Molecular and structural patterns of bone regeneration in surgically created defects containing bone substitutes

Biomaterials

Volumn 35, Issue 10, 2014, Pages 3229-3242

  Elgali, Ibrahim ^a,e   Igawa, Kazuyo ^a,e   Palmquist, Anders ^a,e   Lennerås, Maria ^a,e   Xia, Wei ^b,e   Choi, Sungjin ^c   Chung, Ung Il ^c,d   Omar, Omar ^a,e   Thomsen, Peter ^a,e  

^a SAHLGRENSKA ACADEMY AT UNIVERSITY OF GOTHENBURG   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e BIOMATCELL VINN Excellence Center of Biomaterials and Cell Therapy   (Sweden)

Author keywords

Deproteinized bovine bone; Gene expression; In vivo; Octacalcium phosphate; Ultrastructure; Tricalcium phosphate

Indexed keywords

CALCIUM PHOSPHATE; GENE EXPRESSION; MAMMALS; MICROSTRUCTURE; TISSUE REGENERATION;

BOVINE BONE; IN-VIVO; OCTACALCIUM PHOSPHATE; TRI-CALCIUM PHOSPHATES; ULTRASTRUCTURE;

DEFECTS;

CALCIUM PHOSPHATE;

ANIMAL TISSUE; ARTICLE; BONE DEFECT; BONE PROSTHESIS; BONE REGENERATION; BONE REMODELING; BONE STRUCTURE; CHEMICAL STRUCTURE; EPIPHYSIS; FEMALE; FEMUR; GENE EXPRESSION; HISTOLOGY; MORPHOMETRICS; NONHUMAN; OSSIFICATION; OSTEOCLAST ACTIVITY; OSTEOGENESIS IMPERFECTA; PRIORITY JOURNAL; RAT; RECEPTOR DOWN REGULATION; TRABECULAR BONE; ULTRASTRUCTURE;

BOVINAE; RATTUS; TETRAPODA;

DEPROTEINIZED BOVINE BONE; GENE EXPRESSION; IN VIVO; OCTACALCIUM PHOSPHATE; ULTRASTRUCTURE; Α-TRICALCIUM PHOSPHATE;

ANIMALS; BONE REGENERATION; BONE REMODELING; BONE SUBSTITUTES; CALCIUM PHOSPHATES; CATTLE; FEMALE; GENE EXPRESSION; MICROSCOPY, ELECTRON, SCANNING; POLYMERASE CHAIN REACTION; RATS; RATS, SPRAGUE-DAWLEY; X-RAY DIFFRACTION;

EID: 84893644395     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.12.084     Document Type: Article

References (50)

1. Brydone A.S., Meek D., Maclaine S. Bone grafting, orthopaedic biomaterials, and the clinical need for bone engineering. Proc Inst Mech Eng H 2010, 224:1329-1343.
2. Eppley B.L., Pietrzak W.S., Blanton M.W. Allograft and alloplastic bone substitutes: a review of science and technology for the craniomaxillofacial surgeon. J Craniofac Surg 2005, 16:981-989.
3. Lee D.Z., Chen S.T., Darby I.B. Maxillary sinus floor elevation and grafting with deproteinized bovine bone mineral: a clinical and histomorphometric study. Clin Oral Implants Res 2012, 23:918-924.
4. Schlegel A.K., Donath K. BIO-OSS-a resorbable bone substituteα. J Long Term Eff Med Implants 1998, 8:201-209.
5. Schlegel A.K., Donath K., Weida S. Histological findings in guided bone regeneration (GBR) around titanium dental implants with autogenous bone chips using a new resorbable membrane. J Long Term Eff Med Implants 1998, 8:211-224.
6. Hwang J.W., Park J.S., Lee J.S., Jung U.W., Kim C.S., Cho K.S., et al. Comparative evaluation of three calcium phosphate synthetic block bone graft materials for bone regeneration in rabbit calvaria. J Biomed Mater Res B Appl Biomater 2012, 100:2044-2052.
7. LeGeros R.Z. Calcium phosphate-based osteoinductive materials. Chem Rev 2008, 108:4742-4753.
8. Choi S., Liu I.L., Yamamoto K., Igawa K., Mochizuki M., Sakai T., et al. Development and evaluation of tetrapod-shaped granular artificial bones. Acta Biomater 2012, 8:2340-2347.
9. Bab I., Sela J. Cellular and molecular aspects of bone repair. Principles of bone regeneration 2012, 11-41. Springer, New York, US. J. Sela, I. Bab (Eds.).
10. Ai-Aql Z.S., Alagl A.S., Graves D.T., Gerstenfeld L.C., Einhorn T.A. Molecular mechanisms controlling bone formation during fracture healing and distraction osteogenesis. J Dent Res 2008, 87:107-118.
11. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
12. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3. RESEARCH0034.
13. Andersen C.L., Jensen J.L., Orntoft T.F. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004, 64:5245-5250.
14. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
15. Jarmar T., Palmquist A., Branemark R., Hermansson L., Engqvist H., Thomsen P. Technique for preparation and characterization in cross-section of oral titanium implant surfaces using focused ion beam and transmission electron microscopy. J Biomed Mater Res A 2008, 87:1003-1009.
16. Omar O., Svensson S., Zoric N., Lenneras M., Suska F., Wigren S., et al. In vivo gene expression in response to anodically oxidized versus machined titanium implants. J Biomed Mater Res A 2010, 92:1552-1566.
17. Omar O.M., Lenneras M.E., Suska F., Emanuelsson L., Hall J.M., Palmquist A., et al. The correlation between gene expression of proinflammatory markers and bone formation during osseointegration with titanium implants. Biomaterials 2011, 32:374-386.
18. Gerstenfeld L.C., Cho T.J., Kon T., Aizawa T., Cruceta J., Graves B.D., et al. Impaired intramembranous bone formation during bone repair in the absence of tumor necrosis factor-alpha signaling. Cells Tissues Organs 2001, 169:285-294.
19. Kon T., Cho T.J., Aizawa T., Yamazaki M., Nooh N., Graves D., et al. Expression of osteoprotegerin, receptor activator of NF-kappaB ligand (osteoprotegerin ligand) and related proinflammatory cytokines during fracture healing. J Bone Miner Res 2001, 16:1004-1014.
20. Mountziaris P.M., Mikos A.G. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng Part B Rev 2008, 14:179-186.
21. Azuma Y., Kaji K., Katogi R., Takeshita S., Kudo A. Tumor necrosis factor-alpha induces differentiation of and bone resorption by osteoclasts. J Biol Chem 2000, 275:4858-4864.
22. Fu X., Han B., Cai S., Lei Y., Sun T., Sheng Z. Migration of bone marrow-derived mesenchymal stem cells induced by tumor necrosis factor-alpha and its possible role in wound healing. Wound Repair Regen 2009, 17:185-191.
23. Hess K., Ushmorov A., Fiedler J., Brenner R.E., Wirth T. TNFalpha promotes osteogenic differentiation of human mesenchymal stem cells by triggering the NF-kappaB signaling pathway. Bone 2009, 45:367-376.
24. Gilbert L., He X., Farmer P., Boden S., Kozlowski M., Rubin J., et al. Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology 2000, 141:3956-3964.
25. Gilbert L., He X., Farmer P., Rubin J., Drissi H., van Wijnen A.J., et al. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem 2002, 277:2695-2701.
26. Klinge B., Alberius P., Isaksson S., Jonsson J. Osseous response to implanted natural bone mineral and synthetic hydroxylapatite ceramic in the repair of experimental skull bone defects. J Oral Maxillofac Surg 1992, 50:241-249.
27. Tapety F.I., Amizuka N., Uoshima K., Nomura S., Maeda T. A histological evaluation of the involvement of Bio-Oss in osteoblastic differentiation and matrix synthesis. Clin Oral Implants Res 2004, 15:315-324.
28. Traini T., Valentini P., Iezzi G., Piattelli A. A histologic and histomorphometric evaluation of anorganic bovine bone retrieved 9 years after a sinus augmentation procedure. J Periodontol 2007, 78:955-961.
29. Bassil J., Senni K., Changotade S., Baroukh B., Kassis C., Naaman N., et al. Expression of MMP-2, 9 and 13 in newly formed bone after sinus augmentation using inorganic bovine bone in human. J Periodont Res 2011, 46:756-762.
30. Schwartz Z., Weesner T., van Dijk S., Cochran D.L., Mellonig J.T., Lohmann C.H., et al. Ability of deproteinized cancellous bovine bone to induce new bone formation. J Periodontol 2000, 71:1258-1269.
31. Mordenfeld A., Hallman M., Johansson C.B., Albrektsson T. Histological and histomorphometrical analyses of biopsies harvested 11 years after maxillary sinus floor augmentation with deproteinized bovine and autogenous bone. Clin Oral Implants Res 2010, 21:961-970.
32. Yildirim M., Spiekermann H., Biesterfeld S., Edelhoff D. Maxillary sinus augmentation using xenogenic bone substitute material Bio-Oss in combination with venous blood. A histologic and histomorphometric study in humans. Clin Oral Implants Res 2000, 11:217-229.
33. Oliveira R., El Hage M., Carrel J.P., Lombardi T., Bernard J.P. Rehabilitation of the edentulous posterior maxilla after sinus floor elevation using deproteinized bovine bone: a 9-year clinical study. Implant Dent 2012, 21:422-426.
34. Kamakura S., Sasano Y., Homma-Ohki H., Nakamura M., Suzuki O., Kagayama M., et al. Multinucleated giant cells recruited by implantation of octacalcium phosphate (OCP) in rat bone marrow share ultrastructural characteristics with osteoclasts. J Electron Microsc (Tokyo) 1997, 46:397-403.
35. Murakami Y., Honda Y., Anada T., Shimauchi H., Suzuki O. Comparative study on bone regeneration by synthetic octacalcium phosphate with various granule sizes. Acta Biomater 2010, 6:1542-1548.
36. Takami M., Mochizuki A., Yamada A., Tachi K., Zhao B., Miyamoto Y., et al. Osteoclast differentiation induced by synthetic octacalcium phosphate through receptor activator of NF-kappaB ligand expression in osteoblasts. Tissue Eng Part A 2009, 15:3991-4000.
37. Oreffo R.O., Mundy G.R., Seyedin S.M., Bonewald L.F. Activation of the bone-derived latent TGF beta complex by isolated osteoclasts. Biochem Biophys Res Commun 1989, 158:817-823.
38. Pfeilschifter J., Bonewald L., Mundy G.R. Characterization of the latent transforming growth factor beta complex in bone. J Bone Miner Res 1990, 5:49-58.
39. Tang Y., Wu X., Lei W., Pang L., Wan C., Shi Z., et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 2009, 15:757-765.
40. Zhao C., Irie N., Takada Y., Shimoda K., Miyamoto T., Nishiwaki T., et al. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 2006, 4:111-121.
41. Pederson L., Ruan M., Westendorf J.J., Khosla S., Oursler M.J. Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate. Proc Natl Acad Sci U S A 2008, 105:20764-20769.
42. Ryu J., Kim H.J., Chang E.J., Huang H., Banno Y., Kim H.H. Sphingosine 1-phosphate as a regulator of osteoclast differentiation and osteoclast-osteoblast coupling. EMBO J 2006, 25:5840-5851.
43. Takeshita S., Fumoto T., Matsuoka K., Park K.A., Aburatani H., Kato S., et al. Osteoclast-secreted CTHRC1 in the coupling of bone resorption to formation. J Clin Invest 2013, 123:3914-3924.
44. de Bruijn J.D., Bovell Y.P., Davies J.E., van Blitterswijk C.A. Osteoclastic resorption of calcium phosphates is potentiated in postosteogenic culture conditions. J Biomed Mater Res 1994, 28:105-112.
45. Gilles J.A., Carnes D.L., Windeler A.S. Development of an in vitro culture system for the study of osteoclast activity and function. J Endod 1994, 20:327-331.
46. Gomi K., Lowenberg B., Shapiro G., Davies J.E. Resorption of sintered synthetic hydroxyapatite by osteoclasts in vitro. Biomaterials 1993, 14:91-96.
47. Yamada S., Heymann D., Bouler J.M., Daculsi G. Osteoclastic resorption of biphasic calcium phosphate ceramic in vitro. J Biomed Mater Res 1997, 37:346-352.
48. Dimitriou R., Tsiridis E., Giannoudis P.V. Current concepts of molecular aspects of bone healing. Injury 2005, 36:1392-1404.
49. Jimi E., Nakamura I., Duong L.T., Ikebe T., Takahashi N., Rodan G.A., et al. Interleukin 1 induces multinucleation and bone-resorbing activity of osteoclasts in the absence of osteoblasts/stromal cells. Exp Cell Res 1999, 247:84-93.
50. Katagiri T., Takahashi N. Regulatory mechanisms of osteoblast and osteoclast differentiation. Oral Dis 2002, 8:147-159.