Polymeric nanoparticle system to target activated microglia/macrophages in spinal cord injury

Journal of Controlled Release

Volumn 174, Issue 1, 2014, Pages 15-26

  Papa, Simonetta ^a   Ferrari, Raffaele ^b   De Paola, Massimiliano ^a   Rossi, Filippo ^b   Mariani, Alessandro ^a   Caron, Ilaria ^a   Sammali, Eliana ^a   Peviani, Marco ^c   Dell'Oro, Valentina ^a   Colombo, Claudio ^b   Morbidelli, Massimo ^f   Forloni, Gianluigi ^a   Perale, Giuseppe ^b,d,e   Moscatelli, Davide ^b   Veglianese, Pietro ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b POLITECNICO DI MILANO   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d UNIVERSITY OF APPLIED SCIENCES AND ARTS OF SOUTHERN SWITZERLAND   (Switzerland)

^e Swiss Institute for Regenerative Medicine   (Switzerland)

^f ETH ZURICH   (Switzerland)

Author keywords

Drug delivery; Macrophage; Microglia; Nanoparticle; Spinal cord injury

Indexed keywords

CONTROLLED DRUG DELIVERY; DRUG DELIVERY; ESTERS; MACROPHAGES; NANOPARTICLES; PATIENT REHABILITATION; POLYMERS;

MICROGLIA; NEURODEGENERATION; POLYMERIC NANOPARTICLES; SECONDARY MECHANISMS; SPINAL CORD INJURIES (SCI); SPINAL CORDS; TOXIC EFFECT; UPTAKE MECHANISM;

TARGETED DRUG DELIVERY;

NANOCARRIER; POLY(METHYL METHACRYLATE);

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; MACROPHAGE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD INJURY;

DRUG DELIVERY; MACROPHAGE; MICROGLIA; NANOPARTICLE; SPINAL CORD INJURY;

ANIMALS; BEHAVIOR, ANIMAL; CARBOCYANINES; CELL SURVIVAL; CELLS, CULTURED; COLORING AGENTS; DRUG CARRIERS; FEMALE; HYDROGELS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROGLIA; NANOPARTICLES; POLYMETHYL METHACRYLATE; SPINAL CORD; SPINAL CORD INJURIES;

EID: 84888196375     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.11.001     Document Type: Article

References (53)

1. R. Ben Borgens, and P. Liu-Snyder Understanding secondary injury Q. Rev. Biol. 87 2012 89 127
2. L.S. Illis Central nervous system regeneration does not occur Spinal Cord 50 2012 259 263
3. S. Thuret, L.D. Moon, and F.H. Gage Therapeutic interventions after spinal cord injury Nat. Rev. Neurosci. 7 2006 628 643 (Pubitemid 44106745)
4. G.W.J. Hawryluk, J. Rowland, B.K. Kwon, and M.G. Fehlings Protection and repair of the injured spinal cord: a review of completed, ongoing, and planned clinical trials for acute spinal cord injury Neurosurg. Focus. 25 2008
5. G. Onose, A. Anghelescu, D.F. Muresanu, L. Padure, M.A. Haras, C.O. Chendreanu, L.V. Onose, A. Mirea, A.V. Ciurea, W.S. El Masri, and K.R.H. von Wild A review of published reports on neuroprotection in spinal cord injury Spinal Cord 47 2009 716 726
6. B.K. Kwon, L.H. Sekhon, and M.G. Fehlings Emerging repair, regeneration, and translational research advances for spinal cord injury Spine (Phila Pa 1976) 35 2010 S263 S270
7. B.K. Kwon, E. Okon, J. Hillyer, C. Mann, D. Baptiste, L.C. Weaver, M.G. Fehlings, and W. Tetzlaff A systematic review of non-invasive pharmacologic neuroprotective treatments for acute spinal cord injury J. Neurotrauma 28 2011 1545 1588
8. S. David, J.G. Zarruk, and N. Ghasemlou Inflammatory pathways in spinal cord injury Int. Rev. Neurobiol. 106 2012 127 152
9. K.D. Beck, H.X. Nguyen, M.D. Galvan, D.L. Salazar, T.M. Woodruff, and A.J. Anderson Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment Brain 133 2010 433 447
10. A. Sierra, O. Abiega, A. Shahraz, and H. Neumann Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis Front. Cell. Neurosci. 7 2013 6
11. D.J. Loane, and K.R. Byrnes Role of microglia in neurotrauma Neurotherapeutics 7 2010 366 377
12. K.A. Kigerl, J.C. Gensel, D.P. Ankeny, J.K. Alexander, D.J. Donnelly, and P.G. Popovich Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord J. Neurosci. 29 2009 13435 13444
13. R. Shechter, O. Miller, G. Yovel, N. Rosenzweig, A. London, J. Ruckh, K.W. Kim, E. Klein, V. Kalchenko, P. Bendel, S.A. Lira, S. Jung, and M. Schwartz Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus Inmmunity 38 2013 555 569
14. S.R. Cerqueira, J.M. Oliveira, N.A. Silva, H. Leite-Almeida, S. Ribeiro-Samy, A. Almeida, J.F. Mano, N. Sousa, A.J. Salgado, and R.L. Reis Microglia response and in vivo therapeutic potential of methylprednisolone- loaded dendrimer nanoparticles in spinal cord injury Small 9 2013 738 749
15. A. Sato, H. Ohtaki, T. Tsumuraya, D. Song, K. Ohara, M. Asano, Y. Iwakura, T. Atsumi, and S. Shioda Interleukin-1 participates in the classical and alternative activation of microglia/macrophages after spinal cord injury J. Neuroinflammation 9 2012 65
16. L. Florez, C. Herrmann, J.M. Cramer, C.P. Hauser, K. Koynov, K. Landfester, D. Crespy, and V. Mailander How shape influences uptake: interactions of anisotropic polymer nanoparticles and human mesenchymal stem cells Small 8 2012 2222 2230
17. J. Nicolas, S. Mura, D. Brambilla, N. Mackiewicz, and P. Couvreur Design, functionalization strategies and biomedical applications of targeted biodegradable/biocompatible polymer-based nanocarriers for drug delivery Chem. Soc. Rev. 42 2013 1147 1235
18. F. Rossi, G. Perale, S. Papa, G. Forloni, and P. Veglianese Current options for drug delivery to the spinal cord Expert Opin. Drug Deliv. 10 2013 385 396
19. J.C. Stanwick, M.D. Baumann, and M.S. Shoichet Enhanced neurotrophin-3 bioactivity and release from a nanoparticle-loaded composite hydrogel J. Control. Release 160 2012 666 675
20. Y.C. Kuo, and H.F. Ko Targeting delivery of saquinavir to the brain using 83-14 monoclonal antibody-grafted solid lipid nanoparticles Biomaterials 34 2013 4818 4830
21. I. Canton, and G. Battaglia Endocytosis at the nanoscale Chem. Soc. Rev. 41 2012 2718 2739
22. D. Di Mascolo, C. Lyon, S. Aryal, M.R. Ramirez, J. Wang, P. Candeloro, M. Guindani, W.A. Hsueh, and P. Decuzzi Rosiglitazone-loaded nanospheres for modulating macrophage-specific inflammation in obesity J. Control. Release 170 2013 460 468
23. G. Sharma, D.T. Valenta, Y. Altman, S. Harvey, H. Xie, S. Mitragotri, and J.W. Smith Polymer particle shape independently influences binding and internalization by macrophages J. Control. Release 147 2010 408 412
24. C. He, L. Yin, C. Tang, and C. Yin Multifunctional polymeric nanoparticles for oral delivery of TNF-alpha siRNA to macrophages Biomaterials 34 2013 2843 2854
25. N.K. Jain, V. Mishra, and N.K. Mehra Targeted drug delivery to macrophages Expert Opin. Drug Deliv. 10 2013 353 367
26. C. Colombo, M. Lupi, P. Ubezio, and D. Moscatelli Cytotoxicity of PMMA-based nanoparticles synthesized adopting SDS and Tween80 Macromol. Symp. 324 2013 134 139
27. L. Cova, P. Bigini, V. Diana, L. Sitia, R. Ferrari, R.M. Pesce, R. Khalaf, P. Bossolasco, P. Ubezio, M. Lupi, M. Tortarolo, L. Colombo, D. Giardino, V. Silani, M. Morbidelli, M. Salmona, and D. Moscatelli Biocompatible fluorescent nanoparticles for in vivo stem cell tracking Nanotechnology 24 2013 245603
28. J. Jung, I.-H. Lee, E. Lee, J. Park, and S. Jon pH-sensitive polymer nanospheres for use as a potential drug delivery vehicle Biomacromolecules 8 2007 3401 3407 (Pubitemid 350193739)
29. A. Bettencourt, and A.J. Almeida Poly(methyl methacrylate) particulate carriers in drug delivery J. Microencapsul. 29 2012 353 367
30. M. Dossi, R. Ferrari, L. Dragoni, C. Martignoni, P. Gaetani, M. D'Incalci, M. Morbidelli, and D. Moscatelli Synthesis of fluorescent PMMA-based nanoparticles Macromol. Mater. Eng. 298 2013 771 778
31. R. Ferrari, C. Colombo, C. Casali, M. Lupi, P. Ubezio, F. Falcetta, M. D'Incalci, M. Morbidelli, and D. Moscatelli Synthesis of surfactant free PCL-PEG brushed nanoparticles with tunable degradation kinetics Int. J. Pharm. 453 2013 551 559
32. M. De Paola, V. Diana, P. Bigini, and T. Mennini Morphological features and responses to AMPA receptor-mediated excitotoxicity of mouse motor neurons: comparison in purified, mixed anterior horn or motor neuron/glia cocultures J. Neurosci. Methods 170 2008 85 95
33. M. De Paola, A. Mariani, P. Bigini, M. Peviani, G. Ferrara, M. Molteni, S. Gemma, P. Veglianese, V. Castellaneta, V. Boldrin, C. Rossetti, C. Chiabrando, G. Forloni, T. Mennini, and R. Fanelli Neuroprotective effects of toll-like receptor 4 antagonism in spinal cord cultures and in a mouse model of motor neuron degeneration Mol. Med. 18 2012 971 981
34. G. Perale, F. Rossi, M. Santoro, M. Peviani, S. Papa, D. Llupi, P. Torriani, E. Micotti, S. Previdi, L. Cervo, E. Sundstrom, A.R. Boccaccini, M. Masi, G. Forloni, and P. Veglianese Multiple drug delivery hydrogel system for spinal cord injury repair strategies J. Control. Release 159 2012 271 280
35. F. Rossi, M. Santoro, T. Casalini, P. Veglianese, M. Masi, and G. Perale Characterization and degradation behavior of agar-carbomer based hydrogels for drug delivery applications: solute effect Int. J. Mol. Sci. 12 2011 3394 3408
36. S.A. Marques, V.F. Garcez, E.A. Del Bel, and A.M. Martinez A simple, inexpensive and easily reproducible model of spinal cord injury in mice: morphological and functional assessment J. Neurosci. Methods 177 2009 183 193
37. F. Rossi, R. Ferrari, S. Papa, D. Moscatelli, T. Casalini, G. Forloni, G. Perale, and P. Veglianese Tunable hydrogel-nanoparticles release system for sustained combination therapies in the spinal cord Colloids Surf. B: Biointerfaces 108 2013 169 177
38. R. Ferrari, Y.C. Yu, M. Morbidelli, R.A. Hutchinson, and D. Moscatelli Epsilon-caprolactone-based macromonomers suitable for biodegradable nanoparticles synthesis through free radical polymerization Macromolecules 44 2011 9205 9212
39. A.R. Carta, and A. Pisanu Modulating microglia activity with PPAR-gamma agonists: a promising therapy for Parkinson's disease? Neurotox. Res. 23 2013 112 123
40. E. Gray, M. Ginty, K. Kemp, N. Scolding, and A. Wilkins The PPAR-gamma agonist pioglitazone protects cortical neurons from inflammatory mediators via improvement in peroxisomal function J. Neuroinflammation 9 2012 63
41. H. Ji, H. Wang, F. Zhang, X. Li, L. Xiang, and S. Aiguo PPARgamma agonist pioglitazone inhibits microglia inflammation by blocking p38 mitogen-activated protein kinase signaling pathways Inflamm. Res. 59 2010 921 929
42. S. Mandrekar-Colucci, J.C. Karlo, and G.E. Landreth Mechanisms underlying the rapid peroxisome proliferator-activated receptor-gamma-mediated amyloid clearance and reversal of cognitive deficits in a murine model of Alzheimer's disease J. Neurosci. 32 2012 10117 10128
43. B.W. Festoff, S. Ameenuddin, P.M. Arnold, A. Wong, K.S. Santacruz, and B.A. Citron Minocycline neuroprotects, reduces microgliosis, and inhibits caspase protease expression early after spinal cord injury J. Neurochem. 97 2006 1314 1326 (Pubitemid 43725571)
44. B.C. Hains, and S.G. Waxman Activated microglia contribute to the maintenance of chronic pain after spinal cord injury J. Neurosci. 26 2006 4308 4317 (Pubitemid 44315390)
45. K. Kobayashi, S. Imagama, T. Ohgomori, K. Hirano, K. Uchimura, K. Sakamoto, A. Hirakawa, H. Takeuchi, A. Suzumura, N. Ishiguro, and K. Kadomatsu Minocycline selectively inhibits M1 polarization of microglia Cell Death Dis. 4 2013 e525
46. M. Ghosh, D. Garcia-Castillo, V. Aguirre, R. Golshani, C.M. Atkins, H.M. Bramlett, W.D. Dietrich, and D.D. Pearse Proinflammatory cytokine regulation of cyclic AMP-phosphodiesterase 4 signaling in microglia in vitro and following CNS injury Glia 60 2012 1839 1859
47. Y.S. Gwak, J. Kang, G.C. Unabia, and C.E. Hulsebosch Spatial and temporal activation of spinal glial cells: role of gliopathy in central neuropathic pain following spinal cord injury in rats Exp. Neurol. 234 2012 362 372
48. R. Vallejo, D.M. Tilley, L. Vogel, and R. Benyamin The role of glia and the immune system in the development and maintenance of neuropathic pain Pain Pract. 10 2010 167 184
49. T. Trang, S. Beggs, and M.W. Salter ATP receptors gate microglia signaling in neuropathic pain Exp. Neurol. 234 2012 354 361
50. S. David, and A. Kroner Repertoire of microglial and macrophage responses after spinal cord injury Nat. Rev. Neurosci. 12 2011 388 399
51. J. Chen, Y. Zhou, S. Mueller-Steiner, L.F. Chen, H. Kwon, S. Yi, L. Mucke, and L. Gan SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling J. Biol. Chem. 280 2005 40364 40374 (Pubitemid 41779174)
52. N. Nayerossadat, T. Maedeh, and P.A. Ali Viral and nonviral delivery systems for gene delivery Adv. Biomed. Res. 1 2012 27
53. S.S. Minami, B. Sun, K. Popat, T. Kauppinen, M. Pleiss, Y. Zhou, M.E. Ward, P. Floreancig, L. Mucke, T. Desai, and L. Gan Selective targeting of microglia by quantum dots J. Neuroinflammation 9 2012 22