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Clinical Oral Investigations

, Volume 21, Issue 9, pp 2695–2707 | Cite as

Novel potential scaffold for periodontal tissue engineering

  • Raquel OsorioEmail author
  • Camilo Andrés Alfonso-Rodríguez
  • Estrella Osorio
  • Antonio L. Medina-Castillo
  • Miguel Alaminos
  • Manuel Toledano-Osorio
  • Manuel Toledano
Original Article

Abstract

Objective

The objective of the study is characterization of novel calcium and zinc-loaded electrospun matrices to be used for periodontal regeneration.

Materials and methods

A polymethylmetacrylate-based membrane was calcium or zinc loaded. Matrices were characterized morphologically by atomic force and scanning electron microscopy and mechanically probed by a nanoindenter. Biomimetic calcium phosphate precipitation on polymeric tissues was assessed. Cell viability tests were performed using oral mucosa fibroblasts. Data were analyzed by Kruskal-Wallis and Mann-Whitney tests or by ANOVA and Student-Newman-Keuls multiple comparisons.

Results

Zinc and calcium loading on matrices did not modify their morphology but increased nanomechanical properties and decreased nanoroughness. Precipitation of calcium and phosphate on the matrix surfaces was observed in zinc-loaded specimens. Matrices were found to be non-toxic to cells in all the assays. Calcium- and zinc-loaded scaffolds presented a very low cytotoxic effect.

Conclusions

Zinc-loaded membranes permit cell viability and promoted mineral precipitation in physiological conditions. Based on the tested nanomechanical properties and scaffold architecture, the proposed membranes may be suitable for cell proliferation.

Clinical relevance

The ability of zinc-loaded matrices to promote precipitation of calcium phosphate deposits, together with their observed non-toxicity and its surface chemistry allowing covalent binding of proteins, may offer new strategies for periodontal regeneration.

Keywords

Regeneration Calcium Zinc Nanopolymers Scaffolds 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

Project MAT2014-52036-P supported by the Ministry of Economy and Competitiveness (MINECO) and European Regional Development Fund (FEDER).

Ethical approval

All procedures performed in the present study, involving human participants, were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Ivanovski S, Vaquette C, Gronthos S, Hutmacher DW, Bartold PM (2014) Multiphasic scaffolds for periodontal tissue engineering. J Dent Res 93(12):1212–1221. doi: 10.1177/0022034514544301 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Shimauchi H, Nemoto E, Ishihata H, Shimomura M (2013) Possible functional scaffolds for periodontal regeneration. Japan Dent Sci Rev 49:118–130. doi: 10.1016/j.jdsr.2013.05.001 CrossRefGoogle Scholar
  3. 3.
    Sam G, Pillai BRM (2014) Evolution of barrier membranes in periodontal regeneration—are the third generation membranes really here? J of Clin Diagn Res 8:14–17. doi: 10.7860/JCDR/2014/9957.5272 Google Scholar
  4. 4.
    Peng F, Yu X, Wei M (2011) In vitro cell performance on hydroxyapatite particles/poly(L-lactic acid) nanofibrous scaffolds with an excellent particle along nanofiber orientation. Acta Biomater 7:2585–2592. doi: 10.1016/j.actbio.2011.02.021 CrossRefPubMedGoogle Scholar
  5. 5.
    Gardin C, Ferroni L, Favero L, Stellini E, Stomaci D, Sivolella S, Bressan E, Zavan B (2012) Nanostructured biomaterials for tissue engineered bone tissue reconstruction. Int J Mol Sci 13:737–757. doi: 10.3390/ijms13010737 CrossRefPubMedGoogle Scholar
  6. 6.
    Lye KW, Tideman H, Wolke JC, Merkx MA, Chin FK, Jansen JA (2013) Biocompatibility and bone formation with porous modified PMMA in normal and irradiated mandibular tissue. Clin Oral Implants Res 24(Suppl A100):100–109. doi: 10.1111/j.1600-0501.2011.02388.x CrossRefPubMedGoogle Scholar
  7. 7.
    Punet X, Mauchauffé R, Rodríguez Cabello JC, Alonso M, Engel E, Mateos-Timoneda MA (2015) Biomolecular functionalization for enhanced cell–material interactions of poly(methyl methacrylate) surface. Regen Biomat 2:167–175. doi: 10.1093/rb/rbv014 CrossRefGoogle Scholar
  8. 8.
    Nandakumar A, Yang L, Habibovic P, van Blitterswijk C (2010) Calcium phosphate coated electrospun fiber matrices as scaffolds for bone tissue engineering. Langmuir 26:7380–7387. doi: 10.1021/ la904406b CrossRefPubMedGoogle Scholar
  9. 9.
    Seol YJ, Kim KH, Kang YM, Kim IA, Rhee SH (2009) Bioactivity, pre-osteoblastic cell responses, and osteoconductivity evaluations of the electrospun non-woven SiO2-CaO gel fabrics. J Biomed Mater Res B Appl Biomater 90:679–687. doi: 10.1002/jbm.b.31334 CrossRefPubMedGoogle Scholar
  10. 10.
    Münchow EA, Albuquerque MT, Zero B, Kamocki K, Piva E, Gregory RL, Bottino MC (2015) Development and characterization of novel ZnO-loaded electrospun membranes for periodontal regeneration. Dent Mater 31:1038–1051. doi: 10.1016/j.dental.2015.06.004 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Münchow EA, Pankajakshan D, Albuquerque MT, Kamocki K, Piva E, Gregory RL, Bottino MC (2016) Synthesis and characterization of CaO-loaded electrospun matrices for bone tissue engineering. Clin Oral Investig 20:1921–1933. doi: 10.1007/s00784-015-1671-5
  12. 12.
    Osorio E, Toledano M, Aguilera FS, Tay FR, Osorio R (2010) Ethanol wet-bonding technique sensitivity assessed by AFM. J Dent Res 89:1264–1269. doi: 10.1177/0022034510376403 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    ISO 23317:2012. Implants for surgery—in vitro evaluation for apatite-forming ability of implant materials. ISO-publisher, GenevaGoogle Scholar
  14. 14.
    Leonor IB, Balas F, Kawashita M, Reis RL, Kokubo T, Nakamura T (2009) Biomimetic apatite deposition on polymeric microspheres treated with a calcium silicate solution. J Biomed Mater Res B Appl Biomat 91:239–247. doi: 10.1002/jbm.b.31395 CrossRefGoogle Scholar
  15. 15.
    Han L, Grodzinsky AJ, Ortiz C (2011) Nanomechanics of the cartilage extracellular matrix. Annu Rev Mater Res 41:133–168. doi: 10.1146/annurev-matsci-062910-100431 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Macosko CW (1994) Rheology: principles, measurements, and applications. VCH, New York, p 568Google Scholar
  17. 17.
    Lopez-Lopez MT, Scionti G, Oliveira AC, Duran JD, Campos A, Alaminos M, Rodriguez IA (2015) Generation and characterization of novel magnetic field-responsive biomaterials. PLoS One 10:e0133878. doi: 10.1371/journal.pone.0133878 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Will J, Detsch R, Boccaccini AR (2013) In: Bandyopadhyay A, Bose S (eds) Structural and biological characterization of scaffolds. Elsevier, Oxford, p 437Google Scholar
  19. 19.
    Zhang Y, Zhang X, Shi B, Miron RJ (2013) Membranes for guided tissue and bone regeneration. Annals Oral & Maxillofac Surg 12:10–17Google Scholar
  20. 20.
    Bružauskaitė I, Bironaitė D, Bagdonas E, Bernotienė E (2016) Scaffolds and cells for tissue regeneration: different scaffold pore sizes-different cell effects. Cytotechnology 68:355–369. doi: 10.1007/s10616-015-9895-4 CrossRefPubMedGoogle Scholar
  21. 21.
    Woo KM, Chen VJ, Ma PX (2003) Nano-fibrous scaffolding architecture selectively enhances protein adsorption contributing to cell attachment. J Biomed Mater Res A 67:531–537. doi: 10.1002/jbm.a.10098 CrossRefPubMedGoogle Scholar
  22. 22.
    Ramon-Marquez T, Medina-Castillo AL, Fernandez-Gutierrez A, Fernandez-Sanchez JF (2016) A novel optical biosensor for direct and selective determination of serotonin in serum by solid surface-room temperature phosphorescence. Biosens Bioelectron 82:217–223. doi: 10.1016/j.bios.2016.04.008 CrossRefPubMedGoogle Scholar
  23. 23.
    Salehi S, Bahners T, Gutmann JS, Gao SL, Mäder E, Fuchsluger TA (2014) Characterization of structural, mechanical and nano-mechanical properties of electrospun PGS/PCL fibers. RSC Adv 4:16951. doi: 10.1039/C4RA01237B CrossRefGoogle Scholar
  24. 24.
    Fratzl P (2008) In: Fratzl P (ed) Collagen: structure and mechanics. Springer US, New York, p 131CrossRefGoogle Scholar
  25. 25.
    Polly BJ, Yuya PA, Akhter MP, Recker RR, Turner JA (2012) Intrinsic material properties of trabecular bone by nanoindentation testing of biopsies taken from healthy women before and after menopause. Calcif Tissue Int 90:286–293. doi: 10.1007/s00223-012-9575-8 CrossRefPubMedGoogle Scholar
  26. 26.
    Xu B, Chow MJ, Zhang Y (2011) Experimental and modeling study of collagen scaffolds with the effects of crosslinking and fiber alignment. Int J Biomat 2011:1–12. doi: 10.1155/2011/172389 CrossRefGoogle Scholar
  27. 27.
    Baker BM, Trappmann B, Wang WY, Sakar MS, Kim IL, Shenoy VB, Burdick JA, Chen CS (2015) Cell-mediated fibre recruitment drives extracellular matrix mechanosensing in engineered fibrillar microenvironments. Nat Mater 14:1262–1268. doi: 10.1038/nmat4444 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Baker SR, Banerjee S, Bonin K, Guthold M (2016) Determining the mechanical properties of electrospun poly-ε-caprolactone (PCL) nanofibers using AFM and a novel fiber anchoring technique. Mat Sci Engineer C 59:203–212. doi: 10.1016/j.msec.2015.09.102 CrossRefGoogle Scholar
  29. 29.
    Agrawal R, Nieto A, Chen H, Mora M, Agarwal A (2013) Nanoscale damping characteristics of boron nitride nanotubes and carbon nanotubes reinforced polymer composites. ACS Appl Mater Interfaces 27:12052–12057. doi: 10.1021/am4038678 CrossRefGoogle Scholar
  30. 30.
    Espino DM, Shepherd DET, Hukins DWL (2014) Viscoelastic properties of bovine knee joint articular cartilage: dependency on thickness and loading frequency. BMC Musculoskelet Disord 15:205. doi: 10.1186/1471-2474-15-205 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Winter HH (1987) Can the gel point of a cross-linking polymer be detected by the G′ – G″ crossover? Polym Eng Sci 27:1698–1702. doi: 10.1002/pen.760272209 CrossRefGoogle Scholar
  32. 32.
    Pietak AM, Reid JW, Stott MJ, Sayer M (2007) Silicon substitution in the calcium phosphate bioceramics. Biomaterials 28:4023–4032. doi: 10.1016/j.biomaterials.2007.05.003 CrossRefPubMedGoogle Scholar
  33. 33.
    Chai YC, Carlier A, Bolander J, Roberts SJ, Geris L, Schrooten J, Van Oosterwyck H, Luyten FP (2012) Current views on calcium phosphate osteogenicity and the translation into effective bone regeneration strategies. Acta Biomater 8:3876–3887. doi: 10.1016/j.actbio.2012.07.002 CrossRefPubMedGoogle Scholar
  34. 34.
    Tada H, Nemoto E, Kanaya S, Hamaji N, Sato H, Shimauchi H (2010) Elevated extracelular calcium increases expression of bone morphogenetic protein-2 gene via a calcium channel and ERK pathway in human dental pulp cells. Biochem Biophys Res Commun 394:1093–1097. doi: 10.1016/j.bbrc.2010.03
  35. 35.
    Kanaya S, Nemoto E, Sakisaka Y, Shimauchi H (2013) Calcium-mediated increased expression of fibroblast growth factor-2acts through NF-κB and PGE2/EP4 receptor signaling pathways in cementoblasts. Bone 56:398–405. doi: 10.1016/j.bone.2013.06.031 CrossRefPubMedGoogle Scholar
  36. 36.
    Riss TL, Moravec RA (2004) Use of multiple assay endpoints to investigate the effects of incubation time, dose of toxin, and plating density in cell-based cytotoxicity assays. ASSAY Drug Develop Technol 2:51–62. doi: 10.1089/154065804322966315 CrossRefGoogle Scholar
  37. 37.
    Bock N, Riminucci A, Dionigi C, Russo A, Tampieri A, Landi E, Goranov VA, Marcacci M, Dediu V (2010) A novel route in bone tissue engineering: magnetic biomimetic scaffolds. Acta Biomater 6:786–796. doi: 10.1016/j.actbio.2009.09.017 CrossRefPubMedGoogle Scholar
  38. 38.
    Santamaría S, Sanchez S, Sanz M, Garcia-Sanz JA (2016) Comparison of periodontal ligament and gingiva-derived mesenchymal stem cells for regenerative therapies. Clin Oral Invest. doi: 10.1007/s00784-016-1867-3 Google Scholar
  39. 39.
    Bottino MC, Arthur RA, Waeiss RA, Kamocki K, Gregson KS, Gregory RL (2014) Biodegradable nanofibrous drug delivery systems: effects of metronidazole and ciprofloxacin on periodontopathogens and commensal oral bacteria. Clin Oral Investig 18:2151–2158. doi: 10.1007/s00784-014-1201-x CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Augustine R, Dominic EA, Reju I, Kaimal B, Kalarikkal N, Thomas S (2014) Electrospun polycrapolactone membranes incorporated with ZnO nanoparticles as skin substitutes with enhanced fibroblast proliferation and wound healing. RSC Adv 4:24777–24785. doi: 10.1039/C4RA02450H CrossRefGoogle Scholar
  41. 41.
    Augustine R, Malik HN, Singhal DK, Mukherjee A, Malakar D, Kalarikkal N, Thomas S (2014) Electrospun polycaprolactone/ZnO nanocomposite membranes as biomaterials with antibacterial and cell adhesion properties. J Polym Res 21:1–17. doi: 10.1007/s10965-013-0347-6 CrossRefGoogle Scholar
  42. 42.
    Ranjbar-Mohammadi M, Zamani M, Prabhakaran MP, Hajir-Bahrami S, Ramakrishna S (2016) Electrospinning of PLGA/gum tragacanth nanofibers containing tetracycline hydrochloride for periodontal regeneration. Mater Sci Engineer C 58:521–531. doi: 10.1016/j.msec.2015.08.066 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Raquel Osorio
    • 1
    Email author
  • Camilo Andrés Alfonso-Rodríguez
    • 2
  • Estrella Osorio
    • 1
  • Antonio L. Medina-Castillo
    • 3
  • Miguel Alaminos
    • 2
  • Manuel Toledano-Osorio
    • 1
  • Manuel Toledano
    • 1
  1. 1.Research Institute IBS, Dental School, Colegio MáximoUniversity of GranadaGranadaSpain
  2. 2.Research Institute IBS, Tissue Engineering Group, Department of HistologyUniversity of GranadaGranadaSpain
  3. 3.NanoMyPSpin-Off Enterprise from University of Granada. Edificio BIC-GranadaArmillaSpain

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