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Coupling (reduced) Graphene Oxide to Mammalian Primary Cortical Neurons In Vitro

1 Theoretical Neurobiology and Neuroengineering Laboratory, Dept. of Biomedical Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium
2 Institute for Materials Research, Material Physics Division, Hasselt University, 3590 Diepenbeek, Belgium; IMOMEC associated laboratory, IMEC, Kapeldreef 75, 3001 Leuven, Belgium
3 Institute of Materials Research and Engineering, Agency for Science, Technology and Research, 3 Research Link, Singapore 117602
4 Department of Chemistry and Graphene Research Centre, National University of Singapore, 3 Science Drive 3, Singapore 117543
5 Brain Mind Institute, Swiss Federal Institute of Technology Lausanne, Switzerland; and Dept. Computer Science, University of Sheffield, S1 4DP, UK

Special Issues: Nanomaterials for Cognitive Technology

Neuronal nanoscale interfacing aims at identifying or designing nanostructured smart materials and validating their applications as novel biocompatible scaffolds with active properties for neuronal networks formation, nerve regeneration, and bidirectional biosignal coupling. Among several carbon-based nanomaterials, Graphene recently attracted great interest for biological applications, given its unique mechanical, optical, electronic properties, and its recent technological applications. Here we explore the use of Graphene Oxide (GO) and reduced Graphene Oxide (rGO) as biocompatible culture substrates for primary neuronal networks developing ex vivo. We quantitatively studied cytotoxicity and cellular viability as well as single-cell and network-level electrophysiological properties of neurons in vitro. Our results confirm previous reports, employing immortalized cell lines or pluripotent stem cells, and extend them to mammalian primary cortical neurons: GO and rGO are biocompatible substrates and do not alter neuronal excitable properties.
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References

1. Alivisatos AP, Andrews AM, Boyden ES, et al. (2013) Nanotools for neuroscience and brain activity mapping. ACS Nano 7: 1850-1866.    

2. Cellot G, Cilia E, Cipollone S, et al. (2009) Carbon nanotubes might improve neuronal performance by favouring electrical shortcuts. Nat Nanotechnol 4: 126-133.    

3. Monaco AM, Giugliano M (2014) Carbon-based smart nanomaterials in biomedicine and neuroengineering. Beilstein J Nanotechnol 5: 1849-1863.    

4. Reinartz S, Biro I, Gal A, et al. (2014) Synaptic dynamics contribute to long-term single neuron response fluctuations. Front Neural Circuits 8: 71.

5. Giugliano M, Martinoia S (2006) Substrate Arrays of Microelectrodes forin vitroElectrophysiology.

6. Pautot S, Wyart C, Isacoff EY (2008) Colloid-guided assembly of oriented 3D neuronal networks. Nat Methods 5: 735-740.    

7. Tang-Schomer MD, White JD, Tien LW, et al. (2014) Bioengineered functional brain-like cortical tissue. Proc Natl Acad Sci U S A 111: 13811-13816.    

8. Kunze A, Bertsch A, Giugliano M, et al. (2009) Microfluidic hydrogel layers with multiple gradients to stimulate and perfuse three-dimensional neuronal cell cultures. Procedia Chem 1: 369-372.    

9. Wick P, Louw-Gaume AE, Kucki M, et al. (2014) Classification framework for graphene-based materials. Angew Chem Int Ed Engl 53: 7714-7718.    

10. Ferrari AC, Bonaccorso F, Fal'ko V, et al. (2015) Science and technology roadmap for graphene, related two-dimensional crystals, and hybrid systems. Nanoscale 7: 4598-4810.    

11. Mazzatenta A, Giugliano M, Campidelli S, et al. (2007) Interfacing neurons with carbon nanotubes: electrical signal transfer and synaptic stimulation in cultured brain circuits. J Neurosci 27: 6931-6936.    

12. Falvo MR, Clary GJ, Taylor RM, et al. (1997) Bending and buckling of carbon nanotubes under large strain. Nature 389: 582-584.    

13. Novoselov KS, Geim AK, Morozov SV, et al. (2004) Electric field effect in atomically thin carbon films. Science 306: 666-669.    

14. Novoselov KS, Jiang D, Schedin F, et al. (2005) Two-dimensional atomic crystals. Proc Natl Acad Sci U S A 102: 10451-10453.    

15. Novoselov KS, Jiang Z, Zhang Y, et al. (2007) Room-temperature quantum Hall effect in graphene. Science 315: 1379.    

16. Katsnelson MI, Novoselov KS, Geim AK (2006) Chiral tunnelling and the Klein paradox in graphene. Nature Physics 2: 620-625.    

17. Lee C, Wei X, Kysar JW, et al. (2008) Measurement of the elastic properties and intrinsic strength of monolayer graphene. Science 321: 385-388.    

18. Nair RR, Blake P, Grigorenko AN, et al. (2008) Fine structure constant defines visual transparency of graphene. Science 320: 1308.    

19. Stoller MD, Park S, Zhu Y, et al. (2008) Graphene-Based Ultracapacitors. Nano Lett 8: 3498-3502.    

20. Feng L, Zhang S, Liu Z (2011) Graphene based gene transfection. Nanoscale 3: 1252-1257.    

21. Dey RS, Raj CR (2010) Development of an Amperometric Cholesterol Biosensor Based on Graphene-Pt Nanoparticle Hybrid Material. J Phys Chem C 114: 21427-21433.    

22. Heo C, Yoo J, Lee S, et al. (2011) The control of neural cell-to-cell interactions through non-contact electrical field stimulation using graphene electrodes. Biomaterials 32: 19-27.    

23. Yang K, Wan J, Zhang S, et al. (2012) The influence of surface chemistry and size of nanoscale graphene oxide on photothermal therapy of cancer using ultra-low laser power. Biomaterials 33: 2206-2214.    

24. Kalbacova M, Broz A, Kong J, et al. (2010) Graphene substrates promote adherence of human osteoblasts and mesenchymal stromal cells. Carbon 48: 4323-4329.    

25. Li N, Zhang X, Song Q, et al. (2011) The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates. Biomaterials 32: 9374-9382.    

26. Sahni D, Jea A, Mata JA, et al. (2013) Biocompatibility of pristine graphene for neuronal interface. J Neurosurg Pediatr 11: 575-583.    

27. Nayak TR, Andersen H, Makam VS, et al. (2011) Graphene for controlled and accelerated osteogenic differentiation of human mesenchymal stem cells. ACS Nano 5: 4670-4678.    

28. Lee WC, Lim CH, Shi H, et al. (2011) Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano 5: 7334-7341.    

29. Li N, Zhang Q, Gao S, et al. (2013) Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci Rep 3: 1604.

30. Kuzum D, Takano H, Shim E, et al. (2014) Transparent and flexible low noise graphene electrodes for simultaneous electrophysiology and neuroimaging. Nat Commun 5: 5259.    

31. Park DW, Schendel AA, Mikael S, et al. (2014) Graphene-based carbon-layered electrode array technology for neural imaging and optogenetic applications. Nat Commun 5: 5258.    

32. Ruardij TG, Goedbloed MH, Rutten WL (2000) Adhesion and patterning of cortical neurons on polyethylenimine- and fluorocarbon-coated surfaces. IEEE Trans Biomed Eng 47: 1593-1599.    

33. Marom S, Shahaf G (2002) Development, learning and memory in large random networks of cortical neurons: lessons beyond anatomy. Quarterly Reviews of Biophysics 35.

34. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671-675.    

35. Aras MA, Hartnett KA, Aizenman E (2008) Assessment of cell viability in primary neuronal cultures. Curr Protoc Neurosci Chapter 7: Unit 7 18.

36. Chan FK, Moriwaki K, De Rosa MJ (2013) Detection of necrosis by release of lactate dehydrogenase activity. Methods Mol Biol 979: 65-70.    

37. Linaro D, Couto J, Giugliano M (2014) Command-line cellular electrophysiology for conventional and real-time closed-loop experiments. J Neurosci Methods 230: 5-19.    

38. Ferrari AC, Robertson J (2000) Interpretation of Raman spectra of disordered and amorphous carbon. Physical Review B 61: 14095-14107.    

39. Ferrari AC, Robertson J (2001) Resonant Raman spectroscopy of disordered, amorphous, and diamondlike carbon. Physical Review B 64.

40. Ferrari AC (2007) Raman spectroscopy of graphene and graphite: Disorder, electron-phonon coupling, doping and nonadiabatic effects. Solid State Communications 143: 47-57.    

41. Stankovich S, Dikin DA, Piner RD, et al. (2007) Synthesis of graphene-based nanosheets via chemical reduction of exfoliated graphite oxide. Carbon 45: 1558-1565.    

42. Cui P, Lee J, Hwang E, et al. (2011) One-pot reduction of graphene oxide at subzero temperatures. Chem Commun (Camb) 47: 12370-12372.    

43. Andre Mkhoyan K, Contryman AW, Silcox J, et al. (2009) Atomic and electronic structure of graphene-oxide. Nano Lett 9: 1058-1063.    

44. Paredes JI, Villar-Rodil S, Solis-Fernandez P, et al. (2009) Atomic force and scanning tunneling microscopy imaging of graphene nanosheets derived from graphite oxide. Langmuir 25: 5957-5968.    

45. Li D, Muller MB, Gilje S, et al. (2008) Processable aqueous dispersions of graphene nanosheets. Nat Nanotechnol 3: 101-105.    

46. Li M-j, Liu C-m, Xie Y-b, et al. (2014) The evolution of surface charge on graphene oxide during the reduction and its application in electroanalysis. Carbon 66: 302-311.    

47. Tu Q, Pang L, Chen Y, et al. (2014) Effects of surface charges of graphene oxide on neuronal outgrowth and branching. Analyst 139: 105-115.    

48. Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8: 451-465.    

49. Lovat V, Pantarotto D, Lagostena L, et al. (2005) Carbon nanotube substrates boost neuronal electrical signaling. Nano Lett 5: 1107-1110.    

50. Tang M, Song Q, Li N, et al. (2013) Enhancement of electrical signaling in neural networks on graphene films. Biomaterials 34: 6402-6411.    

51. Giugliano M, Darbon P, Arsiero M, et al. (2004) Single-neuron discharge properties and network activity in dissociated cultures of neocortex. J Neurophysiol 92: 977-996.    

52. Biffi E, Regalia G, Menegon A, et al. (2013) The influence of neuronal density and maturation on network activity of hippocampal cell cultures: a methodological study. PLoS One 8: e83899.    

53. Wagenaar DA, Pine J, Potter SM (2006) An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neurosci 7: 11.    

54. Cohen E, Ivenshitz M, Amor-Baroukh V, et al. (2008) Determinants of spontaneous activity in networks of cultured hippocampus. Brain Res 1235: 21-30.    

55. Turrigiano GG, Leslie KR, Desai NS, et al. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391: 892-896.    

56. Cullen DK, Gilroy ME, Irons HR, et al. (2010) Synapse-to-neuron ratio is inversely related to neuronal density in mature neuronal cultures. Brain Res 1359: 44-55.    

Copyright Info: © 2015, Michele Giugliano, et al., licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

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