavior during adhesion of human monocytic THP-1 cells to red blood cells. J. Leukocyte Biol. 61:609–618, 1997

    Google Scholar 

  66. Taubenberger A., D. A. Cisneros, J. Friedrichs, P. H. Puech, D. J. Muller, and C. M. Franz. Revealing early steps of α2β1 integrin-mediated adhesion to collagen type I by using single-cell force spectroscopy. Mol. Biol. Cell 18:1634–1644, 2007

    Article  Google Scholar 

  67. Uetz P., L. Giot, G. Cagney, T. A. Mansfield, R. S. Judson, J. R. Knight, D. Lockshon, V. Narayan, M. Srinivasan, P. Pochart, A. Qureshi-Emili, Y. Li, B. Godwin, D. Conover, T. Kalbfleisch, G. Vijayadamovar, M. Yang, M. Johnston, S. Fields, and J. M. Rothberg. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403:623–627, 2000

    Article  Google Scholar 

  68. Vitte J., A. M. Benoliel, A. Pierres, and P. Bongrand. Is there a predictable relationship between surface physical–chemical properties and cell behaviour at the interface? Eur. Cells Mater. 7:52–63, 2004

    Google Scholar 

  69. Williams T. E., S. Nagarajan, P. Selvaraj, and C. Zhu. Quantifying the impact of membrane microtopology on effective two-dimensional affinity. J. Biol. Chem. 276:13283–13288, 2001

    Article  Google Scholar 

  70. Zhao X. H., C. Lashinger, P. Arora, K. Szaszi, A. Kapus, and C. A. McCulloch. Force activates smooth muscle α-actin promoter activity through the Rho signaling pathway. J. Cell Sci. 120:1801–1809, 2007

    Article  Google Scholar 

  71. Zidovska A., and E. Sackmann. Brownian motion of nucleated cell envelopes impedes adhesion. Phys. Rev. Lett. 96:048103, 2006

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pierre Bongrand.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cretel, E., Pierres, A., Benoliel, AM. et al. How Cells Feel Their Environment: A Focus on Early Dynamic Events. Cel. Mol. Bioeng. 1, 5–14 (2008). https://doi.org/10.1007/s12195-008-0009-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12195-008-0009-7

Keywords

Navigation