journal article·2021-09-25Open access

Electrospun core-shell nanofibers with encapsulated enamel matrix derivative for guided periodontal tissue regeneration

Linda R. WANG LAM, Kevin SCHILLING, Stephen ROMAS, Ravi MISRA, Zhuang ZHOU, Jack G. CATON, Xinping ZHANG

Dental Materials Journal· Volume 40· Issue 5

Abstract

(EMD) was evaluated. The membrane was developed through coaxial electrospinning using polycaprolactone as the shell and polyethylene glycol as the core. The effects of the membrane on the osteogenic differentiation of periodontal ligament stem cells (PDLSCs) were examined using Alizarin Red S staining and qRT-PCR. Characterization of the nanofiber membrane demonstrated core-shell morphology with a mean diameter of ~1 µm. Examination of the release of fluorescein isothiocyanate-conjugated bovine serum albumin (FITC-BSA) from core-shell nanofibers over a 22-day period showed improved release profile of encapsulated proteins as compared to solid nanofibers. When cultured on EMD-containing core-shell nanofibers, PDLSCs showed significantly improved osteogenic differentiation with increased Alizarin Red S staining and enhanced osteogenic gene expression, namely OCN, RUNX2, ALP, and OPN. Core-shell nanofiber membranes may improve outcomes in periodontal regenerative therapy through simultaneous mechanical barrier and controlled drug delivery function.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Periodontal Regeneration and Treatments · Electrospun Nanofibers in Biomedical Applications · Bone and Dental Protein Studies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Center for Musculoskeletal Research, University of Rochester, School of Medicine and Dentistry

Department of Periodontology, Eastman Institute for Oral Health, University of Rochester, School of Medicine and Dentistry

Department of Biomedical Engineering, University of Rochester

Department of Pediatrics, University of Rochester, School of Medicine and Dentistry

References (49)

Show source-provided references
1. 1) Eke PI, Dye BA, Wei L, Slade GD, Thornton-Evans GO, Borgnakke WS, et al. Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. J Periodontol 2015; 86: 611-622.10.1902/jop.2015.140520 ↗
2. 2) Hajishengallis G. Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 2014; 35: 3-11.10.1016/j.it.2013.09.001 ↗
3. 3) Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 1976; 34: 235-249.
4. 4) Caton JG, Zander HA. The attachment between tooth and gingival tissues after periodic root planing and soft tissue curettage. J Periodontol 1979; 50: 462-466.10.1902/jop.1979.50.9.462 ↗
5. 5) Caton J, Nyman S, Zander H. Histometric evaluation of periodontal surgery. II. Connective tissue attachment levels after four regenerative procedures. J Clin Periodontol 1980; 7: 224-231.10.1111/j.1600-051X.1980.tb01965.x ↗
6. 6) Gottlow J, Nyman S, Lindhe J, Karring T, Wennström J. New attachment formation in the human periodontium by guided tissue regeneration. Case reports. J Clin Periodontol 1986; 13: 604-616.10.1111/j.1600-051X.1986.tb00854.x ↗
7. 7) Bottino MC, Thomas V, Schmidt G, Vohra YK, Chu TM, Kowolik MJ, et al. Recent advances in the development of GTR/GBR membranes for periodontal regeneration —a materials perspective. Dent Mater 2012; 28: 703-721.10.1016/j.dental.2012.04.022 ↗
8. 8) Miron RJ, Sculean A, Cochran DL, Froum S, Zucchelli G, Nemcovsky C, et al. Twenty years of enamel matrix derivative: the past, the present and the future. J Clin Periodontol 2016; 43: 668-683.10.1111/jcpe.12546 ↗
9. 9) Gestrelius S, Andersson C, Lidström D, Hammarström L, Somerman M. In vitro studies on periodontal ligament cells and enamel matrix derivative. J Clin Periodontol 1997; 24: 685-692.10.1111/j.1600-051X.1997.tb00250.x ↗
10. 10) Rodrigues TL, Marchesan JT, Coletta RD, Novaes AB Jr, Grisi MF, Souza SL, et al. Effects of enamel matrix derivative and transforming growth factor-beta1 on human periodontal ligament fibroblasts. J Clin Periodontol 2007; 34: 514-522.10.1111/j.1600-051X.2007.01090.x ↗
11. 11) Galli C, Macaluso GM, Guizzardi S, Vescovini R, Passeri M, Passeri G. Osteoprotegerin and receptor activator of nuclear factor-kappa B ligand modulation by enamel matrix derivative in human alveolar osteoblasts. J Periodontol 2006; 77: 1223-1228.10.1902/jop.2006.050304 ↗
12. 12) Yukna R, Mellonig JT. Histologic evaluation of periodontal healing in humans following regenerative therapy with enamel matrix derivative. A 10-case series. J Periodontol 2000; 71: 752-759.10.1902/jop.2000.71.5.752 ↗
13. 13) Trombelli L, Farina R. Clinical outcomes with bioactive agents alone or in combination with grafting or guided tissue regeneration. J Clin Periodontol 2008; 35(Suppl 8): 117-135.10.1111/j.1600-051X.2008.01265.x ↗
14. 14) Froum SJ, Weinberg MA, Rosenberg E, Tarnow D. A comparative study utilizing open flap debridement with and without enamel matrix derivative in the treatment of periodontal intrabony defects: a 12-month re-entry study. J Clin Periodontol 2001; 72: 25-34.10.1902/jop.2001.72.1.25 ↗
15. 15) Tonetti MS, Lang NP, Cortellini P, Suvan JE, Adriaens P, Dubravec D, et al. Enamel matrix proteins in the regenerative therapy of deep intrabony defects. A multicentre randomized controlled clinical trial. J Clin Periodontol 2002; 29: 317-325.10.1034/j.1600-051X.2002.290407.x ↗
16. 16) Chen YT, Wang HL, Lopatin DE, O’Neal R, MacNeil RL. Bacterial adherence to guided tissue regeneration barrier membranes exposed to the oral environment. J Periodontol 1997; 68: 172-179.10.1902/jop.1997.68.2.172 ↗
17. 17) Liu W, Thomopoulos S, Xia Y. Electrospun nanofibers for regenerative medicine. Adv Healthc Mater 2012; 1: 10-25.10.1002/adhm.201100021 ↗
18. 18) Gao X, Song J, Zhang Y, Xu X, Xu X, Zhang S, et al. Bioinspired design of polycaprolactone composite nanofibers as artificial bone extracellular matrix for bone regeneration application. ACS Appl Mater Interfaces 2016; 8: 27594-27610.10.1021/acsami.6b10417 ↗
19. 19) Dahlin RL, Kasper FK, Mikos AG. Polymeric nanofibers in tissue engineering. Tissue Eng Part B Rev 2011; 17: 349-364.10.1089/ten.teb.2011.0238 ↗
20. 20) Wang T, Zhai Y, Nuzzo M, Yang X, Yang Y, Zhang X. Layer-by-layer nanofiber-enabled engineering of biomimetic periosteum for bone repair and reconstruction. Biomaterials 2018; 182: 279-288.10.1016/j.biomaterials.2018.08.028 ↗
21. 21) Sill TJ, von Recum HA. Electrospinning: applications in drug delivery and tissue engineering. Biomaterials 2008; 29: 1989-2006.10.1016/j.biomaterials.2008.01.011 ↗
22. 22) Sultanova Z, Kaleli G, Kabay G, Mutlu M. Controlled release of a hydrophilic drug from coaxially electrospun polycaprolactone nanofibers. Int J Pharm 2016; 505: 133-138.10.1016/j.ijpharm.2016.03.032 ↗
23. 23) Schilling K, El Khatib M, Plunkett S, Xue J, Xia Y, Vinogradov SA, et al. Electrospun fiber mesh for high-resolution measurements of oxygen tension in cranial bone defect repair. ACS Appl Mater Interfaces 2019; 11: 33548-33558.10.1021/acsami.9b08341 ↗
24. 24) Zhang YZ, Wang X, Feng Y, Li J, Lim CT, Ramakrishna S. Coaxial electrospinning of (fluorescein isothiocyanate-conjugated bovine serum albumin)-encapsulated poly(epsilon-caprolactone) nanofibers for sustained release. Biomacromolecules 2006; 7: 1049-1057.10.1021/bm050743i ↗
25. 25) Li X, Su Y, Liu S, Tan L, Mo X, Ramakrishna S. Encapsulation of proteins in poly(L-lactide-co-caprolactone) fibers by emulsion electrospinning. Colloids Surf B Biointerfaces 2010; 75: 418-424.10.1016/j.colsurfb.2009.09.014 ↗
26. 26) Baek J, Lee E, Lotz MK, D’Lima DD. Bioactive proteins delivery through core-shell nanofibers for meniscal tissue regeneration. Nanomedicine 2020; 23: 102090.10.1016/j.nano.2019.102090 ↗
27. 27) Ji W, Yang F, van den Beucken JJJP, Bian Z, Fan M, Chen Z, et al. Fibrous scaffolds loaded with protein prepared by blend or coaxial electrospinning. Acta Biomater 2010; 6: 4199-4207.10.1016/j.actbio.2010.05.025 ↗
28. 28) Peppas NA. 1. Commentary on an exponential model for the analysis of drug delivery: Original research article: a simple equation for description of solute release: I II. Fickian and non-Fickian release from non-swellable devices in the form of slabs, spheres, cylinders or discs, 1987. J Control Release 2014; 190: 31-32.
29. 29) Maleki H, Gharehaghaji AA, Toliyat T, Dijkstra PJ. Drug release behavior of electrospun twisted yarns as implantable medical devices. Biofabrication 2016; 8: 035019.10.1088/1758-5090/8/3/035019 ↗
30. 30) Unpublished observations. (Manuscript in preparation, Misra R.)
31. 31) Nagatomo K, Komaki M, Sekiya I, Sakaguchi Y, Noguchi K, Oda S, et al. Stem cell properties of human periodontal ligament cells. J Periodont Res 2006; 41: 303-310.10.1111/j.1600-0765.2006.00870.x ↗
32. 32) Hu J, Tian L, Prabhakaran MP, Ding X, Ramakrishna S. Fabrication of nerve growth factor encapsulated aligned poly(ε-caprolactone) nanofibers and their assessment as a potential neural tissue engineering scaffold. Polymers (Basel) 2016; 8: 54.10.3390/polym8020054 ↗
33. 33) Chaparro FJ, Presley KF, Coutinho da Silva MA, Lannutti JJ.Sintered electrospun polycaprolactone for controlled model drug delivery. Mater Sci Eng C Mater Biol Appl 2019; 99: 112-120.10.1016/j.msec.2019.01.095 ↗
34. 34) Rosenberg R, Devenney W, Siegel S, Dan N. Anomalous release of hydrophilic drugs from poly(epsilon-caprolactone) matrices. Mol Pharm 2007; 4: 943-948.10.1021/mp700097x ↗
35. 35) Huang X, Brazel CS. On the importance and mechanisms of burst release in matrix-controlled drug delivery systems. J Control Release 2001; 73: 121-136.10.1016/S0168-3659(01)00248-6 ↗
36. 36) Zafar M, Najeeb S, Khurshid Z, Vazirzadeh M, Zohaib S, Najeeb B, et al. Potential of electrospun nanofibers for biomedical and dental applications. Materials 2016; 9: 73.10.3390/ma9020073 ↗
37. 37) Zamani M, Morshed M, Varshosaz J, Jannesari M. Controlled release of metronidazole benzoate from poly epsilon-caprolactone electrospun nanofibers for periodontal diseases. Eur J Pharm Biopharm 2010; 75: 179-185.10.1016/j.ejpb.2010.02.002 ↗
38. 38) Ranjbar-Mohammadi M, Zamani M, Prabhakaran MP, Bahrami SH, Ramakrishna S. Electrospinning of PLGA/gum tragacanth nanofibers containing tetracycline hydrochloride for periodontal regeneration. Mater Sci Eng C Mater Biol Appl 2016; 58: 521-531.10.1016/j.msec.2015.08.066 ↗
39. 39) Zhu H, Yu D, Zhou Y, Wang C, Gao M, Jiang H, et al Biological activity of a nanofibrous barrier membrane containing bone morphogenetic protein formed by core-shell electrospinning as a sustained delivery vehicle. J Biomed Mater Res B Appl Biomater 2013; 101: 541-552.10.1002/jbm.b.32854 ↗
40. 40) Zhang E, Zhu C, Yang J, Sun H, Zhang X, Li S, et al. Electrospun PDLLA/PLGA composite membranes for potential application in guided tissue regeneration. Mater Sci Eng C Mater Biol Appl 2016; 58: 278-285.10.1016/j.msec.2015.08.032 ↗
41. 41) Pontoriero R, Wennström J, Lindhe J. The use of barrier membranes and enamel matrix proteins in the treatment of angular bone effects. A prospective controlled clinical study. J Clin Periodontol 1999; 26: 833-840.10.1034/j.1600-051X.1997.00833.x ↗
42. 42) Sanz M, Tonetti MS, Zabalegui I, Sicilia A, Blanco J, Rebelo H, et al. Treatment of intrabony defects with enamel matrix proteins or barrier membranes: results from a multicenter practice-based clinical trial. J Periodontol 2004; 75: 726-733.10.1902/jop.2004.75.5.726 ↗
43. 43) Sculean A, Kiss A, Miliauskaite A, Schwarz F, Arweiler NB, Hannig M. Ten-year results following treatment of intra-bony defects with enamel matrix proteins and guided tissue regeneration. J Clin Periodontol 2008; 35: 817-824.10.1111/j.1600-051X.2008.01295.x ↗
44. 44) Cortellini P, Tonetti MS. Clinical performance of a regenerative strategy for intrabony defects: scientific evidence and clinical experience. J Periodontol 2005; 76: 341-350.10.1902/jop.2005.76.3.341 ↗
45. 45) Froum S, Lemler J, Horowitz R, Davidson B. The use of enamel matrix derivative in the treatment of periodontal osseous defects: a clinical decision tree based on biologic principles of regeneration. Int J Periodontics Restorative Dent 2001; 21: 437-449.
46. 46) Rincon JC, Xiao Y, Young WG, Bartold PM. Enhanced proliferation, attachment and osteopontin expression by porcine periodontal cells exposed to Emdogain. Arch Oral Biol 2005; 50: 1047-1054.10.1016/j.archoralbio.2005.04.006 ↗
47. 47) Parkar MH, Tonetti M. Gene expression profiles of periodontal ligament cells treated with enamel matrix proteins in vitro: analysis using cDNA arrays. J Periodontol 2004; 75: 1539-1546.10.1902/jop.2004.75.11.1539 ↗
48. 48) Hamamoto Y, Kawasaki N, Jarnbring F, Hammarström L.Effects and distribution of the enamel matrix derivative Emdogain in the periodontal tissues of rat molars transplanted to the abdominal wall. Dent Traumatol 2002; 18: 12-23.10.1034/j.1600-9657.2002.180102.x ↗
49. 49) Miron RJ, Zhang YF. Osteoinduction: a review of old concepts with new standards. J Dent Res 2012; 91: 736-744.10.1177/0022034511435260 ↗