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CC BY 4.0 · Eur J Dent 2024; 18(03): 712-742
DOI: 10.1055/s-0043-1776315
DOI: 10.1055/s-0043-1776315
Review Article
Angiogenic Potential of Various Oral Cavity–Derived Mesenchymal Stem Cells and Cell-Derived Secretome: A Systematic Review and Meta-Analysis
Abstract
Recent evidence suggests the immense potential of human mesenchymal stem cell (hMSC) secretome conditioned medium-mediated augmentation of angiogenesis. However, angiogenesis potential varies from source and origin. The hMSCs derived from the oral cavity share an exceptional quality due to their origin from a hypoxic environment. Our systematic review aimed to compare the mesenchymal stem cells (MSCs) derived from various oral cavity sources and cell-derived secretomes, and evaluate their angiogenic potential. A literature search was conducted using PubMed and Scopus from January 2000 to September 2020. Source-wise outcomes were systematically analyzed using in vitro, in vivo, and in ovo studies, emphasizing endothelial cell migration, tube formation, and blood vessel formation. Ninety-four studies were included in the systematic review, out of which 4 studies were subsequently included in the meta-analysis. Prominent growth factors and other bioactive components implicated in improving angiogenesis were included in the respective studies. The findings suggest that oral tissues are a rich source of hMSCs. The meta-analysis revealed a positive correlation between dental pulp–derived MSCs (DPMSCs) and stem cells derived from apical papilla (SCAP) compared to human umbilical cord–derived endothelial cell lines as a control. It shows a statistically significant positive correlation between the co-culture of human umbilical vein endothelial cells (HUVECs) and DPMSCs with tubule length formation and total branching points. Our meta-analysis revealed that oral-derived MSCs (dental pulp stem cells and SCAP) carry a better angiogenic potential in vitro than endothelial cell lines alone. The reviewed literature illustrates that oral cavity–derived MSCs (OC-MSCs) increased angiogenesis. The present literature reveals a dearth of investigations involving sources other than dental pulp. Even though OC-MSCs have revealed more significant potential than other MSCs, more comprehensive, target-oriented interinstitutional prospective studies are warranted to determine whether oral cavity–derived stem cells are the most excellent sources of significant angiogenic potential.
Authors' Contribution
All the authors contributed to the concept and design of the study.
Data Availability Statement
The datasets generated and/or analyzed during the current study are available from the corresponding author on request.
Publication History
Article published online:
23 November 2023
© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)
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References
- 1 Honnegowda TM, Kumar P, Udupa EG, Kumar S, Kumar U, Rao P. Role of angiogenesis and angiogenic factors in acute and chronic wound healing. Plast Aesthet Res 2015; 2: 243-249
- 2 Auerbach R, Auerbach W, Polakowski I. Assays for angiogenesis: a review. Pharmacol Ther 1991; 51 (01) 1-11
- 3 Adair TH, Montani JP. Angiogenesis. In: Granger DN, Granger JP. eds. Colloquium Series on Integrated Systems Physiology: From Molecule to Function. San Rafael, CA: Morgan & Claypool Life Sciences; 2010: 1-84
- 4 Wang P, Zhu S, Yuan C, Wang L, Xu J, Liu Z. Shear stress promotes differentiation of stem cells from human exfoliated deciduous teeth into endothelial cells via the downstream pathway of VEGF-Notch signaling. Int J Mol Med 2018; 42 (04) 1827-1836
- 5 King A, Balaji S, Keswani SG, Crombleholme TM. The role of stem cells in wound angiogenesis. Adv Wound Care (New Rochelle) 2014; 3 (10) 614-625
- 6 Bindal P, Gnanasegaran N, Bindal U. et al. Angiogenic effect of platelet-rich concentrates on dental pulp stem cells in inflamed microenvironment. Clin Oral Investig 2019; 23 (10) 3821-3831
- 7 Chakraborty S, Ponrasu T, Chandel S, Dixit M, Muthuvijayan V. Reduced graphene oxide-loaded nanocomposite scaffolds for enhancing angiogenesis in tissue engineering applications. R Soc Open Sci 2018; 5 (05) 172017
- 8 Kerkis I, Kerkis A, Dozortsev D. et al. Isolation and characterization of a population of immature dental pulp stem cells expressing OCT-4 and other embryonic stem cell markers. Cells Tissues Organs 2006; 184 (3–4): 105-116
- 9 Miran S, Mitsiadis TA, Pagella P. Innovative dental stem cell-based research approaches: the future of dentistry. Stem Cells Int 2016; 2016: 7231038
- 10 Li J, Zhu Y, Li N. et al. Upregulation of ETV2 expression promotes endothelial differentiation of human dental pulp stem cells. Cell Transplant 2021; 30: 963689720978739
- 11 Boreak N, Khayrat NMA, Shami AO. et al. Metformin pre-conditioning enhances the angiogenic ability of the secretome of dental pulp stem cells. Saudi Pharm J 2021; 29 (08) 908-913
- 12 Li Y, Zhang Y, Wang H. et al. Dental pulp mesenchymal stem cells attenuate limb ischemia via promoting capillary proliferation and collateral development in a preclinical model. Stem Cells Int 2021; 2021: 5585255
- 13 Li M, Wang Q, Han Q. et al. Novel molecule Nell-1 promotes the angiogenic differentiation of dental pulp stem cells. Front Physiol 2021; 12: 703593
- 14 Alghutaimel H, Yang X, Drummond B, Nazzal H, Duggal M, Raïf E. Investigating the vascularization capacity of a decellularized dental pulp matrix seeded with human dental pulp stem cells: in vitro and preliminary in vivo evaluations. Int Endod J 2021; 54 (08) 1300-1316
- 15 Zhou H, Li X, Wu RX. et al. Periodontitis-compromised dental pulp stem cells secrete extracellular vesicles carrying miRNA-378a promote local angiogenesis by targeting Sufu to activate the Hedgehog/Gli1 signalling. Cell Prolif 2021; 54 (05) e13026
- 16 Huang X, Qiu W, Pan Y. et al. Exosomes from LPS-stimulated hDPSCs activated the angiogenic potential of HUVECs in vitro . Stem Cells Int 2021; 2021: 6685307
- 17 Afami ME, El Karim I, About I, Coulter SM, Laverty G, Lundy FT. Ultrashort peptide hydrogels display antimicrobial activity and enhance angiogenic growth factor release by dental pulp stem/stromal cells. Materials (Basel) 2021; 14 (09) 2237
- 18 Liao ZH, Zhu HQ, Chen YY. et al. The epigallocatechin gallate derivative Y6 inhibits human hepatocellular carcinoma by inhibiting angiogenesis in MAPK/ERK1/2 and PI3K/AKT/ HIF-1α/VEGF dependent pathways. J Ethnopharmacol 2020; 259: 112852
- 19 He Y, Cao Y, Xiang Y. et al. An evaluation of norspermidine on anti-fungal effect on mature Candida albicans biofilms and angiogenesis potential of dental pulp stem cells. Front Bioeng Biotechnol 2020; 8: 948
- 20 Guo S, Redenski I, Landau S, Szklanny A, Merdler U, Levenberg S. Prevascularized scaffolds bearing human dental pulp stem cells for treating complete spinal cord injury. Adv Healthc Mater 2020; 9 (20) e2000974
- 21 Luzuriaga J, Irurzun J, Irastorza I, Unda F, Ibarretxe G, Pineda JR. Vasculogenesis from human dental pulp stem cells grown in matrigel with fully defined serum-free culture media. Biomedicines 2020; 8 (11) 483
- 22 Merckx G, Hosseinkhani B, Kuypers S. et al. Angiogenic effects of human dental pulp and bone marrow-derived mesenchymal stromal cells and their extracellular vesicles. Cells 2020; 9 (02) 312
- 23 Caseiro AR, Santos Pedrosa S, Ivanova G. et al. Mesenchymal Stem/ Stromal Cells metabolomic and bioactive factors profiles: a comparative analysis on the umbilical cord and dental pulp derived stem/stromal cells secretome. PLoS One 2019; 14 (11) e0221378
- 24 Makino E, Nakamura N, Miyabe M. et al. Conditioned media from dental pulp stem cells improved diabetic polyneuropathy through anti-inflammatory, neuroprotective and angiogenic actions: cell-free regenerative medicine for diabetic polyneuropathy. J Diabetes Investig 2019; 10 (05) 1199-1208
- 25 Chen Y, Li X, Wu J, Lu W, Xu W, Wu B. Dental pulp stem cells from human teeth with deep caries displayed an enhanced angiogenesis potential in vitro . J Dent Sci 2021; 16 (01) 318-326
- 26 Li J, Rao Z, Zhao Y. et al. A decellularized matrix hydrogel derived from human dental pulp promotes dental pulp stem cell proliferation, migration, and induced multidirectional differentiation in vitro . J Endod 2020; 46 (10) 1438-1447.e5
- 27 Wang D, Lyu Y, Yang Y. et al. Schwann cell-derived EVs facilitate dental pulp regeneration through endogenous stem cell recruitment via SDF-1/CXCR4 axis. Acta Biomater 2022; 140: 610-624
- 28 Zhou J, Sun C. SENP1/HIF-1α axis works in angiogenesis of human dental pulp stem cells. J Biochem Mol Toxicol 2020; 34 (03) e22436
- 29 Qu C, Brohlin M, Kingham PJ, Kelk P. Evaluation of growth, stemness, and angiogenic properties of dental pulp stem cells cultured in cGMP xeno-/serum-free medium. Cell Tissue Res 2020; 380 (01) 93-105
- 30 Zhu L, Dissanayaka WL, Zhang C. Dental pulp stem cells overexpressing stromal-derived factor-1α and vascular endothelial growth factor in dental pulp regeneration. Clin Oral Investig 2019; 23 (05) 2497-2509
- 31 Li J, Diao S, Yang H, Cao Y, Du J, Yang D. IGFBP5 promotes angiogenic and neurogenic differentiation potential of dental pulp stem cells. Dev Growth Differ 2019; 61 (09) 457-465
- 32 Lu W, Xu W, Li J, Chen Y, Pan Y, Wu B. Effects of vascular endothelial growth factor and insulin growth factor–1 on proliferation, migration, osteogenesis and vascularization of human carious dental pulp stem cells. Mol Med Rep 2019; 20 (04) 3924-3932
- 33 Youssef AR, Emara R, Taher MM. et al. Effects of mineral trioxide aggregate, calcium hydroxide, Biodentine and Emdogain on osteogenesis, Odontogenesis, angiogenesis and cell viability of dental pulp stem cells. BMC Oral Health 2019; 19 (01) 133
- 34 Rapino M, Di Valerio V, Zara S. et al. Chitlac-coated thermosets enhance osteogenesis and angiogenesis in a co-culture of dental pulp stem cells and endothelial cells. Nanomaterials (Basel) 2019; 9 (07) 928
- 35 Dubey N, Xu J, Zhang Z, Nör JE, Bottino MC. Comparative evaluation of the cytotoxic and angiogenic effects of minocycline and clindamycin: an in vitro study. J Endod 2019; 45 (07) 882-889
- 36 Delle Monache S, Martellucci S, Clementi L. et al. In vitro conditioning determines the capacity of dental pulp stem cells to function as pericyte-like cells. Stem Cells Dev 2019; 28 (10) 695-706
- 37 Gong T, Xu J, Heng B. et al. EphrinB2/EphB4 signaling regulates DPSCs to induce sprouting angiogenesis of endothelial cells. J Dent Res 2019; 98 (07) 803-812
- 38 Schertl P, Volk J, Perduns R. et al. Impaired angiogenic differentiation of dental pulp stem cells during exposure to the resinous monomer triethylene glycol dimethacrylate. Dent Mater 2019; 35 (01) 144-155
- 39 Luzuriaga J, Pastor-Alonso O, Encinas JM, Unda F, Ibarretxe G, Pineda JR. Human dental pulp stem cells grown in neurogenic media differentiate into endothelial cells and promote neovasculogenesis in the mouse brain. Front Physiol 2019; 10: 347
- 40 Zou T, Jiang S, Dissanayaka WL. et al. Sema4D/PlexinB1 promotes endothelial differentiation of dental pulp stem cells via activation of AKT and ERK1/2 signaling. J Cell Biochem 2019; 120 (08) 13614-13624
- 41 Jin R, Song G, Chai J, Gou X, Yuan G, Chen Z. Effects of concentrated growth factor on proliferation, migration, and differentiation of human dental pulp stem cells in vitro . J Tissue Eng 2018; 9: 2041731418817505
- 42 Gharaei MA, Xue Y, Mustafa K, Lie SA, Fristad I. Human dental pulp stromal cell conditioned medium alters endothelial cell behavior. Stem Cell Res Ther 2018; 9 (01) 69
- 43 Dou L, Yan Q, Liang P, Zhou P, Zhang Y, Ji P. iTRAQ-based proteomic analysis exploring the influence of hypoxia on the proteome of dental pulp stem cells under 3D culture. Proteomics 2018; 18 (3–4): 1700215
- 44 Aksel H, Öztürk Ş, Serper A, Ulubayram K. VEGF/BMP-2 loaded three-dimensional model for enhanced angiogenic and odontogenic potential of dental pulp stem cells. Int Endod J 2018; 51 (04) 420-430
- 45 Lambrichts I, Driesen RB, Dillen Y. et al. Dental pulp stem cells: their potential in reinnervation and angiogenesis by using scaffolds. J Endod 2017; 43 (9S): S12-S16
- 46 Silva GO, Zhang Z, Cucco C, Oh M, Camargo CHR, Nör JE. Lipoprotein receptor–related protein 6 signaling is necessary for vasculogenic differentiation of human dental pulp stem cells. J Endod 2017; 43 (9S): S25-S30
- 47 Aksel H, Huang GT. Human and swine dental pulp stem cells form a vascularlike network after angiogenic differentiation in comparison with endothelial cells: a quantitative analysis. J Endod 2017; 43 (04) 588-595
- 48 Zou T, Dissanayaka WL, Jiang S. et al. Semaphorin 4D enhances angiogenic potential and suppresses osteo-/odontogenic differentiation of human dental pulp stem cells. J Endod 2017; 43 (02) 297-305
- 49 Nam H, Kim GH, Bae YK. et al. Angiogenic capacity of dental pulp stem cell regulated by SDF-1 α-CXCR4 axis. Stem Cells Int 2017; 2017: 8085462
- 50 Lee SI, Lee ES, El-Fiqi A, Lee SY, Eun-Cheol Kim Kim HW. Stimulation of odontogenesis and angiogenesis via bioactive nanocomposite calcium phosphate cements through integrin and VEGF signaling pathways. J Biomed Nanotechnol 2016; 12 (05) 1048-1062
- 51 Lee SI, Kim SY, Park KR, Kim EC. Baicalein promotes angiogenesis and odontoblastic differentiation via the BMP and Wnt pathways in human dental pulp cells. Am J Chin Med 2016; 44 (07) 1457-1472
- 52 Spina A, Montella R, Liccardo D. et al. NZ-GMP approved serum improve hDPSC osteogenic commitment and increase angiogenic factor expression. Front Physiol 2016; 7: 354
- 53 Kuang R, Zhang Z, Jin X. et al. Nanofibrous spongy microspheres for the delivery of hypoxia-primed human dental pulp stem cells to regenerate vascularized dental pulp. Acta Biomater 2016; 33: 225-234
- 54 Shen C, Li L, Feng T. et al. Dental pulp stem cells derived conditioned medium promotes angiogenesis in hindlimb ischemia. J Tissue Eng Regen Med 2015; 12 (01) 59-68
- 55 Dissanayaka WL, Zhu L, Hargreaves KM, Jin L, Zhang C. In vitro analysis of scaffold-free prevascularized microtissue spheroids containing human dental pulp cells and endothelial cells. J Endod 2015; 41 (05) 663-670
- 56 Boyle M, Chun C, Strojny C. et al. Chronic inflammation and angiogenic signaling axis impairs differentiation of dental-pulp stem cells. PLoS One 2014; 9 (11) e113419
- 57 Liu W, Gong Q, Ling J, Zhang W, Liu Z, Quan J. Role of miR-424 on angiogenic potential in human dental pulp cells. J Endod 2014; 40 (01) 76-82
- 58 Bronckaers A, Hilkens P, Fanton Y. et al. Angiogenic properties of human dental pulp stem cells. PLoS One 2013; 8 (08) e71104
- 59 Janebodin K, Zeng Y, Buranaphatthana W, Ieronimakis N, Reyes M. VEGFR2-dependent angiogenic capacity of pericyte-like dental pulp stem cells. J Dent Res 2013; 92 (06) 524-531
- 60 Ishizaka R, Hayashi Y, Iohara K. et al. Stimulation of angiogenesis, neurogenesis and regeneration by side population cells from dental pulp. Biomaterials 2013; 34 (08) 1888-1897
- 61 Dissanayaka WL, Zhan X, Zhang C, Hargreaves KM, Jin L, Tong EH. Coculture of dental pulp stem cells with endothelial cells enhances osteo-/odontogenic and angiogenic potential in vitro . J Endod 2012; 38 (04) 454-463
- 62 Iohara K, Zheng L, Wake H. et al. A novel stem cell source for vasculogenesis in ischemia: subfraction of side population cells from dental pulp. Stem Cells 2008; 26 (09) 2408-2418
- 63 Wu M, Liu X, Li Z. et al. SHED aggregate exosomes shuttled miR-26a promote angiogenesis in pulp regeneration via TGF-β/SMAD2/3 signalling. Cell Prolif 2021; 54 (07) e13074
- 64 Han Y, Chen Q, Zhang L, Dissanayaka WL. Indispensable role of HIF-1α signaling in post-implantation survival and angio-/vasculogenic properties of SHED. Front Cell Dev Biol 2021; 9: 655073
- 65 Zaw SYM, Kaneko T, Zaw ZCT. et al. Crosstalk between dental pulp stem cells and endothelial cells augments angiogenic factor expression. Oral Dis 2020; 26 (06) 1275-1283
- 66 Atlas Y, Gorin C, Novais A. et al. Microvascular maturation by mesenchymal stem cells in vitro improves blood perfusion in implanted tissue constructs. Biomaterials 2021; 268: 120594
- 67 Guo H, Zhao W, Liu A. et al. SHED promote angiogenesis in stem cell-mediated dental pulp regeneration. Biochem Biophys Res Commun 2020; 529 (04) 1158-1164
- 68 Gong T, Heng BC, Xu J. et al. Decellularized extracellular matrix of human umbilical vein endothelial cells promotes endothelial differentiation of stem cells from exfoliated deciduous teeth. J Biomed Mater Res A 2017; 105 (04) 1083-1093
- 69 Kim JH, Kim GH, Kim JW. et al. In vivo angiogenic capacity of stem cells from human exfoliated deciduous teeth with human umbilical vein endothelial cells. Mol Cells 2016; 39 (11) 790-796
- 70 Gorin C, Rochefort GY, Bascetin R. et al. Priming dental pulp stem cells with fibroblast growth factor-2 increases angiogenesis of implanted tissue-engineered constructs through hepatocyte growth factor and vascular endothelial growth factor secretion. Stem Cells Transl Med 2016; 5 (03) 392-404
- 71 Bento LW, Zhang Z, Imai A. et al. Endothelial differentiation of SHED requires MEK1/ERK signaling. J Dent Res 2013; 92 (01) 51-57
- 72 Iwasaki K, Akazawa K, Nagata M. et al. Angiogenic effects of secreted factors from periodontal ligament stem cells. Dent J 2021; 9 (01) 9
- 73 Zhang Z, Shuai Y, Zhou F. et al. PDLSCs regulate angiogenesis of periodontal ligaments via VEGF transferred by exosomes in periodontitis. Int J Med Sci 2020; 17 (05) 558-567
- 74 Diomede F, Marconi GD, Cavalcanti MFXB. et al. VEGF/VEGF-R/RUNX2 upregulation in human periodontal ligament stem cells seeded on dual acid etched titanium disk. Materials (Basel) 2020; 13 (03) 706
- 75 Marconi GD, Diomede F, Pizzicannella J. et al. Enhanced VEGF/VEGF-R and RUNX2 expression in human periodontal ligament stem cells cultured on sandblasted/etched titanium disk. Front Cell Dev Biol 2020; 8: 315
- 76 Kim HJ, Yoo JH, Choi Y, Joo JY, Lee JY, Kim HJ. Assessing the effects of cyclosporine A on the osteoblastogenesis, osteoclastogenesis, and angiogenesis mediated by human periodontal ligament stem cells. J Periodontol 2020; 91 (06) 836-848
- 77 Iwasaki K, Nagata M, Akazawa K, Watabe T, Morita I. Changes in characteristics of periodontal ligament stem cells in spheroid culture. J Periodontal Res 2019; 54 (04) 364-373
- 78 Jearanaiphaisarn T, Sanharati T, Pavasant P, Nakalekha Limjeerajarus C. The effect of iloprost on cell proliferation and angiogenesis-related gene expression in human periodontal ligament cells. Odontology 2018; 106 (01) 11-18
- 79 Wei W, An Y, An Y, Fei D, Wang Q. Activation of autophagy in periodontal ligament mesenchymal stem cells promotes angiogenesis in periodontitis. J Periodontol 2018; 89 (06) 718-727
- 80 Bae YK, Kim GH, Lee JC. et al. The significance of SDF-1α-CXCR4 axis in in vivo angiogenic ability of human periodontal ligament stem cells. Mol Cells 2017; 40 (06) 386-392
- 81 Yi B, Ding T, Jiang S. et al. Conversion of stem cells from apical papilla into endothelial cells by small molecules and growth factors. Stem Cell Res Ther 2021; 12 (01) 266
- 82 Liu J, Zou T, Yao Q, Zhang Y, Zhao Y, Zhang C. Hypoxia-mimicking cobalt-doped multi-walled carbon nanotube nanocomposites enhance the angiogenic capacity of stem cells from apical papilla. Mater Sci Eng C 2021; 120: 111797
- 83 Yu S, Zhao Y, Fang TJ, Ge L. Effect of the soluble factors released by dental apical papilla-derived stem cells on the osteo/odontogenic, angiogenic, and neurogenic differentiation of dental pulp cells. Stem Cells Dev 2020; 29 (12) 795-805
- 84 Yuan C, Wang P, Zhu S. et al. Overexpression of ephrinB2 in stem cells from apical papilla accelerates angiogenesis. Oral Dis 2019; 25 (03) 848-859
- 85 Koutsoumparis A, Vassili A, Bakopoulou A, Ziouta A, Tsiftsoglou AS. Erythropoietin (rhEPOa) promotes endothelial transdifferentiation of stem cells of the apical papilla (SCAP). Arch Oral Biol 2018; 96: 96-103
- 86 Yadlapati M, Biguetti C, Cavalla F. et al. Characterization of a vascular endothelial growth factor–loaded bioresorbable delivery system for pulp regeneration. J Endod 2017; 43 (01) 77-83
- 87 Yuan C, Wang P, Zhu S. et al. EphrinB2 stabilizes vascularlike structures generated by endothelial cells and stem cells from apical papilla. J Endod 2016; 42 (09) 1362-1370
- 88 Peters OA, Galicia J, Arias A, Tolar M, Ng E, Shin SJ. Effects of two calcium silicate cements on cell viability, angiogenic growth factor release and related gene expression in stem cells from the apical papilla. Int Endod J 2016; 49 (12) 1132-1140
- 89 Bakopoulou A, Kritis A, Andreadis D. et al. Angiogenic potential and secretome of human apical papilla mesenchymal stem cells in various stress microenvironments. Stem Cells Dev 2015; 24 (21) 2496-2512
- 90 Yuan C, Wang P, Zhu L. et al. Coculture of stem cells from apical papilla and human umbilical vein endothelial cell under hypoxia increases the formation of three-dimensional vessel-like structures in vitro . Tissue Eng Part A 2015; 21 (5–6): 1163-1172
- 91 Jin S, Yang C, Huang J. et al. Conditioned medium derived from FGF-2-modified GMSCs enhances migration and angiogenesis of human umbilical vein endothelial cells. Stem Cell Res Ther 2020; 11 (01) 68
- 92 Zhu SY, Yuan CY, Lin YF. et al. Stem cells from human exfoliated deciduous teeth (SHEDs) and dental pulp stem cells (DPSCs) display a similar profile with pericytes. Stem Cells Int 2021; 2021: 8859902
- 93 Xie J, Zhao YM, Rao NQ. et al. Comparative study of differentiation potential of mesenchymal stem cells derived from orofacial system into vascular endothelial cells. Beijing Da Xue Xue Bao Yi Xue Ban 2019; 51 (05) 900-906
- 94 Angelopoulos I, Brizuela C, Khoury M. Gingival mesenchymal stem cells outperform haploidentical dental pulp-derived mesenchymal stem cells in proliferation rate, migration ability, and angiogenic potential. Cell Transplant 2018; 27 (06) 967-978
- 95 Xu JG, Gong T, Wang YY. et al. Inhibition of TGF-β signaling in SHED enhances endothelial differentiation. J Dent Res 2018; 97 (02) 218-225
- 96 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 (07) 639-651
- 97 Zhang Z, Oh M, Sasaki JI, Nör JE. Inverse and reciprocal regulation of p53/p21 and Bmi-1 modulates vasculogenic differentiation of dental pulp stem cells. Cell Death Dis 2021; 12 (07) 644
- 98 Olcay K, Taşli PN, Güven EP. et al. Effect of a novel bioceramic root canal sealer on the angiogenesis-enhancing potential of assorted human odontogenic stem cells compared with principal tricalcium silicate-based cements. J Appl Oral Sci 2020; 28: e20190215
- 99 Hilkens P, Bronckaers A, Ratajczak J, Gervois P, Wolfs E, Lambrichts I. The angiogenic potential of DPSCs and SCAPs in an in vivo model of dental pulp regeneration. Stem Cells Int 2017; 2017: 2582080
- 100 Zhang Z, Nör F, Oh M, Cucco C, Shi S, Nör JE. Wnt/β-catenin signaling determines the vasculogenic fate of postnatal mesenchymal stem cells. Stem Cells 2016; 34 (06) 1576-1587
- 101 Hilkens P, Fanton Y, Martens W. et al. Pro-angiogenic impact of dental stem cells in vitro and in vivo . Stem Cell Res (Amst) 2014; 12 (03) 778-790
- 102 Gandia C, Armiñan A, García-Verdugo JM. et al. Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction. Stem Cells 2008; 26 (03) 638-645
- 103 Zeidán-Chuliá F, Noda M. “Opening” the mesenchymal stem cell tool box. Eur J Dent 2009; 3 (03) 240-249
- 104 Fiorillo L. Fi-index: a new method to evaluate authors Hirsch-index reliability. Publ Res Q 2022; 38: 465-474
- 105 Fiorillo L, Cicciù M. The use of Fi-index tool to assess per-manuscript self-citations. Publ Res Q 2022; 38: 684-692