Role of integrin subunits in mesenchymal stem cell differentiation and osteoblast maturation on graphitic carbon-coated microstructured surfaces

Biomaterials

Volumn 51, Issue , 2015, Pages 69-79

  Olivares Navarrete, Rene ^a   Rodil, Sandra E ^b   Hyzy, Sharon L ^a   Dunn, Ginger R ^c   Almaguer Flores, Argelia ^b   Schwartz, Zvi ^a   Boyan, Barbara D ^a,c  

^a Virginia Commonwealth University   (United States)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Graphitic carbon coating; Growth factors; Mesenchymal stem cells; Osteoblast differentiation; Titanium

Indexed keywords

BONE; CARBON; CELL CULTURE; COATINGS; STEM CELLS; SURFACE CHEMISTRY; SURFACE MEASUREMENT; SURFACE MORPHOLOGY; TITANIUM; TOPOGRAPHY;

GRAPHITIC CARBONS; GROWTH FACTOR; HUMAN MESENCHYMAL STEM CELLS; MAGNETRON SPUTTERING SYSTEMS; MESENCHYMAL STEM CELL; MICRO-STRUCTURED SURFACES; OSTEOBLAST DIFFERENTIATION; OSTEOGENIC DIFFERENTIATION;

SURFACE ROUGHNESS;

ALPHA1 INTEGRIN; ALPHA2 INTEGRIN; ALPHA5 INTEGRIN; CARBON; GRAPHITE; INTEGRIN; MESSENGER RNA; TITANIUM; VERY LATE ACTIVATION ANTIGEN 3; BIOMATERIAL; PROTEIN SUBUNIT;

ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL MATURATION; CHEMICAL MODIFICATION; COMPARATIVE STUDY; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MICROWAVE OVEN; MORPHOLOGY; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURFACE PROPERTY; CELL ADHESION; CELL LINE; CYTOLOGY; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM; PROTEIN SUBUNIT;

CELL ADHESION; CELL DIFFERENTIATION; CELL LINE; COATED MATERIALS, BIOCOMPATIBLE; GENE SILENCING; GRAPHITE; HUMANS; INTEGRINS; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS; PROTEIN SUBUNITS; SURFACE PROPERTIES; TITANIUM;

EID: 84924870879     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.01.035     Document Type: Article

References (69)

1. Wilson C.J., Clegg R.E., Leavesley D.I., Pearcy M.J. Mediation of biomaterial-cell interactions by adsorbed proteins: a review. Tissue Eng 2005, 11:1-18.
2. Garcia A.J. Get a grip: integrins in cell-biomaterial interactions. Biomaterials 2005, 26:7525-7529.
3. Campbell I.D., Humphries M.J. Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol 2011, 3. 10.1101/cshperspect.a004994.
4. Lennon F.E., Hermann C.D., Olivares-Navarrete R., Rhee W.J., Schwartz Z., Bao G., et al. Use of molecular beacons to image effects of titanium surface microstructure on beta1 integrin expression in live osteoblast-like cells. Biomaterials 2010, 31:7640-7647.
5. Keselowsky B.G., Collard D.M., Garcia A.J. Surface chemistry modulates focal adhesion composition and signaling through changes in integrin binding. Biomaterials 2004, 25:5947-5954.
6. Boyan B.D., Schwartz Z. Response of musculoskeletal cells to biomaterials. JAm Acad Orthop Surg 2006, 14:S157-S162.
7. Olivares-Navarrete R., Raz P., Zhao G., Chen J., Wieland M., Cochran D.L., et al. Integrin alpha2beta1 plays a critical role in osteoblast response to micron-scale surface structure and surface energy of titanium substrates. Proc Natl Acad Sci U S A 2008, 105:15767-15772.
8. Wang L., Zhao G., Olivares-Navarrete R., Bell B.F., Wieland M., Cochran D.L., et al. Integrin beta1 silencing in osteoblasts alters substrate-dependent responses to 1,25-dihydroxy vitamin D3. Biomaterials 2006, 27:3716-3725.
9. Olivares-Navarrete R., Hyzy S.L., Gittens R.A., Schneider J.M., Haithcock D.A., Ullrich P.F., et al. Rough titanium alloys regulate osteoblast production of angiogenic factors. Spine J 2013, 13:1563-1570.
10. Park J.H., Wasilewski C.E., Almodovar N., Olivares-Navarrete R., Boyan B.D., Tannenbaum R., et al. The responses to surface wettability gradients induced by chitosan nanofilms on microtextured titanium mediated by specific integrin receptors. Biomaterials 2012, 33:7386-7393.
11. Park J.H., Schwartz Z., Olivares-Navarrete R., Boyan B.D., Tannenbaum R. Enhancement of surface wettability via the modification of microtextured titanium implant surfaces with polyelectrolytes. Langmuir 2011, 27:5976-5985.
12. Ratner B.D. Plasma deposition for biomedical applications: a brief review. JBiomater Sci Polym Ed 1992, 4:3-11.
13. Park J.H., Olivares-Navarrete R., Wasilewski C.E., Boyan B.D., Tannenbaum R., Schwartz Z. Use of polyelectrolyte thin films to modulate osteoblast response to microstructured titanium surfaces. Biomaterials 2012, 33:5267-5277.
14. Sukenik C.N., Balachander N., Culp L.A., Lewandowska K., Merritt K. Modulation of cell adhesion by modification of titanium surfaces with covalently attached self-assembled monolayers. JBiomed Mater Res 1990, 24:1307-1323.
15. Song Y.F., McMillan N., Long D.L., Kane S., Malm J., Riehle M.O., et al. Micropatterned surfaces with covalently grafted unsymmetrical polyoxometalate-hybrid clusters lead to selective cell adhesion. JAm Chem Soc 2009, 131:1340-1341.
16. Prime K.L., Whitesides G.M. Self-assembled organic monolayers: model systems for studying adsorption of proteins at surfaces. Science 1991, 252:1164-1167.
17. Bell B.F., Schuler M., Tosatti S., Textor M., Schwartz Z., Boyan B.D. Osteoblast response to titanium surfaces functionalized with extracellular matrix peptide biomimetics. Clin Oral Implants Res 2011, 22:865-872.
18. Reyes C.D., Petrie T.A., Burns K.L., Schwartz Z., Garcia A.J. Biomolecular surface coating to enhance orthopaedic tissue healing and integration. Biomaterials 2007, 28:3228-3235.
19. Reyes C.D., Garcia A.J. Alpha2beta1 integrin-specific collagen-mimetic surfaces supporting osteoblastic differentiation. JBiomed Mater Res A 2004, 69:591-600.
20. Tosatti S., Schwartz Z., Campbell C., Cochran D.L., VandeVondele S., Hubbell J.A., et al. RGD-containing peptide GCRGYGRGDSPG reduces enhancement of osteoblast differentiation by poly(L-lysine)-graft-poly(ethylene glycol)-coated titanium surfaces. JBiomed Mater Res A 2004, 68:458-472.
21. Zhao G., Schwartz Z., Wieland M., Rupp F., Geis-Gerstorfer J., Cochran D.L., et al. High surface energy enhances cell response to titanium substrate microstructure. JBiomed Mater Res A 2005, 74:49-58.
22. Bretaudiere J.P., Spillman T. Alkaline phosphatases. Methods of enzymatic analysis 1984, 75-92. Verlag Chemie, Weinheim, Germany. B. Hu (Ed.).
23. Rodil S.E., Olivares R., Arzate H., Muhl S. Biocompatibility, cytotoxicity and bioactivity of amorphous carbon films. Carbon Future Mat Adv Technol Appl 2006, 100:55-75.
24. Olivares-Navarrete R., Hyzy S., Wieland M., Boyan B.D., Schwartz Z. The roles of Wnt signaling modulators Dickkopf-1 (Dkk1) and Dickkopf-2 (Dkk2) and cell maturation state in osteogenesis on microstructured titanium surfaces. Biomaterials 2010, 31:2015-2024.
25. Olivares-Navarrete R., Hyzy S.L., Hutton D.L., Erdman C.P., Wieland M., Boyan B.D., et al. Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage. Biomaterials 2010, 31:2728-2735.
26. Togashi A.Y., Cirano F.R., Marques M.M., Pustiglioni F.E., Lang N.P., Lima L.A. Effect of recombinant human bone morphogenetic protein-7 (rhBMP-7) on the viability, proliferation and differentiation of osteoblast-like cells cultured on a chemically modified titanium surface. Clin Oral Implants Res 2009, 20:452-457.
27. Martin J.Y., Schwartz Z., Hummert T.W., Schraub D.M., Simpson J., Lankford J., et al. Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). JBiomed Mater Res 1995, 29:389-401.
28. Lincks J., Boyan B.D., Blanchard C.R., Lohmann C.H., Liu Y., Cochran D.L., et al. Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. Biomaterials 1998, 19:2219-2232.
29. Martin J.Y., Dean D.D., Cochran D.L., Simpson J., Boyan B.D., Schwartz Z. Proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63) cultured on previously used titanium surfaces. Clin Oral Implants Res 1996, 7:27-37.
30. Stein G.S., Lian J.B., Owen T.A. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J 1990, 4:3111-3123.
31. Raines A.L., Olivares-Navarrete R., Wieland M., Cochran D.L., Schwartz Z., Boyan B.D. Regulation of angiogenesis during osseointegration by titanium surface microstructure and energy. Biomaterials 2010, 31:4909-4917.
32. Zinger O., Zhao G., Schwartz Z., Simpson J., Wieland M., Landolt D., et al. Differential regulation of osteoblasts by substrate microstructural features. Biomaterials 2005, 26:1837-1847.
33. Schwartz Z., Olivares-Navarrete R., Wieland M., Cochran D.L., Boyan B.D. Mechanisms regulating increased production of osteoprotegerin by osteoblasts cultured on microstructured titanium surfaces. Biomaterials 2009, 30:3390-3396.
34. Olivares-Navarrete R., Hyzy S.L., Hutton D.L., Dunn G.R., Appert C., Boyan B.D., et al. Role of non-canonical Wnt signaling in osteoblast maturation on microstructured titanium surfaces. Acta Biomater 2011, 7:2740-2750.
35. Olivares-Navarrete R., Hyzy S.L., Park J.H., Dunn G.R., Haithcock D.A., Wasilewski C.E., et al. Mediation of osteogenic differentiation of human mesenchymal stem cells on titanium surfaces by a Wnt-integrin feedback loop. Biomaterials 2011, 32:6399-6411.
36. Anselme K., Bigerelle M., Noel B., Dufresne E., Judas D., Iost A., et al. Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses. JBiomed Mater Res 2000, 49:155-166.
37. Anselme K. Osteoblast adhesion on biomaterials. Biomaterials 2000, 21:667-681.
38. Mizuno M., Fujisawa R., Kuboki Y. Type I collagen-induced osteoblastic differentiation of bone-marrow cells mediated by collagen-alpha2beta1 integrin interaction. JCell Physiol 2000, 184:207-213.
39. Xiao G., Wang D., Benson M.D., Karsenty G., Franceschi R.T. Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. JBiol Chem 1998, 273:32988-32994.
40. Keselowsky B.G., Wang L., Schwartz Z., Garcia A.J., Boyan B.D. Integrin α5 controls osteoblastic proliferation and differentiation responses to titanium substrates presenting different roughness characteristics in a roughness independent manner. JBiomed Mater Res Part A 2007, 80A:700-710.
41. Schneider G.B., Zaharias R., Stanford C. Osteoblast integrin adhesion and signaling regulate mineralization. JDent Res 2001, 80:1540-1544.
42. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
43. Schwartz Z., Bell B.F., Wang L., Zhao G., Olivares-Navarrete R., Boyan B.D. Beta-1 integrins mediate substrate dependent effects of 1alpha, 25(OH)2D3 on osteoblasts. JSteroid Biochem Mol Biol 2007, 103:606-609.
44. Yamashita D., Machigashira M., Miyamoto M., Takeuchi H., Noguchi K., Izumi Y., et al. Effect of surface roughness on initial responses of osteoblast-like cells on two types of zirconia. Dent Mater J 2009, 28:461-470.
45. Kokkinos P.A., Koutsoukos P.G., Deligianni D.D. Detachment strength of human osteoblasts cultured on hydroxyapatite with various surface roughness. Contribution of integrin subunits. JMater Sci Mater Med 2012, 23:1489-1498.
46. Ramaglia L., Postiglione L., Di Spigna G., Capece G., Salzano S., Rossi G. Sandblasted-acid-etched titanium surface influences invitro the biological behavior of SaOS-2 human osteoblast-like cells. Dent Mater J 2011, 30:183-192.
47. Luthen F., Lange R., Becker P., Rychly J., Beck U., Nebe J.G. The influence of surface roughness of titanium on beta1- and beta3-integrin adhesion and the organization of fibronectin in human osteoblastic cells. Biomaterials 2005, 26:2423-2440.
48. Omar O., Lenneras M., Svensson S., Suska F., Emanuelsson L., Hall J., et al. Integrin and chemokine receptor gene expression in implant-adherent cells during early osseointegration. JMater Sci Mater Med 2010, 21:969-980.
49. Bougas K., Jimbo R., Xue Y., Mustafa K., Wennerberg A. Novel implant coating agent promotes gene expression of osteogenic markers in rats during early osseointegration. Int J Biomater 2012, 2012:579274.
50. Gronthos S., Stewart K., Graves S.E., Hay S., Simmons P.J. Integrin expression and function on human osteoblast-like cells. JBone Miner Res 1997, 12:1189-1197.
51. Lee J.W., Kim Y.H., Park K.D., Jee K.S., Shin J.W., Hahn S.B. Importance of integrin beta1-mediated cell adhesion on biodegradable polymers under serum depletion in mesenchymal stem cells and chondrocytes. Biomaterials 2004, 25:1901-1909.
52. Yao W., Guan M., Jia J., Dai W., Lay Y.A., Amugongo S., et al. Reversing bone loss by directing mesenchymal stem cells to the bone. Stem Cells 2013 Sep, 31(9):2003-2014.
53. El-Amin S.F., Kofron M.D., Attawia M.A., Lu H.H., Tuan R.S., Laurencin C.T. Molecular regulation of osteoblasts for tissue engineered bone repair. Clin Orthop Relat Res 2004, 427:220-225.
54. Nakayamada S., Okada Y., Saito K., Tamura M., Tanaka Y. Beta1 integrin/focal adhesion kinase-mediated signaling induces intercellular adhesion molecule 1 and receptor activator of nuclear factor kappaB ligand on osteoblasts and osteoclast maturation. JBiol Chem 2003, 278:45368-45374.
55. Schreiber T.D., Steinl C., Essl M., Abele H., Geiger K., Muller C.A., et al. The integrin alpha9beta1 on hematopoietic stem and progenitor cells: involvement in cell adhesion, proliferation and differentiation. Haematologica 2009, 94:1493-1501.
56. Huang Y., Lu X., Qian W., Tang Z., Zhong Y. Competitive protein adsorption on biomaterial surface studied with reflectometric interference spectroscopy. Acta Biomater 2010, 6:2083-2090.
57. Dupont-Gillain C.C., Mc Evoy K.M., Henry M., Bertrand P. Surface spectroscopy of adsorbed proteins: input of data treatment by principal component analysis. JMater Sci Mater Med 2010, 21:955-961.
58. Anthis N.J., Campbell I.D. The tail of integrin activation. Trends Biochem Sci 2011, 36:191-198.
59. Tulla M., Pentikainen O.T., Viitasalo T., Kapyla J., Impola U., Nykvist P., et al. Selective binding of collagen subtypes by integrin alpha 1I, alpha 2I, and alpha 10I domains. JBiol Chem 2001, 276:48206-48212.
60. Gardner H., Broberg A., Pozzi A., Laato M., Heino J. Absence of integrin alpha1beta1 in the mouse causes loss of feedback regulation of collagen synthesis in normal and wounded dermis. JCell Sci 1999, 112(Pt 3):263-272.
61. Gardner H., Kreidberg J., Koteliansky V., Jaenisch R. Deletion of integrin alpha 1 by homologous recombination permits normal murine development but gives rise to a specific deficit in cell adhesion. Dev Biol 1996, 175:301-313.
62. Chen X., Abair T.D., Ibanez M.R., Su Y., Frey M.R., Dise R.S., et al. Integrin alpha1beta1 controls reactive oxygen species synthesis by negatively regulating epidermal growth factor receptor-mediated Rac activation. Mol Cell Biol 2007, 27:3313-3326.
63. Macias-Perez I., Borza C., Chen X., Yan X., Ibanez R., Mernaugh G., et al. Loss of integrin alpha1beta1 ameliorates Kras-induced lung cancer. Cancer Res 2008, 68:6127-6135.
64. Hu H.M., Yang L., Wang Z., Liu Y.W., Fan J.Z., Fan J., et al. Overexpression of integrin a2 promotes osteogenic differentiation of hBMSCs from senile osteoporosis through the ERK pathway. Int J Clin Exp Pathol 2013, 6:841-852.
65. Venstrom K., Reichardt L. Beta 8 integrins mediate interactions of chick sensory neurons with laminin-1, collagen IV, and fibronectin. Mol Biol Cell 1995, 6:419-431.
66. Martin P.T., Sanes J.R. Integrins mediate adhesion to agrin and modulate agrin signaling. Development 1997, 124:3909-3917.
67. Felding-Habermann B., Cheresh D.A. Vitronectin and its receptors. Curr Opin Cell Biol 1993, 5:864-868.
68. Wennerberg K., Lohikangas L., Gullberg D., Pfaff M., Johansson S., Fassler R. Beta 1 integrin-dependent and -independent polymerization of fibronectin. JCell Biol 1996, 132:227-238.
69. Bader B.L., Rayburn H., Crowley D., Hynes R.O. Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all alpha v integrins. Cell 1998, 95:507-519.