Issue 23-3, 2024

Review

Rationale of using magnetically sensitive biomaterials in bone tissue therapy: a review



1 ORCIDPavel A. Markov, 1 ORCIDElena Yu. Kostromina, 1 ORCIDPetr S. Eremin, 1 ORCIDAnatoliy D. Fesyun

1National Medical Research Center for Rehabilitation and Balneology, Moscow, Russia


ABSTRACT

INTRODUCTION. Currently, new biomaterials are being intensively developed to improve the efficiency of repair of damage to hard and soft tissues. New approaches and methods for functionalizing biomaterials have been proposed. One such method is the use of magnetic nanoparticles. This approach is new and still little studied, however, the annual increase in the number of publications on this topic indicates the promise of studying the osteogenic effect of magnetic nanoparticles.

AIM. To summarize the results of current research devoted to studying the effect of magnetically sensitive biomaterials on the functional activity of cells involved in the reparation of bone tissue damage.

MATERIALS AND METHODS. A literature review was conducted using the databases PubMed and Scopus. Keywords used to conduct the search: electromagnetic field, magnetic nanoparticles, biomaterials, osteoinduction, bone regeneration. Request dates: February-March 2024, publication period 2000–2024 years.

MAIN CONTENT. New approaches and methods for functionalizing biomaterials have been proposed. One such approach is the use of magnetic nanoparticles (MNPs). Traditionally, in medicine, MNPs are used as a contrast agent to improve the visualization of cancer tumors; in addition, MNPs can act as a matrix in targeted drug delivery systems and in hyperthermic therapy of cancer tumors. New experimental data show that the use of MNPs as a magnetically sensitive component in biomaterials is a promising way to stimulate the repair of bone defects and fractures. It has been shown that biomaterials modified by nanoparticles stimulate osteogenic differentiation of stem cells, increase proliferative activity and secretion of extracellular matrix proteins by bone cells.

CONCLUSION. Integration of MNPs with organic and synthetic polymers, and other biomimetic constructs is a promising direction for creating osteogenic biomaterials for medical use, including those aimed at increasing the efficiency of regeneration of bone defects. The use of magnetically sensitive biomaterials makes it possible to create “smart” tissue-engineered structures controlled by external electromagnetic stimulus.


KEYWORDS: magnetic nanoparticles, biomaterials, osteoinduction, bone regeneration

FUNDING: The authors declare no external funding in the conduct of the study.

CONFLICT OF INTEREST: The authors declare no apparent or potential conflicts of interest related to the publication of this article.

FOR CITATION:

Markov P.A., Kostromina E.Yu., Fesyun A.D., Eremin P.S. Rationale of Using Magnetically Sensitive Biomaterials in Bone Tissue Therapy: a Review. Bulletin of Rehabilitation Medicine. 2024; 23(3):69-76. https://doi.org/10.38025/2078-1962-2024-23-3-69-76

FOR CORRESPONDENCE:

Pavel A. Markov, E-mail: markovpa@nmicrk.ru, p.a.markov@mail.ru


References:

  1. Battafarano G., Rossi M., De Martino V., et al. Strategies for Bone Regeneration: From Graft to Tissue Engineering. International Journal of Molecular Sciences. 2021; 22(3): 1128. https://doi.org/10.3390/ijms22031128
  2. Sawkins M.J., Bowen W., Dhadda P., et al. Hydrogels derived from demineralized and decellularized bone extracellular matrix. Acta Biomatererials. 2013; 9(8): 7865–7873. https://doi.org/10.1016/j.actbio.2013.04.029
  3. Zhai P., Peng X., Li B., et al. The application of hyaluronic acid in bone regeneration. International Journal of Biological Macromolecules. 2020; 151: 1224–1239. https://doi.org/10.1016/j.ijbiomac.2019.10.169
  4. Yu L., Wei M. Biomineralization of Collagen-Based Materials for Hard Tissue Repair. International Journal of Molecular Sciences. 2021; 22(2): 944. https://doi.org/10.3390/ijms22020944
  5. Jooken S., Deschaume O., Bartic C. Nanocomposite Hydrogels as Functional Extracellular Matrices. Gels. 2023; 9(2): 153. https://doi.org/10.3390/gels9020153
  6. Vermeulen S., Tahmasebi Birgani Z., Habibovic P. Biomaterial-induced pathway modulation for bone regeneration. Biomaterials. 2022; 283: 121431. https://doi.org/10.1016/j.biomaterials.2022.121431
  7. Noro J., Vilaça-Faria H., Reis R.L., Pirraco R.P. Extracellular matrix-derived materials for tissue engineering and regenerative medicine: A journey from isolation to characterization and application. Bioactive Materials. 2024; 17(34): 494–519. https://doi.org/10.1016/j.bioactmat.2024.01.004
  8. Amani H., Kazerooni H., Hassanpoor H., et al. Tailoring synthetic polymeric biomaterials towards nerve tissue engineering: a review. Artificial Cells, Nanomedicine, and Biotechnology. 2019; 47(1): 3524–3539. https://doi.org/10.1080/21691401.2019.1639723
  9. Bonewald L.F. The amazing osteocyte. Journal of Bone and Mineral Research. 2011; 26(2): 229–38. https://doi.org/10.1002/jbmr.320
  10. Delgado-Calle J., Bellido T. The osteocyte as a signaling cell. Physiological Reviews. 2022; 102(1): 379–410. https://doi.org/10.1152/physrev.00043.2020
  11. Cui J., Shibata Y., Zhu T., et al. Osteocytes in bone aging: Advances, challenges, and future perspectives. Ageing Research Reviews. 2022; 77: 101608. https://doi.org/10.1016/j.arr.2022.101608
  12. Shen L., Hu G., Karner C.M. Bioenergetic metabolism in osteoblast differentiation. Current Osteoporosis Reports. 2022; 20(1): 53–64. https://doi.org/10.1007/s11914-022-00721-2
  13. Ponzetti M., Rucci N. Osteoblast differentiation and signaling: established concepts and emerging topics. International Journal of Molecular Sciences. 2021; 22(13): 6651. https://doi.org/10.3390/ijms22136651
  14. Everts V., Delaissé J.M., Korper W., et al. The bone lining cell: its role in cleaning Howship’s lacunae and initiating bone formation. Journal of Bone and Mineral Research. 2002; 17(1): 77–90. https://doi.org/10.1359/jbmr.2002.17.1.77
  15. Clarke B. Normal bone anatomy and physiology. Clinical Journal Of The American Society Of Nephrology. 2008; 3(3): S131–S139. https://doi.org/10.2215/CJN.04151206
  16. Hong A.R., Kim K., Lee J.Y., et al. Transformation of mature osteoblasts into bone lining cells and RNA sequencing-based transcriptome profiling of mouse bone during mechanical unloading [published correction appears in Endocrinology and Metabolism (Seoul). 2021; 36(6): 1314]. Endocrinology and Metabolism (Seoul). 2020; 35(2): 456–469. https://doi.org/10.3803/EnM.2020.35.2.456
  17. Kim S.W., Pajevic P.D., Selig M., et al. Intermittent parathyroid hormone administration converts quiescent lining cells to active osteoblasts. Journal of Bone and Mineral Research. 2012; 27(10): 2075–2084. https://doi.org/10.1002/jbmr.1665
  18. Madel M.B., Ibáñez L., Wakkach A., et al. Immune function and diversity of osteoclasts in normal and pathological conditions. Frontiers in Immunology. 2019; 10: 1408. https://doi.org/10.3389/fimmu.2019.01408
  19. Takegahara N., Kim H., Choi Y. Unraveling the intricacies of osteoclast differentiation and maturation: insight into novel therapeutic strategies for bone-destructive diseases. Experimental & Molecular Medicine. 2024; 56: 264–272. https://doi.org/10.1038/s12276-024-01157-7
  20. Dominici M., Le Blanc K., Mueller I., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006; 8(4): 315–317. https://doi.org/10.1080/14653240600855905
  21. Lee Y.C., Chan Y.H., Hsieh S.C., et al. Comparing the osteogenic potentials and bone regeneration capacities of bone marrow and dental pulp mesenchymal stem cells in a rabbit calvarial bone defect model. International Journal of Molecular Sciences. 2019; 20(20): 5015. https://doi.org/10.3390/ijms20205015
  22. Xu W., Yang Y., Li N., Hua J. Interaction between mesenchymal stem cells and immune cells during bone injury repair. International Journal of Molecular Sciences. 2023; 24(19): 14484. https://doi.org/10.3390/ijms241914484
  23. Song N., Scholtemeijer M., Shah K. Mesenchymal stem cell immunomodulation: mechanisms and therapeutic potential. Trends in Pharmacological Sciences. 2020; 41: 653–664. https://doi.org/10.1016/j.tips.2020.06.009
  24. Dunn C.M., Kameishi S., Grainger D.W., Okano T. Strategies to address mesenchymal stem/stromal cell heterogeneity in immunomodulatory profiles to improve cell-based therapies. Acta Biomaterialia. 2021; 133: 114–125. https://doi.org/10.1016/j.actbio.2021.03.069
  25. Nurettin S., İbrahim A., Yusuf B., Muammer K. Superparamagnetic nanoarchitectures: Multimodal functionalities and applications. Journal of Magnetism and Magnetic Materials. 2021; 538: 168300. https://doi.org/10.1016/j.jmmm.2021.168300.
  26. Rarokar N., Yadav S., Saoji S., et al. Magnetic nanosystem a tool for targeted delivery and diagnostic application: Current challenges and recent advancement. International Journal of Pharmaceutics. 2024; 7: 100231. https://doi.org/10.1016/j.ijpx.2024.100231
  27. Akbarzadeh A., Samiei M., Davaran S. Magnetic nanoparticles: preparation, physical properties, and applications in biomedicine. Nanoscale Research Letters. 2012 21; 7(1): 144. https://doi.org/10.1186/1556-276X-7-144
  28. Andrade R.G.D., Veloso S.R.S., Castanheira E.M.S. Shape Anisotropic Iron Oxide-Based Magnetic Nanoparticles: Synthesis and Biomedical Applications. International Journal of Molecular Sciences. 2020; 21(7): 2455. https://doi.org/10.3390/ijms21072455
  29. Elahi N., Rizwan M. Progress and prospects of magnetic iron oxide nanoparticles in biomedical applications: A review. Artificial Organs. 2021; 45(11): 1272–1299. https://doi.org/10.1111/aor.14027
  30. Nemati Z., Alonso J., Rodrigo I., et al. Improving the heating efficiency of iron oxide nanoparticles by tuning their shape and size. Journal of Physical Chemistry C. 2018; 122: 2367–81. https://doi.org/10.1021/acs.jpcc.7b10528
  31. Arami H., Teeman E., Troksa A., et al. Tomographic magnetic particle imaging of cancer targeted nanoparticles. Nanoscale. 2017; 9(47): 18723–18730. https://doi.org/10.1039/c7nr05502a
  32. Lin J., Wang M., Hu H., et al. Multimodal-Imaging-Guided Cancer Phototherapy by Versatile Biomimetic Theranostics with UV and γ-Irradiation Protection. Advanced Materials. 2016; 28(17): 3273–3279. https://doi.org/10.1002/adma.201505700
  33. Estelrich J., Sánchez-Martín M.J., Busquets M.A. Nanoparticles in magnetic resonance imaging: from simple to dual contrast agents. International Journal of Nanomedicine. 2015; 10: 1727–1741. https://doi.org/10.2147/IJN.S76501
  34. Baki A., Wiekhorst F., Bleul R. Advances in magnetic nanoparticles engineering for biomedical applications- A review. Bioengineering (Basel). 2021; 8(10): 134. https://doi.org/10.3390/bioengineering8100134
  35. Tayyaba A., Nazim H., Hafsa, et al. Magnetic nanomaterials as drug delivery vehicles and therapeutic constructs to treat cancer. Journal of Drug Delivery Science and Technology. 2023; 80: 104103. https://doi.org/10.1016/j.jddst.2022.104103
  36. Ulbrich K., Holá K., Šubr V., et al. Targeted Drug Delivery with Polymers and Magnetic Nanoparticles: Covalent and Noncovalent Approaches, Release Control, and Clinical Studies. Chemical Reviews. 2016; 116(9): 5338–5431. https://doi.org/10.1021/acs.chemrev.5b00589
  37. Cao Z, Wang D., Li Y., et al. Effect of nanoheat stimulation mediated by magnetic nanocomposite hydrogel on the osteogenic differentiation of mesenchymal stem cells. Science China Life Sciences. 2018; 61(4): 448–456. https://doi.org/10.1007/s11427-017-9287-8
  38. Li Z., Xue L., Wang P., et al. Biological Scaffolds Assembled with Magnetic Nanoparticles for Bone Tissue Engineering: A Review. Materials (Basel). 2023; 16(4): 1429. https://doi.org/10.3390/ma16041429
  39. Li M., Fu S., Cai Z., et al. Dual Regulation of Osteoclastogenesis and Osteogenesis for Osteoporosis Therapy by Iron Oxide Hydroxyapatite Core/Shell Nanocomposites. Regenerative Biomatererials. 2021; 8(5): rbab027. https://doi.org/10.1093/rb/rbab027.
  40. Wang Q., Chen B., Cao M., et al. Response of MAPK Pathway to Iron Oxide Nanoparticles in Vitro Treatment Promotes Osteogenic Differentiation of hBMSCs. Biomaterials. 2016; 86: 11–20. https://doi.org/10.1016/j.bimaterials.2016.02.004
  41. Liu W., Zhao H., Zhang C., et al. In situ activation of flexible magnetoelectric membrane enhances bone defect repair. Nature Communications. 2023; 14(1): 4091. https://doi.org/10.1038/s41467-023-39744-3
  42. Hu S., Zhou Y., Zhao Y., et al. Enhanced bone regeneration and visual monitoring via superparamagnetic iron oxide nanoparticle scaffold in rats. Journal of Tissue Engineering and Regenerative Medicine. 2018; 12(4): e2085–e2098. https://doi.org/10.1002/term.2641
  43. Hao L., Li L., Wang P., et al. Synergistic osteogenesis promoted by magnetically actuated nano-mechanical stimuli. Nanoscale. 2019; 11(48): 23423–23437. https://doi.org/10.1039/c9nr07170a
  44. Silva E.D., Babo P.S., Costa-Almeida R., et al. Multifunctional magnetic-responsive hydrogels to engineer tendon-to-bone interface. Nanomedicine. 2018; 14(7): 2375–2385. https://doi.org/10.1016/j.nano.2017.06.002
  45. Shou Y., Le Z., Cheng H.S., et al. Mechano-Activated Cell Therapy for Accelerated Diabetic Wound Healing. Advanced Materials. 2023; 35(47): e2304638. https://doi.org/10.1002/adma.202304638
  46. Safronov A.P., Beketov I.V., Bagazeev A.V., et al. In Situ Encapsulation of Nickel Nanoparticles in Polysaccharide Shells during Their Fabrication by Electrical Explosion of Wire. Colloid Journal. 2023; 85: 541–553. https://doi.org/10.1134/S1061933X23600410
  47. Popov S.V., Markov P.A., Popova G.Yu., et al. Anti-inflammatory activity of low and high methoxylated citrus pectins. Biomedicine & Preventive Nutrition. 2013; 3(1): 59–63. https://doi.org/10.1016/j.bionut.2012.10.008
  48. Марков П.А., Волкова М.В., Хасаншина З.Р. и др. Противовоспалительное действие высоко- и низкометилэтерифицированных яблочных пектинов in vivo и in vitro. Вопросы питания. 2021; 90 (6): 92–100. https://doi.org/10.33029/0042-8833-2021-90-6-92-100 [Markov P.A., Volkova M.V., Khasanshina Z.R., et al. Anti-inflammatory activity of high and low methoxylated apple pectins, in vivo and in vitro. Voprosy pitaniia [Problems of Nutrition]. 2021; 90(6): 92–100. https://doi.org/10.33029/0042-8833-2021-90-6-92-100 (In Russ.).]
  49. Gerstenfeld L.C., Cullinane D.M., Barnes G.L., et al. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. Journal of Cellular Biochemistry. 2003; 88(5): 873–884. https://doi.org/10.1002/jcb.10435
  50. Özkale B., Sakar M.S., Mooney D.J. Active biomaterials for mechanobiology. Biomaterials. 2021; 267: 120497. https://doi.org/10.1016/j.biomaterials.2020.120497
  51. Elashry M.I., Baulig N., Wagner A.S., et al. Combined macromolecule biomaterials together with fluid shear stress promote the osteogenic differentiation capacity of equine adipose-derived mesenchymal stem cells. Stem Cell Research & Therapy. 2021; 12(1): 116. https://doi.org/10.1186/s13287-021-02146-7
  52. Chen G., Dong C., Yang L., Lv Y. 3D Scaffolds with Different Stiffness but the Same Microstructure for Bone Tissue Engineering. ACS Applied Materials & Interfaces. 2015; 7(29): 15790–15802. https://doi.org/10.1021/acsami.5b02662
  53. Lo C.M., Wang H.B., Dembo M., Wang Y.L. Cell movement is guided by the rigidity of the substrate. Biophysical Journal. 2000; 79(1): 144–152. https://doi.org/10.1016/S0006-3495(00)76279-5
  54. Horie S., Nakatomi C., Ito-Sago M., et al. PIEZO1 promotes ATP release from periodontal ligament cells following compression force. European Orthodontic Society. 2023; 45(5): 565–574. https://doi.org/10.1093/ejo/cjad052
  55. McWhorter F.Y., Wang T., Nguyen P., et al. Modulation of macrophage phenotype by cell shape. Proceedings of the National Academy of Sciences. 2013; 110(43): 17253–17258. https://doi.org/10.1073/pnas.1308887110
  56. Goswami R., Arya R.K., Sharma S., et al. Mechanosensing by TRPV4 mediates stiffness-induced foreign body response and giant cell formation. Science Signaling. 2021; 14(707): eabd4077. https://doi.org/10.1126/scisignal.abd4077
  57. Di X., Gao X., Peng L., et al. Cellular mechanotransduction in health and diseases: from molecular mechanism to therapeutic targets. Signal Transduction and Targeted Therapy. 2023; 8(1): 282. https://doi.org/10.1038/s41392-023-01501-9
  58. Mariño K.V., Cagnoni A.J., Croci D.O., Rabinovich G.A. Targeting galectin-driven regulatory circuits in cancer and fibrosis. Nature Reviews Drug Discovery. 2023; 22(4): 295–316. https://doi.org/10.1038/s41573-023-00636-2
  59. Dees C., Chakraborty D., Distler J.H.W. Cellular and molecular mechanisms in fibrosis. Experimental Dermatology. 2021; 30(1): 121-131. https://doi.org/10.1111/exd.14193
  60. Przekora A. Current trends in fabrication of biomaterials for bone and cartilage regeneration: materials modifications and biophysical stimulations. International Journal of Molecular Sciences. 2019; 20(2): 435. https://doi.org/10.3390/ijms20020435
  61. Babaniamansour P., Salimi M., Dorkoosh F., Mohammadi M. Magnetic Hydrogel for Cartilage Tissue Regeneration as well as a Review on Advantages and Disadvantages of Different Cartilage Repair Strategies. BioMed Research International. 2022; 2022: 7230354. https://doi.org/10.1155/2022/7230354
  62. Bettaie F., Khiari R., Dufresne A., et al. Mechanical and thermal properties of Posidoniaoceanica cellulose nanocrystal reinforced polymer. Carbohydrate Polymers. 2015; 123: 99–104. https://doi.org/10.1016/j.carbpol.2015.01.026
  63. Shi Y., Li Y., Coradin T. Magnetically-oriented type I collagen-SiO2@Fe3O4 rods composite hydrogels tuning skin cell growth. Colloids and Surfaces B: Biointerfaces. 2020; 185: 110597. https://doi.org/10.1016/j.colsurfb.2019.110597



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