The Pro-Angiogenic Potential of Periodontal Ligament Stem Cells and Dental Pulp Stem Cells: A Comparative Analysis
Abstract
1. Introduction
2. Materials and Methods
2.1. Isolation and Expansion of PDLSCs and DPSCs
2.2. Immunophenotype Analysis
2.3. Assays of Multi-Differentiation Capability
2.4. RNA Isolation and Real-Time
2.5. In Vitro Tube Formation Assay
2.6. VEGF Dosage in PDLSC and DPSC Supernatants
2.7. Immunofluorescence Staining of HMEC Co-Cultured with PDLSCs and DPSCs
2.8. Statistical Analysis
3. Results
3.1. The Immunophenotype of DPSCs and PDLSCs Differs in the CD146+ Cell Subset
3.2. The Multi-Differentiation Capability of PDLSCs and DPSCs
3.3. PDLSCs and DPSCs Show Comparable Angiogenic Potential
3.4. VEGF Release by PDLSCs and DPSCs
3.5. PDLSCs and DPSCs Promote HMEC-1 Vessel-like Structures in Co-Cultures
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Poliwoda, S.; Noor, N.; Downs, E.; Schaaf, A.; Cantwell, A.; Ganti, L.; Kaye, A.D.; Mosel, L.I.; Carroll, C.B.; Viswanath, O.; et al. Stem Cells: A Comprehensive Review of Origins and Emerging Clinical Roles in Medical Practice. Orthop. Rev. 2022, 14, 37498. [Google Scholar] [CrossRef] [PubMed]
- Dominici, M.; Le Blanc, K.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.C.; Krause, D.S.; Deans, R.J.; Keating, A.; Prockop, D.J.; Horwitz, E.M. Minimal Criteria for Defining Multipotent Mesenchymal Stromal Cells. The International Society for Cellular Therapy Position Statement. Cytotherapy 2006, 8, 315–317. [Google Scholar] [CrossRef]
- Roato, I.; Chinigò, G.; Genova, T.; Munaron, L.; Mussano, F. Oral Cavity as a Source of Mesenchymal Stem Cells Useful for Regenerative Medicine in Dentistry. Biomedicines 2021, 9, 1085. [Google Scholar] [CrossRef] [PubMed]
- Creuzet, S.; Couly, G.; Le Douarin, N.M. Patterning the Neural Crest Derivatives during Development of the Vertebrate Head: Insights from Avian Studies. J. Anat. 2005, 207, 447–459. [Google Scholar] [CrossRef]
- Kaucka, M.; Ivashkin, E.; Gyllborg, D.; Zikmund, T.; Tesarova, M.; Kaiser, J.; Xie, M.; Petersen, J.; Pachnis, V.; Nicolis, S.K.; et al. Analysis of Neural Crest–Derived Clones Reveals Novel Aspects of Facial Development. Sci. Adv. 2016, 2, e1600060. [Google Scholar] [CrossRef] [PubMed]
- Kulesa, P.M.; Bailey, C.M.; Kasemeier-Kulesa, J.C.; McLennan, R. Cranial Neural Crest Migration: New Rules for an Old Road. Dev. Biol. 2010, 344, 543–554. [Google Scholar] [CrossRef]
- Noden, D.M.; Trainor, P.A. Relations and Interactions between Cranial Mesoderm and Neural Crest Populations. J. Anat. 2005, 207, 575–601. [Google Scholar] [CrossRef]
- Santagati, F.; Rijli, F.M. Cranial Neural Crest and the Building of the Vertebrate Head. Nat. Rev. Neurosci. 2003, 4, 806–818. [Google Scholar] [CrossRef]
- Catón, J.; Tucker, A.S. Current Knowledge of Tooth Development: Patterning and Mineralization of the Murine Dentition. J. Anat. 2009, 214, 502–515. [Google Scholar] [CrossRef]
- Miletich, I.; Sharpe, P.T. Neural Crest Contribution to Mammalian Tooth Formation. Birth Defects Res. Part C 2004, 72, 200–212. [Google Scholar] [CrossRef]
- Guo, J.; Jia, H. DNMT3A Transcriptionally Downregulated by KLF5 Alleviates LPS-Induced Inflammatory Response and Promotes Osteogenic Differentiation in hPDLSCs. J. Appl. Oral Sci. 2024, 32, e20240268. [Google Scholar] [CrossRef] [PubMed]
- Lan, X.; Wang, Y.; Yin, M. Enhancing Periodontal Ligament Regeneration via PDLSC Delivery Using Electrospun PCL/Collagen/Cellulose Acetate Scaffolds and Collagen Hydrogel Incorporated with Curcumin-Loaded ZIF-8 Nanoparticles. Int. J. Nanomed. 2025, 20, 887–906. [Google Scholar] [CrossRef] [PubMed]
- Bright, R.; Hynes, K.; Gronthos, S.; Bartold, P.M. Periodontal Ligament-derived Cells for Periodontal Regeneration in Animal Models: A Systematic Review. J. Periodontal Res. 2015, 50, 160–172. [Google Scholar] [CrossRef]
- Nagata, M.; Iwasaki, K.; Akazawa, K.; Komaki, M.; Yokoyama, N.; Izumi, Y.; Morita, I. Conditioned Medium from Periodontal Ligament Stem Cells Enhances Periodontal Regeneration. Tissue Eng. Part A 2017, 23, 367–377. [Google Scholar] [CrossRef]
- Iwasaki, K.; Komaki, M.; Yokoyama, N.; Tanaka, Y.; Taki, A.; Honda, I.; Kimura, Y.; Takeda, M.; Akazawa, K.; Oda, S.; et al. Periodontal Regeneration Using Periodontal Ligament Stem Cell-Transferred Amnion. Tissue Eng. Part A 2013, 20, 693–704. [Google Scholar] [CrossRef] [PubMed]
- Iwata, T.; Yamato, M.; Tsuchioka, H.; Takagi, R.; Mukobata, S.; Washio, K.; Okano, T.; Ishikawa, I. Periodontal Regeneration with Multi-Layered Periodontal Ligament-Derived Cell Sheets in a Canine Model. Biomaterials 2009, 30, 2716–2723. [Google Scholar] [CrossRef]
- Iwata, T.; Yamato, M.; Washio, K.; Yoshida, T.; Tsumanuma, Y.; Yamada, A.; Onizuka, S.; Izumi, Y.; Ando, T.; Okano, T.; et al. Periodontal Regeneration with Autologous Periodontal Ligament-Derived Cell Sheets—A Safety and Efficacy Study in Ten Patients. Regen. Ther. 2018, 9, 38–44. [Google Scholar] [CrossRef]
- Itoh, Y.; Sasaki, J.I.; Hashimoto, M.; Katata, C.; Hayashi, M.; Imazato, S. Pulp Regeneration by 3-Dimensional Dental Pulp Stem Cell Constructs. J. Dent. Res. 2018, 97, 1137–1143. [Google Scholar] [CrossRef]
- Aimetti, M.; Ferrarotti, F.; Mariani, G.M.; Cricenti, L.; Romano, F. Use of Dental Pulp Stem Cells/Collagen Sponge Biocomplex in the Treatment of Non-Contained Intrabony Defects: A Case Series. Clin. Adv. Periodontics 2015, 5, 104–109. [Google Scholar] [CrossRef]
- Huang, G.T.-J.; Liu, J.; Zhu, X.; Yu, Z.; Li, D.; Chen, C.-A.; Azim, A.A. Pulp/Dentin Regeneration: It Should Be Complicated. J. Endod. 2020, 46, S128–S134. [Google Scholar] [CrossRef]
- Han, Y.; Xu, J.; Chopra, H.; Zhang, Z.; Dubey, N.; Dissanayaka, W.L.; Nör, J.E.; Bottino, M.C. Injectable Tissue-Specific Hydrogel System for Pulp–Dentin Regeneration. J. Dent. Res. 2024, 103, 398–408. [Google Scholar] [CrossRef] [PubMed]
- Krivanek, J.; Soldatov, R.A.; Kastriti, M.E.; Chontorotzea, T.; Herdina, A.N.; Petersen, J.; Szarowska, B.; Landova, M.; Matejova, V.K.; Holla, L.I.; et al. Dental Cell Type Atlas Reveals Stem and Differentiated Cell Types in Mouse and Human Teeth. Nat. Commun. 2020, 11, 4816. [Google Scholar] [CrossRef]
- Kotova, A.V.; Lobov, A.A.; Dombrovskaya, J.A.; Sannikova, V.Y.; Ryumina, N.A.; Klausen, P.; Shavarda, A.L.; Malashicheva, A.B.; Enukashvily, N.I. Comparative Analysis of Dental Pulp and Periodontal Stem Cells: Differences in Morphology, Functionality, Osteogenic Differentiation and Proteome. Biomedicines 2021, 9, 1606. [Google Scholar] [CrossRef] [PubMed]
- Amghar-Maach, S.; Gay-Escoda, C.; Sanchez-Garces, M. Regeneration of Periodontal Bone Defects with Dental Pulp Stem Cells Grafting: Systematic Review. J. Clin. Exp. Dent. 2019, 11, e373. [Google Scholar] [CrossRef]
- David, L.; Polo, J.M. Phases of Reprogramming. Stem Cell Res. 2014, 12, 754–761. [Google Scholar] [CrossRef]
- Shekatkar, M.R.; Kheur, S.M.; Kharat, A.H.; Deshpande, S.S.; Sanap, A.P.; Kheur, M.G.; Bhonde, R.R. Assessment of Angiogenic Potential of Mesenchymal Stem Cells Derived Conditioned Media from Various Oral Sources. J. Clin. Transl. Res. 2022, 8, 323. [Google Scholar] [CrossRef]
- 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, 524–531. [Google Scholar] [CrossRef] [PubMed]
- Bergamo, E.T.P.; Zahoui, A.; Barrera, R.B.; Huwais, S.; Coelho, P.G.; Karateew, E.D.; Bonfante, E.A. Osseodensification Effect on Implants Primary and Secondary Stability: Multicenter Controlled Clinical Trial. Clin. Implant Dent. Relat. Res. 2021, 23, 317–328. [Google Scholar] [CrossRef]
- Saghiri, M.A.; Asatourian, A.; Sorenson, C.M.; Sheibani, N. Role of Angiogenesis in Endodontics: Contributions of Stem Cells and Proangiogenic and Antiangiogenic Factors to Dental Pulp Regeneration. J. Endod. 2015, 41, 797–803. [Google Scholar] [CrossRef]
- Emerson, D.; Rentz, J.A.; Lilburn, T.G.; Davis, R.E.; Aldrich, H.; Chan, C.; Moyer, C.L. A Novel Lineage of Proteobacteria Involved in Formation of Marine Fe-Oxidizing Microbial Mat Communities. PLoS ONE 2007, 2, e667. [Google Scholar] [CrossRef]
- Li, A.; Sasaki, J.-I.; Huang, H.; Abe, G.L.; Inubushi, T.; Takahashi, Y.; Hayashi, M.; Imazato, S. Effect of Heparan Sulfate on Vasculogenesis and Dentinogenesis of Dental Pulp Stem Cells. J. Endod. 2024, 50, 1108–1116. [Google Scholar] [CrossRef] [PubMed]
- Yeasmin, S.; Ceccarelli, J.; Vigen, M.; Carrion, B.; Putnam, A.J.; Tarle, S.A.; Kaigler, D. Stem Cells Derived from Tooth Periodontal Ligament Enhance Functional Angiogenesis by Endothelial Cells. Tissue Eng. Part A 2014, 20, 1188–1196. [Google Scholar] [CrossRef]
- Roato, I.; Baima, G.; Orrico, C.; Mosca Balma, A.; Alotto, D.; Romano, F.; Ferracini, R.; Aimetti, M.; Mussano, F. Senescent Markers Expressed by Periodontal Ligament-Derived Stem Cells (PDLSCs) Harvested from Patients with Periodontitis Can Be Rejuvenated by RG108. Biomedicines 2023, 11, 2535. [Google Scholar] [CrossRef]
- Petrillo, S.; Genova, T.; Chinigò, G.; Roato, I.; Scarpellino, G.; Kopecka, J.; Altruda, F.; Tolosano, E.; Riganti, C.; Mussano, F.; et al. Endothelial Cells Promote Osteogenesis by Establishing a Functional and Metabolic Coupling With Human Mesenchymal Stem Cells. Front. Physiol. 2022, 12, 813547. [Google Scholar] [CrossRef]
- Carpentier, G.; Berndt, S.; Ferratge, S.; Rasband, W.; Cuendet, M.; Uzan, G.; Albanese, P. Angiogenesis Analyzer for ImageJ—A Comparative Morphometric Analysis of “Endothelial Tube Formation Assay” and “Fibrin Bead Assay”. Sci. Rep. 2020, 10, 11568. [Google Scholar] [CrossRef]
- Crisan, M.; Yap, S.; Casteilla, L.; Chen, C.-W.; Corselli, M.; Park, T.S.; Andriolo, G.; Sun, B.; Zheng, B.; Zhang, L.; et al. A Perivascular Origin for Mesenchymal Stem Cells in Multiple Human Organs. Cell Stem Cell 2008, 3, 301–313. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, K.; Komaki, M.; Yokoyama, N.; Tanaka, Y.; Taki, A.; Kimura, Y.; Takeda, M.; Oda, S.; Izumi, Y.; Morita, I. Periodontal Ligament Stem Cells Possess the Characteristics of Pericytes. J. Periodontol. 2013, 84, 1425–1433. [Google Scholar] [CrossRef]
- Cao, G.; O’Brien, C.D.; Zhou, Z.; Sanders, S.M.; Greenbaum, J.N.; Makrigiannakis, A.; DeLisser, H.M. Involvement of Human PECAM-1 in Angiogenesis and in Vitro Endothelial Cell Migration. Am. J. Physiol.-Cell Physiol. 2002, 282, C1181–C1190. [Google Scholar] [CrossRef]
- Oh, M.; Zhang, Z.; Mantesso, A.; Oklejas, A.E.; Nör, J.E. Endothelial-Initiated Crosstalk Regulates Dental Pulp Stem Cell Self-Renewal. J. Dent. Res. 2020, 99, 1102–1111. [Google Scholar] [CrossRef]
- Zhang, Z.; Oh, M.; Sasaki, J.-I.; Nör, J.E. Inverse and Reciprocal Regulation of P53/P21 and Bmi-1 Modulates Vasculogenic Differentiation of Dental Pulp Stem Cells. Cell Death Dis. 2021, 12, 644. [Google Scholar] [CrossRef] [PubMed]
- Armulik, A.; Abramsson, A.; Betsholtz, C. Endothelial/Pericyte Interactions. Circ. Res. 2005, 97, 512–523. [Google Scholar] [CrossRef] [PubMed]
- Gaengel, K.; Genové, G.; Armulik, A.; Betsholtz, C. Endothelial-Mural Cell Signaling in Vascular Development and Angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2009, 29, 630–638. [Google Scholar] [CrossRef]
- Oh, M.; Nör, J.E. The Perivascular Niche and Self-Renewal of Stem Cells. Front. Physiol. 2015, 6, 367. [Google Scholar] [CrossRef]
- Jafar, H.; Abuarqoub, D.; Ababneh, N.; Hasan, M.; Al-Sotari, S.; Aslam, N.; Kailani, M.; Ammoush, M.; Shraideh, Z.; Awidi, A. hPL Promotes Osteogenic Differentiation of Stem Cells in 3D Scaffolds. PLoS ONE 2019, 14, e0215667. [Google Scholar] [CrossRef]
- Bakopoulou, A.; Apatzidou, D.; Aggelidou, E.; Gousopoulou, E.; Leyhausen, G.; Volk, J.; Kritis, A.; Koidis, P.; Geurtsen, W. Isolation and Prolonged Expansion of Oral Mesenchymal Stem Cells under Clinical-Grade, GMP-Compliant Conditions Differentially Affects “Stemness” Properties. Stem Cell Res Ther 2017, 8, 247. [Google Scholar] [CrossRef] [PubMed]
- Aydin, S.; Şahin, F. Stem Cells Derived from Dental Tissues. In Cell Biology and Translational Medicine, Volume 5; Turksen, K., Ed.; Advances in Experimental Medicine and Biology; Springer International Publishing: Cham, Switzerland, 2019; Volume 1144, pp. 123–132. ISBN 978-3-030-17588-7. [Google Scholar]
- Sui, B.; Wu, D.; Xiang, L.; Fu, Y.; Kou, X.; Shi, S. Dental Pulp Stem Cells: From Discovery to Clinical Application. J. Endod. 2020, 46, S46–S55. [Google Scholar] [CrossRef]
- Vasandan, A.B.; Shankar, S.R.; Prasad, P.; Sowmya Jahnavi, V.; Bhonde, R.R.; Jyothi Prasanna, S. Functional Differences in Mesenchymal Stromal Cells from Human Dental Pulp and Periodontal Ligament. J. Cell. Mol. Med. 2014, 18, 344–354. [Google Scholar] [CrossRef]
- 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, 6332–6343. [Google Scholar] [CrossRef]
- Ng, Y.; Krilleke, D.; Shima, D. VEGF Function in Vascular Pathogenesis. Exp. Cell Res. 2006, 312, 527–537. [Google Scholar] [CrossRef]
- Zhao, Z.; Sun, Y.; Qiao, Q.; Zhang, L.; Xie, X.; Weir, M.D.; Schneider, A.; Xu, H.H.K.; Zhang, N.; Zhang, K.; et al. Human Periodontal Ligament Stem Cell and Umbilical Vein Endothelial Cell Co-Culture to Prevascularize Scaffolds for Angiogenic and Osteogenic Tissue Engineering. Int. J. Mol. Sci. 2021, 22, 12363. [Google Scholar] [CrossRef]
- Malyaran, H.; Radermacher, C.; Craveiro, R.B.; Kühnel, M.P.; Jonigk, D.; Wolf, M.; Neuss, S. Angiogenic Potential in Periodontal Stem Cells from Upper and Lower Jaw: A Pilot Study. J. Periodontol. 2024, 95, 662–672. [Google Scholar] [CrossRef] [PubMed]
- Bae, Y.-K.; Kim, G.-H.; Lee, J.C.; Seo, B.-M.; Joo, K.-M.; Lee, G.; Nam, H. The Significance of SDF-1α-CXCR4 Axis in in Vivo Angiogenic Ability of Human Periodontal Ligament Stem Cells. Mol. Cells 2017, 40, 386–392. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.-H.; Kim, G.-H.; Kim, J.-W.; Pyeon, H.J.; Lee, J.C.; Lee, G.; Nam, H. In Vivo Angiogenic Capacity of Stem Cells from Human Exfoliated Deciduous Teeth with Human Umbilical Vein Endothelial Cells. Mol. Cells 2016, 39, 790–796. [Google Scholar] [CrossRef] [PubMed]
- Bronckaers, A.; Hilkens, P.; Martens, W.; Gervois, P.; Ratajczak, J.; Struys, T.; Lambrichts, I. Mesenchymal Stem/Stromal Cells as a Pharmacological and Therapeutic Approach to Accelerate Angiogenesis. Pharmacol. Ther. 2014, 143, 181–196. [Google Scholar] [CrossRef]
- Martínez-Sarrà, E.; Montori, S.; Gil-Recio, C.; Núñez-Toldrà, R.; Costamagna, D.; Rotini, A.; Atari, M.; Luttun, A.; Sampaolesi, M. Human Dental Pulp Pluripotent-like Stem Cells Promote Wound Healing and Muscle Regeneration. Stem Cell Res. Ther. 2017, 8, 175. [Google Scholar] [CrossRef]
- Zhu, G.; Meng, H.; Yang, Y.; Yuwen, Q.; Zhou, Y.; Han, M.; Xia, X.; Song, S. Efficacy of Human Dental-Pulp MSCs Modified by Double-Genes on Wound Healing in Diabetic-Foot Model. Curr. Stem Cell Res. Ther. 2025, 20. [Google Scholar] [CrossRef]
- Iohara, K.; Zheng, L.; Wake, H.; Ito, M.; Nabekura, J.; Wakita, H.; Nakamura, H.; Into, T.; Matsushita, K.; Nakashima, M. A Novel Stem Cell Source for Vasculogenesis in Ischemia: Subfraction of Side Population Cells from Dental Pulp. Stem Cells 2008, 26, 2408–2418. [Google Scholar] [CrossRef]
- Di, T.; Wang, L.; Cheng, B.; Guo, M.; Feng, C.; Wu, Z.; Wang, L.; Chen, Y. Single-Cell RNA Sequencing Reveals Vascularization-Associated Cell Subpopulations in Dental Pulp: PDGFRβ+ DPSCs with Activated PI3K/AKT Pathway. Stem Cells 2024, 42, 914–927. [Google Scholar] [CrossRef]
- Barabaschi, G.D.G.; Manoharan, V.; Li, Q.; Bertassoni, L.E. Engineering Pre-Vascularized Scaffolds for Bone Regeneration. In Engineering Mineralized and Load Bearing Tissues; Bertassoni, L.E., Coelho, P.G., Eds.; Advances in Experimental Medicine and Biology; Springer International Publishing: Cham, Switzerland, 2015; Volume 881, pp. 79–94. ISBN 978-3-319-22344-5. [Google Scholar]
- Dissanayaka, W.L.; Zhan, X.; Zhang, C.; Hargreaves, K.M.; Jin, L.; Tong, E.H.Y. Coculture of Dental Pulp Stem Cells with Endothelial Cells Enhances Osteo-/Odontogenic and Angiogenic Potential In Vitro. J. Endod. 2012, 38, 454–463. [Google Scholar] [CrossRef]
- Du, L.; Feng, R.; Ge, S. PTH / SDF-1α Cotherapy Promotes Proliferation, Migration and Osteogenic Differentiation of Human Periodontal Ligament Stem Cells. Cell Prolif. 2016, 49, 599–608. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Zhang, Y.; Wan, C.; Sun, Z.; Nie, S.; Jian, S.; Zhang, L.; Song, G.; Chen, Z. Autophagy in SDF-1α-Mediated DPSC Migration and Pulp Regeneration. Biomaterials 2015, 44, 11–23. [Google Scholar] [CrossRef] [PubMed]
- Du, L.; Yang, P.; Ge, S. Stromal Cell–Derived Factor-1 Significantly Induces Proliferation, Migration, and Collagen Type I Expression in a Human Periodontal Ligament Stem Cell Subpopulation. J. Periodontol. 2012, 83, 379–388. [Google Scholar] [CrossRef] [PubMed]
- Das, R.; Jahr, H.; Van Osch, G.J.V.M.; Farrell, E. The Role of Hypoxia in Bone Marrow–Derived Mesenchymal Stem Cells: Considerations for Regenerative Medicine Approaches. Tissue Eng. Part B Rev. 2010, 16, 159–168. [Google Scholar] [CrossRef] [PubMed]
- Grunewald, M.; Avraham, I.; Dor, Y.; Bachar-Lustig, E.; Itin, A.; Yung, S.; Chimenti, S.; Landsman, L.; Abramovitch, R.; Keshet, E. VEGF-Induced Adult Neovascularization: Recruitment, Retention, and Role of Accessory Cells. Cell 2006, 124, 175–189. [Google Scholar] [CrossRef]
- Zhang, L.; Zhou, Y.; Sun, X.; Zhou, J.; Yang, P. CXCL12 Overexpression Promotes the Angiogenesis Potential of Periodontal Ligament Stem Cells. Sci. Rep. 2017, 7, 10286. [Google Scholar] [CrossRef]
- Nam, H.; Kim, G.-H.; Bae, Y.-K.; Jeong, D.-E.; Joo, K.-M.; Lee, K.; Lee, S.-H. Angiogenic Capacity of Dental Pulp Stem Cell Regulated by SDF-1 α -CXCR4 Axis. Stem Cells Int. 2017, 2017, 1–10. [Google Scholar] [CrossRef]
- Zhu, L.; Dissanayaka, W.L.; 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, 2497–2509. [Google Scholar] [CrossRef]
- Kim, J.Y.; Xin, X.; Moioli, E.K.; Chung, J.; Lee, C.H.; Chen, M.; Fu, S.Y.; Koch, P.D.; Mao, J.J. Regeneration of Dental-Pulp-like Tissue by Chemotaxis-Induced Cell Homing. Tissue Eng. Part A 2010, 16, 3023–3031. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Roato, I.; Orrico, C.; Meinardi, S.; Pedraza, R.; Mosca Balma, A.; Baima, G.; Genova, T.; Aimetti, M.; Mussano, F. The Pro-Angiogenic Potential of Periodontal Ligament Stem Cells and Dental Pulp Stem Cells: A Comparative Analysis. Cells 2025, 14, 864. https://doi.org/10.3390/cells14120864
Roato I, Orrico C, Meinardi S, Pedraza R, Mosca Balma A, Baima G, Genova T, Aimetti M, Mussano F. The Pro-Angiogenic Potential of Periodontal Ligament Stem Cells and Dental Pulp Stem Cells: A Comparative Analysis. Cells. 2025; 14(12):864. https://doi.org/10.3390/cells14120864
Chicago/Turabian StyleRoato, Ilaria, Clarissa Orrico, Sara Meinardi, Riccardo Pedraza, Alessandro Mosca Balma, Giacomo Baima, Tullio Genova, Mario Aimetti, and Federico Mussano. 2025. "The Pro-Angiogenic Potential of Periodontal Ligament Stem Cells and Dental Pulp Stem Cells: A Comparative Analysis" Cells 14, no. 12: 864. https://doi.org/10.3390/cells14120864
APA StyleRoato, I., Orrico, C., Meinardi, S., Pedraza, R., Mosca Balma, A., Baima, G., Genova, T., Aimetti, M., & Mussano, F. (2025). The Pro-Angiogenic Potential of Periodontal Ligament Stem Cells and Dental Pulp Stem Cells: A Comparative Analysis. Cells, 14(12), 864. https://doi.org/10.3390/cells14120864