Engineering Craniofacial Structures: Facing the Challenge

The human innate regenerative ability is known to be limited by the intensity of the insult together with the availability of progenitor cells, which may cause certain irreparable damage. It is only recently that the paradigm of tissue engineering found its way to the treatment of irreversibly affected body structures with the challenge of reconstructing the lost part. In the current review, we underline recent trials that target engineering of human craniofacial structures, mainly bone, cartilage, and teeth. We analyze the applied engineering strategies relative to the selection of cell types to lay down a specific targeted tissue, together with their association with an escorting scaffold for a particular engineered site, and discuss their necessity to be sustained by growth factors. Challenges and expectations for facial skeletal engineering are discussed in the context of future treatment.

[1]  R. Reis,et al.  Osteochondral defects: present situation and tissue engineering approaches , 2007, Journal of tissue engineering and regenerative medicine.

[2]  R Cancedda,et al.  Repair of large bone defects with the use of autologous bone marrow stromal cells. , 2001, The New England journal of medicine.

[3]  Cun-Yu Wang,et al.  Telomerase Accelerates Osteogenesis of Bone Marrow Stromal Stem Cells by Upregulation of CBFA1, Osterix, and Osteocalcin , 2003, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[4]  Kai Sun,et al.  Self-assembly of synthetic hydroxyapatite nanorods into an enamel prism-like structure. , 2005, Journal of colloid and interface science.

[5]  Michael S Detamore,et al.  A comparison of human umbilical cord matrix stem cells and temporomandibular joint condylar chondrocytes for tissue engineering temporomandibular joint condylar cartilage. , 2007, Tissue engineering.

[6]  Deepak M. Gupta,et al.  Tissue Engineering in Cleft Palate and Other Congenital Malformations , 2008, Pediatric Research.

[7]  B. Johansson,et al.  Production of extracellular matrix components in tissue-engineered blood vessels. , 2006, Tissue engineering.

[8]  J. Jansen,et al.  Effect of platelet-rich plasma on bone regeneration in dentistry: a systematic review. , 2008, Clinical oral implants research.

[9]  M. Soleimani,et al.  Sinus augmentation using human mesenchymal stem cells loaded into a beta-tricalcium phosphate/hydroxyapatite scaffold. , 2008, Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics.

[10]  S. Shi,et al.  The hidden treasure in apical papilla: the potential role in pulp/dentin regeneration and bioroot engineering. , 2008, Journal of endodontics.

[11]  DW Hutmacher,et al.  Concepts of scaffold-based tissue engineering—the rationale to use solid free-form fabrication techniques , 2007, Journal of cellular and molecular medicine.

[12]  P. Coulthard,et al.  The efficacy of various bone augmentation procedures for dental implants: a Cochrane systematic review of randomized controlled clinical trials. , 2006, The International journal of oral & maxillofacial implants.

[13]  Hyunjin Cho,et al.  Expression of Telomerase Extends Longevity and Enhances Differentiation in Human Adipose Tissue-derived Stromal Cells , 2004, Cellular Physiology and Biochemistry.

[14]  Paul T. Sharpe,et al.  Stem cells and tooth tissue engineering , 2007, Cell and Tissue Research.

[15]  R. Rutherford,et al.  Bone Regeneration in Cranial Defects Previously Treated with Radiation , 2005, The Laryngoscope.

[16]  F. Rose,et al.  Delivery systems for bone growth factors — the new players in skeletal regeneration , 2004, The Journal of pharmacy and pharmacology.

[17]  B. Sacchetti,et al.  Self-Renewing Osteoprogenitors in Bone Marrow Sinusoids Can Organize a Hematopoietic Microenvironment , 2007, Cell.

[18]  H. Wiesmann,et al.  Principles of cartilage tissue engineering in TMJ reconstruction , 2008, Head & face medicine.

[19]  J. Rubin,et al.  The Osteogenic Potential of Adipose-Derived Stem Cells for the Repair of Rabbit Calvarial Defects , 2006, Annals of plastic surgery.

[20]  P. Bianco,et al.  The use of adult stem cells in rebuilding the human face. , 2006, Journal of the American Dental Association.

[21]  M. Mastrogiacomo,et al.  Role of scaffold internal structure on in vivo bone formation in macroporous calcium phosphate bioceramics. , 2006, Biomaterials.

[22]  Peter X. Ma,et al.  Nanofibrous Scaffolds Incorporating PDGF-BB Microspheres Induce Chemokine Expression and Tissue Neogenesis In Vivo , 2008, PloS one.

[23]  T. Einhorn Clinical applications of recombinant human BMPs: early experience and future development. , 2003, The Journal of bone and joint surgery. American volume.

[24]  Zhiyong Tang,et al.  Acellular Synthesis of a Human Enamel‐like Microstructure , 2006 .

[25]  E. Tanaka,et al.  Platelet-derived growth factor enhances proliferation and matrix synthesis of temporomandibular joint disc-derived cells. , 2006, The Angle orthodontist.

[26]  D. Heath,et al.  Expression Profiling and Functional Analysis of Wnt Signaling Mechanisms in Mesenchymal Stem Cells , 2004, Stem cells.

[27]  Stan Gronthos,et al.  Investigation of multipotent postnatal stem cells from human periodontal ligament , 2004, The Lancet.

[28]  J. Fisher,et al.  Tissue engineering solutions for cleft palates. , 2007, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[29]  K. Shakesheff,et al.  The effect of mesenchymal populations and vascular endothelial growth factor delivered from biodegradable polymer scaffolds on bone formation. , 2008, Biomaterials.

[30]  M L Paine,et al.  Regulated gene expression dictates enamel structure and tooth function. , 2001, Matrix biology : journal of the International Society for Matrix Biology.

[31]  A. Rabie,et al.  Recombinant AAV-mediated VEGF gene therapy induces mandibular condylar growth , 2007, Gene Therapy.

[32]  R. Rutherford,et al.  Ex vivo gene therapy for skeletal regeneration in cranial defects compromised by postoperative radiotherapy. , 2003, Human gene therapy.

[33]  Cinzia Marchese,et al.  The clinical application of autologous bioengineered skin based on a hyaluronic acid scaffold. , 2008, Biomaterials.

[34]  I. Kerkis,et al.  Reconstruction of Large Cranial Defects in Nonimmunosuppressed Experimental Design With Human Dental Pulp Stem Cells , 2008, The Journal of craniofacial surgery.

[35]  L. Cooper,et al.  Evaluation of mesenchymal stem cells following implantation in alveolar sockets: a canine safety study. , 2005, The International journal of oral & maxillofacial implants.

[36]  T. van Eijden,et al.  Changed Morphology and Mechanical Properties of Cancellous Bone in the Mandibular Condyles of Edentate People , 2004, Journal of dental research.

[37]  Xuebin B. Yang,et al.  Human osteoprogenitor bone formation using encapsulated bone morphogenetic protein 2 in porous polymer scaffolds. , 2004, Tissue engineering.

[38]  G. Orive,et al.  Effectiveness of autologous preparation rich in growth factors for the treatment of chronic cutaneous ulcers. , 2008, Journal of biomedical materials research. Part B, Applied biomaterials.

[39]  R. M. Nerem,et al.  Tissue engineering in the USA , 1992, Medical and Biological Engineering and Computing.

[40]  R Cancedda,et al.  Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. , 2000, Journal of cell science.

[41]  Christof Niehrs,et al.  Fibroblast growth factor signaling during early vertebrate development. , 2005, Endocrine reviews.

[42]  J. Mao,et al.  Tissue-engineered Neogenesis of Human-shaped Mandibular Condyle from Rat Mesenchymal Stem Cells , 2003, Journal of dental research.

[43]  Swee Hin Teoh,et al.  Repair of calvarial defects with customised tissue-engineered bone grafts II. Evaluation of cellular efficiency and efficacy in vivo. , 2003, Tissue engineering.

[44]  R. Willemze,et al.  Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. , 2006, Blood.

[45]  F. Mcdowell Plastic surgery in the twentieth century. , 1978, Annals of plastic surgery.

[46]  M. Rudnicki,et al.  Niche regulation of muscle satellite cell self-renewal and differentiation. , 2008, Cell stem cell.

[47]  Shu Li,et al.  Osterix overexpression in mesenchymal stem cells stimulates healing of critical-sized defects in murine calvarial bone. , 2007, Tissue engineering.

[48]  I. Weissman,et al.  Wnt proteins are lipid-modified and can act as stem cell growth factors , 2003, Nature.

[49]  T. Adachi,et al.  Framework for optimal design of porous scaffold microstructure by computational simulation of bone regeneration. , 2006, Biomaterials.

[50]  W. Giannobile,et al.  Recombinant human osteogenic protein-1 (OP-1) stimulates periodontal wound healing in class III furcation defects. , 1998, Journal of periodontology.

[51]  T. Fleming,et al.  Role of alpha beta receptor heterodimer formation in beta platelet-derived growth factor (PDGF) receptor activation by PDGF-AB. , 1991, The Journal of biological chemistry.

[52]  P. Yelick,et al.  Accurately shaped tooth bud cell-derived mineralized tissue formation on silk scaffolds. , 2008, Tissue engineering. Part A.

[53]  J Tramper,et al.  The effect of PEGT/PBT scaffold architecture on oxygen gradients in tissue engineered cartilaginous constructs. , 2004, Biomaterials.

[54]  N. L'Heureux,et al.  Human tissue-engineered blood vessels for adult arterial revascularization , 2007, Nature Medicine.

[55]  A. Friedenstein,et al.  Stromal stem cells: marrow-derived osteogenic precursors. , 1988, Ciba Foundation symposium.

[56]  S. Gronthos,et al.  Comparison of human dental pulp and bone marrow stromal stem cells by cDNA microarray analysis. , 2001, Bone.

[57]  P H Krebsbach,et al.  Engineering craniofacial scaffolds. , 2005, Orthodontics & craniofacial research.

[58]  D. Mooney,et al.  Re-engineering primary epithelial cells from rhesus monkey parotid glands for use in developing an artificial salivary gland. , 2006, Tissue engineering.

[59]  S. Gronthos,et al.  Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[60]  David J Mooney,et al.  Quantitative assessment of scaffold and growth factor‐mediated repair of critically sized bone defects , 2007, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[61]  I. Thesleff,et al.  Regulation of epithelial stem cells in tooth regeneration. , 2007, Comptes rendus biologies.

[62]  I. Thesleff,et al.  Epithelial-mesenchymal signalling regulating tooth morphogenesis , 2003, Journal of Cell Science.

[63]  Y. Shimabukuro,et al.  Recombinant human basic fibroblast growth factor (bFGF) stimulates periodontal regeneration in class II furcation defects created in beagle dogs. , 2003, Journal of periodontal research.

[64]  Yilin Cao,et al.  Repair of experimental alveolar bone defects by tissue-engineered bone. , 2006, Tissue engineering.

[65]  Zhi-yong Li,et al.  Odontogenic potential of bone marrow mesenchymal stem cells. , 2007, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[66]  Paolo A. Netti,et al.  The performance of poly-ε-caprolactone scaffolds in a rabbit femur model with and without autologous stromal cells and BMP4 , 2007 .

[67]  Dietmar W Hutmacher,et al.  Assessment of bone ingrowth into porous biomaterials using MICRO-CT. , 2007, Biomaterials.

[68]  M. Shokrgozar,et al.  Culture of human gingival fibroblasts on a biodegradable scaffold and evaluation of its effect on attached gingiva: a randomized, controlled pilot study. , 2007, The Journal of Periodontology.

[69]  P. Yelick,et al.  Bioengineered Teeth from Cultured Rat Tooth Bud Cells , 2004, Journal of dental research.

[70]  Y. Nabeshima,et al.  Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. , 2007, Developmental cell.

[71]  Kirk R. Johnson,et al.  In vivo bone strain patterns in the zygomatic arch of macaques and the significance of these patterns for functional interpretations of craniofacial form. , 1997, American journal of physical anthropology.

[72]  Rodolfo Quarto,et al.  Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. , 2003, Experimental cell research.

[73]  M. Somerman,et al.  Advances in defining regulators of cementum development and periodontal regeneration. , 2007, Current topics in developmental biology.

[74]  H. V. von Recum,et al.  Endothelial stem cells and precursors for tissue engineering: cell source, differentiation, selection, and application. , 2008, Tissue engineering. Part B, Reviews.

[75]  M. Snead,et al.  Tooth developmental biology: disruptions to enamel-matrix assembly and its impact on biomineralization. , 2005, Orthodontics & craniofacial research.

[76]  Klaus Ludwig,et al.  The mechanical integrity of in vivo engineered heterotopic bone. , 2006, Biomaterials.

[77]  E. D. Rekow,et al.  Performance of degradable composite bone repair products made via three-dimensional fabrication techniques. , 2003, Journal of biomedical materials research. Part A.

[78]  M. Ferguson,et al.  Epithelial-mesenchymal interactions are required for msx 1 and msx 2 gene expression in the developing murine molar tooth. , 1993, Development.

[79]  S. Modino,et al.  Stem-cell-based Tissue Engineering of Murine Teeth , 2004, Journal of dental research.

[80]  M. McKee,et al.  Endocrine Regulation of Energy Metabolism by the Skeleton , 2007, Cell.

[81]  N. Kübler,et al.  Cell-based bone reconstruction therapies--cell sources. , 2006, The International journal of oral & maxillofacial implants.

[82]  Y. Haikel,et al.  Bone Marrow Cells Can Give Rise to Ameloblast-like Cells , 2006, Journal of dental research.

[83]  Soo-Chang Song,et al.  A thermosensitive poly(organophosphazene) hydrogel for injectable tissue-engineering applications , 2007, Journal of biomaterials science. Polymer edition.

[84]  Elaine Fuchs,et al.  Skin stem cells: rising to the surface , 2008, The Journal of cell biology.

[85]  T. Karring,et al.  New attachment formation as the result of controlled tissue regeneration. , 1984, Journal of clinical periodontology.

[86]  H. Eufinger,et al.  Growth and transplantation of a custom vascularised bone graft in a man , 2004, The Lancet.

[87]  D. Marsh,et al.  Healing of an ulnar defect using a proprietary TCP bone graft substitute, JAX, in association with autologous osteogenic cells and growth factors. , 2007, Bone.

[88]  J. Mulliken,et al.  Donor-site morbidity after harvesting rib and iliac bone. , 1984, Plastic and reconstructive surgery.

[89]  R. Cancedda,et al.  Recruitment of a host's osteoprogenitor cells using exogenous mesenchymal stem cells seeded on porous ceramic. , 2009, Tissue engineering. Part A.

[90]  M. Ueda,et al.  Alveolar cleft osteoplasty using tissue-engineered osteogenic material. , 2006, International journal of oral and maxillofacial surgery.

[91]  M. Ueda,et al.  Clinical case reports of injectable tissue-engineered bone for alveolar augmentation with simultaneous implant placement. , 2005, The International journal of periodontics & restorative dentistry.

[92]  R Shah,et al.  Craniofacial muscle engineering using a 3-dimensional phosphate glass fibre construct. , 2005, Biomaterials.

[93]  H. Ohgushi,et al.  Tissue engineering approach to the treatment of bone tumors: three cases of cultured bone grafts derived from patients' mesenchymal stem cells. , 2006, Artificial organs.

[94]  M. Ueda,et al.  Translational Research for Injectable Tissue-Engineered Bone Regeneration Using Mesenchymal Stem Cells and Platelet-Rich Plasma: From Basic Research to Clinical Case Study , 2004, Cell transplantation.

[95]  M. Urist,et al.  Bone: Formation by Autoinduction , 1965, Science.

[96]  S. Sen,et al.  Matrix Elasticity Directs Stem Cell Lineage Specification , 2006, Cell.

[97]  A. Meunier,et al.  Prolonged hypoxia concomitant with serum deprivation induces massive human mesenchymal stem cell death. , 2007, Tissue engineering.

[98]  Michael S Detamore,et al.  Tissue engineering the mandibular condyle. , 2007, Tissue engineering.

[99]  W. Butler,et al.  Dentin matrix proteins. , 1998, European journal of oral sciences.

[100]  Alexander M Seifalian,et al.  The roles of tissue engineering and vascularisation in the development of micro-vascular networks: a review. , 2005, Biomaterials.

[101]  P. Bianco,et al.  Mesenchymal stem cells: revisiting history, concepts, and assays. , 2008, Cell stem cell.

[102]  Pierre-Yves Zambelli,et al.  Repair of critical size defects in the rat cranium using ceramic-reinforced PLA scaffolds obtained by supercritical gas foaming. , 2007, Journal of biomedical materials research. Part A.

[103]  Lichun Lu,et al.  Effect of autologous bone marrow stromal cell seeding and bone morphogenetic protein-2 delivery on ectopic bone formation in a microsphere/poly(propylene fumarate) composite. , 2009, Tissue engineering. Part A.

[104]  F Peyrin,et al.  Kinetics of in vivo bone deposition by bone marrow stromal cells within a resorbable porous calcium phosphate scaffold: An X‐ray computed microtomography study , 2007, Biotechnology and bioengineering.

[105]  B. Avalos,et al.  Granulocyte colony-stimulating factor receptor mutations in severe congenital neutropenia transforming to acute myelogenous leukemia confer resistance to apoptosis and enhance cell survival. , 2000, Blood.

[106]  S. Shi,et al.  Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. , 2006, Bone.

[107]  H. Fujioka,et al.  In vitro multipotentiality and characterization of human unfractured traumatic hemarthrosis‐derived progenitor cells: A potential cell source for tissue repair , 2007, Journal of cellular physiology.

[108]  M. Ueda,et al.  A novel approach to periodontal tissue regeneration with mesenchymal stem cells and platelet-rich plasma using tissue engineering technology: A clinical case report. , 2006, The International journal of periodontics & restorative dentistry.

[109]  Miho Ogawa,et al.  The development of a bioengineered organ germ method , 2007, Nature Methods.

[110]  W. Giannobile,et al.  Periodontal tissue engineering by growth factors. , 1996, Bone.

[111]  Robert Langer,et al.  Biodegradable Polymer Scaffolds for Tissue Engineering , 1994, Bio/Technology.

[112]  L Savarino,et al.  The performance of poly-epsilon-caprolactone scaffolds in a rabbit femur model with and without autologous stromal cells and BMP4. , 2007, Biomaterials.

[113]  S. Gronthos,et al.  Comparison of Stem-cell-mediated Osteogenesis and Dentinogenesis , 2003, Journal of dental research.

[114]  K. Red-Horse,et al.  Endothelium-microenvironment interactions in the developing embryo and in the adult. , 2007, Developmental cell.

[115]  B. Sacchetti,et al.  Human maxillary tuberosity and jaw periosteum as sources of osteoprogenitor cells for tissue engineering. , 2007, Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics.

[116]  S. Hollister Porous scaffold design for tissue engineering , 2005, Nature materials.

[117]  D. Scharnweber,et al.  Evaluation of osseointegration of dental implants coated with collagen, chondroitin sulphate and BMP-4: an animal study. , 2008, International journal of oral and maxillofacial surgery.

[118]  J. Sharp,et al.  Does the Number or Quality of Pluripotent Bone Marrow Stem Cells Decrease with Age? , 2007, Clinical orthopaedics and related research.

[119]  R. Cancedda,et al.  Clonal analysis of stably transduced human epidermal stem cells in culture. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[120]  I. Martin,et al.  Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. , 1997, Endocrinology.

[121]  M. Longaker,et al.  Formation of In Vitro Murine Cleft Palate by Abrogation of Fibroblast Growth Factor Signaling , 2008, Plastic and reconstructive surgery.

[122]  Taka Nakahara,et al.  Tooth regeneration: Implications for the use of bioengineered organs in first-wave organ replacement , 2007, Human Cell.

[123]  M. Risbud,et al.  Stem cells in craniofacial and dental tissue engineering. , 2005, Orthodontics & craniofacial research.

[124]  Antonio Nanci,et al.  Ten Cate's Oral Histology: Development, Structure, and Function , 2003 .

[125]  二村 昭元,et al.  Increased proliferation of human synovial mesenchymal stem cells with autologous human serum : comparisons with bone marrow mesenchymal stem cells and with fetal bovine serum , 2008 .

[126]  Stan Gronthos,et al.  SHED: Stem cells from human exfoliated deciduous teeth , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[127]  G. Finkenzeller,et al.  In vivo engineering of a human vasculature for bone tissue engineering applications , 2008, Journal of cellular and molecular medicine.

[128]  S. Cohen,et al.  A Genetic Screen in Drosophila for Identifying Novel Components of the Hedgehog Signaling Pathway , 2005, Genetics.

[129]  M. Lewis,et al.  Myogenic precursor cells in craniofacial muscles. , 2007, Oral diseases.

[130]  Adriano Piattelli,et al.  Scaffold's surface geometry significantly affects human stem cell bone tissue engineering , 2008, Journal of cellular physiology.

[131]  L. Niklason,et al.  Small‐diameter human vessel wall engineered from bone marrow‐derived mesenchymal stem cells (hMSCs) , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[132]  C. V. van Blitterswijk,et al.  Engineering vascularised tissues in vitro. , 2008, European cells & materials.

[133]  S W Herring,et al.  Bone--special problems of the craniofacial region. , 2005, Orthodontics & craniofacial research.

[134]  William V Giannobile,et al.  Engineering of tooth-supporting structures by delivery of PDGF gene therapy vectors. , 2004, Molecular therapy : the journal of the American Society of Gene Therapy.

[135]  M. Marei,et al.  Preservation and regeneration of alveolar bone by tissue-engineered implants. , 2005, Tissue engineering.

[136]  M. Uusitupa,et al.  Does lactose intolerance predispose to low bone density? A population-based study of perimenopausal Finnish women. , 1996, Bone.

[137]  Paolo Giannoni,et al.  A tissue engineering approach to bone repair in large animal models and in clinical practice. , 2007, Biomaterials.

[138]  C James Kirkpatrick,et al.  Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillary-like structures on three-dimensional porous biomaterials. , 2007, Biomaterials.

[139]  P. Simonian,et al.  Characterization of a novel dentin matrix acidic phosphoprotein. Implications for induction of biomineralization. , 1993, The Journal of biological chemistry.

[140]  I. Sekiya,et al.  Synovial fluid-derived mesenchymal stem cells increase after intra-articular ligament injury in humans. , 2008, Rheumatology.

[141]  C. A. Dunn,et al.  BMP gene delivery for alveolar bone engineering at dental implant defects. , 2005, Molecular therapy : the journal of the American Society of Gene Therapy.

[142]  P. Edwards,et al.  Gene-enhanced tissue engineering for dental hard tissue regeneration: (2) dentin-pulp and periodontal regeneration , 2006, Head & face medicine.

[143]  A. Friedenstein,et al.  Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers , 1987, Cell and tissue kinetics.

[144]  Y. Tabata,et al.  In situ tissue engineering of periodontal tissues by seeding with periodontal ligament-derived cells. , 2004, Tissue engineering.

[145]  Andrej-Nikolai Spiess,et al.  Accelerated and safe expansion of human mesenchymal stromal cells in animal serum‐free medium for transplantation and regenerative medicine , 2007, Journal of cellular physiology.

[146]  Beatriz Garcillán,et al.  In vitro manipulation of cleft palate connective tissue: setting the bases of a proposed new treatment. , 2007, The Journal of surgical research.

[147]  V. Bousson,et al.  Induction of a barrier membrane to facilitate reconstruction of massive segmental diaphyseal bone defects: an ovine model. , 2006, Veterinary surgery : VS.

[148]  N. Gellrich,et al.  Bone formation after sinus augmentation with engineered bone. , 2007, Clinical oral implants research.

[149]  Cun-Yu Wang,et al.  Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression , 2002, Nature Biotechnology.

[150]  M. Casati,et al.  Physiological features of periodontal regeneration and approaches for periodontal tissue engineering utilizing periodontal ligament cells. , 2007, Journal of bioscience and bioengineering.

[151]  Henning Schliephake,et al.  Mandibular bone repair by implantation of rhBMP-2 in a slow release carrier of polylactic acid--an experimental study in rats. , 2008, Biomaterials.

[152]  Antonios G Mikos,et al.  Microcomputed tomography characterization of neovascularization in bone tissue engineering applications. , 2008, Tissue engineering. Part B, Reviews.

[153]  M. Ueda,et al.  Tissue-engineered injectable bone regeneration for osseointegrated dental implants. , 2004, Clinical oral implants research.

[154]  Vasif Hasirci,et al.  Sequential growth factor delivery from complexed microspheres for bone tissue engineering. , 2008, Biomaterials.

[155]  T. Ichisaka,et al.  Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors , 2007, Cell.

[156]  Stefan Wolfart,et al.  Man as living bioreactor: fate of an exogenously prepared customized tissue-engineered mandible. , 2006, Biomaterials.

[157]  M. Sefton,et al.  Tissue engineering. , 1998, Journal of cutaneous medicine and surgery.

[158]  N. Ferrara,et al.  The Role of Vascular Endothelial Growth Factor in Angiogenesis , 2002, Acta Haematologica.

[159]  P H Krebsbach,et al.  Craniofacial Tissue Engineering by Stem Cells , 2006, Journal of dental research.

[160]  Mario Calvitti,et al.  Multipotent Mesenchymal Stem Cells with Immunosuppressive Activity Can Be Easily Isolated from Dental Pulp , 2005, Transplantation.

[161]  Pamela C Yelick,et al.  Tissue-engineered hybrid tooth and bone. , 2005, Tissue engineering.

[162]  T. Komori,et al.  Clinical and histopathological analysis of healing process of intraoral reconstruction with ex vivo produced oral mucosa equivalent. , 2007, The Kobe journal of medical sciences.

[163]  Q. Jin,et al.  Current concepts in periodontal bioengineering. , 2005, Orthodontics & craniofacial research.

[164]  K. Benirschke,et al.  Aberrant Pax1 and Pax9 expression in Jarcho‐Levin syndrome: Report of two Caucasian siblings and literature review , 2003, American journal of medical genetics. Part A.

[165]  Jeroen Rouwkema,et al.  Endothelial cells assemble into a 3-dimensional prevascular network in a bone tissue engineering construct. , 2006, Tissue engineering.

[166]  S. Gronthos,et al.  Bone marrow-derived mesenchymal stem cells for regenerative medicine in craniofacial region. , 2006, Oral diseases.

[167]  P. Sheridan,et al.  Is platelet-rich plasma the perfect enhancement factor? A current review. , 2003, The International journal of oral & maxillofacial implants.

[168]  M. Almeida,et al.  Oxidative Stress Antagonizes Wnt Signaling in Osteoblast Precursors by Diverting β-Catenin from T Cell Factor- to Forkhead Box O-mediated Transcription* , 2007, Journal of Biological Chemistry.

[169]  Masayuki Yamato,et al.  Application of periodontal ligament cell sheet for periodontal regeneration: a pilot study in beagle dogs. , 2005, Journal of periodontal research.

[170]  Takashi Nakamura,et al.  Transcription factor ERG and joint and articular cartilage formation during mouse limb and spine skeletogenesis. , 2007, Developmental biology.

[171]  G. Ambrosano,et al.  A double-blind randomized clinical evaluation of enamel matrix derivative proteins for the treatment of proximal class-II furcation involvements. , 2008, Journal of clinical periodontology.

[172]  C. McCulloch,et al.  Transplantation of labeled periodontal ligament cells promotes regeneration of alveolar bone , 2001, The Anatomical record.

[173]  S. Gronthos,et al.  Perivascular Niche of Postnatal Mesenchymal Stem Cells in Human Bone Marrow and Dental Pulp , 2003, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[174]  Benjamin Wu,et al.  A study of the role of nell-1 gene modified goat bone marrow stromal cells in promoting new bone formation. , 2007, Molecular therapy : the journal of the American Society of Gene Therapy.

[175]  K. Koval,et al.  Bone grafts and bone graft substitutes in orthopaedic trauma surgery. A critical analysis. , 2007, The Journal of bone and joint surgery. American volume.

[176]  C. Verfaillie,et al.  Self-renewal and differentiation capacity of young and aged stem cells. , 2008, Experimental cell research.

[177]  G. Dini,et al.  Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study , 2008, The Lancet.

[178]  G. Reilly,et al.  BMP Responsiveness in Human Mesenchymal Stem Cells , 2003, Connective tissue research.

[179]  Jack C. Yu,et al.  Age‐Related Changes in the Osteogenic Differentiation Potential of Mouse Bone Marrow Stromal Cells , 2008, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[180]  M. A. Silva,et al.  Growth and phenotypic expression of human endothelial cells cultured on a glass-reinforced hydroxyapatite , 2009, Journal of materials science. Materials in medicine.

[181]  Cun-Yu Wang,et al.  Mesenchymal Stem Cell-Mediated Functional Tooth Regeneration in Swine , 2006, PloS one.

[182]  Min Zhao,et al.  Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-γ and PTEN , 2006, Nature.

[183]  M. Somerman,et al.  Cementoblast delivery for periodontal tissue engineering. , 2004, Journal of periodontology.

[184]  H. Sagara,et al.  The sequential seeding of epithelial and mesenchymal cells for tissue-engineered tooth regeneration. , 2007, Biomaterials.

[185]  Pol Maria Rommens,et al.  The effect of human osteoblasts on proliferation and neo-vessel formation of human umbilical vein endothelial cells in a long-term 3D co-culture on polyurethane scaffolds. , 2008, Biomaterials.

[186]  C. Colnot,et al.  Indian hedgehog synchronizes skeletal angiogenesis and perichondrial maturation with cartilage development , 2005, Development.

[187]  M. Mastrogiacomo,et al.  Platelet lysate favours in vitro expansion of human bone marrow stromal cells for bone and cartilage engineering , 2008, Journal of tissue engineering and regenerative medicine.