Comparison of Periodontal Ligament Stem Cells with Mesenchymal Stem Cells from Other Sources: A Scoping Systematic Review of In vitro and In vivo Studies
- Authors: Kadkhoda Z.1, Motie P.2, Rad M.3, Mohaghegh S.4, Kouhestani F.5, Motamedian S.6
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Affiliations:
- Department of Periodontology, School of Dentistry,, Shahid Beheshti University of Medical Science
- OrthStudent Research Committee, School of Dentistryodontics, Shahid Beheshti University of Medical Science
- Dental Research Center, Research Institute of Dental Sciences, School of Dentistry, Shahid Beheshti University of Medical Sciences
- Student Research Committee, School of Dentistry,, Shahid Beheshti University of Medical Science
- Department of Periodontics, School of Dentistry,, Bushehr University of Medical Sciences
- Dentofacial Deformities Research Center, Research Institute of Dental Sciences, Department of Orthodontics, School of Dentistry, Shahid Beheshti University of Medical Sciences
- Issue: Vol 19, No 4 (2024)
- Pages: 497-522
- Section: Medicine
- URL: https://rjpbr.com/1574-888X/article/view/645792
- DOI: https://doi.org/10.2174/1574888X17666220429123319
- ID: 645792
Cite item
Full Text
Abstract
Objective:The application of stem cells in regenerative medicine depends on their biological properties. This scoping review aimed to compare the features of periodontal ligament stem cells (PDLSSCs) with stem cells derived from other sources.
Design:An electronic search in PubMed/Medline, Embase, Scopus, Google Scholar and Science Direct was conducted to identify in vitro and in vivo studies limited to English language.
Results:Overall, 65 articles were included. Most comparisons were made between bone marrow stem cells (BMSCs) and PDLSCs. BMSCs were found to have lower proliferation and higher osteogenesis potential in vitro and in vivo than PDLSCs; on the contrary, dental follicle stem cells and umbilical cord mesenchymal stem cells (UCMSCs) had a higher proliferative ability and lower osteogenesis than PDLSCs. Moreover, UCMSCs exhibited a higher apoptotic rate, hTERT expression, and relative telomerase length. The immunomodulatory function of adipose-derived stem cells and BMSCs was comparable to PDLSCs. Gingival mesenchymal stem cells showed less sensitivity to long-term culture. Both pure and mixed gingival cells had lower osteogenic ability compared to PDLSCs. Comparison of dental pulp stem cells (DPSCs) with PDLSCs regarding proliferation rate, osteo/adipogenesis, and immunomodulatory properties was contradictory; however, in vivo bone formation of DPSCs seemed to be lower than PDLSCs.
Conclusion:In light of the performed comparative studies, PDLSCs showed comparable results to stem cells derived from other sources; however, further in vivo studies are needed to determine the actual pros and cons of stem cells in comparison to each other.
About the authors
Zeinab Kadkhoda
Department of Periodontology, School of Dentistry,, Shahid Beheshti University of Medical Science
Email: info@benthamscience.net
Parisa Motie
OrthStudent Research Committee, School of Dentistryodontics, Shahid Beheshti University of Medical Science
Email: info@benthamscience.net
Maryam Rad
Dental Research Center, Research Institute of Dental Sciences, School of Dentistry, Shahid Beheshti University of Medical Sciences
Email: info@benthamscience.net
Sadra Mohaghegh
Student Research Committee, School of Dentistry,, Shahid Beheshti University of Medical Science
Email: info@benthamscience.net
Farnaz Kouhestani
Department of Periodontics, School of Dentistry,, Bushehr University of Medical Sciences
Email: info@benthamscience.net
Saeed Motamedian
Dentofacial Deformities Research Center, Research Institute of Dental Sciences, Department of Orthodontics, School of Dentistry, Shahid Beheshti University of Medical Sciences
Author for correspondence.
Email: info@benthamscience.net
References
- Niibe K, Zhang M, Nakazawa K, et al. The potential of enriched mesenchymal stem cells with neural crest cell phenotypes as a cell source for regenerative dentistry. Jpn Dent Sci Rev 2017; 53(2): 25-33. doi: 10.1016/j.jdsr.2016.09.001 PMID: 28479933
- Chen Q, Shou P, Zheng C, et al. Fate decision of mesenchymal stem cells: Adipocytes or osteoblasts? Cell Death Differ 2016; 23(7): 1128-39. doi: 10.1038/cdd.2015.168 PMID: 26868907
- Almalki SG, Agrawal DK. Key transcription factors in the differentiation of mesenchymal stem cells. Differentiation; research in biological diversity 2016; 92(1-2): 41-51.
- Fang CH, Jin J, Joe JH, et al. In vivo differentiation of human amniotic epithelial cells into cardiomyocyte-like cells and cell transplantation effect on myocardial infarction in rats: Comparison with cord blood and adipose tissue-derived mesenchymal stem cells. Cell Transplant 2012; 21(8): 1687-96. doi: 10.3727/096368912X653039 PMID: 22776022
- Krampera M, Marconi S, Pasini A, et al. Induction of neural-like differentiation in human mesenchymal stem cells derived from bone marrow, fat, spleen and thymus. Bone 2007; 40(2): 382-90. doi: 10.1016/j.bone.2006.09.006 PMID: 17049329
- Fox IJ, Strom SC. To be or not to be: Generation of hepatocytes from cells outside the liver. Gastroenterology 2008; 134(3): 878-81. doi: 10.1053/j.gastro.2008.01.065 PMID: 18325397
- Langer R, Vacanti JP. Tissue engineering. Science 1993; 260(5110): 920-6. doi: 10.1126/science.8493529 PMID: 8493529
- Caplan AI. Why are MSCs therapeutic? New data: New insight. J Pathol 2009; 217(2): 318-24. doi: 10.1002/path.2469 PMID: 19023885
- Abedian Z, Jenabian N, Moghadamnia AA, et al. A comparative study on immunophenotypic characterization and osteogenic differentiation of human mesenchymal stromal cells derived from periodontal ligament and gingiva. J Periodontol 2020; 91(9): 1194-202. doi: 10.1002/JPER.19-0535 PMID: 31960428
- Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 2000; 97(25): 13625-30. doi: 10.1073/pnas.240309797 PMID: 11087820
- Miura M, Gronthos S, Zhao M, et al. SHED: Stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 2003; 100(10): 5807-12. doi: 10.1073/pnas.0937635100 PMID: 12716973
- Seo BM, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004; 364(9429): 149-55. doi: 10.1016/S0140-6736(04)16627-0 PMID: 15246727
- Sonoyama W, Liu Y, Fang D, et al. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One 2006; 1(1): e79. doi: 10.1371/journal.pone.0000079 PMID: 17183711
- Egusa H, Sonoyama W, Nishimura M, Atsuta I, Akiyama K. Stem cells in dentistry-part I: Stem cell sources. J Prosthodont Res 2012; 56(3): 151-65. doi: 10.1016/j.jpor.2012.06.001 PMID: 22796367
- Tomokiyo A, Wada N, Maeda H. Periodontal Ligament Stem Cells: Regenerative Potency in Periodontium. Stem Cells Dev 2019; 28(15): 974-85. doi: 10.1089/scd.2019.0031 PMID: 31215350
- Moher D, Shamseer L, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 2015; 4(1): 1-9. doi: 10.1186/2046-4053-4-1 PMID: 25554246
- Gay IC, Chen S, MacDougall M. Isolation and characterization of multipotent human periodontal ligament stem cells. Orthod Craniofac Res 2007; 10(3): 149-60. doi: 10.1111/j.1601-6343.2007.00399.x PMID: 17651131
- Wang L, Shen H, Zheng W, et al. Characterization of stem cells from alveolar periodontal ligament. Tissue Eng Part A 2011; 17(7-8): 1015-26. doi: 10.1089/ten.tea.2010.0140 PMID: 21186958
- Gao LN, An Y, Lei M, et al. The effect of the coumarin-like derivative osthole on the osteogenic properties of human periodontal ligament and jaw bone marrow mesenchymal stem cell sheets. Biomaterials 2013; 34(38): 9937-51. doi: 10.1016/j.biomaterials.2013.09.017 PMID: 24095254
- Zhu B, Liu W, Zhang H, et al. Tissue-specific composite cell aggregates drive periodontium tissue regeneration by reconstructing a regenerative microenvironment. J Tissue Eng Regen Med 2017; 11(6): 1792-805. doi: 10.1002/term.2077 PMID: 26455905
- Jo YY, Lee HJ, Kook SY, et al. Isolation and characterization of postnatal stem cells from human dental tissues. Tissue Eng 2007; 13(4): 767-73. doi: 10.1089/ten.2006.0192 PMID: 17432951
- Zhang Y, Xing Y, Jia L, et al. An in vitro comparative study of multisource derived human mesenchymal stem cells for bone tissue engineering. Stem Cells Dev 2018; 27(23): 1634-45. doi: 10.1089/scd.2018.0119 PMID: 30234437
- Tamaki Y, Nakahara T, Ishikawa H, Sato S. In vitro analysis of mesenchymal stem cells derived from human teeth and bone marrow. Odontology / the Society of the Nippon Dental University 2013; 101(2): 121-32.
- Eleuterio E, Trubiani O, Sulpizio M, et al. Proteome of human stem cells from periodontal ligament and dental pulp. PLoS One 2013; 8(8): e71101. doi: 10.1371/journal.pone.0071101 PMID: 23940696
- Song JS, Kim SO, Kim SH, et al. In vitro and in vivo characteristics of stem cells derived from the periodontal ligament of human deciduous and permanent teeth. Tissue Eng Part A 2012; 18(19-20): 2040-51. doi: 10.1089/ten.tea.2011.0318 PMID: 22571499
- Pettersson LF, Kingham PJ, Wiberg M, Kelk P. In vitro osteogenic differentiation of human mesenchymal stem cells from jawbone compared with dental tissue. Tissue Eng Regen Med 2017; 14(6): 763-74. doi: 10.1007/s13770-017-0071-0 PMID: 30603526
- Lin NH, Menicanin D, Mrozik K, Gronthos S, Bartold PM. Putative stem cells in regenerating human periodontium. J Periodontal Res 2008; 43(5): 514-23. doi: 10.1111/j.1600-0765.2007.01061.x PMID: 18624941
- Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 2009; 219(3): 667-76. doi: 10.1002/jcp.21710 PMID: 19160415
- Vasandan AB, Shankar SR, Prasad P, Sowmya Jahnavi V, Bhonde RR, Jyothi Prasanna S. Functional differences in mesenchymal stromal cells from human dental pulp and periodontal ligament. J Cell Mol Med 2014; 18(2): 344-54. doi: 10.1111/jcmm.12192 PMID: 24393246
- Iwata T, Yamato M, Zhang Z, et al. Validation of human periodontal ligament-derived cells as a reliable source for cytotherapeutic use. J Clin Periodontol 2010; 37(12): 1088-99. doi: 10.1111/j.1600-051X.2010.01597.x PMID: 20618549
- Foudah D, Monfrini M, Donzelli E, et al. Expression of neural markers by undifferentiated mesenchymal-like stem cells from different sources. Journal of Immunology Research 2014; 2014 doi: 10.1155/2014/987678
- Lee SJ, Yi T, Ahn SH, et al. Comparative study on metabolite level in tissue-specific human mesenchymal stem cells by an ultra-performance liquid chromatography quadrupole time of flight mass spectrometry. Anal Chim Acta 2018; 1024: 112-22. doi: 10.1016/j.aca.2018.04.018 PMID: 29776537
- Moshaverinia A, Chen C, Xu X, et al. Bone regeneration potential of stem cells derived from periodontal ligament or gingival tissue sources encapsulated in RGD-modified alginate scaffold. Tissue Eng Part A 2014; 20(3-4): 611-21. PMID: 24070211
- Trivanović D, Jauković A, Popović B, et al. Mesenchymal stem cells of different origin: Comparative evaluation of proliferative capacity, telomere length and pluripotency marker expression. Life Sci 2015; 141: 61-73. doi: 10.1016/j.lfs.2015.09.019 PMID: 26408916
- Kim JH, Jo CH, Kim HR, Hwang YI. Comparison of immunological characteristics of mesenchymal stem cells from the periodontal ligament, umbilical cord, and adipose tissue Stem Cells International 2018; (2018): doi: 10.1155/2018/8429042
- Yu S, Long J, Yu J, et al. Analysis of differentiation potentials and gene expression profiles of mesenchymal stem cells derived from periodontal ligament and Whartons jelly of the umbilical cord. Cells Tissues Organs 2013; 197(3): 209-23. doi: 10.1159/000343740 PMID: 23257615
- Shang F, Liu S, Ming L, et al. Human umbilical cord mscs as new cell sources for promoting periodontal regeneration in inflammatory periodontal defect. Theranostics 2017; 7(18): 4370-82. doi: 10.7150/thno.19888 PMID: 29158833
- Szepesi Á, Matula Z, Szigeti A, Várady G, Szalma J, Szabó G. In vitro characterization of human mesenchymal stem cells isolated from different tissues with a potential to promote complex bone regeneration Stem Cells International 2016; 2016
- Fang TJ, Wang DH, Wang CY, et al. Osteogenic prospective of deriving human dental stem cells in collagen matrix boost. J Mater Sci Mater Med 2017; 28(12): 192. doi: 10.1007/s10856-017-6001-9 PMID: 29143185
- Fujita T, Iwata T, Shiba H, et al. Identification of marker genes distinguishing human periodontal ligament cells from human mesenchymal stem cells and human gingival fibroblasts. J Periodontal Res 2007; 42(3): 283-6. doi: 10.1111/j.1600-0765.2006.00944.x PMID: 17451549
- Xing Y, Zhang Y, Wu X, Zhao B, Ji Y, Xu X. A comprehensive study on donor-matched comparisons of three types of mesenchymal stem cells-containing cells from human dental tissue. J Periodontal Res 2019; 54(3): 286-99. doi: 10.1111/jre.12630 PMID: 30474138
- Yang H, Gao L-N, An Y, et al. Comparison of mesenchymal stem cells derived from gingival tissue and periodontal ligament in different incubation conditions. Biomaterials 2013; 34(29): 7033-47. doi: 10.1016/j.biomaterials.2013.05.025 PMID: 23768902
- Santamaría S, Sanchez N, Sanz M, Garcia-Sanz JA. Comparison of periodontal ligament and gingiva-derived mesenchymal stem cells for regenerative therapies. Clin Oral Investig 2017; 21(4): 1095-102. doi: 10.1007/s00784-016-1867-3 PMID: 27270903
- Proksch S, Kirsch K, Vach K, Hellwig E, Tomakidi P. Comparative differentiation analysis of distinct oral tissue-derived cells in response to osteogenic stimulation. Clin Oral Investig 2019; 23(3): 1077-89. doi: 10.1007/s00784-018-2529-4 PMID: 29955966
- Gao Y, Zhao G, Li D, Chen X, Pang J, Ke J. Isolation and multiple differentiation potential assessment of human gingival mesenchymal stem cells. Int J Mol Sci 2014; 15(11): 20982-96. doi: 10.3390/ijms151120982 PMID: 25405732
- Otabe K, Muneta T, Kawashima N, Suda H, Tsuji K, Sekiya I. Comparison of gingiva, dental pulp, and periodontal ligament cells from the standpoint of mesenchymal stem cell properties. Cell Med 2012; 4(1): 13-21. doi: 10.3727/215517912X653319 PMID: 26858852
- Hakki SS, Kayis SA, Hakki EE, et al. Comparison of mesenchymal stem cells isolated from pulp and periodontal ligament. J Periodontol 2015; 86(2): 283-91. doi: 10.1902/jop.2014.140257 PMID: 25325708
- Navabazam AR, Sadeghian Nodoshan F, Sheikhha MH, Miresmaeili SM, Soleimani M, Fesahat F. Characterization of mesenchymal stem cells from human dental pulp, preapical follicle and periodontal ligament. Iran J Reprod Med 2013; 11(3): 235-42. PMID: 24639751
- Osman A, Gnanasegaran N, Govindasamy V, et al. Basal expression of growth-factor-associated genes in periodontal ligament stem cells reveals multiple distinctive pathways. Int Endod J 2014; 47(7): 639-51. doi: 10.1111/iej.12200 PMID: 24182326
- Wang W, Yuan C, Liu Z, et al. Characteristic comparison between canine and human dental mesenchymal stem cells for periodontal regeneration research in preclinical animal studies. Tissue Cell 2020; 67: 101405. doi: 10.1016/j.tice.2020.101405 PMID: 32835938
- Winning L, El Karim IA, Lundy FT. A comparative analysis of the osteogenic potential of dental mesenchymal stem cells. Stem Cells Dev 2019; 28(15): 1050-8. doi: 10.1089/scd.2019.0023 PMID: 31169063
- Ai T, Zhang J, Wang X, et al. DNA methylation profile is associated with the osteogenic potential of three distinct human odontogenic stem cells. Signal Transduct Target Ther 2018; 3(1): 1. doi: 10.1038/s41392-017-0001-6 PMID: 29527327
- Chen K, Xiong H, Huang Y, Liu C. Comparative analysis of in vitro periodontal characteristics of stem cells from apical papilla (SCAP) and periodontal ligament stem cells (PDLSCs). Arch Oral Biol 2013; 58(8): 997-1006. doi: 10.1016/j.archoralbio.2013.02.010 PMID: 23582988
- Kolar MK, Itte VN, Kingham PJ, Novikov LN, Wiberg M, Kelk P. The neurotrophic effects of different human dental mesenchymal stem cells. Sci Rep 2017; 7(1): 12605. doi: 10.1038/s41598-017-12969-1 PMID: 28974767
- Shinagawa-Ohama R, Mochizuki M, Tamaki Y, Suda N, Nakahara T. Heterogeneous human periodontal ligament-committed progenitor and stem cell populations exhibit a unique cementogenic property under in vitro and in vivo conditions. Stem Cells Dev 2017; 26(9): 632-45. doi: 10.1089/scd.2016.0330 PMID: 28136695
- Tian Y, Bai D, Guo W, et al. Comparison of human dental follicle cells and human periodontal ligament cells for dentin tissue regeneration. Regen Med 2015; 10(4): 461-79. doi: 10.2217/rme.15.21 PMID: 26022765
- Han C, Yang Z, Zhou W, et al. Periapical follicle stem cell: A promising candidate for cementum/periodontal ligament regeneration and bio-root engineering. Stem Cells Dev 2010; 19(9): 1405-15. doi: 10.1089/scd.2009.0277 PMID: 19995154
- Guo S, Guo W, Ding Y, et al. Comparative study of human dental follicle cell sheets and periodontal ligament cell sheets for periodontal tissue regeneration. Cell Transplant 2013; 22(6): 1061-73. doi: 10.3727/096368912X656036 PMID: 23007138
- Açil Y, Yang F, Gulses A, Ayna M, Wiltfang J, Gierloff M. Isolation, characterization and investigation of differentiation potential of human periodontal ligament cells and dental follicle progenitor cells and their response to BMP-7 in vitro. Odontology 2016; 104(2): 123-35. doi: 10.1007/s10266-015-0198-1 PMID: 25757659
- Lindroos B, Mäenpää K, Ylikomi T, Oja H, Suuronen R, Miettinen S. Characterisation of human dental stem cells and buccal mucosa fibroblasts. Biochem Biophys Res Commun 2008; 368(2): 329-35. doi: 10.1016/j.bbrc.2008.01.081 PMID: 18230338
- Park JY, Jeon SH, Choung PH. Efficacy of periodontal stem cell transplantation in the treatment of advanced periodontitis. Cell Transplant 2011; 20(2): 271-85. doi: 10.3727/096368910X519292 PMID: 20719084
- 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. doi: 10.1902/jop.2010.090729 PMID: 20476882
- Ji K, Liu Y, Lu W, et al. Periodontal tissue engineering with stem cells from the periodontal ligament of human retained deciduous teeth. J Periodontal Res 2013; 48(1): 105-16. doi: 10.1111/j.1600-0765.2012.01509.x PMID: 22881344
- Khoshhal M, Amiri I, Gholami L. Comparison of in vitro properties of periodontal ligament stem cells derived from permanent and deciduous teeth. J Dent Res Dent Clin Dent Prospect 2017; 11(3): 140-8. doi: 10.15171/joddd.2017.026 PMID: 29184628
- Park JC, Kim JM, Jung IH, et al. Isolation and characterization of human periodontal ligament (PDL) stem cells (PDLSCs) from the inflamed PDL tissue: In vitro and in vivo evaluations. J Clin Periodontol 2011; 38(8): 721-31. doi: 10.1111/j.1600-051X.2011.01716.x PMID: 21449989
- Tang HN, Xia Y, Yu Y, Wu RX, Gao LN, Chen FM. Stem cells derived from "inflamed" and healthy periodontal ligament tissues and their sheet functionalities: A patient-matched comparison. J Clin Periodontol 2016; 43(1): 72-84. doi: 10.1111/jcpe.12501 PMID: 26719165
- Liu D, Xu J, Liu O, et al. Mesenchymal stem cells derived from inflamed periodontal ligaments exhibit impaired immunomodulation. J Clin Periodontol 2012; 39(12): 1174-82. doi: 10.1111/jcpe.12009 PMID: 23005571
- Dalband M, Amiri I, Soltanian AR, Gholami M, Khayati A, Keshmirypor V. Comparing viability of periodontal ligament stem cells isolated from erupted and impacted tooth root. J Craniofac Surg 2015; 26(7): e608-12. doi: 10.1097/SCS.0000000000002112 PMID: 26468840
- Wang WJ, Zhao YM, Lin BC, Yang J, Ge LH. Identification of multipotent stem cells from adult dog periodontal ligament. Eur J Oral Sci 2012; 120(4): 303-10. doi: 10.1111/j.1600-0722.2012.00975.x PMID: 22813220
- Chopra H, Liao C, Zhang CF, Pow EHN. Lapine periodontal ligament stem cells for musculoskeletal research in preclinical animal trials. J Transl Med 2018; 16(1): 174. doi: 10.1186/s12967-018-1551-2 PMID: 29929550
- Mensing N, Gasse H, Hambruch N, Haeger JD, Pfarrer C, Staszyk C. Isolation and characterization of multipotent mesenchymal stromal cells from the gingiva and the periodontal ligament of the horse. BMC Vet Res 2011; 7(1): 42. doi: 10.1186/1746-6148-7-42 PMID: 21810270
- Yu BH, Zhou Q, Wang ZL. Periodontal ligament versus bone marrow mesenchymal stem cells in combination with Bio-Oss scaffolds for ectopic and in situ bone formation: A comparative study in the rat. J Biomater Appl 2014; 29(2): 243-53. doi: 10.1177/0885328214521846 PMID: 24487130
- Yu BH, Zhou Q, Wang ZL. Comparison of tissue-engineered bone from different stem cell sources for maxillary sinus floor augmentation: A study in a canine model. J Oral Maxillofac Surg 2014; 72(6): 1084-92. doi: 10.1016/j.joms.2013.12.024 PMID: 24576438
- Kadkhoda Z, Safarpour A, Azmoodeh F, Adibi S, Khoshzaban A, Bahrami N. Histopathological comparison between bone marrow- and periodontium-derived stem cells for bone regeneration in rabbit calvaria. Int J Organ Transplant Med 2016; 7(1): 9-18. PMID: 26889369
- Kato T, Hattori K, Deguchi T, et al. Osteogenic potential of rat stromal cells derived from periodontal ligament. J Tissue Eng Regen Med 2011; 5(10): 798-805. doi: 10.1002/term.379 PMID: 22002923
- Shrivats AR, McDermott MC, Hollinger JO. Bone tissue engineering: State of the union. Drug Discov Today 2014; 19(6): 781-6. doi: 10.1016/j.drudis.2014.04.010 PMID: 24768619
- Motamedian SR, Hosseinpour S, Ahsaie MG, Khojasteh A. Smart scaffolds in bone tissue engineering: A systematic review of literature. World J Stem Cells 2015; 7(3): 657-68. doi: 10.4252/wjsc.v7.i3.657 PMID: 25914772
- Motamedian SR, Iranparvar P, Nahvi G, Khojasteh A. Bone tissue engineering: A literature review. Journal of "Regeneration, Reconstruction & Restoration" (Triple R) 2016; 1(3): 103-20.
- Leyendecker A. Junior, Gomes Pinheiro CC, Lazzaretti Fernandes T, Franco Bueno D. The use of human dental pulp stem cells for in vivo bone tissue engineering: A systematic review. J Tissue Eng 2018; 2018(Jan-Dec): 9. doi: 10.1177/2041731417752766
- Mantesso A, Sharpe P. Dental stem cells for tooth regeneration and repair. Expert Opin Biol Ther 2009; 9(9): 1143-54. doi: 10.1517/14712590903103795 PMID: 19653863
- Sharpe PT. Dental mesenchymal stem cells. Development 2016; 143(13): 2273-80. doi: 10.1242/dev.134189 PMID: 27381225
- Lian JB, Stein GS. Concepts of osteoblast growth and differentiation: Basis for modulation of bone cell development and tissue formation. Crit Rev Oral Biol Med 1992; 3(3): 269-305. doi: 10.1177/10454411920030030501 PMID: 1571474
- Stoltz J. Ed. Osteogenic induction comparison between dental pulp stem cells and periodontal ligament stem cells in a transcriptional level. Stem cells and regenerative medicine Proceedings of the 8th International China-Europe Symposium. Wuhan, China. 2018
- Roura S, Farré J, Soler-Botija C, et al. Effect of aging on the pluripotential capacity of human CD105+ mesenchymal stem cells. Eur J Heart Fail 2006; 8(6): 555-63. doi: 10.1016/j.ejheart.2005.11.006 PMID: 16507351
- Bakopoulou A, Leyhausen G, Volk J, et al. Comparative analysis of in vitro osteo/odontogenic differentiation potential of human dental pulp stem cells (DPSCs) and stem cells from the apical papilla (SCAP). Arch Oral Biol 2011; 56(7): 709-21. doi: 10.1016/j.archoralbio.2010.12.008 PMID: 21227403
- Isaka J, Ohazama A, Kobayashi M, et al. Participation of periodontal ligament cells with regeneration of alveolar bone. J Periodontol 2001; 72(3): 314-23. doi: 10.1902/jop.2001.72.3.314 PMID: 11327058
- Li J, Zhang F, Zhang N, et al. Osteogenic capacity and cytotherapeutic potential of periodontal ligament cells for periodontal regeneration in vitro and in vivo. PeerJ 2019; 7(3): e6589. doi: 10.7717/peerj.6589 PMID: 30867997
- Ma L, Hu J, Cao Y, et al. Maintained properties of aged dental pulp stem cells for superior periodontal tissue regeneration. Aging Dis 2019; 10(4): 793-806. doi: 10.14336/AD.2018.0729 PMID: 31440385
- Moshaverinia A, Chen C, Akiyama K, et al. Encapsulated dental-derived mesenchymal stem cells in an injectable and biodegradable scaffold for applications in bone tissue engineering. J Biomed Mater Res A 2013; 101(11): 3285-94. doi: 10.1002/jbm.a.34546 PMID: 23983201
- Tsumanuma Y, Iwata T, Washio K, et al. Comparison of different tissue-derived stem cell sheets for periodontal regeneration in a canine 1-wall defect model. Biomaterials 2011; 32(25): 5819-25. doi: 10.1016/j.biomaterials.2011.04.071 PMID: 21605900
- Vaquette C, Saifzadeh S, Farag A, Hutmacher DW, Ivanovski S. Periodontal tissue engineering with a multiphasic construct and cell sheets. J Dent Res 2019; 98(6): 673-81. doi: 10.1177/0022034519837967 PMID: 30971166
- Volponi AA, Gentleman E, Fatscher R, Pang YW, Gentleman MM, Sharpe PT. Composition of mineral produced by dental mesenchymal stem cells. J Dent Res 2015; 94(11): 1568-74. doi: 10.1177/0022034515599765 PMID: 26253190
- Wang H, Ma D, Zhang X, Xu S, Ning T, Wu B. Comparative proteomic profiling of human dental pulp stem cells and periodontal ligament stem cells under in vitro osteogenic induction. Arch Oral Biol 2018; 89: 9-19. doi: 10.1016/j.archoralbio.2018.01.015 PMID: 29407636
- Ansari S, Diniz IM, Chen C, et al. Alginate/hyaluronic acid hydrogel delivery system characteristics regulate the differentiation of periodontal ligament stem cells toward chondrogenic lineage. J Mater Sci Mater Med 2017; 28(10): 162. doi: 10.1007/s10856-017-5974-8 PMID: 28914392
- Fu X, Jin L, Ma P, Fan Z, Wang S. Allogeneic stem cells from deciduous teeth in treatment for periodontitis in miniature swine. J Periodontol 2014; 85(6): 845-51. doi: 10.1902/jop.2013.130254 PMID: 24001042
- Giovani PA, Salmon CR, Martins L, et al. Membrane proteome characterization of periodontal ligament cell sets from deciduous and permanent teeth. J Periodontol 2019; 90(7): 775-87. PMID: 30499115
- Jayaraman P, Govindasamy V, Gnanasegaran N, et al. Expression patterns of immune genes in long-term cultured dental stem cells. Clin Oral Investig 2016; 20(1): 109-16. doi: 10.1007/s00784-015-1497-1 PMID: 26048030
- Jung IH, Park JC, Kim JC, et al. Novel application of human periodontal ligament stem cells and water-soluble chitin for collagen tissue regeneration: In vitro and in vivo investigations. Tissue Eng Part A 2012; 18(5-6): 643-53. doi: 10.1089/ten.tea.2011.0164 PMID: 21981356
- Kim K, Jeon M, Lee HS, et al. Comparative analysis of secretory factors from permanent- and deciduous-teeth periodontal ligament cells. Arch Oral Biol 2016; 71: 65-79. doi: 10.1016/j.archoralbio.2016.07.003 PMID: 27448989
- Lee JH, Um S, Song IS, Kim HY, Seo BM. Neurogenic differentiation of human dental stem cells in vitro. J Korean Assoc Oral Maxillofac Surg 2014; 40(4): 173-80. doi: 10.5125/jkaoms.2014.40.4.173 PMID: 25247147
- Dangaria SJ, Ito Y, Luan X, Diekwisch TG. Successful periodontal ligament regeneration by periodontal progenitor preseeding on natural tooth root surfaces. Stem Cells Dev 2011; 20(10): 1659-68. doi: 10.1089/scd.2010.0431 PMID: 21250830
- Kim SH, Kim KH, Seo BM, et al. Alveolar bone regeneration by transplantation of periodontal ligament stem cells and bone marrow stem cells in a canine peri-implant defect model: A pilot study. J Periodontol 2009; 80(11): 1815-23. doi: 10.1902/jop.2009.090249 PMID: 19905951
- Li K, Lei M, Gao L, Li B, Chen F-m, Jin Y. Characterization of dental pulp stem cells and periodontal ligament stem cells from miniature pig. Yati Yasui Yazhoubingxue Zazhi 2014; 24(2): 61-5.
- Mrozik KM, Zilm PS, Bagley CJ, et al. Proteomic characterization of mesenchymal stem cell-like populations derived from ovine periodontal ligament, dental pulp, and bone marrow: Analysis of differentially expressed proteins. Stem Cells Dev 2010; 19(10): 1485-99. doi: 10.1089/scd.2009.0446 PMID: 20050811
- Shin C, Kim M, Han JA, et al. Human periodontal ligament stem cells suppress T-cell proliferation via down-regulation of non-classical major histocompatibility complex-like glycoprotein CD1b on dendritic cells. J Periodontal Res 2017; 52(1): 135-46. doi: 10.1111/jre.12378 PMID: 27021598
- Han NY, Hong JY, Park JM, et al. Label-free quantitative proteomic analysis of human periodontal ligament stem cells by high-resolution mass spectrometry. J Periodontal Res 2019; 54(1): 53-62. doi: 10.1111/jre.12604 PMID: 30298515
- Hu L, Zhao B, Gao Z, Xu J, Fan Z, Zhang C, et al. Regeneration characteristics of different dental derived stem cell sheets. J Oral Rehabil 2019. PMID: 31211857
- Kim SH, Kim YS, Lee SY, et al. Gene expression profile in mesenchymal stem cells derived from dental tissues and bone marrow. J Periodontal Implant Sci 2011; 41(4): 192-200. doi: 10.5051/jpis.2011.41.4.192 PMID: 21954424
- Mehrazarin S, Oh JE, Chung CL, et al. Impaired odontogenic differentiation of senescent dental mesenchymal stem cells is associated with loss of Bmi-1 expression. J Endod 2011; 37(5): 662-6. doi: 10.1016/j.joen.2011.02.009 PMID: 21496667
- Xu J, Wang W, Kapila Y, Lotz J, Kapila S. Multiple differentiation capacity of STRO-1+/CD146+ PDL mesenchymal progenitor cells. Stem Cells Dev 2009; 18(3): 487-96. doi: 10.1089/scd.2008.0113 PMID: 18593336
- Prateeptongkum E, Klingelhöffer C, Müller S, Ettl T, Morsczeck C. Characterization of progenitor cells and stem cells from the periodontal ligament tissue derived from a single person. J Periodontal Res 2016; 51(2): 265-72. doi: 10.1111/jre.12306 PMID: 26108342
- Lei M, Li K, Li B, Gao L-N, Chen F-M, Jin Y. Mesenchymal stem cell characteristics of dental pulp and periodontal ligament stem cells after in vivo transplantation. Biomaterials 2014; 35(24): 6332-43. doi: 10.1016/j.biomaterials.2014.04.071 PMID: 24824581
- Menicanin D, Bartold PM, Zannettino ACW, Gronthos S. Identification of a common gene expression signature associated with immature clonal mesenchymal cell populations derived from bone marrow and dental tissues. Stem Cells Dev 2010; 19(10): 1501-10. doi: 10.1089/scd.2009.0492 PMID: 20128661
- Menicanin D, Mrozik KM, Wada N, et al. Periodontal-ligament-derived stem cells exhibit the capacity for long-term survival, self-renewal, and regeneration of multiple tissue types in vivo. Stem Cells Dev 2014; 23(9): 1001-11. doi: 10.1089/scd.2013.0490 PMID: 24351050
- Park JY, Jeon HJ, Kim TY, et al. Comparative analysis of mesenchymal stem cell surface marker expression for human dental mesenchymal stem cells. Regen Med 2013; 8(4): 453-66. doi: 10.2217/rme.13.23 PMID: 23826699
- Ponnaiyan D, Bhat KM, Bhat GS. Comparison of immuno-phenotypes of stem cells from human dental pulp and periodontal ligament. Int J Immunopathol Pharmacol 2012; 25(1): 127-34. doi: 10.1177/039463201202500115 PMID: 22507325
- Kumar A, Kumar V, Rattan V, Jha V, Bhattacharyya S. Secretome proteins regulate comparative osteogenic and adipogenic potential in bone marrow and dental stem cells. Biochimie 2018; 155: 129-39. doi: 10.1016/j.biochi.2018.10.014 PMID: 30367923
- Banavar SR, Rawal SY, Paterson IC, et al. Establishing a technique for isolation and characterization of human periodontal ligament derived mesenchymal stem cells. Saudi Dent J 2020. PMID: 34803321
- Choi JK, Hwang HI, Jang YJ. The efficiency of the in vitro osteo/dentinogenic differentiation of human dental pulp cells, periodontal ligament cells and gingival fibroblasts. Int J Mol Med 2015; 35(1): 161-8. doi: 10.3892/ijmm.2014.1986 PMID: 25355399
- Kadar K, Kiraly M, Porcsalmy B, et al. Differentiation potential of stem cells from human dental origin - promise for tissue engineering. Journal of physiology and pharmacology : An official journal of the Polish Physiological Society 2009; 60 (Suppl 7): 167-75.
- Al-Habib M, Huang GT. Dental mesenchymal stem cells: Dental pulp stem cells, periodontal ligament stem cells, apical papilla stem cells, and primary teeth stem cells-isolation, characterization, and expansion for tissue engineering. Methods Mol Biol 2019; 1922: 59-76. doi: 10.1007/978-1-4939-9012-2_7 PMID: 30838565
- Alvarez R. The characterization of dental mesenchymal stem cells from human dental pulp and periodontal ligament based on cell surface markers. UCLA 2016.
- Shi S, Bartold PM, Miura M, Seo BM, Robey PG, Gronthos S. The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res 2005; 8(3): 191-9. doi: 10.1111/j.1601-6343.2005.00331.x PMID: 16022721
- Lee J-K, Lee J-H. A study on differentiation potency of adult stem cells from pulp, periodontal ligament, and dental follicle to osteoblast. J Korean Assoc Oral Maxillofac Surg 2010; 36(1): 7-15. doi: 10.5125/jkaoms.2010.36.1.7
- Yeasmin S, Ceccarelli J, Vigen M, et al. Stem cells derived from tooth periodontal ligament enhance functional angiogenesis by endothelial cells. Tissue Eng Part A 2014; 20(7-8): 1188-96. doi: 10.1089/ten.tea.2013.0512 PMID: 24147894
- Taraslia V, Lymperi S, Pantazopoulou V, et al. A high-resolution proteomic landscaping of primary human dental stem cells: Identification of SHED- and PDLSC-specific biomarkers. Int J Mol Sci 2018; 19(1): E158. doi: 10.3390/ijms19010158 PMID: 29304003
- Qiu J, Wang X, Zhou H, et al. Enhancement of periodontal tissue regeneration by conditioned media from gingiva-derived or periodontal ligament-derived mesenchymal stem cells: A comparative study in rats. Stem Cell Res Ther 2020; 11(1): 42. doi: 10.1186/s13287-019-1546-9 PMID: 32014015
- Wu T, Xu W, Chen H, et al. Comparison of the differentiation of dental pulp stem cells and periodontal ligament stem cells into neuron-like cells and their effects on focal cerebral ischemia. Acta Biochim Biophys Sin (Shanghai) 2020; 52(9): 1016-29. doi: 10.1093/abbs/gmaa082 PMID: 32845287
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