DOI QR코드

DOI QR Code

Two-dimensional material-based bionano platforms to control mesenchymal stem cell differentiation

  • Kang, Ee-Seul (School of Integrative Engineering, Chung-Ang University) ;
  • Kim, Da-Seul (School of Integrative Engineering, Chung-Ang University) ;
  • Suhito, Intan Rosalina (School of Integrative Engineering, Chung-Ang University) ;
  • Lee, Wanhee (School of Integrative Engineering, Chung-Ang University) ;
  • Song, Inbeom (School of Integrative Engineering, Chung-Ang University) ;
  • Kim, Tae-Hyung (School of Integrative Engineering, Chung-Ang University)
  • 투고 : 2017.12.28
  • 심사 : 2018.03.09
  • 발행 : 2018.06.01

초록

Background: In the past decade, stem cells, with their ability to differentiate into various types of cells, have been proven to be resourceful in regenerative medicine and tissue engineering. Despite the ability to repair damaged parts of organs and tissues, the use of stem cells still entails several limitations, such as low differentiation efficiency and difficulties in guiding differentiation. To address these limitations, nanotechnology approaches have been recently implemented in stem cell research. It has been discovered that stem cells, in combination with carbon-based functional materials, show enhanced regenerative performances in varying biophysical conditions. In particular, several studies have reported solutions to the conventional quandaries in biomedical engineering, using synergetic effects of nanohybrid materials, as well as further development of technologies to recover from diverse health conditions such as bone fracture and strokes. Main text: In this review, we discuss several prior studies regarding the application of various nanomaterials in controlling the behavior of stem cells. We focus on the potential of different types of nanomaterials, such as two-dimensional materials, gold nanoparticles, and three-dimensional nanohybrid composites, to control the differentiation of human mesenchymal stem cells (hMSCs). These materials have been found to affect stem cell functions via the adsorption of growth/differentiation factors on the surfaces of nanomaterials and the activation of signaling pathways that are mostly related to cell adhesion and differentiation (e.g., FAK, Smad, Erk, and Wnt). Conclusion: Controlling stem cell differentiation using biophysical factors, especially the use of nanohybrid materials to functionalize underlying substrates wherein the cells attach and grow, is a promising strategy to achieve cells of interest in a highly efficient manner. We hope that this review will facilitate the use of other types of newly discovered and/or synthesized nanomaterials (e.g., metal transition dichalcogenides, non-toxic quantum dots, and metal oxide frameworks) for stem cell-based regenerative therapies.

키워드

과제정보

연구 과제 주관 기관 : Korea Health Industry Development Institute (KHIDI), National Research Foundation of Korea (NRF)

참고문헌

  1. Kim YJ, Hwang SJ, Bae YC, Jung JS. MiR-21 regulates Adipogenic differentiation through the modulation of TGF-${\beta}$ signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells. 2009;27:3093-102.
  2. zur Nieden NI, Kempka G, Rancourt DE, Ahr HJ. Induction of chondro-, osteoand adipogenesis in embryonic stem cells by bone morphogenetic protein-2: effect of cofactors on differentiating lineages. BMC Dev Biol. 2005;5:1. https://doi.org/10.1186/1471-213X-5-1
  3. Derfoul A, Perkins GL, Hall DJ, Tuan RS. Glucocorticoids promote Chondrogenic differentiation of adult human mesenchymal stem cells by enhancing expression of cartilage extracellular matrix genes. Stem Cells. 2006;24:1487-95. https://doi.org/10.1634/stemcells.2005-0415
  4. Lee WC, Lim CHYX, Shi H, Tang LAL, Wang Y, Lim CT, Loh KP. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano. 2011;5:7334-41. https://doi.org/10.1021/nn202190c
  5. Christopherson GT, Song H, Mao H-Q. The influence of fiber diameter of electrospun substrates on neural stem cell differentiation and proliferation. Biomaterials. 2009;30:556-64. https://doi.org/10.1016/j.biomaterials.2008.10.004
  6. Discher DE, Mooney DJ, Zandstra PW. Growth factors, matrices, and forces combine and control stem cells. Science. 2009;324:1673. https://doi.org/10.1126/science.1171643
  7. Du J, Chen X, Liang X, Zhang G, Xu J, He L, Zhan Q, Feng X-Q, Chien S, Yang C. Integrin activation and internalization on soft ECM as a mechanism of induction of stem cell differentiation by ECM elasticity. Proc Natl Acad Sci. 2011;108:9466. https://doi.org/10.1073/pnas.1106467108
  8. Engler A, Sweeney H, Discher D, Schwarzbauer J. Extracellular matrix elasticity directs stem cell differentiation. J Musculoskelet Neuronal Interact. 2007;7:335.
  9. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677-89. https://doi.org/10.1016/j.cell.2006.06.044
  10. Mooney E, Dockery P, Greiser U, Murphy M, Barron V. Carbon nanotubes and mesenchymal stem cells: biocompatibility, proliferation and differentiation. Nano Lett. 2008;8:2137-43. https://doi.org/10.1021/nl073300o
  11. Nayak TR, Andersen H, Makam VS, Khaw C, Bae S, Xu X, Ee P-LR, Ahn J-H, Hong BH, Pastorin G, Ozyilmaz B. Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano. 2011;5:4670-8. https://doi.org/10.1021/nn200500h
  12. Allen MJ, Tung VC, Kaner RB. Honeycomb carbon: a review of graphene. Chem Rev. 2010;110:132-45. https://doi.org/10.1021/cr900070d
  13. Geim AK, Novoselov KS. The rise of graphene. Nat Mater. 2007;6:183. https://doi.org/10.1038/nmat1849
  14. Chang Y, Yang S-T, Liu J-H, Dong E, Wang Y, Cao A, Liu Y, Wang H. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett. 2011;200:201-10. https://doi.org/10.1016/j.toxlet.2010.11.016
  15. Jeon J, Lee MS, Yang HS. Differentiated osteoblasts derived decellularized extracellular matrix to promote osteogenic differentiation. Biomater Res. 2018;22:4. https://doi.org/10.1186/s40824-018-0115-0
  16. Wang Y, Lee WC, Manga KK, Ang PK, Lu J, Liu YP, Lim CT, Loh KP. Fluorinated graphene for promoting neuro-induction of stem cells. Adv Mater. 2012;24: 4285-90. https://doi.org/10.1002/adma.201200846
  17. Akhavan O, Ghaderi E. Differentiation of human neural stem cells into neural networks on graphene nanogrids. J Mat Chem B. 2013;1:6291. https://doi.org/10.1039/c3tb21085e
  18. Akhavan O, Ghaderi E, Shahsavar M. Graphene nanogrids for selective and fast osteogenic differentiation of human mesenchymal stem cells. Carbon. 2013;59:200-11. https://doi.org/10.1016/j.carbon.2013.03.010
  19. Kim J, Kim HD, Park J, Lee ES, Kim E, Lee SS, Yang JK, Lee YS, Hwang NS. Enhanced osteogenic commitment of murine mesenchymal stem cells on graphene oxide substrate. Biomater Res. 2018;22:1. https://doi.org/10.1186/s40824-017-0112-8
  20. Kim T-H, Shah S, Yang L, Yin PT, Hossain MK, Conley B, Choi J-W, Lee K-B. Controlling differentiation of adipose-derived stem cells using combinatorial graphene hybrid-pattern arrays. ACS Nano. 2015;9:3780-90. https://doi.org/10.1021/nn5066028
  21. Shah S, Yin PT, Uehara TM, Chueng S-TD, Yang L, Lee K-B. Guiding stem cell differentiation into oligodendrocytes using graphene-nanofiber hybrid scaffolds. Adv Mater. 2014;26:3673-80. https://doi.org/10.1002/adma.201400523
  22. Solanki A, Shah S, Memoli KA, Park SY, Hong S, Lee K-B. Controlling differentiation of neural stem cells using extracellular matrix protein patterns. Small. 2010;6:2509-13. https://doi.org/10.1002/smll.201001341
  23. Cha C, Shin SR, Annabi N, Dokmeci MR, Khademhosseini A. Carbon-based nanomaterials: multifunctional materials for biomedical engineering. ACS Nano. 2013;7:2891-7. https://doi.org/10.1021/nn401196a
  24. Dubey N, Bentini R, Islam I, Cao T, Castro Neto AH, Rosa V. Graphene: a versatile carbon-based material for bone tissue engineering. Stem Cells Int. 2015;2015:12.
  25. Ilie I, Ilie R, Mocan T, Bartos D, Mocan L. Influence of nanomaterials on stem cell differentiation: designing an appropriate nanobiointerface. Int J Nanomedicine. 2012;7:2211-25.
  26. Solanki A, Kim JD, Lee K-B. Nanotechnology for regenerative medicine: nanomaterials for stem cell imaging. Nanomedicine. 2008;3:567-78. https://doi.org/10.2217/17435889.3.4.567
  27. Zhao C, Tan A, Pastorin G, Ho HK. Nanomaterial scaffolds for stem cell proliferation and differentiation in tissue engineering. Biotechnol Adv. 2013; 31:654-68. https://doi.org/10.1016/j.biotechadv.2012.08.001
  28. Goenka S, Sant V, Sant S. Graphene-based nanomaterials for drug delivery and tissue engineering. J Control Release. 2014;173:75-88. https://doi.org/10.1016/j.jconrel.2013.10.017
  29. Hubbell JA, Chilkoti A. Nanomaterials for drug delivery. Science. 2012;337:303. https://doi.org/10.1126/science.1219657
  30. Lock J, Liu H. Nanomaterials enhance osteogenic differentiation of human mesenchymal stem cells similar to a short peptide of BMP-7. Int J Nanomedicine. 2011;6:2769-77.
  31. Li J, Zhang J, Wang X, Kawazoe N, Chen G. Gold nanoparticle size and shape influence on osteogenesis of mesenchymal stem cells. Nanoscale. 2016;8:7992-8007. https://doi.org/10.1039/C5NR08808A
  32. Li JEJ, Kawazoe N, Chen G. Gold nanoparticles with different charge and moiety induce differential cell response on mesenchymal stem cell osteogenesis. Biomaterials. 2015;54:226-36. https://doi.org/10.1016/j.biomaterials.2015.03.001
  33. Yi C, Liu D, Fong C-C, Zhang J, Yang M. Gold nanoparticles promote osteogenic differentiation of mesenchymal stem cells through p38 MAPK pathway. ACS Nano. 2010;4:6439-48. https://doi.org/10.1021/nn101373r
  34. Grayson WL, Zhao F, Izadpanah R, Bunnell B, Ma T. Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. J Cell Physiol. 2006;207:331-9. https://doi.org/10.1002/jcp.20571
  35. Martino MM, Mochizuki M, Rothenfluh DA, Rempel SA, Hubbell JA, Barker TH. Controlling integrin specificity and stem cell differentiation in 2D and 3D environments through regulation of fibronectin domain stability. Biomaterials. 2009;30:1089-97. https://doi.org/10.1016/j.biomaterials.2008.10.047
  36. Pek YS, Wan ACA, Ying JY. The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials. 2010;31:385-91. https://doi.org/10.1016/j.biomaterials.2009.09.057
  37. Abdallah BM, Kassem M. Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther. 2007;15:109.
  38. Sila-Asna M, Bunyaratvej A, Maeda S, Kitaguchi H, Bunyaratavej N. Osteoblast differentiation and bone formation gene expression in strontium-inducing bone marrow mesenchymal stem cell. Kobe J Med Sci. 2007;53:25-35.
  39. Ng F, Boucher S, Koh S, Sastry KS, Chase L, Lakshmipathy U, Choong C, Yang Z, Vemuri MC, Rao MS. PDGF, TGF-${\beta}$, and FGF signaling is important for differentiation and growth of mesenchymal stem cells (MSCs): transcriptional profiling can identify markers and signaling pathways important in differentiation of MSCs into adipogenic, chondrogenic, and osteogenic lineages. Blood. 2008;112:295-307. https://doi.org/10.1182/blood-2007-07-103697
  40. Yoon D, Kim H, Lee E, Park MH, Chung S, Jeon H, Ahn C-H, Lee K. Study on chemotaxis and chemokinesis of bone marrow-derived mesenchymal stem cells in hydrogel-based 3D microfluidic devices. Biomater Res. 2016;20:25. https://doi.org/10.1186/s40824-016-0070-6
  41. Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 2006;7:14. https://doi.org/10.1186/1471-2121-7-14
  42. Yoshimura H, Muneta T, Nimura A, Yokoyama A, Koga H, Sekiya I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res. 2007;327:449-62. https://doi.org/10.1007/s00441-006-0308-z
  43. Akhavan O, Ghaderi E, Emamy H, Akhavan F. Genotoxicity of graphene nanoribbons in human mesenchymal stem cells. Carbon. 2013;54:419-31. https://doi.org/10.1016/j.carbon.2012.11.058
  44. Chao T-I, Xiang S, Chen C-S, Chin W-C, Nelson A, Wang C, Lu J. Carbon nanotubes promote neuron differentiation from human embryonic stem cells. Biochem Biophys Res Commun. 2009;384:426-30. https://doi.org/10.1016/j.bbrc.2009.04.157
  45. Liu D, Yi C, Zhang D, Zhang J, Yang M. Inhibition of proliferation and differentiation of mesenchymal stem cells by carboxylated carbon nanotubes. ACS Nano. 2010;4:2185-95. https://doi.org/10.1021/nn901479w
  46. Akhavan O, Ghaderi E, Abouei E, Hatamie S, Ghasemi E. Accelerated differentiation of neural stem cells into neurons on ginseng-reduced graphene oxide sheets. Carbon. 2014;66:395-406. https://doi.org/10.1016/j.carbon.2013.09.015
  47. Kim J, Choi KS, Kim Y, Lim KT, Seonwoo H, Park Y, Kim DH, Choung PH, Cho CS, Kim SY. Bioactive effects of graphene oxide cell culture substratum on structure and function of human adipose-derived stem cells. J Biomed Mater Res Part A. 2013;101:3520-30. https://doi.org/10.1002/jbm.a.34659
  48. Weaver CL, Cui XT. Directed neural stem cell differentiation with a functionalized graphene oxide nanocomposite. Adv Healthc Mater. 2015;4:1408-16. https://doi.org/10.1002/adhm.201500056
  49. Tehrani Z, Burwell G, Azmi MM, Castaing A, Rickman R, Almarashi J, Dunstan P, Beigi AM, Doak S, Guy O. Generic epitaxial graphene biosensors for ultrasensitive detection of cancer risk biomarker. 2D Mater. 2014;1:025004. https://doi.org/10.1088/2053-1583/1/2/025004
  50. Elkhenany H, Amelse L, Lafont A, Bourdo S, Caldwell M, Neilsen N, Dervishi E, Derek O, Biris AS, Anderson D. Graphene supports in vitro proliferation and osteogenic differentiation of goat adult mesenchymal stem cells: potential for bone tissue engineering. J Appl Toxicol. 2015;35:367-74. https://doi.org/10.1002/jat.3024
  51. Lee JH, Shin YC, Jin OS, Kang SH, Hwang Y-S, Park J-C, Hong SW, Han D-W. Reduced graphene oxide-coated hydroxyapatite composites stimulate spontaneous osteogenic differentiation of human mesenchymal stem cells. Nano. 2015;7:11642-51.
  52. Gu M, Liu Y, Chen T, Du F, Zhao X, Xiong C, Zhou Y. Is graphene a promising nano-material for promoting surface modification of implants or scaffold materials in bone tissue engineering? Tissue Eng Part B Rev. 2014;20:477-91. https://doi.org/10.1089/ten.teb.2013.0638
  53. Tatavarty R, Ding H, Lu G, Taylor RJ, Bi X. Synergistic acceleration in the osteogenesis of human mesenchymal stem cells by graphene oxide-calcium phosphate nanocomposites. Chem Commun. 2014;50:8484-7. https://doi.org/10.1039/C4CC02442G
  54. Suhito IR, Han Y, Kim D-S, Son H, Kim T-H. Effects of two-dimensional materials on human mesenchymal stem cell behaviors. Biochem Biophys Res Commun. 2017;493:578-84. https://doi.org/10.1016/j.bbrc.2017.08.149
  55. Chen G-Y, Pang D-P, Hwang S-M, Tuan H-Y, Hu Y-C. A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials. 2012;33:418-27. https://doi.org/10.1016/j.biomaterials.2011.09.071
  56. Chen Y-S, Hung Y-C, Liau I, Huang GS. Assessment of the in vivo toxicity of gold nanoparticles. Nanoscale Res Lett. 2009;4:858. https://doi.org/10.1007/s11671-009-9334-6
  57. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol. 2007;2:751. https://doi.org/10.1038/nnano.2007.387
  58. Zhang L, Gu F, Chan J, Wang A, Langer R, Farokhzad O. Nanoparticles in medicine: therapeutic applications and developments. Clin Pharmacol Ther. 2008;83:761-9. https://doi.org/10.1038/sj.clpt.6100400
  59. Boisselier E, Astruc D. Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. Chem Soc Rev. 2009;38:1759-82. https://doi.org/10.1039/b806051g
  60. Zhang X. Gold nanoparticles: recent advances in the biomedical applications. Cell Biochem Biophys. 2015;72:771-5. https://doi.org/10.1007/s12013-015-0529-4
  61. Yoo D, Lee D. Oligochitosan-stabilized photoluminescent gold nanoconstructs for optical bioimaging. Biomater Res. 2017;21:20. https://doi.org/10.1186/s40824-017-0107-5
  62. Dreaden EC, Austin LA, Mackey MA, El-Sayed MA. Size matters: gold nanoparticles in targeted cancer drug delivery. Ther Deliv. 2012;3:457-78. https://doi.org/10.4155/tde.12.21
  63. Kong F-Y, Zhang J-W, Li R-F, Wang Z-X, Wang W-J, Wang W. Unique roles of gold nanoparticles in drug delivery, targeting and imaging applications. Molecules. 2017;22:1445. https://doi.org/10.3390/molecules22091445
  64. Fratoddi I, Venditti I, Cametti C, Russo MV. How toxic are gold nanoparticles? The state-of-the-art. Nano Res. 2015;8:1771-99. https://doi.org/10.1007/s12274-014-0697-3
  65. Choi SY, Song MS, Ryu PD, Lam ATN, Joo S-W, Lee SY. Gold nanoparticles promote osteogenic differentiation in human adipose-derived mesenchymal stem cells through the Wnt/${\beta}$-catenin signaling pathway. Int J Nanomedicine. 2015;10:4383.
  66. Venkatesan J, Kim S-K. Chitosan composites for bone tissue engineering-an overview. Mar Drugs. 2010;8:2252. https://doi.org/10.3390/md8082252
  67. Peschel D, Zhang K, Fischer S, Groth T. Modulation of osteogenic activity of BMP-2 by cellulose and chitosan derivatives. Acta Biomater. 2012;8:183-93. https://doi.org/10.1016/j.actbio.2011.08.012
  68. Poudel B, Lim S-W, Ki H-H, Nepali S, Lee Y-M, Kim D-K. Dioscin inhibits adipogenesis through the AMPK/MAPK pathway in 3T3-L1 cells and modulates fat accumulation in obese mice. Int J Mol Med. 2014;34:1401-8. https://doi.org/10.3892/ijmm.2014.1921
  69. Tang Q, Chen C, Zhang Y, Dai M, Jiang Y, Wang H, Yu M, Jing W, Tian W. Wnt5a regulates the cell proliferation and adipogenesis via MAPKindependent pathway in early stage of obesity. Cell Biol Int. 2018;42:63-74. https://doi.org/10.1002/cbin.10862
  70. Habibovic P, Yuan H, van der Valk CM, Meijer G, van Blitterswijk CA, de Groot K. 3D microenvironment as essential element for osteoinduction by biomaterials. Biomaterials. 2005;26:3565-75. https://doi.org/10.1016/j.biomaterials.2004.09.056
  71. Lobo SE, Livingston Arinzeh T. Biphasic calcium phosphate ceramics for bone regeneration and tissue engineering applications. Materials. 2010;3:815-26. https://doi.org/10.3390/ma3020815
  72. Rosa V, Zhang Z, Grande R, Nor J. Dental pulp tissue engineering in full-length human root canals. J Dent Res. 2013;92:970-5. https://doi.org/10.1177/0022034513505772
  73. Miramond T, Corre P, Borget P, Moreau F, Guicheux J, Daculsi G, Weiss P. Osteoinduction of biphasic calcium phosphate scaffolds in a nude mouse model. J Biomater Appl. 2014;29:595-604. https://doi.org/10.1177/0885328214537859
  74. Jager M, Feser T, Denck H, Krauspe R. Proliferation and osteogenic differentiation of mesenchymal stem cells cultured onto three different polymers in vitro. Ann Biomed Eng. 2005;33:1319-32. https://doi.org/10.1007/s10439-005-5889-2
  75. Rosa V, Della Bona A, Cavalcanti BN, Nor JE. Tissue engineering: from research to dental clinics. Dent Mater. 2012;28:341-8. https://doi.org/10.1016/j.dental.2011.11.025
  76. Chung T-H, Wu S-H, Yao M, Lu C-W, Lin Y-S, Hung Y, Mou C-Y, Chen Y-C, Huang D-M. The effect of surface charge on the uptake and biological function of mesoporous silica nanoparticles in 3T3-L1 cells and human mesenchymal stem cells. Biomaterials. 2007;28:2959-66. https://doi.org/10.1016/j.biomaterials.2007.03.006
  77. Curran JM, Chen R, Hunt JA. The guidance of human mesenchymal stem cell differentiation in vitro by controlled modifications to the cell substrate. Biomaterials. 2006;27:4783-93. https://doi.org/10.1016/j.biomaterials.2006.05.001
  78. Sundelacruz S, Levin M, Kaplan DL. Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS One. 2008; 3:e3737. https://doi.org/10.1371/journal.pone.0003737
  79. Benoit DS, Schwartz MP, Durney AR, Anseth KS. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat Mater. 2008;7:816. https://doi.org/10.1038/nmat2269
  80. Wang H, Kwok DT, Xu M, Shi H, Wu Z, Zhang W, Chu PK. Tailoring of mesenchymal stem cells behavior on plasma-modified polytetrafluoroethylene. Adv Mater. 2012;24:3315-24. https://doi.org/10.1002/adma.201104967
  81. Crowder SW, Prasai D, Rath R, Balikov DA, Bae H, Bolotin KI, Sung H-J. Threedimensional graphene foams promote osteogenic differentiation of human mesenchymal stem cells. Nano. 2013;5:4171-6.
  82. Dong X, Wang X, Wang L, Song H, Zhang H, Huang W, Chen P. 3D graphene foam as a monolithic and macroporous carbon electrode for electrochemical sensing. ACS Appl Mater Interfaces. 2012;4:3129-33. https://doi.org/10.1021/am300459m
  83. Li N, Chen Z, Ren W, Li F, Cheng H-M. Flexible graphene-based lithium ion batteries with ultrafast charge and discharge rates. Proc Natl Acad Sci. 2012; 109:17360-5. https://doi.org/10.1073/pnas.1210072109
  84. Zhou G, Li L, Ma C, Wang S, Shi Y, Koratkar N, Ren W, Li F, Cheng H-M. A graphene foam electrode with high sulfur loading for flexible and high energy li-S batteries. Nano Energy. 2015;11:356-65. https://doi.org/10.1016/j.nanoen.2014.11.025
  85. Zhao Y, Liu J, Hu Y, Cheng H, Hu C, Jiang C, Jiang L, Cao A, Qu L. Highly compression-tolerant supercapacitor based on polypyrrole-mediated graphene foam electrodes. Adv Mater. 2013;25:591-5. https://doi.org/10.1002/adma.201203578
  86. Akhavan O, Ghaderi E, Shirazian SA, Rahighi R. Rolled graphene oxide foams as three-dimensional scaffolds for growth of neural fibers using electrical stimulation of stem cells. Carbon. 2016;97:71-7. https://doi.org/10.1016/j.carbon.2015.06.079
  87. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell. 2004;6:483-95. https://doi.org/10.1016/S1534-5807(04)00075-9
  88. Mathieu PS, Loboa EG. Cytoskeletal and focal adhesion influences on mesenchymal stem cell shape, mechanical properties, and differentiation down osteogenic, adipogenic, and chondrogenic pathways. Tissue Eng Part B Rev. 2012;18:436-44. https://doi.org/10.1089/ten.teb.2012.0014
  89. Tercero JE, Namin S, Lahiri D, Balani K, Tsoukias N, Agarwal A. Effect of carbon nanotube and aluminum oxide addition on plasma-sprayed hydroxyapatite coating's mechanical properties and biocompatibility. Mater Sci Eng C Mater Biol Appl. 2009;29:2195-202. https://doi.org/10.1016/j.msec.2009.05.001
  90. Balani K, Anderson R, Laha T, Andara M, Tercero J, Crumpler E, Agarwal A. Plasma-sprayed carbon nanotube reinforced hydroxyapatite coatings and their interaction with human osteoblasts in vitro. Biomaterials. 2007;28:618-24. https://doi.org/10.1016/j.biomaterials.2006.09.013
  91. Balani K, Chen Y, Harimkar SP, Dahotre NB, Agarwal A. Tribological behavior of plasma-sprayed carbon nanotube-reinforced hydroxyapatite coating in physiological solution. Acta Biomater. 2007;3:944-51. https://doi.org/10.1016/j.actbio.2007.06.001
  92. Lee J-R, Ryu S, Kim S, Kim B-S. Behaviors of stem cells on carbon nanotube. Biomater Res. 2015;19:3. https://doi.org/10.1186/s40824-014-0024-9
  93. Gao W, The chemistry of graphene oxide, Graphene oxide, Springer2015, pp. 61-95.
  94. Xie Y, Li H, Zhang C, Gu X, Zheng X, Huang L. Graphene-reinforced calcium silicate coatings for load-bearing implants. Biomed Mater. 2014;9:025009. https://doi.org/10.1088/1748-6041/9/2/025009
  95. Kang SM, Park S, Kim D, Park SY, Ruoff RS, Lee H. Simultaneous reduction and surface functionalization of graphene oxide by mussel-inspired chemistry. Adv Funct Mater. 2011;21:108-12. https://doi.org/10.1002/adfm.201001692
  96. Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani MH, Baharvand H, Kiani S, Al-Deyab SS, Ramakrishna S. Application of conductive polymers, scaffolds and electrical stimulation for nerve tissue engineering. J Tissue Eng Regen Med. 2011;5:e17-35. https://doi.org/10.1002/term.383
  97. Gomez N, Lee JY, Nickels JD, Schmidt CE. Micropatterned polypyrrole: a combination of electrical and topographical characteristics for the stimulation of cells. Adv Funct Mater. 2007;17:1645-53. https://doi.org/10.1002/adfm.200600669
  98. Svennersten K, Larsson KC, Berggren M, Richter-Dahlfors A. Organic bioelectronics in nanomedicine. Biochim Biophys Acta Gen Subj. 2011; 1810:276-85. https://doi.org/10.1016/j.bbagen.2010.10.001
  99. Hsiao YS, Kuo CW, Chen P. Multifunctional graphene-PEDOT microelectrodes for on-chip manipulation of human mesenchymal stem cells. Adv Funct Mater. 2013;23:4649-56.
  100. Hsiao Y-S, Lin C-C, Hsieh H-J, Tsai S-M, Kuo C-W, Chu C-W, Chen P. Manipulating location, polarity, and outgrowth length of neuron-like pheochromocytoma (PC-12) cells on patterned organic electrode arrays. Lab Chip. 2011;11:3674-80. https://doi.org/10.1039/c1lc20675c
  101. Kang E-S, Kim D-S, Suhito IR, Choo S-S, Kim S-J, Song I, Kim T-H. Guiding osteogenesis of mesenchymal stem cells using carbon-based nanomaterials. Nano Converg. 2017;4:2. https://doi.org/10.1186/s40580-017-0096-z
  102. Guo W, Wang S, Yu X, Qiu J, Li J, Tang W, Li Z, Mou X, Liu H, Wang Z. Construction of a 3D rGO-collagen hybrid scaffold for enhancement of the neural differentiation of mesenchymal stem cells. Nano. 2016;8:1897-904.

피인용 문헌

  1. Application of black phosphorus nanodots to live cell imaging vol.22, pp.1, 2018, https://doi.org/10.1186/s40824-018-0142-x
  2. Combined Application of Graphene‐Family Materials and Silk Fibroin in Biomedicine vol.4, pp.19, 2019, https://doi.org/10.1002/slct.201804034
  3. Molecular-Level Interactions between Engineered Materials and Cells vol.20, pp.17, 2018, https://doi.org/10.3390/ijms20174142
  4. The design and biomedical applications of self-assembled two-dimensional organic biomaterials vol.48, pp.23, 2018, https://doi.org/10.1039/c8cs01003j
  5. Combined photodynamic-chemotherapy investigation of cancer cells using carbon quantum dot-based drug carrier system vol.27, pp.1, 2020, https://doi.org/10.1080/10717544.2020.1765431
  6. Mechanophysical Cues in Extracellular Matrix Regulation of Cell Behavior vol.21, pp.9, 2018, https://doi.org/10.1002/cbic.201900686
  7. Graphene Hybrid Materials for Controlling Cellular Microenvironments vol.13, pp.18, 2018, https://doi.org/10.3390/ma13184008
  8. Topography: A Biophysical Approach to Direct the Fate of Mesenchymal Stem Cells in Tissue Engineering Applications vol.10, pp.10, 2018, https://doi.org/10.3390/nano10102070
  9. From the Matrix to the Nucleus and Back: Mechanobiology in the Light of Health, Pathologies, and Regeneration of Oral Periodontal Tissues vol.11, pp.6, 2018, https://doi.org/10.3390/biom11060824
  10. Enhancing osteogenesis of adipose-derived mesenchymal stem cells using gold nanostructure/peptide-nanopatterned graphene oxide vol.204, pp.None, 2021, https://doi.org/10.1016/j.colsurfb.2021.111807
  11. Emerging 2D nanomaterials for biomedical applications vol.50, pp.None, 2018, https://doi.org/10.1016/j.mattod.2021.04.020