Brain-derived neurotrophic factor delivered to the brain using poly (lactide-co-glycolide) nanoparticles improves neurological and cognitive outcome in mice with traumatic brain injury

Drug Delivery

Volumn 23, Issue 9, 2016, Pages 3520-3528

  Khalin, Igor ^a   Alyautdin, Renad ^b   Wong, Tin Wui ^c   Gnanou, Justin ^a   Kocherga, Ganna ^d   Kreuter, Jörg ^e  

^a NATIONAL DEFENCE UNIVERSITY OF MALAYSIA   (Malaysia)

^b Scientific Centre for Expert Evaluation of Medicinal Products   (Russian Federation)

^c UNIVERSITI TEKNOLOGI MARA   (Malaysia)

^d Ophthalmic Microsurgery Department International Medical Center Oftalmika   (Ukraine)

^e GOETHE UNIVERSITY   (Germany)

Author keywords

Blood brain barrier; brain derived neurotrophic factor; drug delivery; nanoparticles; traumatic brain injury

Indexed keywords

ABRINEURIN; NANOCARRIER; NEUROPROTECTIVE AGENT; POLOXAMER; POLYGLACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR; LACTIC ACID; NANOPARTICLE; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER; SURFACTANT;

ADSORPTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DISPERSION; DRUG BRAIN LEVEL; DRUG DELIVERY SYSTEM; DRUG FORMULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HEAD INJURY; IN VIVO STUDY; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; PASSIVE AVOIDANCE TEST; PRIORITY JOURNAL; TRAUMATIC BRAIN INJURY; ANIMAL; BLOOD BRAIN BARRIER; BRAIN; BRAIN INJURIES, TRAUMATIC; C57BL MOUSE; CHEMISTRY; COGNITION; DRUG EFFECTS; HALF LIFE TIME; METABOLISM;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN INJURIES, TRAUMATIC; BRAIN-DERIVED NEUROTROPHIC FACTOR; COGNITION; HALF-LIFE; LACTIC ACID; MALE; MICE; MICE, INBRED C57BL; NANOPARTICLES; NEUROPROTECTIVE AGENTS; POLOXAMER; POLYGLYCOLIC ACID; SURFACE-ACTIVE AGENTS;

EID: 84978484103     PISSN: 10717544     EISSN: 15210464     Source Type: Journal    
DOI: 10.1080/10717544.2016.1199609     Document Type: Article

References (67)

1. Allen SJ, Watson JJ, Shoemark DK, et al. (2013). GDNF, NGF and BDNF as therapeutic options for neurodegeneration. Pharmacol Ther 138:155–75
2. Alyautdin R, Kreuter J., (2000). Using nanoparticles to target drugs to the central nervous system. In:Kreuter J, Begley DJ, Bradbury MW, eds. The blood-brain barrier and drug delivery to the CNS. USA:CRC Press
3. Alyautdin RN, Petrov VE, Langer K, et al. (1997). Delivery of loperamide across the blood-brain barrier with polysorbate 80-coated polybutylcyanoacrylate nanoparticles. Pharm Res 14:325–8
4. Alyautdin RN, Tezikov EB, Ramge P, et al. (1998). Significant entry of tubocurarine into the brain of rats by adsorption to polysorbate 80-coated polybutylcyanoacrylate nanoparticles:an in situ brain perfusion study. J Microencapsul 15:67–74
5. Anderson KD, Alderson RF, Altar CA, et al. (1995). Differential distribution of exogenous BDNF, NGF, and NT‐3 in the brain corresponds to the relative abundance and distribution of high‐affinity and low‐affinity neurotrophin receptors. J Comp Neurol 357:296–317
6. Başkaya MK, Rao AM, Doğan A, et al. (1997). The biphasic opening of the blood–brain barrier in the cortex and hippocampus after traumatic brain injury in rats. Neurosci Lett 226:33–6
7. Berninger B, García DE, Inagaki N, et al. (1993). BDNF and NT-3 induce intracellular Ca2+ elevation in hippocampal neurones. Neuroreport 4:1303–6
8. Blaha GR, Raghupathi R, Saatman KE, McIntosh TK., (2000). Brain-derived neurotrophic factor administration after traumatic brain injury in the rat does not protect against behavioral or histological deficits. Neuroscience 99:483–93
9. Blurton-Jones M, Kitazawa M, Martinez-Coria H, et al. (2009). Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci U S A 106:13594–9
10. Casalbore P, Barone I, Felsani A, et al. (2010). Neural stem cells modified to express BDNF antagonize trimethyltin-induced neurotoxicity through PI3K/Akt and MAP kinase pathways. J Cell Physiol 224:710–21
11. Chodobski A, Zink BJ, Szmydynger-Chodobska J., (2011). Blood-brain barrier pathophysiology in traumatic brain injury. Transl Stroke Res 2:492–516
12. Cowansage KK, Ledoux JE, Monfils MH., (2010). Brain-derived neurotrophic factor:a dynamic gatekeeper of neural plasticity. Curr Mol Pharmacol 3:12–29
13. Flierl MA, Stahel PF, Beauchamp KM, et al. (2009). Mouse closed head injury model induced by a weight-drop device. Nat Protoc 4:1328–37
14. Gelperina S, Maksimenko O, Khalansky A, et al. (2010). Drug delivery to the brain using surfactant-coated poly(lactide-co-glycolide) nanoparticles:influence of the formulation parameters. Eur J Pharm Biopharm 74:157–63
15. Géral C, Angelova A, Lesieur S., (2013). From molecular to nanotechnology strategies for delivery of neurotrophins:emphasis on brain-derived neurotrophic factor (BDNF). Pharmaceutics 5:127–67
16. Grafman J, Salazar AM., 2015. Traumatic brain injury, Part I:handbook of clinical neurology (Series editors:Aminoff, Boller and Swaab). Amsterdam:Elsevier
17. Graham Di GT, McIntosh TK., 2002. Trauma. In:Graham Di LP, ed. Greenfield's neuropathology. London:Arnold
18. Grazu VMM., 2012. Nanocarriers as nanomedicines:design concepts and recent advances. In:De La Fuente JGV, ed. Nanobiotechnology inorganic nanoparticles vs organic nanoparticle. Amsterdam:Elsevier
19. Griesbach GS, Hovda DA, Molteni R, Gomez-Pinilla F., (2002). Alterations in BDNF and synapsin I within the occipital cortex and hippocampus after mild traumatic brain injury in the developing rat:reflections of injury-induced neuroplasticity. J Neurotrauma 19:803–14
20. Group BS., (1999). A controlled trial of recombinant methionyl human BDNF in ALS:the BDNF Study Group (Phase III). Neurology 52:1427–33
21. Guidelines. (2007). Guidelines for the management of severe traumatic brain injury. J Neurotrauma 24:S1–106
22. Hicks RR, Zhang L, Dhillon HS, et al. (1998). Expression of trkB mRNA is altered in rat hippocampus after experimental brain trauma. Brain Res Mol Brain Res 59:264–8
23. Kabadi SV, Faden AI., (2014). Neuroprotective strategies for traumatic brain injury:improving clinical translation. Int J Mol Sci 15:1216–36
24. Khalin I, Alyautdin R, Kocherga G, Bakar MA., (2015). Targeted delivery of brain-derived neurotrophic factor for the treatment of blindness and deafness. Int J Nanomedicine 10:3245–67
25. Khalin I, Jamari NLA, Razak NBA, et al. (2016). A mouse model of weight-drop closed head injury:emphasis on cognitive and neurological deficiency. Neural Regen Res 11:630–5
26. Kiprianova I, Sandkuhler J, Schwab S, et al. (1999). Brain-derived neurotrophic factor improves long-term potentiation and cognitive functions after transient forebrain ischemia in the rat. Exp Neurol 159:511–19
27. Klein AB, Williamson R, Santini MA, et al. (2011). Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol 14:347–53
28. Kreuter J., (2014). Drug delivery to the central nervous system by polymeric nanoparticles:what do we know? Adv Drug Deliv Rev 71:2–14
29. Kreuter J, Alyautdin RN, Kharkevich DA, Ivanov AA., (1995). Passage of peptides through the blood-brain barrier with colloidal polymer particles (nanoparticles). Brain Res 674:171–4
30. Kume T, Kouchiyama H, Kaneko S, et al. (1997). BDNF prevents NO mediated glutamate cytotoxicity in cultured cortical neurons. Brain Res 756:200–4
31. Kurakhmaeva KB, Djindjikhashvili IA, Petrov VE, et al. (2009). Brain targeting of nerve growth factor using poly(butyl cyanoacrylate) nanoparticles. J Drug Target 17:564–74
32. Li JT, Caldwell KD, Rapoport N., (1994). Surface properties of pluronic-coated polymeric colloids. Langmuir 10:4475–82
33. Liu Z, Ma D, Feng G, et al. (2007). Recombinant AAV-mediated expression of human BDNF protects neurons against cell apoptosis in Abeta-induced neuronal damage model. J Huazhong Univ Sci Technolog Med Sci 27:233–6
34. Lu JM, Wang X, Marin-Muller C, et al. (2009). Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Rev Mol Diagn 9:325–41
35. Ma H, Yu B, Kong L, et al. (2012). Neural stem cells over-expressing brain-derived neurotrophic factor (BDNF) stimulate synaptic protein expression and promote functional recovery following transplantation in rat model of traumatic brain injury. Neurochem Res 37:69–83
36. Mahmood A, Lu D, Wang L, Chopp M., (2002). Intracerebral transplantation of marrow stromal cells cultured with neurotrophic factors promotes functional recovery in adult rats subjected to traumatic brain injury. J Neurotrauma 19:1609–17
37. Mey J, Thanos S., (1993). Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res 602:304–17
38. Michaelis K, Hoffmann MM, Dreis S, et al. (2006). Covalent linkage of apolipoprotein e to albumin nanoparticles strongly enhances drug transport into the brain. J Pharmacol Exp Ther 317:1246–53
39. Moghimi SM., (1997). Prolonging the circulation time and modifying the body distribution of intravenously injected polystyrene nanospheres by prior intravenous administration of poloxamine-908. A 'hepatic-blockade' event or manipulation of nanosphere surface in vivo? Biochim Biophys Acta 1336:1–6
40. Moghimi SM, Hunter AC., (2000). Poloxamers and poloxamines in nanoparticle engineering and experimental medicine. Trends Biotechnol 18:412–20
41. Numakawa T, Suzuki S, Kumamaru E, et al. (2010). BDNF function and intracellular signaling in neurons. Histol Histopathol 25:237–58
42. Oyesiku NM, Evans CO, Houston S, et al. (1999). Regional changes in the expression of neurotrophic factors and their receptors following acute traumatic brain injury in the adult rat brain. Brain Res 833:161–72
43. Pan W, Banks WA, Fasold MB, et al. (1998). Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology 37:1553–61
44. Pardridge WM., (2016). CSF, blood-brain barrier, and brain drug delivery. Expert Opin Drug Deliv. [Epub ahead of print]. DOI:10.1517/17425247.2016.1171315
45. Pardridge WM, Kang YS, Buciak JL., (1994). Transport of human recombinant brain-derived neurotrophic factor (BDNF) through the rat blood-brain barrier in vivo using vector-mediated peptide drug delivery. Pharm Res 11:738–46
46. Petri B, Bootz A, Khalansky A, et al. (2007). Chemotherapy of brain tumour using doxorubicin bound to surfactant-coated poly(butyl cyanoacrylate) nanoparticles:revisiting the role of surfactants. J Control Release 117:51–8
47. Poduslo JF, Curran GL., (1996). Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors:NGF, CNTF, NT-3, BDNF. Brain Res Mol Brain Res 36:280–6
48. Quertemont E, Tambour S, Bernaerts P, et al. (2004). Behavioral characterization of acetaldehyde in C57BL/6J mice:locomotor, hypnotic, anxiolytic and amnesic effects. Psychopharmacology (Berl) 177:84–92
49. Reichardt LF., (2006). Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361:1545–64
50. Sakane T, Pardridge WM., (1997). Carboxyl-directed pegylation of brain-derived neurotrophic factor markedly reduces systemic clearance with minimal loss of biologic activity. Pharm Res 14:1085–91
51. Schroeder U, Schroeder H, Sabel BA., (2000). Body distribution of 3H-labelled dalargin bound to poly(butyl cyanoacrylate) nanoparticles after i.v. injections to mice. Life Sci 66:495–502
52. Sharma A, Madhunapantula SV, Robertson GP., (2012). Toxicological considerations when creating nanoparticle-based drugs and drug delivery systems. Expert Opin Drug Metab Toxicol 8:47–69
53. Singh M, Sumien N, Kyser C, Simpkins JW., (2008). Estrogens and progesterone as neuroprotectants:what animal models teach us. Front Biosci 13:1083–9
54. Smith DH, Hicks R, Povlishock JT., (2013). Therapy development for diffuse axonal injury. J Neurotrauma 30:307–23
55. Steiniger SC, Kreuter J, Khalansky AS, et al. (2004). Chemotherapy of glioblastoma in rats using doxorubicin-loaded nanoparticles. Int J Cancer 109:759–67
56. Tosi G, Vergoni AV, Ruozi B, et al. (2010). Sialic acid and glycopeptides conjugated PLGA nanoparticles for central nervous system targeting:in vivo pharmacological evidence and biodistribution. J Control Release 145:49–57
57. Wagner S, Zensi A, Wien SL, et al. (2012). Uptake mechanism of ApoE-modified nanoparticles on brain capillary endothelial cells as a blood-brain barrier model. PLoS One 7:e32568
58. Wallace SJ, Li J, Nation RL, Boyd BJ., (2012). Drug release from nanomedicines:selection of appropriate encapsulation and release methodology. Drug Deliv Transl Res 2:284–92
59. Wang Z, Yao W, Deng Q, et al. (2013). Protective effects of BDNF overexpression bone marrow stromal cell transplantation in rat models of traumatic brain injury. J Mol Neurosci 49:409–16
60. Wohlfart S, Gelperina S, Kreuter J., (2012). Transport of drugs across the blood-brain barrier by nanoparticles. J Control Release 161:264–73
61. Wu CH, Hung TH, Chen CC, et al. (2014). Post-injury treatment with 7,8-dihydroxyflavone, a TrkB receptor agonist, protects against experimental traumatic brain injury via PI3K/Akt signaling. PLoS One 9:e113397
62. Xiong Y, Mahmood A, Chopp M., (2013). Animal models of traumatic brain injury. Nat Rev Neurosci 14:128–42
63. Yan Q, Matheson C, Sun J, et al. (1994). Distribution of intracerebral ventricularly administered neurotrophins in rat brain and its correlation with trk receptor expression. Exp Neurol 127:23–36
64. Zensi A, Begley D, Pontikis C, et al. (2009). Albumin nanoparticles targeted with Apo E enter the CNS by transcytosis and are delivered to neurones. J Control Release 137:78–86
65. Zhang J, Geula C, Lu C, et al. (2003). Neurotrophins regulate proliferation and survival of two microglial cell lines in vitro. Exp Neurol 183:469–81
66. Zheng WH, Quirion R., (2004). Comparative signaling pathways of insulin-like growth factor-1 and brain-derived neurotrophic factor in hippocampal neurons and the role of the PI3 kinase pathway in cell survival. J Neurochem 89:844–52
67. Zhu JM, Zhao YY, Chen SD, et al. (2011). Functional recovery after transplantation of neural stem cells modified by brain-derived neurotrophic factor in rats with cerebral ischaemia. J Int Med Res 39:488–98