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Harnessing the Noncovalent Interactions of DNA Backbone with 2D Silicate Nanodisks To Fabricate Injectable Therapeutic Hydrogels

  • Sayantani Basu
    Sayantani Basu
    BioIntel Research Laboratory, Department of Chemical and Petroleum Engineering, School of Engineering, University of Kansas, Lawrence, Kansas 66045, United States
    More by Sayantani Basu
    • , 
  • Settimio Pacelli
    Settimio Pacelli
    BioIntel Research Laboratory, Department of Chemical and Petroleum Engineering, School of Engineering, University of Kansas, Lawrence, Kansas 66045, United States
    More by Settimio Pacelli
    Orcidhttp://orcid.org/0000-0002-4879-3615
    • , 
  • Yi Feng
    Yi Feng
    Harrington Laboratory for Molecular Orthopedics, Department of Orthopedic Surgery, Department of Biochemistry & Molecular Biology, University of Kansas Medical Center, Kansas City, Kansas 66160, United States
    More by Yi Feng
    • , 
  • Qinghua Lu
    Qinghua Lu
    Harrington Laboratory for Molecular Orthopedics, Department of Orthopedic Surgery, Department of Biochemistry & Molecular Biology, University of Kansas Medical Center, Kansas City, Kansas 66160, United States
    More by Qinghua Lu
    • , 
  • Jinxi Wang
    Jinxi Wang
    Harrington Laboratory for Molecular Orthopedics, Department of Orthopedic Surgery, Department of Biochemistry & Molecular Biology, University of Kansas Medical Center, Kansas City, Kansas 66160, United States
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    • , and 
  • Arghya Paul*
    Arghya Paul
    BioIntel Research Laboratory, Department of Chemical and Petroleum Engineering, School of Engineering, University of Kansas, Lawrence, Kansas 66045, United States
    *E-mail: [email protected]
    More by Arghya Paul
    Orcidhttp://orcid.org/0000-0003-4788-0378
Cite this: ACS Nano 2018, 12, 10, 9866–9880
Publication Date (Web):September 6, 2018
https://doi.org/10.1021/acsnano.8b02434
Copyright © 2018 American Chemical Society
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Abstract

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Injectable hydrogels present several advantages over prefabricated scaffolds including ease of delivery, shear-thinning property, and broad applicability in the fields of drug delivery and tissue engineering. Here, we report an approach to develop injectable hydrogels with sustained drug release properties, exploiting the chemical nature of the DNA backbone and silicate nanodisks. A two-step gelation method is implemented for generating a combination of noncovalent network points, leading to a physically cross-linked hydrogel. The first step initiates the development of an interconnected structure by utilizing DNA denaturation and rehybridization mechanism to form hydrogen bonds between complementary base pairs of neighboring DNA strands. The anisotropic charge distribution of two-dimensional silicate nanodisks (nSi) makes them an active center in the second step of the gelation process. Silicate nanodisks create additional network points via attractive electrostatic interactions with the DNA backbone, thereby enhancing the mechanical resilience of the formulated hydrogel. The thermally stable hydrogels displayed an increase in elasticity and yield stress as a function of nSi concentration. They were able to form self-supporting structures post injection due to their rapid recovery after removal of cyclic stress. Moreover, the presence of nanosilicate was shown to modulate the release of a model osteogenic drug dexamethasone (Dex). The bioactivity of released Dex was confirmed from in vitro osteogenic differentiation of human adipose stem cells and in vivo bone formation in a rat cranial bone defect model. Overall, our DNA-based nanocomposite hydrogel obtained from a combination of noncovalent network points can serve as an injectable material for bone regeneration and carrier for sustained release of therapeutics.

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The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.8b02434.

  • Rheological, structural and biological characterization of the nanocomposite hydrogels (PDF)

  • Movie S1: Video displaying the injection of 0.5% nSi through a 22 gauge surgical needle; the hydrogel is colored in blue for better visualization (AVI)

  • Movie S2: Video displaying the internal porosity of 0.5% nSi (AVI)

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Cited By

This article is cited by 19 publications.

  1. Xiao Zhang, Jiabing Fan, Chung-Sung Lee, Soyon Kim, Chen Chen, Min Lee. Supramolecular Hydrogels Based on Nanoclay and Guanidine-Rich Chitosan: Injectable and Moldable Osteoinductive Carriers. ACS Applied Materials & Interfaces 2020, 12 (14) , 16088-16096. https://doi.org/10.1021/acsami.0c01241
  2. Settimio Pacelli, Patrizia Paolicelli, Stefania Petralito, Siddharth Subham, Drake Gilmore, Gabriele Varani, Guang Yang, Dong Lin, Maria Antonietta Casadei, Arghya Paul. Investigating the Role of Polydopamine to Modulate Stem Cell Adhesion and Proliferation on Gellan Gum-Based Hydrogels. ACS Applied Bio Materials 2020, 3 (2) , 945-951. https://doi.org/10.1021/acsabm.9b00989
  3. Sayantani Basu, Abdul-Rahman Alkiswani, Settimio Pacelli, Arghya Paul. Nucleic Acid-Based Dual Cross-Linked Hydrogels for in Situ Tissue Repair via Directional Stem Cell Migration. ACS Applied Materials & Interfaces 2019, 11 (38) , 34621-34633. https://doi.org/10.1021/acsami.9b10074
  4. Yunfan Zhang, Tingting Yu, Liying Peng, Qiannan Sun, Yan Wei, Bing Han. Advancements in Hydrogel-Based Drug Sustained Release Systems for Bone Tissue Engineering. Frontiers in Pharmacology 2020, 11 https://doi.org/10.3389/fphar.2020.00622
  5. Qingqing Yao, Kirby E. Fuglsby, Xiao Zheng, Hongli Sun. Nanoclay-functionalized 3D nanofibrous scaffolds promote bone regeneration. Journal of Materials Chemistry B 2020, 8 (17) , 3842-3851. https://doi.org/10.1039/C9TB02814E
  6. Babatunde O. Okesola, Shilei Ni, Burak Derkus, Carles C. Galeano, Abshar Hasan, Yuanhao Wu, Jopeth Ramis, Lee Buttery, Jonathan I. Dawson, Matteo D'Este, Richard O. C. Oreffo, David Eglin, Hongchen Sun, Alvaro Mata. Growth‐Factor Free Multicomponent Nanocomposite Hydrogels That Stimulate Bone Formation. Advanced Functional Materials 2020, 30 (14) , 1906205. https://doi.org/10.1002/adfm.201906205
  7. Selvakumar Murugesan, Thomas Scheibel. Copolymer/Clay Nanocomposites for Biomedical Applications. Advanced Functional Materials 2020, 30 (17) , 1908101. https://doi.org/10.1002/adfm.201908101
  8. Liping Zhou, Xiangyu Jiao, Songyang Liu, Mingda Hao, Siyang Cheng, Peixun Zhang, Yongqiang Wen. Functional DNA-based hydrogel intelligent materials for biomedical applications. Journal of Materials Chemistry B 2020, 8 (10) , 1991-2009. https://doi.org/10.1039/C9TB02716E
  9. Sayantani Basu, Settimio Pacelli, Arghya Paul. Self-healing DNA-based injectable hydrogels with reversible covalent linkages for controlled drug delivery. Acta Biomaterialia 2020, 105 , 159-169. https://doi.org/10.1016/j.actbio.2020.01.021
  10. Kaivalya A. Deo, Kanwar Abhay Singh, Charles W. Peak, Daniel L. Alge, Akhilesh K. Gaharwar. Bioprinting 101: Design, Fabrication, and Evaluation of Cell-Laden 3D Bioprinted Scaffolds. Tissue Engineering Part A 2020, 26 (5-6) , 318-338. https://doi.org/10.1089/ten.tea.2019.0298
  11. Jianpu Tang, Chi Yao, Zi Gu, Sunghwan Jung, Dan Luo, Dayong Yang. Super‐Soft and Super‐Elastic DNA Robot with Magnetically Driven Navigational Locomotion for Cell Delivery in Confined Space. Angewandte Chemie 2020, 132 (6) , 2511-2516. https://doi.org/10.1002/ange.201913549
  12. Jianpu Tang, Chi Yao, Zi Gu, Sunghwan Jung, Dan Luo, Dayong Yang. Super‐Soft and Super‐Elastic DNA Robot with Magnetically Driven Navigational Locomotion for Cell Delivery in Confined Space. Angewandte Chemie International Edition 2020, 59 (6) , 2490-2495. https://doi.org/10.1002/anie.201913549
  13. Yuanhao Zhang, Mingjiao Chen, Zhaobo Dai, Hongliang Cao, Jin Li, Weian Zhang. Sustained protein therapeutics enabled by self-healing nanocomposite hydrogels for non-invasive bone regeneration. Biomaterials Science 2020, 8 (2) , 682-693. https://doi.org/10.1039/C9BM01455A
  14. Lijing Teng, Yunhua Chen, Yong-Guang Jia, Li Ren. Supramolecular and dynamic covalent hydrogel scaffolds: from gelation chemistry to enhanced cell retention and cartilage regeneration. Journal of Materials Chemistry B 2019, 7 (43) , 6705-6736. https://doi.org/10.1039/C9TB01698H
  15. Feng Li, Jianpu Tang, Jinhui Geng, Dan Luo, Dayong Yang. Polymeric DNA hydrogel: Design, synthesis and applications. Progress in Polymer Science 2019, 98 , 101163. https://doi.org/10.1016/j.progpolymsci.2019.101163
  16. Yali Miao, Xuetao Shi, Qingtao Li, Lijing Hao, Lei Liu, Xiao Liu, Yunhua Chen, Yingjun Wang. Engineering natural matrices with black phosphorus nanosheets to generate multi-functional therapeutic nanocomposite hydrogels. Biomaterials Science 2019, 7 (10) , 4046-4059. https://doi.org/10.1039/C9BM01072F
  17. Akhilesh K. Gaharwar, Lauren M. Cross, Charles W. Peak, Karli Gold, James K. Carrow, Anna Brokesh, Kanwar Abhay Singh. 2D Nanoclay for Biomedical Applications: Regenerative Medicine, Therapeutic Delivery, and Additive Manufacturing. Advanced Materials 2019, 31 (23) , 1900332. https://doi.org/10.1002/adma.201900332
  18. Shuai Cao, Xin Tong, Kun Dai, Qun Xu. A super-stretchable and tough functionalized boron nitride/PEDOT:PSS/poly( N -isopropylacrylamide) hydrogel with self-healing, adhesion, conductive and photothermal activity. Journal of Materials Chemistry A 2019, 7 (14) , 8204-8209. https://doi.org/10.1039/C9TA00618D
  19. Yuxin Zhang, Wenjuan Ma, Yuxi Zhan, Chenchen Mao, Xiaoru Shao, Xueping Xie, Xiawei Wei, Yunfeng Lin. Nucleic acids and analogs for bone regeneration. Bone Research 2018, 6 (1) https://doi.org/10.1038/s41413-018-0042-7

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