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Bioglass Incorporation Improves Mechanical Properties and Enhances Cell-Mediated Mineralization on Electrochemically Aligned Collagen Threads

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Bioglass Incorporation Improves Mechanical Properties and Enhances Cell-Mediated Mineralization on Electrochemically Aligned Collagen Threads Bioglass incorporation improves mechanical properties and enhances cell-mediated mineralization on electrochemically aligned collagen threads Madhura P. Nijsure,1 Meet Pastakia,2 Joseph Spano,2,3 Michael B. Fenn,2,3 Vipuil Kishore1,2,3 1Department of Chemical Engineering, Florida Institute of Technology, Melbourne, Florida 32901 2Department of Biomedical Engineering, Florida Institute of Technology, Melbourne, Florida 32901 3Center for Medical Materials and Biophotonics, Florida Institute of Technology, Melbourne, Florida 32901 Received 21 December 2016; revised 3 April 2017; accepted 26 April 2017 Published online 00 Month 2017 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/jbm.a.36102 Abstract: Bone tissue engineering mandates the development investigated. The results indicated that BG can be successfully of a functional scaffold that mimics the physicochemical prop- incorporated within ELAC threads, without disturbing collagen erties of native bone. Bioglass 45S5 (BG) is a highly bioactive fibril alignment. Further, BG incorporation significantly material known to augment bone formation and restoration. increased the ultimate tensile stress (UTS) and modulus of Hybrid scaffolds fabricated using collagen type I and BG resem- ELAC threads (p < 0.05). SBF conditioning showed extensive ble the organic and inorganic composition of the bone extracel- mineralization on BG-ELAC threads that increased over time lular matrix and hence have been extensively investigated for demonstrating the bone bioactivity of BG-ELAC threads. Addi- bone tissue engineering applications. However, collagen–BG tionally, BG incorporation into ELAC threads resulted in scaffolds developed thus far do not recapitulate the aligned increased cell proliferation (p < 0.05) and deposition of a highly structure of collagen found in native bone. In this study, an dense and continuous mineralized matrix. In conclusion, incor- electrochemical fabrication method was employed to synthe- poration of BG into ELAC threads is a viable strategy for the size BG-incorporated electrochemically aligned collagen (BG- development of an osteoconductive material for bone tissue ELAC) threads that are compositionally similar to native bone. engineering applications. VC 2017 Wiley Periodicals, Inc. J Biomed Further, aligned collagen fibrils within BG-ELAC threads mimic Mater Res Part A: 00A:000–000, 2017. the anisotropic arrangement of collagen fibrils in native bone. The effect of BG incorporation on the mechanical properties Key Words: aligned collagen, bioglass, mineralization, bone and cell-mediated mineralization on ELAC threads was tissue engineering How to cite this article: Nijsure MP, Pastakia M, Spano J, Fenn MB, Kishore V. 2017. Bioglass incorporation improves mechanical properties and enhances cell-mediated mineralization on electrochemically aligned collagen threads. J Biomed Mater Res Part A 2017:00A:000–000. INTRODUCTION that recapitulates composition, mechanics, and anisotropic Physicochemical cues from the extracellular matrix (ECM) architecture of native bone is imperative to guide cell differen- microenvironment have been shown to play a critical role in tiation, and highly ordered cell-mediated de novo mineraliza- cell proliferation, migration, and tissue-specific differentia- tion that is akin to the native tissue.8 tion.1–4 While several studies have attempted to develop bio- Bioglass 45S5 (BG) is an osteostimulative glass ceramic mimetic scaffolds that resemble individual facets of native that has been previously shown to be more bioactive com- bone ECM (i.e., composition, structure, or mechanics), little pared to HA.9,10 Specifically, Oonishi et al. have shown that work is done on the fabrication of scaffolds that mimic multi- BG implantation into a critical sized bone defect in a rabbit ple aspects of the bone ECM. For example, collagen–hydroxy- model resulted in significantly faster bone restoration (2 apatite hybrid scaffolds resemble the composition of native weeks) compared to HA (12 weeks).10 Furthermore, con- bone5,6; however, most existing scaffolds are mechanically trolled release of ions (e.g., Ca, Si) from BG have been weak with randomly oriented collagen fibers. On the other shown to stimulate bone marrow stem cell differentiation,11 12–14 hand, electrospun aligned composites of poly(D,L-lactide-co- osteoblast proliferation and differentiation, and matrix glycolide) (PLGA) and hydroxyapatite (HA) mimic the highly mineralization15,16. Collagen type I and BG have been com- oriented ECM structure of native bone tissue, but are not com- bined in numerous studies for the fabrication of biomimetic positionally similar.7 Development of a biomimetic scaffold scaffolds for bone tissue engineering applications.17 While Correspondence to: V. Kishore; e-mail: [email protected] Contract grant sponsor: College of Engineering, Florida Institute of Technology VC 2017 WILEY PERIODICALS, INC. 1 pure collagen gel-based scaffolds are mechanically weak for Corporation, MO) was prepared by suspending the particles at use in load-bearing applications, incorporation of an inorganic a concentration of 200 mg/mL in water. An appropriate vol- phase within the collagen framework has been shown to ume of BG particles was suspended into dialyzed collagen structurally reinforce the collagen fibers and thereby signifi- solution to make a composite mixture of BG:collagen 60:40 cantly improve the mechanical properties of collagen-based (w/w). The BG:collagen mixture was loaded between two scaffolds.18–20 Another limitation of collagen gels is the stainless-steel wire electrodes (electrode spacing: 1.8 mm) loosely packed network of collagen fibers resulting in low col- and an electric field of 3 V was applied for 30 min. The electric lagen fibrillar density compared to native bone. Unconfined field triggers the formation of a pH gradient between the elec- plastic compression of collagen gels has been reported to trodes resulting in the collagen molecules close to the anode densify collagen fibers and generate mechanically competent gaining a positive charge and the ones close to the cathode scaffolds that mimic the microstructural properties of the gaining a negative charge. The like-charged electrodes repel bone ECM.21 Furthermore, incorporation of BG within plasti- the collagen molecules away resulting in aggregation of the cally compressed collagen matrices has been shown to expe- collagen molecules at the isoelectric point (pI). During the dite cell-mediated mineralization.15,22 Although plastic alignment process, the BG particles become entrapped within compression yields mechanically stiff and dense collagen scaf- aligned collagen to form BG-ELAC threads. Collagen-only folds, the collagen fibers in these scaffolds are randomly ori- threads were prepared in a similar manner but without the ented and do not mimic the aligned collagen network found in addition of BG particles. ELAC and BG–ELAC threads were native bone. Therefore, there is a need for an alternative colla- freshly prepared for all the experiments. In case of overnight gen densification method that yields highly oriented collagen– storage, excess water was blotted on a Kim Wipe and the BG scaffolds for bone tissue engineering applications. threads were stored in a semi-wet condition in the refrigera- In this study, an electrochemical method based on the prin- tor at 48C. The term thread is used in this study to signify bun- ciples of isoelectric focusing was employed to synthesize BG dles of densely packed collagen microfibrils within ELAC. incorporated electrochemically aligned collagen (BG-ELAC) threads. To the best of our knowledge, this is the first attempt Confirmation of bioglass incorporation within to incorporate BG particles into aligned collagen network. ELAC threads via Alizarin Red S staining Native bone is a composite mixture of 50–70% inorganic min- Alizarin Red S is commonly used to identify the presence of eral and 20–40% organic matrix that is mostly comprised of calcium in tissue sections.28 As BG is rich in calcium, the collagen type I.23,24 BG-ELAC threads developed in this study presence of BG within ELAC threads can be confirmed by mimic the compositional and structural (highly aligned and staining the BG–ELAC threads with Alizarin Red S. ELAC densely packed collagen fibers) aspects of the native bone ECM threads (without BG) were used as control. Threads were niche. In this study, two different hypotheses were tested: (1) stained with 40 mM Alizarin Red S stain for 20 min at room tissue-level (60 wt %) BG can be incorporated within aligned temperature and washed with copious amounts of water to collagen threads using the electrochemical process, and (2) BG remove excess dye. Following this, the threads were imaged incorporation will enhance mechanical properties and cell- under a microscope to examine the presence and distribu- mediated mineralization on electrochemically aligned collagen tion of BG in BG–ELAC threads. (ELAC) threads. BG incorporation into ELAC threads was con- firmed via Alizarin red S staining and Raman spectroscopy. The Effect of bioglass incorporation on alignment effect of BG incorporation on the alignment of ELAC threads of ELAC threads was assessed by polarized microscopy. Monotonic tensile tests Polarized imaging was employed to assess the effect of BG were performed to assess the effect of BG incorporation on the incorporation on the alignment of ELAC threads as described mechanical properties of ELAC threads. Bone bioactivity of BG– in a previous publication.29
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