Electrical stimulation in bone tissue engineering treatments

1.

Oryan A, Alidadi S, Moshiri A, et al. Bone regenerative medicine: classic options, novel strategies, and future directions. J Orthop Surg Res. 2014;9(1):18. https://doi.org/10.1186/1749-799X-9-18.CrossRefPubMedPubMedCentral

2.

Kargozar S, Mozafari M, Hamzehlou S, et al. Bone tissue engineering using human cells: a comprehensive review on recent trends, current prospects, and recommendations. Appl Sci. 2019;9(1):174. https://doi.org/10.3390/app9010174.CrossRef

3.

Murphy CM, O'Brien FJ, Little DG, et al. Cell-scaffold interactions in the bone tissue engineering triad. Eur Cell Mater. 2013;26:120–32.CrossRefPubMed

4.

Seebach C, Henrich D, Meier S, et al. Safety and feasibility of cell-based therapy of autologous bone marrow-derived mononuclear cells in plate-stabilized proximal humeral fractures in humans. J Transl Med. 2016;14(1):314. https://doi.org/10.1186/s12967-016-1066-7.CrossRefPubMedPubMedCentral

5.

Verboket R, Leiblein M, Seebach C, et al. Autologous cell-based therapy for treatment of large bone defects: from bench to bedside. Eur J Trauma Emerg Surg. 2018;44(5):649–65. https://doi.org/10.1007/s00068-018-0906-y.CrossRefPubMedPubMedCentral

6.

Bhavsar MB, Han Z, DeCoster T, et al. Electrical stimulation-based bone fracture treatment, if it works so well why do not more surgeons use it? Eur J Trauma Emerg Surg. 2019. https://doi.org/10.1007/s00068-019-01127-z.CrossRefPubMed

7.

Tai G, Tai M, Zhao M. Electrically stimulated cell migration and its contribution to wound healing. Burns Trauma. 2018;6:20. https://doi.org/10.1186/s41038-018-0123-2.CrossRefPubMedPubMedCentral

8.

Yuan X, Arkonac DE, Chao P-HG, et al. Electrical stimulation enhances cell migration and integrative repair in the meniscus. Sci Rep. 2014;4:3674. https://doi.org/10.1038/srep03674.CrossRefPubMedPubMedCentral

9.

Ercan B, Webster TJ. Greater osteoblast proliferation on anodized nanotubular titanium upon electrical stimulation. Int J Nanomed. 2008;3(4):477–85.

10.

Eischen-Loges M, Oliveira KMC, Bhavsar MB, et al. Pretreating mesenchymal stem cells with electrical stimulation causes sustained long-lasting pro-osteogenic effects. PeerJ. 2018;6:e4959. https://doi.org/10.7717/peerj.4959.CrossRefPubMedPubMedCentral

11.

Mobini S, Leppik L, Thottakkattumana Parameswaran V, et al. In vitro effect of direct current electrical stimulation on rat mesenchymal stem cells. PeerJ. 2017;5:e2821. https://doi.org/10.7717/peerj.2821.CrossRefPubMedPubMedCentral

12.

Jayanand, Behari J. Effect of electrical stimulation in mineralization and collagen enrichment of osteoporotic rat bones. In: 2008 International conference on recent advances in microwave theory and applications. Jaipur; 2008. pp. 568–571. https://doi.org/10.1109/AMTA.2008.4763231.

13.

Durigan JLQ, Peviani SM, Delfino GB, et al. Neuromuscular electrical stimulation induces beneficial adaptations in the extracellular matrix of quadriceps muscle after anterior cruciate ligament transection of rats. Am J Phys Med Rehabil. 2014;93(11):948–61. https://doi.org/10.1097/PHM.0000000000000110.CrossRefPubMed

14.

George PM, Bliss TM, Hua T, et al. Electrical preconditioning of stem cells with a conductive polymer scaffold enhances stroke recovery. Biomaterials. 2017;142:31–40. https://doi.org/10.1016/j.biomaterials.2017.07.020.CrossRefPubMedPubMedCentral

15.

Tsai M-T, Li W-J, Tuan RS, et al. Modulation of osteogenesis in human mesenchymal stem cells by specific pulsed electromagnetic field stimulation. J Orthop Res. 2009;27(9):1169–74. https://doi.org/10.1002/jor.20862.CrossRefPubMedPubMedCentral

16.

Griffin M, Iqbal SA, Sebastian A, et al. Degenerate wave and capacitive coupling increase human MSC invasion and proliferation while reducing cytotoxicity in an in vitro wound healing model. PLoS ONE. 2011;6(8):e23404. https://doi.org/10.1371/journal.pone.0023404.CrossRefPubMedPubMedCentral

17.

Zhao Z, Watt C, Karystinou A, et al. Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. eCM. 2011;22:344–58. https://doi.org/10.22203/eCM.v022a26.CrossRefPubMed

18.

Hwang SJ, Song YM, Cho TH, et al. The implications of the response of human mesenchymal stromal cells in three-dimensional culture to electrical stimulation for tissue regeneration. Tissue Eng Part A. 2012;18(3–4):432–45. https://doi.org/10.1089/ten.tea.2010.0752.CrossRefPubMed

19.

Hu W-W, Hsu Y-T, Cheng Y-C, et al. Electrical stimulation to promote osteogenesis using conductive polypyrrole films. Mater Sci Eng C Mater Biol Appl. 2014;37:28–36. https://doi.org/10.1016/j.msec.2013.12.019.CrossRefPubMed

20.

Ongaro A, Pellati A, Bagheri L, et al. Pulsed electromagnetic fields stimulate osteogenic differentiation in human bone marrow and adipose tissue derived mesenchymal stem cells. Bioelectromagnetics. 2014;35(6):426–36. https://doi.org/10.1002/bem.21862.CrossRefPubMed

21.

Thrivikraman G, Lee PS, Hess R, et al. Interplay of substrate conductivity, cellular microenvironment, and pulsatile electrical stimulation toward osteogenesis of human mesenchymal stem cells in vitro. ACS Appl Mater Interfaces. 2015;7(41):23015–28. https://doi.org/10.1021/acsami.5b06390.CrossRefPubMed

22.

Wang X, Gao Y, Shi H, et al. Influence of the intensity and loading time of direct current electric field on the directional migration of rat bone marrow mesenchymal stem cells. Front Med. 2016;10(3):286–96. https://doi.org/10.1007/s11684-016-0456-9.CrossRefPubMed

23.

Kwon HJ, Lee GS, Chun H. Electrical stimulation drives chondrogenesis of mesenchymal stem cells in the absence of exogenous growth factors. Sci Rep. 2016;6:39302. https://doi.org/10.1038/srep39302.CrossRefPubMedPubMedCentral

24.

Damaraju SM, Shen Y, Elele E, et al. Three-dimensional piezoelectric fibrous scaffolds selectively promote mesenchymal stem cell differentiation. Biomaterials. 2017;149:51–62. https://doi.org/10.1016/J.BIOMATERIALS.2017.09.024.CrossRefPubMed

25.

Jezierska-Woźniak K, Lipiński S, Huflejt M, et al. Migration of human mesenchymal stem cells stimulated with pulsed electric field and the dynamics of the cell surface glycosylation. Adv Clin Exp Med. 2018;27(9):1181–93. https://doi.org/10.17219/acem/90872.CrossRefPubMed

26.

Hernández-Bule ML, Paíno CL, Trillo MÁ, et al. Electric stimulation at 448 kHz promotes proliferation of human mesenchymal stem cells. Cell Physiol Biochem. 2014;34(5):1741–55. https://doi.org/10.1159/000366375.CrossRefPubMed

27.

Kang KS, Hong JM, Seol Y-J, et al. Short-term evaluation of electromagnetic field pretreatment of adipose-derived stem cells to improve bone healing. J Tissue Eng Regen Med. 2015;9(10):1161–71. https://doi.org/10.1002/term.1664.CrossRefPubMed

28.

Zhang J, Li M, Kang E-T, et al. Electrical stimulation of adipose-derived mesenchymal stem cells in conductive scaffolds and the roles of voltage-gated ion channels. Acta Biomater. 2016;32:46–56. https://doi.org/10.1016/j.actbio.2015.12.024.CrossRefPubMed

29.

Leppik L, Zhihua H, Mobini S, et al. Combining electrical stimulation and tissue engineering to treat large bone defects in a rat model. Sci Rep. 2018;8(1):6307. https://doi.org/10.1038/s41598-018-24892-0.CrossRefPubMedPubMedCentral

30.

Tandon N, Goh B, Marsano A, et al. Alignment and elongation of human adipose-derived stem cells in response to direct-current electrical stimulation. Conf Proc IEEE Eng Med Biol Soc. 2009;2009:6517–21. https://doi.org/10.1109/IEMBS.2009.5333142.CrossRef

31.

Diniz P, Shomura K, Soejima K, et al. Effects of pulsed electromagnetic field (PEMF) stimulation on bone tissue like formation are dependent on the maturation stages of the osteoblasts. Bioelectromagnetics. 2002;23(5):398–405. https://doi.org/10.1002/bem.10032.CrossRefPubMed

32.

Liu L, Li P, Zhou G, et al. Increased proliferation and differentiation of pre-osteoblasts MC3T3-E1 cells on nanostructured polypyrrole membrane under combined electrical and mechanical stimulation. J Biomed Nanotechnol. 2013;9(9):1532–9.CrossRefPubMed

33.

Liu Z, Dong L, Wang L, et al. Mediation of cellular osteogenic differentiation through daily stimulation time based on polypyrrole planar electrodes. Sci Rep. 2017;7(1):17926. https://doi.org/10.1038/s41598-017-17120-8.CrossRefPubMedPubMedCentral

34.

Cheng Y, Chen C, Kuo H, et al. Electrical stimulation through conductive substrate to enhance osteo-differentiation of human dental pulp-derived stem cells. Appl Sci. 2019;9(18):3938. https://doi.org/10.3390/app9183938.CrossRef

35.

Debnath T, Chelluri LK. Standardization and quality assessment for clinical grade mesenchymal stem cells from human adipose tissue. Hematol Transfus Cell Ther. 2019;41(1):7–16. https://doi.org/10.1016/j.htct.2018.05.001.CrossRefPubMed

36.

Love MR, Palee S, Chattipakorn SC, et al. Effects of electrical stimulation on cell proliferation and apoptosis. J Cell Physiol. 2018;233(3):1860–76. https://doi.org/10.1002/jcp.25975.CrossRefPubMed

37.

Mobini S, Leppik L, Barker JH. Direct current electrical stimulation chamber for treating cells in vitro. Biotechniques. 2016;60(2):95–8. https://doi.org/10.2144/000114382.CrossRefPubMed

38.

Kumar A, Nune KC, Misra RDK. Electric field-mediated growth of osteoblasts—the significant impact of dynamic flow of medium. Biomater Sci. 2016;4(1):136–44. https://doi.org/10.1039/c5bm00350d.CrossRefPubMed

39.

Bodhak S, Bose S, Kinsel WC, et al. Investigation of in vitro bone cell adhesion and proliferation on Ti using direct current stimulation. Mater Sci Eng C Mater Biol Appl. 2012;32(8):2163–8. https://doi.org/10.1016/j.msec.2012.05.032.CrossRefPubMedPubMedCentral

40.

Shao S, Zhou S, Li L, et al. Osteoblast function on electrically conductive electrospun PLA/MWCNTs nanofibers. Biomaterials. 2011;32(11):2821–33. https://doi.org/10.1016/j.biomaterials.2011.01.051.CrossRefPubMed

41.

Wang Q, Zhong S, Ouyang J, et al. Osteogenesis of electrically stimulated bone cells mediated in part by calcium ions. Clin Orthop Relat Res. 1998;348:259–68.CrossRef

42.

Hipfner DR, Cohen SM. Connecting proliferation and apoptosis in development and disease. Nat Rev Mol Cell Biol. 2004;5(10):805–15. https://doi.org/10.1038/nrm1491.CrossRefPubMed

43.

Thrivikraman G, Mallik PK, Basu B. Substrate conductivity dependent modulation of cell proliferation and differentiation in vitro. Biomaterials. 2013;34(29):7073–85. https://doi.org/10.1016/j.biomaterials.2013.05.076.CrossRefPubMed

44.

Mobini S, Talts Ü-L, Xue R, et al. Electrical stimulation changes human mesenchymal stem cells orientation and cytoskeleton organization. J Biomater Tissue Eng. 2017;7(9):829–33. https://doi.org/10.1166/jbt.2017.1631.CrossRef

45.

Zhu S, Jing W, Hu X, et al. Time-dependent effect of electrical stimulation on osteogenic differentiation of bone mesenchymal stromal cells cultured on conductive nanofibers. J Biomed Mater Res A. 2017;105(12):3369–83. https://doi.org/10.1002/jbm.a.36181.CrossRefPubMed

46.

Li Y, Huang G, Zhang X, et al. Engineering cell alignment in vitro. Biotechnol Adv. 2014;32(2):347–65. https://doi.org/10.1016/j.biotechadv.2013.11.007.CrossRefPubMed

47.

Curtze S, Dembo M, Miron M, et al. Dynamic changes in traction forces with DC electric field in osteoblast-like cells. J Cell Sci. 2004;117(Pt 13):2721–9. https://doi.org/10.1242/jcs.01119.CrossRefPubMed

48.

Yang G, Long H, Ren X, et al. Regulation of adipose-tissue-derived stromal cell orientation and motility in 2D- and 3D-cultures by direct-current electrical field. Dev Growth Differ. 2017;59(2):70–82. https://doi.org/10.1111/dgd.12340.CrossRefPubMed

49.

Zhao M, Forrester JV, McCaig CD. A small, physiological electric field orients cell division. Proc Natl Acad Sci USA. 1999;96(9):4942–6. https://doi.org/10.1073/pnas.96.9.4942.CrossRefPubMedPubMedCentral

50.

Cunha F, Rajnicek AM, McCaig CD. Electrical stimulation directs migration, enhances and orients cell division and upregulates the chemokine receptors CXCR4 and CXCR2 in endothelial cells. J Vasc Res. 2019;56(1):39–533. https://doi.org/10.1159/000495311.CrossRefPubMed

51.

Wang E-t, Zhao M. Regulation of tissue repair and regeneration by electric fields. Chin J Traumatol. 2010;13(1):55–61.PubMed

52.

Cortese B, Palamà IE, D'Amone S, et al. Influence of electrotaxis on cell behaviour. Integr Biol (Camb). 2014;6(9):817–30. https://doi.org/10.1039/C4IB00142G.CrossRef

53.

Ozkucur N, Perike S, Sharma P, et al. Persistent directional cell migration requires ion transport proteins as direction sensors and membrane potential differences in order to maintain directedness. BMC Cell Biol. 2011;12:4. https://doi.org/10.1186/1471-2121-12-4.CrossRefPubMedPubMedCentral

54.

Funk RHW. Endogenous electric fields as guiding cue for cell migration. Front Physiol. 2015;6:143. https://doi.org/10.3389/fphys.2015.00143.CrossRefPubMedPubMedCentral

55.

El-Badawy A, Amer M, Abdelbaset R, et al. Adipose stem cells display higher regenerative capacities and more adaptable electro-kinetic properties compared to bone marrow-derived mesenchymal stromal cells. Sci Rep. 2016;6:37801. https://doi.org/10.1038/srep37801.CrossRefPubMedPubMedCentral

56.

Zhao Z, Watt C, Karystinou A, et al. Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. Eur Cell Mater. 2011;22:344–58.CrossRefPubMed

57.

Boyan BD, Lossdörfer S, Wang L, et al. Osteoblasts generate an osteogenic microenvironment when grown on surfaces with rough microtopographies. eCM. 2003;6:22–7. https://doi.org/10.22203/eCM.v006a03.CrossRefPubMed

58.

Placzek MR, Chung I-M, Macedo HM, et al. Stem cell bioprocessing: fundamentals and principles. J R Soc Interface. 2009;6(32):209–32. https://doi.org/10.1098/rsif.2008.0442.CrossRefPubMed

59.

Sun S, Titushkin I, Cho M. Regulation of mesenchymal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus. Bioelectrochemistry. 2006;69(2):133–41. https://doi.org/10.1016/j.bioelechem.2005.11.007.CrossRefPubMed

60.

Dubey AK, Gupta SD, Basu B. Optimization of electrical stimulation parameters for enhanced cell proliferation on biomaterial surfaces. J Biomed Mater Res Part B Appl Biomater. 2011;98(1):18–29. https://doi.org/10.1002/jbm.b.31827.CrossRef

61.

Zhang K, Wang S, Zhou C, et al. Advanced smart biomaterials and constructs for hard tissue engineering and regeneration. Bone Res. 2018;6(1):31. https://doi.org/10.1038/s41413-018-0032-9.CrossRefPubMedPubMedCentral

62.

Cho MR, Thatte HS, Silvia MT, et al. Transmembrane calcium influx induced by ac electric fields. FASEB J. 1999;13(6):677–83. https://doi.org/10.1096/fasebj.13.6.677.CrossRefPubMed

63.

Sun Y, Liu W-Z, Liu T, et al. Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis. J Recept Signal Transduct Res. 2015;35(6):600–4. https://doi.org/10.3109/10799893.2015.1030412.CrossRefPubMed

64.

Shaul YD, Seger R. The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim Biophys Acta. 2007;1773(8):1213–26. https://doi.org/10.1016/j.bbamcr.2006.10.005.CrossRefPubMed

65.

Rubinfeld H, Seger R. The ERK cascade as a prototype of MAPK signaling pathways. Methods Mol Biol. 2004;250:1–28. https://doi.org/10.1385/1-59259-671-1:1.CrossRefPubMed

66.

Zhao M, Pu J, Forrester JV, et al. Membrane lipids, EGF receptors, and intracellular signals colocalize and are polarized in epithelial cells moving directionally in a physiological electric field. FASEB J. 2002;16(8):857–9. https://doi.org/10.1096/fj.01-0811fje.CrossRefPubMed

67.

Zhao M, Song B, Pu J, et al. Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature. 2006;442(7101):457–60. https://doi.org/10.1038/nature04925.CrossRefPubMed

68.

Nakano T, Moore MJ, Wei F, et al. Molecular communication and networking: opportunities and challenges. IEEE Trans Nanobiosci. 2012;11(2):135–48. https://doi.org/10.1109/TNB.2012.2191570.CrossRef

69.

Perez-Zoghbi JF, Karner C, Ito S, et al. Ion channel regulation of intracellular calcium and airway smooth muscle function. Pulm Pharmacol Ther. 2009;22(5):388–97. https://doi.org/10.1016/j.pupt.2008.09.006.CrossRefPubMed

70.

Dolmetsch RE, Xu K, Lewis RS. Calcium oscillations increase the efficiency and specificity of gene expression. Nature. 1998;392(6679):933–6. https://doi.org/10.1038/31960.CrossRefPubMed

71.

Fields RD, Eshete F, Stevens B, et al. Action potential-dependent regulation of gene expression: temporal specificity in ca2+, cAMP-responsive element binding proteins, and mitogen-activated protein kinase signaling. J Neurosci. 1997;17(19):7252–66.CrossRefPubMedPubMedCentral

72.

Sun S, Liu Y, Lipsky S, et al. Physical manipulation of calcium oscillations facilitates osteodifferentiation of human mesenchymal stem cells. FASEB J. 2007;21(7):1472–80. https://doi.org/10.1096/fj.06-7153com.CrossRefPubMed

73.

van Westering TLE, Betts CA, Wood MJA. Current understanding of molecular pathology and treatment of cardiomyopathy in duchenne muscular dystrophy. Molecules. 2015;20(5):8823–55. https://doi.org/10.3390/molecules20058823.CrossRefPubMedPubMedCentral

74.

Pall ML. Electromagnetic fields act via activation of voltage-gated calcium channels to produce beneficial or adverse effects. J Cell Mol Med. 2013;17(8):958–65. https://doi.org/10.1111/jcmm.12088.CrossRefPubMedPubMedCentral

75.

Martinac B. Mechanosensitive ion channels: molecules of mechanotransduction. J Cell Sci. 2004;117(Pt 12):2449–600. https://doi.org/10.1242/jcs.01232.CrossRefPubMed

76.

Titushkin I, Cho M. Regulation of cell cytoskeleton and membrane mechanics by electric field: role of linker proteins. Biophys J. 2009;96(2):717–28. https://doi.org/10.1016/j.bpj.2008.09.035.CrossRefPubMedPubMedCentral

77.

Onuma EK, Hui SW. Electric field-directed cell shape changes, displacement, and cytoskeletal reorganization are calcium dependent. J Cell Biol. 1988;106(6):2067–75. https://doi.org/10.1083/jcb.106.6.2067.CrossRefPubMed

78.

Wolf-Goldberg T, Barbul A, Ben-Dov N, et al. (2013) Low electric fields induce ligand-independent activation of EGF receptor and ERK via electrochemical elevation of H(+) and ROS concentrations. Biochim Biophys Acta. 1833;6:1396–408. https://doi.org/10.1016/j.bbamcr.2013.02.011.CrossRef

79.

Zhao M, Dick A, Forrester JV, et al. Electric field-directed cell motility involves up-regulated expression and asymmetric redistribution of the epidermal growth factor receptors and is enhanced by fibronectin and laminin. Mol Biol Cell. 1999;10(4):1259–76. https://doi.org/10.1091/mbc.10.4.1259.CrossRefPubMedPubMedCentral

80.

Cheng N, van Hoof H, Bockx E, et al. The effects of electric currents on ATP generation, protein synthesis, and membrane transport of rat skin. Clin Orthop Relat Res. 1982;171:264–72.

81.

Titushkin I, Cho M. Modulation of cellular mechanics during osteogenic differentiation of human mesenchymal stem cells. Biophys J. 2007;93(10):3693–702. https://doi.org/10.1529/biophysj.107.107797.CrossRefPubMedPubMedCentral

82.

Atkinson SJ, Hosford MA, Molitoris BA. Mechanism of actin polymerization in cellular ATP depletion. J Biol Chem. 2004;279(7):5194–9. https://doi.org/10.1074/jbc.M306973200.CrossRefPubMed

83.

Delle Monache S, Angelucci A, Sanità P, et al. Inhibition of angiogenesis mediated by extremely low-frequency magnetic fields (ELF-MFs). PLoS ONE. 2013;8(11):e79309. https://doi.org/10.1371/journal.pone.0079309.CrossRefPubMedPubMedCentral

84.

Esfandiari E, Roshankhah S, Mardani M, et al. The effect of high frequency electric field on enhancement of chondrogenesis in human adipose-derived stem cells. Iran J Basic Med Sci. 2014;17(8):571–6.PubMedPubMedCentral

85.

Díaz-Vegas A, Campos CA, Contreras-Ferrat A, et al. ROS production via P2Y1-PKC-NOX2 is triggered by extracellular ATP after electrical stimulation of skeletal muscle cells. PLoS ONE. 2015;10(6):e0129882. https://doi.org/10.1371/journal.pone.0129882.CrossRefPubMedPubMedCentral

86.

Schmelter M, Ateghang B, Helmig S, et al. Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J. 2006;20(8):1182–4. https://doi.org/10.1096/fj.05-4723fje.CrossRefPubMed

87.

Sart S, Song L, Li Y. Controlling redox status for stem cell survival, expansion, and differentiation. Oxid Med Cell Longev. 2015;2015:105135. https://doi.org/10.1155/2015/105135.CrossRefPubMedPubMedCentral

88.

Liu H, Zhang H, Iles KE, et al. The ADP-stimulated NADPH oxidase activates the ASK-1/MKK4/JNK pathway in alveolar macrophages. Free Radic Res. 2006;40(8):865–74. https://doi.org/10.1080/10715760600758514.CrossRefPubMedPubMedCentral

89.

Srirussamee K, Mobini S, Cassidy NJ, et al. Direct electrical stimulation enhances osteogenesis by inducing Bmp2 and Spp1 expressions from macrophages and preosteoblasts. Biotechnol Bioeng. 2019. https://doi.org/10.1002/bit.27142.CrossRefPubMedPubMedCentral

90.

Lozano MM, Hovis JS, Moss FR, et al. Dynamic reorganization and correlation among lipid raft components. J Am Chem Soc. 2016;138(31):9996–10001. https://doi.org/10.1021/jacs.6b05540.CrossRefPubMedPubMedCentral

91.

Lin B-J, Tsao S-H, Chen A, et al. Lipid rafts sense and direct electric field-induced migration. Proc Natl Acad Sci USA. 2017;114(32):8568–73. https://doi.org/10.1073/pnas.1702526114.CrossRefPubMedPubMedCentral

92.

Marsell R, Einhorn TA. The biology of fracture healing. Injury. 2011;42(6):551–5. https://doi.org/10.1016/j.injury.2011.03.031.CrossRefPubMedPubMedCentral

93.

Aleem IS, Aleem I, Evaniew N, et al. Efficacy of electrical stimulators for bone healing: a meta-analysis of randomized sham-controlled trials. Sci Rep. 2016;6(1):31724. https://doi.org/10.1038/srep31724.CrossRefPubMedPubMedCentral

94.

Wang K, Parekh U, Ting JK, et al. A platform to study the effects of electrical stimulation on immune cell activation during wound healing. Adv Biosys. 2019;3(10):1900106. https://doi.org/10.1002/adbi.201900106.CrossRef

95.

Hu DP, Ferro F, Yang F, et al. Cartilage to bone transformation during fracture healing is coordinated by the invading vasculature and induction of the core pluripotency genes. Development. 2017;144(2):221–34. https://doi.org/10.1242/dev.130807.CrossRefPubMedPubMedCentral

96.

Leppik LP, Froemel D, Slavici A, et al. Effects of electrical stimulation on rat limb regeneration, a new look at an old model. Sci Rep. 2015;5:18353. https://doi.org/10.1038/srep18353.CrossRefPubMedPubMedCentral

97.

Oliveira KMC, Barker JH, Berezikov E, et al. Electrical stimulation shifts healing/scarring towards regeneration in a rat limb amputation model. Sci Rep. 2019;9(1):11433. https://doi.org/10.1038/s41598-019-47389-w.CrossRefPubMedPubMedCentral

98.

Uzieliene I, Bernotas P, Mobasheri A, et al. The role of physical stimuli on calcium channels in chondrogenic differentiation of mesenchymal stem cells. Int J Mol Sci. 2018. https://doi.org/10.3390/ijms19102998.CrossRefPubMedPubMedCentral

99.

Ning T, Zhang K, Heng BC, et al. Diverse effects of pulsed electrical stimulation on cells—with a focus on chondrocytes and cartilage regeneration. Eur Cell Mater. 2019;38:79–93. https://doi.org/10.22203/eCM.v038a07.CrossRefPubMed

100.

Mardani M, Roshankhah S, Hashemibeni B, et al. Induction of chondrogenic differentiation of human adipose-derived stem cells by low frequency electric field. Adv Biomed Res. 2016;5:97. https://doi.org/10.4103/2277-9175.183146.CrossRefPubMedPubMedCentral

101.

Hernandez Bule ML, Angeles Trillo M, Martinez Garcia MA, et al. Chondrogenic differentiation of adipose-derived stem cells by radiofrequency electric stimulation. J Stem Cell Res Ther. 2017. https://doi.org/10.4172/2157-7633.1000407.CrossRef

102.

Ning T, Guo J, Zhang K, et al. Nanosecond pulsed electric fields enhanced chondrogenic potential of mesenchymal stem cells via JNK/CREB-STAT3 signaling pathway. Stem Cell Res Ther. 2019;10(1):45. https://doi.org/10.1186/s13287-019-1133-0.CrossRefPubMedPubMedCentral

103.

Mercado-Pagán ÁE, Stahl AM, Shanjani Y, et al. Vascularization in bone tissue engineering constructs. Ann Biomed Eng. 2015;43(3):718–29. https://doi.org/10.1007/s10439-015-1253-3.CrossRefPubMedPubMedCentral

104.

Kim S, von Recum H. Endothelial stem cells and precursors for tissue engineering: cell source, differentiation, selection, and application. Tissue Eng Part B Rev. 2008;14(1):133–47. https://doi.org/10.1089/teb.2007.0304.CrossRefPubMed

105.

Sheikh I, Tchekanov G, Krum D, et al. Effect of electrical stimulation on arteriogenesis and angiogenesis after bilateral femoral artery excision in the rabbit hind-limb ischemia model. Vasc Endovasc Surg. 2005;39(3):257–65. https://doi.org/10.1177/153857440503900307.CrossRef

106.

Sebastian A, Syed F, Perry D, et al. Acceleration of cutaneous healing by electrical stimulation: degenerate electrical waveform down-regulates inflammation, up-regulates angiogenesis and advances remodeling in temporal punch biopsies in a human volunteer study. Wound Repair Regen. 2011;19(6):693–708. https://doi.org/10.1111/j.1524-475X.2011.00736.x.CrossRefPubMed

107.

Ud-Din S, Sebastian A, Giddings P, et al. Angiogenesis is induced and wound size is reduced by electrical stimulation in an acute wound healing model in human skin. PLoS ONE. 2015;10(4):e0124502. https://doi.org/10.1371/journal.pone.0124502.CrossRefPubMedPubMedCentral

108.

Chen Y, Ye L, Guan L, et al. Physiological electric field works via the VEGF receptor to stimulate neovessel formation of vascular endothelial cells in a 3D environment. Biol Open. 2018. https://doi.org/10.1242/bio.035204.CrossRefPubMedPubMedCentral

109.

Zhao M. Electrical stimulation and angiogenesis. In: Janigro D, editor. The cell cycle in the central nervous system, vol. 1. NJ: Humana Press; 2006. p. 495–509.CrossRef

110.

Bai H, Forrester JV, Zhao M. DC electric stimulation upregulates angiogenic factors in endothelial cells through activation of VEGF receptors. Cytokine. 2011;55(1):110–5. https://doi.org/10.1016/j.cyto.2011.03.003.CrossRefPubMedPubMedCentral

111.

Bai H, McCaig CD, Forrester JV, et al. DC electric fields induce distinct preangiogenic responses in microvascular and macrovascular cells. Arterioscler Thromb Vasc Biol. 2004;24(7):1234–9. https://doi.org/10.1161/01.ATV.0000131265.76828.8a.CrossRefPubMed

112.

Mountziaris PM, Mikos AG. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng Part B Rev. 2008;14(2):179–86. https://doi.org/10.1089/ten.teb.2008.0038.CrossRefPubMedPubMedCentral

113.

Wendler S, Schlundt C, Bucher CH, et al. Immune modulation to enhance bone healing-a new concept to induce bone using prostacyclin to locally modulate immunity. Front Immunol. 2019;10:713. https://doi.org/10.3389/fimmu.2019.00713.CrossRefPubMedPubMedCentral

114.

Chung L, Maestas DR, Housseau F, et al. Key players in the immune response to biomaterial scaffolds for regenerative medicine. Adv Drug Deliv Rev. 2017;114:184–92. https://doi.org/10.1016/j.addr.2017.07.006.CrossRefPubMed

115.

Kearns KR, Thompson DM. Macrophage response to electrical stimulation. 2015 41st Annual Northeast Biomedical Engineering Conference (NEBEC). Troy, NY; 2015. pp. 1–2. https://doi.org/10.1109/NEBEC.2015.7117101(NEBEC).

116.

Hoare JI, Rajnicek AM, McCaig CD, et al. Electric fields are novel determinants of human macrophage functions. J Leukoc Biol. 2016;99(6):1141–51. https://doi.org/10.1189/jlb.3A0815-390R.CrossRefPubMed

117.

Balint R, Cassidy NJ, Cartmell SH. Electrical stimulation: a novel tool for tissue engineering. Tissue Eng Part B Rev. 2013;19(1):48–57. https://doi.org/10.1089/ten.TEB.2012.0183.CrossRefPubMed

118.

Hughes MS, Anglen JO. The use of implantable bone stimulators in nonunion treatment. Orthopedics. 2010. https://doi.org/10.3928/01477447-20100129-15.CrossRefPubMed

119.

Haglin JM, Jain S, Eltorai AEM, et al. Bone growth stimulation: a critical analysis review. JBJS Rev. 2017;5(8):e8. https://doi.org/10.2106/JBJS.RVW.16.00117.CrossRefPubMed

120.

Visone R, Talò G, Lopa S, et al. Enhancing all-in-one bioreactors by combining interstitial perfusion, electrical stimulation, on-line monitoring and testing within a single chamber for cardiac constructs. Sci Rep. 2018;8(1):16944. https://doi.org/10.1038/s41598-018-35019-w.CrossRefPubMedPubMedCentral

121.

Wang Y, Cui H, Wu Z, et al. Modulation of osteogenesis in MC3T3-E1 cells by different frequency electrical stimulation. PLoS ONE. 2016;11(5):e0154924. https://doi.org/10.1371/journal.pone.0154924.CrossRefPubMedPubMedCentral

122.

Leppik L, Bhavsar MB, Oliveira KMC, et al. Construction and use of an electrical stimulation chamber for enhancing osteogenic differentiation in mesenchymal stem/stromal cells in vitro. J Vis Exp. 2019. https://doi.org/10.3791/59127.CrossRefPubMed

123.

Xiong GM, Do AT, Wang JK, et al. Development of a miniaturized stimulation device for electrical stimulation of cells. J Biol Eng. 2015;9:14. https://doi.org/10.1186/s13036-015-0012-1.CrossRefPubMedPubMedCentral

124.

Jennings J, Chen D, Feldman D. Transcriptional response of dermal fibroblasts in direct current electric fields. Bioelectromagnetics. 2008;29(5):394–405. https://doi.org/10.1002/bem.20408.CrossRefPubMed

125.

Cogan SF. Neural stimulation and recording electrodes. Annu Rev Biomed Eng. 2008;10:275–309. https://doi.org/10.1146/annurev.bioeng.10.061807.160518.CrossRefPubMed

126.

Kim HB, Ahn S, Jang HJ, et al. Evaluation of corrosion behaviors and surface profiles of platinum-coated electrodes by electrochemistry and complementary microscopy: biomedical implications for anticancer therapy. Micron. 2007;38(7):747–53. https://doi.org/10.1016/j.micron.2007.04.003.CrossRefPubMed

127.

Song B, Gu Y, Pu J, et al. Application of direct current electric fields to cells and tissues in vitro and modulation of wound electric field in vivo. Nat Protoc. 2007;2(6):1479–89. https://doi.org/10.1038/nprot.2007.205.CrossRefPubMed

128.

Hronik-Tupaj M, Kaplan DL. A review of the responses of two- and three-dimensional engineered tissues to electric fields. Tissue Eng Part B Rev. 2012;18(3):167–80. https://doi.org/10.1089/ten.TEB.2011.0244.CrossRefPubMedPubMedCentral

129.

Huang C-W, Cheng J-Y, Yen M-H, et al. Electrotaxis of lung cancer cells in a multiple-electric-field chip. Biosens Bioelectron. 2009;24(12):3510–6. https://doi.org/10.1016/j.bios.2009.05.001.CrossRefPubMed

130.

Tsai C-H, Lin B-J, Chao P-HG. α2β1 integrin and RhoA mediates electric field-induced ligament fibroblast migration directionality. J Orthop Res. 2013;31(2):322–7. https://doi.org/10.1002/jor.22215.CrossRefPubMed

131.

Tsai H-F, Huang C-W, Chang H-F, et al. Evaluation of EGFR and RTK signaling in the electrotaxis of lung adenocarcinoma cells under direct-current electric field stimulation. PLoS ONE. 2013;8(8):e73418. https://doi.org/10.1371/journal.pone.0073418.CrossRefPubMedPubMedCentral

132.

Tsai H-F, Cheng J-Y, Chang H-F, et al. Uniform electric field generation in circular multi-well culture plates using polymeric inserts. Sci Rep. 2016;6:26222. https://doi.org/10.1038/srep26222.CrossRefPubMedPubMedCentral

133.

Ni L, Kc P, Mulvany E, et al. A microfluidic device for noninvasive cell electrical stimulation and extracellular field potential analysis. Biomed Microdevices. 2019;21(1):20. https://doi.org/10.1007/s10544-019-0364-2.CrossRefPubMed

134.

Bancroft GN, Sikavitsas VI, van den Dolder J, et al. Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner. Proc Natl Acad Sci USA. 2002;99(20):12600–5. https://doi.org/10.1073/pnas.202296599.CrossRefPubMedPubMedCentral

135.

Grayson WL, Fröhlich M, Yeager K, et al. Engineering anatomically shaped human bone grafts. Proc Natl Acad Sci USA. 2010;107(8):3299–304. https://doi.org/10.1073/pnas.0905439106.CrossRefPubMed

136.

Kim JH, Lee TH, Song YM, et al. An implantable electrical bioreactor for enhancement of cell viability. Conf Proc IEEE Eng Med Biol Soc. 2011;2011:3601–4. https://doi.org/10.1109/IEMBS.2011.6090603.CrossRef

137.

Cochran GV. Experimental methods for stimulation of bone healing by means of electrical energy. Bull N Y Acad Med. 1972;48(7):899–911.PubMedPubMedCentral

138.

Cook JJ, Summers NJ, Cook EA. Healing in the new millennium: bone stimulators: an overview of where we've been and where we may be heading. Clin Podiatr Med Surg. 2015;32(1):45–59. https://doi.org/10.1016/j.cpm.2014.09.003.CrossRefPubMed

139.

Atalay B, Aybar B, Ergüven M, et al. The effects of pulsed electromagnetic field (PEMF) on osteoblast-like cells cultured on titanium and titanium-zirconium surfaces. J Craniofac Surg. 2013;24(6):2127–34. https://doi.org/10.1097/SCS.0b013e31829a7ebc.CrossRefPubMed

140.

Goldstein C, Sprague S, Petrisor BA. Electrical stimulation for fracture healing: current evidence. J Orthop Trauma. 2010;24(Suppl 1):S62–S6565. https://doi.org/10.1097/BOT.0b013e3181cdde1b.CrossRefPubMed

141.

Pickering SAW, Scammell BE. Electromagnetic fields for bone healing. Int J Low Extrem Wounds. 2002;1(3):152–60. https://doi.org/10.1177/153473460200100302.CrossRefPubMed

142.

Kuzyk PR, Schemitsch EH. The science of electrical stimulation therapy for fracture healing. Indian J Orthop. 2009;43(2):127–31. https://doi.org/10.4103/0019-5413.50846.CrossRefPubMedPubMedCentral

143.

Victoria G, Petrisor B, Drew B, et al. Bone stimulation for fracture healing: what's all the fuss? Indian J Orthop. 2009;43(2):117–20. https://doi.org/10.4103/0019-5413.50844.CrossRefPubMedPubMedCentral

144.

Ryan Martin J, Vestermark G, Mullis B, et al. A retrospective comparative analysis of the use of implantable bone stimulators in nonunions. J Surg Orthop Adv. 2017;26(3):128–33.CrossRefPubMed

145.

Holmes GB, Wydra F, Hellman M, et al. A unique treatment for talar osteonecrosis: placement of an internal bone stimulator: a case report. JBJS Case Connect. 2015;5(1):e4–e5. https://doi.org/10.2106/JBJS.CC.N.00092.CrossRefPubMed

146.

Bilgin HM, Çelik F, Gem M, et al. Effects of local vibration and pulsed electromagnetic field on bone fracture: a comparative study. Bioelectromagnetics. 2017;38(5):339–48. https://doi.org/10.1002/bem.22043.CrossRefPubMed

147.

Yao Q, Liu H, Lin X, et al. 3D interpenetrated graphene Foam/58S bioactive glass scaffolds for electrical-stimulation-assisted differentiation of rabbit mesenchymal stem cells to enhance bone regeneration. J Biomed Nanotechnol. 2019;15(3):602–11. https://doi.org/10.1166/jbn.2019.2703.CrossRefPubMed

148.

Wang W, Junior JRP, Nalesso PRL, et al. Engineered 3D printed poly(ɛ-caprolactone)/graphene scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2019;100:759–70. https://doi.org/10.1016/j.msec.2019.03.047.CrossRefPubMed

149.

Otter MW, McLeod KJ, Rubin CT. Effects of electromagnetic fields in experimental fracture repair. Clin Orthop Relat Res. 1998. https://doi.org/10.1097/00003086-199810001-00011.CrossRefPubMed

150.

Palza H, Zapata PA, Angulo-Pineda C. electroactive smart polymers for biomedical applications. Materials (Basel). 2019. https://doi.org/10.3390/ma12020277.CrossRef

151.

Allison S, Ahumada M, Andronic C, et al. Electroconductive nanoengineered biomimetic hybrid fibers for cardiac tissue engineering. J Mater Chem B. 2017;5(13):2402–6. https://doi.org/10.1039/c7tb00405b.CrossRefPubMed

152.

Li S, Lu D, Tang J, et al. Electrical stimulation activates fibroblasts through the elevation of intracellular free Ca2+: potential mechanism of pelvic electrical stimulation therapy. Biomed Res Int. 2019;2019:7387803. https://doi.org/10.1155/2019/7387803.CrossRefPubMedPubMedCentral

153.

Rahmani A, Nadri S, Kazemi HS, et al. Conductive electrospun scaffolds with electrical stimulation for neural differentiation of conjunctiva mesenchymal stem cells. Artif Organs. 2019;43(8):780–90. https://doi.org/10.1111/aor.13425.CrossRefPubMed

154.

Guo B, Glavas L, Albertsson A-C. Biodegradable and electrically conducting polymers for biomedical applications. Prog Polym Sci. 2013;38(9):1263–86. https://doi.org/10.1016/j.progpolymsci.2013.06.003.CrossRef

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Electrical stimulation in bone tissue engineering treatments

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