Craniofacial Tissue Engineering by Stem Cells

Craniofacial tissue engineering promises the regeneration or de novo formation of dental, oral, and craniofacial structures lost to congenital anomalies, trauma, and diseases. Virtually all craniofacial structures are derivatives of mesenchymal cells. Mesenchymal stem cells are the offspring of mesenchymal cells following asymmetrical division, and reside in various craniofacial structures in the adult. Cells with characteristics of adult stem cells have been isolated from the dental pulp, the deciduous tooth, and the periodontium. Several craniofacial structures—such as the mandibular condyle, calvarial bone, cranial suture, and subcutaneous adipose tissue—have been engineered from mesenchymal stem cells, growth factor, and/or gene therapy approaches. As a departure from the reliance of current clinical practice on durable materials such as amalgam, composites, and metallic alloys, biological therapies utilize mesenchymal stem cells, delivered or internally recruited, to generate craniofacial structures in temporary scaffolding biomaterials. Craniofacial tissue engineering is likely to be realized in the foreseeable future, and represents an opportunity that dentistry cannot afford to miss.

[1]  Dietmar W Hutmacher,et al.  Scaffold-based tissue engineering: rationale for computer-aided design and solid free-form fabrication systems. , 2004, Trends in biotechnology.

[2]  Beat Hammer,et al.  In vivo efficacy of bone-marrow-coated polycaprolactone scaffolds for the reconstruction of orbital defects in the pig. , 2003, Journal of biomedical materials research. Part B, Applied biomaterials.

[3]  D J Mooney,et al.  Craniofacial tissue engineering. , 2001, Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists.

[4]  J. Cirelli,et al.  Regeneration of Class III furcation defects with basic fibroblast growth factor (b-FGF) associated with GTR. A descriptive and histometric study in dogs. , 2000, Journal of periodontology.

[5]  A. McMahon,et al.  Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. , 2001, Development.

[6]  S. Creuzet,et al.  Patterning of the hyoid cartilage depends upon signals arising from the ventral foregut endoderm , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[7]  J. Gimble,et al.  Human adipose-derived adult stem cells produce osteoid in vivo. , 2004, Tissue engineering.

[8]  W. Giannobile,et al.  Gene Transfer and Expression of Platelet-derived Growth Factors Modulate Periodontal Cellular Activity , 2001, Journal of dental research.

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

[10]  S J Hollister,et al.  Manufacturing and Characterization of 3‐D Hydroxyapatite Bone Tissue Engineering Scaffolds , 2002, Annals of the New York Academy of Sciences.

[11]  Adel Alhadlaq,et al.  Adult Stem Cell Driven Genesis of Human-Shaped Articular Condyle , 2004, Annals of Biomedical Engineering.

[12]  T. Albert,et al.  Donor Site Morbidity After Anterior Iliac Crest Bone Harvest for Single-Level Anterior Cervical Discectomy and Fusion , 2003, Spine.

[13]  D. Prockop,et al.  Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation. , 2005, Experimental cell research.

[14]  L. Donahue,et al.  Histomorphometric studies show that bone formation and bone mineral apposition rates are greater in C3H/HeJ (high-density) than C57BL/6J (low-density) mice during growth. , 1999, Bone.

[15]  Hung Li,et al.  Isolation and Characterization of Size‐Sieved Stem Cells from Human Bone Marrow , 2002, Stem cells.

[16]  Taylor Murray,et al.  Cancer Statistics, 2001 , 2001, CA: a cancer journal for clinicians.

[17]  J. Wozney,et al.  Periodontal repair in dogs: recombinant human bone morphogenetic protein-2 significantly enhances periodontal regeneration. , 1995, Journal of periodontology.

[18]  Rik Huiskes,et al.  Comparison of biophysical stimuli for mechano-regulation of tissue differentiation during fracture healing. , 2006, Journal of biomechanics.

[19]  Min Zhu,et al.  Human adipose tissue is a source of multipotent stem cells. , 2002, Molecular biology of the cell.

[20]  S. Shabahang,et al.  Evaluation of the long-term effect of function on rhBMP-2 regenerated hemimandibulectomy defects. , 1999, The British journal of oral & maxillofacial surgery.

[21]  William V Giannobile,et al.  Adenoviral gene transfer of PDGF downregulates gas gene product PDGFalphaR and prolongs ERK and Akt/PKB activation. , 2002, American journal of physiology. Cell physiology.

[22]  R. Rutherford,et al.  Gene therapy-directed osteogenesis: BMP-7-transduced human fibroblasts form bone in vivo. , 2000, Human gene therapy.

[23]  P. Okunieff,et al.  In vivo radioprotective effects of angiogenic growth factors on the small bowel of C3H mice. , 1998, Radiation research.

[24]  J. Compston,et al.  Estrogen receptors alpha and beta are differentially expressed in developing human bone. , 2001, The Journal of clinical endocrinology and metabolism.

[25]  C. Anderson,et al.  Bone-remodeling rates of the Beagle: a comparison between different sites on the same rib. , 1978, American journal of veterinary research.

[26]  Dennis R. Carter,et al.  Mechanobiology of Skeletal Regeneration , 1998, Clinical orthopaedics and related research.

[27]  H. Pieterman,et al.  Porous Polymethylmethacrylate as Bone Substitute in the Craniofacial Area , 2003, The Journal of craniofacial surgery.

[28]  J. Vacanti,et al.  Tissue engineering : Frontiers in biotechnology , 1993 .

[29]  S. Gerson,et al.  G156A MGMT-transduced human mesenchymal stem cells can be selectively enriched by O6-benzylguanine and BCNU. , 2001, Journal of hematotherapy & stem cell research.

[30]  J. Fiorellini,et al.  A feasibility study evaluating rhBMP-2/absorbable collagen sponge device for local alveolar ridge preservation or augmentation. , 1997, The International journal of periodontics & restorative dentistry.

[31]  J. Fiorellini,et al.  A phase I/II clinical trial to evaluate a combination of recombinant human platelet-derived growth factor-BB and recombinant human insulin-like growth factor-I in patients with periodontal disease. , 1997, Journal of periodontology.

[32]  J. Hock,et al.  Autoradiographic study of the effect of 1,25-dihydroxyvitamin D3 on bone matrix synthesis in vitamin D replete rats , 1982, Calcified Tissue International.

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

[34]  G. Rasperini,et al.  Comparison of treatments of infrabony defects with enamel matrix derivative, guided tissue regeneration with a nonresorbable membrane and Widman modified flap. A pilot study. , 2000, Journal of clinical periodontology.

[35]  David M. Bodine,et al.  Bone marrow cells regenerate infarcted myocardium , 2001, Nature.

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

[37]  N. L. Le Douarin,et al.  Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. , 1975, Journal of embryology and experimental morphology.

[38]  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.

[39]  A. Mikos,et al.  Angiogenesis with biomaterial-based drug- and cell-delivery systems , 2004, Journal of biomaterials science. Polymer edition.

[40]  Esmaiel Jabbari,et al.  Quantitative analysis of interconnectivity of porous biodegradable scaffolds with micro-computed tomography. , 2004, Journal of biomedical materials research. Part A.

[41]  J. Myers,et al.  Extracapsular spread , 2001, Cancer.

[42]  A. McMahon,et al.  Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. , 2000, Development.

[43]  H. Broxmeyer,et al.  Modulation of Hematopoietic Stem Cell Homing and Engraftment by CD26 , 2004, Science.

[44]  M S Reddy,et al.  The effects of short-term application of a combination of platelet-derived and insulin-like growth factors on periodontal wound healing. , 1991, Journal of periodontology.

[45]  Prosper Benhaim,et al.  Bone induction by BMP‐2 transduced stem cells derived from human fat , 2003, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[46]  P. Manson,et al.  Craniofacial Distraction Osteogenesis: A Review of 3278 Cases , 2001, Plastic and reconstructive surgery.

[47]  A. Yamaguchi,et al.  Radiation retards muscle differentiation but does not affect osteoblastic differentiation induced by bone morphogenetic protein-2 in C2C12 myoblasts. , 2000, International journal of radiation biology.

[48]  S. Gronthos,et al.  Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow , 2003, Journal of Cell Science.

[49]  Bobbi K Lewis,et al.  In vivo trafficking and targeted delivery of magnetically labeled stem cells. , 2004, Human gene therapy.

[50]  J. Wataha,et al.  Cloned 3T6 cell line from CD-1 mouse fetal molar dental papillae. , 1998, Connective tissue research.

[51]  N M Le Douarin,et al.  The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. , 1993, Development.

[52]  B. Epker,et al.  A histological study of remodeling at the periosteal, haversian canal, cortical endosteal, and trabecular endosteal surfaces in human rib , 1965, The Anatomical record.

[53]  R. Taichman Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. , 2005, Blood.

[54]  R. Loukota The effect of pre-operative perioral skin preparation with aqueous povidone-iodine on the incidence of infection after third molar removal. , 1991, The British journal of oral & maxillofacial surgery.

[55]  Paul Emery,et al.  Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. , 2002, Arthritis and rheumatism.

[56]  G. Heden,et al.  Enamel matrix derivative (EMDOGAIN) in the treatment of intrabony periodontal defects. , 1997, Journal of clinical periodontology.

[57]  J. Nicholson Glass-ionomers in medicine and dentistry , 1998, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[58]  Gordana Vunjak-Novakovic,et al.  Silk implants for the healing of critical size bone defects. , 2005, Bone.

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

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

[61]  Freddie H Fu,et al.  Structural and functional healing of critical‐size segmental bone defects by transduced muscle‐derived cells expressing BMP4 , 2004, The journal of gene medicine.

[62]  Min Zhu,et al.  Comparison of Multi-Lineage Cells from Human Adipose Tissue and Bone Marrow , 2003, Cells Tissues Organs.

[63]  S. Lynch,et al.  Periodontal regeneration in human Class II furcations using purified recombinant human platelet-derived growth factor-BB (rhPDGF-BB) with bone allograft. , 2003, The International journal of periodontics & restorative dentistry.

[64]  B. Baum,et al.  The impact of gene therapy on dentistry: a revisiting after six years. , 2002, Journal of the American Dental Association.

[65]  P. Conget,et al.  Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells , 1999, Journal of cellular physiology.

[66]  S. Lynch,et al.  Evaluation of periodontal regeneration following grafting intrabony defects with bio-oss collagen: a human histologic report. , 2003, The International journal of periodontics & restorative dentistry.

[67]  J. Dragoo,et al.  Tissue-Engineered Bone from BMP-2–Transduced Stem Cells Derived from Human Fat , 2005, Plastic and reconstructive surgery.

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

[69]  C. Stohler Muscle-related temporomandibular disorders. , 1999, Journal of orofacial pain.

[70]  B H Grayson,et al.  Lengthening the human mandible by gradual distraction. , 1992, Plastic and reconstructive surgery.

[71]  M. Boudeulle,et al.  Odontoblast Differentiation of Human Dental Pulp Cells in Explant Cultures , 2000, Calcified Tissue International.

[72]  J. Fiorellini,et al.  Evaluation of recombinant human bone morphogenetic protein-2 in oral applications including the use of endosseous implants: 3-year results of a pilot study in humans. , 2000, Journal of periodontology.

[73]  H. Lorenz,et al.  Multilineage cells from human adipose tissue: implications for cell-based therapies. , 2001, Tissue engineering.

[74]  M. Tang,et al.  Engineered adipose tissue from human mesenchymal stem cells maintains predefined shape and dimension: implications in soft tissue augmentation and reconstruction. , 2005, Tissue engineering.

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

[76]  William V Giannobile,et al.  Effect of sustained gene delivery of platelet-derived growth factor or its antagonist (PDGF-1308) on tissue-engineered cementum. , 2004, Journal of periodontology.

[77]  F. Barry,et al.  Mesenchymal stem cells: clinical applications and biological characterization. , 2004, The international journal of biochemistry & cell biology.

[78]  Freddie H. Fu,et al.  Ex vivo gene therapy-induced endochondral bone formation: comparison of muscle-derived stem cells and different subpopulations of primary muscle-derived cells. , 2004, Bone.

[79]  S. Iseki,et al.  Tissue origins and interactions in the mammalian skull vault. , 2002, Developmental biology.

[80]  J. Okeson Orofacial pain : guidelines for assessment, diagnosis, and management , 1996 .

[81]  P. Boyne Animal studies of application of rhBMP-2 in maxillofacial reconstruction. , 1996, Bone.

[82]  J. Engh,et al.  The Use of Bone Morphogenetic Protein Gene Therapy in Craniofacial Bone Repair , 2000, The Journal of craniofacial surgery.

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

[84]  William V Giannobile,et al.  Platelet-derived growth factor stimulates bone fill and rate of attachment level gain: results of a large multicenter randomized controlled trial. , 2005, Journal of periodontology.

[85]  S. Caputi,et al.  Morphological and Cytofluorimetric Analysis of Adult Mesenchymal Stem Cells Expanded Ex Vivo from Periodontal Ligament , 2005, International journal of immunopathology and pharmacology.

[86]  S. Miller,et al.  Calcium absorption and osseous organ-, tissue-, and envelope-specific changes following ovariectomy in rats. , 1991, Bone.

[87]  Stephen E. Feinberg,et al.  An image-based approach for designing and manufacturing craniofacial scaffolds. , 2000, International journal of oral and maxillofacial surgery.

[88]  Michael S. Detamore,et al.  Evaluation of Three Growth Factors for TMJ Disc Tissue Engineering , 2005, Annals of Biomedical Engineering.

[89]  P Okunieff,et al.  Radiation-induced changes in bone perfusion and angiogenesis. , 1998, International journal of radiation oncology, biology, physics.

[90]  S. Gronthos,et al.  Skeletal stem cells in regenerative medicine. , 2005, Current topics in developmental biology.

[91]  S. Mckercher,et al.  Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. , 2000, Science.

[92]  M. Somerman,et al.  Growth and amelogenin-like factors in periodontal wound healing. A systematic review. , 2003, Annals of periodontology.

[93]  A. Reddi,et al.  Radiation-induced impairment of bone healing can be overcome by recombinant human bone morphogenetic protein-2. , 1998, The Journal of craniofacial surgery.

[94]  D. Hu,et al.  Common Molecular Pathways in Skeletal Morphogenesis and Repair , 1998, Annals of the New York Academy of Sciences.

[95]  J. Fiorellini,et al.  Randomized study evaluating recombinant human bone morphogenetic protein-2 for extraction socket augmentation. , 2005, Journal of periodontology.

[96]  D. Noden Interactions and fates of avian craniofacial mesenchyme. , 1988, Development.

[97]  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.

[98]  H. Broxmeyer,et al.  Stem cells: shibboleths of development. , 2004, Stem cells and development.

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

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

[101]  J. Mao Stem‐cell‐driven regeneration of synovial joints , 2005, Biology of the cell.

[102]  R. Weber Wound Infection in Head and Neck Surgery: Implications for Perioperative Antibiotic Treatment , 1997, Ear, nose, & throat journal.

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

[104]  Kyriacos A Athanasiou,et al.  Seeding techniques and scaffolding choice for tissue engineering of the temporomandibular joint disk. , 2004, Tissue engineering.

[105]  M. Nunn,et al.  Evaluation of the safety and efficacy of periodontal applications of a living tissue-engineered human fibroblast-derived dermal substitute. I. Comparison to the gingival autograft: a randomized controlled pilot study. , 2005, Journal of periodontology.

[106]  R. Rutherford,et al.  Platelet-derived and insulin-like growth factors stimulate regeneration of periodontal attachment in monkeys. , 1992, Journal of periodontal research.

[107]  A. Friedenstein,et al.  THE DEVELOPMENT OF FIBROBLAST COLONIES IN MONOLAYER CULTURES OF GUINEA‐PIG BONE MARROW AND SPLEEN CELLS , 1970, Cell and tissue kinetics.

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

[109]  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.

[110]  A Daluiski,et al.  The effect of regional gene therapy with bone morphogenetic protein-2-producing bone-marrow cells on the repair of segmental femoral defects in rats. , 1999, The Journal of bone and joint surgery. American volume.

[111]  I. About,et al.  Human dentin production in vitro. , 2000, Experimental cell research.

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

[113]  P. Logan,et al.  Radiation-induced changes in bone. , 1998, Radiographics : a review publication of the Radiological Society of North America, Inc.

[114]  R. Rutherford,et al.  Gene therapy of bone morphogenetic protein for periodontal tissue engineering. , 2003, Journal of periodontology.

[115]  Masayuki Yamato,et al.  Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. , 2005, Tissue engineering.

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

[117]  J. Hollinger,et al.  Tissue Engineering of Bone in the Craniofacial Complex , 1999, Annals of the New York Academy of Sciences.

[118]  J. Mao,et al.  Tissue-engineered Rabbit Cranial Suture from Autologous Fibroblasts and BMP2 , 2004, Journal of dental research.

[119]  D. Jones,et al.  Biochemical signal transduction of mechanical strain in osteoblast-like cells. , 1991, Biomaterials.

[120]  Q. Jin,et al.  Platelet-derived growth factor gene delivery stimulates ex vivo gingival repair. , 2003, Tissue engineering.

[121]  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.

[122]  N. Lang,et al.  Enamel matrix proteins in the regenerative therapy of deep intrabony defects. , 2002, Journal of clinical periodontology.

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

[124]  Jeremy J Mao,et al.  Mesenchymal stem cells: isolation and therapeutics. , 2004, Stem cells and development.

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

[126]  H. Blau,et al.  From marrow to brain: expression of neuronal phenotypes in adult mice. , 2000, Science.

[127]  J. Mao,et al.  Stem cell‐based composite tissue constructs for regenerative medicine , 2005, Biotechnology and bioengineering.

[128]  D. Mooney,et al.  Hydrogels for tissue engineering: scaffold design variables and applications. , 2003, Biomaterials.

[129]  S. Creuzet,et al.  Neural crest cell plasticity and its limits , 2004, Development.

[130]  J. Mao,et al.  Sustained release of TGFbeta3 from PLGA microspheres and its effect on early osteogenic differentiation of human mesenchymal stem cells. , 2006, Tissue engineering.

[131]  Tatsuo Nakamura,et al.  Novel approach to regeneration of periodontal tissues based on in situ tissue engineering: effects of controlled release of basic fibroblast growth factor from a sandwich membrane. , 2003, Tissue engineering.

[132]  Y. Shimabukuro,et al.  Periodontal Regeneration by Fgf-2 (bfgf) in Primate Models on Behalf Of: International and American Associations for Dental Research Periodontal Regeneration by Fgf-2 (bfgf) in Primate Models , 2001 .

[133]  Christopher H Contag,et al.  Adipose-derived adult stromal cells heal critical-size mouse calvarial defects , 2004, Nature Biotechnology.

[134]  M. Burnett,et al.  Local Delivery of Marrow-Derived Stromal Cells Augments Collateral Perfusion Through Paracrine Mechanisms , 2004, Circulation.

[135]  Matthew R Allen,et al.  Periosteum: biology, regulation, and response to osteoporosis therapies. , 2004, Bone.

[136]  U. Wikesjö,et al.  Tissue engineering with recombinant human bone morphogenetic protein-2 for alveolar augmentation and oral implant osseointegration: experimental observations and clinical perspectives. , 2005, Clinical implant dentistry and related research.

[137]  D. K. Rah Art of replacing craniofacial bone defects. , 2000, Yonsei medical journal.

[138]  L. Gilula,et al.  Repair of calvarial defects with flap tissue: role of bone morphogenetic proteins and competent responding tissues. , 1996, Plastic and reconstructive surgery.

[139]  Jeremy J. Mao,et al.  Sustained Release of TGFβ3 from PLGA Microspheres and Its Effect on Early Osteogenic Differentiation of Human Mesenchymal Stem Cells , 2006 .

[140]  R. Midura,et al.  Parathyroid Hormone Rapidly Stimulates Hyaluronan Synthesis by Periosteal Osteoblasts in the Tibial Diaphysis of the Growing Rat* , 2003, Journal of Biological Chemistry.

[141]  V. Ritsilä,et al.  Healing of Membranous and Long Bone Defects , 1979 .

[142]  P. Robbins,et al.  Genetic enhancement of fracture repair: healing of an experimental segmental defect by adenoviral transfer of the BMP-2 gene , 2000, Gene Therapy.

[143]  S. Gerson,et al.  Human mesenchymal stem cells provide stromal support for efficient CD34+ transduction. , 1999, Journal of hematotherapy & stem cell research.

[144]  I. Thesleff,et al.  Stem Cells and Tissue Engineering: Prospects for Regenerating Tissues in Dental Practice , 2003, Medical Principles and Practice.

[145]  G. Reilly,et al.  Borate Glass Supports the In Vitro Osteogenic Differentiation of Human Mesenchymal Stem Cells , 2005 .

[146]  Anthony Atala,et al.  Tissue engineering, stem cells and cloning: current concepts and changing trends , 2005, Expert opinion on biological therapy.

[147]  J. Laser,et al.  Biological Alchemy: Engineering Bone and Fat From Fat-Derived Stem Cells , 2003, Annals of plastic surgery.

[148]  S. Hollister,et al.  Optimal design and fabrication of scaffolds to mimic tissue properties and satisfy biological constraints. , 2002, Biomaterials.

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

[150]  Jeremy J Mao,et al.  Tissue-engineered osteochondral constructs in the shape of an articular condyle. , 2005, The Journal of bone and joint surgery. American volume.

[151]  Trevor Williams,et al.  Wnt1-Cre-mediated deletion of AP-2alpha causes multiple neural crest-related defects. , 2004, Developmental biology.

[152]  I. About,et al.  Restorative pulpal and repair responses. , 2000, Journal of the American Dental Association.

[153]  G. Sukhikh,et al.  Mesenchymal Stem Cells , 2002, Bulletin of Experimental Biology and Medicine.

[154]  F. Unda,et al.  Dissection of the odontoblast differentiation process in vitro by a combination of FGF1, FGF2, and TGFβ1 , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[155]  Stephen E. Feinberg,et al.  Image-Based Biomimetic Approach to Reconstruction of the Temporomandibular Joint , 2001, Cells Tissues Organs.

[156]  J. Helms,et al.  Head, shoulders, knees and toes , 2020 .

[157]  S. Gronthos,et al.  The efficacy of mesenchymal stem cells to regenerate and repair dental structures. , 2005, Orthodontics & craniofacial research.

[158]  E. Halpern,et al.  Tolerance of autologous and allogeneic bone grafts to therapeutic radiation in humans. , 1999, International journal of radiation oncology, biology, physics.

[159]  J. Taboas,et al.  Skeletal homeostasis in tissue‐engineered bone , 2003, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

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

[161]  O. Zetterström,et al.  Clinical safety of enamel matrix derivative (EMDOGAIN) in the treatment of periodontal defects. , 1997, Journal of clinical periodontology.

[162]  R. Yukna,et al.  Thirty-six month follow-up of 25 patients treated with combination anorganic bovine-derived hydroxyapatite matrix (ABM)/cell-binding peptide (P-15) bone replacement grafts in human infrabony defects. I. Clinical findings. , 2002, Journal of periodontology.

[163]  M. Kyba Genesis of Hematopoietic Stem Cells In Vitro and In Vivo: New Insights into Developmental Maturation , 2005, International journal of hematology.

[164]  R. Yukna,et al.  Multi-center clinical comparison of combination anorganic bovine-derived hydroxyapatite matrix (ABM)/cell binding peptide (P-15) and ABM in human periodontal osseous defects. 6-month results. , 2000, Journal of periodontology.

[165]  E. Rodríguez‐Merchán,et al.  Nonunion: general principles and experimental data. , 2004, Clinical orthopaedics and related research.

[166]  R. Marx,et al.  A feasibility study evaluating rhBMP-2/absorbable collagen sponge for maxillary sinus floor augmentation. , 1997, The International journal of periodontics & restorative dentistry.

[167]  Margam Chandrasekaran,et al.  Rapid prototyping in tissue engineering: challenges and potential. , 2004, Trends in biotechnology.

[168]  P. Frenette,et al.  Enforced fucosylation of neonatal CD34+ cells generates selectin ligands that enhance the initial interactions with microvessels but not homing to bone marrow. , 2005, Blood.

[169]  R. Donoff,et al.  Healing of bony defects in the irradiated and unirradiated rat mandible. , 1992, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[170]  A. Kubar,et al.  Healing of artificial fenestration defects by seeding of fibroblast-like cells derived from regenerated periodontal ligament in a dog: a preliminary study. , 2003, Tissue engineering.

[171]  D. Marchac Split-rib grafts in craniofacial surgery. , 1982, Plastic and Reconstructive Surgery.

[172]  M. Somerman,et al.  Noggin Gene Delivery Inhibits Cementoblast-Induced Mineralization , 2004, Connective tissue research.

[173]  D. Callender Antibiotic prophylaxis in head and neck oncologic surgery: the role of gram-negative coverage. , 1999, International journal of antimicrobial agents.

[174]  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.

[175]  A. Jödicke,et al.  Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. , 2004, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

[176]  J. Mao,et al.  Adipose Tissue Engineering from Human Adult Stem Cells: Clinical Implications in Plastic and Reconstructive Surgery , 2007, Plastic and reconstructive surgery.

[177]  W. Mars,et al.  Bone marrow as a potential source of hepatic oval cells. , 1999, Science.

[178]  G. Finerman,et al.  Regional gene therapy with a BMP‐2‐producing murine stromal cell line induces heterotopic and orthotopic bone formation in rodents , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[179]  J. Wozney,et al.  Bone formation and osseointegration stimulated by rhBMP-2 following subantral augmentation procedures in nonhuman primates. , 1997, The International journal of oral & maxillofacial implants.

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

[181]  K. Moriyama,et al.  MC3T3-E1-conditioned medium-induced mineralization by clonal rat dental pulp cells. , 2001, Matrix biology : journal of the International Society for Matrix Biology.

[182]  Ayech Benjeddou,et al.  A Piezoelectric Mixed Variational Theorem for Smart Multilayered Composites , 2005 .

[183]  A. Reddi,et al.  The application of bone morphogenetic proteins to dental tissue engineering , 2003, Nature Biotechnology.

[184]  V. Ritsilä,et al.  Healing of membranous and long bone defects. An experimental study in growing rabbits. , 1979, Scandinavian journal of plastic and reconstructive surgery.

[185]  I. Taylor Discussion: Lengthening the Human Mandible by Gradual Distraction by Joseph G. McCarthy, M.D., Jonathan Schreiber, M.D., Nolan Karp, M.D., Charles H. Thorne, M.D., and Barry H. Grayson, D.M.D. , 1992 .

[186]  S. Lynch,et al.  Comparison of canine and non-human primate animal models for periodontal regenerative therapy: results following a single administration of PDGF/IGF-I. , 1994, Journal of periodontology.

[187]  M. Somerman,et al.  Cementum engineering with three-dimensional polymer scaffolds. , 2003, Journal of biomedical materials research. Part A.

[188]  L. Peters,et al.  Is it time for a new formalism to categorize normal tissue radiation injury? , 2001, International journal of radiation oncology, biology, physics.

[189]  C. Hall,et al.  Split-thickness bone grafts in complex craniofacial reconstructions. , 1992, Pediatric neurosurgery.

[190]  D. Rosenthal,et al.  Osteoinduction using bone morphogenic protein in irradiated tissue. , 1998, Archives of otolaryngology--head & neck surgery.

[191]  Jeremy J. Mao,et al.  Calvarial development: cells and mechanics , 2005 .

[192]  N. Dubrawsky Cancer statistics , 1989, CA: a cancer journal for clinicians.

[193]  D. M. Spolidorio,et al.  Influence of sample type and collection method on Streptococcus mutans and Lactobacillus spp. counts in the oral cavity. , 2005, Archives of oral biology.

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

[195]  Farshid Guilak,et al.  Differentiation potential of adipose derived adult stem (ADAS) cells. , 2003, Current topics in developmental biology.

[196]  J. Compston,et al.  Estrogen Receptors α and β Are Differentially Expressed in Developing Human Bone1 , 2001 .

[197]  J. Gunsolley,et al.  The efficacy of bone replacement grafts in the treatment of periodontal osseous defects. A systematic review. , 2003, Annals of periodontology.

[198]  Christine Vincent,et al.  Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. , 2002, Development.

[199]  M. Pittenger,et al.  Multilineage potential of adult human mesenchymal stem cells. , 1999, Science.

[200]  T. Hunt,et al.  Bone marrow stem cells contribute to healing of the kidney. , 2003, Journal of the American Society of Nephrology : JASN.

[201]  K. G. Murphy,et al.  Guided tissue regeneration for the treatment of periodontal intrabony and furcation defects. A systematic review. , 2003, Annals of periodontology.

[202]  S. Shenaq Reconstruction of complex cranial and carniofacial defects utilizing iliac crest‐internal oblique microsurgical free flap , 1988, Microsurgery.