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Title: A pH-Triggered, Self-Assembled, and Bioprintable Hybrid Hydrogel Scaffold for Mesenchymal Stem Cell Based Bone Tissue Engineering

Abstract

Effective bone tissue engineering can restore bone and skeletal functions that are impaired by traumas and/or certain medical conditions. Bone is a complex tissue and functions through orchestrated interactions between cells, biomechanical forces, and biofactors. To identify ideal scaffold materials for effective mesenchymal stem cell (MSC)-based bone tissue regeneration, here we develop and characterize a composite nanoparticle hydrogel by combining carboxymethyl chitosan (CMCh) and amorphous calcium phosphate (ACP) (designated as CMCh-ACP hydrogel). We demonstrate that the CMCh-ACP hydrogel is readily prepared by incorporating glucono delta-lactone (GDL) into an aqueous dispersion or rehydrating the acidic freeze-dried nanoparticles in a pH-triggered controlled-assembly fashion. The CMCh-ACP hydrogel exhibits excellent biocompatibility and effectively supports MSC proliferation and cell adhesion. Moreover, while augmenting BMP9-induced osteogenic differentiation, the CMCh-ACP hydrogel itself is osteoinductive and induces the expression of osteoblastic regulators and bone markers in MSCs in vitro. The CMCh-ACP scaffold markedly enhances the efficiency and maturity of BMP9-induced bone formation in vivo, while suppressing bone resorption occurred in long-term ectopic osteogenesis. Thus, these results suggest that the pH-responsive self-assembled CMCh-ACP injectable and bioprintable hydrogel may be further exploited as a novel scaffold for osteoprogenitor-cell-based bone tissue regeneration.

Authors:
 [1];  [2];  [3];  [4];  [1];  [5];  [6];  [1];  [1];  [7];  [8];  [9];  [10];  [6];  [6];  [1];  [1];  [11];  [1];  [12] more »;  [11];  [11];  [11];  [11];  [11];  [11];  [3];  [13];  [3]; ORCiD logo [11] « less
+ Show Author Affiliations
  1. First Affiliated Hospital of Chongqing Medical Univ., Chongqing (China); Univ. of Chicago Medical Center, Chicago, IL (United States)
  2. Univ. of Chicago, IL (United States)
  3. Univ. of Chicago, IL (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
  4. Univ. of Chicago Medical Center, Chicago, IL (United States); Chongqing Medical Univ., Chongqing (China)
  5. Imperial College London, London (United Kingdom)
  6. Univ. of Chicago Medical Center, Chicago, IL (United States); Affiliated Hospitals of Chongqing Medical Univ., Chongqing (China)
  7. Univ. of Chicago Medical Center, Chicago, IL (United States); Affiliated Hospitals of Chongqing Medical Univ., Chongqing (China); Second Affiliated Hospital of Nanchang Univ., Nanchang (China)
  8. Univ. of Chicago Medical Center, Chicago, IL (United States); Second Hospital of Lanzhou Univ., Lanzhou (China)
  9. Univ. of Chicago Medical Center, Chicago, IL (United States); Chongqing Hospital of Traditional Chinese Medicine, Chongqing (China)
  10. Univ. of Chicago Medical Center, Chicago, IL (United States); Xiangya Second Hospital of Central South Univ., Changsha (China)
  11. Univ. of Chicago Medical Center, Chicago, IL (United States)
  12. Univ. of Chicago Medical Center, Chicago, IL (United States); Affiliated Hospitals of Chongqing Medical Univ., Chongqing (China); Chongqing General Hospital, Chongqing (China)
  13. First Affiliated Hospital of Chongqing Medical Univ., Chongqing (China)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Institutes of Health (NIH); National Key Research and Development Program of China; USDOD; National Institute of Standards and Technology (NIST) - Center for Hierarchical Materials Design (CHiMaD); National Natural Science Foundation of China (NSFC); National Institutes of Health (NIH) - National Center for Advancing Translational Sciences (NCATS); National Science Foundation (NSF)
OSTI Identifier:
1558013
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
ACS Applied Materials and Interfaces
Additional Journal Information:
Journal Volume: 11; Journal Issue: 9; Journal ID: ISSN 1944-8244
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; BMP9; amorphous calcium phosphate (ACP); carboxymethyl chitosan (CMCh); hydrogels; mesenchymal stem cells; nanoparticles; bone tissue engineering

Citation Formats

Zhao, Chen, Qazvini, Nader Taheri, Sadati, Monirosadat, Zeng, Zongyue, Huang, Shifeng, De La Lastra, Ana Losada, Zhang, Linghuan, Feng, Yixiao, Liu, Wei, Huang, Bo, Zhang, Bo, Dai, Zhengyu, Shen, Yi, Wang, Xi, Luo, Wenping, Liu, Bo, Lei, Yan, Ye, Zhenyu, Zhao, Ling, Cao, Daigui, Yang, Lijuan, Chen, Xian, Athiviraham, Aravind, Lee, Michael J., Wolf, Jennifer Moriatis, Reid, Russell R., Tirrell, Matthew, Huang, Wei, de Pablo, Juan J., and He, Tong-Chuan. A pH-Triggered, Self-Assembled, and Bioprintable Hybrid Hydrogel Scaffold for Mesenchymal Stem Cell Based Bone Tissue Engineering. United States: N. p., 2019. Web. doi:10.1021/acsami.8b19094.
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Zhao, Chen, Qazvini, Nader Taheri, Sadati, Monirosadat, Zeng, Zongyue, Huang, Shifeng, De La Lastra, Ana Losada, Zhang, Linghuan, Feng, Yixiao, Liu, Wei, Huang, Bo, Zhang, Bo, Dai, Zhengyu, Shen, Yi, Wang, Xi, Luo, Wenping, Liu, Bo, Lei, Yan, Ye, Zhenyu, Zhao, Ling, Cao, Daigui, Yang, Lijuan, Chen, Xian, Athiviraham, Aravind, Lee, Michael J., Wolf, Jennifer Moriatis, Reid, Russell R., Tirrell, Matthew, Huang, Wei, de Pablo, Juan J., & He, Tong-Chuan. A pH-Triggered, Self-Assembled, and Bioprintable Hybrid Hydrogel Scaffold for Mesenchymal Stem Cell Based Bone Tissue Engineering. United States. https://doi.org/10.1021/acsami.8b19094
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Zhao, Chen, Qazvini, Nader Taheri, Sadati, Monirosadat, Zeng, Zongyue, Huang, Shifeng, De La Lastra, Ana Losada, Zhang, Linghuan, Feng, Yixiao, Liu, Wei, Huang, Bo, Zhang, Bo, Dai, Zhengyu, Shen, Yi, Wang, Xi, Luo, Wenping, Liu, Bo, Lei, Yan, Ye, Zhenyu, Zhao, Ling, Cao, Daigui, Yang, Lijuan, Chen, Xian, Athiviraham, Aravind, Lee, Michael J., Wolf, Jennifer Moriatis, Reid, Russell R., Tirrell, Matthew, Huang, Wei, de Pablo, Juan J., and He, Tong-Chuan. Fri . "A pH-Triggered, Self-Assembled, and Bioprintable Hybrid Hydrogel Scaffold for Mesenchymal Stem Cell Based Bone Tissue Engineering". United States. https://doi.org/10.1021/acsami.8b19094. https://www.osti.gov/servlets/purl/1558013.
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@article{osti_1558013,
title = {A pH-Triggered, Self-Assembled, and Bioprintable Hybrid Hydrogel Scaffold for Mesenchymal Stem Cell Based Bone Tissue Engineering},
author = {Zhao, Chen and Qazvini, Nader Taheri and Sadati, Monirosadat and Zeng, Zongyue and Huang, Shifeng and De La Lastra, Ana Losada and Zhang, Linghuan and Feng, Yixiao and Liu, Wei and Huang, Bo and Zhang, Bo and Dai, Zhengyu and Shen, Yi and Wang, Xi and Luo, Wenping and Liu, Bo and Lei, Yan and Ye, Zhenyu and Zhao, Ling and Cao, Daigui and Yang, Lijuan and Chen, Xian and Athiviraham, Aravind and Lee, Michael J. and Wolf, Jennifer Moriatis and Reid, Russell R. and Tirrell, Matthew and Huang, Wei and de Pablo, Juan J. and He, Tong-Chuan},
abstractNote = {Effective bone tissue engineering can restore bone and skeletal functions that are impaired by traumas and/or certain medical conditions. Bone is a complex tissue and functions through orchestrated interactions between cells, biomechanical forces, and biofactors. To identify ideal scaffold materials for effective mesenchymal stem cell (MSC)-based bone tissue regeneration, here we develop and characterize a composite nanoparticle hydrogel by combining carboxymethyl chitosan (CMCh) and amorphous calcium phosphate (ACP) (designated as CMCh-ACP hydrogel). We demonstrate that the CMCh-ACP hydrogel is readily prepared by incorporating glucono delta-lactone (GDL) into an aqueous dispersion or rehydrating the acidic freeze-dried nanoparticles in a pH-triggered controlled-assembly fashion. The CMCh-ACP hydrogel exhibits excellent biocompatibility and effectively supports MSC proliferation and cell adhesion. Moreover, while augmenting BMP9-induced osteogenic differentiation, the CMCh-ACP hydrogel itself is osteoinductive and induces the expression of osteoblastic regulators and bone markers in MSCs in vitro. The CMCh-ACP scaffold markedly enhances the efficiency and maturity of BMP9-induced bone formation in vivo, while suppressing bone resorption occurred in long-term ectopic osteogenesis. Thus, these results suggest that the pH-responsive self-assembled CMCh-ACP injectable and bioprintable hydrogel may be further exploited as a novel scaffold for osteoprogenitor-cell-based bone tissue regeneration.},
doi = {10.1021/acsami.8b19094},
journal = {ACS Applied Materials and Interfaces},
number = 9,
volume = 11,
place = {United States},
year = {Fri Feb 08 00:00:00 EST 2019},
month = {Fri Feb 08 00:00:00 EST 2019}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1021/acsami.8b19094
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Cited by: 88 works
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Figures / Tables:

Figure 1 Figure 1: Characterization of the CMCh-ACP hybrid nanoparticles. (A) $ζ$-potential for the hybrid nanoparticles determined by DLS at pH 11.0 and 8.0. (B) Synchrotron WAXS profiles of the CMCh-ACP hybrid gel and its control materials CMCh and ACP. (C) FTIR spectra of the hybrid nanoparticles and the control materials CMChmore » and ACP. (D) TEM analysis of the CMCh-ACP nanoparticles at two different magnifications. The red arrows indicate representative ACP nanoclusters dispersed in a hybrid nanoparticle at a higher magnification. The fast Fourier transformation of the image (inset) confirms that the nanoparticles are amorphous. (E) SEM micrographs of the hybrid nanoparticles. The experiments were repeated for at least three independent trials. Representative images are shown. ACP, amorphous calcium phosphate; CMCh, carboxymethyl chitosan; DLS, dynamic light scattering; FTIR, Fourier transform infrared spectroscopy; SEM, scanning electron microscopy; TEM, transmission electron microscopy; WAXS, wide-angle X-ray scattering.« less
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Osteoblast proliferation or differentiation is regulated by relative strengths of opposing signaling pathways
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journal, November 2015

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journal, December 2015

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Chitosan-Based Particles as Controlled Drug Delivery Systems
journal, January 2004

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journal, June 2014

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Retinoic acid signalling induces the differentiation of mouse fetal liver-derived hepatic progenitor cells
journal, November 2009

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journal, July 2013

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BMP 9 induces osteogenesis and adipogenesis in the immortalized human cranial suture progenitors from the patent sutures of craniosynostosis patients
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journal, October 2010

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Multilineage Potential of Adult Human Mesenchymal Stem Cells
journal, April 1999

The Calcium-Binding Protein S100A6 Accelerates Human Osteosarcoma Growth by Promoting Cell Proliferation and Inhibiting Osteogenic Differentiation
journal, January 2015

  • Li, Yasha; Wagner, Eric R.; Yan, Zhengjian
  • Cellular Physiology and Biochemistry, Vol. 37, Issue 6
  • DOI: 10.1159/000438591

Amorphous calcium phosphate and its application in dentistry
journal, July 2011

Retinoic Acids Potentiate BMP9-Induced Osteogenic Differentiation of Mesenchymal Progenitor Cells
journal, July 2010

Gene Therapy for Bone Regeneration
journal, April 2005

BMP-9 Induced Osteogenic Differentiation of Mesenchymal Stem Cells: Molecular Mechanism and Therapeutic Potential
journal, June 2011

Targeting BMP9-Promoted Human Osteosarcoma Growth by Inactivation of Notch Signaling
journal, April 2014

Regulation of osteogenic differentiation during skeletal development
journal, January 2008

  • Deng, Zhong-Liang
  • Frontiers in Bioscience, Vol. 13, Issue 13
  • DOI: 10.2741/2819

Mesenchymal Progenitor Cells and Their Orthopedic Applications: Forging a Path towards Clinical Trials
journal, January 2010

  • Shenaq, Deana S.; Rastegar, Farbod; Petkovic, Djuro
  • Stem Cells International, Vol. 2010
  • DOI: 10.4061/2010/519028

Mesenchymal stem cells: Molecular characteristics and clinical applications
journal, January 2010

Our Fat Future: Translating Adipose Stem Cell Therapy: Translating Adipose Stem Cell Therapy
journal, July 2015

  • Nordberg, Rachel C.; Loboa, Elizabeth G.
  • STEM CELLS Translational Medicine, Vol. 4, Issue 9
  • DOI: 10.5966/sctm.2015-0071

The Prodomain-Containing BMP9 Produced from a Stable Line Effectively Regulates the Differentiation of Mesenchymal Stem Cells
journal, January 2016

  • Li, Ruifang; Yan, Zhengjian; Ye, Jixing
  • International Journal of Medical Sciences, Vol. 13, Issue 1
  • DOI: 10.7150/ijms.13333
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