The Emerging Role of Stem Cells in Regenerative Dentistry

Author(s): Paolo Capparè*, Giulia Tetè, Maria Teresa Sberna, Paola Panina-Bordignon*

Journal Name: Current Gene Therapy

Volume 20 , Issue 4 , 2020


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Graphical Abstract:


Abstract:

Progress of modern dentistry is accelerating at a spectacular speed in the scientific, technological and clinical areas. Practical examples are the advancement in the digital field, which has guaranteed an average level of prosthetic practices for all patients, as well as other scientific developments, including research on stem cell biology. Given their plasticity, defined as the ability to differentiate into specific cell lineages with a capacity of almost unlimited self-renewal and release of trophic/immunomodulatory factors, stem cells have gained significant scientific and commercial interest in the last 15 years. Stem cells that can be isolated from various tissues of the oral cavity have emerged as attractive sources for bone and dental regeneration, mainly due to their ease of accessibility. This review will present the current understanding of emerging conceptual and technological issues of the use of stem cells to treat bone and dental loss defects. In particular, we will focus on the clinical application of stem cells, either directly isolated from oral sources or in vitro reprogrammed from somatic cells (induced pluripotent stem cells). Research aimed at further unraveling stem cell plasticity will allow to identify optimal stem cell sources and characteristics, to develop novel regenerative tools in dentistry.

Keywords: Stem cells, progenitor cells, tissue regeneration, bone, dental pulp, regenerative dentistry.

[1]
Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008; 132(4): 598-611.
[http://dx.doi.org/10.1016/j.cell.2008.01.038] [PMID: 18295578]
[2]
Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292(5819): 154-6.
[http://dx.doi.org/10.1038/292154a0] [PMID: 7242681]
[3]
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-76.
[http://dx.doi.org/10.1016/j.cell.2006.07.024] [PMID: 16904174]
[4]
Amit M, Carpenter MK, Inokuma MS, et al. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 2000; 227(2): 271-8.
[http://dx.doi.org/10.1006/dbio.2000.9912] [PMID: 11071754]
[5]
Wray J, Kalkan T, Smith AG. The ground state of pluripotency. Biochem Soc Trans 2010; 38(4): 1027-32.
[http://dx.doi.org/10.1042/BST0381027] [PMID: 20658998]
[6]
Hayashi Y, Ohnuma K, Furue MK. Pluripotent stem cell heterogeneity. Adv Exp Med Biol 2019; 1123: 71-94.
[http://dx.doi.org/10.1007/978-3-030-11096-3_6] [PMID: 31016596]
[7]
Wobus AM, Boheler KR. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 2005; 85(2): 635-78.
[http://dx.doi.org/10.1152/physrev.00054.2003] [PMID: 15788707]
[8]
Trounson A, McDonald C. Stem cell therapies in clinical trials: progress and challenges. Cell Stem Cell 2015; 17(1): 11-22.
[http://dx.doi.org/10.1016/j.stem.2015.06.007] [PMID: 26140604]
[9]
Egusa H, Sonoyama W, Nishimura M, Atsuta I, Akiyama K. Stem cells in dentistry--Part II: clinical applications. J Prosthodont Res 2012; 56(4): 229-48.
[http://dx.doi.org/10.1016/j.jpor.2012.10.001] [PMID: 23137671]
[10]
Zhai Q, Dong Z, Wang W, Li B, Jin Y. Dental stem cell and dental tissue regeneration. Front Med 2019; 13(2): 152-9.
[http://dx.doi.org/10.1007/s11684-018-0628-x] [PMID: 29971640]
[11]
Seo BM, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004; 364(9429): 149-55.
[http://dx.doi.org/10.1016/S0140-6736(04)16627-0] [PMID: 15246727]
[12]
Cordeiro MM, Dong Z, Kaneko T, et al. Dental pulp tissue engineering with stem cells from exfoliated deciduous teeth. J Endod 2008; 34(8): 962-9.
[http://dx.doi.org/10.1016/j.joen.2008.04.009] [PMID: 18634928]
[13]
Yamamoto A, Sakai K, Matsubara K, Kano F, Ueda M. Multifaceted neuro-regenerative activities of human dental pulp stem cells for functional recovery after spinal cord injury. Neurosci Res 2014; 78: 16-20.
[http://dx.doi.org/10.1016/j.neures.2013.10.010] [PMID: 24252618]
[14]
Wang J, Wang X, Sun Z, et al. Stem cells from human-exfoliated deciduous teeth can differentiate into dopaminergic neuron-like cells. Stem Cells Dev 2010; 19(9): 1375-83.
[http://dx.doi.org/10.1089/scd.2009.0258] [PMID: 20131979]
[15]
Silvério KG, Rodrigues TL, Coletta RD, et al. Mesenchymal stem cell properties of periodontal ligament cells from deciduous and permanent teeth. J Periodontol 2010; 81(8): 1207-15.
[http://dx.doi.org/10.1902/jop.2010.090729] [PMID: 20476882]
[16]
Chen FM, Sun HH, Lu H, Yu Q. Stem cell-delivery therapeutics for periodontal tissue regeneration. Biomaterials 2012; 33(27): 6320-44.
[http://dx.doi.org/10.1016/j.biomaterials.2012.05.048] [PMID: 22695066]
[17]
Park CH, Rios HF, Jin Q, et al. Tissue engineering bone-ligament complexes using fiber-guiding scaffolds. Biomaterials 2012; 33(1): 137-45.
[http://dx.doi.org/10.1016/j.biomaterials.2011.09.057] [PMID: 21993234]
[18]
Feng F, Akiyama K, Liu Y, et al. Utility of PDL progenitors for in vivo tissue regeneration: a report of 3 cases. Oral Dis 2010; 16(1): 20-8.
[http://dx.doi.org/10.1111/j.1601-0825.2009.01593.x] [PMID: 20355278]
[19]
Kim HS, Kim KH, Kim SH, et al. Immunomodulatory effect of canine periodontal ligament stem cells on allogenic and xenogenic peripheral blood mononuclear cells. J Periodontal Implant Sci 2010; 40(6): 265-70.
[http://dx.doi.org/10.5051/jpis.2010.40.6.265] [PMID: 21246016]
[20]
Han N, Zhang F, Li G, et al. Local application of IGFBP5 protein enhanced periodontal tissue regeneration via increasing the migration, cell proliferation and osteo/dentinogenic differentiation of mesenchymal stem cells in an inflammatory niche. Stem Cell Res Ther 2017; 8(1): 210.
[http://dx.doi.org/10.1186/s13287-017-0663-6] [PMID: 28962660]
[21]
Sonoyama W, Liu Y, Fang D, et al. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One 2006; 1e79
[http://dx.doi.org/10.1371/journal.pone.0000079] [PMID: 17183711]
[22]
Morsczeck C, Götz W, Schierholz J, et al. Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 2005; 24(2): 155-65.
[http://dx.doi.org/10.1016/j.matbio.2004.12.004] [PMID: 15890265]
[23]
Derubeis AR, Cancedda R. Bone marrow stromal cells (BMSCs) in bone engineering: limitations and recent advances. Ann Biomed Eng 2004; 32(1): 160-5.
[http://dx.doi.org/10.1023/B:ABME.0000007800.89194.95] [PMID: 14964731]
[24]
Lombaert IM, Brunsting JF, Wierenga PK, et al. Rescue of salivary gland function after stem cell transplantation in irradiated glands. PLoS One 2008; 3(4)e2063
[http://dx.doi.org/10.1371/journal.pone.0002063] [PMID: 18446241]
[25]
Matsumoto S, Okumura K, Ogata A, et al. Isolation of tissue progenitor cells from duct-ligated salivary glands of swine. Cloning Stem Cells 2007; 9(2): 176-90.
[http://dx.doi.org/10.1089/clo.2006.0022] [PMID: 17579551]
[26]
Chen H, Fu H, Wu X, Duan Y, Zhang S, Hu H, et al. Regeneration of pulpo-dentinal-like complex by a group of unique multipotent CD24a(+) stem cells. Sci Adv 2020; 6(15): 1514.
[http://dx.doi.org/10.1126/sciadv.aay1514] [PMID: 32284993]
[27]
Orkin SH, Hochedlinger K. Chromatin connections to pluripotency and cellular reprogramming. Cell 2011; 145(6): 835-50.
[http://dx.doi.org/10.1016/j.cell.2011.05.019] [PMID: 21663790]
[28]
Kim K, Doi A, Wen B, et al. Epigenetic memory in induced pluripotent stem cells. Nature 2010; 467(7313): 285-90.
[http://dx.doi.org/10.1038/nature09342] [PMID: 20644535]
[29]
Silva M, Daheron L, Hurley H, et al. Generating iPSCs: translating cell reprogramming science into scalable and robust biomanufacturing strategies. Cell Stem Cell 2015; 16(1): 13-7.
[http://dx.doi.org/10.1016/j.stem.2014.12.013] [PMID: 25575079]
[30]
Nakagawa M, Takizawa N, Narita M, Ichisaka T, Yamanaka S. Promotion of direct reprogramming by transformation-deficient Myc. Proc Natl Acad Sci USA 2010; 107(32): 14152-7.
[http://dx.doi.org/10.1073/pnas.1009374107] [PMID: 20660764]
[31]
Yan X, Qin H, Qu C, Tuan RS, Shi S, Huang GT. iPS cells reprogrammed from human mesenchymal-like stem/progenitor cells of dental tissue origin. Stem Cells Dev 2010; 19(4): 469-80.
[http://dx.doi.org/10.1089/scd.2009.0314] [PMID: 19795982]
[32]
Amabile G, Meissner A. Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol Med 2009; 15(2): 59-68.
[http://dx.doi.org/10.1016/j.molmed.2008.12.003] [PMID: 19162546]
[33]
Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318(5858): 1917-20.
[http://dx.doi.org/10.1126/science.1151526] [PMID: 18029452]
[34]
Egusa H, Okita K, Kayashima H, et al. Gingival fibroblasts as a promising source of induced pluripotent stem cells. PLoS One 2010; 5(9)e12743
[http://dx.doi.org/10.1371/journal.pone.0012743] [PMID: 20856871]
[35]
Eming SA, Martin P, Tomic-Canic M. Wound repair and regeneration: mechanisms, signaling, and translation. Sci Transl Med 2014; 6(265)265sr6
[http://dx.doi.org/10.1126/scitranslmed.3009337] [PMID: 25473038]
[36]
Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003; 83(3): 835-70.
[http://dx.doi.org/10.1152/physrev.2003.83.3.835] [PMID: 12843410]
[37]
Ahmed GM, Abouauf EA, AbuBakr N, Dörfer CE, El-Sayed KF. Tissue engineering approaches for enamel, dentin, and pulp regeneration: an update. Stem Cells Int 2020; 20205734539
[http://dx.doi.org/10.1155/2020/5734539] [PMID: 32184832]
[38]
Berardinelli P, Valbonetti L, Muttini A, et al. Role of amniotic fluid mesenchymal cells engineered on MgHA/collagen-based scaffold allotransplanted on an experimental animal study of sinus augmentation. Clin Oral Investig 2013; 17(7): 1661-75.
[http://dx.doi.org/10.1007/s00784-012-0857-3] [PMID: 23064983]
[39]
Choi JY, Lai JK, Xiong ZM, et al. Diminished canonical β-catenin signaling during osteoblast differentiation contributes to osteopenia in progeria. J Bone Miner Res 2018; 33(11): 2059-70.
[http://dx.doi.org/10.1002/jbmr.3549] [PMID: 30001457]
[40]
Tetè S, Vinci R, Zizzari VL, et al. Maxillary sinus augmentation procedures through equine-derived biomaterial or calvaria autologous bone: immunohistochemical evaluation of OPG/RANKL in humans. Eur J Histochem 2013; 57(1)e10
[http://dx.doi.org/10.4081/ejh.2013.e10] [PMID: 23549459]
[41]
Karring T, Nyman S, Gottlow J, Laurell L. Development of the biological concept of guided tissue regeneration--animal and human studies. Periodontol 2000 1993; 1(1): 26-35.
[http://dx.doi.org/10.1111/j.1600-0757.1993.tb00204.x] [PMID: 8401858]
[42]
Crespi R, Capparè P, Gherlone E. Dental implants placed in extraction sites grafted with different bone substitutes: radiographic evaluation at 24 months. J Periodontol 2009; 80(10): 1616-21.
[http://dx.doi.org/10.1902/jop.2009.090156] [PMID: 19792851]
[43]
Kubo T, Doi K, Hayashi K, et al. Comparative evaluation of bone regeneration using spherical and irregularly shaped granules of interconnected porous hydroxylapatite. A beagle dog study. J Prosthodont Res 2011; 55(2): 104-9.
[http://dx.doi.org/10.1016/j.jpor.2010.10.001] [PMID: 21300584]
[44]
Crespi R, Capparé P, Romanos GE, Mariani E, Benasciutti E, Gherlone E. Corticocancellous porcine bone in the healing of human extraction sockets: combining histomorphometry with osteoblast gene expression profiles in vivo. Int J Oral Maxillofac Implants 2011; 26(4): 866-72.
[PMID: 21841997]
[45]
Long F. Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol 2011; 13(1): 27-38.
[http://dx.doi.org/10.1038/nrm3254] [PMID: 22189423]
[46]
Teti A. Bone development: overview of bone cells and signaling. Curr Osteoporos Rep 2011; 9(4): 264-47.
[PMID: 22007726]
[47]
Orhan EO, Maden M, Senguuven B. Odontoblast-like cell numbers and reparative dentine thickness after direct pulp capping with platelet-rich plasma and enamel matrix derivative: a histomorphometric evaluation. Int Endod J 2012; 45(4): 317-25.
[PMID: 22007726]
[48]
Urist MR. Bone: formation by autoinduction. Science 1965; 150(3698): 893-9.
[http://dx.doi.org/10.1126/science.150.3698.893] [PMID: 5319761]
[49]
Duprez DM, Coltey M, Amthor H, Brickell PM, Tickle C. Bone morphogenetic protein-2 (BMP-2) inhibits muscle development and promotes cartilage formation in chick limb bud cultures. Dev Biol 1996; 174(2): 448-52.
[http://dx.doi.org/10.1006/dbio.1996.0087] [PMID: 8631514]
[50]
Becker W, Becker BE, Caffesse R. A comparison of demineralized freeze-dried bone and autologous bone to induce bone formation in human extraction sockets. J Periodontol 1994; 65(12): 1128-33.
[http://dx.doi.org/10.1902/jop.1994.65.12.1128] [PMID: 7877084]
[51]
Hu K, Olsen BR. The roles of vascular endothelial growth factor in bone repair and regeneration. Bone 2016; 91: 30-8.
[http://dx.doi.org/10.1016/j.bone.2016.06.013] [PMID: 27353702]
[52]
Majidinia M, Sadeghpour A, Yousefi B. The roles of signaling pathways in bone repair and regeneration. J Cell Physiol 2018; 233(4): 2937-48.
[http://dx.doi.org/10.1002/jcp.26042] [PMID: 28590066]
[53]
Ito H, Koefoed M, Tiyapatanaputi P, et al. Remodeling of cortical bone allografts mediated by adherent rAAV-RANKL and VEGF gene therapy. Nat Med 2005; 11(3): 291-7.
[http://dx.doi.org/10.1038/nm1190] [PMID: 15711561]
[54]
Chai J, Jin R, Yuan G, Kanter V, Miron RJ, Zhang Y. Effect of Liquid Platelet-rich Fibrin and Platelet-rich Plasma on the Regenerative Potential of Dental Pulp Cells Cultured under Inflammatory Conditions: A Comparative Analysis. J Endod 2019; 45(8): 1000-8.
[http://dx.doi.org/10.1016/j.joen.2019.04.002] [PMID: 31248700]
[55]
Chisini LA, Conde MCM, Grazioli G, et al. Bone, Periodontal and Dental Pulp Regeneration in Dentistry: A Systematic Scoping Review. Braz Dent J 2019; 30(2): 77-95.
[http://dx.doi.org/10.1590/0103-6440201902053] [PMID: 30970065]
[56]
ElSheshtawy AS, Nazzal H, El Shahawy OI, et al. The effect of platelet-rich plasma as a scaffold in regeneration/revitalization endodontics of immature permanent teeth assessed using 2-dimensional radiographs and cone beam computed tomography: a randomized controlled trial. Int Endod J 2020; 53(7): 905-21.
[http://dx.doi.org/10.1111/iej.13303] [PMID: 32249441]
[57]
Chang CC, Lin TA, Wu SY, Lin CP, Chang HH. Regeneration of Tooth with Allogenous, Autoclaved Treated Dentin Matrix with Dental Pulpal Stem Cells: An In Vivo Study. J Endod 2020; 46(9): 1256-64.
[PMID: 32505637]
[58]
Huang GT. Pulp and dentin tissue engineering and regeneration: current progress. Regen Med 2009; 4(5): 697-707.
[http://dx.doi.org/10.2217/rme.09.45] [PMID: 19761395]
[59]
Rosa V, Zhang Z, Grande RH, Nör JE. Dental pulp tissue engineering in full-length human root canals. J Dent Res 2013; 92(11): 970-5.
[http://dx.doi.org/10.1177/0022034513505772] [PMID: 24056227]
[60]
Qu T, Jing J, Ren Y, et al. Complete pulpodentin complex regeneration by modulating the stiffness of biomimetic matrix. Acta Biomater 2015; 16: 60-70.
[http://dx.doi.org/10.1016/j.actbio.2015.01.029] [PMID: 25644448]
[61]
Ma L, Makino Y, Yamaza H, et al. Cryopreserved dental pulp tissues of exfoliated deciduous teeth is a feasible stem cell resource for regenerative medicine. PLoS One 2012; 7(12)e51777
[http://dx.doi.org/10.1371/journal.pone.0051777] [PMID: 23251621]
[62]
Buduru SD, Gulei D, Zimta AA, Tigu AB, Cenariu D, Berindan-Neagoe I. The Potential of Different Origin Stem Cells in Modulating Oral Bone Regeneration Processes. Cells 2019; 8(1)E29
[http://dx.doi.org/10.3390/cells8010029] [PMID: 30625993]
[63]
Ballini A, Mastrangelo F, Gastaldi G, et al. Osteogenic differentiation and gene expression of dental pulp stem cells under low-level laser irradiation: a good promise for tissue engineering. J Biol Regul Homeost Agents 2015; 29(4): 813-22.
[PMID: 26753641]
[64]
Cattoni F, Teté G, Calloni AM, Manazza F, Gastaldi G, Capparè P. Milled versus moulded mock-ups based on the superimposition of 3D meshes from digital oral impressions: a comparative in vitro study in the aesthetic area. BMC Oral Health 2019; 19(1): 230.
[http://dx.doi.org/10.1186/s12903-019-0922-2] [PMID: 31664999]
[65]
Vinci R, Teté G, Lucchetti FR, Capparé P, Gherlone EF. Implant survival rate in calvarial bone grafts: A retrospective clinical study with 10 year follow-up. Clin Implant Dent Relat Res 2019; 21(4): 662-8.
[http://dx.doi.org/10.1111/cid.12799] [PMID: 31140209]
[66]
Sheikh Z, Hamdan N, Ikeda Y, Grynpas M, Ganss B, Glogauer M. Natural graft tissues and synthetic biomaterials for periodontal and alveolar bone reconstructive applications: a review. Biomater Res 2017; 21: 9.
[http://dx.doi.org/10.1186/s40824-017-0095-5] [PMID: 28593053]
[67]
Walmsley GG, Ransom RC, Zielins ER, et al. Stem Cells in Bone Regeneration. Stem Cell Rev Rep 2016; 12(5): 524-9.
[http://dx.doi.org/10.1007/s12015-016-9665-5] [PMID: 27250635]
[68]
Bielby RC, Boccaccini AR, Polak JM, Buttery LD. In vitro differentiation and in vivo mineralization of osteogenic cells derived from human embryonic stem cells. Tissue Eng 2004; 10(9-10): 1518-25.
[http://dx.doi.org/10.1089/ten.2004.10.1518] [PMID: 15588411]
[69]
Liu X, Wang P, Chen W, Weir MD, Bao C, Xu HH. Human embryonic stem cells and macroporous calcium phosphate construct for bone regeneration in cranial defects in rats. Acta Biomater 2014; 10(10): 4484-93.
[http://dx.doi.org/10.1016/j.actbio.2014.06.027] [PMID: 24972090]
[70]
Marolt D, Campos IM, Bhumiratana S, et al. Engineering bone tissue from human embryonic stem cells. Proc Natl Acad Sci USA 2012; 109(22): 8705-9.
[http://dx.doi.org/10.1073/pnas.1201830109] [PMID: 22586099]
[71]
Ichiyanagi T, Anabuki K, Nishijima Y, Ono H. Isolation of mesenchymal stem cells from bone marrow wastes of spinal fusion procedure (TLIF) for low back pain patients and preparation of bone dusts for transplantable autologous bone graft with a serum glue. Biosci Trends 2010; 4(3): 110-8.
[PMID: 20592461]
[72]
Massa A, Perut F, Chano T, et al. The effect of extracellular acidosis on the behaviour of mesenchymal stem cells in vitro. Eur Cell Mater 2017; 33: 252-67.
[http://dx.doi.org/10.22203/eCM.v033a19] [PMID: 28368079]
[73]
Yusa K, Yamamoto O, Iino M, et al. Eluted zinc ions stimulate osteoblast differentiation and mineralization in human dental pulp stem cells for bone tissue engineering. Arch Oral Biol 2016; 71: 162-9.
[http://dx.doi.org/10.1016/j.archoralbio.2016.07.010] [PMID: 27521529]
[74]
Zorin VL, Komlev VS, Zorina AI, et al. Octacalcium phosphate ceramics combined with gingiva-derived stromal cells for engineered functional bone grafts. Biomed Mater 2014; 9(5)055005
[http://dx.doi.org/10.1088/1748-6041/9/5/055005] [PMID: 25167539]
[75]
Cai X, Yang F, Yan X, et al. Influence of bone marrow-derived mesenchymal stem cells pre-implantation differentiation approach on periodontal regeneration in vivo. J Clin Periodontol 2015; 42(4): 380-9.
[http://dx.doi.org/10.1111/jcpe.12379] [PMID: 25692209]
[76]
Peterkova R, Hovorakova M, Peterka M, Lesot H. Three-dimensional analysis of the early development of the dentition. Aust Dent J 2014; 59(Suppl. 1): 55-80.
[http://dx.doi.org/10.1111/adj.12130] [PMID: 24495023]
[77]
Li Q, Zhang S, Sui Y, Fu X, Li Y, Wei S. Sequential stimulation with different concentrations of BMP4 promotes the differentiation of human embryonic stem cells into dental epithelium with potential for tooth formation. Stem Cell Res Ther 2019; 10(1): 276.
[http://dx.doi.org/10.1186/s13287-019-1378-7] [PMID: 31464646]
[78]
Duailibi SE, Duailibi MT, Vacanti JP, Yelick PC. Prospects for tooth regeneration. Periodontol 2000 2006; 41: 177-87.
[http://dx.doi.org/10.1111/j.1600-0757.2006.00165.x] [PMID: 16686933]
[79]
Komine A, Suenaga M, Nakao K, Tsuji T, Tomooka Y. Tooth regeneration from newly established cell lines from a molar tooth germ epithelium. Biochem Biophys Res Commun 2007; 355(3): 758-63.
[http://dx.doi.org/10.1016/j.bbrc.2007.02.039] [PMID: 17321500]
[80]
Anderson TR, Toverud SU, Yung RC, Hanks MH, Palik JF. Separation and partial purification of acid phosphates of the enamel organ of rat molars. Arch Oral Biol 1982; 27(2): 129-32.
[http://dx.doi.org/10.1016/0003-9969(82)90132-7] [PMID: 6952825]
[81]
Ning F, Guo Y, Tang J, et al. Differentiation of mouse embryonic stem cells into dental epithelial-like cells induced by ameloblasts serum-free conditioned medium. Biochem Biophys Res Commun 2010; 394(2): 342-7.
[http://dx.doi.org/10.1016/j.bbrc.2010.03.007] [PMID: 20206604]
[82]
Cai J, Zhang Y, Liu P, et al. Generation of tooth-like structures from integration-free human urine induced pluripotent stem cells. Cell Regen (Lond) 2013; 2(1): 6.
[http://dx.doi.org/10.1186/2045-9769-2-6] [PMID: 25408878]
[83]
An Z, Sabalic M, Bloomquist RF, Fowler TE, Streelman T, Sharpe PT. A quiescent cell population replenishes mesenchymal stem cells to drive accelerated growth in mouse incisors. Nat Commun 2018; 9(1): 378.
[http://dx.doi.org/10.1038/s41467-017-02785-6] [PMID: 29371677]
[84]
Sonoyama W, Liu Y, Yamaza T, et al. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 2008; 34(2): 166-71.
[http://dx.doi.org/10.1016/j.joen.2007.11.021] [PMID: 18215674]
[85]
Huang XF, Chai Y. Molecular regulatory mechanism of tooth root development. Int J Oral Sci 2012; 4(4): 177-81.
[http://dx.doi.org/10.1038/ijos.2012.61] [PMID: 23222990]
[86]
Piva E, Tarlé SA, Nör JE, et al. Dental Pulp tissue regeneration using dental pulp stem cells isolated and expanded in human serum. J Endod 2017; 43(4): 568-74.
[http://dx.doi.org/10.1016/j.joen.2016.11.018] [PMID: 28216268]
[87]
Kim JH, Jeon M, Song JS, et al. Distinctive genetic activity pattern of the human dental pulp between deciduous and permanent teeth. PLoS One 2014; 9(7)e102893
[http://dx.doi.org/10.1371/journal.pone.0102893] [PMID: 25047033]
[88]
Lu X, Liu SF, Wang HH, et al. A biological study of supernumerary teeth derived dental pulp stem cells based on RNA-seq analysis. Int Endod J 2019; 52(6): 819-28.
[http://dx.doi.org/10.1111/iej.13060] [PMID: 30565714]
[89]
Needleman IG, Worthington HV, Giedrys-Leeper E, Tucker RJ. Guided tissue regeneration for periodontal infra-bony defects. Cochrane Database Syst Rev 2006; 2CD001724
[http://dx.doi.org/10.1002/14651858.CD001724.pub2] [PMID: 16625546]
[90]
Sculean A, Chapple IL, Giannobile WV. Wound models for periodontal and bone regeneration: the role of biologic research. Periodontol 2000 2015; 68(1): 7-20.
[http://dx.doi.org/10.1111/prd.12091] [PMID: 25867976]
[91]
Tobita M, Mizuno H. Adipose-derived stem cells and periodontal tissue engineering. Int J Oral Maxillofac Implants 2013; 28(6): e487-93.
[http://dx.doi.org/10.11607/jomi.te29] [PMID: 24278946]
[92]
Kinnaird T, Stabile E, Burnett MS, et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 2004; 109(12): 1543-9.
[http://dx.doi.org/10.1161/01.CIR.0000124062.31102.57] [PMID: 15023891]
[93]
Pierdomenico L, Bonsi L, Calvitti M, et al. Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 2005; 80(6): 836-42.
[http://dx.doi.org/10.1097/01.tp.0000173794.72151.88] [PMID: 16210973]
[94]
Ding G, Liu Y, Wang W, et al. Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells 2010; 28(10): 1829-38.
[http://dx.doi.org/10.1002/stem.512] [PMID: 20979138]
[95]
Du J, Shan Z, Ma P, Wang S, Fan Z. Allogeneic bone marrow mesenchymal stem cell transplantation for periodontal regeneration. J Dent Res 2014; 93(2): 183-8.
[http://dx.doi.org/10.1177/0022034513513026] [PMID: 24226426]
[96]
Nosrat IV, Smith CA, Mullally P, Olson L, Nosrat CA. Dental pulp cells provide neurotrophic support for dopaminergic neurons and differentiate into neurons in vitro; implications for tissue engineering and repair in the nervous system. Eur J Neurosci 2004; 19(9): 2388-98.
[http://dx.doi.org/10.1111/j.0953-816X.2004.03314.x] [PMID: 15128393]
[97]
Denny PC, Denny PA. Dynamics of parenchymal cell division, differentiation, and apoptosis in the young adult female mouse submandibular gland. Anat Rec 1999; 254(3): 408-17.
[http://dx.doi.org/10.1002/(SICI)1097-0185(19990301)254:3<408:AID-AR12>3.0.CO;2-G] [PMID: 10096673]
[98]
Kishi T, Takao T, Fujita K, Taniguchi H. Clonal proliferation of multipotent stem/progenitor cells in the neonatal and adult salivary glands. Biochem Biophys Res Commun 2006; 340(2): 544-52.
[http://dx.doi.org/10.1016/j.bbrc.2005.12.031] [PMID: 16376857]
[99]
Wada N, Wang B, Lin NH, Laslett AL, Gronthos S, Bartold PM. Induced pluripotent stem cell lines derived from human gingival fibroblasts and periodontal ligament fibroblasts. J Periodontal Res 2011; 46(4): 438-7.
[PMID: 26084043]
[100]
Umezaki Y, Hashimoto Y, Nishishita N, Kawamata S, Baba S. Human gingival integration-free ipscs; a source for MSC-Like Cells. Int J Mol Sci 2015; 16(6): 13633-48.
[PMID: 26084043]
[101]
Zhou W, Freed CR. Adenoviral gene delivery can reprogram human fibroblasts to induced pluripotent stem cells. Stem Cells 2009; 27(11): 2667-74.
[http://dx.doi.org/10.1002/stem.201] [PMID: 19697349]
[102]
Yoshida K, Sato J, Takai R, et al. Differentiation of mouse iPS cells into ameloblast-like cells in cultures using medium conditioned by epithelial cell rests of Malassez and gelatin-coated dishes. Med Mol Morphol 2015; 48(3): 138-45.
[http://dx.doi.org/10.1007/s00795-014-0088-6] [PMID: 25319805]
[103]
Liu L, Liu YF, Zhang J, Duan YZ, Jin Y. Ameloblasts serum-free conditioned medium: bone morphogenic protein 4-induced odontogenic differentiation of mouse induced pluripotent stem cells. J Tissue Eng Regen Med 2016; 10(6): 466-74.
[http://dx.doi.org/10.1002/term.1742] [PMID: 23606575]
[104]
Lee JI, Kang SJ, Jeon SP, Sun H. Stafne bone cavity of the mandible. Arch Craniofac Surg 2016; 17(3): 162-4.
[http://dx.doi.org/10.7181/acfs.2016.17.3.162] [PMID: 28913275]
[105]
Xie H, Dubey N, Shim W, et al. Functional odontoblastic-like cells derived from human iPSCs. J Dent Res 2018; 97(1): 77-83.
[http://dx.doi.org/10.1177/0022034517730026] [PMID: 28898112]
[106]
Sedlaczek J, Lohmann CH, Lotz EM, Hyzy SL, Boyan BD, Schwartz Z. Effects of low-frequency ultrasound treatment of titanium surface roughness on osteoblast phenotype and maturation. Clin Oral Implants Res 2017; 28(10): e151-8.
[http://dx.doi.org/10.1111/clr.12976] [PMID: 27596293]
[107]
Seki D, Takeshita N, Oyanagi T, et al. Differentiation of odontoblast-like cells from mouse induced pluripotent stem cells by pax9 and bmp4 transfection. Stem Cells Transl Med 2015; 4(9): 993-7.
[http://dx.doi.org/10.5966/sctm.2014-0292] [PMID: 26136503]
[108]
Xiao L, Ide R, Saiki C, Kumazawa Y, Okamura H. Human dental pulp cells differentiate toward neuronal cells and promote neuroregeneration in adult organotypic hippocampal slices in vitro. Int J Mol Sci 2017; 18(8)E1745
[http://dx.doi.org/10.3390/ijms18081745] [PMID: 28800076]
[109]
Malhotra N. Induced pluripotent stem (iPS) cells in dentistry: a review. Int J Stem Cells 2016; 9(2): 176-85.
[PMID: 27572712]
[110]
Duan X, Tu Q, Zhang J, et al. Application of induced pluripotent stem (iPS) cells in periodontal tissue regeneration. J Cell Physiol 2011; 226(1): 150-7.
[http://dx.doi.org/10.1002/jcp.22316] [PMID: 20658533]
[111]
Ono H, Obana A, Usami Y, et al. Regenerating salivary glands in the microenvironment of induced pluripotent stem cells. BioMed Res Int 2015; 2015293570
[http://dx.doi.org/10.1155/2015/293570] [PMID: 26185754]
[112]
Heffernan C, Sumer H, Verma PJ. Generation of clinically relevant “induced pluripotent stem” (iPS) cells. J Stem Cells 2011; 6(3): 109-27.
[PMID: 23264997]
[113]
Egusa H, Kayashima H, Miura J, et al. Comparative analysis of mouse-induced pluripotent stem cells and mesenchymal stem cells during osteogenic differentiation in vitro. Stem Cells Dev 2014; 23(18): 2156-69.
[http://dx.doi.org/10.1089/scd.2013.0344] [PMID: 24625139]
[114]
Polo JM, Liu S, Figueroa ME, Kulalert W, Eminli S, Tan KY, et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol 2010; 28(8): 848-55.
[PMID: 21726830]
[115]
Bar-Nur O, Russ HA, Efrat S, Benvenisty N. Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells. Cell Stem Cell 2011; 9(1): 17-23.
[PMID: 21726830]
[116]
Stadtfeld M, Apostolou E, Akutsu H, et al. Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 2010; 465(7295): 175-81.
[http://dx.doi.org/10.1038/nature09017] [PMID: 20418860]
[117]
Ma H, Morey R, O’Neil RC, et al. Abnormalities in human pluripotent cells due to reprogramming mechanisms. Nature 2014; 511(7508): 177-83.
[http://dx.doi.org/10.1038/nature13551] [PMID: 25008523]
[118]
Schuldiner M, Itskovitz-Eldor J, Benvenisty N. Selective ablation of human embryonic stem cells expressing a “suicide” gene. Stem Cells 2003; 21(3): 257-65.
[http://dx.doi.org/10.1634/stemcells.21-3-257] [PMID: 12743320]
[119]
Ben-David U, Gan QF, Golan-Lev T, et al. Selective elimination of human pluripotent stem cells by an oleate synthesis inhibitor discovered in a high-throughput screen. Cell Stem Cell 2013; 12(2): 167-79.
[http://dx.doi.org/10.1016/j.stem.2012.11.015] [PMID: 23318055]
[120]
Ben-David U, Gan QF, Golan-Lev T, et al. Selective elimination of human pluripotent stem cells by an oleate synthesis inhibitor discovered in a high-throughput screen. Cell Stem Cell 2013; 12(2): 167-79.
[http://dx.doi.org/10.1016/j.stem.2012.11.015] [PMID: 23318055]
[121]
Okita K, Matsumura Y, Sato Y, et al. A more efficient method to generate integration-free human iPS cells. Nat Methods 2011; 8(5): 409-12.
[http://dx.doi.org/10.1038/nmeth.1591] [PMID: 21460823]
[122]
Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008; 322(5903): 949-53.
[http://dx.doi.org/10.1126/science.1164270] [PMID: 18845712]
[123]
Kim D, Kim CH, Moon JI, et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009; 4(6): 472-6.
[http://dx.doi.org/10.1016/j.stem.2009.05.005] [PMID: 19481515]
[124]
Ebert AD, Liang P, Wu JC. Induced pluripotent stem cells as a disease modeling and drug screening platform. J Cardiovasc Pharmacol 2012; 60(4): 408-16.
[http://dx.doi.org/10.1097/FJC.0b013e318247f642] [PMID: 22240913]
[125]
Nakao K, Morita R, Saji Y, et al. The development of a bioengineered organ germ method. Nat Methods 2007; 4(3): 227-30.
[http://dx.doi.org/10.1038/nmeth1012] [PMID: 17322892]
[126]
Nait Lechguer A, Couble ML, Labert N, et al. Cell differentiation and matrix organization in engineered teeth. J Dent Res 2011; 90(5): 583-9.
[http://dx.doi.org/10.1177/0022034510391796] [PMID: 21297012]
[127]
Nait Lechguer A, Kuchler-Bopp S, Hu B, Haïkel Y, Lesot H. Vascularization of engineered teeth. J Dent Res 2008; 87(12): 1138-43.
[http://dx.doi.org/10.1177/154405910808701216] [PMID: 19029082]
[128]
Ohazama A, Sharpe PT. TNF signalling in tooth development. Curr Opin Genet Dev 2004; 14(5): 513-9.
[http://dx.doi.org/10.1016/j.gde.2004.07.008]
[129]
Zhang Q, Shi S, Liu Y, et al. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 2009; 183(12): 7787-98.
[http://dx.doi.org/10.4049/jimmunol.0902318] [PMID: 19923445]
[130]
Rasmusson I, Uhlin M, Le Blanc K, Levitsky V. Mesenchymal stem cells fail to trigger effector functions of cytotoxic T lymphocytes. J Leukoc Biol 2007; 82(4): 887-93.
[http://dx.doi.org/10.1189/jlb.0307140] [PMID: 17609339]
[131]
Yamaza T, Kentaro A, Chen C, et al. Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Res Ther 2010; 1(1): 5.
[http://dx.doi.org/10.1186/scrt5] [PMID: 20504286]
[132]
Davies LC, Lönnies H, Locke M, et al. Oral mucosal progenitor cells are potently immunosuppressive in a dose-independent manner. Stem Cells Dev 2012; 21(9): 1478-87.
[http://dx.doi.org/10.1089/scd.2011.0434] [PMID: 21988324]


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VOLUME: 20
ISSUE: 4
Year: 2020
Page: [259 - 268]
Pages: 10
DOI: 10.2174/1566523220999200818115803

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