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Multifunctional Silk Fibroin/Carbon Nanofiber Scaffolds for In Vitro Cardiomyogenic Differentiation of Induced Pluripotent Stem Cells and Energy Harvesting from Simulated Cardiac Motion.

ABSTRACT: In this proof-of-concept study, cardiomyogenic differentiation of induced pluripotent stem cells (iPSCs) is combined with energy harvesting from simulated cardiac motion in vitro. To achieve this, silk fibroin (SF)-based porous scaffolds are designed to mimic the mechanical and physical properties of cardiac tissue and used as triboelectric nanogenerator (TENG) electrodes. The load-carrying mechanism, β-sheet content, degradation characteristics, and iPSC interactions of the scaffolds are observed to be interrelated and regulated by their pore architecture. The SF scaffolds with a pore size of 379 ± 34 μm, a porosity of 79 ± 1%, and a pore interconnectivity of 67 ± 1% upregulated the expression of cardiac-specific gene markers TNNT2 and NKX2.5 from iPSCs. Incorporating carbon nanofibers (CNFs) enhances the elastic modulus of the scaffolds to 45 ± 3 kPa and results in an electrical conductivity of 0.021 ± 0.006 S/cm. The SF and SF/CNF scaffolds are used as conjugate TENG electrodes and generate a maximum power output of 0.37 × 10^-3 mW/m², with an open-circuit voltage and a short circuit current of 0.46 V and 4.5 nA, respectively, under simulated cardiac motion. A novel approach is demonstrated for fabricating scaffold-based cardiac patches that can serve as tissue scaffolds and simultaneously allow energy harvesting.

SUBMITTER: Tufan Y

PROVIDER: S-EPMC10510024 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Multifunctional Silk Fibroin/Carbon Nanofiber Scaffolds for In Vitro Cardiomyogenic Differentiation of Induced Pluripotent Stem Cells and Energy Harvesting from Simulated Cardiac Motion.

Tufan Yiğithan Y Öztatlı Hayriye H Doganay Doga D Buyuksungur Arda A Cicek Melih Ogeday MO Döş İpek Tuğçe İT Berberoğlu Çağla Ç Unalan Husnu Emrah HE Garipcan Bora B Ercan Batur B

ACS applied materials & interfaces 20230829 36

In this proof-of-concept study, cardiomyogenic differentiation of induced pluripotent stem cells (iPSCs) is combined with energy harvesting from simulated cardiac motion in vitro. To achieve this, silk fibroin (SF)-based porous scaffolds are designed to mimic the mechanical and physical properties of cardiac tissue and used as triboelectric nanogenerator (TENG) electrodes. The load-carrying mechanism, β-sheet content, degradation characteristics, and iPSC interactions of the scaffolds are observ ...[more]

PMID: 37643896

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Project description:Three-dimensional porous scaffolds prepared from regenerated silk fibroin using either an all-aqueous process or a process involving an organic solvent, hexafluoroisopropanol (HFIP), have shown promise in cell culture and tissue engineering applications. However, their biocompatibility and in vivo degradation have not been fully established. The present study was conducted to systematically investigate how processing method (aqueous vs. organic solvent) and processing variables (silk fibroin concentration and pore size) affect the short-term (up to 2 months) and long-term (up to 1 year) in vivo behavior of the protein scaffolds in both nude and Lewis rats. The samples were analyzed by histology for scaffold morphological changes and tissue ingrowth, and by real-time RT-PCR and immunohistochemistry for immune responses. Throughout the period of implantation, all scaffolds were well tolerated by the host animals and immune responses to the implants were mild. Most scaffolds prepared from the all-aqueous process degraded to completion between 2 and 6 months, while those prepared from organic solvent (hexafluoroisopropanol (HFIP)) process persisted beyond 1 year. Due to widespread cellular invasion throughout the scaffold, the degradation of aqueous-derived scaffolds appears to be more homogeneous than that of HFIP-derived scaffolds. In general and especially for the HFIP-derived scaffolds, a higher original silk fibroin concentration (e.g. 17%) and smaller pore size (e.g. 100-200microm) resulted in lower levels of tissue ingrowth and slower degradation. These results demonstrate that the in vivo behavior of the three-dimensional silk fibroin scaffolds is related to the morphological and structural features that resulted from different scaffold preparation processes. The insights gained in this study can serve as a guide for processing scenarios to match desired morphological and structural features and degradation time with tissue-specific applications.

Project description:The dissolution of Bombyx mori silk fibroin (SF) films in formic acid (FA) for the preparation of electrospinning dopes is widely exploited to produce electrospun SF scaffolds. The SILKBridge® nerve conduit is an example of medical device having in its wall structure an electrospun component produced from an FA spinning dope. Though highly volatile, residual FA remains trapped into the bulk of the SF nanofibers. The purpose of this work is to investigate the type and strength of the interaction between FA and SF in electrospun mats, to quantify its amount and to evaluate its possible toxicological impact on human health. The presence of residual FA in SF mats was detected by FTIR and Raman spectroscopy (new carbonyl peak at about 1,725 cm-1) and by solid state NMR, which revealed a new carbonyl signal at about 164.3 ppm, attributed to FA by isotopic 13C substitution. Changes occurred also in the spectral ranges of hydroxylated amino acids (Ser and Thr), demonstrating that FA interacted with SF by forming formyl esters. The total amount of FA was determined by HS-GC/MS analysis and accounted for 247 ± 20 μmol/g. The greatest part was present as formyl ester, a small part (about 3%) as free FA. Approximately 17% of the 1,500 μmol/g of hydroxy amino acids (Ser and Thr) theoretically available were involved in the formation of formyl esters. Treatment with alkali (Na2CO3) succeeded to remove the greatest part of FA, but not all. Alkali-treated electrospun SF mats underwent morphological, physical, and mechanical changes. The average diameter of the fibers increased from about 440 nm to about 480 nm, the mat shrunk, became stiffer (the modulus increased from about 5.5 MPa to about 7 MPa), and lost elasticity (the strain decreased from about 1 mm/mm to about 0.8 mm/mm). Biocompatibility studies with human adult dermal fibroblasts did not show significant difference in cell proliferation (313 ± 18 and 309 ± 23 cells/mm2 for untreated and alkali-treated SF mat, respectively) and metabolic activity. An in-depth evaluation of the possible toxicological impact of residual FA was made using the SILKBridge® nerve conduit as case study, following the provisions of the ISO 10993-1 standard. The Potential Patient Daily Intake, calculated from the total amount of FA determined by HS-GC/MS, was 2.4 mg/day and the Tolerable Exposure level was set to 35.4 mg/day. This allowed to obtain a value of the Margin of Safety of 15, indicating that the amount of FA left on SF mats after electrospinning does not raise concerns for human health.

Dataset Information

Multifunctional Silk Fibroin/Carbon Nanofiber Scaffolds for In Vitro Cardiomyogenic Differentiation of Induced Pluripotent Stem Cells and Energy Harvesting from Simulated Cardiac Motion.

Publications

Multifunctional Silk Fibroin/Carbon Nanofiber Scaffolds for In Vitro Cardiomyogenic Differentiation of Induced Pluripotent Stem Cells and Energy Harvesting from Simulated Cardiac Motion.

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