Journal Home > Volume 1 , Issue 1

Porous inorganic materials such as mesoporous silica nanoparticles (MSNs), mesoporous bioactive glasses (MBGs), porous calcium phosphates, and metal–organic frameworks (MOFs) are used for bone regeneration due to their osteoinductive and porous properties. The direct osteogenesis ability can be adjusted by the design and composition of those inorganic materials. With porous structure, adjustable pore size and high surface area, they are used as carriers to deliver various small molecular drugs, proteins, and genes locally to promote bone generation. The surface of those porous inorganic materials can be further functionalized to control the loading and release of drugs and modulate the behaviour of host cells. This review summarizes the recent advances of various porous inorganic nanomaterials for bone repairing with a focus on their performance as scaffolds and drug delivery systems. We also discuss the challenges and prospects of porous inorganic nanomaterials for the future clinical application for bone regeneration.


menu
Abstract
Full text
Outline
About this article

Advances in porous inorganic nanomaterials for bone regeneration

Show Author's information Huan Dai1,2Sepanta Hosseinpour1,2Shu Hua1,2Chun Xu1,2( )
School of Dentistry, The University of Queensland, Brisbane, Queensland 4006, Australia
Centre for Orofacial Regeneration, Reconstruction and Rehabilitation (COR3), School of Dentistry, The University of Queensland, Brisbane, Queensland 4006, Australia

Abstract

Porous inorganic materials such as mesoporous silica nanoparticles (MSNs), mesoporous bioactive glasses (MBGs), porous calcium phosphates, and metal–organic frameworks (MOFs) are used for bone regeneration due to their osteoinductive and porous properties. The direct osteogenesis ability can be adjusted by the design and composition of those inorganic materials. With porous structure, adjustable pore size and high surface area, they are used as carriers to deliver various small molecular drugs, proteins, and genes locally to promote bone generation. The surface of those porous inorganic materials can be further functionalized to control the loading and release of drugs and modulate the behaviour of host cells. This review summarizes the recent advances of various porous inorganic nanomaterials for bone repairing with a focus on their performance as scaffolds and drug delivery systems. We also discuss the challenges and prospects of porous inorganic nanomaterials for the future clinical application for bone regeneration.

Keywords: angiogenesis, drug delivery system, bone tissue engineering, osteogenesis, porous nanomaterials

References(112)

1

Dimitriou, R.; Jones, E.; McGonagle, D.; Giannoudis, P. V. Bone regeneration: Current concepts and future directions. BMC Med. 2011, 9, 66.

2

Giannoudis, P. V.; Dinopoulos, H.; Tsiridis, E. Bone substitutes: An update. Injury 2005, 36 Suppl 3, S20–S27.

3

Giannoudis, P. V.; Einhorn, T. A. Bone morphogenetic proteins in musculoskeletal medicine. Injury 2009, 40 Suppl 3, S1–S3.

4

Lee, J. H.; Hutzler, L. H.; Shulman, B. S.; Karia, R. J.; Egol, K. A. Does risk for malnutrition in patients presenting with fractures predict lower quality measures? J. Orthop. Trauma 2015, 29, 373–378.

5

Reddy, S.; Khalifian, S.; Flores, J. M.; Bellamy, J.; Manson, P. N.; Rodriguez, E. D.; Dorafshar, A. H. Clinical outcomes in cranioplasty: Risk factors and choice of reconstructive material. Plast. Reconstr. Surg. 2014, 133, 864–873.

6

Yan, X. X.; Yu, C. Z.; Zhou, X. F.; Tang, J. W.; Zhao, D. Y. Highly ordered mesoporous bioactive glasses with superior in vitro bone-forming bioactivities. Angew. Chem., Int. Ed. 2004, 43, 5980–5984.

7

Mora-Raimundo, P.; Lozano, D.; Benito, M.; Mulero, F.; Manzano, M.; Vallet-Regí, M. Osteoporosis remission and new bone formation with mesoporous silica nanoparticles. Adv. Sci. 2021, 8, 2101107.

8

Wang, N. Y.; Dheen, S. T.; Fuh, J. Y. H.; Kumar, A. S. A review of multi-functional ceramic nanoparticles in 3D printed bone tissue engineering. Bioprinting 2021, 23, e00146.

9

Xu, C.; Lei, C.; Huang, L. L.; Zhang, J.; Zhang, H. W.; Song, H.; Yu, M. H.; Wu, Y. D.; Chen, C.; Yu, C. Z. Glucose-responsive nanosystem mimicking the physiological insulin secretion via an enzyme- polymer layer-by-layer coating strategy. Chem. Mater. 2017, 29, 7725–7732.

10

Chen, Y.; Chen, H. R.; Shi, J. L. In vivo bio-safety evaluations and diagnostic/therapeutic applications of chemically designed mesoporous silica nanoparticles. Adv. Mater. 2013, 25, 3144–3176.

11

Manzano, M.; Vallet-Regí, M. Mesoporous silica nanoparticles for drug delivery. Adv. Funct. Mater. 2020, 30, 1902634.

12

Xu, C.; Lei, C.; Yu, C. Z. Mesoporous silica nanoparticles for protein protection and delivery. Front. Chem. 2019, 7, 290.

13

Xu, C.; Lei, C.; Wang, Y.; Yu, C. Z. Dendritic mesoporous nano-particles: Structure, synthesis and properties. Angew. Chem., Int. Ed., 2021: e202112752.

14

Zhang, P. H.; Cheng, F. F.; Zhou, R.; Cao, J. T.; Li, J. J.; Burda, C.; Min, Q. H.; Zhu, J. J. DNA-hybrid-gated multifunctional mesoporous silica nanocarriers for dual-targeted and microRNA-responsive controlled drug delivery. Angew. Chem., Int. Ed. 2014, 126, 2403–2407.

15

Hosseinpour, S.; Walsh, L. J.; Xu, C. Biomedical application of mesoporous silica nanoparticles as delivery systems: A biological safety perspective. J. Mater. Chem. B 2020, 8, 9863–9876.

16

Hosseinpour, S.; Walsh, L. J.; Xu, C. Modulating osteoimmune responses by mesoporous silica nanoparticles. ACS Biomater. Sci. Eng. 2021, https://doi.org/10.1021/acsbiomaterials.

17

Jugdaohsingh, R. Silicon and bone health. J. Nutr. Health Aging 2007, 11, 99–110.

18

Shi, M. C.; Zhou, Y. H.; Shao, J.; Chen, Z. T.; Song, B. T.; Chang, J.; Wu, C. T.; Xiao, Y. Stimulation of osteogenesis and angiogenesis of hBMSCs by delivering Si ions and functional drug from mesoporous silica nanospheres. Acta Biomater. 2015, 21, 178–189.

19

Mao, L. X.; Xia, L. G.; Chang, J.; Liu, J. Q.; Jiang, L. Y.; Wu, C. T.; Fang, B. The synergistic effects of Sr and Si bioactive ions on osteogenesis, osteoclastogenesis and angiogenesis for osteoporotic bone regeneration. Acta Biomater. 2017, 61, 217–232.

20

Xu, C.; Xiao, L.; Cao, Y. X.; He, Y.; Lei, C.; Xiao, Y.; Sun, W. J.; Ahadian, S.; Zhou, X. T.; Khademhosseini, A. et al. Mesoporous silica rods with cone shaped pores modulate inflammation and deliver BMP-2 for bone regeneration. Nano Res. 2020, 13, 2323–2331.

21

Xu, C.; Niu, Y. T.; Popat, A.; Jambhrunkar, S.; Karmakar, S.; Yu, C. Z. Rod-like mesoporous silica nanoparticles with rough surfaces for enhanced cellular delivery. J. Mater. Chem. B 2014, 2, 253–256.

22

Lei, C.; Cao, Y. X.; Hosseinpour, S.; Gao, F.; Liu, J. Y.; Fu, J. Y.; Staples, R.; Ivanovski, S.; Xu, C. Hierarchical dual-porous hydroxyapatite doped dendritic mesoporous silica nanoparticles based scaffolds promote osteogenesis in vitro and in vivo. Nano Res. 2021, 14, 770–777.

23

Liu, X. Z.; Sun, Y.; Shen, J. J.; Min, H. S.; Xu, J.; Chai, Y. M. Strontium doped mesoporous silica nanoparticles accelerate osteogenesis and angiogenesis in distraction osteogenesis by activation of Wnt pathway. Nanomedicine 2022, 41, 102496.

24

Mir, E.; Hossein-Nezhad, A.; Bahrami, A.; Bekheirnia, M. R.; Javadi, E.; Naderi, A. A.; Larijani, B. Adequate serum copper concentration could improve bone density, postpone bone loss and protect osteoporosis in women. Iran. J. Public Health 2007, 36, 24–29.

25

Feng, W. K.; Ye, F.; Xue, W. L.; Zhou, Z. X.; Kang, Y. J. Copper regulation of hypoxia-inducible factor-1 activity. Mol. Pharmacol. 2009, 75, 174–182.

26

Shi, M. C.; Chen, Z. T.; Farnaghi, S.; Friis, T.; Mao, X. L.; Xiao, Y.; Wu, C. T. Copper-doped mesoporous silica nanospheres, a promising immunomodulatory agent for inducing osteogenesis. Acta Biomater. 2016, 30, 334–344.

27

Liang, H.; Jin, C.; Ma, L.; Feng, X. B.; Deng, X. Y.; Wu, S. L.; Liu, X. M.; Yang, C. Accelerated bone regeneration by gold-nanoparticle- loaded mesoporous silica through stimulating immunomodulation. ACS Appl. Mater. Interfaces 2019, 11, 41758–41769.

28

Barta, C. A.; Sachs-Barrable, K.; Jia, J.; Thompson, K. H.; Wasan, K. M.; Orvig, C. Lanthanide containing compounds for therapeutic care in bone resorption disorders. Dalton Trans. 2007, 43, 5019–5030.

29

Shi, M. C.; Xia, L. G.; Chen, Z. T.; Lv, F.; Zhu, H. Y.; Wei, F.; Han, S. W.; Chang, J.; Xiao, Y.; Wu, C. T. Europium-doped mesoporous silica nanosphere as an immune-modulating osteogenesis/angiogenesis agent. Biomaterials 2017, 144, 176–187.

30

Zhou, X. J.; Feng, W.; Qiu, K. X.; Chen, L.; Wang, W. Z.; Nie, W.; Mo, X. M.; He, C. L. BMP-2 derived peptide and dexamethasone incorporated mesoporous silica nanoparticles for enhanced osteogenic differentiation of bone mesenchymal stem cells. ACS Appl. Mater. Interfaces 2015, 7, 15777–15789.

31

Iñiguez-Ariza, N. M.; Clarke, B. L. Bone biology, signaling pathways, and therapeutic targets for osteoporosis. Maturitas 2015, 82, 245–255.

32

Tang, F. Q.; Li, L. L.; Chen, D. Mesoporous silica nanoparticles: Synthesis, biocompatibility and drug delivery. Adv. Mater. 2012, 24, 1504–1534.

33

Wu, C. T.; Zhang, Y. F.; Zhou, Y. H.; Fan, W.; Xiao, Y. A comparative study of mesoporous glass/silk and non-mesoporous glass/silk scaffolds: Physiochemistry and in vivo osteogenesis. Acta Biomater. 2011, 7, 2229–2236.

34

Wu, C. T.; Ramaswamy, Y.; Zhu, Y. F.; Zheng, R. K.; Appleyard, R.; Howard, A.; Zreiqat, H. The effect of mesoporous bioactive glass on the physiochemical, biological and drug-release properties of poly(DL-lactide-co-glycolide) films. Biomaterials 2009, 30, 2199–2208.

35

Gómez-Cerezo, N.; Casarrubios, L.; Morales, I.; Feito, M. J.; Vallet-Regí, M.; Arcos, D.; Portolés, M. T. Effects of a mesoporous bioactive glass on osteoblasts, osteoclasts and macrophages. J. Colloid Interface Sci. 2018, 528, 309–320.

36

Westhauser, F.; Wilkesmann, S.; Nawaz, Q.; Hohenbild, F.; Rehder, F.; Saur, M.; Fellenberg, J.; Moghaddam, A.; Ali, M. S.; Peukert, W. et al. Effect of manganese, zinc, and copper on the biological and osteogenic properties of mesoporous bioactive glass nanoparticles. J. Biomed. Mater. Res. Part A 2021, 109, 1457–1467.

37

Kwun, I. S.; Cho, Y. E.; Lomeda, R. A. R.; Shin, H. I.; Choi, J. Y.; Kang, Y. H.; Beattie, J. H. Zinc deficiency suppresses matrix mineralization and retards osteogenesis transiently with catch-up possibly through Runx 2 modulation. Bone 2010, 46, 732–741.

38

Westhauser, F.; Wilkesmann, S.; Nawaz, Q.; Schmitz, S. I.; Moghaddam, A.; Boccaccini, A. R. Osteogenic properties of manganese-doped mesoporous bioactive glass nanoparticles. J. Biomed. Mater. Re. Part A 2020, 108, 1806–1815.

39

Wu, C. T.; Xia, L. G.; Han, P. P.; Mao, L. X.; Wang, J. C.; Zhai, D.; Fang, B.; Chang, J.; Xiao, Y. Europium-containing mesoporous bioactive glass scaffolds for stimulating in vitro and in vivo osteogenesis. ACS Appl. Mater. Interfaces 2016, 8, 11342–11354.

40

Kurtuldu, F.; Mutlu, N.; Michálek, M.; Zheng, K.; Masar, M.; Liverani, L.; Chen, S.; Galusek, D.; Boccaccini, A. R. Cerium and gallium containing mesoporous bioactive glass nanoparticles for bone regeneration: Bioactivity, biocompatibility and antibacterial activity. Mater. Sci. Eng. C 2021, 124, 112050.

41

Gargiulo, N.; Cusano, A. M.; Causa, F.; Caputo, D.; Netti, P. A. Silver- containing mesoporous bioactive glass with improved antibacterial properties. J. Mater. Sci. Mat. Med. 2013, 24, 2129–2135.

42

Wu, C. T.; Zhou, Y. H.; Lin, C. C.; Chang, J.; Xiao, Y. Strontium- containing mesoporous bioactive glass scaffolds with improved osteogenic/cementogenic differentiation of periodontal ligament cells for periodontal tissue engineering. Acta Biomater. 2012, 8, 3805–3815.

43

Bari, A.; Bloise, N.; Fiorilli, S.; Novajra, G.; Vallet-Regí, M.; Bruni, G.; Torres-Pardo, A.; González-Calbet, J. M.; Visai, L.; Vitale-Brovarone, C. Copper-containing mesoporous bioactive glass nanoparticles as multifunctional agent for bone regeneration. Acta Biomater. 2017, 55, 493–504.

44

Baino, F.; Fiorilli, S.; Vitale-Brovarone, C. Bioactive glass-based materials with hierarchical porosity for medical applications: Review of recent advances. Acta Biomater. 2016, 42, 18–32.

45

Perez, R. A.; El-Fiqi, A.; Park, J. H.; Kim, T. H.; Kim, J. H.; Kim, H. W. Therapeutic bioactive microcarriers: Co-delivery of growth factors and stem cells for bone tissue engineering. Acta Biomater. 2014, 10, 520–530.

46

López-Noriega, A.; Arcos, D.; Vallet-Regí, M. Functionalizing mesoporous bioglasses for long-term anti-osteoporotic drug delivery. Chem. Eur. J. 2010, 16, 10879–10886.

47

Wu, C. T.; Zhou, Y. H.; Chang, J.; Xiao, Y. Delivery of dimethyloxallyl glycine in mesoporous bioactive glass scaffolds to improve angiogenesis and osteogenesis of human bone marrow stromal cells. Acta Biomater. 2013, 9, 9159–9168.

48

Liu, L.; Zhao, F. J.; Chen, X. Y.; Luo, M.; Yang, Z.; Cao, X. D.; Miao, G. H.; Chen, D. F.; Chen, X. F. Local delivery of FTY720 in mesoporous bioactive glass improves bone regeneration by synergistically immunomodulating osteogenesis and osteoclastogenesis. J. Mater. Chem. B 2020, 8, 6148–6158.

49

Hosseinpour, S.; Ahsaie, M. G.; Rad, M. R.; Baghani, M. T.; Motamedian, S. R.; Khojasteh, A. Application of selected scaffolds for bone tissue engineering: A systematic review. Oral Maxillofac. Surg. 2017, 21, 109–129.

50

Hench, L. L.; Polak, J. M. Third-generation biomedical materials. Science 2002, 295, 1014–1017.

51

Dorozhkin, S. V. Calcium orthophosphates as bioceramics: State of the art. J. Funct. Biomater. 2010, 1, 22–107.

52

LeGeros, R. Z. Properties of osteoconductive biomaterials: Calcium phosphates. Clin. Orthop. Relat. Res. 2002, 395, 81–98.

53

Hing, K. A. Bioceramic bone graft substitutes: Influence of porosity and chemistry. Int. J. Appl. Ceram. Technol. 2005, 2, 184–199.

54

Wegst, U. G. K.; Bai, H.; Saiz, E.; Tomsia, A. P.; Ritchie, R. O. Bioinspired structural materials. Nat. Mater. 2015, 14, 23–36.

55

Jones, J. R.; Hench, L. L. Regeneration of trabecular bone using porous ceramics. Curr. Opin. Solid State Mater. Sci. 2003, 7, 301–307.

56

Zhou, K.; Yu, P.; Shi, X. J.; Ling, T. X.; Zeng, W. N.; Chen, A. J.; Yang, W.; Zhou, Z. K. Hierarchically porous hydroxyapatite hybrid scaffold incorporated with reduced graphene oxide for rapid bone ingrowth and repair. Acs Nano 2019, 13, 9595–9606.

57

Xu, Y. L.; Zhang, D. Y.; Zhou, Y.; Wang, W. D.; Cao, X. Y. Study on topology optimization design, manufacturability, and performance evaluation of Ti-6Al-4V porous structures fabricated by selective laser melting (SLM). Materials (Basel) 2017, 10, 1048.

58

Liu, Y. J.; Wang, H. L.; Li, S. J.; Wang, S. G.; Wang, W. J.; Hou, W. T.; Hao, Y. L.; Yang, R.; Zhang, L. C. Compressive and fatigue behavior of beta-type titanium porous structures fabricated by electron beam melting. Acta Mater. 2017, 126, 58–66.

59

Zhang, G. Q.; Li, J. X.; Zhang, C. G.; Xiao, Z. F. Simulation analysis and performance study of CoCrMo porous structure manufactured by selective laser melting. J. Mater. Eng. Perform. 2018, 27, 2271– 2280.

60

Zhu, Y. T.; Beyerlein, I. J. Bone-shaped short fiber composites—An overview. Mater. Sci. Eng. A 2002, 326, 208–227.

61

Claussen, N. Strengthening strategies for ZrO2-toughened ceramics at high temperatures. Mater. Sci. Eng. 1985, 71, 23–38.

62

Wahi, R. P.; Ilschner, B. Fracture behaviour of composites based on Al2O3-TiC. J. Mater. Sci. 1980, 15, 875–885.

63

Ramay, H. R. R.; Zhang, M. Biphasic calcium phosphate nanocomposite porous scaffolds for load-bearing bone tissue engineering. Biomaterials 2004, 25, 5171–5180.

64

Klein, C. P. A. T.; Driessen, A. A.; De Groot, K. Relationship between the dégradation behaviour of calcium phosphate ceramics and their physical-chemical characteristics and ultrastructural geometry. Biomaterials 1984, 5, 157–160.

65

Tas, A. C.; Korkusuz, F.; Timucin, M.; Akkas, N. An investigation of the chemical synthesis and high-temperature sintering behaviour of calcium hydroxyapatite (HA) and tricalcium phosphate (TCP) bioceramics. J. Mater. Sci. Mater. Med. 1997, 8, 91–96.

66

Klein, C. P. A. T.; De Blieck-Hogemrst, J. M.; Wolket, J. G. C.; De Groot, K. Studies of the solubility of different calcium phosphate ceramic particles in vitro. Biomaterials 1990, 11, 509–512.

67

Chen, Z. M.; Li, X. L.; Yang, C. Q.; Cheng, K. P.; Tan, T. W.; Lv, Y. Q.; Liu, Y. Hybrid porous crystalline materials from metal organic frameworks and covalent organic frameworks. Adv. Sci. 2021, 8, 2101883.

68

Kitagawa, S.; Kitaura, R.; Noro, S. I. Functional porous coordination polymers. Angew. Chem., Int. Ed. 2004, 43, 2334–2375.

69

Férey, G. Hybrid porous solids: Past, present, future. Chem. Soc. Rev. 2008, 37, 191–214.

70

Zhou, H. C.; Long, J. R.; Yaghi, O. M. Introduction to metal-organic frameworks. Chem. Rev. 2012, 112, 673–674.

71

Furukawa, H.; Cordova, K. E.; O'Keeffe, M.; Yaghi, O. M. The chemistry and applications of metal-organic frameworks. Science 2013, 341, 1230444.

72

Furukawa, S.; Reboul, J.; Diring, S.; Sumida, K.; Kitagawa, S. Structuring of metal-organic frameworks at the mesoscopic/macroscopic scale. Chem. Soc. Rev. 2014, 43, 5700–5734.

73

Gao, W. Y.; Chrzanowski, M.; Ma, S. Q. Metal-metalloporphyrin frameworks: A resurging class of functional materials. Chem. Soc. Rev. 2014, 43, 5841–5866.

74

Eddaoudi, M.; Sava, D. F.; Eubank, J. F.; Adil, K.; Guillerm, V. Zeolite-like metal–organic frameworks (ZMOFs): Design, synthesis, and properties. Chem. Soc. Rev. 2015, 44, 228–249.

75

Sun, Y. J.; Zhou, H. C. Recent progress in the synthesis of metal-organic frameworks. Sci. Technol. Adv. Mater. 2015, 16, 054202.

76

Koo, W. T.; Jang, J. S.; Kim, I. D. Metal-organic frameworks for chemiresistive sensors. Chem 2019, 5, 1938–1963.

77

Zhao, X.; Wang, Y. X.; Li, D. S.; Bu, X. H.; Feng, P. Y. Metal- organic frameworks for separation. Adv. Mater. 2018, 30, 1705189.

78

Liu, J. W.; Chen, L. F.; Cui, H.; Zhang, J. Y.; Zhang, L.; Su, C. Y. Applications of metal–organic frameworks in heterogeneous supramolecular catalysis. Chem. Soc. Rev. 2014, 43, 6011–6061.

79

Shyngys, M.; Ren, J.; Liang, X. Q.; Miao, J. C.; Blocki, A.; Beyer, S. Metal-organic framework (MOF)-based biomaterials for tissue engineering and regenerative medicine. Front. Bioeng. Biotechnol. 2021, 9, 603608.

80

Banerjee, R.; Furukawa, H.; Britt, D.; Knobler, C.; O'Keeffe, M.; Yaghi, O. M. Control of pore size and functionality in isoreticular zeolitic imidazolate frameworks and their carbon dioxide selective capture properties. J. Am. Chem. Soc. 2009, 131, 3875–3877.

81
Zuckerkandl, E.; Pauling, L. Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins. Bryson, V., Vogel, H. J., Eds.; Elsevier: New York, 1965; pp 97–166.https://doi.org/10.1016/B978-1-4832-2734-4.50017-6
DOI
82

Pan, H. M.; Beyer, S.; Zhu, Q. D.; Trau, D. Inwards interweaving of polymeric layers within hydrogels: Assembly of spherical multi- shells with discrete porosity differences. Adv. Funct. Mater. 2013, 23, 5108–5115.

83

Zhong, L. N.; Chen, J. Y.; Ma, Z. Y.; Feng, H.; Chen, S.; Cai, H.; Xue, Y. Y.; Pei, X. B.; Wang, J.; Wan, Q. B. 3D printing of metal–organic framework incorporated porous scaffolds to promote osteogenic differentiation and bone regeneration. Nanoscale 2020, 12, 24437–24449.

84

Zhu, Z.; Jiang, S. K.; Liu, Y. H.; Gao, X. M.; Hu, S. S.; Zhang, X.; Huang, C.; Wan, Q. B.; Wang, J.; Pei, X. B. Micro or nano: Evaluation of biosafety and biopotency of magnesium metal organic framework-74 with different particle sizes. Nano Res. 2020, 13, 511–526.

85

Li, Z.; Peng, Y.; Pang, X. C.; Tang, B. Potential therapeutic effects of Mg/HCOOH metal organic framework on relieving osteoarthritis. ChemMedChem 2020, 15, 13–16.

86

Joseph, N.; Lawson, H. D.; Overholt, K. J.; Damodaran, K.; Gottardi, R.; Acharya, A. P.; Little, S. R. Synthesis and characterization of CaSr-metal organic frameworks for biodegradable orthopedic applications. Sci. Rep. 2019, 9, 13024.

87

Chen, J. Y.; Zhang, X.; Huang, C.; Cai, H.; Hu, S. S.; Wan, Q. B.; Pei, X. B.; Wang, J. Osteogenic activity and antibacterial effect of porous titanium modified with metal-organic framework films. J. Biomed. Mater. Res. A 2017, 105, 834–846.

88

Zhang, Y. F.; Xu, J. K.; Ruan, Y. C.; Yu, M. K.; O'Laughlin, M.; Wise, H.; Chen, D.; Tian, L.; Shi, D. F.; Wang, J. L. et al. Implant- derived magnesium induces local neuronal production of CGRP to improve bone-fracture healing in rats. Nat. Med. 2016, 22, 1160–1169.

89

Zhang, Y. Y.; Shen, X. K.; Ma, P. P.; Peng, Z. H.; Cai, K. Y. Composite coatings of Mg-MOF74 and Sr-substituted hydroxyapatite on titanium substrates for local antibacterial, anti-osteosarcoma and pro-osteogenesis applications. Mater. Lett. 2019, 241, 18–22.

90

Liu, W.; Yan, Z. J.; Zhang, Z. D.; Zhang, Y. X.; Cai, G. Y.; Li, Z. Y. Bioactive and anti-corrosive bio-MOF-1 coating on magnesium alloy for bone repair application. J. Alloys Compd. 2019, 788, 705–711.

91

Tao, B. L.; Zhao, W. K.; Lin, C. C.; Yuan, Z.; He, Y.; Lu, L.; Chen, M. W.; Ding, Y.; Yang, Y. L.; Xia, Z. et al. Surface modification of titanium implants by ZIF-8@Levo/LBL coating for inhibition of bacterial- associated infection and enhancement of in vivo osseointegration. Chem. Eng. J. 2020, 390, 124621.

92

Zhou, J. L.; Wang, C. C.; Cunningham, A. J.; Hu, Z. X.; Xiang, H. X.; Sun, B.; Zuo, W. W.; Zhu, M. F. Synthesis and characterization of size-controlled nano-Cu2O deposited on alpha-zirconium phosphate with excellent antibacterial property. Mater. Sci. Eng. C 2019, 101, 499–504.

93

Pei, P.; Tian, Z. F.; Zhu, Y. F. 3D printed mesoporous bioactive glass/metal-organic framework scaffolds with antitubercular drug delivery. Microporous Mesoporous Mater. 2018, 272, 24–30.

94

Yu, M. F.; You, D. Q.; Zhuang, J. J.; Lin, S. Y.; Dong, L. Q.; Weng, S. T.; Zhang, B.; Cheng, K.; Weng, W. J.; Wang, H. M. Controlled release of naringin in metal-organic framework-loaded mineralized collagen coating to simultaneously enhance osseointegration and antibacterial activity. ACS Appl. Mater. Interfaces 2017, 9, 19698–19705.

95

Ran, J. B.; Zeng, H.; Cai, J.; Jiang, P.; Yan, P.; Zheng, L. Y.; Bai, Y.; Shen, X. Y.; Shi, B.; Tong, H. Rational design of a stable, effective, and sustained dexamethasone delivery platform on a titanium implant: An innovative application of metal organic frameworks in bone implants. Chem. Eng. J. 2018, 333, 20–33.

96

Telgerd, M. D.; Sadeghinia, M.; Birhanu, G.; Daryasari, M. P.; Zandi-Karimi, A.; Sadeghinia, A.; Akbarijavar, H.; Karami, M. H.; Seyedjafari, E. Enhanced osteogenic differentiation of mesenchymal stem cells on metal–organic framework based on copper, zinc, and imidazole coated poly-l-lactic acid nanofiber scaffolds. J. Biomed. Mater. Res. A 2019, 107, 1841–1848.

97

Tan, L. L.; Song, N.; Zhang, S. X. A.; Li, H.; Wang, B.; Yang, Y. W. Ca2+, pH and thermo triple-responsive mechanized Zr-based MOFs for on-command drug release in bone diseases. J. Mater. Chem. B 2016, 4, 135–140.

98

Sarkar, C.; Chowdhuri, A. R.; Garai, S.; Chakraborty, J.; Sahu, S. K. Three-dimensional cellulose-hydroxyapatite nanocomposite enriched with dexamethasone loaded metal–organic framework: A local drug delivery system for bone tissue engineering. Cellulose 2019, 26, 7253–7269.

99

Pereira, H. F.; Cengiz, I. F.; Silva, F. S.; Reis, R. L.; Oliveira, J. M. Scaffolds and coatings for bone regeneration. Journal of Materials Science: Materials in Medicine. 2020, 31, 1–16.

100

Chen, Y.; Kawazoe, N.; Chen, G. P. Preparation of dexamethasone- loaded biphasic calcium phosphate nanoparticles/collagen porous composite scaffolds for bone tissue engineering. Acta Biomater. 2018, 67, 341–353.

101

Qiu, Y. B.; Xu, X. D.; Guo, W. Z.; Zhao, Y.; Su, J. H.; Chen, J. Mesoporous hydroxyapatite nanoparticles mediate the release and bioactivity of BMP-2 for enhanced bone regeneration. ACS Biomater. Sci. Eng. 2020, 6, 2323–2335.

102

Balagangadharan, K.; Dhivya, S.; Selvamurugan, N. Chitosan based nanofibers in bone tissue engineering. Int. J. Biol. Macromol. 2017, 104, 1372–1382.

103

Melke, J.; Midha, S.; Ghosh, S.; Ito, K.; Hofmann, S. Silk fibroin as biomaterial for bone tissue engineering. Acta Biomater. 2016, 31, 1–16.

104

Tian, H. Y.; Tang, Z. H.; Zhuang, X. L.; Chen, X. S.; Jing, X. B. Biodegradable synthetic polymers: Preparation, functionalization and biomedical application. Progr. Polym. Sci. 2012, 37, 237–280.

105

Wang, J.; Wang, M. L.; Chen, F. Y.; Wei, Y. H.; Chen, X. N.; Zhou, Y.; Yang, X.; Zhu, X. D.; Tu, C. Q.; Zhang, X. D. Nano-hydroxyapatite coating promotes porous calcium phosphate ceramic-induced osteogenesis via BMP/Smad signaling pathway. Int. J. Nanomed. 2019, 14, 7987–8000.

106

Cao, Y. X.; Xiao, L.; Cao, Y. F.; Nanda, A.; Xu, C.; Ye, Q. S. 3D printed β-TCP scaffold with sphingosine 1-phosphate coating promotes osteogenesis and inhibits inflammation. Biochem. Biophys. Res. Commun. 2019, 512, 889–895.

107

He, C. F.; Wang, S. H.; Yu, Y. J.; Shen, H. Y.; Zhao, Y.; Gao, H. L.; Wang, H.; Li, L. L.; Liu, H. Y. Advances in biodegradable nano-materials for photothermal therapy of cancer. Cancer Biol. Med. 2016, 13, 299–312.

108

Croissant, J. G.; Fatieiev, Y.; Khashab, N. M. Degradability and clearance of silicon, organosilica, silsesquioxane, silica mixed oxide, and mesoporous silica nanoparticles. Adv. Mater. 2017, 29, 1604634.

109

Yu, M. X.; Zheng, J. Clearance pathways and tumor targeting of imaging nanoparticles. ACS Nano 2015, 9, 6655–6674.

110

Wang, X. W.; Zhong, X. Y.; Li, J. X.; Liu, Z.; Cheng, L. Inorganic nanomaterials with rapid clearance for biomedical applications. Chem. Soc. Rev. 2021, 50, 8669–8742.

111

Ball, A. N.; Donahue, S. W.; Wojda, S. J.; McIlwraith, C. W.; Kawcak, C. E.; Ehrhart, N.; Goodrich, L. R. The challenges of promoting osteogenesis in segmental bone defects and osteoporosis. J. Orthop. Res. 2018, 36, 1559–1572.

112

Henkel, J.; Woodruff, M. A.; Epari, D. R.; Steck, R.; Glatt, V.; Dickinson, I. C.; Choong, P. F. M.; Schuetz, M. A.; Hutmacher, D. W. Bone regeneration based on tissue engineering conceptions—A 21st century perspective. Bone Res. 2013, 1, 216–248.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 01 February 2022
Revised: 01 March 2022
Accepted: 02 March 2022
Published: 12 March 2022
Issue date: March 2022

Copyright

© The Author(s) 2022. Nano TransMed published by Tsinghua University Press.

Acknowledgements

Acknowledgements

The authors acknowledge the support from the Australian Dental Research Foundation (No. 0115-2021). C. X. acknowledges the support of the Early Career Fellowship from the National Health & Medical Research Council of Australia (NHMRC) and UQ Amplify Fellow from The University of Queensland.

Rights and permissions

The articles published in this open access journal are distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Return