Analytical investigation of protein mediation between biomaterials and cells

Materials Express

Volumn 2, Issue 1, 2012, Pages 1-22

  Tagaya, Motohiro ^a,b   Ikoma, Toshiyuki ^b,c   Hanagata, Nobutaka ^b   Tanaka, Junzo ^b,c  

^a NAGAOKA UNIVERSITY OF TECHNOLOGY   (Japan)

^b NATIONAL INSTITUTE FOR MATERIALS SCIENCE   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Cell adhesion; Hydroxyapatite; Interfacial viscoelasticity; Protein Adsorption; QCM D

Indexed keywords

EID: 84871599971     PISSN: 21585849     EISSN: 21585857     Source Type: Journal    
DOI: 10.1166/mex.2012.1053     Document Type: Review

References (214)

1. B. Kasemo; Biological surface science; Surface Science 500, 656 (2002).
2. A. El-Ghannam, P. Ducheyne, and I. M. Shapiro; The effect of serum protein adsorption on osteoblast adhesion to bioactive glass and hydroxyapatite; Journal of Orthopaedic Research 17, 340 (1999).
3. M. Rouahi, E. Champion, O. Gallet, A. Jada, and K. Anselme; Physico-chemical characteristics and protein adsorption potential of hydroxyapatite particles: Influence on in vitro biocompatibility of ceramics after sintering; Colloids Surf., B: Biointerfaces 47, 10 (2006).
4. K. Aneslme; Osteoblast adhesion on biomaterials; Biomaterials 21, 667 (2000).
5. M. D. Pierschbacher and E. Ruoslahti; Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule; Nature 309, 30 (1984).
6. F. Barrere, T. Mahmood, K. Degroot, and C. Vanblitterswijk; Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule; Mater. Sci. Eng. R 59, 38 (2008).
7. N. Nath, J. Hyun, H. Ma, and A. Chilkoti; Surface engineering strategies for control of protein and cell interactions; Surface Science 570, 98 (2004).
8. J. G. Steele, G. Johnson, and P. A. Underwood; Role of serum vitronectin and fibronectin in adhesion of fibroblasts following seeding onto tissue culture polystyrene; J. Biomed. Mater. Res. 26, 681 (1992).
9. S. J. Huang and D. E. Ingber; Shape-dependent control of cell growth, differentiation, and apoptosis: Switching between attractors in cell regulatory networks; Experimental Cell Research 261, 91 (2000).
10. S. Chen, M. Mrksich, S. Huang, G. M. Whitesides, and D. E. Ingber; Geometric control of cell life and death; Science 276, 1425 (1997).
11. N. Hanagata, T. Takemura, A. Monkawa, T. Ikoma, and J. Tanaka; Pre-adsorbed Type-I collagen structure-dependent changes in osteoblastic phenotype; Biochem. Biophys. Res. Commun. 344, 1234 (2006).
12. N. Hanagata, T. Takemura, A. Monkawa, T. Ikoma, and J. Tanaka; Phenotype and gene expression pattern of osteoblast-like cells cultured on polystyrene and hydroxyapatite with pre-adsorbed type-I collagen; J. Biomed. Mater. Res. A 83A, 362 (2007).
13. E. Ruoslahti and M. D. Pierschbacher; New perspectives in cell adhesion: RGD and integrins; Science 238, 491 (1987).
14. M. Arnold, E. A. Cavalcanti-Adam, R. Glass, J. Bluemmel, W. Eck, M. Kantlehner, H. Kessler, and J. P. Spatz; Activation of integrin function by nanopatterned adhesive interface; Chem. Phys. Chem. 75, 383 (2004).
15. K. E. Michael, V. N. Vernekar, B. G. Keselowsky, J. C. Meredith, R. A. Latour, and A. J. Garcia; Adsorption-induced conformational changes in fibronectin due to interactions with well-defined surface chemistries; Langmuir 19, 8033 (2003).
16. G. Keselowsky, D. M. Collard, and A. J. Garcia; Surface chemistry modulates fibronectin conformation and directs integrin binding and specifity to control cell adhesion; J. Biomed. Mater. Res. Part A 66A, 247 (2003).
17. W. Grainger, G. Pavon-Djavid, V. Migonney, and M. Josefowicz; Assessment of fibronectin conformation adsorbed to polytetrafluoroethylene surfaces from serum protein mixtures and correlation to support of cell attachment in culture; J. Biomater. Sci. Polym. Ed. 14, 973 (2003).
18. N. A. Kefalides and R. J Winzler; The chemistry of glomerular basement mem brane and its relation to collagen; Biochemistry 5, 702 (1966).
19. N. A. Kefalides and B. Denduchis; Structural components of epithelial and endothelial basement membranes; Biochemistry 8, 4613 (1969).
20. R. J. Spiro; Studies on the renal glomerular basement membrane: Preparation and chemical composition; J. Biol. Chem. 242, 1915 (1967).
21. R. J. Pei, X. Q. Cui, X. R. Yang, and E. K. R. Wang; Real-time immunoassay of antibody activity in serum by surface plasmon resonance biosensor; Talanta 53, 481 (2000).
22. A. N. Asanov, W. W. Wilson, and P. B. Odham; Regenerable biosensor platform: A total internal reflection fluorescence cell with electrochemical control; Anal. Chem. 70, 1156 (1998).
23. B. Lassen and M. Malmsten; Competitive protein adsorption studied with TIRF and ellipsometry; J. Colloid Interface Sci. 179, 470 (1996).
24. G. H. Cross, A. Reeves, S. Brand, M. J. Swann, L. L. Peel, N. J. Freeman, and J. R. Lu; The metrics of surface adsorbed small molecules on the Young's fringe dual-slab waveguide interferometer more options; J. Phys. D: Appl. Phys. 37, 74 (2004).
25. N. J. Freeman, L. L. Peel, M. J. Swann, G. H. Cross, A. Reeves, S. Brand, and J. R. Lu; Real time, high resolution studies of protein adsorption and structure at the solid-liquid interface using dual polarization interferometry; J. Phys.: Condens. Matter 16, S2493 (2004).
26. R. Goobes, G. Goobes, C. T. Campbell, and P. S. Stayton; Thermodynamics of statherin adsorption onto hydroxyapatite more options; Biochemistry 45, 5576 (2006).
27. M. J. Pollitt, G. Buckton, S. Brocchini, and H. O. Alpar; Calorimetric study of bovine serum albumin dilution and adsorption onto polystyrene particles; Int. J. Pharm. 298, 333 (2005).
28. R. M. A. Azzam, P. G. Rigby, and J. A. Krueger; Kinetics of protein adsorption and immunological reactions at a liquid-solid interface by ellipsometry; Physics in Medicine and Biology 22, 422 (1977).
29. R. Seitz, R. Brings, and R. Geiger; Protein adsorption on solidliquid interfaces monitored by laser-ellipsometry; Appl. Surf. Sci. 252, 154 (2005).
30. J. L. Ong, K. K. Chittur, and L. C. Lucas; Dissolution/ repricipitation and protein adsorption studies of calcium phosphate coatings by FTIR/ATR techniques; J. Biomed. Mater. Res. 28, 1337 (1994).
31. H. Zeng, K. K. Chittur, and W. R. Lacefield; Analysis of bovine serum albumin adsorption on calcium phosphate and titanium surfaces; Biomaterials 20, 377 (1999).
32. T. Nomura and M. Okuhara; Frequency shifts of piezoelectric quartz crystals immersed in organic liquids; Anal. Chim. Acta 142, 281 (1982).
33. R. C. Ebersole, R. P. Foss, and M. D. Ward; Piezoelectric cell growth sensor; Bio/Technology 9, 450 (1991).
34. M. Edvardsson, S. Svedhem, G. Wang, R. Richter, M. Rodahl, and B. Kasemo; QCM-D and reflectometry instrument: Applications to supported lipid structures and their biomolecular interactions; Anal. Chem. 81, 349 (2009).
35. F. Höök, J. Voros, M. Rodahl, R. Kurrat, P. Boni, J. J. Ramsden, M. Textor, N. D. Spencer, P. Tengvall, J. Gold, and B. Kasemo; A comparative study of protein adsorption on titanium oxide surfaces using in situ elipsometry, optical waveguide lightmode spectroscopy, and quartz crystal microbalance/dissipation; Colloids Surf., B: Biointerfaces 24, 155 (2002).
36. M. Berglin, E. Pinori, A. Sellborn, M. Andersson, M. Hulander, and H. Elwing; Fibrinogen adsorption and conformational change on model polymers: Novel aspects of mutual molecular Rearrangement; Langmuir 25, 5602 (2009).
37. J. Curie and P. Curie; Sur l'électricité polaire dans les cristaux hémièdres à faces inclinées; Comptes Rendus de l'Académie des Sciences, Paris 91, 294 (1880).
38. L. Rayleigh; On the free vibrations of an infinite plate of homogeneous isotropic elastic matter; Proceedings of the London Mathematical Society 20, 225 (1889).
39. W. G. Cady; The piezoelectric resonator; Phys. Rev. 17, 531 (1921).
40. F. R. Lack, G. W. Willard, and I. E. Fair; Some improvements in quartz crystal circuit elements; Bell System Technical Journal 13, 453 (1934).
41. C. K. O'Sullivan and G. G. Guilbault; Commercial quartz crystal microbalances: Theory and applications; Biosens. Bioelectron. 14, 663 (1999).
42. A. Janshoff, H. J. Galla, and C. Steinem; The quartz crystal microbalance in life science; Angewandte Chemie International Edition 39, 4004 (2000).
43. K. D. Pavey; Quartz crystal analytical sensors: The future of labelfree, real-time diagnostics; Expert Review of Molecular Diagnostics 2, 173 (2002).
44. G. Sauerbrey; Quartz crystal microbalance theory and calibration; Zeitschrift für Physik 155, 206 (1959).
45. T. Omura and M. Okuhara; Frequency shifts of piezoelectric quartz crystals immersed in organic liquids; Anal. Chim. Acta 142, 281 (1982).
46. P. L. Konash and G. J. Bastiaans; Piezoelectric crystals as detectors in liquid chromatography; Anal. Chem. 52, 1929 (1980).
47. L. D. Landau and E. M. Lifshtz; Oscillation Motion in a Viscous Fluid in Fluid Mechanics; edited by L. D. Landau and E. M. Lifshtz; Pergamon Press, Oxford (1959), pp. 88-90.
48. K. K. Kanazawa and J. G. Gordon; The oscillation frequency of a quartz resonator in contact with a liquid; Anal. Chim. Acta 175, 99 (1985).
49. M. Rodahl, F. Höök, A. Krozer, B. Kasemo, and P. Breszinsky; A quartz crystal microbalance setup for frequency and Q-factor measurements in gaseous and liquid environments; Rev. Sci. Instrum. 66, 3924 (1995).
50. F. Höök, M. Rodahl, P. Brzezinski, and B. Kasemo; Measurements using the quartz crystal microbalance technique of ferritin monolayers on methyl-thiolated gold: Dependence of energy dissipation and saturation coverage on salt concentration; J. Colloid Interface Sci. 208, 63 (1998).
51. M. Rodahl and B. Kasemo; A simple setup to simultaneously measure the resonant frequency and the absolute dissipation factor of a quartz crystal microbalance; Rev. Sci. Instrum. 67, 3238 (1996).
52. H. Muramatsu, E. Tamiya, and I. Karube; Computation of equivalent circuit parameters of quartz crystals in contact with liquids and study of liquid properties; Anal. Chem. 60, 2142 (1988).
53. T. Ozeki, M. Morita, H. Yoshimine, H. Furusawa, and Y. Okahata; Hydration and energy dissipation measurements of biomolecules on a piezoelectric quartz oscillator by admittance analyses; Anal. Chem. 79, 79 (2007).
54. A. Tsumagari, A. Nakamura, K. Hashimoto, Y. Tada, and Y. Yamashita; Protein adsorption onto hydroxyapatite thin films with QCM measurements; Bioceramics 12, 361 (1999).
55. J. Langford, K. D. Pavey, C. J. Olliff, P. J. Cragg, G. W. Hanlon, F. Paul, and G. D. Rees; Real-time monitoring of stain formation and removal on calcium hydroxyapatite surfaces using quartz crystal sensor technology; Analyst. 127, 360 (2002).
56. L. Zhitomirsky and L. Galor; Electrophoretic deposition of hydroxyapatite; J. Mater. Sci.: Materials in Medicine 8, 213 (1997).
57. M. Wei, A. J. Ruys, B. K. Milthorpe, and C. C. Sorrell; Precipitation of hydroxyapatite nanoparticles: Effects of precipitation method on electrophoretic deposition; J. Mater. Sci.: Mater. Med. 16, 319 (2005).
58. L. Sun, C. C. Berndt, K. A. Gross, and A. Kucuk; Material fundamentals and clinical performance of plasma-sprayed hydroxyapatite coatings: A review; J. Biomed. Mater. Res. Part B: Appl. Biomater. 58, 570 (2001).
59. P. Cheang and K. A. Khor; Influence of powder characteristics on plasma sprayed hydroxyapatite coatings; J. Therm. Spray Technol. 5, 310 (1996).
60. C. Wang, Z. Chen, L. Guan, Z. Liu, P. Wang, S. Zheng, S. Zheng, and X. Liao; Structural characterization of ion beam sputter deposited calcium phosphate coatings; Surf. Coat. Technol. 130, 39 (2000).
61. L. Cleries, E. Martinez, J. M. Fernandez-Pradas, G. Sardin, J. Esteve, and J. L. Morenza; Mechanical properties of calcium phosphate coatings deposited by laser ablation; Biomaterials 21, 967 (2000).
62. A. Monkawa, T. Ikoma, S. Yunoki, T. Yoshioka, J. Tanaka, D. Chakarov, and B. Kasemo; Fabrication of hydroxyapatite ultrathin layer on gold surface and its application for quartz crystal microbalance technique; Biomaterials 27, 5748 (2006).
63. T. Ikoma, M. Tagaya, T. Tonegawa, T. Takemura, M. Okuda, N. Hanagata, J. Tanaka, D. Chakarov, and B. Kasemo; The surface property of hydroxyapatite: Sensing with quartz crystal microbalance; Key Eng. Mater. 396-398, 89 (2009).
64. M. Javidi, M. E. Bahrololoom, S. Javadpour, and J. Ma; Studying surface charge and suspension stability of hydroxyapatite powder in isopropyl alcohol to prepare stable suspension for electrophoretic deposition; Advances in Applied Ceramics 108, 241 (2009).
65. I. Zhitomirsky; Cathodic electrodeposition of ceramic and organoceramic materials. Fundamental aspects; Adv. Colloid Interface Sci. 97, 279 (2002).
66. X. F. Xiao and R. F. Liu; Effect of suspension stability on electrophoretic deposition of hydroxyapatite coatings; Mater. Lett. 60, 2627 (2006).
67. M. Tagaya, T. Ikoma, D. Chakarov, B. Kasemo, and J. Tanaka; Cleaning methods of proteins adsorbed on hydroxyapatite nanocrystal sensor; Science and Technology of Advanced Materials 11, 045002 (2010).
68. T. Yoshioka, T. lkoma, A. Monkawa, T. Tonegawa, D. Chakarov, B. Kasemo, N. Hanagata, and J. Tanaka; Proteins adsorption on hydroxyapatite nano-crystals with quartz crystal microbalance technique; Key Eng. Mater. 361, 1119 (2008).
69. T. Ikoma, M. Tagaya, N. Hanagata, T. Yoshioka, D. Chakarov, B. Kasemo, and J. Tanaka; Protein adsorption on hydroxyapatite nanosensors with different crystal sizes studied in situ by quartz crystal microbalance with dissipation method; J. Am. Ceram. Soc. 92, 1125 (2009).
70. T. Ikoma, A. Yamazaki, S. Nakamura, and M. Akao; Preparation and structure refinement of monoclinic hydroxylapatite; J. Solid State Chem. 44, 272 (1999).
71. M. Tagaya, T. Ikoma, T. Takemura, M. Okuda, N. Hanagat, T. Yoshioka, D. Chakarov, B. Kasemo, and J. Tanaka; Adsorption of proteins derived from fetal bovine serum onto hydroxyapatite nanocrystals with quartz crystal microbalance technique; Key Eng. Mater. 396-398, 47 (2009).
72. J. Redepenning, T. K. Schlesinger, E. J. Mechalke, D. A. Puleo, and R. Bizios; Osteoblast attachment monitored with a quartz crystal microbalance; Anal. Chem. 65, 3378 (1993).
73. A. Weerawardena, C. J. Drummond, F. Caruso, and M. McCormick; Real time monitoring of the detergency process by using a quartz crystal microbalance; Langmuir 14, 575 (1998).
74. V. Payet, S. Brunner, A. Galtayries, I. Frateur, and P. Marcus; Cleaning of albumin-contaminated Ti and Cr surfaces: An XPS and QCM study; Surf. Interface Anal. 40, 215 (2008).
75. J. Langford, K. D. Pavey, C. J. Olliff, P. J. Cragg, G. W. Hanlon, F. Paul, and G. D. Rees; Real-time monitoring of stain formation and removal on calcium hydroxyapatite surfaces using quartz crystal sensor technology; Analyst 127, 360 (2002).
76. S. Bose and S. K. Saha; Synthesis and characterization of hydroxyapatite nanopowders by emulsion technique; Chem. Mater. 15, 4464 (2003).
77. G. C. Koumoulidis, A. P. Katsoulidis, A. K. Ladavos, P. J. Pomonis, C. C. Trapalis, A. T. Sdoukos, and T. C. Vaimakis; Preparation of hydroxyapatite via microemulsion route; J. Colloid Interface Sci. 259, 254 (2003).
78. G. K. Lim, J. Wang, S. C. Ng, and L. M. Gan; Nanosized hydroxyapatite powders from microemulsions and emulsions stabilized by a biodegradable surfactant; J. Mater. Chem. 9, 1635 (1999).
79. S. Shimabayashi, H. Tanaka, and M. Nakagaki; Adsorption of dodecyl sulfate ion on hydroxyapatite and concurrent release of phosphate and calcium ions from the surface of hydroxyapatite; Chem. Pharm. Bull. 34, 4474 (1986).
80. W. Kern and D. A. Puotinen; Clean solutions based on. Hydrogen peroxide for use in silicon semiconductor technology; RCA review 31, 187 (1970).
81. 2 cleaning solutions; J. Electrochem. Soc. 137, 1239 (1990).
82. K. Yamamoto, A. Nakamura, and U. Hase; Control of cleaning performance of an ammonia and hydrogen peroxide mixture (APM) on the basis of a kinetic reaction model; IEEE Transactions on Semiconductor Manufacturing 12, 288 (1999).
83. A. Hiroki and J. A. LaVerne; Decomposition of hydrogen peroxide at water-ceramic oxide interfaces; J. Phys. Chem. B 109, 3364 (2005).
84. R. Stadtman and R. L. Levine; Free radical-mediated oxidation of free amino acids and amino acid residues in proteins; Amino Acids 25, 207 (2003).
85. D. A. Bolon and C. O. Kunz; Free radical-mediated oxidation of free amino acids and amino acid residues in proteins; Polym. Eng. Sci. 12, 109 (1972).
86. R. R. Sowell, R. E. Cuthrell, D. M. Mattox, and R. D. Bland; Surface cleaning by ultraviolet radiation;J. Vac. Sci. Technol. 11, 474 (1974).
87. J. R. Vig; UV ozone cleaning of surfaces; J. Vac. Sci. Technol. A3, 1027 (1985).
88. T. Ye, E. A. McArthur, and E. Borguet; Mechanism of UV photoreactivity of alkylsiloxane self-assembled monolayers; J. Phys. Chem. B 109, 9927 (2005).
89. 1D) with saturated hydrocarbon; J. Phys. Chem. 72, 1143 (1980).
90. W. Norde; Adsorption of proteins from solution at the solid-liquid interface; Adv. Colloid Interface Sci. 25, 267 (1986).
91. J. L. Brash and T. A. Horbett; Proteins at Interfaces II: Fundamentals and Applications; edited by T. A. Horbett and J. L. Brash, ACS Symposium Series 602, American Chemical Society, Washington DC (1995), pp. 1-23.
92. G. Yin, Z. Liu, J. Zhan, F. Ding, and N. Yuan; Impacts of the surface charge property on protein adsorption on hydroxyapatite; Chemical Engineering Journal 87, 181 (2002).
93. R. Kurrat, J. E. Prenosil, and J. J. Ramsden; Kinetics of human and bovine serum albumin adsorption at silica-titania surfaces; J. Colloid Interface Sci. 185, 1 (1997).
94. T. Wei, S. Kaewtathip, and K. Shing; Buffer effect on protein adsorption at liquid/solid interface; J. Phys. Chem. C 113, 2053 (2009).
95. G. V. Lubarsky, M. R. Davidson, and R. H. Bradley; Hydration-dehydration of adsorbed protein films studied by AFM and QCM-D; Biosens. Bioelectron. 22, 1275 (2007).
96. A. G. Hemmersama, K. Rechendorffa, M. Foss, D. S. Sutherlanda, and F. Besenbachera; Fibronectin adsorption on gold, Ti-, and Ta-oxide investigated by QCM-D and RSA modeling; J. Colloid Interface Sci. 320, 110 (2008).
97. F. Höök, M. Rodahl, P. Brzezinski, and B. Kasemo; Energy dissipation kinetics for protein and antibody-antigen adsorption under shear oscillation on a quartz crystal microbalance; Langmuir 14, 729 (1998).
98. A. Dolatshahi-Pirouz, T. Jensen, M. Foss, J. Chevallier, and F. Besenbacher; Enhanced surface activation of fibronectin upon adsorption on hydroxyapatite; Langmuir 25, 2971 (2009).
99. M. Rodahl and B. Kasemo; On the measurement of thin liquid overlayers with the quartz-crystal microbalance; Sens. Actuators, A 54, 448 (1996).
100. H. Bannasch, M. Fohn, T. Unterberg, A. D. Bach, B. Weyand, and G. B. Stark; Skin tissue engineering; Clinics in plastic surgery 30, 573 (2003).
101. N. J. Cho, K. K. Kanazawa, J. S. Glenn, and C. W. Frank; Employing two different quartz crystal microbalance models to study changes in viscoelastic behavior upon transformation of lipid vesicles to a bilayer on a gold surface; Anal. Chem. 79, 7027 (2007).
102. A. G. Hemmersam, F. Foss, J. Chevallier, and F. Besenbacher; Adsorption of fibrinogen on tantalum oxide, titanium oxide and gold studied by the QCM-D technique; Colloids Surf., B 43, 208 (2005).
103. P. Roach, D. Farrar, and C. C. Perry; Interpretation of protein adsorption: Surface-induced conformational changes; J. Am. Chem. Soc. 127, 8168 (2005).
104. K. H. Choi, J. M. Friedt, F. Frederix, A. Campitelli, and G. Borghs; Simultaneous atomic force microscope and quartz crystal microbalance measurements: Investigation of human plasma fibrinogen adsorption; Appl. Phys. Lett. 81, 1335 (2002).
105. C. E. Hall and H. S. Slayter; The fibrinogen molecule: Its size, shape, and mode of polymerization; Journal of Biophysical and Biochemical Cytology 5, 11 (1959).
106. A. P. Serro, M. Bastos, J. C. Pessoa, and B. Saramago; Bovine serum albumin conformational changes upon adsorption on titania and on hydroxyapatite and their relation with biomineralization; J. Biomed. Mater. Res. 70A, 420 (2004).
107. R. L. Beissinger and E. F. Leonard; Plasma protein adsorption and desorption rates on quartz: Approach to multi-component systems; Transactions-American Society for Artificial Internal Organs 27, 225 (1981).
108. I. Lundstrom and H. Elwing; Simple kinetic models for protein exchange reactions on solid surfaces; J. Colloid Interface Sci. 136, 68 (1990).
109. L. Vroman and A. L. Adams; Findings with the recording ellipsometer suggesting rapid exchange of specific plasma proteins at liquid/solid interfaces; Surface Science 16, 438 (1969).
110. M. E. Soderquist and A. G. Walton; Structural changes in proteins adsorbed on polymer surfaces; J. Colloid Interface Sci. 75, 386 (1980).
111. F. Höök, B. Kasemo, T. Nylander, C. Fant, K. Sott, and H. Elwing; Variations in coupled water, viscoelastic properties, and film thickness of a Mefp-1 protein film during adsorption and cross-Linking: A monitoring, ellipsometry, and surface plasmon resonance study; Anal. Chem. 73, 5796 (2001).
112. T. A. Horbett; Mass action effects on the adsorption of fibrinogen from hemoglobin solutions and from plasma; Thrombosis and Haemostasis 51, 174 (1984).
113. E. Lutanie, J. C. Voegel, P. Schaaf, M. Freund, J. P. Cazenave, and A. Schmitt; Competitive adsorption of human immunoglobulin G and albumin: Consequences for structure and reactivity of the adsorbed layer; Proceedings of the National Academy of Sciences of USA 89, 9890 (1992).
114. C. A. Haynes and W. Norde; Structures and stabilities of adsorbed proteins; J. Colloid Interface Sci. 169, 313 (1995).
115. P. Déjardin, P. Ten, X. Hove, J. Yu, and J. L. Brash; Competitive adsorption of high molecular weight kininogen and fibrinogen from binary mixtures to glass surface; Langmuir 11, 4001 (1995).
116. M. Holmberg, K. B. Stibius, N. B. Larsen, and X. Hou; Competitive protein adsorption to polymer surfaces from human serum; J. Mater. Sci. 19, 2179 (2008).
117. M. Holmberg and X. Hou; Competitive protein adsorption: Multilayer adsorption and surface induced protein aggregation; Langmuir 25, 2081 (2009).
118. R. J. Green, M. C. Davies, C. J. Roberts, and S. J. B. Tendler; Competitive adsorption as observed by surface plasmon resonance; Biomaterials 20, 385 (1999).
119. K. McClary, T. P. Ugarova, and D. W. Grainger; Modulating fibroblast adhesion, spreading, and proliferation using self-assembled monolayer films of alkylthiolates on gold; J. Biomed. Mater. Res. 50, 428 (2000).
120. A. L. Koenig, V. Gambillara, and D. W. Grainger; Correlating fibronectin adsorption with endothelial cell adhesion and signaling on polymer substrates; J. Biomed. Mater. Res. 64A, 20 (2003).
121. M. Tagaya, T. Ikoma, S. Migita, M. Okuda, T. Takemura, N. Hanagata, T. Yoshioka, and J. Tanaka; Fetal bovine serum adsorption onto hydroxyapatite sensor monitoring by quartz crystal microbalance with dissipation technique; Mater. Sci. Eng. B 173, 176 (2010).
122. M. V. Voinova, M. Rodahl, M. Jonson, and B. Kasemo; Viscoelastic acoustic response of layered polymer films at fluid-solid interfaces: Continuum mechanics approach; Phys. Scr. 59, 391 (1999).
123. M. Rodahl, F. Höök, C. Fredriksson, C. A. Keller, A. Krozer, P. Brzezinski, M. Voinova, and B. Kasemo; Simultaneous frequency and dissipation factor QCM measurements of biomolecular adsorption and cell adhesion; Faraday Discuss. 107, 229 (1997).
124. M. Jenny, A. Hossein, K. Peter, and S. S. Duncan; Viscoelastic modeling of highly hydrated laminin layers at homogeneous and nanostructured surfaces: Quantification of protein layer properties using QCM-D and SPR; Langmuir 23, 9760 (2007).
125. E. Gurak, C. C. Dupont-Gillain, J. Booth, C. J. Roberts, and P. G. Rouxhet; Resolution of the vertical and horizontal heterogeneity of adsorbed collagen layers by combination of QCM-D and AFM; Langmuir 212, 10684 (2005).
126. T. J. Webster, R. W. Siegel, and R. Bizios; Osteoblast adhesion on nanophase ceramics; Biomaterials 20, 1221 (1999).
127. T. Zhou, K. A. Marx, M. Warren, H. Schulze, and S. J. Braunhut; Osteoblast adhesion on nanophase ceramics; Biotechnology Program 16, 268 (2000).
128. K. A. Marx, T. Zhou, A. Montrone, H. Schulze, and S. J. Braunhut; A quartz crystal microbalance cell biosensor: Detection of microtubule alterations in living cells at nM nocodazole concentrations; Biosens. Bioelectron. 16, 773 (2001).
129. K. A. Marx, T. Zhou, M. Warren, and S. J. Braunhut; Quartz crystal microlbalance study of endothelial cell number dependent differences in initial adhesion and steady-state behavior: Evidence for cell-cell cooperativity in initial adhesion and spreading; Biotechnol. Progr. 19, 987 (2003).
130. K. A. Marx, T. Zhou, A. Montrone, D. McIntosh, and S. J. Braunhut; 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, 23 (2005).
131. D. Le Guillou-Buffello, R. Bareille, M. Gindre, A. Sewing, P. Laugier, and J. Amedee; Additive effect of RGD coating to functionalized titanium surfaces on human oseoprogenitor cell adhesion and spreading; Tissue Eng. A 14, 1445 (2008).
132. Z. Fohlerová, P. Skládal, and J. Turánek; Adhesion of eukaryotic cell lines on the gold surface modified with extracellular matrix proteins monitored by the piezoelectric sensor; Biosens. Bioelectron. 22, 1896 (2007).
133. J. Wegener, J. Seebach, A. Janshoff, and H. J. Galla; Analysis of the composite response of shear wave resonators to the attachment of mammalian cells; European Biophysics Journal 78, 2821 (2000).
134. A. Janshoff, J. Wegener, M. Sieber, and H. J. Galla; Double-mode impedance analysis of epithelial cell monolayers cultured on shear wave resonators; European Biophysics Journal 25, 93 (1996).
135. C. M. Marxer, M. C. Coen, T. Greber, U. F. Greber, and L. Schlapbach; Cell spreading on quartz crystal microbalance elicits positive frequency shifts indicative of viscosity changes; Analytical and Bioanalytical Chemistry 377, 578 (2003).
136. M. Rodahl, F. Höök, and B. Kasemo; QCM operation in liquids: Explanation of measured variations in frequency and Q factor with liquid conductivity; Anal. Chem. 68, 2219 (1996).
137. C. Fredriksson, S. Khilman, B. Kasemo, and D. M. Steel; In vitro real-time characterization of cell attachment and spreading; J. Mater. Sci.: Mater. Med. 9, 785 (1998).
138. C. Fredriksson, S. Khilman, M. Rodahl, and B. Kasemo; The piezoelectric quartz crystal mass and dissipation sensor: A means of studying cell adhesion; Langmuir 14, 248 (1998).
139. A. S. Cans, F. Höök, O. Shupliakov, A. G. Ewing, P. S. Eriksson, L. Brodin, and O. Orwar; Measurement of the dynamics of exocytosis and vesicle retrieval at cell populations using a quartz crystal microbalance; Anal. Chem. 73, 5805 (2001).
140. C. Modin, A. L. Stranne, M. Foss, M. Duch, J. Justesen, J. Chevallier, L. K. Andersen, A. G. Hemmersam, F. S. Pedersen, and F. Besenbacher; QCM-D studies of attachment and differential spreading of pre-osteoblastic cells on Ta and Cr surfaces; Biomaterials 27, 1346 (2006).
141. M. S. Lord, C. Modin, M. Foss, M. Duch, A. Simmons, F. S. Pedersen, B. K. Milthorpea, and F. Besenbacher; Monitoring cell adhesion on tantalum and oxidized polystyrene using a quartz crystal microbalance with dissipation; Biomaterials 27, 4529 (2006).
142. M. S. Lord, C. Modin, M. Foss, M. Duch, A. Simmons, F. S. Pedersen, F. Besenbacher, and B. K. Milthorpe; Extracellular matrix remodelling during cell adhesion monitored by the quartz crystal microbalance; Biomaterials 29, 2581 (2008).
143. C. Moseke and A. Ewald; Cell and protein adsorption studies using quartz microgravimetry with dissipation monitoring; Materialwiss. Werkstofftech. 40, 36 (2009).
144. M. Tagaya, T. Ikoma, T. Takemura, S. Migita, M. Okuda, T. Yoshioka, N. Hanagata, and J. Tanaka; Initial adhesion behavior of fibroblasts onto hydroxyapatite nano-crystals; Bioceramics Development and Applications 1, D110165 (2011).
145. M. Tagaya, T. Yamazaki, S. Migita, N. Hanagata, and T. Ikoma; Hepatocyte adhesion behavior on modified hydroxyapatite nanocrystals with quartz crystal microbalance; Bioceramics Development and Applications 1, D110157 (2011).
146. M. Tagaya, T. Ikoma, T. Takemura, N. Hanagata, T. Yoshioka, and J. Tanaka; Protein adsorption and subsequent fibroblasts adhesion on hydroxyapatite nanocrystals; IOP Conference Series: Mater. Sci. Eng. 18, 192009 (2011).
147. F. Li, H. C. Wang, and Q. M. Wang; Thickness shear mode acoustic wave sensors for characterizing the viscoelastic properties of cell monolayer; Sens. Actuators, B 128, 399 (2008).
148. P. Fernández, L. Heymann, A. Ott, N. Aksel, and P. A. Pullarkat; Shear rheology of a cell monolayer; New Journal of Physics 9, 419 (2007).
149. A. Palmer, T. G. Mason, J. Xu, S. C. Kuo, and D. Wirtz; Diffusing wave spectroscopy microrheology of actin filament networks; Biophys. J. 76, 1063 (1999).
150. H. Aoki, M. Akao, Y. Shin, T. Tsuzi, and T. Togawa; Sintered hydroxyapatite for a percutaneous device and its clinical application; Medical Progress Through Technology 12, 213 (1987).
151. F. Furuzono, M. Ueki, H. Kitamura, K. Oka, and E. Imai; Histological reaction of sintered nano-hydroxyapatite-coated cuff and its fibroblast-like cell hybrid for an indwelling catheter; J. Biomed. Mater. Res. Part B Appl. Biomater. 89B, 77 (2009).
152. M. Tagaya, C. J. Scott, T. Ikoma, and J. Tanaka; Application of a quartz crystal microbalance with dissipation for in situ monitoring of interfacial phenomena between bioceramics and cells in Handbook of Advanced Ceramics: Materials, Applications, Processing and Properties; edited by S. Somiya, F. Aldinger, R. M. Spriggs, K. Uchino, K. Koumoto, and M. Kaneno; 2nd edn., Academic Press Inc., London, UK (2012).
153. M. Tagaya, T. Ikoma, N. Hanagata, and J. Tanaka; Competitive adsorption of fibronectin and lbumin on hydroxyapatite nanocrystals; Science and Technology of Advanced Materials 12, 034411 (2011).
154. L. L. Hench and J. Wilson; Surface active biomaterials; Science 226, 630 (1984).
155. K. Kokubo; Surface chemistry of bioactive glassceramics; J. Non-Cryst. Solids 120, 138 (1990).
156. W. Cao and L. L. Hench; Bioactive materials; Ceram. Int. 22, 493 (1996).
157. 3; J. Biomed. Mater. Res. 24, 721 (1990).
158. T. Kokubo and H. Takadama; How useful is SBF in predicting in vivo bone bioactivity; Biomaterials 27, 2907 (2006).
159. 5 glasses in a simulated body fluid; J. Non-Cryst. Solids 143, 84 (1992).
160. M. Tanahashi, T. Kokubo, and T. Matsuda; Quantitative assessment of apatite formation via a biomimetic method using quartz crystal microbalance; J. Biomed. Mater. Res. 31, 243 (1996).
161. M. Tanahashi and T. Matsuda; Surface functional group dependence on apatite formation on self-assembled monolayers in a simulated body fluid; J. Biomed. Mater. Res. 34, 305 (1997).
162. T. Miyazaki, C. Ohtsuki, Y. Akioka, M. Tanihara, J. Nakao, Y. Sakaguchi, and S. Konagaya; Apatite deposition on polyamide films containing carboxyl group in a biomimetic solution; J. Mater. Sci.: Mater. Med. 14, 569 (2003).
163. G. Daculsi, P. Pilet, M. Cottrel, and G. Guicheux: Role of fibronectin during biological apatite crystal nucleation: Ultrastructural characterization; J. Biomed. Mater. Res. 47, 228 (1999).
164. A. P. do Serro, A. C. Fernandes, B. Saramago, J. Lima, and M. A. Barbpsa; Apatite deposition on titanium surfaces-the role of albumin adsorption; Biomaterials 18, 963 (1997).
165. A. P. do Serro, A. C. Fernandes, and B. de Jesus Vieira Saramago; Calcium phosphate deposition on titanium surfaces in the presence of fibronectin; J. Biomed. Mater. Res. 49, 345 (2000).
166. S. Areva, T. Peltola, E. Sailynoja, K. Laajalehto, M. Linden, and J. B. Rosenholm, Effect of albumin and fibrinogen on calcium phosphate formation on sol-gel-derived titania coatings in vitro; Chemisry of Materials 14, 1614 (2000).
167. P. Liu, J. H. Tao, Y. R. Cai, H. H. Pan, X. R. Xu, and R. K. Tang; Role of fetal bovine serum in the prevention of calcification in biological fluids; Journal of Crystal Growth 310, 4672 (2008).
168. J. Lima, S. R. Sousa, A. Ferreira, and M. A. Barbosa; Interactions between calcium, phosphate and albumin on the surface of Titanium; J. Biomed. Mater. Res. Part A 55, 45 (2001).
169. A. P. do Serro, M. Bastos, J. C. Pessoa, and B. J. Saramago; Bovine serum albumin conformational changes upon adsorption on titania and on hydroxyapatite and their relation with biomineralization; J. Biomed. Mater. Res. Part A 70A, 420 (2004).
170. A. P. Marques, A. P. Serro, B. J. Saramago, A. C. Fernandes, M. C. F. Magalhaes, and R. N. Correia; Mineralisation of two phosphate ceramics in HBSS: role of albumin; Biomaterials 24, 451 (2003).
171. C. Prin, M. C. Bene, B. Gobert, P. Montagne, and G. C. Faure; Isoelectric restriction of human immunoglobulin isotypes; Biochim. Biophys. Acta 1243, 287 (1995).
172. G. K. Toworfe, R. J. Composto, I. M. Shapiro, and P. Ducheyne; Nucleation and growth of calcium phosphate on amine-, carboxyland hydroxyl-silane self assembled monolayers; Biomaterials 27, 631 (2006).
173. P. Zhu, Y. Masuda, and K. Koumoto; Site-selective adhesion of hydroxyapatite microparticles on charged surfaces in a supersaturated solution; J. Colloid Interface Sci. 243, 31 (2001).
174. M. Hashizume, A. Sakai, Y. Sakamoto, H. Matsuno, and T. Serizawa; Facile Surface functionalization of polystyrene substrates with biomimetic apatite by utilizing serum proteins; Chem. Lett. 39, 220 (2010).
175. F. G. Giancotti and R. E. uoslahti; Integrin signaling; Science 285, 1028 (1999).
176. M. Tagaya, T. Ikoma, M. Takeguchi, N. Hanagata, and J. Tanaka; Interfacial serum protein effect on biological apatite growth; J. Phys. Chem. C 115, 22523 (2011).
177. M. Okuda, N. Ogawa, M. Takeguchi, A. Hashimoto, M. Tagaya, S. Chen, N. Hanagata, and T. Ikoma; Minerals and aligned collagen fibrils in tilapia fish scales: Structural analysis using dark-field and energy-filtered transmission electron microscopy and electron tomography; Microsc. Microanal. 17, 788 (2011).
178. M. Okuda, M. Takeguchi, M. Tagaya, T. Tonegawa, A. Hashimoto, N. Hanagata, and T. Ikoma; Elemental distribution analysis of Type I collagen fibrils in tilapia fish scale with energy-filtered transmission electron microscope; Micron 40, 665 (2009).
179. F. Nudelman, K. Pieterse, A. George, P. H. H. Bomans, H. Friedrich1, L. J. Brylka1, P. A. J. Hilbers, G. de With, and N. A. J. M. Sommerdijk; The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors; Nat. Mater. 9, 1004 (2010).
180. M. J. Glimcher and H. Muir; Recent studies of the mineral phase in bone and its possible linkage to the organic matrix by proteinbound phosphate bonds; Philos. Trans. R. Soc. B 304, 479 (1994).
181. W. J. Landis, M. J. Song, A. Leith, L. McEwen, and B. F. McEwen; Mineral and organic matrix interaction in normally calcifying tendon visualized in three dimensions by high-voltage electron microscopic tomography and graphic image reconstruction; Journal of Structural Biology 110, 39 (1993).
182. C. Berthet-Colominas, A. Miller, and S. W. White; Structural study of the calcifying collagen in turkey leg tendons; J. Mol. Biol. 134, 431 (1994).
183. E. P. Katz and S.-T. Li; Structure and function of bone collagen fibrils; J. Mol. Biol. 80, 1 (1993).
184. M. Tagaya, T. Ikoma, T. Takemura, N. Hanagata, M. Okuda, T. Yoshioka, and J. Tanaka; Detection of interfacial phenomena with osteoblast-like cell adhesion on hydroxyapatite and oxidized polystyrene by the quartz crystal microbalance with dissipation; Langmuir 27, 7635 (2011).
185. M. Tagaya, T. Ikoma, T. Takemura, N. Hanagata, and J. Tanaka; Effect of Interfacial proteins on osteoblast-like cell adhesion to hydroxyapatite nanocrystals; Langmuir 27, 7645 (2011).
186. A. Abbott; Cell culture: Biology's new dimension; Nature 424, 870 (2003).
187. R. Langer and J. P. Vacanti; Tissue engineering; Science 260, 920 (1993).
188. S. Levenberg and R. Langer; Advances in tissue engineering; Current Topics in Developmental Biology 61, 113 (2004).
189. A. Khademhosseini, R. Langer, J. Borenstein, and J. P. Vacanti; Microscale technologies for tissue engineering and biology; Proceedings of the National Academy of Sciences of the United States of America 103, 2480 (2006).
190. A. Khademhosseini, J. Yeh, S. Jon, G. Eng, K. Y. Suh, J. A. Burdick, and R. Langer; Molded poly(ethylene glycol) microstructures for docking and shear protecting cells within microfluidic channels; Lab on a chip 4, 425 (2004).
191. J. Fukuda, Y. Sakai, and K. Nakazawa; Novel hepatocyte culture system developed using microfabrication and collagen/PEG microcantact printing; Biomaterials 27, 1061 (2006).
192. J. Fukuda and K. Nakazawa; Orderly arrangement of hepatocyte spheroids on a microfabricated chip; Tissue Eng. 11, 1254 (2005).
193. J. Fukuda, A. Khademhosseini, Y. Yeo, X. Yang, J. Yeh, G. Eng, J. Blumling, C.-F. Wang, D. S. ohane, and R. Langer; Micromolding of photocrosslinkable chitosan hydrogel for spheroid microarray and co-cultures; Biomaterials 27, 5259 (2006).
194. M. Tagaya, T. Yamazaki, D. Tsuya, Y. Sugimoto, N. Hanagata, and T. Ikoma; Nano/microstructural effect of hydroxyapatite nanocrystals on hepatocyte cell aggregation and adhesion; Macromolecular Bioscience 11, 1586 (2011).
195. M. I. Kay, R. A. Young, and A. S. Posner; Crystal structure of hydroxyapatite; Nature 204, 1050 (1964).
196. W. Suchanek and M. Yoshimura; Processing and properties of hydroxyapatite-based biomaterials for use as hard tissue replacement implants; J. Mater. Res. 13, 94 (1998).
197. C. Yongli, Z. Xiufang, G. Yandao, Z. Nanming, Z. Tingying, and S. Xinqi; Conformational changes of fibrinogen adsorption onto hydroxyapatite and titanium oxide nanoparticles; J. Colloid Interface Sci. 214, 38 (1999).
198. K. Kandori, K. Miyagawa, and T. Ishikawa; Adsorption of immunogamma globulin onto various synthetic calcium hydroxyapatite particles; J. Colloid Interface Sci. 273, 406 (2004).
199. M. Kikuchi, S. Itoh, S. Ichinose, K. Shinomiya, and J. Tanaka; Selforganization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vivo and its biological reaction in vivo; Biomaterials 22, 1705 (2001).
200. L. Letic-Gavrilovic, A. Piattelli, and K. Abe; Nerve growth factor beta (NGF beta) delivery via a collagen/hydroxyapatite (Col/HAp) composite and its effects on new bone in growth; J. Mater. Sci.: Mater. Med. 14, 95 (2003).
201. S. S. Liao and F. Z. Cui; In vitro and in vivo degradation of mineralized collagen-based composite scaffold: nanohydroxyapatite/ collagen/poly(L-lactide); Tissue Eng. 10, 73 (2004).
202. S. Yunoki, T. Ikoma, A. Monkawa, K. Ohta, M. Kikuchi, S. Sotome, K. Shinomiya, and J. Tanaka; Control of pore structure and mechanical property in hydroxyapatite/collagen composite using unidirectional ice growth; Mater. Lett. 60, 999 (2006).
203. T. Kadoya, T. Ogawa, H. Kuwahara, and T. Okuyama; High performance liquid chromatography of proteins on a hydroxyapatite column; J. Liq. Chromatogr. 11, 2951 (1988).
204. T. Kadoya; High-performance liquid chromatography of proteins on a ceramic hydroxyapatite with volatile buffers; J. Chromatogr. 515, 521 (1990).
205. M. Itokazu, T. Sugiyama, T. Ohno, E. Wada, and Y. Katagiri; Development of porous apatite ceramic for local delivery of chemotherapeutic agents; J. Biomed. Mater. Res. 39, 536 (1998).
206. W. Paul and C. P. Sharma; Ceramic drug delivery: A perspective; J. Biomater. Appl. 17, 253 (2003).
207. H. W. Kim, J. C. Knowles, and H. E. Kim; Porous scaffolds of gelatin-hydroxyapatite nanocomposites obtained by biomimetic approach: Characterization and antibiotic drug release; J. Biomed. Mater. Res. B 74B, 686 (2005).
208. Y. Mizushima, T. Ikoma, J. Tanaka, K. Hoshi, T. Ishihara, Y. Ogawa, and A. Ueno; Porous scaffolds of gelatin-hydroxyapatite nanocomposites obtained by biomimetic approach: Characterization and antibiotic drug release; J. Controlled Release 110, 260 (2006).
209. T. Ikoma, T. Tonegawa, H. Watanabe, G. P. Chen, J. Tanaka, and Y. Mizushima; Drug-supported microparticle of calcium carbonate nanocrystals and its covering with hydroxyapatite; J. Nanosci. Nanotechnol. 7, 822 (2007).
210. R. Nemoto, L. Wang, T. Ikoma, J. Tanaka, and M. Senna; Preferential alignment of hydroxyapatite crystallites in nanocomposites with chemically disintegrated silk fibroin; J. Nanopart. Res. 6, 259 (2004).
211. A. Matsuda, T. Ikoma, H. Kobayashi, and J. Tanaka; Preparation and mechanical property of core-shell type chitosan/calcium phosphate composite fiber; Mater. Sci. Eng. C 24, 723 (2004).
212. C. Fredriksson, S. Khilman, B. Kasemo, and D. M. Steel; In vitro real-time characterization of cell attachment and spreading; J. Mater. Sci.: Mater. Med. 9, 785 (1998).
213. A central hydrophobic E domain is connected to two hydrophobic D domains by a coiled-coil chain. These hydrophobic domains are charged negative under a neutral pH condition. The °C domains, with Arg and Lys residues, are charged positive and are substantially more hydrophilic than the E and D domains.
214. The protein surface has many carboxyl groups and 19 imidazole groups. These groups affect the effective binding to calcium ions, and represent a negatively charged surface due to dissociation of the side chains of acidic amino acids, such as glutamic acid, under the experimental pH conditions.