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Title: Gelatin-Derived Graphene–Silicate Hybrid Materials Are Biocompatible and Synergistically Promote BMP9-Induced Osteogenic Differentiation of Mesenchymal Stem Cells

Abstract

Graphene-based materials are used in many fields but have found only limited applications in biomedicine, including bone tissue engineering. Here, we demonstrate that novel hybrid materials consisting of gelatin-derived graphene and silicate nanosheets of Laponite (GL) are biocompatible and promote osteogenic differentiation of mesenchymal stem cells (MSCs). Homogeneous cell attachment, long-term proliferation, and osteogenic differentiation of MSCs on a GL-scaffold were confirmed using optical microscopy and scanning electron microscopy. GL-powders made by pulverizing the GL-scaffold were shown to promote bone morphogenetic protein (BMP9)-induced osteogenic differentiation. GL-powders increased the alkaline phosphatase (ALP) activity in immortalized mouse embryonic fibroblasts but decreased the ALP activity in more-differentiated immortalized mouse adipose-derived cells. Note, however, that GL-powders promoted BMP9-induced calcium mineral deposits in both MSC lines, as assessed using qualitative and quantitative alizarin red assays. Furthermore, the expression of chondro-osteogenic regulator markers such as Runx2, Sox9, osteopontin, and osteocalcin was upregulated by the GL-powder, independent of BMP9 stimulation; although the powder synergistically upregulated the BMP9-induced Osterix expression, the adipogenic marker PPAR gamma was unaffected. Furthermore, in vivo stem cell implantation experiments demonstrated that GL-powder could significantly enhance the BMP9-induced ectopic bone formation from MSCs. Collectively, our results strongly suggest that the GL hybrid materials promotemore » BMP9-induced osteogenic differentiation of MSCs and hold promise for the development of bone tissue engineering platforms.« less

Authors:
 [1];  [2];  [3];  [2];  [4];  [4];  [4];  [5];  [6];  [7];  [4];  [4];  [4];  [6];  [4];  [4];  [4];  [4];  [7];  [4] more »;  [4];  [4];  [8];  [9];  [10];  [10];  [2];  [4]; ORCiD logo [2]; ORCiD logo [11] « less
  1. Department of Orthopaedic Surgery, The Second Affiliated Hospital of Chongqing Medical University, Chongqing 400010, China; Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, Illinois 60637, United States
  2. Institute for Molecular Engineering, The University of Chicago, Chicago, Illinois 60637, United States; Argonne National Laboratory, Argonne, Illinois 60439, United States
  3. Institute for Molecular Engineering, The University of Chicago, Chicago, Illinois 60637, United States
  4. Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, Illinois 60637, United States; Ministry of Education Key Laboratory of Diagnostic Medicine, The Affiliated Hospitals of Chongqing Medical University, Chongqing 400016, China
  5. Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, Illinois 60637, United States; Department of Conservative Dentistry and Endodontics, West China School of Stomatology, Sichuan University, Chengdu 610041, China
  6. Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, Illinois 60637, United States; Department of Orthopaedic Surgery, Union Hospital of Tongji Medical College, Huazhong University of Science &, Technology, Wuhan 430022, China
  7. Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, Illinois 60637, United States; Departments of Neurosurgery and Otolaryngology-Head &, Neck Surgery, The Affiliated Zhongnan Hospital of Wuhan University, Wuhan 430071, China
  8. Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, Illinois 60637, United States; Department of Laboratory Medicine and Clinical Diagnostics, the Affiliated Yantai Hospital, Binzhou Medical University, Yantai 264100, China
  9. Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, Illinois 60637, United States; Department of Surgery, Section of Plastic Surgery, The University of Chicago Medical Center, Chicago, Illinois 60637, United States
  10. Molecular Oncology Laboratory, Department of Orthopaedic Surgery and Rehabilitation Medicine, The University of Chicago Medical Center, Chicago, Illinois 60637, United States
  11. Department of Orthopaedic Surgery, The Second Affiliated Hospital of Chongqing Medical University, Chongqing 400010, China
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Institute of Standards and Technology (NIST) - Center for Hierarchical Materials Design (CHiMaD); National Natural Science Foundation of China (NNSFC); National Institutes of Health (NIH); USDOD; National Science Foundation (NSF)
OSTI Identifier:
1393461
DOE Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article
Resource Relation:
Journal Name: ACS Applied Materials and Interfaces; Journal Volume: 9; Journal Issue: 19
Country of Publication:
United States
Language:
English

Citation Formats

Zou, Yulong, Qazvini, Nader Taheri, Zane, Kylie, Sadati, Monirosadat, Wei, Qiang, Liao, Junyi, Fan, Jiaming, Song, Dongzhe, Liu, Jianxiang, Ma, Chao, Qu, Xiangyang, Chen, Liqun, Yu, Xinyi, Zhang, Zhicai, Zhao, Chen, Zeng, Zongyue, Zhang, Ruyi, Yan, Shujuan, Wu, Tingting, Wu, Xingye, Shu, Yi, Li, Yasha, Zhang, Wenwen, Reid, Russell R., Lee, Michael J., Wolf, Jennifer Moritis, Tirrell, Matthew, He, Tong-Chuan, de Pablo, Juan J., and Deng, Zhong-Liang. Gelatin-Derived Graphene–Silicate Hybrid Materials Are Biocompatible and Synergistically Promote BMP9-Induced Osteogenic Differentiation of Mesenchymal Stem Cells. United States: N. p., 2017. Web. doi:10.1021/acsami.7b00272.
Zou, Yulong, Qazvini, Nader Taheri, Zane, Kylie, Sadati, Monirosadat, Wei, Qiang, Liao, Junyi, Fan, Jiaming, Song, Dongzhe, Liu, Jianxiang, Ma, Chao, Qu, Xiangyang, Chen, Liqun, Yu, Xinyi, Zhang, Zhicai, Zhao, Chen, Zeng, Zongyue, Zhang, Ruyi, Yan, Shujuan, Wu, Tingting, Wu, Xingye, Shu, Yi, Li, Yasha, Zhang, Wenwen, Reid, Russell R., Lee, Michael J., Wolf, Jennifer Moritis, Tirrell, Matthew, He, Tong-Chuan, de Pablo, Juan J., & Deng, Zhong-Liang. Gelatin-Derived Graphene–Silicate Hybrid Materials Are Biocompatible and Synergistically Promote BMP9-Induced Osteogenic Differentiation of Mesenchymal Stem Cells. United States. doi:10.1021/acsami.7b00272.
Zou, Yulong, Qazvini, Nader Taheri, Zane, Kylie, Sadati, Monirosadat, Wei, Qiang, Liao, Junyi, Fan, Jiaming, Song, Dongzhe, Liu, Jianxiang, Ma, Chao, Qu, Xiangyang, Chen, Liqun, Yu, Xinyi, Zhang, Zhicai, Zhao, Chen, Zeng, Zongyue, Zhang, Ruyi, Yan, Shujuan, Wu, Tingting, Wu, Xingye, Shu, Yi, Li, Yasha, Zhang, Wenwen, Reid, Russell R., Lee, Michael J., Wolf, Jennifer Moritis, Tirrell, Matthew, He, Tong-Chuan, de Pablo, Juan J., and Deng, Zhong-Liang. Thu . "Gelatin-Derived Graphene–Silicate Hybrid Materials Are Biocompatible and Synergistically Promote BMP9-Induced Osteogenic Differentiation of Mesenchymal Stem Cells". United States. doi:10.1021/acsami.7b00272.
@article{osti_1393461,
title = {Gelatin-Derived Graphene–Silicate Hybrid Materials Are Biocompatible and Synergistically Promote BMP9-Induced Osteogenic Differentiation of Mesenchymal Stem Cells},
author = {Zou, Yulong and Qazvini, Nader Taheri and Zane, Kylie and Sadati, Monirosadat and Wei, Qiang and Liao, Junyi and Fan, Jiaming and Song, Dongzhe and Liu, Jianxiang and Ma, Chao and Qu, Xiangyang and Chen, Liqun and Yu, Xinyi and Zhang, Zhicai and Zhao, Chen and Zeng, Zongyue and Zhang, Ruyi and Yan, Shujuan and Wu, Tingting and Wu, Xingye and Shu, Yi and Li, Yasha and Zhang, Wenwen and Reid, Russell R. and Lee, Michael J. and Wolf, Jennifer Moritis and Tirrell, Matthew and He, Tong-Chuan and de Pablo, Juan J. and Deng, Zhong-Liang},
abstractNote = {Graphene-based materials are used in many fields but have found only limited applications in biomedicine, including bone tissue engineering. Here, we demonstrate that novel hybrid materials consisting of gelatin-derived graphene and silicate nanosheets of Laponite (GL) are biocompatible and promote osteogenic differentiation of mesenchymal stem cells (MSCs). Homogeneous cell attachment, long-term proliferation, and osteogenic differentiation of MSCs on a GL-scaffold were confirmed using optical microscopy and scanning electron microscopy. GL-powders made by pulverizing the GL-scaffold were shown to promote bone morphogenetic protein (BMP9)-induced osteogenic differentiation. GL-powders increased the alkaline phosphatase (ALP) activity in immortalized mouse embryonic fibroblasts but decreased the ALP activity in more-differentiated immortalized mouse adipose-derived cells. Note, however, that GL-powders promoted BMP9-induced calcium mineral deposits in both MSC lines, as assessed using qualitative and quantitative alizarin red assays. Furthermore, the expression of chondro-osteogenic regulator markers such as Runx2, Sox9, osteopontin, and osteocalcin was upregulated by the GL-powder, independent of BMP9 stimulation; although the powder synergistically upregulated the BMP9-induced Osterix expression, the adipogenic marker PPAR gamma was unaffected. Furthermore, in vivo stem cell implantation experiments demonstrated that GL-powder could significantly enhance the BMP9-induced ectopic bone formation from MSCs. Collectively, our results strongly suggest that the GL hybrid materials promote BMP9-induced osteogenic differentiation of MSCs and hold promise for the development of bone tissue engineering platforms.},
doi = {10.1021/acsami.7b00272},
journal = {ACS Applied Materials and Interfaces},
number = 19,
volume = 9,
place = {United States},
year = {Thu May 04 00:00:00 EDT 2017},
month = {Thu May 04 00:00:00 EDT 2017}
}