Carbon nanotube scaffolds tune synaptic strength in cultured neural circuits: Novel frontiers in nanomaterial-tissaue interactions

Journal of Neuroscience

Volumn 31, Issue 36, 2011, Pages 12945-12953

  Cellot, Giada ^a   Toma, Francesca Maria ^a   Varley, Zeynep Kasap ^b   Laishram, Jummi ^a   Villari, Ambra ^a   Quintana, Mildred ^a   Cipollone, Sara ^a   Prato, Maurizio ^a   Ballerini, Laura ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

^b SISSA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MULTI WALLED NANOTUBE; NANOMATERIAL; TISSUE SCAFFOLD;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL FUNCTION; CELL MEMBRANE; CONTROLLED STUDY; INTRACELLULAR RECORDING; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROSCIENCE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION; TISSUE ENGINEERING; TISSUE INTERACTION; TISSUE REGENERATION; TISSUE REPAIR;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; CEREBRAL CORTEX; ELECTROPHYSIOLOGICAL PHENOMENA; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NANOSTRUCTURES; NANOTUBES, CARBON; NERVE NET; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; SYNAPSES; THERMOGRAVIMETRY; TISSUE SCAFFOLDS;

EID: 80052589030     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1332-11.2011     Document Type: Article

References (63)

1. Abbott LF, Varela JA, Sen K, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275:220-224
2. Atwood HL, Karunanithi S (2002) Diversification of synaptic strength: presynaptic elements. Nat Rev Neurosci 3:497-516.
3. Avossa D, Rosato-Siri MD, Mazzarol F, Ballerini L (2003) Spinal circuits formation: a study of developmentally regulated markers in organotypic cultures of embryonic mouse spinal cord. Neuroscience 122:391-405.
4. Basarsky TA, Parpura V, Haydon PG (1994) Hippocampal synaptogenesis in cell culture: developmental time course of synapse formation, calcium influx, and synaptic protein distribution. J Neurosci 14:6402-6411.
5. Berardi N, Pizzorusso T, Maffei L (2004) Extracellular matrix and visual cortical plasticity: freeing the synapse. Neuron 44:905-908.
6. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472.
7. Bolton MM, Pittman AJ, Lo DC (2000) Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. J Neurosci 20:3221-3232.
8. Cellot G, Cilia E, Cipollone S, Rancic V, Sucapane A, Giordani S, Gambazzi L, Markram H, Grandolfo M, Scaini D, Gelain F, Casalis L, Prato M, Giugliano M, Ballerini L (2009) Carbon nanotubes might improve neuronal performance by favouring electrical shortcuts. Nat Nanotechnol 4: 126-133.
9. Cellot G, Ballerini L, Prato M, Bianco A (2010) Neurons are able to internalize soluble carbon nanotubes: new opportunities or old risks? Small 6:2630-2633.
10. Chudotvorova I, Ivanov A, Rama S, Hübner CA, Pellegrino C, Ben-Ari Y, Medina I (2005) Early expression of KCC2 in rat hippocampal cultures augments expression of functional GABA synapses. J Physiol 566:671-679.
11. Cui H, Webber MJ, Stupp SI (2010) Self-assembly of peptide amphiphiles: from molecules to nanostructures to biomaterials. Biopolymers 94:1-18.
12. Dan Y, Poo MM (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44:23-30.
13. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147-6162.
14. Dittman JS, Kreitzer AC, Regehr WG (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20:1374-1385.
15. Dityatev A, Brückner G, Dityateva G, Grosche J, Kleene R, Schachner M (2007) Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev Neurobiol 67:570-588.
16. Dumoulin A, Lévi S, Riveau B, Gasnier B, Triller A (2000) Formation of mixed glycine and GABAergic synapses in cultured spinal cord neurons. Eur J Neurosci 12:3883-3892.
17. Dvir T, Timko BP, Kohane DS, Langer R (2011) Nanotechnological strategies for engineering complex tissues. Nat Nanotechnol 6:13-22.
18. Ellis-Behnke RG, Liang YX, You SW, Tay DK, Zhang S, So KF, Schneider GE (2006) Nano neuro knitting: peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. Proc Natl Acad Sci U S A 103:5054-5059.
19. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12:897-904.
20. Galante M, Nistri A, Ballerini L (2000) Opposite changes in synaptic activity of organotypic rat spinal cord cultures after chronic block of AMPA/ kainate or glycine and GABAA receptors. J Physiol 523:639-651.
21. Galvan-Garcia P, Keefer EW, Yang F, Zhang M, Fang S, Zakhidov AA, Baughman RH, Romero MI (2007) Robust cell migration and neuronal growth on pristine carbon nanotube sheets and yarns. J Biomater Sci Polym Ed 18:1245-1261.
22. Geller HM, Fawcett JW (2002) Building a bridge: engineering spinal cord repair. Exp Neurol 174:125-136.
23. Georgakilas V, Voulgaris D, Vázquez E, Prato M, Guldi DM, Kukovecz A, Kuzmany H (2002) Purification of HiPCO carbon nanotubes via organic functionalization. J Am Chem Soc 124:14318-14319.
24. Hu H, Ni Y, Mandal SK, Montana V, Zhao B, Haddon RC, Parpura V (2005) Polyethyleneimine functionalized single-walled carbon nanotubes as a substrate for neuronal growth. J Phys Chem B 109:4285-4289.
25. Ivenshitz M, Segal M (2010) Neuronal density determines network connec-tivity and spontaneous activity in cultured hippocampus. J Neurophysiol 104:1052-1060.
26. Jensen K, Lambert JD, Jensen MS (1999) Activity-dependent depression of GABAergic IPSCs in cultured hippocampal neurons. J Neurophysiol 82:42-49.
27. Kasap Varley Z, Pizzarelli R, Antonelli R, Stancheva SH, Kneussel M, Cherubini E, Zacchi P (2011) Gephyrin regulates GABAergic and glutamatergic synaptic transmission in hippocampal cell cultures. J Biol Chem 286:20942-20951.
28. Keefer EW, Botterman BR, Romero MI, Rossi AF, Gross GW (2008) Carbon nanotube coating improves neuronal recordings. Nat Nanotechnol 3:434-439.
29. Kotov NA, Winter JO, Clements IP, Jan E, Timko BP, Campidelli S, Pathak S, Mazzatenta A, Lieber CM, Prato M, Bellamkonda RV, Silva GA, Shi Kam NW, Patolsky F, Ballerini L (2009) Nanomaterials for neural interfaces. Adv Mater 21:3970-4004.
30. Kuczewski N, Porcher C, Ferrand N, Fiorentino H, Pellegrino C, Kolarow R, Lessmann V, Medina I, Gaiarsa JL (2008) Backpropagating action potentials trigger dendritic release of BDNF during spontaneous network activity. J Neurosci 28:7013-7023.
31. Lovat V, Pantarotto D, Lagostena L, Cacciari B, Grandolfo M, Righi M, Spalluto G, Prato M, Ballerini L (2005) Carbon nanotube substrates boost neuronal electrical signaling. Nano Lett 5:1107-1110.
32. Marchionni I, Kasap Z, Mozrzymas JW, Sieghart W, Cherubini E, Zacchi P (2009) New insights on the role of gephyrin in regulating both phasic and tonic GABAergic inhibition in rat hippocampal neurons in culture. Neuroscience 164:552-562.
33. Markram H, Lübke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
34. Mattson MP, Haddon RC, Rao AM (2000) Molecular functionalization of carbon nanotubes and use as substrates for neuronal growth. J Mol Neurosci 14:175-182.
35. Mazzatenta A, Giugliano M, Campidelli S, Gambazzi L, Businaro L, Markram H, Prato M, Ballerini L (2007) Interfacing neurons with carbon nanotubes: electrical signal transfer and synaptic stimulation in cultured brain circuits. J Neurosci 27:6931-6936.
36. Melnick IV, Chvanov MA, Belan PV (1999) Rat hippocampal neurons maintain their own GABAergic synaptic transmission in culture. Neurosci Lett 262:151-154.
37. Miyata S, Nishimura Y, Hayashi N, Oohira A (2005) Construction of perineuronal net-like structure by cortical neurons in culture. Neuroscience 136:95-104.
38. Ni Y, Hu H, Malarkey EB, Zhao B, Montana V, Haddon RC, Parpura V (2005) Chemically functionalized water soluble single-walled carbon nanotubes modulate neurite outgrowth. J Nanosci Nanotechnol 5:1707-1712.
39. Orive G, Anitua E, Pedraz JL, Emerich DF (2009) Biomaterials for promoting brain protection, repair and regeneration. Nat Rev Neurosci 10:682-692.
40. Pavlidis P, Montgomery J, Madison DV (2000) Presynaptic protein kinase activity supports long-term potentiation at synapses between individual hippocampal neurons. J Neurosci 20:4497-4505.
41. Place ES, Evans ND, Stevens MM (2009) Complexity in biomaterials for tissue engineering. Nat Mater 8:457-470.
42. Plant GW, Woerly S, Harvey AR (1997) Hydrogels containing peptide or aminosugar sequences implanted into the rat brain: influence on cellular migration and axonal growth. Exp Neurol 143:287-299.
43. Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WA, Seaton A, Stone V, Brown S, Macnee W, Donaldson K (2008) Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol 3:423-428.
44. + currents in cultured hippocampal neurons from postnatal rats. Proc Biol Sci 264:367-373.
45. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337-351.
46. Raastad M, Storm JF, Andersen P (1992) Putative single quantum and single fibre excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur J Neurosci 4:113-117.
47. Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206-212.
48. SegalM (1983) Rat hippocampal neurons in culture: responses to electrical and chemical stimuli. J Neurophysiol 50:1249-1264.
49. Shoval A, Adams C, David-Pur M, Shein M, Hanein Y, Sernagor E (2009) Carbon nanotube electrodes for effective interfacing with retinal tissue. Front Neuroeng 2:1-8.
50. SilvaGA (2006) Neuroscience nanotechnology: progress, opportunities and challenges. Nat Rev Neurosci 7:65-74.
51. Silva GA (2009) Nanomedicine: shorting neurons with nanotubes. Nat Nanotechnol 4:82-83.
52. Singh B, Henneberger C, Betances D, Arevalo MA, Rodríguez-Tébar A, Meier JC, Grantyn R (2006) Altered balance of glutamatergic/GABAergic synaptic input and associated changes in dendrite morphology after BDNF expression in BDNF-deficient hippocampal neurons. J Neurosci 26:7189-7200.
53. Sucapane A, Cellot G, Prato M, Giugliano M, Parpura V, Ballerini L (2009) Interactions between cultured neurons and carbon nanotubes: a nanoneuroscience vignette. J Nanoneurosci 1:10-16.
54. Vittorio O, Raffa V, Cuschieri A (2009) Influence of purity and surface oxidation on cytotoxicity of multiwalled carbon nanotubes with human neuroblastoma cells. Nanomedicine 5:424-431.
55. Waters J, Schaefer A, Sakmann B (2005) Backpropagating action potentials in neurones: measurement, mechanisms and potential functions. Prog Biophys Mol Biol 87:145-170.
56. Wilcox KS, Buchhalter J, Dichter MA (1994) Properties of inhibitory and excitatory synapses between hippocampal neurons in very low density cultures. Synapse 18:128-151.
57. Woo KM, Chen VJ, Ma PX (2003) Nano-fibrous scaffolding architecture selectively enhances protein adsorption contributing to cell attachment. J Biomed Mater Res A 67:531-537.
58. Wu Z, Chen Z, Du X, Logan JM, Sippel J, Nikolou M, Kamaras K, Reynolds JR, Tanner DB, Hebard AF, Rinzler AG (2004) Transparent, conductive carbon nanotube films. Science 305:1273-1276.
59. Zhou X, Moran-Mirabal JM, Craighead HG, McEuen PL (2007) Supported lipid bilayer/carbon nanotube hybrids. Nat Nanotechnol 2:185-190.
60. Zilberter Y, Harkany T, Holmgren CD (2005) Dendritic release of retrograde messengers controls synaptic transmission in local neocortical networks. Neuroscientist 11:334-344.
61. Zsiros V, Aradi I, Maccaferri G (2007) Propagation of postsynaptic currents and potentials via gap junctions in GABAergic networks of the rat hippocampus. J Physiol 578:527-544.
62. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13-31.
63. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.