Nanomedicine and its application in treatment of microglia-mediated neuroinflammation

Current Medicinal Chemistry

Volumn 21, Issue 37, 2014, Pages 4215-4226

  Baby, N ^a   Patnala, R ^a   Ling, Eng Ang ^a   Dheen, S T ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Microglia; Nano particles; Neurodegeneration

Indexed keywords

ANTIINFLAMMATORY AGENT; CARBON NANOTUBE; DENDRIMER; GOLD NANOPARTICLE; NANOMATERIAL; SILICA NANOPARTICLE; NONSTEROID ANTIINFLAMMATORY AGENT;

ARTICLE; BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; DEGENERATIVE DISEASE; DRUG DELIVERY SYSTEM; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; MICROGLIA; NANOMEDICINE; NANOTECHNOLOGY; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHAGOCYTOSIS; REGULATORY MECHANISM; TOXICITY; CENTRAL NERVOUS SYSTEM DISEASES; DRUG EFFECTS; NEURODEGENERATIVE DISEASES; PATHOLOGY; PROCEDURES;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CENTRAL NERVOUS SYSTEM DISEASES; DRUG DELIVERY SYSTEMS; HUMANS; INFLAMMATION; MICROGLIA; NANOMEDICINE; NEURODEGENERATIVE DISEASES;

EID: 84918767482     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867321666140716101258     Document Type: Article

References (105)

1. Re, F.; Gregori, M.; Masserini, M. Nanotechnology for neurodegenerative disorders. Nanomedicine: Nanotechnol. Biol. Med., 2012, 8, S51-S58.
2. Roney, C; Kulkarni, P.; Arora, V.; Antich, P.; Bonte, F.; Wu, A.; Mallikarjuana, N.; Manohar, S.; Liang, H.-F.; Kulkarni, A. R. Targeted nanoparticles for drug delivery through the blood-brain barrier for Alzheimer's disease. J. Control. Release, 2005, 108(2), 193-214.
3. Singh, R.; Lillard Jr, J. W. Nanoparticle-based targeted drug delivery. Exp. Mol. Pathol, 2009, 86(3), 215-223.
4. Batrakova, E. V.; Li, S.; Reynolds, A. D.; Mosley, R. L.; Bronich, T. K.; Kabanov, A. V.; Gendelman, H. E. A macrophage-nanozyme delivery system for Parkinson's disease. Bioconjugate Chem., 2007, 18(5), 1498-1506.
5. Sahoo, S. K.; Labhasetwar, V. Nanotech approaches to drug delivery and imaging. Drug Discover. Today, 2003, 8(24), 1112-1120.
6. Panyam, J.; Labhasetwar, V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv. Drug Deliv. Rev., 2003, 55(3), 329-347.
7. Thameem Dheen, S.; Kaur, C; Ling, E.-A. Microglial activation and its implications in the brain diseases. Curr. Med. Chem., 2007, 14(11), 1189-1197.
8. Ling, E. A.; Leblond, C. Investigation of glial cells in semithin sections. II. Variation with age in the numbers of the various glial cell types in rat cortex and corpus callosum. J. Comparative Neurol, 1973, 149(1), 73-81.
9. Kaur, C; Hao, A. J.; Wu, C. H.; Ling, E. A. Origin of microglia. Microscop. Res. Technique, 2001, 54(1), 2-9.
10. Figuera-Losada, M.; Rojas, C; Slusher, B. S. Inhibition of Microglia Activation as a Phenotypic Assay in Early Drug Discovery. J. Biomol. Screen., 2014, 19(1), 17-31.
11. Sarma, J. D., Microglia-mediated neuroinflammation is an amplifier of virus-induced neuropathology. J. NeuroVirol, 2013, 1-15.
12. Kaur, C; Ling, E.; Wong, W. Transformation of amoeboid microglial cells into microglia in the corpus callosum of the postnatal rat brain. An electron microscopical study. Archivum Histologicum Japonicum, 1985, 48(1), 17-25.
13. Dheen, S.; Hao, A.; Ng, Y.; Ling, E. Regulatory factors and functions of microglia during development. Neuroembryol. Aging, 2002, 1(3), 105-112.
14. Ling, E. A.; Wong, W. C. The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia, 1993, 7(1), 9-18.
15. Qin, L.; Liu, Y.; Cooper, C; Liu, B.; Wilson, B.; Hong, J. S. Microglia enhance β-amyloid peptide-induced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J. Neurochem., 2002, 83(4), 973-983.
16. McGeer, P.; Itagaki, S.; Boyes, B.; McGeer, E. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology, 1988, 38(8), 1285-1285.
17. Benveniste, E. N. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J. Mol. Med., 1997, 75(3), 165-173.
18. Delgado, R.; Carlin, A.; Airaghi, L.; Demitri, M. T.; Meda, L.; Galimberti, D.; Baron, P.; Lipton, J. M.; Catania, A. Melanocortin peptides inhibit production of proinflammatory cytokines and nitric oxide by activated microglia. J. Leukocyte Biol, 1998, 63(6), 740-745.
19. Jordan, C. A.; Watkins, B. A.; Kufta, C; Dubois-Dalcq, M. Infection of brain microglial cells by human immunodeficiency virus type 1 is CD4 dependent. J. Virol, 1991, 65(2), 736-742.
20. Tai, Y. F.; Pavese, N.; Gerhard, A.; Tabrizi, S. J.; Barker, R. A.; Brooks, D. J.; Piccini, P. Microglial activation in presymptomatic Huntington's disease gene carriers. Brain, 2007, 130(7), 1759-1766.
21. Pavese, N.; Gerhard, A.; Tai, Y.; Ho, A.; Turkheimer, F.; Barker, R.; Brooks, D.; Piccini, P. Microglial activation correlates with severity in Huntington disease A clinical and PET study. Neurology, 2006, 66(11), 1638-1643.
22. Paulus, W.; Bancher, C; Jellinger, K. Microglial reaction in Pick's disease. Neurosci. Lett., 1993, 161(1), 89-92.
23. Raghavendra Rao, V. L.; Dogan, A.; Bowen, K. K.; Dempsey, R. J. Traumatic brain injury leads to increased expression of peripheraltype benzodiazepine receptors, neuronal death, and activation of astrocytes and microglia in rat thalamus. Exp. Neurol., 2000, 161(1), 102-114.
24. Huo, Y.; Rangarajan, P.; Ling, E.-A.; Dheen, S. T. Dexamethasone inhibits the Nox-dependent ROS production via suppression of MKP-1-dependent MAPK pathways in activated microglia. BMC Neurosci., 2011, 12(1), 49.
25. Tikka, T.; Fiebich, B. L.; Goldsteins, G.; Keinänen, R.; Koistinaho, J, Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neuroscience, 2001, 21(8), 2580-2588.
26. Kaur, C; Sivakumar, V.; Lu, J.; Tang, F. R.; Ling, E. A. Melatonin Attenuates Hypoxia-Induced Ultrastructural Changes and Increased Vascular Permeability in the Developing Hippocampus. Brain Pathol, 2008, 18(4), 533-547.
27. Chung, S. Y.; Han, S. H. Melatonin attenuates kainic acid-induced hippocampal neurodegeneration and oxidative stress through microglial inhibition. J. Pineal Res., 2003, 34(2), 95-102.
28. Dheen, S. T.; Jun, Y.; Yan, Z.; Tay, S. S.; Ang Ling, E. Retinoic acid inhibits expression of TNF-a and iNOS in activated rat microglia. Glia, 2005, 50(1), 21-31.
29. Shakespear, M. R.; Halili, M. A.; Irvine, K. M.; Fairlie, D. P.; Sweet, M. J. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol, 2011, 32(7), 335-343.
30. Huuskonen, J.; Suuronen, T.; Nuutinen, T.; Kyrylenko, S.; Salminen, A. Regulation of microglial inflammatory response by sodium butyrate and short-chain fatty acids. Brit. J. Pharmacol, 2004, 141(5), 874-880.
31. Suuronen, T.; Huuskonen, J.; Pihlaja, R.; Kyrylenko, S.; Salminen, A. Regulation of microglial inflammatory response by histone deacetylase inhibitors. J. Neurochem., 2003, 87(2), 407-416.
32. Rayan, N. A.; Baby, N.; Pitchai, D.; Indraswari, F.; Ling, E. A.; Lu, J.; Dheen, T. Costunolide inhibits proinflammatory cytokines and iNOS in activated murine BV2 microglia. Front. Biosci. (Elite Ed.), 2011, 3, 1079-1091.
33. Rangarajan, P.; Eng-Ang, L.; Thameem Dheen, S. Potential Drugs Targeting Microglia: Current Knowledge and Future Prospects. CNS Neurol. Disorders-Drug Targets, 2013, 12(6), 799-806.
34. Park, J.-S.; Park, E.-M.; Kim, D.-H.; Jung, K.; Jung, J.-S.; Lee, E.-J.; Hyun, J.-W.; Kang, J. L.; Kim, H.-S. Anti-inflammatory mechanism of ginseng saponins in activated microglia. J. Neuroimmunol., 2009, 209(1), 40-49.
35. Magni, P.; Ruscica, M.; Dozio, E.; Rizzi, E.; Beretta, G.; Facino, R. M. Parthenolide Inhibits the LPS-induced Secretion of IL-6 and TNF-α and NF-κB Nuclear Translocation in BV-2 Microglia. Phytother. Res., 2012, 26(9), 1405-1409.
36. Nowacek, A.; Gendelman, H. E. NanoART, neuroAIDS and CNS drug delivery. Nanomedicine, 2009, 4(5), 557-574.
37. Ohtsuki, S.; Terasaki, T. Contribution of carrier-mediated transport systems to the blood-brain barrier as a supporting and protecting interface for the brain; importance for CNS drug discovery and development. Pharmaceut. Res., 2007, 24(9), 1745-1758.
38. Fernandes, C.; Soni, U.; Patravale, V. Nano-interventions for neurodegenerative disorders. Pharmacol. Res., 2010, 62(2), 166-178.
39. Setyawati, M. I.; Tay, C. Y.; Chia, S. L.; Goh, S. L.; Fang, W.; Neo, M. J.; Chong, H. C.; Tan, S. M.; Loo, S. C. J.; Ng, K. W.; Xie, J. P.; Ong, C. N.; Tan, N. S.; Leong, D. T. Titanium dioxide nanomaterials cause endothelial cell leakiness by disrupting the homophilic interaction of VE-cadherin. Nat. Commun., 2013, 4, 1673.
40. Kateb, B.; Van Handel, M.; Zhang, L.; Bronikowski, M. J.; Manohara, H.; Badie, B. Internalization of MWCNTs by microglia: possible application in immunotherapy of brain tumors. Neuroimage, 2007, 37, S9-S17.
41. Kim, B. Y.; Rutka, J. T.; Chan, W. C. Nanomedicine. New Engl. J. Med., 2010, 363(25), 2434-2443.
42. Bianco, A. Carbon nanotubes for the delivery of therapeutic molecules. Expert Opin. Drug Deliver., 2004, 1(1), 57-65.
43. Salvador-Morales, C.; Flahaut, E.; Sim, E.; Sloan, J. H.; Green, M. L.; Sim, R. B. Complement activation and protein adsorption by carbon nanotubes. Mol. Immunol., 2006, 43(3), 193-201.
44. Nunes, A.; Bussy, C.; Gherardini, L.; Meneghetti, M.; Herrero, M. A.; Bianco, A.; Prato, M.; Pizzorusso, T.; Al-Jamal, K. T.; Kostarelos, K. In vivo degradation of functionalized carbon nanotubes after stereotactic administration in the brain cortex. Nanomedicine, 2012, 7(10), 1485-1494.
45. Lee, H. J.; Park, J.; Yoon, O. J.; Kim, H. W.; Lee, D. Y.; Kim, D. H.; Lee, W. B.; Lee, N.-E.; Bonventre, J. V.; Kim, S. S. Amine-modified single-walled carbon nanotubes protect neurons from injury in a rat stroke model. Nat. Nanotechnol., 2011, 6(2), 121-125.
46. Luo, X.; Matranga, C.; Tan, S.; Alba, N.; Cui, X. T. Carbon nanotube nanoreservior for controlled release of anti-inflammatory dexamethasone. Biomaterials, 2011, 32(26), 6316-6323.
47. Bharali, D. J.; Klejbor, I.; Stachowiak, E. K.; Dutta, P.; Roy, I.; Kaur, N.; Bergey, E. J.; Prasad, P. N.; Stachowiak, M. K. Organically modified silica nanoparticles: a nonviral vector for in vivo gene delivery and expression in the brain. Proc. Natl. Acad. Sci. USA, 2005, 102(32), 11539-11544.
48. Roy, I.; Ohulchanskyy, T. Y.; Bharali, D. J.; Pudavar, H. E.; Mistretta, R. A.; Kaur, N.; Prasad, P. N. Optical tracking of organically modified silica nanoparticles as DNA carriers: a nonviral, nanomedicine approach for gene delivery. Proc. Natl. Acad. Sci. USA, 2005, 102(2), 279-284.
49. Ribot, E.; Bouzier-Sore, A.-K.; Bouchaud, V.; Miraux, S.; Delville, M.-H.; Franconi, J.-M.; Voisin, P. Microglia used as vehicles for both inducible thymidine kinase gene therapy and MRI contrast agents for glioma therapy. Cancer Gene Ther., 2007, 14(8), 724-737.
50. Zhang, J.; Sarkar, S.; Cua, R.; Zhou, Y.; Hader, W.; Yong, V. W. A dialog between glioma and microglia that promotes tumor invasiveness through the CCL2/CCR2/interleukin-6 axis. Carcinogenesis, 2012, 33(2), 312-319.
51. Choi, J.; Zheng, Q.; Katz, H. E.; Guilarte, T. R. Silica-based nanoparticle uptake and cellular response by primary microglia. Environ. Health Perspect., 2010, 118(5), 589.
52. Kim, C.-K.; Ghosh, P.; Rotello, V. M. Multimodal drug delivery using gold nanoparticles. Nanoscale, 2009, 1(1), 61-67.
53. Wang, H.; Huff, T. B.; Zweifel, D. A.; He, W.; Low, P. S.; Wei, A.; Cheng, J.-X. In vitro and in vivo two-photon luminescence imaging of single gold nanorods. Proc. Natl. Acad. Sci. USA, 2005, 102(44), 15752-15756.
54. Hutter, E.; Boridy, S.; Labrecque, S.; Lalancette-Hébert, M.; Kriz, J.; Winnik, F. M.; Maysinger, D., Microglial response to gold nanoparticles. ACS nano, 2010, 4(5), 2595-2606.
55. Tan, Y. H.; Terrill, S. E.; Paranjape, G. S.; Stine, K. J.; Nichols, M. R. The influence of gold surface texture on microglia morphology and activation. Biomaterials Sci., 2014, 2, 110-120.
56. Boridy, S.; Soliman, G. M.; Maysinger, D., Modulation of inflammatory signaling and cytokine release from microglia by celastrol incorporated into dendrimer nanocarriers. Nanomedicine, 2012, 7(8), 1149-1165.
57. Tomalia, D.; Baker, H.; Dewald, J.; Hall, M.; Kallos, G.; Martin, S.; Roeck, J.; Ryder, J.; Smith, P., A new class of polymers: starburst-dendritic macromolecules. Polymer J., 1985, 17(1), 117-132.
58. Malam, Y.; Loizidou, M.; Seifalian, A. M., Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer. Trends Pharmacol. Sci., 2009, 30(11), 592-599.
59. Gabizon, A.; Catane, R.; Uziely, B.; Kaufman, B.; Safra, T.; Cohen, R.; Martin, F.; Huang, A.; Barenholz, Y. Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes. Cancer Res., 1994, 54(4), 987-992.
60. Gabizon, A.; Shmeeda, H.; Barenholz, Y. Pharmacokinetics of pegylated liposomal doxorubicin. Clin. Pharmacokinet., 2003, 42(5), 419-436.
61. Sharpe, M.; Easthope, S. E.; Keating, G. M.; Lamb, H. M. Polyethylene glycol-liposomal doxorubicin. Drugs, 2002, 62(14), 2089-2126.
62. Morigi, V.; Tocchio, A.; Bellavite Pellegrini, C; Sakamoto, J. H.; Arnone, M.; Tasciotti, E. Nanotechnology in medicine: From inception to market domination. J. Drug Deliver., 2012, 2012.
63. Chekhonin, V.; Zhirkov, Y. A.; Gurina, O.; Ryabukhin, I.; Lebedev, S.; Kashparov, I.; Dmitriyeva, T. PEGylated immunoliposomes directed against brain astrocytes. Drug Deliver., 2004, 12(1), 1-6.
64. Omori, N.; Maruyama, K.; Jin, G.; Wang, S.; Hamakawa, Y.; Sato, K.; Nagano, I.; Shoji, M.; Abe, K. Targeting of post-ischemic cerebral endothelium in rat by liposomes bearing polyethylene glycolcoupled transferrin. Neurol. Res., 2003, 25(3), 275-279.
65. Wiley, N. J.; Madhankumar, A.; Mitchell, R. M.; Neely, E. B.; Rizk, E.; Douds, G. L.; Simmons, Z.; Connor, J. R. Lipopolysaccharide modified liposomes for amyotropic lateral sclerosis therapy: Efficacy in SOD1 mouse model. Adv. Nanoparticles, 2012, 1, 44.
66. Pardridge, W. M. Tyrosine hydroxylase replacement in experimental Parkinson's disease with transvascular gene therapy. NeuroRx, 2005, 2(1), 129-138.
67. Chiba, T.; Umegaki, K. Pivotal roles of monocytes/macrophages in stroke. Mediators Inflammation, 2013, 2013, 759103.
68. Kadiu, I.; Glanzer, J.; Kipnis, J.; Gendelman, H.; Thomas, M. Mononuclear phagocytes in the pathogenesis of neurodegenerative diseases. Neurotoxicity Res., 2005, 8(1-2), 25-50.
69. Kabanov, A.; Gendelman, H. Nanomedicine in the diagnosis and therapy of neurodegenerative disorders. Prog. Polymer Sci., 2007, 32(8), 1054-1082.
70. Jain, S.; Mishra, V.; Singh, P.; Dubey, P. K.; Saraf, D. K.; Vyas, S. P. RGD-anchored magnetic liposomes for monocytes/neutrophilsmediated brain targeting. Int. J. Pharmaceut., 2003, 261(1-2), 43-55.
71. Tay, C. Y.; Fang, W.; Setyawati, M. I.; Sum, C. P.; Xie, J.; Ng, K. W.; Chen, X.; Hong, C. H. L.; Leong, D. T. Reciprocal response of human oral epithelial cells to internalized silica nanoparticles. Part. Part. Syst. Charact., 2013, 30(9), 784-793.
72. Setyawati, M. I.; Fang, W.; Chia, S. L.; Leong, D. T. Nanotoxicology of common metal oxide based nanomaterials: their ROS-y and non-ROS-y consequences. Asia-Pacific J. Chem. Eng., 2013, 8(2), 205-217.
73. McDermott, J.; Smith, A.; Ward, M.; Parkinson, I.; Kerr, D. Brainaluminium concentration in dialysis encephalopathy. Lancet, 1978, 311(8070), 901-904.
74. Li, X.-B.; Zheng, H.; Zhang, Z.-R.; Li, M.; Huang, Z.-Y.; Schluesener, H. J.; Li, Y.-Y.; Xu, S.-Q. Glia activation induced by peripheral administration of aluminum oxide nanoparticles in rat brains. Nanomedicine, 2009, 5(4), 473-479.
75. Setyawati, M. I.; Tay, C. Y.; Leong, D. T. Effect of zinc oxide nanomaterials-induced oxidative stress on the p53 pathway. Biomaterials, 2013, 34(38), 10133-10142.
76. Setyawati, M. I.; Khoo, P. K. S.; Eng, B. H.; Xiong, S.; Zhao, X.; Das, G. K.; Tan, T. T.-Y.; Loo, J. S. C.; Leong, D. T.; Ng, K. W. Cytotoxic and genotoxic characterization of titanium dioxide, gadolinium oxide, and poly (lactic-co-glycolic acid) nanoparticles in human fibroblasts. J. Biomed. Mater. Res. Part A., 2013, 101A (3), 633-640.
77. George, S.; Pokhrel, S.; Ji, Z.; Henderson, B. L.; Xia, T.; Li, L.; Zink, J. I.; Nel, A. E.; Mädler, L. Role of Fe Doping in Tuning the Band Gap of TiO2 for the Photo-Oxidation-Induced Cytotoxicity Paradigm. J. Am. Chem. Soc, 2011, 133(29), 11270-11278.
78. Griffin, W.; Sheng, J.; Royston, M.; Gentleman, S.; McKenzie, J.; Graham, D.; Roberts, G.; Mrak, R. Glial-Neuronal Interactions in Alzheimer's Disease: The Potential Role of a 'Cytokine Cycle'in Disease Progression. Brain Pathol., 1998, 8(1), 65-72.
79. Combs, C. K.; Johnson, D. E.; Karlo, J. C.; Cannady, S. B.; Landreth, G. E. Inflammatory mechanisms in Alzheimer's disease: inhibition of p-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARy agonists. J. Neurosci., 2000, 20(2), 558-567.
80. Sasaki, A.; Yamaguchi, H.; Ogawa, A.; Sugihara, S.; Nakazato, Y. Microglial activation in early stages of amyloid p protein deposition. Acta Neuropathologica, 1997, 94(4), 316-322.
81. Rogers, J.; Lue, L.-F. Microglial chemotaxis, activation, and phagocytosis of amyloid p-peptide as linked phenomena in Alzheimer's disease. Neurochem. Int., 2001, 39(5), 333-340.
82. Xiang, Z.; Haroutunian, V.; Ho, L.; Purohit, D.; Pasinetti, G. M. Microglia activation in the brain as inflammatory biomarker of Alzheimer's disease neuropathology and clinical dementia. Dis. Markers, 2006, 22(1-2), 95-102.
83. Zhang, W.; Wang, T.; Pei, Z.; Miller, D. S.; Wu, X.; Block, M. L.; Wilson, B.; Zhang, W.; Zhou, Y.; Hong, J.-S. Aggregated asynuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J., 2005, 19(6), 533-542.
84. Langston, J.; Forno, L.; Tetrud, J.; Reeves, A.; Kaplan, J.; Karluk, D. Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine exposure. Ann. Neurol, 1999, 46(4), 598-605.
85. Kim, Y. S.; Choi, D. H.; Block, M. L.; Lorenzl, S.; Yang, L.; Kim, Y. J.; Sugama, S.; Cho, B. P.; Hwang, O.; Browne, S. E. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB J., 2007, 21(1), 179-187.
86. Losy, J. Is MS an inflammatory or primary degenerative disease? J. Neural Transm., 2013, 120(10), 1459-1462.
87. Brasier, A. R. The NF-kB regulatory network. Cardiovasc. Toxicol, 2006, 6(2), 111-130.
88. Dohi, K.; Ohtaki, H.; Nakamachi, T.; Yofu, S.; Satoh, K.; Miyamoto, K.; Song, D.; Tsunawaki, S.; Shioda, S.; Aruga, T. Gp91phox (NOX2) in classically activated microglia exacerbates traumatic brain injury. J. Neuroinflammation, 2010, 7(1), 41.
89. Zhou, Y.; Ling, E. A.; Dheen, S. T. Dexamethasone suppresses monocyte chemoattractant protein-1 production via mitogen activated protein kinase phosphatase-1 dependent inhibition of Jun. N-terminal kinase and p38 mitogen-activated protein kinase in activated rat microglia. J. Neurochem., 2007, 102(3), 667-678.
90. Cao, Q.; Kaur, C; Wu, C.-Y.; Lu, J.; Ling, E.-A. Nuclear factorkappa β regulates Notch signaling in production of proinflammatory cytokines and nitric oxide in murine BV-2 microglial cells. Neuroscience, 2011, 192, 140-154.
91. Cao, Q.; Lu, J.; Kaur, C; Sivakumar, V.; Li, F.; Cheah, P. S.; Dheen, S. T.; Ling, E. A. Expression of Notch-1 receptor and its ligands Jagged-1 and Delta-1 in amoeboid microglia in postnatal rat brain and murine BV-2 cells. Glia, 2008, 56(11), 1224-1237.
92. Mumm, J. S.; Schroeter, E. H.; Saxena, M. T.; Griesemer, A.; Tian, X.; Pan, D.; Ray, W. J.; Kopan, R. A ligand-induced extracellular cleavage regulates y-secretase-like proteolytic activation of Notch 1. Mol Cell, 2000, 5(2), 197-206.
93. Yao, L.; Kan, E. M.; Kaur, C; Dheen, S. T.; Hao, A.; Lu, J.; Ling, E.-A. Notch-1 Signaling Regulates Microglia Activation via NF-KB Pathway after Hypoxic Exposure In Vivo and In Vitro. PloS One, 2013, 8(11), e78439.
94. Nayak, D.; Huo, Y.; Kwang, W.; Pushparaj, P.; Kumar, S.; Ling, E.-A.; Dheen, S. Sphingosine kinase 1 regulates the expression of proinflammatory cytokines and nitric oxide in activated microglia. Neuroscience, 2010, 166(1), 132-144.
95. Lin, H.; Baby, N.; Lu, J.; Kaur, C; Zhang, C; Xu, J.; Ling, E.-A.; Dheen, S. T. Expression of sphingosine kinase 1 in amoeboid microglial cells in the corpus callosum of postnatal rats. J. Neuroinflammation, 2011, 8(1), 13.
96. Parakalan, R.; Jiang, B.; Nimmi, B.; Janani, M.; Jayapal, M.; Lu, J.; Tay, S. S.; Ling, E. A.; Dheen, S. T. Transcriptome analysis of amoeboid and ramified microglia isolated from the corpus callosum of rat brain. BMC Neurosci., 2012, 13, 64.
97. Logan, T. T.; Villapol, S.; Symes, A. J. TGF-β Superfamily Gene Expression and Induction of the Runx1 Transcription Factor in Adult Neurogenic Regions after Brain Injury. PloS One, 2013, 8(3), e59250.
98. Zusso, M.; Methot, L.; Lo, R.; Greenhalgh, A. D.; David, S.; Stifani, S. Regulation of postnatal forebrain amoeboid microglial cell proliferation and development by the transcription factor runx1. J. Neurosci., 2012, 32(33), 11285-11298.
99. Ginhoux, F.; Greter, M.; Leboeuf, M.; Nandi, S.; See, P.; Gokhan, S.; Mehler, M. F.; Conway, S. J.; Ng, L. G.; Stanley, E. R. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science, 2010, 330(6005), 841-845.
100. Kateb, B.; Van Handel, M.; Zhang, L. Y.; Bronikowski, M. J.; Manohara, H.; Badie, B. Internalization of MWCNTs by microglia: Possible application in immunotherapy of brain tumors. Neuroimage, 2007, 37, S9-S17.
101. Singh, R.; Pantarotto, D.; McCarthy, D.; Chaloin, O.; Hoebeke, J.; Partidos, CD.; Briand, J.-P.; Prato, M.; Bianco, A.; Kostarelos, K. Binding and Condensation of Plasmid DNA onto Functionalized Carbon Nanotubes: Toward the Construction of Nanotube-Based Gene Delivery Vectors. J. Am. Chem. Soc, 2005, 127(12), 4388-4396.
102. Wang, L.; Shi, J.; Zhang, H.; Li, H.; Gao, Y.; Wang, Z.; Wang, H.; Li, L.; Zhang, C; Chen, C; Zhang, Z.; Zhang, Y. Synergistic anticancer effect of RNAi and photothermal therapy mediated by functionalized single-walled carbon nanotubes. Biomaterials, 2013, 34(1), 262-274.
103. Hadjipanayis, C. G.; Machaidze, R.; Kaluzova, M.; Wang, L.; Schuette, A. J.; Chen, H.; Wu, X.; Mao, H. EGFRvIII Antibody-Conjugated Iron Oxide Nanoparticles for Magnetic Resonance Imaging-Guided Convection-Enhanced Delivery and Targeted Therapy of Glioblastoma. Cancer Res., 2010, 70(15), 6303-6312.
104. Guerra, J.; Herrero, M. A.; Carrión, B.; Pérez-Martínez, F. C.; Lucío, M.; Rubio, N.; Meneghetti, M.; Prato, M.; Ceña, V.; Vázquez, E. Carbon nanohorns functionalized with polyamidoamine dendrimers as efficient biocarrier materials for gene therapy. Carbon, 2012, 50(8), 2832-2844.
105. Minami, S. S.; Sun, B.; Popat, K.; Kauppinen, T.; Pleiss, M.; Zhou, Y.; Ward, M.; Floreancig, P.; Mucke, L.; Desai, T.; Gan, L. Selective targeting of microglia by quantum dots. Journal of Neuroinflammation, 2012, 9(1), 22.