TGF-β1 and BMP-4 carried by liposomes enhance the healing process in alveolar bone

Archives of Oral Biology

Volumn 58, Issue 6, 2013, Pages 646-656

  Ferreira, Cynthia Lopes ^a   Abreu, Fernando Antônio Mauad De ^a   Silva, Gerluza Aparecida Borges ^a   Silveira, Frank Ferreira ^b   Barreto, Luana Beatriz Araújo ^c   Paulino, Tony De Paiva ^c   Miziara, Melissa Nunes ^c   Alves, José Bento ^a,c  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b PONTIFICAL CATHOLIC UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITY OF UBERABA   (Brazil)

Author keywords

Bone regeneration; Controlled delivery; Liposome; Tooth socket

Indexed keywords

BMP4 PROTEIN, RAT; BONE MORPHOGENETIC PROTEIN 4; COLLAGEN TYPE 3; DRUG CARRIER; FIBRONECTIN; LIPOSOME; TRANSFORMING GROWTH FACTOR BETA1;

ANGIOGENESIS; ANIMAL; ARTICLE; BLOOD CLOTTING; BONE DEVELOPMENT; COMPARATIVE STUDY; DRUG EFFECT; JAW; MALE; MAXILLA; OSTEOBLAST; OSTEOCLAST; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; RAT; TIME; TOOTH EXTRACTION; TOOTH SOCKET; VASCULARIZATION; WISTAR RAT; WOUND HEALING;

ALVEOLAR PROCESS; ANIMALS; BLOOD COAGULATION; BONE MORPHOGENETIC PROTEIN 4; COLLAGEN TYPE III; DRUG CARRIERS; FIBRONECTINS; LIPOSOMES; MALE; MAXILLA; NEOVASCULARIZATION, PHYSIOLOGIC; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; RANDOM ALLOCATION; RATS; RATS, WISTAR; TIME FACTORS; TOOTH EXTRACTION; TOOTH SOCKET; TRANSFORMING GROWTH FACTOR BETA1; WOUND HEALING;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 84877582403     PISSN: 00039969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.archoralbio.2012.11.013     Document Type: Article

References (71)

1. F.B. Basmanav, G.T. Kose, and V. Hasirci Sequential growth factor delivery from complexed microspheres for bone tissue engineering Biomaterials 29 31 2008 4195 4204
2. R. Dimitriou, E. Jones, D. McGonagle, and P.V. Giannoudis Bone regeneration: current concepts and future directions BMC Medicine 31 9 2011 66
3. C.R. Reis-Filho, E.R. Silva, A.B. Martins, F.F. Pessoa, P.V. Gomes, and M.S. de Araújo Demineralised human dentine matrix stimulates the expression of VEGF and accelerates the bone repair in tooth sockets of rats Archives of Oral Biology 57 2012 469 476
4. C.T. Laurencin, A.M.A. Ambrosio, M.D. Borden, and J.A. Cooper Tissue engineering: orthopedic applications Annual Review of Biomedical Engineering 1 1999 19 46
5. U. Meyer, U. Joos, and H.P. Wiesmann Biological and biophysical principles in extracorporal bone tissue engineering. Part I International Journal of Oral and Maxillofacial Surgery 33 4 2004 325 332
6. S.F. El-Amin, M.V. Hogan, A.A. Allen, J. Hinds, and C.T. Laurencin The indications and use of bone morphogenetic proteins in foot, ankle, and tibia surgery Foot and Ankle Clinics 15 4 2010 543 551
7. A. Abarrategi, M.C. Gutiérrez, C. Moreno-Vicente, M.J. Hortigüela, V. Ramos, and J.L. López-Lacomba Multiwall carbon nanotube scaffolds for tissue engineering purposes Biomaterials 29 1 2008 94 102
8. S. Bhattacharyya, S. Guillot, H. Dabboue, J.F. Tranchant, and J.P. Salvetat Carbon nanotubes as structural nanofibers for hyaluronic acid hydrogel scaffolds Biomacromolecules 9 2 2008 505 510
9. B. Sitharaman, X. Shi, X.F. Walboomers, H. Liao, V. Cuijpers, and L.J. Wilson In vivo biocompatibility of ultra-short single-walled carbon nanotube/biodegradable polymer nanocomposites for bone tissue engineering Bone 43 2 2008 362 370
10. W. Tutak, K.H. Park, A. Vasilov, V. Starovoytov, G. Fanchini, and S.-Q. Cai Toxicity induced enhanced extracellular matrix production in osteoblastic cells cultured on single-walled carbon nanotube networks Nanotechnology 20 25 2009 255101
11. G.E. Friedlaender, C.R. Perry, J.D. Cole, S.D. Cook, G. Cierny, and G.F. Muschler Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions Journal of Bone and Joint Surgery 83-A Suppl. 1 (Pt 2) 2001 S151 S158
12. I. Seto, N. Tachikawa, M. Mori, S. Hoshino, E. Marukawa, and I. Asahina Restoration of occlusal function using osseointegrated implants in the canine mandible reconstructed by rhBMP-2 Clinical Oral Implants Research 13 5 2002 536 541
13. A.T. Raiche, and D.A. Puleo In vitro effects of combined and sequential delivery of two bone growth factors Biomaterials 25 4 2004 677 685
14. C.N. Manning, H.M. Kim, S. Sakiyama-Elbert, L.M. Galatz, N. Havlioglu, and S. Thomopoulos Sustained delivery of transforming growth factor beta three enhances tendon-to-bone healing in a rat model Journal of Orthopaedic Research 29 7 2011 1099 1105
15. K. Lee, E.A. Silva, and D.J. Mooney Growth factor delivery-based tissue engineering: general approaches and a review of recent developments Journal of the Royal Society, Interface 8 55 2011 153 170
16. Y.H. Shen, M.S. Shoichet, and M. Radisic Vascular endothelial growth factor immobilized in collagen scaffold promotes penetration and proliferation of endothelial cells Acta Biomaterialia 4 3 2008 477 489
17. S.H. Lee, and H. Shin Matrices and scaffolds for delivery of bioactive molecules in bone and cartilage tissue engineering Advanced Drug Delivery Reviews 59 4-5 2007 339 359
18. U. Edlund, S. Danmark, and A.C. Albertsson A strategy for the covalent functionalization of resorbable polymers with heparin and osteoinductive growth factor Biomacromolecules 9 3 2008 901 905
19. D. Kaigler, J.A. Cirelli, and W.V. Giannobile Growth factor delivery for oral and periodontal tissue engineering Expert Opinion on Drug Delivery 3 5 2006 647 662
20. V. Luginbuehl, L. Meinel, H.P. Merkle, and B. Gander Localized delivery of growth factors for bone repair European Journal of Pharmaceutics and Biopharmaceutics 58 2 2004 197 208
21. G. Schmidmaier, B. Wildemann, J. Heeger, T. Gäbelein, A. Flyvbjerg, and H.J. Bail Improvement of fracture healing by systemic administration of growth hormone and local application of insulin-like growth factor-1 and transforming growth factor-beta1 Bone 31 1 2002 165 172
22. I. Ono, T. Yamashita, H.Y. Jin, Y. Ito, H. Hamada, and Y. Akasaka Combination of porous hydroxyapatite and cationic liposomes as a vector for BMP-2 gene therapy Biomaterials 25 19 2004 4709 4718
23. J.E. Babensee, L.V. McIntire, and A.G. Mikos Growth factor delivery for tissue engineering Pharmaceutical Research 17 5 2000 497 504
24. E. Anitua, M. Sánchez, G. Orive, and I. Andía The potential impact of the preparation rich in growth factors (PRGF) in different medical fields Biomaterials 28 31 2007 4551 4560
25. S. Zhang, and H. Uludaǧ Nanoparticulate systems for growth factor delivery Pharmaceutical Research 26 7 2009 1561 1580
26. E.R. Edelman, M.A. Nugent, and M.J. Karnovsky Perivascular and intravenous administration of basic fibroblast growth factor: vascular and solid organ deposition Proceedings of the National Academy of Sciences of the United States of America 90 4 1993 1513 1517
27. J.D. Golden, A.L. Jones, R.W. Bucholz, M.J. Bosse, T.R. Lyon, and L.X. Webb Recombinant human BMP-2 and allograft compared with autogenous bone graft for reconstruction of diaphyseal tibial fractures with cortical defects Journal of Bone and Joint Surgery 90 5 2008 1168 1169
28. P. Couvreur, and F. Puisieux Nano- and microparticles for the delivery of polypeptides and proteins Advanced Drug Delivery Reviews 10 1993 141 162
29. S.L. Law, K.J. Huang, and C.H. Chiang Acyclovir-containing liposomes for potential ocular delivery. Corneal penetration and absorption Journal of Controlled Release 63 1-2 2000 135 140
30. T. Kubo, T. Sugita, S. Shimose, Y. Nitta, Y. Ikuta, and T. Murakami Targeted systemic chemotherapy using magnetic liposomes with incorporated adriamycin for osteosarcoma in hamsters International Journal of Oncology 18 1 2001 121 125
31. T. Matsuo, T. Sugita, T. Kubo, Y. Yasunaga, M. Ochi, and T. Murakami Injectable magnetic liposomes as a novel carrier of recombinant human BMP-2 for bone formation in a rat bone-defect model Journal of Biomedical Materials Research A 66 4 2003 747 754
32. S.S. Ling, E. Magosso, N.A. Khan, K.H. Yuen, and S.A. Barker Enhanced oral bioavailability and intestinal lymphatic transport of a hydrophilic drug using liposomes Drug Development and Industrial Pharmacy 32 3 2006 335 345
33. K. Sou, B. Goins, M.M. Leland, E. Tsuchida, and W.T. Phillips Bone marrow-targeted liposomal carriers: a feasibility study in nonhuman primates Nanomedicine (London) 5 1 2010 41 49
34. C. Spuch, and C. Navarro Liposomes for targeted delivery of active agents against neurodegenerative diseases (Alzheimer's disease and Parkinson's disease) Journal of Drug Delivery 2011 2011 469679
35. X. Chen, W. Huang, B.C. Wong, L. Yin, Y.F. Wong, and M. Xu Liposomes prolong the therapeutic effect of anti-asthmatic medication via pulmonary delivery International Journal of Nanomedicine 7 2012 1139 1148
36. H.K. Han, H.J. Shin, and D.H. Ha Improved oral bioavailability of alendronate via the mucoadhesive liposomal delivery system European Journal of Pharmaceutical Sciences 46 2012 500 507
37. M. Rampichová, L. Martinová, E. Koštá ková, E. Filová, A. Míčková, and M. Buzgo A simple drug anchoring microfiber scaffold for chondrocyte seeding and proliferation Journal of Materials Science Materials in Medicine 23 2 2012 555 563
38. F. Xie, N. Yao, Y. Qin, Q. Zhang, H. Chen, and M. Yuan Investigation of glucose-modified liposomes using polyethylene glycols with different chain lengths as the linkers for brain targeting International Journal of Nanomedicine 7 2012 163 175
39. G. Zhang, B. Guo, H. Wu, T. Tang, B.T. Zhang, and L. Zheng A delivery system targeting bone formation surfaces to facilitate RNAi-based anabolic therapy Nature Medicine 18 2 2012 307 314
40. A. Samad, Y. Sultana, and M. Aqil Liposomal drug delivery systems: an update review Current Drug Delivery 4 4 2007 297 305
41. J.B. Alves, C.L. Ferreira, A.F. Martins, G.A. Silva, G.D. Alves, and T.P. Paulino Local delivery of EGF-liposome mediated bone modeling in orthodontic tooth movement by increasing RANKL expression Life Sciences 85 19-20 2009 693 699
42. P.A. Harper, and R.L. Juliano Two distinct mechanisms of fibroblast adhesion Nature 12 1981 136 138
43. M. Ranson, A. Howell, S. Cheeseman, and J. Margison Liposomal drug delivery Cancer Treatment Reviews 22 1996 365 379
44. S. Siler-Marinkovic, L. Mojovic, V. Davinic, and B. Bugarski Liposomes as carriers of antimicrobial drugs Drug Development and Industrial Pharmacy 23 1997 483 488
45. K.R. Saddi, G.D. Alves, T.P. Paulino, P. Ciancaglini, and J.B. Alves Epidermal growth factor in liposomes may enhance osteoclast recruitment during tooth movement in rats Angle Orthodontist 78 4 2008 604 609
46. A.C. Allori, A.M. Sailon, and S.M. Warren Biological basis of bone formation, remodeling, and repair. Part I. Biochemical signaling molecules Tissue Engineering Part B Review 14 3 2008 259 273
47. E. Argintar, S. Edwards, and J. Delahay Bone morphogenetic proteins in orthopaedic trauma surgery Injury 42 8 2011 730 734
48. P.V. Giannoudis, and H.T. Dinopoulos BMPs: options, indications, and effectiveness Journal of Orthopaedic Trauma 24 Suppl. 1 2010 S9 S16
49. A. Nauth, P.V. Giannoudis, T.A. Einhorn, K.D. Hankenson, G.E. Friedlaender, and R. Li Growth factors: beyond bone morphogenetic proteins Journal of Orthopaedic Trauma 24 9 2010 543 546
50. J.R. Lieberman, A. Daluiski, and T.A. Einhorn The role of growth factors in the repair of bone. Biology and clinical applications Journal of Bone and Joint Surgery 84-A 6 2002 1032 1044
51. M.P. Bostrom Expression of bone morphogenetic proteins in fracture healing Clinical Orthopaedics and Related Research 355 Suppl. 1998 S116 S123
52. D.M. Kingsley The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms Genes and Development 8 2 1994 133 146
53. M.M. Sandberg, H.T. Aro, and E.I. Vuorio Gene expression during bone repair Clinical Orthopaedics and Related Research 289 1993 292 312
54. G.R. Mundy Regulation of bone formation by bone morphogenetic proteins and other growth factors Clinical Orthopaedics and Related Research 324 1996 24 28
55. A. Nauth, B. Ristevski, R. Li, and E.H. Schemitsch Growth factors and bone regeneration: how much bone can we expect? Injury 42 6 2011 574 579
56. R.M. Mendes, G.A.B. Silva, M.V. Caliari, E.E. Silva, L.O. Ladeira, and A.J. Ferreira Effects of single wall carbon nanotubes and its functionalization with sodium hyaluronate on bone repair Life Sciences 87 7-8 2010 215 222
57. Z. Lalani, M. Wong, E.M. Brey, A.G. Mikos, P.J. Duke, and M.J. Miller Spacial and temporal localization of FGF-2 and VEGF in healing tooth extraction sockets in a rabbit model Journal of Oral and Maxillofacial Surgery 63 2005 1500 1508
58. P. Yilgor, K. Tuzlakoglu, R.L. Reis, N. Hasirci, and V. Hasirci Incorporation of a sequential BMP-2/BMP-7 delivery system into chitosan-based scaffolds for bone tissue engineering Biomaterials 30 21 2009 3551 3559
59. C.A. Simmons, E. Alsberg, S. Hsiong, W.J. Kim, and D.J. Mooney Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells Bone 35 2 2004 562 569
60. Z.S. Patel, S. Young, Y. Tabata, J.A. Jansen, M.E.K. Wong, and A.G. Mikos Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model Bone 43 2008 931 940
61. G. Cardaropoli, M. Araújo, and J. Lindhe Dynamics of bone tissue formation in tooth extraction sites. An experimental study in dogs Journal of Clinical Periodontology 30 9 2003 809 818
62. K.S. Midwood, L.V. Williams, and J.E. Schwarzbauer Tissue repair and the dynamics of the extracellular matrix International Journal of Biochemistry and Cell Biology 36 6 2004 1031 1037
63. M.P. Welch, G.F. Odland, and R.A. Clark Temporal relationships of F-actin bundle formation, collagen and fibronectin matrix assembly, and fibronectin receptor expression to wound contraction Journal of Cell Biology 110 1 1990 133 145
64. F. Lin, X.D. Ren, Z. Pan, L. Macri, W.X. Zong, and M.G. Tonnesen Fibronectin growth factor-binding domains are required for fibroblast survival Journal of Investigative Dermatology 131 1 2011 84 98
65. Y.C. Shyng, H. Devlin, D. Riccardi, and P. Sloan Expression of cartilage-derived retinoic acid-sensitive protein during healing of the rat tooth-extraction socket Archives of Oral Biology 44 9 1999 751 757
66. P.J. Bouletreau, S.M. Warren, and M.T. Longaker The molecular biology of distraction osteogenesis Journal of Cranio-Maxillo-Facial Surgery 30 1 2002 1 11
67. M.E. Joyce, S. Jingushi, and M.E. Bolander Transforming growth factors-beta in the regulation of fracture repair Orthopedic Clinics of North America 21 1 1990 199 209
68. M. Lind, B. Schumacker, K. Soballe, J. Keller, F. Melsen, and C. Bunger Transforming growth factor-beta enhances fracture healing in rabbit tibae Acta Orthopaedica Scandinavica 64 5 1993 553 556
69. H.M. Nielsen, T.T. Andreassen, T. Ledet, and H. Oxlund Local injection of TGF-beta increases the strength of tibial fractures in the rat Acta Orthopaedica Scandinavica 65 1 1994 37 41
70. M.A. Critchlow, Y.S. Bland, and D.E. Ashhurst The effect of exogenous transforming growth factor beta 2 on healing fractures in the rat Acta Orthopaedica Scandinavica 65 1994 37 41
71. U.A. Gurkan, J. Gargac, and O. Akkus The sequential production profiles of growth factors and their relations to bone volume in ossifying bone marrow explants Tissue Engineering Part A 16 7 2010 2295 2306