Dental Materials
Volume 26, Issue 4 , Pages 275-287 , April 2010

Selective cell affinity of biomimetic micro-nano-hybrid structured TiO2 overcomes the biological dilemma of osteoblasts

  • Norio Hori

      Affiliations

    • The Jane and Jerry Weintraub Center for Reconstructive Biotechnology, Division of Advanced Prosthodontics, Biomaterials and Hospital Dentistry, UCLA School of Dentistry, Los Angeles, CA, USA
    • These authors equally contributed.
    • ,
  • Fuminori Iwasa

      Affiliations

    • The Jane and Jerry Weintraub Center for Reconstructive Biotechnology, Division of Advanced Prosthodontics, Biomaterials and Hospital Dentistry, UCLA School of Dentistry, Los Angeles, CA, USA
    • These authors equally contributed.
    • ,
  • Takeshi Ueno

      Affiliations

    • The Jane and Jerry Weintraub Center for Reconstructive Biotechnology, Division of Advanced Prosthodontics, Biomaterials and Hospital Dentistry, UCLA School of Dentistry, Los Angeles, CA, USA
    • These authors equally contributed.
    • ,
  • Kazuo Takeuchi

      Affiliations

    • Department of Prosthodontics, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan
    • ,
  • Naoki Tsukimura

      Affiliations

    • The Jane and Jerry Weintraub Center for Reconstructive Biotechnology, Division of Advanced Prosthodontics, Biomaterials and Hospital Dentistry, UCLA School of Dentistry, Los Angeles, CA, USA
    • ,
  • Masahiro Yamada

      Affiliations

    • The Jane and Jerry Weintraub Center for Reconstructive Biotechnology, Division of Advanced Prosthodontics, Biomaterials and Hospital Dentistry, UCLA School of Dentistry, Los Angeles, CA, USA
    • ,
  • Masami Hattori

      Affiliations

    • Department of Prosthodontics, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan
    • ,
  • Akiko Yamamoto

      Affiliations

    • Biomaterials Center, National Institute for Materials Science, Tsukuba, 305-0044, Japan
    • ,
  • Takahiro Ogawa

      Affiliations

    • The Jane and Jerry Weintraub Center for Reconstructive Biotechnology, Division of Advanced Prosthodontics, Biomaterials and Hospital Dentistry, UCLA School of Dentistry, Los Angeles, CA, USA
    • Corresponding Author InformationCorresponding author at: Laboratory for Bone and Implant Sciences (LBIS), The Jane and Jerry Weintraub Center for Reconstructive Biotechnology, Division of Advanced Prosthodontics, Biomaterials and Hospital Dentistry, UCLA School of Dentistry, 10833 Le Conte Avenue (B3-081 CHS), Box 951668, Los Angeles, CA 90095-1668, USA. Tel.: +1 310 825 0727; fax: +1 310 825 6345.

Received 19 July 2009 ,Revised 13 November 2009 ,Accepted 18 November 2009.

References 

  1. Masuda T, Yliheikkila PK, Felton DA, Cooper LF. Generalizations regarding the process and phenomenon of osseointegration. Part I. In vivo studies. Int J Oral Maxillofac Implants. 1998;13:17–29
  2. Brunski JB, Puleo DA, Nanci A. Biomaterials and biomechanics of oral and maxillofacial implants: current status and future developments. Int J Oral Maxillofac Implants. 2000;15:15–46
  3. 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
  4. Olivares-Navarrete R, Raz P, Zhao G, Chen J, Wieland M, Cochran DL, 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 USA. 2008;105:15767–15772
  5. Albrektsson T, Wennerberg A. Oral implant surfaces: Part 1—review focusing on topographic and chemical properties of different surfaces and in vivo responses to them. Int J Prosthodont. 2004;17:536–543
  6. Takeuchi K, Saruwatari L, Nakamura HK, Yang JM, Ogawa T. Enhanced intrinsic biomechanical properties of osteoblastic mineralized tissue on roughened titanium surface. J Biomed Mater Res A. 2005;72A:296–305
  7. Kubo K, Att W, Yamada M, Ohmi K, Tsukimura N, Suzuki T, et al. Microtopography of titanium suppresses osteoblastic differentiation but enhances chondroblastic differentiation of rat femoral periosteum-derived cells. J Biomed Mater Res A. 2008;87:380–391
  8. Matsuzaka K, Walboomers F, de Ruijter A, Jansen JA. Effect of microgrooved poly-l-lactic (PLA) surfaces on proliferation, cytoskeletal organization, and mineralized matrix formation of rat bone marrow cells. Clin Oral Implants Res. 2000;11:325–333
  9. Boyan BD, Hummert TW, Dean DD, Schwartz Z. Role of material surfaces in regulating bone and cartilage cell response. Biomaterials. 1996;17:137–146
  10. Wennerberg A, Albrektsson T. Suggested guidelines for the topographic evaluation of implant surfaces. Int J Oral Maxillofac Implants. 2000;15:331–344
  11. Cooper LF, Masuda T, Yliheikkila PK, Felton DA. Generalizations regarding the process and phenomenon of osseointegration. Part II. In vitro studies. Int J Oral Maxillofac Implants. 1998;13:163–174
  12. Ogawa T, Nishimura I. Genes differentially expressed in titanium implant healing. J Dent Res. 2006;85:566–570
  13. Albrektsson T, Wennerberg A. Oral implant surfaces: Part 2--review focusing on clinical knowledge of different surfaces. Int J Prosthodont. 2004;17:544–564
  14. Stein GS, Lian JB. Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. Endocr Rev. 1993;14:424–442
  15. Siddhanti SR, Quarles LD. Molecular to pharmacologic control of osteoblast proliferation and differentiation. J Cell Biochem. 1994;55:310–320
  16. Alborzi A, Mac K, Glackin CA, Murray SS, Zernik JH. Endochondral and intramembranous fetal bone development: osteoblastic cell proliferation, and expression of alkaline phosphatase, m-twist, and histone H4. J Craniofac Genet Dev Biol. 1996;16:94–106
  17. Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS, et al. Progressive development of the rat osteoblast phenotype in vitro: reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol. 1990;143:420–430
  18. Spinella-Jaegle S, Roman-Roman S, Faucheu C, Dunn FW, Kawai S, Gallea S, et al. Opposite effects of bone morphogenetic protein-2 and transforming growth factor-beta1 on osteoblast differentiation. Bone. 2001;29:323–330
  19. Alliston T, Choy L, Ducy P, Karsenty G, Derynck R. TGF-beta-induced repression of CBFA1 by Smad3 decreases cbfa1 and osteocalcin expression and inhibits osteoblast differentiation. EMBO J. 2001;20:2254–2272
  20. Ogawa T, Sukotjo C, Nishimura I. Modulated bone matrix-related gene expression is associated with differences in interfacial strength of different implant surface roughness. J Prosthodont. 2002;11:241–247
  21. Ogawa T, Nishimura I. Different bone integration profiles of turned and acid-etched implants associated with modulated expression of extracellular matrix genes. Int J Oral Maxillofac Implants. 2003;18:200–210
  22. Bachle M, Kohal RJ. A systematic review of the influence of different titanium surfaces on proliferation, differentiation and protein synthesis of osteoblast-like MG63 cells. Clin Oral Implants Res. 2004;15:683–692
  23. Zhao G, Schwartz Z, Wieland M, Rupp F, Geis-Gerstorfer J, Cochran DL, et al. High surface energy enhances cell response to titanium substrate microstructure. J Biomed Mater Res A. 2005;74:49–58
  24. Boyan BD, Bonewald LF, Paschalis EP, Lohmann CH, Rosser J, Cochran DL, et al. Osteoblast-mediated mineral deposition in culture is dependent on surface microtopography. Calcif Tissue Int. 2002;71:519–529
  25. Lu L, Yaszemski MJ, Mikos AG. TGF-beta1 release from biodegradable polymer microparticles: its effects on marrow stromal osteoblast function. J Bone Joint Surg Am. 2001;83-A(Suppl. 1):S82–S91
  26. Bonewald LF, Dallas SL. Role of active and latent transforming growth factor beta in bone formation. J Cell Biochem. 1994;55:350–357
  27. Centrella M, Horowitz MC, Wozney JM, McCarthy TL. Transforming growth factor-beta gene family members and bone. Endocr Rev. 1994;15:27–39
  28. Sanchez C, Arribart H, Guille MM. Biomimetism and bioinspiration as tools for the design of innovative materials and systems. Nat Mater. 2005;4:277–288
  29. Tamerler C, Sarikaya M. Molecular biomimetics: utilizing nature's molecular ways in practical engineering. Acta Biomater. 2007;3:289–299
  30. Fantner GE, Hassenkam T, Kindt JH, Weaver JC, Birkedal H, Pechenik L, et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat Mater. 2005;4:612–616
  31. Tai K, Dao M, Suresh S, Palazoglu A, Ortiz C. Nanoscale heterogeneity promotes energy dissipation in bone. Nat Mater. 2007;6:454–462
  32. Balasundaram G, Webster TJ. Nanotechnology and biomaterials for orthopedic medical applications. Nanomedicine. 2006;1:169–176
  33. Dalby MJ, Gadegaard N, Curtis AS, Oreffo RO. Nanotopographical control of human osteoprogenitor differentiation. Curr Stem Cell Res Ther. 2007;2:129–138
  34. Smith LJ, Swaim JS, Yao C, Haberstroh KM, Nauman EA, Webster TJ. Increased osteoblast cell density on nanostructured PLGA-coated nanostructured titanium for orthopedic applications. Int J Nanomed. 2007;2:493–499
  35. Variola F, Yi JH, Richert L, Wuest JD, Rosei F, Nanci A. Tailoring the surface properties of Ti6Al4V by controlled chemical oxidation. Biomaterials. 2008;29:1285–1298
  36. Dalby MJ, McCloy D, Robertson M, Agheli H, Sutherland D, Affrossman S, et al. Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials. 2006;27:2980–2987
  37. Sarikaya M, Tamerler C, Jen AK, Schulten K, Baneyx F. Molecular biomimetics: nanotechnology through biology. Nat Mater. 2003;2:577–585
  38. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, et al. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater. 2007;6:997–1003
  39. Lim JY, Donahue HJ. Cell sensing and response to micro- and nanostructured surfaces produced by chemical and topographic patterning. Tissue Eng. 2007;13:1879–1891
  40. Ogawa T, Saruwatari L, Takeuchi K, Aita H, Ohno N. Ti nano-nodular structuring for bone integration and regeneration. J Dent Res. 2008;87:751–756
  41. Aita H, Hori N, Takeuchi M, Suzuki T, Yamada M, Anpo M, et al. The effect of ultraviolet functionalization of titanium on integration with bone. Biomaterials. 2009;30:1015–1025
  42. Hori N, Att W, Ueno T, Sato N, Yamada M, Saruwatari L, et al. Age-dependent degradation of protein adsorption capacity of Ti. J Dent Res. 2009;88:663–667
  43. Suzuki T, Hori N, Att W, Kubo K, Iwasa F, Ueno T, et al. UV treatment overcomes time-related degrading bioactivity of titanium. Tissue Eng Part A Epub ahead of print, doi: 10.1089/ten.TEA.2008.0568.
  44. Saruwatari L, Aita H, Butz F, Nakamura HK, Ouyang J, Yang Y, et al. Osteoblasts generate harder, stiffer, and more delamination-resistant mineralized tissue on titanium than on polystyrene, associated with distinct tissue micro- and ultrastructure. J Bone Miner Res. 2005;20:2002–2016
  45. Kessler G, Wolfman M. An automated procedure for the simultaneous determination of calcium and phosphorus. Clin Chem. 1964;10:686–703
  46. Dieudonne SC, van den Dolder J, de Ruijter JE, Paldan H, Peltola T, van’t Hof MA, et al. Osteoblast differentiation of bone marrow stromal cells cultured on silica gel and sol–gel-derived titania. Biomaterials. 2002;23:3041–3051
  47. Tullberg-Reinert H, Jundt G. In situ measurement of collagen synthesis by human bone cells with a sirius red-based colorimetric microassay: effects of transforming growth factor beta2 and ascorbic acid 2-phosphate. Histochem Cell Biol. 1999;112:271–276
  48. Woo KM, Seo J, Zhang R, Ma PX. Suppression of apoptosis by enhanced protein adsorption on polymer/hydroxyapatite composite scaffolds. Biomaterials. 2007;28:2622–2630
  49. Mata A, Su X, Fleischman AJ, Roy S, Banks BA, Miller SK, et al. Osteoblast attachment to a textured surface in the absence of exogenous adhesion proteins. IEEE Trans Nanobiosci. 2003;2:287–294
  50. Dalby MJ, McCloy D, Robertson M, Wilkinson CD, Oreffo RO. Osteoprogenitor response to defined topographies with nanoscale depths. Biomaterials. 2006;27:1306–1315
  51. Dalby MJ, Gadegaard N, Wilkinson CD. The response of fibroblasts to hexagonal nanotopography fabricated by electron beam lithography. J Biomed Mater Res A. 2008;84:973–979
  52. Seunarine K, Curtis A, Meredith D, Wilkinson C, Riehle M, Gadegaard N. A hierarchical response of cells to perpendicular micro- and nanometric textural cues. IEEE Trans Nanobiosci. 2009;
  53. LeGeros RZ, Craig RG. Strategies to affect bone remodeling: osteointegration. J Bone Miner Res. 1993;8(Suppl. 2):S583–S596
  54. Puleo DA, Nanci A. Understanding and controlling the bone–implant interface. Biomaterials. 1999;20:2311–2321
  55. Pilliar RM. Cementless implant fixation—toward improved reliability. Orthop Clin North Am. 2005;36:113–119
  56. Ogawa T, Ozawa S, Shih JH, Ryu KH, Sukotjo C, Yang JM, et al. Biomechanical evaluation of osseous implants having different surface topographies in rats. J Dent Res. 2000;79:1857–1863
  57. Klokkevold PR, Johnson P, Dadgostari S, Caputo A, Davies JE, Nishimura RD. Early endosseous integration enhanced by dual acid etching of titanium: a torque removal study in the rabbit. Clin Oral Implants Res. 2001;12:350–357
  58. Att W, Hori N, Takeuchi M, Ouyang J, Yang Y, Anpo M, et al. Time-dependent degradation of titanium osteoconductivity: an implication of biological aging of implant materials. Biomaterials. 2009;30:5352–5363

PII: S0109-5641(09)00422-9

doi: 10.1016/j.dental.2009.11.077

Dental Materials
Volume 26, Issue 4 , Pages 275-287 , April 2010

Article Tools

* Image Usage & Resolution