The effects of graphene nanostructures on mesenchymal stem cells

Biomaterials

Volumn 35, Issue 18, 2014, Pages 4863-4877

  Talukdar, Yahfi ^a   Rashkow, Jason T ^a   Lalwani, Gaurav ^a   Kanakia, Shruti ^a   Sitharaman, Balaji ^a  

^a St Francis Hospital The Heart Center   (United States)

Author keywords

Carbon nanoparticles; Differentiation; Graphene; Stem cells

Indexed keywords

DIFFERENTIATION (CALCULUS); GRAPHENE; NANOPARTICLES; NANORIBBONS; PHOSPHATASES; STEM CELLS; TRANSMISSION ELECTRON MICROSCOPY;

ADIPOSE-DERIVED MESENCHYMAL STEM CELLS; ALKALINE PHOSPHATASE ACTIVITY; BONE MARROW-DERIVED MESENCHYMAL STEM CELLS; CARBON NANO-PARTICLES; CONFOCAL RAMAN SPECTROSCOPY; HUMAN MESENCHYMAL STEM CELLS; MESENCHYMAL STEM CELL; OIL RED O STAINING;

CELL CULTURE;

ALIZARIN RED S; ALKALINE PHOSPHATASE; CALCIUM; GRAPHENE; GRAPHENE OXIDE; NANOMATERIAL; NANORIBBON; GRAPHITE;

ADIPOCYTE; ARTICLE; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; OSTEOBLAST; PRIORITY JOURNAL; RAMAN SPECTROMETRY; TRANSMISSION ELECTRON MICROSCOPY; CELL SURVIVAL; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM;

ADIPOCYTES; ALKALINE PHOSPHATASE; CELL DIFFERENTIATION; CELL SURVIVAL; GRAPHITE; HUMANS; MESENCHYMAL STROMAL CELLS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NANOSTRUCTURES; OSTEOBLASTS; SPECTRUM ANALYSIS, RAMAN;

EID: 84897917056     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.02.054     Document Type: Article

References (59)

1. Xia Y., Yang P., Sun Y., Wu Y., Mayers B., Gates B., et al. One-dimensional nanostructures: synthesis, characterization, and applications. Adv Mater 2003, 15:353-389.
2. Mendes R.G., Bachmatiuk A., Büchner B., Cuniberti G., Rümmeli M.H. Carbon nanostructures as multi-functional drug delivery platforms. J Mater Chem B Mater Biol Med 2013, 1:401-428.
3. Yang K., Hu L., Ma X., Ye S., Cheng L., Shi X., et al. Multimodal imaging guided photothermal therapy using functionalized graphene nanosheets anchored with magnetic nanoparticles. Adv Mater 2012, 24:1868-1872.
4. Yang K., Zhang S., Zhang G., Sun X., Lee S.T., Liu Z. Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett 2010, 10:3318-3323.
5. Lalwani G., Sitharaman B. Multifunctional fullerene- and metallofullerene-based nanobiomaterials. Nano Life 2013, 03:1342003.
6. Lalwani G., Cai X., Nie L., Wang L.V., Sitharaman B. Graphene-based contrast agents for photoacoustic and thermoacoustic tomography. Photoacoustics 2013, 1:62-67.
7. Avti P.K., Talukdar Y., Sirotkin M.V., Shroyer K.R., Sitharaman B. Toward single-walled carbon nanotube-gadolinium complex as advanced MRI contrast agents: pharmacodynamics and global genomic response in small animals. J Biomed Mater Res B Appl Biomater 2013, 101:1039-1049.
8. Kanakia S., Toussaint J.D., Chowdhury S.M., Lalwani G., Tembulkar T., Button T., et al. Physicochemical characterization of a novel graphene-based magnetic resonance imaging contrast agent. Int J Nanomed 2013, 8:2821-2833.
9. Lalwani G., Henslee A.M., Farshid B., Lin L., Kasper F.K., Qin Y.X., et al. Two-dimensional nanostructure-reinforced biodegradable polymeric nanocomposites for bone tissue engineering. Biomacromolecules 2013, 14:900-909.
10. Friedenstein A., Piatetzky-Shapiro I., Petrakova K. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 1966, 16:381-390.
11. Young R.G., Butler D.L., Weber W., Caplan A.I., Gordon S.L., Fink D.J. Use of mesenchymal stem cells in a collagen matrix for Achilles tendon repair. J Orthop Res 2005, 16:406-413.
12. Smith R.K.W., Korda M., Blunn G.W., Goodship A.E. Isolation and implantation of autologous equine mesenchymal stem cells from bone marrow into the superficial digital flexor tendon as a potential novel treatment. Equine Vet J 2003, 35:99-102.
13. Caplan A.I. Mesenchymal stem cells. J Orthop Res 1991, 9:641-650.
14. Shang Q., Wang Z., Liu W., Shi Y., Cui L., Cao Y. Tissue-engineered bone repair of Sheep Cranial defects with autologous bone marrow stromal cells. J Craniofac Surg 2001, 12:586-593.
15. Kang H.-J., Kim H.-S., Koo B.-K., Kim Y.-J., Lee D., Sohn D.-W., et al. Intracoronary infusion of the mobilized peripheral blood stem cell by G-CSF is better than mobilization alone by G-CSF for improvement of cardiac function and remodeling: 2-year follow-up results of the Myocardial Regeneration and Angiogenesis in Myocardial Infarction with G-CSF and Intra-Coronary Stem Cell Infusion (MAGIC Cell) 1 trial. Am Heart J 2007, 153. 237e1-e8.
16. Janssens S., Dubois C., Bogaert J., Theunissen K., Deroose C., Desmet W., et al. Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 2006, 367:113-121.
17. Corsi K., Chellat F., Yahia L.H., Fernandes J.C. Mesenchymal stem cells, MG63 and HEK293 transfection using chitosan-DNA nanoparticles. Biomaterials 2003, 24:1255-1264.
18. Cao X., Deng W., Wei Y., Yang Y., Su W., Wei Y., et al. Incorporating pTGF-β1/calcium phosphate nanoparticles with fibronectin into 3-dimensional collagen/chitosan scaffolds: efficient, sustained gene delivery to stem cells for chondrogenic differentiation. Eur Cell Mater 2012, 23:81-93.
19. Lee J.H., Jung M.J., Hwang Y.H., Lee Y.J., Lee S., Lee D.Y., et al. Heparin-coated superparamagnetic iron oxide for in vivo MR imaging of human MSCs. Biomaterials 2012, 33:4861-4871.
20. Reddy A.M., Kwak B.K., Shim H.J., Ahn C., Lee H.S., Suh Y.J., et al. In vivo tracking of mesenchymal stem cells labeled with a novel chitosan-coated superparamagnetic iron oxide nanoparticles using 3.0T MRI. J Korean Med Sci 2010, 25:211-219.
21. Paratala B.S., Jacobson B.D., Kanakia S., Francis L.D., Sitharaman B. Physicochemical characterization, and relaxometry studies of micro-graphite oxide, graphene nanoplatelets, and nanoribbons. PLoS One 2012, 7:e38185.
22. Bao H., Pan Y., Ping Y., Sahoo N.G., Wu T., Li L., et al. Chitosan-Functionalized graphene oxide as a nanocarrier for drug and gene delivery. Small 2011, 7:1569-1578.
23. Chen B., Liu M., Zhang L., Huang J., Yao J., Zhang Z. Polyethylenimine-functionalized graphene oxide as an efficient gene delivery vector. J Mater Chem 2011, 21:7736-7741.
24. Zhang M., Bai L., Shang W., Xie W., Ma H., Fu Y., et al. Facile synthesis of water-soluble, highly fluorescent graphene quantum dots as a robust biological label for stem cells. J Mater Chem 2012, 22:7461-7467.
25. Akhavan O., Ghaderi E., Akhavan A. Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials 2012, 33:8017-8025.
26. Wang X., Podila R., Shannahan J.H., Rao A.M., Brown J.M. Intravenously delivered graphene nanosheets and multiwalled carbon nanotubes induce site-specific Th2 inflammatory responses via the IL-33/ST2 axis. Int J Nanomed 2013, 8:1733.
27. Shen J., Hu Y., Li C., Qin C., Ye M. Synthesis of amphiphilic graphene nanoplatelets. Small 2009, 5:82-85.
28. Kosynkin D.V., Higginbotham A.L., Sinitskii A., Lomeda J.R., Dimiev A., Price B.K., et al. Longitudinal unzipping of carbon nanotubes to form graphene nanoribbons. Nature 2009, 458:872-876.
29. Delgado J.L., Herranz M.Á., Martín N. The nano-forms of carbon. J Mater Chem 2008, 18:1417-1426.
30. Mullick Chowdhury S., Lalwani G., Zhang K., Yang J.Y., Neville K., Sitharaman B. Cell specific cytotoxicity and uptake of graphene nanoribbons. Biomaterials 2013, 34:283-293.
31. Hong L., Peptan I.A., Colpan A., Daw J.L. Adipose tissue engineering by human adipose-derived stromal cells. Cells Tissues Organs 2006, 183:133-140.
32. Majors A.K., Boehm C.A., Nitto H., Midura R.J., Muschler G.F. Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation. J Orthop Res 2005, 15:546-557.
33. Boufker H.I., Lagneaux L., Najar M., Piccart M., Ghanem G., Body J.J., et al. The Src inhibitor dasatinib accelerates the differentiation of human bone marrow-derived mesenchymal stromal cells into osteoblasts. BMC Cancer 2010, 10:298.
34. Mikos A.G. Effect of bone extracellular matrix synthesized in vitro on the osteoblastic differentiation of marrow stromal cells. Biomaterials 2005, 26:971-977.
35. O'Brien J., Wilson I., Orton T., Pognan F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 2003, 267:5421-5426.
36. Gupta A.K., Wells S. Surface-modified superparamagnetic nanoparticles for drug delivery: preparation, characterization, and cytotoxicity studies. IEEE Trans Nanobioscience 2004, 3:66-73.
37. Mehlem A., Hagberg C.E., Muhl L., Eriksson U., Falkevall A. Imaging of neutral lipids by oil red O for analyzing the metabolic status in health and disease. Nat Protoc 2013, 8:1149-1154.
38. Krause U., Seckinger A., Gregory C.A. Assays of osteogenic differentiation by cultured human mesenchymal stem cells. Science 2011, 215-230.
39. Toquet J., Rohanizadeh R., Guicheux J., Couillaud S., Passuti N., Daculsi G., et al. Osteogenic potential in vitro of human bone marrow cells cultured on macroporous biphasic calcium phosphate ceramic. J Biomed Mater Res 1999, 44:98-108.
40. Heller D.A., Baik S., Eurell T.E., Strano M.S. Single-Walled carbon nanotube spectroscopy in live cells: towards Long-Term labels and optical sensors. Adv Mater 2005, 17:2793-2799.
41. Strano M.S., Huffman C.B., Moore V.C., O'Connell M.J., Haroz E.H., Hubbard J., et al. Reversible, band-gap-selective protonation of single-walled carbon nanotubes in solution. J Phys Chem B 2003, 107:6979-6985.
42. Liao K.-H., Lin Y.-S., Macosko C.W., Haynes C.L. Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl Mater Interfaces 2011, 3:2607-2615.
43. Mao H.Y., Laurent S., Chen W., Akhavan O., Imani M., Ashkarran A.A., et al. Graphene: promises, facts, opportunities, and challenges in nanomedicine. Chem Rev 2013, 113:3407-3424.
44. Khurana A., Chapelin F., Beck G., Lenkov O.D., Donig J., Nejadnik H., et al. Iron administration before stem cell harvest enables MR imaging tracking after transplantation. Radiology 2013, 269:186-197.
45. Murphy J.M., Fink D.J., Hunziker E.B., Barry F.P. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 2003, 48:3464-3474.
46. Strauer B.E., Kornowski R. Stem cell therapy in perspective. Circulation 2003, 107:929-934.
47. Dresselhaus M.S., Dresselhaus G., Saito R., Jorio A. Raman spectroscopy of carbon nanotubes. Phys Rep 2005, 409:47-99.
48. Salzmann C.G., Llewellyn S.A., Tobias G., Ward M.A., Huh Y., Green M.L. The role of carboxylated carbonaceous fragments in the functionalization and spectroscopy of a Single-Walled-Nanotube material. Adv Mater 2007, 19:883-887.
49. Lalwani G., Kwaczala A.T., Kanakia S., Patel S.C., Judex S., Sitharaman B. Fabrication and characterization of three-dimensional macroscopic all-carbon scaffolds. Carbon N Y 2013, 53:90-100.
50. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
51. Jaiswal R.K., Jaiswal N., Bruder S.P., Mbalaviele G., Marshak D.R., Pittenger M.F. Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 2000, 275:9645-9652.
52. Raffa V., Ciofani G., Vittorio O., Riggio C., Cuschieri A. Physicochemical properties affecting cellular uptake of carbon nanotubes. Nanomedicine 2010, 5:89-97.
53. Rejman J., Oberle V., Zuhorn I.S., Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 2004, 377:159-169.
54. Chang Y., Yang S.-T., Liu J.-H., Dong E., Wang Y., Cao A., et al. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett 2011, 200:201-210.
55. Shvedova A.A., Pietroiusti A., Fadeel B., Kagan V.E. Mechanisms of carbon nanotube-induced toxicity: focus on oxidative stress. Toxicol Appl Pharm 2012, 261:121-133.
56. Liu S., Wei L., Hao L., Fang N., Chang M.W., Xu R., et al. Sharper and faster "nano darts" kill more bacteria: a study of antibacterial activity of individually dispersed pristine single-walled carbon nanotube. ACS Nano 2009, 3:3891-3902.
57. Arvizo R.R., Miranda O.R., Thompson M.A., Pabelick C.M., Bhattacharya R., Robertson J.D., et al. Effect of nanoparticle surface charge at the plasma membrane and beyond. Nano Lett 2010, 10:2543-2548.
58. Zhang L., Xia J., Zhao Q., Liu L., Zhang Z. Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs. Small 2010, 6:537-544.
59. Cong H.P., He J.J., Lu Y., Yu S.H. Water-soluble magnetic functionalized reduced graphene oxide sheets: in situ synthesis and magnetic resonance imaging applications. Small 2010, 6:169-173.