Skip to main content
SpringerLink
Log in

2D nanomaterials for tissue engineering application

  • Review Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

Recently, tissue engineering has developed into a powerful tool for repairing and reconstructing damaged tissues and organs. Tissue engineering scaffolds play a vital role in tissue engineering, as they not only provide structural support for targeted cells but also serve as templates that guide tissue regeneration and control the tissue structure. Over the past few years, owing to unique physicochemical properties and excellent biocompatibility, various types of two-dimensional (2D) nanomaterials have been developed as candidates for the construction of tissue engineering scaffolds, enabling remarkable achievements in bone repair, wound healing, neural regeneration, and cardiac tissue engineering. These efforts have significantly advanced the development of tissue engineering. In this review, we summarize the latest advancements in the application of 2D nanomaterials in tissue engineering. First, each typical 2D nanomaterial is introduced briefly, followed by a detailed description of its applications in tissue engineering. Finally, the existing challenges and prospects for the future of the application of 2D nanomaterials in tissue engineering are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Léonard, F.; Talin, A. A. Electrical contacts to one- and two-dimensional nanomaterials. Nat. Nanotechnol.2011, 6, 773–783.

    Google Scholar 

  2. Kim, M. H.; Hur, W.; Choi, G.; Min, H. S.; Choi, T. H.; Choy, Y. B.; Choy, J. H. Theranostic bioabsorbable bone fixation plate with drug-layered double hydroxide nanohybrids. Adv. Healthc. Mater.2016, 5, 2765–2775.

    CAS  Google Scholar 

  3. Luo, M. M.; Fan, T. J.; Zhou, Y.; Zhang, H.; Mei, L. 2D black phosphorus-based biomedical applications. Adv. Healthc. Mater.2019, 29, 1808306.

    Google Scholar 

  4. Liu, Z. M.; Chen, H. L.; Jia, Y. L.; Zhang, W.; Zhao, H. A.; Fan, W. D.; Zhang, W. L.; Zhong, H. Q.; Ni, Y. R.; Guo, Z. Y. A two-dimensional fingerprint nanoprobe based on black phosphorus for bio-SERS analysis and chemo-photothermal therapy. Nanoscale2018, 10, 18795–18804.

    CAS  Google Scholar 

  5. Shah, S.; Yin, P. T.; Uehara, T. M.; Chueng, S. T. D.; Yang, L. T.; Lee, K. B. Guiding stem cell differentiation into oligodendrocytes using graphene-nanofiber hybrid scaffolds. Adv. Mater.2014, 26, 3673–3680.

    CAS  Google Scholar 

  6. Coleman, J. N.; Lotya, M.; O’Neill, A.; Bergin, S. D.; King, P. J.; Khan, U.; Young, K.; Gaucher, A.; De, S.; Smith, R. J. et al. Two-dimensional nanosheets produced by liquid exfoliation of layered materials. Science2011, 331, 568–571.

    CAS  Google Scholar 

  7. Novoselov, K. S.; Geim, A. K.; Morozov, S. V.; Jiang, D.; Zhang, Y.; Dubonos, S. V.; Grigorieva, I. V.; Firsov, A. A. Electric field effect in atomically thin carbon films. Science2004, 306, 666–669.

    CAS  Google Scholar 

  8. Kurapati, R.; Kostarelos, K.; Prato, M.; Bianco, A. Biomedical uses for 2D materials beyond graphene: Current advances and challenges ahead. Adv. Mater.2016, 28, 6052–6074.

    CAS  Google Scholar 

  9. Tu, Z. X.; Guday, G.; Adeli, M.; Haag, R. Multivalent interactions between 2D nanomaterials and biointerfaces. Adv. Mater.2018, 30, 1706709.

    Google Scholar 

  10. Chen, W. S.; Ouyang, J.; Yi, X. Y.; Xu, Y.; Niu, C. C.; Zhang, W. Y.; Wang, L. Q.; Sheng, J. P.; Deng, L.; Liu, Y. N. et al. Black phosphorus nanosheets as a neuroprotective nanomedicine for neurodegenerative disorder therapy. Adv. Mater.2018, 30, 1703458.

    Google Scholar 

  11. Guo, Z. N.; Chen, S.; Wang, Z. Z.; Yang, Z. Y.; Liu, F.; Xu, Y. H.; Wang, J. H.; Yi, Y.; Zhang, H.; Liao, L. et al. Metal-ion-modified black phosphorus with enhanced stability and transistor performance. Adv. Mater.2017, 29, 1703811.

    Google Scholar 

  12. Tao, W.; Zhu, X. B.; Yu, X. H.; Zeng, X. W.; Xiao, Q. L.; Zhang, X. D.; Ji, X. Y.; Wang, X. S.; Shi, J. J.; Zhang, H. et al. Black phosphorus nanosheets as a robust delivery platform for cancer theranostics. Adv. Mater.2017, 29, 1603276.

    Google Scholar 

  13. Chen, W. S.; Ouyang, J.; Liu, H.; Chen, M.; Zeng, K.; Sheng, J. P.; Liu, Z. J.; Han, Y. J.; Wang, L. Q.; Li, J. et al. Black phosphorus nanosheet-based drug delivery system for synergistic photodynamic/photothermal/chemotherapy of cancer. Adv. Mater.2017, 29, 1603864.

    Google Scholar 

  14. Wang, S. H.; Shao, J. D.; Li, Z. B.; Ren, Q. Z.; Yu, X. F.; Liu, S. J. Black phosphorus-based multimodal nanoagent: Showing targeted combinatory therapeutics against cancer metastasis. Nano Lett.2019, 19, 5587–5594.

    CAS  Google Scholar 

  15. Lee, H. U.; Park, S. Y.; Lee, S. C.; Choi, S.; Seo, S.; Kim, H.; Won, J.; Choi, K.; Kang, K. S.; Park, H. G. et al. Black Phosphorus (BP) nanodots for potential biomedical applications. Small.2016, 12, 214–9.

    CAS  Google Scholar 

  16. Banerjee, A. N. Graphene and its derivatives as biomedical materials: Future prospects and challenges. Interface Focus2018, 8, 20170056.

    Google Scholar 

  17. Munhoz, D. R.; Bernardo, M. P.; Malafatti, J. O. D.; Moreira, F. K. V.; Mattoso, L. H. C. Alginate films functionalized with silver sulfadiazine-loaded [Mg-Al] layered double hydroxide as antimicrobial wound dressing. Int. J. Biol. Macromol.2019, 141, 504–510.

    CAS  Google Scholar 

  18. Kenry; Lee, W. C.; Loh, K. P.; Lim, C. T. When stem cells meet graphene: Opportunities and challenges in regenerative medicine. Biomaterials2018, 155, 236–250.

    CAS  Google Scholar 

  19. Feng, L. Z.; Liu, Z. Graphene in biomedicine: Opportunities and challenges. Nanomedicine2011, 6, 317–324.

    CAS  Google Scholar 

  20. Lu, N.; Wang, L. Q.; Lv, M.; Tang, Z. S.; Fan, C. H. Graphene-based nanomaterials in biosystems. Nano Res.2019, 12, 247–264.

    CAS  Google Scholar 

  21. Diez-Pascual, A. M.; Diez-Vicente, A. L. Poly (propylene fumarate)/polyethylene glycol-modified graphene oxide nanocomposites for tissue engineering. ACS Appl. Mater. Interfaces2016, 8, 17902–17914.

    CAS  Google Scholar 

  22. Park, K. O.; Lee, J. H.; Park, J. H.; Shin, Y. C.; Huh, J. B.; Bae, J. H.; Kang, S. H.; Hong, S. W.; Kim, B.; Yang, D. J. et al. Graphene oxide-coated guided bone regeneration membranes with enhanced osteogenesis: Spectroscopic analysis and animal study. Appl. Spectrosc. Rev.2016, 51, 540–551.

    CAS  Google Scholar 

  23. Zhao, Y.; Chen, J. D.; Zou, L.; Xu, G.; Geng, Y. S. Facile one-step bioinspired mineralization by chitosan functionalized with graphene oxide to activate bone endogenous regeneration. Chem. Eng. J.2019, 378, 122174.

    CAS  Google Scholar 

  24. Lee, J. H.; Shin, Y. C.; Lee, S. M.; Jin, O. S.; Kang, S. H.; Hong, S. W.; Jeong, C. M.; Huh, J. B.; Han, D. W. Enhanced osteogenesis by reduced graphene oxide/hydroxyapatite nanocomposites. Sci. Rep.2015, 5, 18833.

    CAS  Google Scholar 

  25. Liang, C. Y.; Luo, Y. C.; Yang, G. D.; Xia, D.; Liu, L.; Zhang, X. M.; Wang, H. S. Graphene oxide hybridized nHAC/PLGA scaffolds facilitate the proliferation of MC3T3-E1 cells. Nanoscale Res. Lett.2018, 13, 15.

    Google Scholar 

  26. Aidun, A.; Firoozabady, A. S.; Moharrami, M.; Ahmadi, A.; Haghighipour, N.; Bonakdar, S.; Faghihi, S. Graphene oxide incorporated polycaprolactone/chitosan/collagen electrospun scaffold: Enhanced osteogenic properties for bone tissue engineering. Artif. Organs2019, 43, E264–E281.

    CAS  Google Scholar 

  27. Jabbari, F.; Hesaraki, S.; Houshmand, B. The physical, mechanical, and biological properties of silk fibroin/chitosan/reduced graphene oxide composite membranes for guided bone regeneration. J. Biomat. Sci. Polym. Ed.2019, 30, 1779–1802.

    CAS  Google Scholar 

  28. Olad, A.; Hagh, H. B. K.; Mirmohseni, A.; Azhar, F. F. Graphene oxide and montmorillonite enriched natural polymeric scaffold for bone tissue engineering. Ceram. Int.2019, 45, 15609–15619.

    CAS  Google Scholar 

  29. Gardin, C.; Piattelli, A.; Zavan, B. Graphene in regenerative medicine: Focus on stem cells and neuronal differentiation. Trends Biotechnol.2016, 34, 435–437.

    CAS  Google Scholar 

  30. Weaver, C. L.; Cui, X. T. Directed neural stem cell differentiation with a functionalized graphene oxide nanocomposite. Adv. Healthc. Mater.2015, 4, 1408–1416.

    CAS  Google Scholar 

  31. Tang, M. L.; Song, Q.; Li, N.; Jiang, Z. Y.; Huang, R.; Cheng, G. S. Enhancement of electrical signaling in neural networks on graphene films. Biomaterials2013, 34, 6402–6411.

    CAS  Google Scholar 

  32. Serrano, M. C.; Patiño, J.; García-Rama, C.; Ferrer, M. L.; Fierro, J. L. G.; Tamayo, A.; Collazos-Castro, J. E.; Del Monte, F.; Gutiérrez, M. C. 3D free-standing porous scaffolds made of graphene oxide as substrates for neural cell growth. J. Mater. Chem. B.2014, 2, 5698–5706.

    CAS  Google Scholar 

  33. Yang, D. H.; Li, T.; Xu, M. H.; Gao, F.; Yang, J.; Yang, Z.; Le, W. D. Graphene oxide promotes the differentiation of mouse embryonic stem cells to dopamine neurons. Nanomedicine2014, 9, 2445–2455.

    CAS  Google Scholar 

  34. Nezakati, T.; Tan, A.; Lim, J.; Cormia, R. D.; Teoh, S. H.; Seifalian, A. M. Ultra-low percolation threshold POSS-PCL/graphene electrically conductive polymer: Neural tissue engineering nanocomposites for neurosurgery. Mater. Sci. Eng. C2019, 104, 109915.

    CAS  Google Scholar 

  35. Lee, J.; Manoharan, V.; Cheung, L.; Lee, S.; Cha, B. H.; Newman, P.; Farzad, R.; Mehrotra, S.; Zhang, K.; Khan, F. et al. Nanoparticle-based hybrid scaffolds for deciphering the role of multimodal cues in cardiac tissue engineering. ACS Nano.2019, 13, 12525–12539.

    CAS  Google Scholar 

  36. Paul, A.; Hasan, A.; Al Kindi, H.; Gaharwar, A. K.; Rao, V. T. S.; Nikkhah, M.; Shin, S. R.; Krafft, D.; Dokmeci, M. R.; Shum-Tim, D. et al. Injectable graphene oxide/hydrogel-based angiogenic gene delivery system for vasculogenesis and cardiac repair. ACS Nano.2014, 8, 8050–8062.

    CAS  Google Scholar 

  37. Choe, G.; Kim, S. W.; Park, J.; Park, J.; Kim, S.; Kim, Y. S.; Ahn, Y.; Jung, D. W.; Williams, D. R.; Lee, J. Y. Anti-oxidant activity reinforced reduced graphene oxide/alginate microgels: Mesenchymal stem cell encapsulation and regeneration of infarcted hearts. Biomaterials2019, 225, 119513.

    CAS  Google Scholar 

  38. Saravanan, S.; Sareen, N.; Abu-El-Rub, E.; Ashour, H.; Sequiera, G. L.; Ammar, H. I.; Gopinath, V.; Shamaa, A. A.; Sayed, S. S. E.; Moudgil, M. et al. Graphene oxide-gold nanosheets containing chitosan scaffold improves ventricular contractility and function after implantation into infarcted heart. Sci. Rep.2018, 8, 15069.

    Google Scholar 

  39. Ghasemi, A.; Imani, R.; Yousefzadeh, M.; Bonakdar, S.; Solouk, A.; Fakhrzadeh, H. Studying the potential application of electrospun polyethylene terephthalate/graphene oxide nanofibers as electro-conductive cardiac patch. Macromol. Mater. Eng.2019, 304, 1900187.

    Google Scholar 

  40. Jiang, L. L.; Chen, D. Y.; Wang, Z.; Zhang, Z. M.; Xia, Y. L.; Xue, H. Y.; Liu, Y. Preparation of an electrically conductive graphene oxide/chitosan scaffold for cardiac tissue engineering. Appl. Biochem. Biotechnol.2019, 188, 952–964.

    CAS  Google Scholar 

  41. Nazari, H.; Azadi, S.; Hatamie, S.; Zomorrod, M. S.; Ashtari, K.; Soleimani, M.; Hosseinzadeh, S. Fabrication of graphene-silver/polyurethane nanofibrous scaffolds for cardiac tissue engineering. Polym. Adv. Technol.2019, 30, 2086–2099.

    CAS  Google Scholar 

  42. Norahan, M. H.; Pourmokhtari, M.; Saeb, M. R.; Bakhshi, B.; Zomorrod, M. S.; Baheiraei, N. Electroactive cardiac patch containing reduced graphene oxide with potential antibacterial properties. Mater. Sci. Eng. C2019, 104, 109921.

    CAS  Google Scholar 

  43. Stone, H.; Lin, S. G.; Mequanint, K. Preparation and characterization of electrospun rGO-poly (ester amide) conductive scaffolds. Mater. Sci. Eng. C2019, 98, 324–332.

    CAS  Google Scholar 

  44. Zargar, S. M.; Mehdikhani, M.; Rafienia, M. Reduced graphene oxide-reinforced gellan gum thermoresponsive hydrogels as a myocardial tissue engineering scaffold. J. Bioact. Compat. Polm.2019, 34, 331–345.

    CAS  Google Scholar 

  45. Zhao, L. A novel graphene oxide polymer gel platform for cardiac tissue engineering application. 3 Biotech2019, 9, 401.

    Google Scholar 

  46. Shin, S. R.; Aghaei-Ghareh-Bolagh, B.; Gao, X. G.; Nikkhah, M.; Jung, S. M.; Dolatshahi-Pirouz, A.; Kim, S. B.; Kim, S. M.; Dokmeci, M. R.; Tang, X. W. et al. Layer-by-layer assembly of 3D tissue constructs with functionalized graphene. Adv. Funct. Mater.2014, 24, 6136–6144.

    CAS  Google Scholar 

  47. Zhang, F.; Zhang, N.; Meng, H. X.; Liu, H. X.; Lu, Y. Q.; Liu, C. M.; Zhang, Z. M.; Qu, K. Y.; Huang, N. P. Easy applied gelatin-based hydrogel system for long-term functional cardiomyocyte culture and myocardium formation. ACS Biomater. Sci. Eng.2019, 5, 3022–3031.

    CAS  Google Scholar 

  48. Shin, S. R.; Li, Y. C.; Jang, H. L.; Khoshakhlagh, P.; Akbari, M.; Nasajpour, A.; Zhang, Y. S.; Tamayol, A.; Khademhosseini, A. Graphene-based materials for tissue engineering. Adv. Drug Deliv. Rev.2016, 105, 255–274.

    CAS  Google Scholar 

  49. Zhou, M.; Lozano, N.; Wychowaniec, J. K.; Hodgkinson, T.; Richardson, S. M.; Kostarelos, K.; Hoyland, J. A. Graphene oxide: A growth factor delivery carrier to enhance chondrogenic differentiation of human mesenchymal stem cells in 3D hydrogels. Acta Biomater.2019, 96, 271–280.

    CAS  Google Scholar 

  50. Holmes, B.; Fang, X. Q.; Zarate, A.; Keidar, M.; Zhang, L. G. Enhanced human bone marrow mesenchymal stem cell chondrogenic differentiation in electrospun constructs with carbon nanomaterials. Carbon2016, 97, 1–13.

    Google Scholar 

  51. Deliormanlı, A. M.; Atmaca, H. Biological response of osteoblastic and chondrogenic cells to graphene-containing PCL/bioactive glass bilayered scaffolds for osteochondral tissue engineering applications. Appl. Biochem. Biotech.2018, 186, 972–989.

    Google Scholar 

  52. Deliormanlı, A. M. Direct write assembly of graphene/poly (ε-Caprolactone) composite scaffolds and evaluation of their biological performance using mouse bone marrow mesenchymal stem cells. Appl. Biochem. Biotech.2019, 188, 1117–1133.

    Google Scholar 

  53. Lee, E. J.; Lee, J. H.; Shin, Y. C.; Hwang, D. G.; Kim, J. S.; Jin, O. S.; Jin, L. H.; Hong, S. W.; Han, D. W. Graphene oxide-decorated PLGA/collagen hybrid fiber sheets for application to tissue engineering scaffolds. Biomater. Res.2014, 18, 18–24.

    Google Scholar 

  54. Li, Z. H.; Wang, H. Q.; Yang, B.; Sun, Y. K.; Huo, R. Three-dimensional graphene foams loaded with bone marrow derived mesenchymal stem cells promote skin wound healing with reduced scarring. Mater. Sci. Eng. C2015, 57, 181–188.

    CAS  Google Scholar 

  55. Azarniya, A.; Eslahi, N.; Mahmoudi, N.; Simchi, A. Effect of graphene oxide nanosheets on the physico-mechanical properties of chitosan/bacterial cellulose nanofibrous composites. Compos. Part. A Appl. Sci Manuf.2016, 85, 113–122.

    CAS  Google Scholar 

  56. Mahmoudi, N.; Simchi, A. On the biological performance of graphene oxide-modified chitosan/polyvinyl pyrrolidone nanocomposite membranes: In vitro and in vivo effects of graphene oxide. Mater. Sci. Eng. C2017, 70, 121–131.

    CAS  Google Scholar 

  57. Chu, J.; Shi, P. P.; Yan, W. X.; Fu, J. P.; Yang, Z.; He, C. M.; Deng, X. Y.; Liu, H. P. PEGylated graphene oxide-mediated quercetin-modified collagen hybrid scaffold for enhancement of MSCs differentiation potential and diabetic wound healing. Nanoscale2018, 10, 9547–9560.

    CAS  Google Scholar 

  58. Hussein, K. H.; Abdelhamid, H. N.; Zou, X. D.; Woo, H. M. Ultrasonicated graphene oxide enhances bone and skin wound regeneration. Mater. Sci. Eng. C2019, 94, 484–492.

    CAS  Google Scholar 

  59. Liang, Y. P.; Zhao, X.; Hu, T. L.; Chen, B. J.; Yin, Z. H.; Ma, P. X.; Guo, B. L. Adhesive hemostatic conducting injectable composite hydrogels with sustained drug release and photothermal antibacterial activity to promote full-thickness skin regeneration during wound healing. Small2019, 15, 1900046.

    Google Scholar 

  60. Chaudhuri, B.; Bhadra, D.; Moroni, L.; Pramanik, K. Myoblast differentiation of human mesenchymal stem cells on graphene oxide and electrospun graphene oxide-polymer composite fibrous meshes: Importance of graphene oxide conductivity and dielectric constant on their biocompatibility. Biofabrication2015, 7, 015009.

    Google Scholar 

  61. Chaudhuri, B.; Mondal, B.; Kumar, S.; Sarkar, S. C. Myoblast differentiation and protein expression in electrospun graphene oxide (GO)-poly (ε-caprolactone, PCL) composite meshes. Mater. Lett.2016, 182, 194–197.

    CAS  Google Scholar 

  62. Patel, A.; Xue, Y. F.; Mukundan, S.; Rohan, L. C.; Sant, V.; Stolz, D. B.; Sant, S. Cell-instructive graphene-containing nanocomposites induce multinucleated myotube formation. Ann. Biomed. Eng.2016, 44, 2036–2048.

    Google Scholar 

  63. Li, L. K.; Yu, Y. J.; Ye, G. J.; Ge, Q. Q.; Ou, X. D.; Wu, H.; Feng, D. L.; Chen, X. H.; Zhang, Y. B. Black phosphorus field-effect transistors. Nat. Nanotechnol.2014, 9, 372–377.

    CAS  Google Scholar 

  64. Luo, M. M.; Fan, T. J.; Zhou, Y.; Zhang, H.; Mei, L. 2D black phosphorus-based biomedical applications. Adv. Funct. Mater.2019, 29, 1808306.

    Google Scholar 

  65. Raucci, M. G.; Fasolino, I.; Caporali, M.; Serrano-Ruiz, M.; Soriente, A.; Peruzzini, M.; Ambrosio, L. Exfoliated black phosphorus promotes in vitro bone regeneration and suppresses osteosarcoma progression through cancer-related inflammation inhibition. ACS Appl. Mater. Interfaces2019, 11, 9333–9342.

    CAS  Google Scholar 

  66. Huang, K. Q.; Wu, J.; Gu, Z. P. Black phosphorus hydrogel scaffolds enhance bone regeneration via a sustained supply of calcium-free phosphorus. ACS Appl. Mater. Interfaces2019, 11, 2908–2916.

    CAS  Google Scholar 

  67. Liu, X. F.; Miller II, A. L.; Park, S.; George, M. N.; Waletzki, B. E.; Xu, H. C.; Terzic, A.; Lu, L. C. Two-dimensional black phosphorus and graphene oxide nanosheets synergistically enhance cell proliferation and osteogenesis on 3D printed scaffolds. ACS Appl. Mater. Interfaces2019, 11, 23558–23572.

    CAS  Google Scholar 

  68. Miao, Y. L.; Shi, X. T.; Li, Q. T.; Hao, L. J.; Liu, L.; Liu, X.; Chen, Y. H.; Wang, Y. J. Engineering natural matrices with black phosphorus nanosheets to generate multi-functional therapeutic nanocomposite hydrogels. Biomater. Sci.2019, 7, 4046–4059.

    CAS  Google Scholar 

  69. Yang, B. W.; Yin, J. H.; Chen, Y.; Pan, S. S.; Yao, H. L.; Gao, Y. S.; Shi, J. L. 2D-black-phosphorus-reinforced 3D-printed scaffolds: A stepwise countermeasure for osteosarcoma. Adv. Mater.2018, 30, 1705611.

    Google Scholar 

  70. Tong, L. P.; Liao, Q.; Zhao, Y. T.; Huang, H.; Gao, A.; Zhang, W.; Gao, X. Y.; Wei, W.; Guan, M.; Chu, P. K. et al. Near-infrared light control of bone regeneration with biodegradable photothermal osteoimplant. Biomaterials2019, 193, 1–11.

    CAS  Google Scholar 

  71. Wang, Y. Q.; Hu, X. X.; Zhang, L. L.; Zhu, C. L.; Wang, J.; Li, Y. X.; Wang, Y. L.; Wang, C.; Zhang, Y. F.; Yuan, Q. Bioinspired extracellular vesicles embedded with black phosphorus for molecular recognition-guided biomineralization. Nat. Commun.2019, 10, 2829.

    Google Scholar 

  72. Huang, X. W.; Wei, J. J.; Zhang, M. Y.; Zhang, X. L.; Yin, X. F.; Lu, C. H.; Song, J. B.; Bai, S. M.; Yang, H. H. Water-based black phosphorus hybrid nanosheets as a moldable platform for wound healing applications. ACS Appl. Mater. Interfaces2018, 10, 35495–35502.

    CAS  Google Scholar 

  73. Mao, C. Y.; Xiang, Y. M.; Liu, X. M.; Cui, Z. D.; Yang, X. J.; Li, Z. Y.; Zhu, S. L.; Zheng, Y. F.; Yeung, K. W. K.; Wu, S. L. Repeatable photodynamic therapy with triggered signaling pathways of fibroblast cell proliferation and differentiation to promote bacteria-accompanied wound healing. ACS Nano2018, 12, 1747–1759.

    CAS  Google Scholar 

  74. Wang, Z. M.; Zhao, J.; Tang, W. Z.; Hu, L. Q.; Chen, X.; Su, Y. P.; Zou, C.; Wang, J. H.; Lu, W. W.; Zhen, W. X. et al. Multifunctional nanoengineered hydrogels consisting of black phosphorus nanosheets upregulate bone formation. Small2019, 15, 1901560.

    CAS  Google Scholar 

  75. Wang, X. Z.; Shao, J. D.; El Raouf, M. A.; Xie, H. H.; Huang, H.; Wang, H. Y.; Chu, P. K.; Yu, X. F.; Yang, Y.; AbdEl-Aal, A. M. et al. Near-infrared light-triggered drug delivery system based on black phosphorus for in vivo bone regeneration. Biomaterials2018, 179, 164–174.

    CAS  Google Scholar 

  76. Chen, W. S.; Ouyang, J.; Yi, X. Y.; Xu, Y.; Niu, C. C.; Zhang, W. Y.; Wang, L. Q.; Sheng, J. P.; Deng, L.; Liu, Y. N. et al. Black phosphorus nanosheets as a neuroprotective nanomedicine for neurodegenerative disorder therapy. Adv. Mater.2018, 30, 1703458.

    Google Scholar 

  77. Qian, Y.; Yuan, W. E.; Cheng, Y.; Yang, Y. Q.; Qu, X. H.; Fan, C. Y. Concentrically integrative bioassembly of a three-dimensional black phosphorus nanoscaffold for restoring neurogenesis, angiogenesis, and immune homeostasis. Nano Lett.2019, 19, 8990–9001.

    CAS  Google Scholar 

  78. Xie, H. H.; Shao, J. D.; Ma, Y. F.; Wang, J. H.; Huang, H.; Yang, N.; Wang, H. Y.; Ruan, C. S.; Luo, Y. F.; Wang, Q. Q. et al. Biodegradable near-infrared-photoresponsive shape memory implants based on black phosphorus nanofillers. Biomaterials2018, 164, 11–21.

    CAS  Google Scholar 

  79. Shao, J. D.; Ruan, C. S.; Xie, H. H.; Li, Z. B.; Wang, H. Y.; Chu, P. K.; Yu, X. F. Black-phosphorus-incorporated hydrogel as a sprayable and biodegradable photothermal platform for postsurgical treatment of cancer. Adv. Sci.2018, 5, 1700848.

    Google Scholar 

  80. Gaharwar, A. K.; Cross, L. M.; Peak, C. W.; Gold, K.; Carrow, J. K.; Brokesh, A.; Singh, K. A. 2D nanoclay for biomedical applications: Regenerative medicine, therapeutic delivery, and additive manufacturing. Adv. Mater.2019, 31, 1900332.

    Google Scholar 

  81. Chen, Y. X.; Zhu, R.; Ke, Q. F.; Gao, Y. S.; Zhang, C. Q.; Guo, Y. P. MgAl layered double hydroxide/chitosan porous scaffolds loaded with PFTα to promote bone regeneration. Nanoscale2017, 9, 6765–6776.

    CAS  Google Scholar 

  82. Fayyazbakhsh, F.; Solati-Hashjin, M.; Keshtkar, A.; Shokrgozar, M. A.; Dehghan, M. M.; Larijani, B. Novel layered double hydroxides-hydroxyapatite/gelatin bone tissue engineering scaffolds: Fabrication, characterization, and in vivo study. Mater. Sci. Eng. C2017, 76, 701–714.

    CAS  Google Scholar 

  83. Peng, F.; Wang, D. H.; Zhang, D. D.; Yan, B. C.; Cao, H. L.; Qiao, Y. Q.; Liu, X. Y. PEO/Mg-Zn-Al LDH composite coating on Mg alloy as a Zn/Mg ion-release platform with multifunctions: Enhanced corrosion resistance, osteogenic, and antibacterial activities. ACS Biomater. Sci. Eng.2018, 4, 4112–4121.

    CAS  Google Scholar 

  84. Cao, D. D.; Xu, Z. L.; Chen, Y. X.; Ke, Q. F.; Zhang, C. Q.; Guo, Y. P. Ag-loaded MgSrFe-layered double hydroxide/chitosan composite scaffold with enhanced osteogenic and antibacterial property for bone engineering tissue. J. Biomed. Mater. Res. Part B Appl. Biomater.2018, 106, 863–873.

    CAS  Google Scholar 

  85. Fayyazbakhsh, F.; Solati-Hashjin, M.; Shokrgozar, M. A.; Bonakdar, S.; Ganji, Y.; Mirjordavi, N.; Ghavimi, S. A.; Khashayar, P. Biological evaluation of a novel tissue engineering scaffold of Layered Double Hydroxides (LDHs). Key Eng. Mater.2011, 493–494, 902–908.

    Google Scholar 

  86. Fayyazbakhsh, F.; Solati-Hashjin, M.; Keshtkar, A.; Shokrgozar, M. A.; Dehghan, M. M.; Larijani, B. Release behavior and signaling effect of vitamin D3 in layered double hydroxides-hydroxyapatite/gelatin bone tissue engineering scaffold: An in vitro evaluation. Colloids Surf. B Biointerfaces2017, 158, 697–708.

    CAS  Google Scholar 

  87. Ramanathan, G.; Sobhana, S. S. L.; Fardim, P.; Sivagnanam, U. T. Fabrication of 3D dual-layered nanofibrous graft loaded with layered double hydroxides and their effects in osteoblastic behavior for bone tissue engineering. Process Biochem.2018, 64, 255–259.

    CAS  Google Scholar 

  88. Piao, H.; Kim, M. H.; Cui, M.; Choi, G.; Choy, J. H. Alendronate-anionic clay nanohybrid for enhanced osteogenic proliferation and differentiation. J. Korean Med. Sci.2019, 34, e37.

    Google Scholar 

  89. Kieke, M. D. K.; Weizbauer, A.; Duda, F.; Badar, M.; Budde, S.; Flörkemeier, T.; Diekmann, J.; Prenzler, N.; Rahim, M. I.; Müller, P. P. et al. Evaluating a novel class of biomaterials: Magnesium-containing layered double hydroxides. Biomed. Tech.2013, 58 Suppl 1.

  90. Weizbauer, A.; Kieke, M.; Rahim, M. I.; Angrisani, G. L.; Willbold, E.; Diekmann, J.; Flörkemeier, T.; Windhagen, H.; Müller, P. P.; Behrens, P. et al. Magnesium-containing layered double hydroxides as orthopaedic implant coating materials-an in vitro and in vivo study. J. Biomed. Mater. Res. Part B Appl. Biomater.2016, 104, 525–531.

    CAS  Google Scholar 

  91. Figueiredo, M. P.; Cunh, V. R. R.; Leroux, F.; Taviot-Gueho, C.; Nakamae, M. N.; Kang, Y. R.; Souza, R. B.; Martins, A. M. C. R. P. F.; Koh, I. H. J.; Constantino, V. R. L. Iron-based layered double hydroxide implants: Potential drug delivery carriers with tissue biointegration promotion and blood microcirculation preservation. ACS Omega2018, 3, 18263–18274.

    CAS  Google Scholar 

  92. Singh, N. K.; Nguyen, Q. V.; Kim, B. S.; Lee, D. S. Nanostructure controlled sustained delivery of human growth hormone using injectable, biodegradable, PH/temperature responsive nanobiohybrid hydrogel. Nanoscale2015, 7, 3043–3054.

    CAS  Google Scholar 

  93. Kang, H. R.; Da Costa Fernandes, C. J.; da Silva, R. A.; Constantino, V. R. L.; Koh, I. H. J.; Zambuzzi, W. F. Mg-Al and Zn-Al layered double hydroxides promote dynamic expression of marker genes in osteogenic differentiation by modulating mitogen-activated protein kinases. Adv. Healthc. Mater.2018, 7, 1700693.

    Google Scholar 

  94. Bernardo, M. P.; Ribeiro, C. Zn-Al-based layered double hydroxides (LDH) active structures for dental restorative materials. J. Mater. Res. Tech.2019, 8, 1250–1257.

    CAS  Google Scholar 

  95. Moghanizadeh-Ashkezari, M.; Shokrollahi, P.; Zandi, M.; Shokrolahi, F.; Daliri, M. J.; Kanavi, M. R.; Balagholi, S. Vitamin C loaded poly (urethane-urea)/ZnAl-LDH aligned scaffolds increase proliferation of corneal keratocytes and up-regulate vimentin secretion. ACS Appl. Mater. Interfaces2019, 11, 35525–35539.

    CAS  Google Scholar 

  96. Shafiei, S. S.; Shavandi, M.; Ahangari, G.; Shokrolahi, F. Electrospun layered double hydroxide/poly (ε-caprolactone) nanocomposite scaffolds for adipogenic differentiation of adipose-derived mesenchymal stem cells. Appl. Clay. Sci.2016, 127–128, 52–63.

    Google Scholar 

  97. Galateanu, B.; Radu, I. C.; Vasile, E.; Hudita, A.; Serban, M. V.; Costache, M.; Iovu, H.; Zaharia, C. Fabrication of novel silk fibroin-LDHs composite arhitectures for potential bone tissue engineering. Mater. Plast.2017, 54, 659–665.

    Google Scholar 

  98. Li, Q. W.; Wang, D. H.; Qiu, J. J.; Peng, F.; Liu, X. Y. Regulating the local PH level of titanium via Mg-Fe layered double hydroxides films for enhanced osteogenesis. Biomater. Sci.2018, 6, 1227–1237.

    CAS  Google Scholar 

  99. Bunea, M. C.; Galateanu, B.; Vasile, E.; Zaharia, C.; Stanescu, P. O.; Andronescu, C.; Radu, I. C.; Fuchs, R.; Iovu, H. Novel biocomposites based on polyhydroxyalkanoates-layered double hydroxides for tissue engineering applications. U.P.B. Sci. Bull. Series B2016, 78, 81–90.

    CAS  Google Scholar 

  100. Cunha, V. R. R.; De Souza, R. B.; Da Fonseca Martins, A. M. C. R. P.; Koh, I. H. J.; Constantino, V. R. L. Accessing the biocompatibility of layered double hydroxide by intramuscular implantation: Histological and microcirculation evaluation. Sci. Rep.2016, 6, 30547.

    Google Scholar 

  101. Radu, I. C.; Vasile, E.; Damian, C. M.; Iovu, H.; Stanescu, P. O.; Zaharia, C. Influence of the double bond LDH clay on the exfoliation/intercalation mechanism of polyacrylamide nanocomposite hydrogels. Mater. Plast.2018, 55, 263–268.

    Google Scholar 

  102. Zhang, Y. P.; Ji, J. W.; Li, H. P.; Du, N.; Song, S.; Hou, W. G. Synthesis of layered double hydroxide/poly(N-isopropylacrylamide) nanocomposite hydrogels with excellent mechanical and thermoresponsive performances. Soft Matter2018, 14, 1789–1798.

    CAS  Google Scholar 

  103. Wang, S.; Zhang, Z. F.; Dong, L. F.; Waterhouse, G. I. N.; Zhang, Q. H.; Li, L. F. A remarkable thermosensitive hydrogel cross-linked by two inorganic nanoparticles with opposite charges. J. Colloid Interf. Sci.2019, 538, 530–540.

    CAS  Google Scholar 

  104. Chakraborti, M.; Jackson, J. K.; Plackett, D.; Brunette, D. M.; Burt, H. M. Drug intercalation in layered double hydroxide clay: Application in the development of a nanocomposite film for guided tissue regeneration. Int. J. Pharm.2011, 416, 305–313.

    CAS  Google Scholar 

  105. Huang, H. Q.; Xu, J. B.; Wei, K. C.; Xu, Y. J.; Choi, C. K. K.; Zhu, M. L.; Bian, L. M. Bioactive nanocomposite poly (ethylene glycol) hydrogels crosslinked by multifunctional layered double hydroxides nanocrosslinkers. Macromol. Biosci.2016, 16, 1019–1026.

    CAS  Google Scholar 

  106. Yang, H. Y.; Van Ee, R. J.; Timmer, K.; Craenmehr, E. G. M.; Huang, J. H.; Öner, F. C.; Dhert, W. J. A.; Kragten, A. H. M.; Willems, N.; Grinwis, G. C. M. et al. A novel injectable thermoresponsive and cytocompatible gel of poly (N-isopropylacrylamide) with layered double hydroxides facilitates siRNA delivery into chondrocytes in 3D culture. Acta Biomater.2015, 23, 214–228.

    CAS  Google Scholar 

  107. Wang, P.; Wei, Z.-Y.; Cheng, J.; Liu, L. Preparation and characterization of a novel hybrid copolymer hydrogel with poly(ethylene glycol) dimethacrylate, 2-hydroxyethyl methacrylate and layered double hydroxides. Journal of Shanghai Jiaotong University (Science)2012, 17, 712–16.

    Google Scholar 

  108. Kapusetti, G.; Misra, N.; Singh, V.; Kushwaha, R. K.; Maiti, P. Bone cement/layered double hydroxide nanocomposites as potential biomaterials for joint implant. J. Biomed. Mater. Res. Part A2012, 100A, 3363–3373.

    CAS  Google Scholar 

  109. Kim, M. H.; Park, D. H.; Yang, J. H.; Choy, Y. B.; Choy, J. H. Drug-inorganic-polymer nanohybrid for transdermal delivery. Int. J. Pharm.2013, 444, 120–127.

    CAS  Google Scholar 

  110. Harris, K. J.; Bugnet, M.; Naguib, M.; Barsoum, M. W.; Goward, G. R. Direct measurement of surface termination groups and their connectivity in the 2D Mxene V2CTx using NMR spectroscopy. J. Phys. Chem. C2015, 119, 13713–13720.

    CAS  Google Scholar 

  111. Annunziata, M.; Oliva, A.; Basile, M. A.; Giordano, M.; Mazzola, N.; Rizzo, A.; Lanza, A.; Guida, L. The effects of titanium nitride-coating on the topographic and biological features of TPS implant surfaces. J. Dent.2011, 39, 720–728.

    CAS  Google Scholar 

  112. Veronesi, F.; Giavaresi, G.; Fini, M.; Longo, G.; Ioannidu, C. A.; d’Abusco, A. S.; Superti, F.; Panzini, G.; Misiano, C.; Palattella, A. et al. Osseointegration is improved by coating titanium implants with a nanostructured thin film with titanium carbide and titanium oxides clustered around graphitic carbon. Mater. Sci. Eng. C2017, 70, 264–271.

    CAS  Google Scholar 

  113. Chen, K.; Qiu, N. X.; Deng, Q. H.; Kang, M. H.; Yang, H.; Baek, J. U.; Koh, Y. H.; Du, S. Y.; Huang, Q.; Kim, H. E. Cytocompatibility of Ti3AlC2, Ti3SiC2, and Ti2AlN: In vitro tests and first-principles calculations. ACS Biomater. Sci. Eng.2017, 3, 2293–2301.

    CAS  Google Scholar 

  114. Mayerberger, E. A.; Street, R. M.; McDaniel, R. M.; Barsoum, M. W.; Schauer, C. L. Antibacterial properties of electrospun Ti3C2Tz (MXene)/Chitosan nanofibers. RSC Adv.2018, 8, 35386–35394.

    CAS  Google Scholar 

  115. Tao, W.; Kong, N.; Ji, X. Y.; Zhang, Y. P.; Sharma, A.; Ouyang, J., Qi, B. W.; Wang, J. Q.; Xie, N.; Kang, C. et al. Emerging two-dimensional monoelemental materials (Xenes) for biomedical applications. Chem. Soc. Rev.2019, 48, 2891–2912.

    CAS  Google Scholar 

  116. Subramanian, B.; Muraleedharan, C. V.; Ananthakumar, R.; Jayachandran, M. A comparative study of titanium nitride (TiN), titanium oxy nitride (TiON) and titanium aluminum nitride (TiAlN), as surface coatings for bio implants. Surf. Coat. Technol.2011, 205, 5014–5020.

    CAS  Google Scholar 

  117. Jeong, Y. H.; Lee, C. H.; Chung, C. H.; Son, M. K.; Choe, H. C. Effects of TiN and WC coating on the fatigue characteristics of dental implant. Surf. Coat. Technol.2014, 243, 71–81.

    CAS  Google Scholar 

  118. Chen, K.; Chen, Y. H.; Deng, Q. H.; Jeong, S. H.; Jang, T. S.; Du, S. Y.; Kim, H. E.; Huang, Q.; Han, C. M. Strong and biocompatible poly(lactic acid) membrane enhanced by Ti3C2Tz (MXene) nanosheets for Guided bone regeneration. Mater. Lett.2018, 229, 114–117.

    CAS  Google Scholar 

  119. Ramezani, M. R.; Ansari-Asl, Z.; Hoveizi, E.; Kiasat, A. R. Polyacrylonitrile/Fe(III) metal-organic framework fibrous nano-composites designed for tissue engineering applications. Mater. Chem. Phys.2019, 229, 242–250.

    CAS  Google Scholar 

  120. Wu, S. Y.; Wang, J. D.; Jin, L.; Li, Y.; Wang, Z. L. Effects of polyacrylonitrile/MoS2 composite nanofibers on the growth behavior of bone marrow mesenchymal stem cells. ACS Appl. Nano Mater.2018, 1, 337–343.

    CAS  Google Scholar 

  121. Unal, S.; Ekren, N.; Sengil, A. Z.; Oktar, F. N.; Irmak, S.; Oral, O.; Sahin, Y. M.; Kilic, O.; Agathopoulos, S.; Gunduz, O. Synthesis, characterization, and biological properties of composites of hydroxyapatite and hexagonal boron nitride. J. Biomed. Mater. Res. Part B Appl. Biomater.2018, 106, 2384–2392.

    CAS  Google Scholar 

  122. Lei, Z. Y.; Zhou, Y. Y.; Wu, P. Y. Simultaneous exfoliation and functionalization of MoSe2 nanosheets to prepare “Smart” nanocomposite hydrogels with tunable dual stimuli-responsive behavior. Small2016, 12, 3112–3118.

    CAS  Google Scholar 

  123. Wang, K.; Li, N.; Hai, X. M.; Dang, F. Q. Lysozyme-mediated fabrication of well-defined core-shell nanoparticle@metal-organic framework nanocomposites. J. Mater. Chem. A2017, 5, 20765–20770.

    CAS  Google Scholar 

  124. Márquez, A. G.; Hidalgo, T.; Lana, H.; Cunha, D.; Blanco-Prieto, M. J.; Álvarez-Lorenzo, C.; Boissière, C.; Sánchez, C.; Serre, C.; Horcajada, P. Biocompatible polymer-metal-organic framework composite patches for cutaneous administration of cosmetic molecules. J. Mater. Chem. B2016, 4, 7031–7040.

    Google Scholar 

  125. Ozbek, B.; Erdogan, B.; Ekren, N.; Oktar, F. N.; Akyol, S.; Ben-Nissan, B.; Sasmazel, H. T.; Kalkandelen, C.; Mergen, A.; Kuruca, S. E. et al. Production of the novel fibrous structure of poly(ε-caprolactone)/tri-calcium phosphate/hexagonal boron nitride composites for bone tissue engineering. J. Aust. Ceram. Soc.2018, 54, 251–260.

    CAS  Google Scholar 

  126. Jing, L.; Li, H. L.; Tay, R. Y.; Sun, B.; Tsang, S. H.; Cometto, O.; Lin, J. J.; Teo, E. H. T.; Tok, A. I. Y. Biocompatible hydroxylated boron nitride nanosheets/poly(vinyl alcohol) interpenetrating hydrogels with enhanced mechanical and thermal responses. ACS Nano2017, 11, 3742–3751.

    CAS  Google Scholar 

  127. Rakhshaei, R.; Namazi, H.; Hamishehkar, H.; Kafil, H. S.; Salehi, R. In situ synthesized chitosan-gelatin/ZnO nanocomposite scaffold with drug delivery properties: Higher antibacterial and lower cytotoxicity effects. J. Appl. Polym. Sci.2019, 136, 47590.

    Google Scholar 

  128. Artifon, W.; Pasini, S. M.; Valério, A.; González, S. Y. G.; De Arruda Guelli Ulson de Souza, S. M.; De Souza, A. A. U. Harsh environment resistant-antibacterial zinc oxide/polyetherimide electrospun composite scaffolds. Mater. Sci. Eng. C2019, 103, 109859.

    CAS  Google Scholar 

  129. Jinga, S. I.; Zamfirescu, A. I.; Voicu, G.; Enculescu, M.; Evanghelidis, A.; Busuioc, C. PCL-ZnO/TiO2/HAP electrospun composite fibers with applications in tissue engineering. Polymers2019, 11, 1793.

    CAS  Google Scholar 

  130. Makiura, R.; Motoyama, S.; Umemura, Y.; Yamanaka, H.; Sakata, O.; Kitagawa, H. Surface nano-architecture of a metal-organic framework. Nat. Mater.2010, 9, 565–571.

    CAS  Google Scholar 

  131. Cheng, L.; Wang, X. W.; Gong, F.; Liu, T.; Liu, Z. 2D nanomaterials for cancer theranostic applications. Adv. Mater.2019, 32, 1902333.

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Science and Technology Major Project of the Ministry of Science and Technology of China (No. 2018ZX10301402), General Program of National Natural Science Foundation of China (No. 51973243), Guangdong Innovative and Entrepreneurial Research Team Program (No. 2016ZT06S029), General Program of Guangdong Natural Science Foundation (No. 2020A1515010983), Science and Technology Planning Project of Shenzhen (Nos. JCYJ20170307141438157 and JCYJ20190807155801657), the Fundamental Research Funds for the Central Universities (No. 191gzd35).

Author information

Authors and Affiliations

  1. Key Laboratory of Sensing Technology and Biomedical Instrument of Guangdong Province, School of Biomedical Engineering, Sun Yat-sen University, Guangzhou, 510006, China

    Jingyang Zhang, Haolin Chen, Guiting Liu & Jun Wu

  2. Shenzhen Lansi Institute of Artificial Intelligence in Medicine, Shenzhen, 518057, China

    Meng Zhao

  3. Research Institute of Sun Yat-Sen University in Shenzhen, Shenzhen, 518057, China

    Jun Wu

Authors
  1. Jingyang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haolin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guiting Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jun Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Guiting Liu or Jun Wu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, J., Chen, H., Zhao, M. et al. 2D nanomaterials for tissue engineering application. Nano Res. 13, 2019–2034 (2020). https://doi.org/10.1007/s12274-020-2835-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-020-2835-4

Keywords

Search

Navigation