The morphology of adsorbed extracellular matrix assemblies is critically dependent on solution calcium concentration

Matrix Biology

Volumn 26, Issue 3, 2007, Pages 156-166

  Sherratt, Michael J ^a   Baldock, Clair ^b   Morgan, Amanda ^b   Kielty, Cay M ^b,c  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Atomic force microscopy; Calcium; Fibrillin microfibrils; Mica; Type VI collagen microfibrils

Indexed keywords

CALCIUM ION; COLLAGEN TYPE 4; FIBRILLIN; MICA; MICROCRYSTALLINE COLLAGEN; POLYLYSINE;

ADSORPTION; AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOLOGICAL ACTIVITY; CHEMISTRY; CONCENTRATION (PARAMETERS); EXTRACELLULAR MATRIX; FETUS; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL;

ADSORPTION; ANIMALS; AORTA; CALCIUM; CATTLE; COLLAGEN TYPE VI; EXTRACELLULAR MATRIX; MICROFIBRILS; MICROFILAMENT PROTEINS; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; SURFACE PROPERTIES; WATER;

EID: 33947120735     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2006.10.015     Document Type: Article

References (52)

1. Angelini T.E., Liang H., Wriggers W., and Wong G.C.L. Direct observation of counterion organization in F-actin polyelectrolyte bundles. Eur. Phys. J., E Soft Matter 16 (2005) 389-400
2. Baldock C., Koster A.J., Ziese U., Rock M.J., Sherratt M.J., Kadler K.E., Shuttleworth C.A., and Kielty C.M. The supramolecular organisation of fibrillin-rich microfibrils. J. Cell Biol. 152 (2001) 1045-1056
3. Baldock C., Sherratt M.J., Shuttleworth C.A., and Kielty C.M. The supramolecular organization of collagen VI microfibrils. J. Mol. Biol. 330 (2003) 297-307
4. Baldock C., Siegler V., Bax D.V., Cain S.A., Mellody K.T., Marson A., Haston J.L., Berry R., Wang M.C., Grossmann J.G., Roessle M., Kielty C.M., and Wess T.J. Nanostructure of fibrillin-1 reveals compact conformation of EGF arrays and mechanism for extensibility. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 11922-11927
5. Bax D.V., Bernard S.E., Lomas A., Morgan A., Humphries J., Shuttleworth C.A., Humphries M.J., and Kielty C.M. Cell adhesion to fibrillin-1 molecules and microfibrils is mediated by α5β1 and αVβ3 integrins. J. Biol. Chem. 278 (2003) 34605-34616
6. Bergkvist M., Carlsson J., and Oscarsson S. Surface-dependent conformations of human plasma fibronectin adsorbed to silica, mica, and hydrophobic surfaces, studied with use of atomic force microscopy. J. Biomed. Mater. Res. 64A (2003) 349-356
7. Bezanilla M., Manne S., Laney D.E., Lyubchenko Y.L., and Hansma H.G. Adsorption of DNA to mica, silylated mica, and minerals: characterization by atomic force microscopy. Langmuir 11 (1995) 655-659
8. Brayshaw D.J., Berry M., and McMaster T.J. Optimisation of sample preparation methods for air imaging of ocular mucins by AFM. Ultramicroscopy 97 (2003) 289-296
9. Bustamante C., Vesenka J., Tang C.L., Rees W., Guthold M., and Keller R. Circular DNA molecules imaged in air by scanning force microscopy. Biochemistry 31 (1992) 22-36
10. Cardy C.M., and Handford P.A. Metal ion dependency of microfibrils supports a rod-like conformation for fibrillin-1 calcium binding epidermal growth factor-like domains. J. Mol. Biol. 276 (1998) 855-860
11. Costa L.T., Pinto J.R., Moraes M.B., de Souza G.G.B., Sorenson M.M., Bisch P.M., and Weissmuller G. Chemical treatment of mica for atomic force microscopy can affect biological sample conformation. Biophys. Chem. 109 (2004) 63-71
12. Czajkowsky D.M., and Shao Z. Inhibition of protein adsorption to muscovite mica by monovalent cations. J. Microsc. Oxford 211 (2003) 1-7
13. Downing A.K., Knott V., Werner J.M., Cardy C.M., Campbell I.D., and Handford P.A. Solution structure of a pair of calcium-binding epidermal growth factor-like domains: implications for the Marfan syndrome and other genetic disorders. Cell 85 (1996) 597-605
14. El Kirat K., Burton I., Dupres V., and Dufrene Y.F. Sample preparation procedures for biological atomic force microscopy. J. Microsc. 218 (2005) 199-207
15. Ellingham R.B., Berry M., Stevenson D., and Corfield A.P. Secreted human conjunctival mucus contains MUC5AC glycoforms. Glycobiology 9 (1999) 1181-1189
16. Ellis J.S., Abdelhady H.G., Allen S., Davies M.C., Roberts C.J., Tendler S.J.B., and Williams P.M. Direct atomic force microscopy observations of monovalent ion induced binding of DNA to mica. J. Microsc. 215 (2004) 297-301
17. Engel A., Schoenenberger C.-A., and Muller D.J. High resolution imaging of native biological sample surfaces using scanning probe microscopy. Curr Opin. Struct. Biol. 7 (1997) 279-284
18. Gaines G.L., and Tabor D. Surface adhesion and elastic properties of mica. Nature 170 (1956) 1304-1305
19. Garcia A.J., Vega M.D., and Boettiger D. Modulation of cell proliferation and differentiation through substrate-dependent changes in fibronectin conformation. Mol. Biol. Cell. 10 (1999) 785-798
20. Glanville R.W., Qian R.Q., McClure D.W., and Maslen C.L. Calcium binding, hydroxylation, and glycosylation of the precursor epidermal growth factor-like domains of fibrillin-1, the Marfan gene protein. J. Biol. Chem. 269 (1994) 26630-26634
21. Hansma H.G., and Laney D.E. DNA binding to mica correlates with cationic radius: assay by atomic force microscopy. Biophys. J. 70 (1996) 1933-1939
22. Kielty C.M., Berry L., Whittaker S.P., Grant M.E., and Shuttleworth C.A. Microfibrillar assemblies of fetal bovine skin-developmental expression and relative abundance of type-vi collagen and fibrillin. Matrix 13 (1993) 103-112
23. Kielty C.M., Cummings C., Whittaker S.P., Shuttleworth C.A., and Grant M.E. Isolation and ultrastructural analysis of microfibrillar structures from fetal bovine elastic tissues - relative abundance and supramolecular architecture of type-VI collagen assemblies and fibrillin. J. Cell Sci. 99 (1991) 797-807
24. Kielty C.M., Sherratt M.J., Marson A., and Baldock C. Fibrillin microfibrils. Adv. Protein Chem. 70 (2005) 405-436
25. Kielty C.M., and Shuttleworth C.A. Microfibrillar elements of the dermal matrix. Microsc. Res. Tech. 38 (1997) 413-427
26. Knupp C., Pinali C., Munro P.M., Gruber H.E., Sherratt M.J., Baldock C., and Squire J.M. Structural correlation between collagen VI microfibrils and collagen banded aggregates. J. Struct. Biol. 154 (2006) 312-326
27. Kocsis E., Trus B.L., Steer C.J., Bisher M.E., and Steven A.C. Image averaging of flexible fibrous macromolecules: the clathrin triskeleton has an elastic proximal segment. J. Struct. Biol. 107 (1991) 6-14
28. Lamblin G., Degroote S., Perini J.M., Delmotte P., Scharfman A.E., Davril M., Lo-Guidice J.M., Houdret N., Dumur V., Klein A., and Roussel P. Human airway mucin glycosylation: a combinatory of carbohydrate determinants which vary in cystic fibrosis. Glycoconj. J. 18 (2001) 661-684
29. Lau A.W.C., and Pincus P. Binding of oppositely charged membranes and membrane reorganization. Eur. Phys. J., B Cond. Matter Phys. 10 (1999) 175-180
30. Leifer D., Lipton S.A., Barnstable C.J., and Masland R.H. Monoclonal antibody to Thy-1 enhances regulation of processes by rat retinal ganglion cells in culture. Science 224 (1984) 303-306
31. Luckham P.F., and Klein J. Forces between mica surfaces bearing adsorbed poly-electrolyte poly-l-lysine, in aqueous-media. J. Chem. Soc., Faraday Trans. I 80 (1984) 865-878
32. Marson A., Rock M.J., Cain S.A., Freeman L.J., Morgan A., Mellody K., Shuttleworth C.A., Baldock C., and Kielty C.M. Homotypic fibrillin-1 interactions in microfibril assembly. J. Biol. Chem. 280 (2005) 5013-5021
33. McMaster T.J., Berry M., Corfield A.P., and Miles M.J. Atomic force microscopy of the submolecular architecture of hydrated ocular mucins. Biophys. J. 77 (1999) 533-541
34. Mould A.P., Holmes D.F., Kadler K.E., and Chapman J.A. Mica sandwich technique for preparing macromolecules for rotary shadowing. J. Ultrastruct. Res. 91 (1985) 66-76
35. Muller D.J., Amrein M., and Engel A. Adsorption of biological molecules to a solid support for scanning probe microscopy. J. Struct. Biol. 119 (1997) 172-188
36. Muller D.J., and Anderson K. Biomolecular imaging using atomic force microscopy. Trends Biotechnol. 20 (2002) S45-S49
37. Nath N., Hyun J., Ma H., and Chilkoti A. Surface engineering strategies for control of protein and cell interactions. Surf. Sci. 570 (2004) 98-110
38. Pamula E., De Cupere V., Dufrene Y.F., and Rouxhet P.G. Nanoscale organization of adsorbed collagen: influence of substrate hydrophobicity and adsorption time. J. Colloid Interface Sci. 271 (2004) 80-91
39. Pastre D., Pietrement O., Fusil S., Landousy F., Jeusset J., David M.-O., Hamon L., Le Cam E., and Zozime A. Adsorption of DNA to mica mediated by divalent counterions: a theoretical and experimental study. Biophys. J. 85 (2003) 2507-2518
40. Raspanti M., Congiu T., and Guizzardi S. Tapping-mode atomic force microscopy in fluid of hydrated extracellular matrix. Matrix Biol. 20 (2001) 601-604
41. Raspanti M., Protasoni M., Manelli A., Guizzardi S., Mantovani V., and Sala A. The extracellular matrix of the human aortic wall: ultrastructural observations by FEG-SEM and tapping-mode AFM. Micron 37 (2006) 81-86
42. Reinhardt D.P., Keene D.R., Corson G.M., Poschl E., Bachinger H.P., Gambee J.E., and Sakai L.Y. Fibrillin-1: organization in microfibrils and structural properties. J. Mol. Biol. 258 (1996) 104-116
43. Rose D.M., Bleam M.L., Record M.T., and Bryant R.G. Mg-25 NMR in DNA solutions: dominance of site binding effects. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 6289-6292
44. Sherratt M.J., Baldock C., Haston J.L., Holmes D.F., Jones C.J.P., Shuttleworth C.A., Wess T.J., and Kielty C.M. Fibrillin microfibrils are stiff reinforcing fibres in compliant tissues. J. Mol. Biol. 332 (2003) 183-193
45. Sherratt M.J., Holmes D.F., Shuttleworth C.A., and Kielty C.M. Substrate-dependent morphology of supramolecular assemblies: fibrillin and type-VI collagen microfibrils. Biophys. J. 86 (2004) 3211-3222
46. Sherratt M.J., Bax D.V., Chaudhry S.S., Hodson N., Lu J.R., Saravanapavan P., and Kielty C.M. Substrate chemistry influences the morphology and biological function of adsorbed extracellular matrix assemblies. Biomaterials 26 (2005) 7192-7206
47. Shin H., Seongbong J., and Mikos A.G. Biomimetic materials for tissue engineering. Biomaterials 24 (2003) 4353-4364
48. Thundat T., Allison D.P., Warmack R.J., Brown G.M., Jacobson K.B., Schrick J.J., and Ferrell T.L. Atomic force microscopy of DNA on mica and chemically modified mica. Scanning Microsc. 6 (1992) 911-918
49. Tulla M., Pentikainen O.T., Viitasalo T., Kapyla J., Impola U., Nykvist P., Nissinen L., Johnson M.S., and Heino J. Selective binding of collagen subtypes by integrin alpha I-1, alpha I-2, and alpha I-10 domains. J. Biol. Chem. 276 (2001) 48206-48212
50. vanHeel M., Harauz G., Orlova E.V., Schmidt R., and Schatz M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116 (1996) 17-24
51. Wagner P. Immobilization strategies for biological scanning probe microscopy. FEBS Lett. 430 (1998) 112-115
52. Wess T.J., Purslow P.P., Sherratt M.J., Ashworth J., Shuttleworth C.A., and Kielty C.M. Calcium determines the supramolecular organization of fibrillin-rich microfibrils. J. Cell Biol. 141 (1998) 829-837