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Table of Contents   
REVIEW ARTICLE  
Year : 2012  |  Volume : 23  |  Issue : 3  |  Page : 393-397
Dental stem cells: Dentinogenic, osteogenic, and neurogenic differentiation and its clinical cell based therapies


1 Department of Pedodontics and Preventive Dentistry, Genesis Institute of Dental Sciences and Research, Ferozepur, Punjab, India
2 Department of Pedodontics, Fortis Hospital, Mohali, Punjab, India

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Date of Submission12-May-2011
Date of Decision25-Sep-2011
Date of Acceptance20-Nov-2011
Date of Web Publication11-Oct-2012
 

   Abstract 

Each year approximately $400 billion is spent treating Americans suffering some type of tissue loss or end-stage organ failure. This includes millions of dental and oral craniofacial procedure, ranging from tooth restorations to major reconstruction of facial soft and mineralized tissue. Recently, a population of putative post-natal stem cells in human dental pulp (DPSCs) has been identified within the "cell- rich zone" of dental pulp. The other type of stem cells from human exfoliated deciduous teeth (SHED) was identified to be a population of highly proliferative, clonogenic cells. Dental Pulp Stem Cells (DPSCs) can not only be derived from a very accessible tissue resource like SHED but are also capable of providing enough cells for potential cell-based therapies.

Keywords: Dental pulp stem cells, stem cells, stem cells from human exfoliated deciduous teeth

How to cite this article:
Brar GS, Toor RS. Dental stem cells: Dentinogenic, osteogenic, and neurogenic differentiation and its clinical cell based therapies. Indian J Dent Res 2012;23:393-7

How to cite this URL:
Brar GS, Toor RS. Dental stem cells: Dentinogenic, osteogenic, and neurogenic differentiation and its clinical cell based therapies. Indian J Dent Res [serial online] 2012 [cited 2014 Nov 26];23:393-7. Available from: http://www.ijdr.in/text.asp?2012/23/3/393/102239
Tooth development, initiating at 6 weeks of intrauterine (IU) life, is a process characterized by a series of complex, reciprocal and sequential interactions taking place between oral epithelium and the underlying neuroectomesenchyme. Under the influence of cell signals, epithelial cells of the dental lamina at predetermined locations proliferate and project into the underlying neural crest derived ectomesenchyme. Initially this projection is in the shape of a bud, and gets pronounced into a cap due to proliferation of cells. Further proliferation leads to the enamel organ assuming a bell shape. Simultaneous with the proliferation, there also occurs morphologic differentiation of cells in the enamel organ. [1]

Key molecular events during this developmental process such as initiation, proliferation, morphogenesis, cytodifferentiation and spatial distribution of cells are principally controlled and mediated by the presence of morphogens / growth factors (GFs) like epidermal growth factor (EGF), members of transforming growth factor (TGF) family [ bone morphogenetic protein (BMP) 2-7,growth differentiation factor ( GDF)], fibroblast growth factor (FGF) family (such as FGF - 3, FGF - 4, FGF -8 and FGF -10), Wnt proteins (such as Wnt - 3, Wnt - 7b, Wnt - 10a and Wnt -10b) and sonic hedgehog (Shh) proteins. Amongst several GFs, the BMP family of GFs seems to be the key factor in controlling tooth development by regulating various activities ranging from epithelial mesenchymal interactions, inducing mesenchyme to become odontogenic (BMP 4), controlling morphogenesis of epithelium to formation and maintenance of enamel knots (BMP 2, BMP 4 and BMP 7). Expression domain of BMP 4 has seen to expand with the loss of transcription factor Osr 2 leading to induction of supernumerary teeth. [2]


   Stem Cell Sources Top


Two populations of stem cells involved in tooth formation are the epithelial stem cells and the mesenchymal stem cells, the latter required for pulp dentin regeneration. Mesenchymal stem cells have the potential to differentiate into tissues of mesodermal lineages - bone, cartilage, adipose tissue, skeletal muscle and connective tissue stroma. Mesenchymal stem cells located in a perivascular niche in the dental pulp, periodontal ligament (PDL), dental follicle and bone marrow may be the potential sources for cell-based therapies in regenerating the tooth. [3] These adult stem cells have been called Dental Pulp Stem Cells (DPSCs), when found in permanent teeth, and Stem cells from Human Exfoliated Deciduous (SHED), when found in deciduous teeth. DPSCs were isolated for the first time in 2000 by Gronthos et al, these cells exhibited a differentiation potential for odontoblastic, adipogenic and neural cytotypes. The same group isolated SHED from deciduous teeth and compared DPSCs with bone marrow stem cells (BMSCs). Autogenous post natal stem cells seem to be the most promising cells for regenerating pulp dentin tissues compared to embryonic and/or allogenic or xenogenic stem cells as they offer relatively easier accessible sources, reduce the possibility of immune rejection, pathogen transmission and have limited legal or ethical concerns. Exfoliating deciduous teeth, impacted third molars that need to be extracted or fractured teeth having exposed pulps that require endodontic treatment offer convenient ways of obtaining stem cells with limited ethical or legal concerns. [4]

Bone marrow stem cells

Both Bone Marrow Stem Cells (BMSCs) and DPSCs can differentiate into osteoblasts, chondrocytes , adipocytes and odontoblasts exhibiting the ability to generate osteoid or odontoid structures, although BMSCs display a lower odontogenic competence than DPSCs. BMSCs have demonstrated good ability to form tooth supporting periodontal structures like cementum, PDL and alveolar bone suggesting their potential use for treating periodontal diseases. However, because of their limited potential to generate odontoblasts, their use in pulp dentin regeneration may be limited and remains to be further explored. [5]

Human dental pulp stem cells

DPSCs / progenitor cells are found to reside in the central cell-rich zone of the pulp particularly in the perivascular and perineurosheath regions. Pericytes have also been suggested in some studies to be able to differentiate into odontoblasts. In an in vitro study by Huang et al [6] adult pulp cells after being seeded onto mechanically and chemically treated dentin surface demonstrated formation of cells having odontoblast like morphologies with processes extending into dentinal tubules. Huang et al reported isolation and characterization of Human DPSCs (hDPSCs) from the pulp tissue of crown fractured teeth that did not require extraction as well as from supernumerary teeth thereby extending the potential available sources of hDPSCs. Compared to BMSCs, hDPSCs can be more easily sourced as they can be obtained from teeth that mandate pulp extirpation or from sound teeth that are deemed for extraction may be due to orthodontic or periodontal reasons. Induced DPSCs compared to native DPSCs may produce more regular dentinogenesis.

Stem cells from human exfoliated deciduous teeth

Exfoliating deciduous teeth contain living pulp remnants are good sources of cells which are highly proliferative, clonogenic and have multi-differentiation potential. These cells have been termed as SHED and were isolated and characterized by Miura et al, SHED offers attractive advantages over other post natal stem cells, as they are derived from a source which is non-invasive, readily accessible, naturally being disposed and with very limited ethical or legal concerns. Compared to BMSCs and hDPSCs, SHED shows a higher proliferation rate, increased cell-population doublings, sphere-like cell-cluster formation, osteoinductive capacity, more immature and higher self-renewal capabilities. [7] They exhibit differentiation ability to convert into adipocytes, neural cells, odontoblasts and osteoblasts. They however exhibit an osteoinductive potential in which the host cells are stimulated to differentiate into bone forming cells. Miura et al also demonstrated the inability of SHED to generate complete dentin-pulp like tissue as did hDPSCs, indicating that perhaps they are immature cells.

SHED could not differentiate directly into osteoblasts but did induce new bone formation by forming an osteoinductive template to recruit murine host osteogenic cells. This indicates that deciduous teeth may not only provide guidance for the eruption of permanent teeth, as generally assumed, but may also be involved in inducing bone formation during the eruption of permanent teeth.

Stem cells from the Apical Papilla

Amongst various post natal stem cells, stem cells from the apical portion of the dental papilla of human immature permanent teeth happen to be a newly discovered population of stem cells by Sonoyama et al who termed them as Stem Cells of Apical Papilla (SCAP) and studied their physical and histological characteristics. It is known that dental papilla participates in tooth formation and later evolves into dental pulp. In immature teeth, when the roots are still developing, dental papilla assumes a position apical to the pulp tissue and the epithelial diaphragm. [8] This apical papilla is loosely attached to the apex of the root from where it can be easily detached. In between the apical papilla and the overlying dental pulp is present a layer of highly populated cell rich zone. Apical papilla is less cellular and vascular compared to dental pulp but SCAP compared to DPSCs shows a proliferation rate higher by two fold to three fold.

The capacity of SCAP to differentiate into functional dentinogenic cells in vivo has been verified using an implantation technique in animal models. Ex vivo expanded SCAP were transplanted into immunocompromised mice using particles of Hydroxyapatite (HA) / Tricalcium Phosphate (TCP) as a carrier. A typical dentin structure was generated in which a layer of dentin tissue was formed on the surface of the HA/TCP along with connective tissue. Cells that are responsible for the dentin formation stained positively with a human-specific antimitochondria antibody. In order to examine whether SCAP are distinct from DPSCs, SCAP and DPSCs from the same tooth were isolated and grown in cultures under the same conditions. It was found that SCAP showed a significantly greater bromodeoxyuridine uptake rate, number of population doublings, tissue regeneration capacity, and number of STRO-1 positive cells when compared with DPSCs. In addition, SCAP express a higher level of survivin (anti-apoptotic protein) than DPSCs and are positive for human telomerase reverse transcriptase (hTERT) that maintains the telomere length activity, which is usually negative in mesenchymal stem cells (MSCs). These lines of evidence suggest that SCAP derived from a developing tissue may represent a population of early stem/progenitor cells, which may be a superior cell source for tissue regeneration. Additionally, these cells also highlight an important fact that developing tissues may contain stem cells distinctive from that of mature tissues. [9]

Despite SCAP expressing many dentinogenic markers after ex vivo expansion, they express lower levels of dentin sialophosphoprotein, matrix extracellular phosphoglycoprotein, TGF βRII, FGFR3, Flt-1 [vascular endothelial growth factor (VEGF) receptor 1], Flg (FGFR1), and MUC18 (melanoma-associated glycoprotein) than do DPSCs. SCAP, as all ex vivo-expanded MSCs, are a heterogeneous population of cells. Subpopulations of STRO-1positive SCAP are coexpressed with a variety of dentinogenic markers. In addition, SCAP show a positive staining for several neural markers including βIII tubulin, glutamic acid decarboxylase, neuronal nuclear antigen (NeuN), nestin, neurofilament M, neuron-specific enolase, and CNPase (glial marker, 2′,3′-cyclic nucleotide 3′-phosphodiesterase) by immunocytochemical staining. The neurogenic potential of SCAP could be because of the fact that SCAP are derived from neural crest cells or at least associated with neural crest cells analogous to other dental stem cells such as DPSCs and SHED that have been shown previously to possess a neurogenic potential. Whether the neurogenicity of dental stem cells is more potent than that of BMMSCs has not been investigated. Evidence has shown that BMMSCs have the potential for neuronal differentiation but at a much lower scale compared with stem cells derived from neural tissues. If dental stem cells are more capable of neurogenic differentiation than BMMSCs, they may present an appropriate cell source for neural tissue regeneration. [10]

Neurogenic potential of dental pulp stem cells

The fact that DPSCs are derived from neural crest mesenchyme raises hope that they may be good sources of stem cells to treat neural tissue injuries or degenerative diseases. Recent studies focusing on alternate stem cell sources for neural regeneration have demonstrated that DPSCs, SHED, SCAP and Dental Follicle Stem Cells (DFSCs) possess differentiation properties of MSCs and Neural Stem Cells (NSCs). These stem cells have expressed a variety of neural cell markers like nestin, βIII tubullin, glutamine acid decorboxylase (GAD), neuronal nuclei (Neu N), glial fibrillary acidic protein (GFAP), neurofilament M (NFM), Neuron Specific Enolase (NSE) and 2'3'-cycle nucleotide- 3' - phosphodiesterase (CNP ase) when induced with neurogenic medium.

Gangliosides may play a possible role in the neuronal differentiation process of hDPSCs. In a study when ganglioside biosynthesis was inhibited in hDPSCs by knockdown of UDP-glucose ceramide glucosyltransferase, differentiation into neural cells was prevented.

DFSCs also exhibit the ability to differentiate into neurons and can be isolated from follicle surrounding human third molars. Post natal stem cells isolated from dental anomalies such as odontomas have shown to be highly proliferative like DPSCs with stronger neural immunophenotypes than both DPSCs and mandible bone marrow stromal cells.

The potential role of SCAP in replantation and transplantation

Andreasen et al. [11] and Kling et al. [12] showed excellent radiographic images of the ingrowth of bone PDL (next to the inner dentinal wall) into the canal space with arrested root formation after the replantation of avulsed maxillary incisors, suggesting a complete loss of the viability of pulp, apical papilla, and/or Hertwig's Epithelial Root Sheath (HERS). Some cases showed partial formation of the root accompanied with ingrowth of bone and PDL into the canal space, and in some cases the teeth continued to develop roots to their completion, suggesting that there was partial or total pulp survival after the replantation. It is noted, however, that a pronounced narrowing of canal space is usually associated with a surviving pulp. Skoglund et al observed revascularization of the pulp of replanted and autotransplanted teeth with incomplete root development in dogs. Ingrowth of new vessels occurs during the first few postoperative days. After 10 days, new vessels are formed in the apical half of the pulp and, after 30 days, in the whole pulp. In some instances, anastomoses seemed to form with preexisting vessels in the pulp. Although revascularization occurs, the pulp space is eventually filled with hard tissue. [13] Other animal studies focusing on the changes in pulp tissue after replantation showed that various hard tissues including dentin, cementum, and bone may form in the pulp space depending on the level of pulp recovery. If pulp and apical papilla are totally lost, then the root canal space may be occupied by cementum, PDL, and bone. By tracing the migration of periodontal cells after pulpectomy in immature teeth, Vojinovic and Vojinovic found that periodontal cells migrate into the apical pulp space during the repair process. Therefore, one may assume that when there is a total loss of pulp tissue but the canal space remains in a sterile condition, the outcome is the ingrowth of periodontal tissues. [14] One of the clinical treatment options for missing teeth is autotransplantation. The process often involves extraction of a supernumerary tooth or third molar and implantation into a recipient site. It has been considered that as long as the HERS remains viable, it stimulates the undifferentiated mesenchymal cells in periradicular tissues to differentiate into odontoblasts that contribute to the formation of new dentin and root maturation. However, the current understanding is that pulp cells are different from periodontal cells. Based on current available information, it is likely that odontoblast lineages are derived from stem cells in pulp tissue or apical papilla. Both SCAP and HERS appear to be important for the continued root development after transplantation. SCAP are also highly probable to survive after transplantation because minimal vascularity is found in apical papilla based on preliminary findings. The reason that transplanting a tooth with little or no root formation results in almost no further root development is unclear. One may speculate that the integrity of the entire tooth organ at that stage is critical for the root development to continue. During the transplantation, any disruption of the structure such as the follicle, HERS, and apical papilla will prevent further root development.

Stem cells for pulp/dentin tissue engineering and regeneration

Bohl et al reported that culturing pulp cells grown on polyglycolic acid (PGA) in vitro resulted in high cell density tissue similar to the native pulp. Burma et al found that pulp cells seeded in PGA and implanted into the subcutaneous space of immunocompromised mice produced extracellular matrix. New blood vessels also penetrated the cells/PGA implants in vivo 3 weeks after the implantation. Since the isolation and characterization of DPSCs and SHED using these stem cells for dentin/pulp tissue regeneration has drawn great interest. Reparative dentin-like structure is deposited on the dentin surface if DPSCs are seeded onto a human dentin surface and implanted into immunocompromised mice, suggesting the possibility of forming additional new dentin on the existing dentin. [15]

Scaffold is a three-dimensional biodegradable porous polymer framework that serves as a potential biologic carrier to facilitate delivery of stem cells and/or growth factors at a local receptor site. It provides a matrix for cell seeding, cell adhesion and growth. Nutrients may be embedded into the scaffold to promote cell survival. To serve as a physical matrix for pulp dentin reconstruction, the scaffold should meet certain requirements like ease of handling, adequate porosity, biodegradability, biocompatibility, good physical and mechanical strengths and ability to support vascularity.

Several synthetic polymers that have been successfully used as a scaffold matrix because of their biocompatibility and biodegradability include polyester materials like polylactic acid (PLA), PGA, poly- (lactic- co-glycolic acid) (PLGA), and poly- caprolactone (PCL). These polymers degrade to form lactic acid or glycolic acid, a natural chemical which is easily removed from the body. Other synthetic polymers that have been advocated as scaffold materials include hydrogels, calcium phosphates, glasses and composites. PGA has shown to be a more conducive scaffold for development of a tissue with cellularity similar to dental pulp than a hydrogel or alginate.

Calcium phosphate (Ca/P) scaffolds include beta-tricalcium phosphate (β -TCP) and HA. Ca/P can be suitable for dentin regeneration as it is similar to the natural mineralized tissue, is biocompatible and osteoconductive. Natural scaffold materials which have been tried are proteins like collagen or fibrin, polysaccharides like chitosan or glycosaminoglycans and alginates. Collagen is a predominant component of dentin and pulp tissues. Collagen scaffolds have hence been popularly used in regenerative studies because of their structural similarity to natural tissues. When PLA polymer, collagen and Ca/P materials were compared as scaffolds, polymer and collagen showed significantly more DPSC survival than Ca/P scaffold.

Possible regenerative endodontic procedures

Technologies for regenerating endodontium can be based on two approaches.

  • Creating a denovo engineered tissue construct in the laboratory and transplanting it into the recipient tooth.
  • Inducing host stem cells from the adjacent site to mobilize and inhabit the implanted/natural host matrix.


Regenerating pulp

Pulp tissue constructs fabricated from SHED and PLA scaffolds with/without added GFs, BMP2 and TGF μ1 have shown a more complete adherence to the coronal dentin and a less complete adherence to the middle and apical aspects of the root canal, which is likely due to the complex anatomy of the root canal toward the apex and the physical constraints of the placement method in narrow canals at the apex.

Injecting a soft scaffold matrix impregnated with pulp stem cells and GFs into areas with accessibility constraints like the root canal system can overcome difficulties associated with implanting a rigid matrix. Scaffold material that can be injected includes synthetic hydrogels like poly ethylene glycol polymers. Though delivery system is relatively easier with these polymers, problems of low cell survival and limited control over tissue formation still exist. Modifying hydrogel polymers with peptides like arginine, glycine or aspartic acid have helped in improving cell adhesion and matrix synthesis rendering them suitable for use.

Whether the engineered tissue is implanted or injected, there always exists a possibility of bacterial ingrowth into the root canal system. Thorough disinfection is essential for cell survival and integration of dental pulp construct with the host tissues. Additionally, antibiotics impregnated into the scaffold matrix possibly by using nano engineering techniques can prevent bacterial growth. Another persistent problem which needs to be addressed is the lack of initial blood supply making sufficient oxygen and nutrients unavailable for the implanted cells. In the laboratory, extensive culturing with closely monitored oxygen, pH, humidity, temperature, nutrients and osmotic pressure promotes cell survival, growth and functionality. When transplanted in vivo, blood vessel ingrowth is important to provide nutrition which in a tooth can occur only through the apical foramen present at the root apex as a tooth lacks collateral circulation. With increasing distance from the apex, cell survival becomes difficult because of the decreasing nutrient supply. Introducing engineered tissue in multiple increments may help overcome this limitation but at the same time would increase the possibility of bacterial contamination due to re-entry into the tooth. [2]

Pulp generation by inducing endogenous stem cells to inhabit a matrix

Generation of pulp tissue within the root canal space by inducing stem cells from the adjacent site to populate the area can be possibly achieved if the following coexist (1) thorough disinfected canal (2) presence of a matrix within the canal on which new tissue can grow (3) appropriate factors or stimuli present locally in the desired concentration and for desired time period and (4) bacteria impermeable seal of the access opening. There are several case reports which have documented regeneration of vital tissue in immature teeth with incompletely formed roots after the canals were thoroughly disinfected and bleeding was established in the canals by over instrumentation. This process has been termed as pulpal revascularization by most authors. Irrigation with sodium hypochlorite (0.5 - 5.2%), hydrogen peroxide (3%) or chlorhexidine gluconate with/without the additional use of antibiotics is used to achieve a high level of disinfection. A combination of ciprofloxacin, metronidazole and minocyclin has shown promising results in effectively eliminating bacteria from carious lesions, infected pulp and infected root dentin. Tetracycline may have an additional possible effect of enhancing growth of pulp cells onto dentin by exposing embedded collagen or growth factors in dentin.


   Conclusion Top


The success of regenerative endodontics will depend on how closely multidisciplinary teams of clinicians, engineers, scientists and technicians can work, each contributing their own area of expertise to expand research. There is an extensive need to translate preclinical research into clinical realities. Forums should be formed by which various agencies involved in tissue science and engineering stay informed of each other's activities and are hence able to coordinate their efforts in a timely and efficient manner. These agencies can help promote the entire field of tissue engineering without wasteful duplication of efforts by creating common websites, organizing scientific meetings and workshops, monitoring technology by undertaking cooperative assessments and advertising for new opportunities.

Even though it is a long way to go, once the potential of regenerative endodontics is unleashed, it would be of immense clinical advantage and benefit millions of patients as an enormous part of dentistry is based on treating patients with dental caries.

 
   References Top

1.Lumsden AG. Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 1988;103: 155-69.  Back to cited text no. 1
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2.Sharma S, Sikri V, Sharma NK,Sharma VM. Regeneration of tooth pulp and dentin: trends and advances. Ann neurosci 2010;17: 31-43.   Back to cited text no. 2
    
3.Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J bone Miner Res 2003;18: 696-704.  Back to cited text no. 3
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4.Seo B, Miura M, Gronthos S. Investigation of multipotent stem cells from human periodontal ligament. Lancet 2004; 364: 149-55.  Back to cited text no. 4
    
5.Yu J, Wang Y, Deng Z. Odontogenic capability: bone marrow stromal stem cells versus dental pulp stem cells. Biol Cell 2007; 99: 465- 74.  Back to cited text no. 5
    
6.Huang A, Chen Y, Chan A. Isolation and characterization of human dental pulp stem/stromal cells from nonextracted crown fractured teeth requiring root canal therapy. J Endod 2009;35: 673-81.  Back to cited text no. 6
    
7.Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, et al. SHED:stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 2003; 100: 5807-12.  Back to cited text no. 7
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8.Sonoyama W, Liu Y, Fang D. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS ONE 2006; 1: e79.  Back to cited text no. 8
    
9.Sonoyama W, LiuY, Yamaza T. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 2008; 34: 166-71.  Back to cited text no. 9
    
10.Huang GT, Sonoyama. The Hidden Treasure in Apical Papilla: The Potential Role in Pulp/Dentin Regeneration and BioRoot engineering. JEndod 2008; 34:645-51.  Back to cited text no. 10
    
11.Andreasen JO, Barum MK, Jacobsen HL, Andreasen FM. Replantation of 400 avulsed permanent incisors. 1. Diagnosis of healing complications. Endod Dent Traumatol 1995; 11:51-8.  Back to cited text no. 11
    
12.Kling M, Cvek M, Mejare I. Rate and Predictability of pulp revascularization in therapeutically reimplanted permanent incisors. Endod Dent Traumatol 1986; 2: 83-9.  Back to cited text no. 12
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13.Skoglund A, Tronstad I. A microangiographic study of vascular changes in replanted and autotransplanted teeth of young dogs. Oral Surg Oral Med Oral Pathol 1978; 45:17-28.  Back to cited text no. 13
    
14.Vojinovic O, Vojinovic J. Periodontal cell migration into the apical pulp during the repair process after pulpectomy in immature teeth:an autoradiographic study. J Oral Rehabil 1993;20:637-52.  Back to cited text no. 14
    
15.Bohl KS, Shan J, Rutherford B, Mooney D. Role of Synthetic extracellular matrix in development of engineered dental pulp. J Biomater Sci Polym Ed 1998; 9: 749-64.  Back to cited text no. 15
    

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Correspondence Address:
Gurlal Singh Brar
Department of Pedodontics and Preventive Dentistry, Genesis Institute of Dental Sciences and Research, Ferozepur, Punjab
India
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DOI: 10.4103/0970-9290.102239

PMID: 23059580

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