Use of reflectance interference contrast microscopy to characterize the endothelial glycocalyx stiffness

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 12, 2012, Pages

  Job, Kathleen M ^a   Dull, Randal O ^a,b   Hlady, Vladimir ^a  

^a University of Utah   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Albumin; Heparan sulfate; Hyaluronan

Indexed keywords

HEPARAN SULFATE; HEPARIN LYASE; HYALURONIC ACID; HYALURONIDASE; MICROSPHERE; PRONASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; GLYCOCALYX; INTERFEROMETRY; LIGHT; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PHASE CONTRAST MICROSCOPY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REFLECTANCE INTERFERENCE CONTRAST MICROSCOPY; RIGIDITY;

ANIMALS; CATTLE; CELLS, CULTURED; ELASTIC MODULUS; ENDOTHELIAL CELLS; GLYCOCALYX; HEPARITIN SULFATE; HYALURONIC ACID; HYALURONOGLUCOSAMINIDASE; LUNG; MICROSCOPY, INTERFERENCE; POLYSACCHARIDE-LYASES; PRONASE; SERUM ALBUMIN, BOVINE; STRESS, MECHANICAL; STRESS, PHYSIOLOGICAL; VASCULAR STIFFNESS;

EID: 84862625041     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00341.2011     Document Type: Article

References (57)

1. Addae-Mensah KA, Wikswo JP. Measurement techniques for cellular biomechanics in vitro. Exp Biol Med (Maywood) 233: 792-809, 2008.
2. Banerjee SD, Toole BP. Hyaluronan-binding protein in endothelial cell morphogenesis. J Cell Biol 119: 643-652, 1992.
3. Bao G, Suresh S. Cell and molecular mechanics of biological materials. Nature Mater 2: 715-725, 2003.
4. Bruinsma R, Behrisch A, Sackmann E. Adhesive switching of membranes: experiment and theory. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 61: 4253-4267, 2000.
5. Callies C, Fels J, Liashkovich I, Kliche K, Jeggle P, Kusche-Vihrog K, Oberleithner H. Membrane potential depolarization decreases the stiffness of vascular endothelial cells. J Cell Sci 124: 1936-1942, 2011.
6. Cooper JA. Effects of cytochalasin and phalloidin on actin. J Cell Biol 105: 1473-1478, 1987.
7. Costa KD. Imaging and probing cell mechanical properties with the atomic force microscope. Methods Mol Biol 319: 331-361, 2006.
8. Costa KD, Yin FC. Analysis of indentation: implications for measuring mechanical properties with atomic force microscopy. J Biomech Eng 121: 462-471, 1999.
9. Curtis AS. The mechanism of adhesion of cells to glass. A study by interference reflection microscopy. J Cell Biol 20: 199-215, 1964.
10. Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev 75: 519-560, 1995.
11. Dull RO, Mecham I, McJames S. Heparan sulfates mediate pressure-induced increase in lung endothelial hydraulic conductivity via nitric oxide/reactive oxygen species. Am J Physiol Lung Cell Mol Physiol 292: L1452-L1458, 2007.
12. Ebong EE, Macaluso FP, Spray DC, Tarbell JM. Imaging the endo-thelial glycocalyx in vitro by rapid freezing/freeze substitution transmission electron microscopy. Arterioscler Thromb Vasc Biol 31: 1908-1915, 2011.
13. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93: e136-e142, 2003.
14. Gao L, Lipowsky HH. Composition of the endothelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvasc Res 80: 394-401, 2010.
15. Georges PC, Miller WJ, Meaney DF, Sawyer ES, Janmey PA. Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J 90: 3012-3018, 2006.
16. Gingell D, Todd I. Interference reflection microscopy. A quantitative theory for image interpretation and its application to cell-substratum separation measurement. Biophys J 26: 507-526, 1979.
17. Gönnenwein S. Generic and Specific Cell Adhesion: Investigations of a Model System by Micro-Interferometry-PhD Dissertation. Munchen, Germany: Physik-Department, Technischen Universitat Munchen, 2003, pp. 1-145.
18. Helmke BP, Thakker DB, Goldman RD, Davies PF. Spatiotemporal analysis of flow-induced intermediate filament displacement in living endothelial cells. Biophys J 80: 184-194, 2001.
19. Hoffman BD, Crocker JC. Cell mechanics: dissecting the physical responses of cells to force. Annu Rev Biomed Eng 11: 259-288, 2009.
20. Huxley VH, Curry FE. Albumin modulation of capillary permeability: test of an adsorption mechanism. Am J Physiol Heart Circ Physiol 248: H264-H273, 1985.
21. Huxley VH, Curry FE. Effect of superfusate albumin on single capillary hydraulic conductivity. Am J Physiol Heart Circ Physiol 252: H395-H401, 1987.
22. Iwaki M, Ito S, Morioka M, Iwata S, Numaguchi Y, Ishii M, Kondo M, Kume H, Naruse K, Sokabe M. Mechanical stretch enhances IL-8 production in pulmonary microvascular endothelial cells. Biochem Bio-phys Res Commun 389: 531-536, 2009.
23. Jacob M, Bruegger D, Rehm M, Stoeckelhuber M, Welsch U, Conzen P, Becker BF. The endothelial glycocalyx affords compatibility of Starling's principle and high cardiac interstitial albumin levels. Cardiovasc Res 73: 575-586, 2007.
24. Janmey PA, McCulloch CA. Cell mechanics: integrating cell responses to mechanical stimuli. Annu Rev Biomed Eng 9: 1-34, 2007.
25. Kamm R, Lammerding J, Mofrad M. Cellular nanomechanics. In: Springer Handbook of Nanotechnology, edited by B. Bhushan. New York, NY: Springer, 2010, p. 1171-1200.
26. Kühner M, Sackmann E. Ultrathin hydrated dextran films grafted on glass: preparation and characterization of structural, viscous, and elastic properties by quantitative microinterferometry. Langmuir 12: 4866-4876, 1996.
27. Lemons DS, Gythiel A. Paul Langevin's 1908 paper "On the Theory of Brownian Motion". Am J Physiol 65: 1079, 1997.
28. Lo CM, Wang HB, Dembo M, Wang YL. Cell movement is guided by the rigidity of the substrate. Biophys J 79: 144-152, 2000.
29. Lopez-Quintero SV, Amaya R, Pahakis M, Tarbell JM. The endothe-lial glycocalyx mediates shear-induced changes in hydraulic conductivity. Am J Physiol Heart Circ Physiol 296: H1451-H1456, 2009.
30. Mathur AB, Truskey GA, Reichert WM. Atomic force and total internal reflection fluorescence microscopy for the study of force transmission in endothelial cells. Biophys J 78: 1725-1735, 2000.
31. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 86: 279-367, 2006.
32. Mochizuki S, Vink H, Hiramatsu O, Kajita T, Shigeto F, Spaan JAE, Kajiya F. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am J Physiol Heart Circ Physiol 285: H722-H726, 2003.
33. Neumaier KR, Elender G, Sackmann E, Merkel R. Ellipsometric microscopy. Europhys Lett 49: 14-19, 2000.
34. O'Callaghan R, Job KM, Dull RO, Hlady V. Stiffness and heterogeneity of the pulmonary endothelial glycocalyx measured by atomic force microscopy. Am J Physiol Lung Cell Mol Physiol 301: L353-L360, 2011.
35. Oberleithner H, Peters W, Kusche-Vihrog K, Korte S, Schillers H, Kliche K, Oberleithner K. Salt overload damages the glycocalyx sodium barrier of vascular endothelium. Pflügers Arch 462: 519-528, 2011.
36. Pahakis MY, Kosky JR, Dull RO, Tarbell JM. The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem Biophys Res Commun 355: 228-233, 2007.
37. Prieve D. Measurement of colloidal forces with TIRM. Adv Colloid Interface Sci 82: 93-125, 1999.
38. Rädler J, Sackmann E. Imaging optical thicknesses and separation distances of phospholipid vesicles at solid surfaces. J Physique II 3: 727-748, 1993.
39. Rädler J, Sackmann E. On the measurement of weak repulsive and frictional colloidal forces by reflection interference contrast microscopy. Langmuir 8: 848-853, 1992.
40. Sackmann E. Supported membranes: scientific and practical applications. Science 271: 43-48, 1996.
41. Satcher RL, Dewey CF. Theoretical estimates of mechanical properties of the endothelial cell cytoskeleton. Biophys J 71: 109-118, 1996.
42. Schilling J, Sengupta K, Goennenwein S, Bausch AR, Sackmann E. Absolute interfacial distance measurements by dual-wavelength reflection interference contrast microscopy. Phys Rev E Stat Nonlin Soft Matter Phys 302: L1242-L1249, 2004.
43. Scott JE, Heatley F. Hyaluronan forms specific stable tertiary structures in aqueous solution: a 13C NMR study. Proc Natl Acad Sci USA 96: 4850-4855, 1999.
44. Scott JE, Thomlinson AM, Prehm P. Supramolecular organization in streptococcal pericellular capsules is based on hyaluronan tertiary structures. Exp Cell Res 285: 1-8, 2003.
45. Simson R, Wallraff E, Faix J, Niewöhner J, Gerisch G, Sackmann E. Membrane bending modulus and adhesion energy of wild-type and mutant cells of Dictyostelium lacking talin or cortexillins. Biophys J 74: 514-522, 1998.
46. Singleton PA, Bourguignon LYW. CD44 interaction with ankyrin and IP3 receptor in lipid rafts promotes hyaluronan-mediated Ca2+ signaling leading to nitric oxide production and endothelial cell adhesion and proliferation. Exp Cell Res 295: 102-118, 2004.
47. Stevens AP, Hlady V, Dull RO. Fluorescence correlation spectroscopy can probe albumin dynamics inside lung endothelial glycocalyx. Am J Physiol Lung Cell Mol Physiol 293: L328-L335, 2007.
48. Suresh S, Spatz J, Mills JP, Micoulet A, Dao M, Lim CT, Beil M, Seufferlein T. Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. Acta Biomater 1: 15-30, 2005.
49. Tarbell JM, Pahakis MY. Mechanotransduction and the glycocalyx. J Intern Med 259: 339-350, 2006.
50. Tarbell JM, Weinbaum S, Kamm RD. Cellular fluid mechanics and mechanotransduction. Ann Biomed Eng 33: 1719-1723, 2005.
51. Thi MM, Tarbell JM, Weinbaum S, Spray DC. The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a "bumper-car" model. Proc Natl Acad Sci USA 101: 16483-16488, 2004.
52. Vogel V, Sheetz M. Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7: 265-275, 2006.
53. Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9: 121-167, 2007.
54. Wiegand G, Neumaier KR, Sackmann E. Microinterferometry: three-dimensional reconstruction of surface microtopography for thin-film and wetting studies by reflection interference contrast microscopy (RICM). Appl Opt 37: 6892-6905, 1998.
55. Zidovska A, Sackmann E. Brownian motion of nucleated cell envelopes impedes adhesion. Phys Rev Lett 96: 048103, 2006.
56. -1 regime by microinterferometry combined with fast image processing. Phys Rev A 46: 7998-8001, 1992.
57. Zwanzig R, Bixon M. Compressibility effects in the hydrodynamic theory of Brownian motion. J Fluid Mech 69; 21-25, 1975.