Functionalized carbon nanotubes in the brain: Cellular internalization and neuroinflammatory responses

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Bardi, Giuseppe ^a,b   Nunes, Antonio ^c,g   Gherardini, Lisa ^a,b   Bates, Katie ^c   Al Jamal, Khuloud T ^c,h   Gaillard, Claire ^d,i   Prato, Maurizio ^e   Bianco, Alberto ^d   Pizzorusso, Tommaso ^a,b,f   Kostarelos, Kostas ^c  

^a CNR   (Italy)

^b SCUOLA SUPERIORE SANT ANNA   (Italy)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^e UNIVERSITY OF TRIESTE   (Italy)

^f UNIVERSITY OF FLORENCE   (Italy)

^g INSTITUTE OF EPIDEMIOLOGY   (Germany)

^h KING'S COLLEGE LONDON   (United Kingdom)

ⁱ CEA SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CARBON NANOTUBE; CD11B ANTIGEN; CYTOKINE; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; NERVE PROTEIN;

ANIMAL; ASTROCYTE; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; FEMALE; GENE EXPRESSION; GENETICS; INFLAMMATION; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; MICROGLIA; MOUSE; NERVE CELL; OXIDATION REDUCTION REACTION; PATHOLOGY; STEREOTACTIC PROCEDURE; TOXICITY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ANTIGENS, CD11B; ASTROCYTES; BIOLOGICAL MARKERS; BIOLOGICAL TRANSPORT; BRAIN; CYTOKINES; FEMALE; GENE EXPRESSION; INFLAMMATION; INJECTIONS, INTRAVENTRICULAR; MICE; MICE, INBRED C57BL; MICROGLIA; NANOTUBES, CARBON; NERVE TISSUE PROTEINS; NEURONS; OXIDATION-REDUCTION; STEREOTAXIC TECHNIQUES;

EID: 84894074762     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080964     Document Type: Article

References (37)

1. Bjartmarz H, Rehncrona S (2007) Comparison of accuracy and precision between frame-based and frameless stereotactic navigation for deep brain stimulation electrode implantation. Stereot Funct Neuros 85: 235-242. (Pubitemid 47254536)
2. Fasano A, Daniele A, Albanese A (2012) Treatment of motor and non-motor features of Parkinson's disease with deep brain stimulation. The Lancet Neurology 11: 429-442
3. Gallina P, Paganini M, Di Rita A, Lombardini L, Moretti M et al. (2008) Human fetal striatal transplantation in huntington's disease: a refinement of the stereotactic procedure. Stereotact Funct Neurosurg 86: 308-313.
4. Kang GA, Heath S, Rothlind J, Starr PA (2011) Long-term follow-up of pallidal deep brain stimulation in two cases of Huntington's disease. J Neurol Neurosurg Psychiatry 82: 272-277.
5. Malarkey EB, Parpura V (2007) Applications of carbon nanotubes in neurobiology. Neurodegener Dis 4: 292-299. (Pubitemid 47026183)
6. Nunes A, Al-Jamal KT, Nakajima T, Hariz M, Kostarelos K (2012) Application of carbon nanotubes in neurology: clinical perspectives and toxicological risks. Arch Toxicol 869: 1009-1020.
7. Matsumoto K, Sato C, Naka Y, Kitazawa A, Whitby RLD et al. (2007) Neurite outgrowths of neurons with neurotrophin-coated carbon nanotubes. J Biosci Bioeng 103: 216-220. (Pubitemid 46552271)
8. Hu H, Ni Y, Montana V, Haddon RC, Parpura V (2004) Chemically functionalized carbon nanotubes as substrates for neuronal growth. Nano Lett 4: 507-511. (Pubitemid 38402642)
9. 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. (Pubitemid 30660807)
10. Cellot G, Cilia E, Cipollone S, Rancic V, Sucapane A et al. (2009) Carbon nanotubes might improve neuronal performance by favouring electrical shortcuts. Nat Nanotechnol 4: 126-133.
11. Al-Jamal KT, Gherardini L, Bardi G, Nunes A, Guo C et al. (2011) Functional motor recovery from brain ischemic insult by carbon nanotube-mediated siRNA silencing. Proc Natl Acad Sci U S A 108: 10952-109597.
12. Lee HJ, Park J, Yoon OJ, Kim HW, Lee do Yet al. (2011) Amine-modified single-walled carbon nanotubes protect neurons from injury in a rat stroke model. Nat Nanotechnol 6: 121-125.
13. Roman JA, Niedzielko TL, Haddon RC, Parpura V, Floyd CL (2011) Single-walled carbon nanotubes chemically functionalized with polyethylene glycol promote tissue repair in a rat model of spinal cord injury. J Neurotrauma 28: 2349-2362.
14. Zhao DC, Alizadeh D, Zhang LY, Liu W, Farrukh O et al. (2011) Carbon nanotubes enhance CpG uptake and potentiate antiglioma immunity. Clin Cancer Res 17: 771-782.
15. Bardi G, Tognini P, Ciofani G, Raffa V, Costa M et al. (2009) Pluronic-coated carbon nanotubes do not induce degeneration of cortical neurons in vivo and in vitro. Nanomedicine 5: 96-104.
16. Nunes A, Bussy C, Gherardini L, Meneghetti M, Herrero MA et al. (2012) In vivo degradation of functionalized carbon nanotubes after stereotactic administration in the brain cortex. Nanomedicine 7: 1485-1494.
17. Georgakilas V, Kordatos K, Prato M, Guldi DM, Holzinger M et al. (2002) Organic functionalization of carbon nanotubes. J Am Chem Soc 124: 760-761. (Pubitemid 34112779)
18. Gaillard C, Cellot G, Li S, Toma FM, Dumortier H et al. (2009) Carbon nanotubes carrying cell-adhesion peptides do not interfere with neuronal functionality. Adv Mat 21: 2903-2908.
19. Al-Jamal KT, Nunes A, Methven L, Ali-Boucetta H, Li SP et al. (2012) Degree of chemical functionalization of carbon nanotubes determines tissue distribution and excretion profile. Angew Chem Int Edit 51: 6389-6393.
20. Ransohoff RM, Perry VH (2009) Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27: 119-145.
21. Metcalfe DD, Baram D, Mekori YA (1997) Mast cells. Physiol Rev 77: 1033-1079. (Pubitemid 27459579)
22. Purcell WM, Atterwill CK (1995) Mast-cells in neuroimmune function - neurotoxicological and neuropharmacological perspectives. Neurochem Res 20: 521-532.
23. Sayes CM, Liang F, Hudson JL, Mendez J, Guo WH et al. (2006) Functionalization density dependence of single-walled carbon nanotubes cytotoxicity in vitro. Toxicol Lett 161: 135-142. (Pubitemid 41790286)
24. Murphy FA, Poland CA, Duffin R, Al-Jamal KT, Ali-Boucetta H et al. (2011) Length-dependent retention of carbon nanotubes in the pleural space of mice initiates sustained inflammation and progressive fibrosis on the parietal pleura. Am J Pathol 178: 2587-2600.
25. Podesta JE, Al-Jamal KT, Herrero MA, Tian BW, Ali-Boucetta H et al. (2009) Antitumor activity and prolonged survival by carbon-nanotube-mediated therapeutic siRNA silencing in a human lung xenograft model. Small 5: 1176-1185.
26. 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.
27. Perez-Martinez FC, Guerra J, Posadas I, Cena V (2011) Barriers to non-viral vector-mediated gene delivery in the nervous system. Pharm Res 28: 1843-1845.
28. Khalil IA, Kogure K, Akita H, Harashima H (2006) Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol Rev 58: 32-45.
29. Kostarelos K, Lacerda L, Pastorin G, Wu W, Wieckowski S et al. (2007) Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type. Nat Nanotechnol 2: 108-113. (Pubitemid 46230832)
30. Kateb B, Van Handel M, Zhang LY, Bronikowski MJ, Manohara H et al. (2007) Internalization of MWCNTs by microglia: possible application in immunotherapy of brain tumors. Neuroimage 37: S9-S17. (Pubitemid 47239427)
31. Mu QX, Broughton DL, Yan B (2009) Endosomal leakage and nuclear translocation of multiwalled carbon nanotubes: developing a model for cell uptake. Nano Lett 9: 4370-4375.
32. Al-Jamal KT, Nerl H, Muller KH, Ali-Boucetta H, Li S et al. (2011) Cellular uptake mechanisms of functionalised multi-walled carbon nanotubes by 3D electron tomography imaging. Nanoscale 3: 2627-2635.
33. Lacerda L, Russier J, Pastorin G, Herrero MA, Venturelli E et al. (2012) Translocation mechanisms of chemically functionalised carbon nanotubes across plasma membranes. Biomaterials 33: 3334-3343.
34. Shih AY, Fernandes HB, Choi FY, Kozoriz MG, Liu YR et al. (2006) Policing the police: astrocytes modulate microglial activation. J Neurosci 26: 3887-3888. (Pubitemid 44315407)
35. Streit WJ, Walter SA, Pennell NA (1999) Reactive microgliosis. Prog Neurobiol 57: 563-581. (Pubitemid 29148415)
36. Roy A, Fung YK, Liu XJ, Pahan K (2006) Up-regulation of microglial CD11b expression by nitric oxide. J Biol Chem 281: 14971-14980. (Pubitemid 43855201)
37. Banati RB (2003) Neuropathological Imaging: in vivo detection of glial activation as a measure of disease and adaptive change in the brain. Br Med Bull 65: 121-131.