Early modulation of pro-inflammatory microglia by minocycline loaded nanoparticles confers long lasting protection after spinal cord injury

Biomaterials

Volumn 75, Issue , 2016, Pages 13-24

  Papa, Simonetta ^a   Caron, Ilaria ^a   Erba, Eugenio ^a   Panini, Nicolò ^a   De Paola, Massimiliano ^a   Mariani, Alessandro ^a   Colombo, Claudio ^b   Ferrari, Raffaele ^c   Pozzer, Diego ^a   Zanier, Elisa R ^a   Pischiutta, Francesca ^a   Lucchetti, Jacopo ^a   Bassi, Andrea ^c   Valentini, Gianluca ^c   Simonutti, Giulio ^c   Rossi, Filippo ^c   Moscatelli, Davide ^c   Forloni, Gianluigi ^a   Veglianese, Pietro ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b ETH ZURICH   (Switzerland)

^c POLITECNICO DI MILANO   (Italy)

Author keywords

Inflammation; Macrophages; Microglia; Minocycline; Nanoaprticles; Spinal cord injury

Indexed keywords

NANOPARTICLES; PATIENT REHABILITATION;

INFLAMMATION; MICROGLIA; MINOCYCLINE; NANOAPRTICLES; SPINAL CORD INJURIES (SCI);

MACROPHAGES;

MINOCYCLINE; MONOCYTE CHEMOTACTIC PROTEIN 1; NANOCARRIER; POLYCAPROLACTONE; NANOPARTICLE; POLYESTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DISEASE COURSE; DRUG DELIVERY SYSTEM; FLOW CYTOMETRY; GLIOSIS; IMMUNOFLUORESCENCE; INFLAMMATORY CELL; INTRAPARENCHYMAL DRUG ADMINISTRATION; MACROPHAGE; MICROGLIA; MOTOR PERFORMANCE; MOUSE; MOUSE MODEL; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; OUTCOME ASSESSMENT; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD INJURY; TARGET CELL; TIME-LAPSE VIDEO MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; ANIMAL BEHAVIOR; BIOLOGICAL MODEL; C57BL MOUSE; CELL MOTION; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; INFLAMMATION; METABOLISM; NERVE REGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; SPINAL CORD INJURIES;

ANIMALS; BEHAVIOR, ANIMAL; CELL MOVEMENT; CHEMOKINE CCL2; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; INFLAMMATION; MACROPHAGES; MICE, INBRED C57BL; MICROGLIA; MINOCYCLINE; MODELS, BIOLOGICAL; NANOPARTICLES; NERVE REGENERATION; PHENOTYPE; POLYESTERS; SPINAL CORD INJURIES;

EID: 84946429469     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.10.015     Document Type: Article

References (46)

1. Silver J., Schwab M.E., Popovich P.G. Central nervous system regenerative failure: role of oligodendrocytes, astrocytes, and microglia. Cold Spring Harb. Perspect. Biol. 2014, 7.
2. Gensel J.C., Zhang B. Macrophage activation and its role in repair and pathology after spinal cord injury. Brain Res. 2015, 1619:1-11.
3. David S., Zarruk J.G., Ghasemlou N. Inflammatory pathways in spinal cord injury. Int. Rev. Neurobiol. 2012, 106:127-152.
4. Shechter R., Schwartz M. Harnessing monocyte-derived macrophages to control central nervous system pathologies: no longer 'if' but 'how'. J. Pathol. 2013, 229:332-346.
5. Alexander J.K., Popovich P.G. Neuroinflammation in spinal cord injury: therapeutic targets for neuroprotection and regeneration. Prog. Brain Res. 2009, 175:125-137.
6. Thawer S.G., Mawhinney L., Chadwick K., de Chickera S.N., Weaver L.C., Brown A., et al. Temporal changes in monocyte and macrophage subsets and microglial macrophages following spinal cord injury in the Lys-Egfp-ki mouse model. J. Neuroimmunol. 2013, 261:7-20.
7. Cohen M., Matcovitch O., David E., Barnett-Itzhaki Z., Keren-Shaul H., Blecher-Gonen R., et al. Chronic exposure to TGFbeta1 regulates myeloid cell inflammatory response in an IRF7-dependent manner. EMBO J. 2014, 33:2906-2921.
8. Raposo C., Schwartz M. Glial scar and immune cell involvement in tissue remodeling and repair following acute CNS injuries. Glia 2014, 62:1895-1904.
9. David S., Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 2011, 12:388-399.
10. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:13435-13444.
11. Rossi F., Perale G., Papa S., Forloni G., Veglianese P. Current options for drug delivery to the spinal cord. Expert Opin. Drug Deliv. 2013, 10:385-396.
12. Lunov O., Syrovets T., Loos C., Beil J., Delacher M., Tron K., et al. Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano 2011, 5:1657-1669.
13. Caron I., Papa S., Rossi F., Forloni G., Veglianese P. Nanovector-mediated drug delivery for spinal cord injury treatment. Wiley Interdiscip. Rev. Nanomed Nanobiotechnol. 2014, 6:506-515.
14. Papa S., Ferrari R., De Paola M., Rossi F., Mariani A., Caron I., et al. Polymeric nanoparticle system to target activated microglia/macrophages in spinal cord injury. J. Control Release 2014, 174:15-26.
15. Papa S., Rossi F., Ferrari R., Mariani A., De Paola M., Caron I., et al. Selective nanovector mediated treatment of activated proinflammatory microglia/macrophages in spinal cord injury. ACS Nano 2013, 7:9881-9895.
16. Cerqueira S.R., Silva B.L., Oliveira J.M., Mano J.F., Sousa N., Salgado A.J., et al. Multifunctionalized CMCht/PAMAM dendrimer nanoparticles modulate the cellular uptake by astrocytes and oligodendrocytes in primary cultures of glial cells. Macromol. Biosci. 2012, 12:591-597.
17. Saxena T., Loomis K.H., Pai S.B., Karumbaiah L., Gaupp E., Patil K., et al. Nanocarrier-mediated inhibition of macrophage migration inhibitory factor attenuates secondary injury after spinal cord injury. ACS Nano 2015, 9:1492-1505.
18. Jain N.K., Mishra V., Mehra N.K. Targeted drug delivery to macrophages. Expert Opin. Drug Deliv. 2013, 10:353-367.
19. Kawabori M., Yenari M.A. The role of the microglia in acute CNS injury. Metab. Brain Dis. 2015, 30:381-392.
20. Zanier E.R., Pischiutta F., Riganti L., Marchesi F., Turola E., Fumagalli S., et al. Bone marrow mesenchymal stromal cells drive protective M2 microglia polarization after brain trauma. Neurotherapeutics 2014, 11:679-695.
21. Festoff B.W., Ameenuddin S., Arnold P.M., Wong A., Santacruz K.S., Citron B.A. Minocycline neuroprotects, reduces microgliosis, and inhibits caspase protease expression early after spinal cord injury. J. Neurochem. 2006, 97:1314-1326.
22. Kobayashi K., Imagama S., Ohgomori T., Hirano K., Uchimura K., Sakamoto K., et al. Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis. 2013, 4:e525.
23. Lee S.M., Yune T.Y., Kim S.J., Park D.W., Lee Y.K., Kim Y.C., et al. Minocycline reduces cell death and improves functional recovery after traumatic spinal cord injury in the rat. J. Neurotrauma 2003, 20:1017-1027.
24. Teng Y.D., Choi H., Onario R.C., Zhu S., Desilets F.C., Lan S., et al. Minocycline inhibits contusion-triggered mitochondrial cytochrome c release and mitigates functional deficits after spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3071-3076.
25. Wells J.E., Hurlbert R.J., Fehlings M.G., Yong V.W. Neuroprotection by minocycline facilitates significant recovery from spinal cord injury in mice. Brain J. Neurol. 2003, 126:1628-1637.
26. Yune T.Y., Lee J.Y., Jung G.Y., Kim S.J., Jiang M.H., Kim Y.C., et al. Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J. Neurosci. Off. J. Soc. Neurosci. 2007, 27:7751-7761.
27. Ferrari R., Yu Y.C., Morbidelli M., Hutchinson R.A., Moscatelli D. epsilon-Caprolactone-based macromonomers suitable for biodegradable nanoparticles synthesis through free radical polymerization. Macromolecules 2011, 44:9205-9212.
28. Basso D.M., Fisher L.C., Anderson A.J., Jakeman L.B., McTigue D.M., Popovich P.G. Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 2006, 23:635-659.
29. Erturk A., Becker K., Jahrling N., Mauch C.P., Hojer C.D., Egen J.G., et al. Three-dimensional imaging of solvent-cleared organs using 3DISCO. Nat. Protoc. 2012, 7:1983-1995.
30. Dodt H.U., Leischner U., Schierloh A., Jahrling N., Mauch C.P., Deininger K., et al. Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain. Nat. Methods 2007, 4:331-336.
31. De Paola M., Diana V., Bigini P., Mennini T. 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 2008, 170:85-95.
32. De Paola M., Mariani A., Bigini P., Peviani M., Ferrara G., Molteni M., et al. Neuroprotective effects of toll-like receptor 4 antagonism in spinal cord cultures and in a mouse model of motor neuron degeneration. Mol. Med. 2012, 18:971-981.
33. Zhang X., Goncalves R., Mosser D.M. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. Nov 2008, Chapter 14:Unit 14.1.
34. Zengel P., Nguyen-Hoang A., Schildhammer C., Zantl R., Kahl V., Horn E. mu-Slide Chemotaxis: a new chamber for long-term chemotaxis studies. BMC Cell Biol. 2011, 12:21.
35. Ferrari R., Colombo C., Casali C., Lupi M., Ubezio P., Falcetta F., et al. Synthesis of surfactant free PCL-PEG brushed nanoparticles with tunable degradation kinetics. Int. J. Pharm. 2013, 453:551-559.
36. Shechter R., Miller O., Yovel G., Rosenzweig N., London A., Ruckh J., et al. Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus. Immunity 2013, 38:555-569.
37. Sundberg L.M., Herrera J.J., Narayana P.A. In vivo longitudinal MRI and behavioral studies in experimental spinal cord injury. J. Neurotrauma 2010, 27:1753-1767.
38. Wieghofer P., Knobeloch K.P., Prinz M. Genetic targeting of microglia. Glia 2015, 63:1-22.
39. Hains B.C., Waxman S.G. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J. Neurosci. Off. J. Soc. Neurosci. 2006, 26:4308-4317.
40. Beck K.D., Nguyen H.X., Galvan M.D., Salazar D.L., Woodruff T.M., Anderson A.J. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain J. Neurol. 2010, 133:433-447.
41. Doring A., Sloka S., Lau L., Mishra M., van Minnen J., Zhang X., et al. Stimulation of monocytes, macrophages, and microglia by amphotericin B and macrophage colony-stimulating factor promotes remyelination. J. Neurosci. Off. J. Soc. Neurosci. 2015, 35:1136-1148.
42. Evans T.A., Barkauskas D.S., Myers J.T., Hare E.G., You J.Q., Ransohoff R.M., et al. High-resolution intravital imaging reveals that blood-derived macrophages but not resident microglia facilitate secondary axonal dieback in traumatic spinal cord injury. Exp. Neurol. 2014, 254:109-120.
43. Guerrero A.R., Uchida K., Nakajima H., Watanabe S., Nakamura M., Johnson W.E., et al. Blockade of interleukin-6 signaling inhibits the classic pathway and promotes an alternative pathway of macrophage activation after spinal cord injury in mice. J. Neuroinflamm. 2012, 9:40.
44. Ma S.F., Chen Y.J., Zhang J.X., Shen L., Wang R., Zhou J.S., et al. Adoptive transfer of M2 macrophages promotes locomotor recovery in adult rats after spinal cord injury. Brain, Behav. Immun. 2015, 45:157-170.
45. Gomes-Leal W. Microglial physiopathology: how to explain the dual role of microglia after acute neural disorders?. Brain Behav. 2012, 2:345-356.
46. Stirling D.P., Khodarahmi K., Liu J., McPhail L.T., McBride C.B., Steeves J.D., et al. Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J. Neurosci. Off. J. Soc. Neurosci. 2004, 24:2182-2190.