Effect of Titanium and Zirconia Nanoparticles on Human Gingival Mesenchymal Stromal Cells
Abstract
:1. Introduction
2. Results
2.1. Cell Proliferation and Viability
2.2. Live–Dead Staining
2.3. Focal Adhesion Staining
2.4. Effect of NPs on the Basal Production of IL-6, IL-8, and MCP-1 in hG-MSCs
2.5. Effect of NPs on the P. gingivalis LPS-Induced Production of IL-6, IL-8, and MCP-1 in hG-MSCs
3. Discussion
4. Materials and Methods
4.1. Ethical Consideration
4.2. Cell Isolation
4.3. Nanoparticles
4.4. Cell Seeding and Stimulation
4.5. Cell Proliferation and Viability
4.6. Live–Dead Staining
4.7. Focal Adhesion Staining
4.8. Production of Inflammatory Mediators by hG-MSCs
4.9. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Howe, M.-S.; Keys, W.; Richards, D. Long-term (10-year) dental implant survival: A systematic review and sensitivity meta-analysis. J. Dent. 2019, 84, 9–21. [Google Scholar] [CrossRef] [PubMed]
- Buser, D.; Sennerby, L.; De Bruyn, H. Modern implant dentistry based on osseointegration: 50 years of progress, current trends and open questions. Periodontology 2000 2017, 73, 7–21. [Google Scholar] [CrossRef] [PubMed]
- Steinemann, S.G. Titanium—The material of choice? Periodontology 2000, 17, 7–21. [Google Scholar] [CrossRef] [PubMed]
- Cionca, N.; Hashim, D.; Mombelli, A. Zirconia dental implants: Where are we now, and where are we heading? Periodontology 2000 2017, 73, 241–258. [Google Scholar] [CrossRef]
- Özkurt, Z.; Kazazoğlu, E. Zirconia Dental Implants: A Literature Review. J. Oral Implantol. 2011, 37, 367–376. [Google Scholar] [CrossRef]
- Welander, M.; Abrahamsson, I.; Berglundh, T. The mucosal barrier at implant abutments of different materials. Clin. Oral Implant. Res. 2008, 19, 635–641. [Google Scholar] [CrossRef]
- Roehling, S.; Schlegel, K.A.; Woelfler, H.; Gahlert, M. Zirconia compared to titanium dental implants in preclinical studies—A systematic review and meta-analysis. Clin. Oral Implant. Res. 2019, 30, 365–395. [Google Scholar] [CrossRef]
- Grassi, F.R.; Capogreco, M.; Consonni, D.; Bilardi, G.; Buti, J.; Kalemaj, Z. Immediate occlusal loading of one-piece zirconia implants: Five-year radiographic and clinical evaluation. Int. J. Oral Maxillofac. Implant. 2015, 30, 671–680. [Google Scholar] [CrossRef]
- Albrektsson, T.; Wennerberg, A. On osseointegration in relation to implant surfaces. Clin. Implant. Dent. Relat. Res. 2019, 21 (Suppl. 1), 4–7. [Google Scholar] [CrossRef]
- Smeets, R.; Stadlinger, B.; Schwarz, F.; Beck-Broichsitter, B.; Jung, O.; Precht, C.; Kloss, F.; Gröbe, A.; Heiland, M.; Ebker, T. Impact of Dental Implant Surface Modifications on Osseointegration. BioMed Res. Int. 2016, 2016, 6285620. [Google Scholar] [CrossRef] [Green Version]
- Bosshardt, D.D.; Chappuis, V.; Buser, D. Osseointegration of titanium, titanium alloy and zirconia dental implants: Current knowledge and open questions. Periodontology 2000 2017, 73, 22–40. [Google Scholar] [CrossRef]
- Guo, T.; Gulati, K.; Arora, H.; Han, P.; Fournier, B.; Ivanovski, S. Race to invade: Understanding soft tissue integration at the transmucosal region of titanium dental implants. Dent. Mater. 2021, 37, 816–831. [Google Scholar] [CrossRef] [PubMed]
- Ivanovski, S.; Lee, R. Comparison of peri-implant and periodontal marginal soft tissues in health and disease. Periodontology 2000 2018, 76, 116–130. [Google Scholar] [CrossRef] [PubMed]
- Guo, T.; Gulati, K.; Arora, H.; Han, P.; Fournier, B.; Ivanovski, S. Orchestrating soft tissue integration at the transmucosal region of titanium implants. Acta Biomater. 2021, 124, 33–49. [Google Scholar] [CrossRef] [PubMed]
- Sgolastra, F.; Petrucci, A.; Severino, M.; Gatto, R.; Monaco, A. Periodontitis, implant loss and peri-implantitis. A meta-analysis. Clin. Oral Implant. Res. 2015, 26, e8–e16. [Google Scholar] [CrossRef] [PubMed]
- Derks, J.; Tomasi, C. Peri-implant health and disease. A systematic review of current epidemiology. J. Clin. Periodontol. 2015, 42 (Suppl. S16), S158–S171. [Google Scholar] [CrossRef]
- Kotsakis, G.A.; Olmedo, D.G. Peri-implantitis is not periodontitis: Scientific discoveries shed light on microbiome-biomaterial interactions that may determine disease phenotype. Periodontology 2000 2021, 86, 231–240. [Google Scholar] [CrossRef]
- Belibasakis, G.N.; Manoil, D. Microbial Community-Driven Etiopathogenesis of Peri-Implantitis. J. Dent. Res. 2021, 100, 21–28. [Google Scholar] [CrossRef]
- Mombelli, A.; Hashim, D.; Cionca, N. What is the impact of titanium particles and biocorrosion on implant survival and complications? A critical review. Clin. Oral Implant. Res. 2018, 29 (Suppl. 18), 37–53. [Google Scholar] [CrossRef]
- Noronha Oliveira, M.; Schunemann, W.V.H.; Mathew, M.T.; Henriques, B.; Magini, R.S.; Teughels, W.; Souza, J.C.M. Can degradation products released from dental implants affect peri-implant tissues? J. Periodontal Res. 2018, 53, 1–11. [Google Scholar] [CrossRef]
- Franchi, M.; Bacchelli, B.; Martini, D.; De Pasquale, V.; Orsini, E.; Ottani, V.; Fini, M.; Giavaresi, G.; Giardino, R.; Ruggeri, A. Early detachment of titanium particles from various different surfaces of endosseous dental implants. Biomaterials 2004, 25, 2239–2246. [Google Scholar] [CrossRef]
- Souza, J.C.; Barbosa, S.L.; Ariza, E.A.; Henriques, M.; Teughels, W.; Ponthiaux, P.; Celis, J.-P.; Rocha, L.A. How do titanium and Ti6Al4V corrode in fluoridated medium as found in the oral cavity? An in vitro study. Mater. Sci. Eng. C Mater. Biol. Appl. 2015, 47, 384–393. [Google Scholar] [CrossRef]
- Barrak, F.N.; Li, S.; Muntane, A.M.; Jones, J.R. Particle release from implantoplasty of dental implants and impact on cells. Int. J. Implant Dent. 2020, 6, 50. [Google Scholar] [CrossRef]
- Bressan, E.; Ferroni, L.; Gardin, C.; Bellin, G.; Sbricoli, L.; Sivolella, S.; Brunello, G.; Schwartz-Arad, D.; Mijiritsky, E.; Penarrocha, M.; et al. Metal Nanoparticles Released from Dental Implant Surfaces: Potential Contribution to Chronic Inflammation and Peri-Implant Bone Loss. Materials 2019, 12, 2036. [Google Scholar] [CrossRef]
- Suárez-López del Amo, F.; Garaicoa-Pazmiño, C.; Fretwurst, T.; Castilho, R.M.; Squarize, C.H. Dental implants-associated release of titanium particles: A systematic review. Clin. Oral Implant. Res. 2018, 29, 1085–1100. [Google Scholar] [CrossRef]
- He, X.; Reichl, F.-X.; Milz, S.; Michalke, B.; Wu, X.; Sprecher, C.M.; Yang, Y.; Gahlert, M.; Röhling, S.; Kniha, H.; et al. Titanium and zirconium release from titanium- and zirconia implants in mini pig maxillae and their toxicity in vitro. Dent. Mater. 2020, 36, 402–412. [Google Scholar] [CrossRef]
- Okuda-Shimazaki, J.; Takaku, S.; Kanehira, K.; Sonezaki, S.; Taniguchi, A. Effects of Titanium Dioxide Nanoparticle Aggregate Size on Gene Expression. Int. J. Mol. Sci. 2010, 11, 2383–2392. [Google Scholar] [CrossRef]
- Chiquet, M.; Katsaros, C.; Kletsas, D. Multiple functions of gingival and mucoperiosteal fibroblasts in oral wound healing and repair. Periodontology 2000 2015, 68, 21–40. [Google Scholar] [CrossRef]
- Andrukhov, O.; Behm, C.; Blufstein, A.; Rausch-Fan, X. Immunomodulatory properties of dental tissue-derived mesenchymal stem cells: Implication in disease and tissue regeneration. World J. Stem Cells 2019, 11, 604–617. [Google Scholar] [CrossRef]
- Andrukhov, O.; Behm, C.; Blufstein, A.; Wehner, C.; Gahn, J.; Pippenger, B.; Wagner, R.; Rausch-Fan, X. Effect of implant surface material and roughness to the susceptibility of primary gingival fibroblasts to inflammatory stimuli. Dent. Mater. 2020, 36, e194–e205. [Google Scholar] [CrossRef]
- Gómez-Florit, M.; Ramis, J.M.; Xing, R.; Taxt-Lamolle, S.; Haugen, H.J.; Lyngstadaas, S.P.; Monjo, M. Differential response of human gingival fibroblasts to titanium- and titanium-zirconium-modified surfaces. J. Periodontal Res. 2014, 49, 425–436. [Google Scholar] [CrossRef] [PubMed]
- Rausch, M.; Shokoohi-Tabrizi, H.; Wehner, C.; Pippenger, B.E.; Wagner, R.S.; Ulm, C.; Moritz, A.; Chen, J.; Andrukhov, O. Impact of Implant Surface Material and Microscale Roughness on the Initial Attachment and Proliferation of Primary Human Gingival Fibroblasts. Biology 2021, 10, 356. [Google Scholar] [CrossRef] [PubMed]
- Happe, A.; Sielker, S.; Hanisch, M.; Jung, S. The Biologic Effect of Particulate Titanium Contaminants of Dental Implants on Human Osteoblasts and Gingival Fibroblasts. Int. J. Oral Maxillofac. Implant. 2019, 34, 673–680. [Google Scholar] [CrossRef] [PubMed]
- Irshad, M.; Scheres, N.; Crielaard, W.; Loos, B.G.; Wismeijer, D.; Laine, M.L. Influence of titanium on in vitro fibroblast-Porphyromonas gingivalis interaction in peri-implantitis. J. Clin. Periodontol. 2013, 40, 841–849. [Google Scholar] [CrossRef]
- Schwarz, F.; Langer, M.; Hagena, T.; Hartig, B.; Sader, R.; Becker, J. Cytotoxicity and proinflammatory effects of titanium and zirconia particles. Int. J. Implant Dent. 2019, 5, 25. [Google Scholar] [CrossRef]
- Lafaurie, G.I.; Sabogal, M.A.; Castillo, D.M.; Rincón, M.V.; Gómez, L.A.; Lesmes, Y.A.; Chambrone, L. Microbiome and Microbial Biofilm Profiles of Peri-Implantitis: A Systematic Review. J. Periodontol. 2017, 88, 1066–1089. [Google Scholar] [CrossRef]
- Hattori, K.; Nakadate, K.; Morii, A.; Noguchi, T.; Ogasawara, Y.; Ishii, K. Exposure to nano-size titanium dioxide causes oxidative damages in human mesothelial cells: The crystal form rather than size of particle contributes to cytotoxicity. Biochem. Biophys. Res. Commun. 2017, 492, 218–223. [Google Scholar] [CrossRef]
- Kilian, K.A.; Bugarija, B.; Lahn, B.T.; Mrksich, M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl. Acad. Sci. USA 2010, 107, 4872–4877. [Google Scholar] [CrossRef]
- Taira, M.; Kagiya, T.; Harada, H.; Sasaki, M.; Kimura, S.; Narushima, T.; Nezu, T.; Araki, Y. Microscopic observations and inflammatory cytokine productions of human macrophage phagocytising submicron titanium particles. J. Mater. Sci. Mater. Med. 2010, 21, 267–275. [Google Scholar] [CrossRef]
- Eger, M.; Sterer, N.; Liron, T.; Kohavi, D.; Gabet, Y. Scaling of titanium implants entrains inflammation-induced osteolysis. Sci. Rep. 2017, 7, 39612. [Google Scholar] [CrossRef]
- Pettersson, M.; Kelk, P.; Belibasakis, G.N.; Bylund, D.; Molin Thorén, M.; Johansson, A. Titanium ions form particles that activate and execute interleukin-1β release from lipopolysaccharide-primed macrophages. J. Periodontal Res. 2017, 52, 21–32. [Google Scholar] [CrossRef] [PubMed]
- Delgado-Ruiz, R.; Romanos, G. Potential Causes of Titanium Particle and Ion Release in Implant Dentistry: A Systematic Review. Int. J. Mol. Sci. 2018, 19, 3585. [Google Scholar] [CrossRef]
- He, X.; Reichl, F.-X.; Wang, Y.; Michalke, B.; Milz, S.; Yang, Y.; Stolper, P.; Lindemaier, G.; Graw, M.; Hickel, R.; et al. Analysis of titanium and other metals in human jawbones with dental implants—A case series study. Dent. Mater. 2016, 32, 1042–1051. [Google Scholar] [CrossRef] [PubMed]
- Gustafson, H.H.; Holt-Casper, D.; Grainger, D.W.; Ghandehari, H. Nanoparticle uptake: The phagocyte problem. Nano Today 2015, 10, 487–510. [Google Scholar] [CrossRef]
- Albrektsson, T.; Jemt, T.; Mölne, J.; Tengvall, P.; Wennerberg, A. On inflammation-immunological balance theory-A critical apprehension of disease concepts around implants: Mucositis and marginal bone loss may represent normal conditions and not necessarily a state of disease. Clin. Implant Dent. Relat. Res. 2018, 21, 183–189. [Google Scholar] [CrossRef]
- Ivanovski, S.; Bartold, P.M.; Huang, Y.S. The role of foreign body response in peri-implantitis: What is the evidence? Periodontology 2000 2022. [Google Scholar] [CrossRef]
- Fretwurst, T.; Buzanich, G.; Nahles, S.; Woelber, J.P.; Riesemeier, H.; Nelson, K. Metal elements in tissue with dental peri-implantitis: A pilot study. Clin. Oral Implant. Res. 2016, 27, 1178–1186. [Google Scholar] [CrossRef]
- Pettersson, M.; Pettersson, J.; Johansson, A.; Molin Thorén, M. Titanium release in peri-implantitis. J. Oral Rehabil. 2019, 46, 179–188. [Google Scholar] [CrossRef] [PubMed]
- Rakic, M.; Radunovic, M.; Petkovic-Curcin, A.; Tatic, Z.; Basta-Jovanovic, G.; Sanz, M. Study on the immunopathological effect of titanium particles in peri-implantitis granulation tissue: A case–control study. Clin. Oral Implant. Res. 2022, 33, 656–666. [Google Scholar] [CrossRef] [PubMed]
- Wennerberg, A.; Ide-Ektessabi, A.; Hatkamata, S.; Sawase, T.; Johansson, C.; Albrektsson, T.; Martinelli, A.; Sodervall, U.; Odelius, H. Titanium release from implants prepared with different surface roughness. An in vitro and in vivo study. Clin. Oral Implant. Res. 2004, 15, 505–512. [Google Scholar] [CrossRef] [PubMed]
- Alrabeah, G.; Knowles, J.; Petridis, H. Reduction of Tribocorrosion Products When Using the Platform-Switching Concept. J. Dent. Res. 2018, 97, 995–1002. [Google Scholar] [CrossRef] [PubMed]
- Behm, C.; Blufstein, A.; Abhari, S.Y.; Koch, C.; Gahn, J.; Schäffer, C.; Moritz, A.; Rausch-Fan, X.; Andrukhov, O. Response of Human Mesenchymal Stromal Cells from Periodontal Tissue to LPS Depends on the Purity but Not on the LPS Source. Mediat. Inflamm. 2020, 2020, 8704896. [Google Scholar] [CrossRef] [PubMed]
- Blufstein, A.; Behm, C.; Kubin, B.; Gahn, J.; Moritz, A.; Rausch-Fan, X.; Andrukhov, O. Anti-apoptotic effects of human gingival mesenchymal stromal cells on polymorphonuclear leucocytes. Oral Dis. 2021, 28, 777–785. [Google Scholar] [CrossRef] [PubMed]
- Andrukhov, O.; Andrukhova, O.; Özdemir, B.; Haririan, H.; Müller-Kern, M.; Moritz, A.; Rausch-Fan, X. Soluble CD14 Enhances the Response of Periodontal Ligament Stem Cells to P. gingivalis Lipopolysaccharide. PLoS ONE 2016, 11, e0160848. [Google Scholar] [CrossRef]
- Zhang, F.; Özdemir, B.; Nguyen, P.Q.; Andrukhov, O.; Rausch-Fan, X. Methanandamide diminish the Porphyromonas gingivalis lipopolysaccharide induced response in human periodontal ligament cells. BMC Oral Health 2020, 20, 107. [Google Scholar] [CrossRef]
- Nemec, M.; Bartholomaeus, H.M.; Bertl, M.H.; Behm, C.; Shokoohi-Tabrizi, H.A.; Jonke, E.; Andrukhov, O.; Rausch-Fan, X. Behaviour of Human Oral Epithelial Cells Grown on Invisalign® SmartTrack® Material. Materials 2020, 13, 5311. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Nemec, M.; Behm, C.; Maierhofer, V.; Gau, J.; Kolba, A.; Jonke, E.; Rausch-Fan, X.; Andrukhov, O. Effect of Titanium and Zirconia Nanoparticles on Human Gingival Mesenchymal Stromal Cells. Int. J. Mol. Sci. 2022, 23, 10022. https://doi.org/10.3390/ijms231710022
Nemec M, Behm C, Maierhofer V, Gau J, Kolba A, Jonke E, Rausch-Fan X, Andrukhov O. Effect of Titanium and Zirconia Nanoparticles on Human Gingival Mesenchymal Stromal Cells. International Journal of Molecular Sciences. 2022; 23(17):10022. https://doi.org/10.3390/ijms231710022
Chicago/Turabian StyleNemec, Michael, Christian Behm, Vera Maierhofer, Jonas Gau, Anastasiya Kolba, Erwin Jonke, Xiaohui Rausch-Fan, and Oleh Andrukhov. 2022. "Effect of Titanium and Zirconia Nanoparticles on Human Gingival Mesenchymal Stromal Cells" International Journal of Molecular Sciences 23, no. 17: 10022. https://doi.org/10.3390/ijms231710022