Adult stem cells in tissue engineering

Tissue engineering is a rapidly evolving field of research that has yet to fulfil its promise in the translation and potential application of adult stem cells in clinical practice. Recently, it has become apparent that specific adult stem cells are capable of transdifferentiation. The successful application of adult stem cells is thought to be central in creating truly biomimetic tissue. Although still most widely utilized, research suggests that in the future, bone marrow-derived stem cells may no longer be considered the most suitable candidates for use in tissue engineering. Independent studies have successfully engineered a range of tissues in vitro and in vivo using hair follicle- and adipose-derived stem cells. Owing to their potency, relative abundance and noninvasive extraction, these populations may be the most promising studied to date. This review aims to discuss these candidate adult stem cell populations in an attempt to assess the most promising avenues of research.

[1]  A I Caplan,et al.  In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. , 1998, Experimental cell research.

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

[3]  Wen Xu,et al.  Characterization of a new tissue-engineered human skin equivalent with hair , 1999, In Vitro Cellular & Developmental Biology - Animal.

[4]  D. Mooney,et al.  Hydrogels for tissue engineering. , 2001, Chemical Reviews.

[5]  M. Aschermann,et al.  Intracoronary injection of autologous bone marrow-derived mononuclear cells in patients with large anterior acute myocardial infarction: a prematurely terminated randomized study. , 2007, Journal of the American College of Cardiology.

[6]  A. Klein,et al.  The history of substances for soft tissue augmentation. , 2000, Dermatologic surgery : official publication for American Society for Dermatologic Surgery [et al.].

[7]  S. Ogawa,et al.  Cardiomyocytes can be generated from marrow stromal cells in vitro. , 1999, The Journal of clinical investigation.

[8]  Stan Gronthos,et al.  The therapeutic applications of multipotential mesenchymal/stromal stem cells in skeletal tissue repair , 2009, Journal of cellular physiology.

[9]  D. Tobin,et al.  Hair-cycle-associated remodeling of the peptidergic innervation of murine skin, and hair growth modulation by neuropeptides. , 2001, The Journal of investigative dermatology.

[10]  H. Papadaki,et al.  Isolation of human bone marrow mesenchymal stem cells using different membrane markers: comparison of colony/cloning efficiency, differentiation potential, and molecular profile. , 2008, Tissue engineering. Part C, Methods.

[11]  Celso Matos,et al.  Treatment of osteonecrosis of the femoral head with implantation of autologous bone-marrow cells. A pilot study. , 2004, The Journal of bone and joint surgery. American volume.

[12]  Gordana Vunjak-Novakovic,et al.  Bone Tissue Engineering Using Human Mesenchymal Stem Cells: Effects of Scaffold Material and Medium Flow , 2004, Annals of Biomedical Engineering.

[13]  Bin Zhou,et al.  Cellular therapy and myocardial tissue engineering: the role of adult stem and progenitor cells. , 2006, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[14]  Florian Tögel,et al.  Adult bone marrow–derived stem cells for organ regeneration and repair , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[15]  T. Roth,et al.  Biochemical assessment of cellular damage after adipocyte harvest. , 1997, The Journal of surgical research.

[16]  Ping Zhang,et al.  Radiolabeled Cell Distribution After Intramyocardial, Intracoronary, and Interstitial Retrograde Coronary Venous Delivery: Implications for Current Clinical Trials , 2005, Circulation.

[17]  Gianpaolo Papaccio,et al.  Dental Pulp Stem Cells: A Promising Tool for Bone Regeneration , 2008, Stem Cell Reviews.

[18]  E. Thomas,et al.  Treatment of bone-marrow failure by isogeneic marrow infusion. , 1967, The New England journal of medicine.

[19]  M. Frankel In Search of Stem Cell Policy , 2000, Science.

[20]  Y. A. Wang,et al.  Localization of Putative Stem Cells in Dental Epithelium and Their Association with Notch and Fgf Signaling , 1999, The Journal of cell biology.

[21]  T. Noma,et al.  Soluble matrix from osteoblastic cells induces mineralization by dental pulp cells. , 2006, The journal of medical investigation : JMI.

[22]  Carina,et al.  Analysis of apoptosis during hair follicle regression (catagen) , 1997, The American journal of pathology.

[23]  C. Jahoda,et al.  Hair follicle dermal sheath cells: unsung participants in wound healing , 2001, The Lancet.

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

[25]  David A. Williams,et al.  Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: Implications for gene therapy , 1996, Nature Medicine.

[26]  H. Fujioka,et al.  Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. , 2007, Osteoarthritis and cartilage.

[27]  F. Deist,et al.  Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. , 2000, Science.

[28]  T. Okano,et al.  Cell sheet engineering for myocardial tissue reconstruction. , 2003, Biomaterials.

[29]  S. Gronthos,et al.  The biology and application of human bone marrow stromal cell precursors. , 1996, Journal of hematotherapy.

[30]  T. Ichisaka,et al.  Generation of germline-competent induced pluripotent stem cells , 2007, Nature.

[31]  P. Genever,et al.  Comparative characterization of hair follicle dermal stem cells and bone marrow mesenchymal stem cells. , 2006, Stem cells and development.

[32]  Gwo‐Jaw Wang,et al.  Steroid-Induced Adipogenesis in a Pluripotential Cell Line from Bone Marrow* , 1997, The Journal of bone and joint surgery. American volume.

[33]  A. Caplan,et al.  The STRO-1+ Marrow Cell Population Is Multipotential , 2001, Cells Tissues Organs.

[34]  R. Pochampally,et al.  Angiogenic Effects of Human Multipotent Stromal Cell Conditioned Medium Activate the PI3K‐Akt Pathway in Hypoxic Endothelial Cells to Inhibit Apoptosis, Increase Survival, and Stimulate Angiogenesis , 2007, Stem cells.

[35]  Neil D. Theise,et al.  Multi-Organ, Multi-Lineage Engraftment by a Single Bone Marrow-Derived Stem Cell , 2001, Cell.

[36]  Ki Suk Park,et al.  Chondrogenic differentiation of bone marrow stromal cells in transforming growth factor-β1 loaded alginate bead , 2005 .

[37]  Bruce J Tromberg,et al.  Imaging wound healing using optical coherence tomography and multiphoton microscopy in an in vitro skin-equivalent tissue model. , 2004, Journal of biomedical optics.

[38]  Robert M Hoffman,et al.  Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Maurilio Marcacci,et al.  Stem cells associated with macroporous bioceramics for long bone repair: 6- to 7-year outcome of a pilot clinical study. , 2007, Tissue engineering.

[40]  Bonpei Takase,et al.  Tissue engineering of articular cartilage with autologous cultured adipose tissue-derived stromal cells using atelocollagen honeycomb-shaped scaffold with a membrane sealing in rabbits. , 2006, Journal of biomedical materials research. Part B, Applied biomaterials.

[41]  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.

[42]  J. Jester,et al.  Hair follicles serve as local reservoirs of skin mast cell precursors. , 2003, Blood.

[43]  D. Katritsis,et al.  CORONARY ARTERY DISEASE Original Studies Transcoronary Transplantation of Autologous Mesenchymal Stem Cells and Endothelial Progenitors Into Infarcted Human Myocardium , 2005 .

[44]  W. Hayes,et al.  Bone regeneration by implantation of purified, culture‐expanded human mesenchymal stem cells , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[45]  E. Fuchs,et al.  NFATc1 Balances Quiescence and Proliferation of Skin Stem Cells , 2008, Cell.

[46]  M. Ogawa,et al.  Reversible expression of CD34 by murine hematopoietic stem cells. , 1999, Blood.

[47]  Yaping Liu,et al.  Capturing and profiling adult hair follicle stem cells , 2004, Nature Biotechnology.

[48]  V. Falanga,et al.  Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. , 2007, Tissue engineering.

[49]  D. Geschwind,et al.  From hematopoiesis to neuropoiesis: Evidence of overlapping genetic programs , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[50]  F. Guilak,et al.  Multipotent Stromal Cells Derived From the Infrapatellar Fat Pad of the Knee , 2003, Clinical orthopaedics and related research.

[51]  Bindiya Patel,et al.  Adipose-derived stem cells: isolation, expansion and differentiation. , 2008, Methods.

[52]  C. Jahoda,et al.  Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages , 2003, Experimental dermatology.

[53]  E. Taraldsrud,et al.  Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. , 2006, The New England journal of medicine.

[54]  I. Kerkis,et al.  Isolation and Characterization of a Population of Immature Dental Pulp Stem Cells Expressing OCT-4 and Other Embryonic Stem Cell Markers , 2007, Cells Tissues Organs.

[55]  W. Rombouts,et al.  Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture , 2003, Leukemia.

[56]  M Grim,et al.  Pluripotent neural crest stem cells in the adult hair follicle , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[57]  D J Prockop,et al.  Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[58]  J. Aubin,et al.  Differentiation of muscle, fat, cartilage, and bone from progenitor cells present in a bone-derived clonal cell population: effect of dexamethasone , 1988, The Journal of cell biology.

[59]  Hiromitsu Nakauchi,et al.  Long-Term Lymphohematopoietic Reconstitution by a Single CD34-Low/Negative Hematopoietic Stem Cell , 1996, Science.

[60]  Julia M Polak,et al.  Stem Cells and Tissue Engineering: Past, Present, and Future , 2006, Annals of the New York Academy of Sciences.

[61]  K. Burg,et al.  Stem cells and adipose tissue engineering. , 2006, Biomaterials.

[62]  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.

[63]  M. Hedrick,et al.  Emerging approaches to the tissue engineering of fat. , 1999, Clinics in plastic surgery.

[64]  H B CHASE,et al.  Growth of the hair. , 1954, Physiological reviews.

[65]  M. Goodell CD34+ or CD34−: Does it Really Matter? , 1999 .

[66]  C. Kruse,et al.  Towards the development of a pragmatic technique for isolating and differentiating nestin‐positive cells from human scalp skin into neuronal and glial cell populations: generating neurons from human skin? , 2006, Experimental dermatology.

[67]  D. Prockop Marrow Stromal Cells as Stem Cells for Nonhematopoietic Tissues , 1997, Science.

[68]  C. Jahoda,et al.  Plasticity of hair follicle dermal cells in wound healing and induction , 2003, Experimental dermatology.

[69]  R. Tuan,et al.  Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. , 2006, Osteoarthritis and cartilage.

[70]  Ralf Paus,et al.  Immunophenotyping of the human bulge region: the quest to define useful in situ markers for human epithelial hair follicle stem cells and their niche , 2008, Experimental dermatology.

[71]  D. Benayahu,et al.  Single‐Colony Derived Strains of Human Marrow Stromal Fibroblasts Form Bone After Transplantation In Vivo , 1997, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[72]  K. Matsushita,et al.  Side Population Cells Isolated from Porcine Dental Pulp Tissue with Self‐Renewal and Multipotency for Dentinogenesis, Chondrogenesis, Adipogenesis, and Neurogenesis , 2006, Stem cells.

[73]  M. Neubauer,et al.  Adipose tissue engineering based on mesenchymal stem cells and basic fibroblast growth factor in vitro. , 2005, Tissue engineering.

[74]  M. Lako,et al.  Hair follicle dermal cells repopulate the mouse haematopoietic system , 2002, Journal of Cell Science.

[75]  K. Satomura,et al.  Repair of craniotomy defects using bone marrow stromal cells. , 1998, Transplantation.

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

[77]  C. Verfaillie,et al.  Origin of endothelial progenitors in human postnatal bone marrow. , 2002, The Journal of clinical investigation.

[78]  C. Potten,et al.  Stem cells in gastrointestinal epithelium: numbers, characteristics and death. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[79]  V. Traynelis,et al.  A comparative analysis of fusion rates and donor-site morbidity for autogeneic rib and iliac crest bone grafts in posterior cervical fusions. , 1998, Journal of neurosurgery.

[80]  W McIntosh,et al.  Transdermal photopolymerization of poly(ethylene oxide)-based injectable hydrogels for tissue-engineered cartilage. , 1999, Plastic and reconstructive surgery.

[81]  A. Meunier,et al.  Tissue-engineered bone regeneration , 2000, Nature Biotechnology.

[82]  H Green,et al.  Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. , 1975, Cell.

[83]  Elaine Fuchs,et al.  Self-Renewal, Multipotency, and the Existence of Two Cell Populations within an Epithelial Stem Cell Niche , 2004, Cell.

[84]  C. Kruse,et al.  Hair follicle stem cells: walking the maze. , 2007, European journal of cell biology.

[85]  G. Isacchi,et al.  Osteogenesis induced by autologous bone marrow cells transplant in the pediatric skull , 2006, Child's Nervous System.

[86]  R. Deans,et al.  Mesenchymal stem cells: biology and potential clinical uses. , 2000, Experimental hematology.

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

[88]  Elaine Fuchs,et al.  Lhx2 Maintains Stem Cell Character in Hair Follicles , 2006, Science.

[89]  A I Caplan,et al.  Chondroprogenitor cells of synovial tissue. , 1999, Arthritis and rheumatism.

[90]  M. Kassem,et al.  Demonstration of the presence of independent pre-osteoblastic and pre-adipocytic cell populations in bone marrow-derived mesenchymal stem cells. , 2008, Bone.

[91]  R. Jaenisch,et al.  In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state , 2007, Nature.

[92]  H. Pinkus EPITHELIAL‐MESODERMAL INTERACTION IN NORMAL HAIR GROWTH, ALOPECIA, AND NEOPLASIA , 1978, The Journal of dermatology.

[93]  M. Kassem,et al.  The use of mesenchymal (skeletal) stem cells for treatment of degenerative diseases: Current status and future perspectives , 2009, Journal of cellular physiology.

[94]  J. Ortonne,et al.  Sox9 Is Essential for Outer Root Sheath Differentiation and the Formation of the Hair Stem Cell Compartment , 2005, Current Biology.

[95]  W. Hao,et al.  A novel injectable scaffold for cartilage tissue engineering using adipose‐derived adult stem cells , 2008, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[96]  S. Coleman Structural Fat Grafting: More Than a Permanent Filler , 2006, Plastic and reconstructive surgery.

[97]  W. Baumgartner,et al.  Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. , 2002, The Annals of thoracic surgery.

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

[99]  Hidezo Mori,et al.  Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction , 2006, Nature Medicine.

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

[101]  M. Hristov,et al.  Endothelial progenitor cells: mobilization, differentiation, and homing. , 2003, Arteriosclerosis, thrombosis, and vascular biology.

[102]  Hans Clevers,et al.  Lgr5 marks cycling, yet long-lived, hair follicle stem cells , 2008, Nature Genetics.

[103]  N. A. Onishchenko,et al.  Mesenchymal Bone Marrow Stem Cells More Effectively Stimulate Regeneration of Deep Burn Wounds than Embryonic Fibroblasts , 2003, Bulletin of Experimental Biology and Medicine.

[104]  A. Flake,et al.  Mesenchymal stem cells: paradoxes of passaging. , 2004, Experimental hematology.

[105]  David A. Williams,et al.  Upping the ante: recent advances in direct reprogramming. , 2009, Molecular therapy : the journal of the American Society of Gene Therapy.

[106]  M. Saito,et al.  Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. , 2002, Osteoarthritis and cartilage.

[107]  I. Weissman,et al.  Purification and characterization of mouse hematopoietic stem cells. , 1988, Science.

[108]  M. Longaker,et al.  Mitogenic and chondrogenic effects of fibroblast growth factor-2 in adipose-derived mesenchymal cells. , 2006, Biochemical and biophysical research communications.

[109]  F. Guilak,et al.  Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. , 2006, Arthritis and rheumatism.

[110]  S. Yamanaka,et al.  Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors , 2006, Cell.

[111]  Masahiro Miyazaki,et al.  Participation of adult mouse bone marrow cells in reconstitution of skin. , 2003, The American journal of pathology.

[112]  C. Dani,et al.  Adipocyte differentiation of multipotent cells established from human adipose tissue. , 2004, Biochemical and biophysical research communications.

[113]  R. Considine,et al.  Viability of fat obtained by syringe suction lipectomy: effects of local anesthesia with lidocaine , 1995, Aesthetic Plastic Surgery.

[114]  Jeffrey C. Wang,et al.  Demineralized bone matrix and spinal arthrodesis. , 2005, The spine journal : official journal of the North American Spine Society.

[115]  J. Mosca,et al.  T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. , 2005, Journal of biomedical science.

[116]  Bernd Hertenstein,et al.  Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial , 2004, The Lancet.

[117]  A. Eaves,et al.  Transplantable hematopoietic stem cells in human fetal liver have a CD34(+) side population (SP)phenotype. , 2001, The Journal of clinical investigation.

[118]  H. Sul,et al.  Understanding adipocyte differentiation. , 1998, Physiological reviews.

[119]  R. Guldberg,et al.  Hydrogel effects on bone marrow stromal cell response to chondrogenic growth factors. , 2007, Biomaterials.

[120]  T. Shimazaki,et al.  [Mammalian neural stem cells]. , 2008, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[121]  L. Niklason,et al.  Clonal Population of Adult Stem Cells: Life Span and Differentiation Potential , 2004, Cell transplantation.

[122]  H. Ohgushi,et al.  Transplantation of Mesenchymal Stem Cells Improves Cardiac Function in a Rat Model of Dilated Cardiomyopathy , 2005, Circulation.

[123]  S. Valiante,et al.  An approachable human adult stem cell source for hard‐tissue engineering , 2006, Journal of cellular physiology.

[124]  J. Dick,et al.  A newly discovered class of human hematopoietic cells with SCID-repopulating activity , 1998, Nature Medicine.

[125]  Yann Barrandon,et al.  Morphogenesis and Renewal of Hair Follicles from Adult Multipotent Stem Cells , 2001, Cell.

[126]  Raymond C. Boston,et al.  Dynamic Imaging of Allogeneic Mesenchymal Stem Cells Trafficking to Myocardial Infarction , 2005, Circulation.

[127]  H. Shimizu,et al.  Mesenchymal Stem Cells Are Recruited into Wounded Skin and Contribute to Wound Repair by Transdifferentiation into Multiple Skin Cell Type1 , 2008, The Journal of Immunology.

[128]  J. Gordon,et al.  Hair follicle growth controls. , 1996, Dermatologic clinics.

[129]  T. Sun,et al.  Label-retaining cells reside in the bulge area of pilosebaceous unit: Implications for follicular stem cells, hair cycle, and skin carcinogenesis , 1990, Cell.

[130]  Mahidhar M. Durbhakula,et al.  Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: A patient‐matched comparison , 2005, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[131]  J. Utikal,et al.  Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. , 2007, Cell stem cell.

[132]  A Kingman,et al.  In vivo bone formation by human bone marrow stromal cells: effect of carrier particle size and shape. , 2001, Biotechnology and bioengineering.

[133]  S. Lehmann,et al.  Functional, molecular and proteomic characterisation of bone marrow mesenchymal stem cells in rheumatoid arthritis , 2007, Annals of the rheumatic diseases.

[134]  E. Fuchs,et al.  Defining the Epithelial Stem Cell Niche in Skin , 2004, Science.

[135]  C. Lawrence,et al.  Plasticity of rodent and human hair follicle dermal cells: implications for cell therapy and tissue engineering. , 2005, The journal of investigative dermatology. Symposium proceedings.

[136]  J. Gimble,et al.  Surface protein characterization of human adipose tissue‐derived stromal cells , 2001, Journal of cellular physiology.

[137]  H. Ouyang,et al.  The Immunogenicity and Immunomodulatory Function of Osteogenic Cells Differentiated from Mesenchymal Stem Cells , 2006, The Journal of Immunology.

[138]  Gina A. Taylor,et al.  Involvement of Follicular Stem Cells in Forming Not Only the Follicle but Also the Epidermis , 2000, Cell.

[139]  G. Im,et al.  Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells? , 2005, Osteoarthritis and cartilage.

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

[141]  R. Mulligan,et al.  Dystrophin expression in the mdx mouse restored by stem cell transplantation , 1999, Nature.

[142]  R. Torensma Blood vessels engineered from human cells , 2005, The Lancet.

[143]  R. Tuan,et al.  Multilineage mesenchymal differentiation potential of human trabecular bone‐derived cells , 2002, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[144]  Takashi Aoi,et al.  Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts , 2008, Nature Biotechnology.

[145]  Hoang Nguyen,et al.  Tcf3 Governs Stem Cell Features and Represses Cell Fate Determination in Skin , 2006, Cell.

[146]  A Boyde,et al.  Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. , 2000, Journal of biomedical materials research.

[147]  G. Salles,et al.  Transplantation with selected autologous peripheral blood CD34+Thy1+ hematopoietic stem cells (HSCs) in multiple myeloma: impact of HSC dose on engraftment, safety, and immune reconstitution. , 2000, Experimental hematology.

[148]  E. Fuchs,et al.  Hair follicle stem cells are specified and function in early skin morphogenesis. , 2008, Cell stem cell.

[149]  J. Vojtaššák,et al.  Autologous biograft and mesenchymal stem cells in treatment of the diabetic foot. , 2006, Neuro endocrinology letters.

[150]  J. Cigudosa,et al.  Spontaneous human adult stem cell transformation. , 2005, Cancer research.

[151]  L. Petrelli,et al.  HUMAN MESENCHYMAL STEM CELLS ARE TOLERIZED BY MICE AND IMPROVE SKIN AND SPINAL CORD INJURIES. , 2004, Transplantation proceedings.

[152]  George Q. Daley,et al.  Reprogramming of human somatic cells to pluripotency with defined factors , 2008, Nature.

[153]  F. Guilak,et al.  Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. , 2003, Cytotherapy.

[154]  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.

[155]  M. Spector,et al.  Regulation of smooth muscle actin expression and contraction in adult human mesenchymal stem cells. , 2002, Experimental cell research.

[156]  H. Ohgushi,et al.  Tissue engineered ceramic artificial joint--ex vivo osteogenic differentiation of patient mesenchymal cells on total ankle joints for treatment of osteoarthritis. , 2005, Biomaterials.

[157]  Ilyas M. Khan,et al.  The surface of articular cartilage contains a progenitor cell population , 2004, Journal of Cell Science.

[158]  A. Ganser,et al.  Monitoring of Bone Marrow Cell Homing Into the Infarcted Human Myocardium , 2005, Circulation.

[159]  K. Ando,et al.  Ex vivo generation of CD34(+) cells from CD34(-) hematopoietic cells. , 1999, Blood.

[160]  A. Kligman Full Length ReportThe Human Hair Cycle1 , 1959 .

[161]  A. Friedenstein Precursor cells of mechanocytes. , 1976, International review of cytology.

[162]  E. Fuchs,et al.  Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. , 2001, Genes & development.

[163]  C. Jahoda Cell movement in the hair follicle dermis - more than a two-way street? , 2003, The Journal of investigative dermatology.

[164]  J. Dick,et al.  Characterization of Cord Blood Hematopoietic Stem Cells , 2003, Annals of the New York Academy of Sciences.

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

[166]  K. Kusumoto,et al.  Bone tissue engineering using human adipose-derived stem cells and honeycomb collagen scaffold. , 2008, Journal of biomedical materials research. Part A.

[167]  H. Green,et al.  Seria cultivation of strains of human epidemal keratinocytes: the formation keratinizin colonies from single cell is , 1975, Cell.

[168]  C. Huet,et al.  New approach to radiation burn treatment by dosimetry-guided surgery combined with autologous mesenchymal stem cell therapy. , 2007, Regenerative medicine.

[169]  S. Bruder,et al.  Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. , 2001, Trends in molecular medicine.

[170]  M. Saitoh,et al.  Human hair cycle. , 1970, The Journal of investigative dermatology.

[171]  Irving L. Weissman,et al.  Stem cells [14] , 1991 .

[172]  S. Rafii,et al.  Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. , 2000, Blood.

[173]  Sheila MacNeil,et al.  Progress and opportunities for tissue-engineered skin , 2007, Nature.

[174]  G. Buttermann Prospective nonrandomized comparison of an allograft with bone morphogenic protein versus an iliac-crest autograft in anterior cervical discectomy and fusion. , 2008, The spine journal : official journal of the North American Spine Society.

[175]  M. Herlyn,et al.  Isolation of a novel population of multipotent adult stem cells from human hair follicles. , 2006, The American journal of pathology.

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

[177]  F. Guilak,et al.  Effects of Transforming Growth Factor β1 and Dexamethasone on the Growth and Chondrogenic Differentiation of Adipose-Derived Stromal Cells , 2003 .

[178]  Paul G Scott,et al.  Mesenchymal Stem Cells Enhance Wound Healing Through Differentiation and Angiogenesis , 2007, Stem cells.

[179]  C. Patrick,et al.  Adipose tissue engineering: the future of breast and soft tissue reconstruction following tumor resection. , 2000, Seminars in surgical oncology.

[180]  Y. Illouz Body Contouring by Lipolysis: A 5‐Year Experience with over 3000 Cases , 1983, Plastic and reconstructive surgery.

[181]  S. Nishikawa,et al.  Dominant role of the niche in melanocyte stem-cell fate determination , 2002, Nature.

[182]  L. Jeng,et al.  Bone marrow mesenchymal stem cells form ectopic woven bone in vivo through endochondral bone formation. , 2009, Artificial organs.

[183]  W. Wilkison,et al.  Adipogenic potential of human adipose derived stromal cells from multiple donors is heterogeneous , 2001, Journal of cellular biochemistry.

[184]  Robert M Hoffman,et al.  The Pluripotency of Hair Follicle Stem Cells , 2006, Cell cycle.

[185]  A. Prematurely Intracoronary Injection of Autologous Bone Marrow-Derived Mononuclear Cells in Patients With Large Anterior Acute Myocardial Infarction A Prematurely Terminated Randomized Study , 2007 .

[186]  Mara Riminucci,et al.  Bone Marrow Stromal Stem Cells: Nature, Biology, and Potential Applications , 2001, Stem cells.

[187]  K. Shimizu,et al.  Thoracolumbar kyphosing scoliosis associated with spondyloepiphyseal dysplasia congenita: a case report. , 2005, The spine journal : official journal of the North American Spine Society.

[188]  Hans Hauner,et al.  Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells. , 2003, Arthritis and rheumatism.

[189]  D. Prockop,et al.  Differentiation, cell fusion, and nuclear fusion during ex vivo repair of epithelium by human adult stem cells from bone marrow stroma , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[190]  C. Patrick,et al.  Tissue engineering strategies for adipose tissue repair , 2001, The Anatomical record.

[191]  M. Goebeler,et al.  Chemokines in cutaneous wound healing , 2001, Journal of leukocyte biology.

[192]  F J van Milligen,et al.  Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. , 2006, Cytotherapy.

[193]  H. Mitsuya,et al.  In vitro transdifferentiation of adult bone marrow Sca-1+ cKit- cells cocultured with fetal liver cells into hepatic-like cells without fusion. , 2006, Experimental hematology.

[194]  M. Ogawa,et al.  CD34+ human marrow cells that express low levels of Kit protein are enriched for long-term marrow-engrafting cells. , 1996, Blood.

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

[196]  E. Caterson,et al.  Human marrow-derived mesenchymal progenitor cells , 2002, Molecular biotechnology.

[197]  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.

[198]  H. Ohgushi,et al.  Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. , 2004, American journal of physiology. Heart and circulatory physiology.

[199]  J. Huard,et al.  Muscle-derived stem cells: potential for muscle regeneration. , 2003, Birth defects research. Part C, Embryo today : reviews.

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

[201]  W. Wilkison,et al.  Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. , 2001, Tissue engineering.

[202]  V. Goldberg,et al.  In vivo osteochondrogenic potential of cultured cells derived from the periosteum. , 1990, Clinical orthopaedics and related research.

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

[204]  D. Kotton,et al.  Derivation of lung epithelium from bone marrow cells. , 2003, Cytotherapy.

[205]  Fei Ye,et al.  Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. , 2004, The American journal of cardiology.

[206]  A. S. Conner,et al.  Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo , 1996, The Journal of experimental medicine.

[207]  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.

[208]  T. Ito,et al.  Developmental changes of CD34 expression by murine hematopoietic stem cells. , 2000, Experimental hematology.

[209]  R. Albertini,et al.  Bone-marrow transplantation in a patient with the Wiskott-Aldrich syndrome. , 1968, Lancet.

[210]  A. Ganser,et al.  Intracoronary Bone Marrow Cell Transfer After Myocardial Infarction: Eighteen Months’ Follow-Up Data From the Randomized, Controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) Trial , 2006, Circulation.

[211]  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.

[212]  F. Guilak,et al.  Mechanical signals as regulators of stem cell fate. , 2004, Current topics in developmental biology.

[213]  Takayuki Asahara,et al.  Isolation of Putative Progenitor Endothelial Cells for Angiogenesis , 1997, Science.

[214]  Meng Liu,et al.  Generation of induced pluripotent stem cells from adult rhesus monkey fibroblasts. , 2008, Cell stem cell.

[215]  O. Matsuo,et al.  Mesenchymal progenitor cells in adult human dental pulp and their ability to form bone when transplanted into immunocompromised mice , 2007, Cell biology international.

[216]  W. Wilkison,et al.  Thiazolidinediones and glucocorticoids synergistically induce differentiation of human adipose tissue stromal cells: biochemical, cellular, and molecular analysis. , 2001, Metabolism: clinical and experimental.

[217]  C. Verfaillie Hematopoietic stem cells for transplantation , 2002, Nature Immunology.

[218]  I. Sekiya,et al.  Isolation and characterization of rapidly self-renewing stem cells from cultures of human marrow stromal cells. , 2001, Cytotherapy.

[219]  Y. Sakaguchi,et al.  Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. , 2005, Arthritis and rheumatism.

[220]  Hermann Eichler,et al.  Comparative Analysis of Mesenchymal Stem Cells from Bone Marrow, Umbilical Cord Blood, or Adipose Tissue , 2006, Stem cells.

[221]  B. Shroot,et al.  Outer root sheath cells of human hair follicle are able to regenerate a fully differentiated epidermis in vitro. , 1988, Developmental biology.

[222]  Robert M Hoffman,et al.  Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[223]  Jason A Burdick,et al.  Engineering cartilage tissue. , 2008, Advanced drug delivery reviews.

[224]  K. McElwee,et al.  Cultured peribulbar dermal sheath cells can induce hair follicle development and contribute to the dermal sheath and dermal papilla. , 2003, The Journal of investigative dermatology.

[225]  F. Guilak,et al.  Clonal analysis of the differentiation potential of human adipose‐derived adult stem cells , 2006, Journal of cellular physiology.

[226]  M. Ginsberg,et al.  Identification of a New Biological Function for the Integrin αvβ3: Initiation of Fibronectin Matrix Assembly , 1996 .

[227]  A R Boccaccini,et al.  Myocardial tissue engineering: a review , 2007, Journal of tissue engineering and regenerative medicine.

[228]  Farshid Guilak,et al.  Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. , 2002, Biochemical and biophysical research communications.

[229]  A. Shuttleworth,et al.  Direct cell contact influences bone marrow mesenchymal stem cell fate. , 2004, The international journal of biochemistry & cell biology.

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

[231]  D. Fisher,et al.  Mechanisms of Hair Graying: Incomplete Melanocyte Stem Cell Maintenance in the Niche , 2005, Science.

[232]  David R. Kaplan,et al.  A dermal niche for multipotent adult skin-derived precursor cells , 2004, Nature Cell Biology.

[233]  M. Burnett,et al.  Marrow-Derived Stromal Cells Express Genes Encoding a Broad Spectrum of Arteriogenic Cytokines and Promote In Vitro and In Vivo Arteriogenesis Through Paracrine Mechanisms , 2004, Circulation research.

[234]  Farshid Guilak,et al.  Chondrocytic differentiation of human adipose-derived adult stem cells in elastin-like polypeptide. , 2006, Biomaterials.