Insight on the fate of CNS-targeted nanoparticles. Part II: Intercellular neuronal cell-to-cell transport

Journal of Controlled Release

Volumn 177, Issue 1, 2014, Pages 96-107

  Tosi, Giovanni ^a   Vilella, Antonietta ^a   Chhabra, Resham ^b   Schmeisser, Michael J ^b   Boeckers, Tobias M ^b   Ruozi, Barbara ^a   Vandelli, Maria Angela ^a   Forni, Flavio ^a   Zoli, Michele ^a   Grabrucker, Andreas M ^b  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

g7 NPs; M Sec; Neuron; TNT; Tunneling nanotubes

Indexed keywords

ANTIBODIES; CELL CULTURE; MAMMALS; NANOPARTICLES; NANOTUBES; NEURONS; TARGETED DRUG DELIVERY;

BLOOD-BRAIN BARRIER; CENTRAL NERVOUS SYSTEMS; GLYCOPEPTIDES; M-SEC; POLY-LACTIDE-CO-GLYCOLIDE; POLYMERIC NANOPARTICLES; POSSIBLE MECHANISMS; TARGETED NANOPARTICLE;

CELLS;

F ACTIN; GLYCOPEPTIDE; GLYCOPEPTIDE NANOPARTICLE; NANOPARTICLE; NANOTUBE; POLYGLACTIN; POLYLACTIDE CO GLYCOLIDE NANOPARTICLE; TUNNELING NANOTUBE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; CELL COMMUNICATION; CELL FATE; CELL LINE; CELL TRANSPORT; CELL VACUOLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; EMBRYO; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; MOUSE; NERVE CELL; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; RAT; SURFACE PROPERTY;

G7-NPS; M-SEC; NEURON; TNT; TUNNELING NANOTUBES;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; ANTIGENS, CD44; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; EMBRYO, MAMMALIAN; GLYCOPEPTIDES; HIPPOCAMPUS; LACTIC ACID; MICE, INBRED C57BL; NANOPARTICLES; NEURAL CELL ADHESION MOLECULES; NEUROGLIA; NEURONS; POLYGLYCOLIC ACID; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84893937925     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.01.004     Document Type: Article

References (84)

1. A.V. Lorenzo, E.T. Hedley-Whyte, and J.M. Eisenberg Increased penetration of horseradish peroxidase across the blood-brain barrier induced by Metrazol seizures Brain Res. 88 1975 136 140
2. E.A. Neuwelt, and S.A. Dahlborg Blood-brain barrier disruption in the treatment of brain tumors: clinical implications E.A. Neuwelt, Implications of the blood brain barrier and its manipulation: clinical aspects vol. 2 1989 Plenum New York 195 262
3. N. Bodor, and P. Buchwald Drug targeting via retrometabolic approaches Pharmacol. Ther. 76 1997 1 27 (Pubitemid 28078557)
4. G. Somogyi, S. Nishitani, D. Nomi, P. Buchwald, L. Prokai, and N. Bodor Targeted drug delivery to the brain via phosphonate derivatives. I: design, synthesis, and evaluation of an anionic chemical delivery system for testosterone Int. J. Pharm. 166 1998 15 26 (Pubitemid 28239735)
5. S. Bahadur, and K. Pathak Physicochemical and physiological considerations for efficient nose-to-brain targeting Expert Opin. Drug Deliv. 9 1 2012 19 31
6. D.I. Sandberg, M.H. Bilsky, M.M. Souweidane, J. Bzdill, and P.H. Gutin Ommaya reservoirs for the treatment of leptomeningeal metastases Neurosurgery 47 1 2000 49 54
7. L. Juillerat-Jeanneret The targeted delivery of cancer drugs across the blood-brain barrier: chemical modifications of drugs or drug-nanoparticles? Drug Discov. Today 13 23-24 2008 1099 1106
8. A. Beduneau, P. Saulnier, and J.P. Benoit Active targeting of brain tumors using nanocarriers Biomaterials 28 2007 4947 4967 (Pubitemid 47362345)
9. S. Wohlfart, S. Gelperina, and J. Kreuter Transport of drugs across the blood-brain barrier by nanoparticles J. Control. Release 161 2012 264 273
10. Y.C. Chen, W.Y. Hsieh, W.F. Lee, and D.T. Zeng Effects of surface modification of PLGA-PEG-PLGA nanoparticles on loperamide delivery efficiency across the blood-brain barrier J. Biomater. Appl. 2011 10.1177/0885328211429495
11. K. Tahara, Y. Miyazaki, Y. Kawashima, J. Kreuter, and H. Yamamoto Brain targeting with surface-modified poly(d, l-lactic-co-glycolic acid) nanoparticles delivered via carotid artery administration Eur. J. Pharm. Biopharm. 77 2011 84 88
12. W. Sun, C. Xie, H. Wang, and Y. Hu Specific role of polysorbate 80 coating on the targeting of nanoparticles to the brain Biomaterials 25 2004 3065 3071 (Pubitemid 38210199)
13. T. Parikh, M.M. Bommana, and E. Squillante III Efficacy of surface charge in targeting pegylated nanoparticles of sulpiride to the brain Eur. J. Pharm. Biopharm. 74 2010 442 450
14. J. Li, L. Feng, L. Fan, Y. Zha, L. Guo, Q. Zhang, J. Chen, Z. Pang, Y. Wang, X. Jiang, V.C. Yang, and L. Wen Targeting the brain with PEG-PLGA nanoparticles modified with phage-displayed peptides Biomaterials 32 2011 4943 4950
15. H.L. Wong, S.Y. Wu, and R. Bendayan Nanotechnological advances for the delivery of CNS therapeutics Adv. Drug Deliv. Rev. 64 2012 686 700
16. E. Garcia-Garcia, K. Andrieux, and S. Gil et al. Colloidal carriers and blood-brain barrier (BBB) translocation: a way to deliver drugs to the brain? Int. J. Pharm. 298 2007 274 923
17. I. van Rooy, E. Mastrobattista, G. Storm, W.E. Hennink, and R.M. Schiffelers Comparison of five different targeting ligands to enhance accumulation of liposomes into the brain J. Control. Release 150 2011 30 36
18. G. Tosi, L. Bondioli, B. Ruozi, L. Badiali, G.M. Severini, S. Biffi, A. De Vita, B. Bortot, D. Dolcetta, F. Forni, and M.A. Vandelli NIR-labeled nanoparticles engineered for brain targeting: in vivo optical imaging application and fluorescent microscopy evidences J. Neural Transm. 118 2011 145 153
19. G. Tosi, R.A. Fano, L. Bondioli, L. Badiali, R. Benassi, F. Rivasi, B. Ruozi, F. Forni, and M.A. Vandelli Investigation on the mechanisms for Blood-Brain Barrier crossing of brain-targeted glycopeptides nanoparticles Nanomedicine 6 3 2011 423 436
20. G. Tosi, A.V. Vergoni, B. Ruozi, L. Bondioli, L. Badiali, F. Rivasi, L. Costantino, F. Forni, and M.A. Vandelli Sialic-acid and glycopeptides conjugated PLGA nanoparticles for Central Nervous System targeting: in vivo pharmacological evidence and biodistribution J. Control. Release 145 2010 49 57
21. G. Tosi, L. Costantino, F. Rivasi, B. Ruozi, E. Leo, A.V. Vergoni, R. Tacchi, A. Bertolini, M.A. Vandelli, and F. Forni Targeting CNS: in vivo experiments with peptide derivatized nanoparticles loaded with Loperamide and Rhodamine 123 J. Control. Release 122 2007 1 9 (Pubitemid 47284547)
22. G. Tosi, L. Costantino, B. Ruozi, F. Forni, and M.A. Vandelli Polymeric nanoparticles for the drug delivery to the Central Nervous System Expert Opin. Drug Deliv. 5 2008 155 174 (Pubitemid 351308309)
23. A.V. Vergoni, G. Tosi, R. Tacchi, M.A. Vandelli, A. Bertolini, and L. Costantino Nanoparticles as drug delivery agents specific for CNS: in vivo biodistribution Nanomedicine: NBM 5 2009 369 377
24. L. Costantino, F. Gandolfi, G. Tosi, F. Rivasi, M.A. Vandelli, and F. Forni Peptide-derivatized biodegradable nanoparticles able to cross the blood brain barrier J. Control. Release 108 2005 84 96 (Pubitemid 41476677)
25. G. Tosi, B. Ruozi, D. Belletti, A. Vilella, M. Zoli, M.A. Vandelli, and F. Forni Brain-targeted polymeric nanoparticles: in vivo evidences after different routes of administration in rodents Nanomedicine (Lond) 8 9 2013 1373 1383
26. A.M. Grabrucker, C.C. Garner, T.M. Boeckers, L. Bondioli, B. Ruozi, F. Forni, M.A. Vandelli, and G. Tosi Development of novel Zn2 + loaded nanoparticles designed for cell-type targeted drug release in CNS neurons: in vitro evidences PLoS One 6 2011 e17851
27. A. Vilella, G. Tosi, A.M. Grabrucker, B. Ruozi, D. Belletti, M.A. Vandelli, T.M. Boeckers, F. Forni, and M. Zoli Insight on the fate of CNS-targeted nanoparticles. Part I: Rab5-dependent cell-specific uptake and distribution J. Control. Release 174C 2014 195 201
28. S. Gurke, J.F. Barroso, and H.H. Gerdes The art of cellular communication: tunneling nanotubes bridge the divide Histochem. Cell Biol. 129 5 2008 539 550
29. K. He, W. Luo, Y. Zhang, F. Liu, D. Liu, L. Xu, L. Qin, C. Xiong, Z. Lu, X. Fang, and Y. Zhang Intercellular transportation of quantum dots mediated by membrane nanotubes ACS Nano 4 6 2010 3015 3022
30. K. Gousset, E. Schiff, C. Langevin, Z. Marijanovic, A. Caputo, D.T. Browman, N. Chenouard, F. de Chaumont, A. Martino, J. Enninga, J.C. Olivo-Marin, D. Männel, and C. Zurzolo Prions hijack tunnelling nanotubes for intercellular spread Nat. Cell Biol. 11 2009 328 336
31. I. Spector, N.R. Schochet, D. Blasberger, and Y. Kashman Latrunculins - novel marine macrolides that disrupt microfilament organization and affect cell growth: I. comparison with cytochalasin D Cell Motil. Cytoskeleton 13 1989 127 144 (Pubitemid 19197366)
32. H. Ohno, K. Hase, and S. Kimura M-Sec: emerging secrets of tunneling nanotube formation Commun. Integr. Biol. 3 3 2010 231 233
33. L. Bondioli, L. Costantino, A. Ballestrazzi, D. Lucchesi, D. Boraschi, F. Pellati, S. Benvenuti, G. Tosi, and M.A. Vandelli PLGA nanoparticles surface decorated with the sialic acid, N-acetylneuraminic acid Biomaterials 31 2010 3395 3403
34. M.D. Blanco, and M.J. Alonso Development and characterization of protein-loaded poly(lactide-co-glycolide) nanospheres Eur. J. Pharm. Biopharm. 43 1997 287 294
35. J.C. Olivier, R. Huertas, H.J. Lee, F. Calon, and W.M. Pardridge Synthesis of pegylated immunonanoparticles Pharm. Res. 19 2002 1137 1143 (Pubitemid 34984997)
36. Y. Liu, K. Li, B. Liu, and S.S. Feng A strategy for precision engineering of nanoparticles of biodegradable copolymers for quantitative control of targeted drug delivery Biomaterials 31 2010 9145 9155
37. G. Banker, and K. Goslin Developments in neuronal cell culture Nature 336 6195 1988 185 186
38. A. Grabrucker, B. Vaida, J. Bockmann, and T.M. Boeckers Synaptogenesis of hippocampal neurons in primary cell culture Cell Tissue Res. 338 3 2009 333 341
39. C. Lois, E.J. Hong, S. Pease, E.J. Brown, and D. Baltimore Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors Science 295 5556 2002 868 872 (Pubitemid 34118370)
40. N.M. Sherer, M.J. Lehmann, L.F. Jimenez-Soto, C. Horensavitz, M. Pypaert, and W. Mothes Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission Nat. Cell Biol. 9 3 2007 310 315 (Pubitemid 46344610)
41. H.R. Chinnery, E. Pearlman, and P.G. Mcmenamin Cutting edge: membrane nanotubes in vivo: a feature of MHC class II + cells in the mouse cornea J. Immunol. 180 9 2008 5779 5783
42. S. Kimura, K. Hase, and H. Ohno Tunneling nanotubes: emerging view of their molecular components and formation mechanisms Exp. Cell Res. 318 14 2012 1699 1706
43. J. Panyam, W.Z. Zhou, S. Prabha, S.K. Sahoo, and V. Labhasetwar Rapid endo-lysosomal escape of poly(DL-lactide-co-glycolide) nanoparticles: implications for drug and gene delivery FASEB J. 16 10 2002 1217 1226 (Pubitemid 34815409)
44. J. Panyam, and V. Labhasetwar Dynamics of endocytosis and exocytosis of poly(d, l-lactide-co-glycolide) nanoparticles in vascular smooth muscle cells Pharm. Res. 20 2 2003 212 220 (Pubitemid 36277684)
45. Y. Feng, S. Yu, T.K. Lasell, A.P. Jadhav, E. Macia, P. Chardin, P. Melancon, M. Roth, T. Mitchison, and T. Kirchhausen Exo1: a new chemical inhibitor of the exocytic pathway Proc. Natl. Acad. Sci. U. S. A. 100 11 2003 6469 6474 (Pubitemid 36666605)
46. K. Hase, S. Kimura, H. Takatsu, M. Ohmae, S. Kawano, H. Kitamura, M. Ito, H. Watarai, C.C. Hazelett, C. Yeaman, and H. Ohno M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex Nat. Cell Biol. 11 12 2009 1427 1432
47. T.E. Buchheit, and M. Tytell Transfer of molecules from glia to axon in the squid may be mediated by glial vesicles J. Neurobiol. 23 3 1992 217 230
48. K. Fuxe, A.B. Dahlström, G. Jonsson, D. Marcellino, M. Guescini, M. Dam, P. Manger, and L. Agnati The discovery of central monoamine neurons gave volume transmission to the wired brain Prog. Neurobiol. 90 2 2010 82 100
49. G.M. Fedorenko, and A.B. Uzdensky Nissl substance and cellular structures involved in the intraneuronal and neuroglial transport in the crayfish stretch receptor A. Méndez-Vilas, J. Díaz, Microscopy: Science, Technology, Applications and Education vol. 4 2010 299 306
50. M.J. Haney, Y. Zhao, S. Li, S.M. Higginbotham, S.L. Booth, H.Y. Han, J.A. Vetro, R.L. Mosley, A.V. Kabanov, H.F. Gendelman, and E.V. Batrakova Cell-mediated transfer of catalase nanoparticles from macrophages to brain endothelial, glial and neuronal cells Nanomedicine (Lond) 6 7 2011 1215 1230
51. G.H. Hansen, K. Rasmussen, L.L. Niels-Christiansen, and E.M. Danielsen Endocytic trafficking from the small intestinal brush border probed with FM dye Am. J. Physiol. Gastrointest. Liver Physiol. 297 4 2009 G708 G715
52. K.Y. Win, and S.S. Feng Effects of particle size and surface coating on cellular uptake of polymeric nanoparticles for oral delivery of anticancer drugs Biomaterials 26 2005 2713 2722
53. A. Rustom, R. Saffrich, I. Markovic, P. Walther, and H.H. Gerdes Nanotubular highways for intercellular organelle transport Science 303 5660 2004 1007 1010 (Pubitemid 38209703)
54. B. Pontes, N.B. Viana, L. Campanati, M. Farina, V.M. Neto, and H.M. Nussenzveig Structure and elastic properties of tunneling nanotubes Eur. Biophys. J. 37 2 2008 121 129
55. H.H. Gerdes, N.V. Bukoreshtliev, and J.F. Barroso Tunneling nanotubes: a new route for the exchange of components between animal cells FEBS Lett. 581 2007 2194 2201 (Pubitemid 46709910)
56. H.H. Gerdes, and R.N. Carvalho Intercellular transfer mediated by tunneling nanotubes Curr. Opin. Cell Biol. 20 2008 470 475
57. B. Önfelt, S. Nedvetzki, K. Yanagi, and D.M. Davis Cutting edge: membrane nanotubes connect immune cells J. Immunol. 173 3 2004 1511 1513 (Pubitemid 38971579)
58. B.D. Chithrani, and W.C. Chan Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes Nano Lett. 7 6 2007 1542 1550 (Pubitemid 47140422)
59. Y. Wang, J. Cui, X. Sun, and Y. Zhang Tunneling-nanotube development in astrocytes depends on p53 activation Cell Death Differ. 18 4 2011 732 742
60. M.S. Shive, and J.M. Anderson Biodegradation and biocompatibility of PLA and PLGA microspheres Adv. Drug Deliv. Rev. 28 1997 5 24 (Pubitemid 27497671)
61. M.N. Cordonnier, D. Dauzonne, D. Louvard, and E. Coudrier Actin filaments and myosin I alpha cooperate with microtubules for the movement of lysosomes Mol. Biol. Cell 12 2001 4013 4029 (Pubitemid 34001089)
62. K. Gousset, and C. Zurzolo Tunnelling nanotubes: a highway for prion spreading? Prion 3 2 2009 94 98
63. L. Marzo, K. Gousset, and C. Zurzolo Multifaceted roles of tunneling nanotubes in intercellular communication Front. Physiol. 3 2012 72
64. X. Wang, N.V. Bukoreshtliev, and H.H. Gerdes Developing neurons form transient nanotubes facilitating electrical coupling and calcium signaling with distant astrocytes PLoS One 7 10 2012 e47429
65. P. Tuma, and A.L. Hubbard Transcytosis: crossing cellular barriers Physiol. Rev. 83 3 2003 871 932 (Pubitemid 36833216)
66. P.A. Stewart Endothelial vesicles in the blood-brain barrier: are they related to permeability? Cell. Mol. Neurobiol. 20 2 2000 149 163 (Pubitemid 30091453)
67. S. Nath, L. Angholme, F.R. Kurudenkandy, B. Granseth, J. Marcusson, and M. Hallbeck Spreading of neurodegenerative pathology via neuron-to-neuron transmission of β-amyloid J. Neurosci. 32 26 2012 8767 8777
68. H.H. Gerdes, A. Rustom, and X. Wang Tunneling nanotubes, an emerging intercellular communication route in development Mech. Dev. 130 2013 381 387
69. C. Frühbeis, D. Fröhlich, and E.M. Krämer-Albers Emerging roles of exosomes in neuron-glia communication Front. Physiol. 3 2012 119
70. M.J. Wood, A.J. O'Loughlin, and L. Samira Exosomes and the blood-brain barrier: implications for neurological diseases Ther. Deliv. 2 9 2011 1095 1099
71. J. Chang, A. Paillard, C. Passirani, M. Morille, J.P. Benoit, D. Betbeder, and E. Garcion Transferrin adsorption onto PLGA nanoparticles governs their interaction with biological systems from blood circulation to brain cancer cells Pharm. Res. 29 6 2012 1495 1505
72. J. Chang, Y. Jallouli, M. Kroubi, X.B. Yuan, W. Feng, C.S. Kang, P.Y. Pu, and D. Betbeder Characterization of endocytosis of transferrin-coated PLGA nanoparticles by the blood-brain barrier Int. J. Pharm. 379 2 2009 285 292
73. J.P. Gorvel, P. Chavrier, M. Zerial, and J. Gruenberg Rab5 controls early endosome fusion in vitro Cell 64 5 1991 915 925 (Pubitemid 121001179)
74. B. Kalmár, A. Kittel, R. Lemmens, Z. Környei, and E. Madarász Cultured astrocytes react to LPS with increased cyclooxygenase activity and phagocytosis Neurochem. Int. 38 5 2001 453 461 (Pubitemid 32166903)
75. G. Guillemin, F.D. Boussin, J. Croitoru, M. Franck-Duchenne, R. Le-Grand, F. Lazarini, and D. Dormont Obtention and characterisation of primary astrocyte and microglial cultures from adult monkey brains J. Neurosci. Res. 49 5 1997 576 591 (Pubitemid 27381245)
76. L. Rinaman, C.E. Milligan, and P. Levitt Persistence of fluorogold following degeneration of labelled motoneurons is due to phagocytosis by microglia and macrophages Neuroscience 44 3 1991 765 776
77. J. Saura Microglial cells in astroglial cultures: a cautionary note J. Neuroinflammation 4 2007 26
78. 3H]glutamate by primary astrocyte cultures. II. Differences in cultures prepared from different brain regions Glia 6 1992 9 18
79. J.T. Rutka, J.R. Giblin, R. Balkissoon, D. Wen, C.A. Myatt, J.R. McCulloch, and M.L. Rosenblum Characterization of fetal human brain cultures. Development of a potential model for selectively purifying human glial cells in culture Dev. Neurosci. 9 3 1987 154 173 (Pubitemid 17145295)
80. I. Macikova, A. Perzelova, P. Mraz, I. Bizik, and J. Steno GFAP-positive astrocytes are rare or absent in primary adult human brain tissue cultures Biologia 64 4 2009 833 839
81. I. Bechmann, and R. Nitsch Identification of phagocytic glial cells after lesion induced anterograde degeneration using doublefluorescence labelling: combination of axonal tracing and lectin or immunostaining Histochem. Cell Biol. 107 1997 391 397 (Pubitemid 27226836)
82. E. Tornquist, L. Liu, P. Mattsson, and M. Svensson Response of glial cells and activation of complement following motoneuron degeneration induced by toxic ricin Neurosci. Res. 28 1997 167 175 (Pubitemid 27267826)
83. J.J. Rodríguez, M. Olabarria, A. Chvatal, and A. Verkhratsky Astroglia in dementia and Alzheimer's disease Cell Death Differ. 16 3 2009 378 385
84. A. Członkowska, and I. Kurkowska-Jastrzȩbska Inflammation and gliosis in neurological diseases - clinical implications J. Neuroimmunol. 231 1-2 2011 78 85