Activation of signaling pathways following localized delivery of systemically administered neurotrophic factors across the bloodbrain barrier using focused ultrasound and microbubbles

Physics in Medicine and Biology

Volumn 57, Issue 7, 2012, Pages

  Baseri, Babak ^a   Choi, James J ^a   Deffieux, Thomas ^a   Samiotaki, Gesthimani ^a   Tung, Yao Sheng ^a   Olumolade, Oluyemi ^a   Small, Scott A ^b   Morrison, Barclay ^a   Konofagou, Elisa E ^a,b  

^a Columbia University ^*  (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD-BRAIN BARRIER; BRAIN-DERIVED NEUROTROPHIC FACTORS; FOCUSED ULTRASOUND; HIPPOCAMPAL NEURONS; LOCALIZED DELIVERY; MICROBUBBLES; MOLECULAR EFFECT; MOLECULAR LEVELS; NEUROPROTECTIVE EFFECTS; NEUROTROPHIC FACTORS; SIGNALING PATHWAYS; WILD TYPES;

BRAIN; DRUG DELIVERY; ENZYME INHIBITION; MAMMALS; ULTRASONICS;

ULTRASONIC APPLICATIONS;

NERVE GROWTH FACTOR;

ANIMAL; ARTICLE; BLOOD BRAIN BARRIER; C57BL MOUSE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOLOGY; DRUG DELIVERY SYSTEM; DRUG EFFECT; FEASIBILITY STUDY; HIPPOCAMPUS; MALE; METABOLISM; METHODOLOGY; MICROBUBBLE; MOUSE; NERVE CELL; SIGNAL TRANSDUCTION; ULTRASOUND;

ANIMALS; BLOOD-BRAIN BARRIER; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DRUG DELIVERY SYSTEMS; FEASIBILITY STUDIES; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICROBUBBLES; NERVE GROWTH FACTORS; NEURONS; SIGNAL TRANSDUCTION; ULTRASONICS;

EID: 84863337655     PISSN: 00319155     EISSN: 13616560     Source Type: Journal    
DOI: 10.1088/0031-9155/57/7/N65     Document Type: Article

References (44)

1. Altar C A, Siuciak J A, Wright P, Ip N Y, Lindsay R M and Wiegand S J 1994 In situ hybridization of trkB and trkC receptor mRNA in rat forebrain and association with high-affinity binding of [125I]BDNF, [125I]NT-4/5 and [125I]NT-3 Eur. J. Neurosci. 6 1389405 (Pubitemid 24280898)
2. Baseri B, Choi J J, Tung Y S and Konofagou E E 2010 Multi-modality safety assessment of bloodbrain barrier opening using focused ultrasound and definity microbubbles: a short-term study Ultrasound Med. Biol. 36 144559
3. Benisty S, Boissiere F, Faucheux B, Agid Y and Hirsch E C 1998 trkB messenger RNA expression in normal human brain and in the substantia nigra of Parkinsonian patients: an in situ hybridization study Neuroscience 86 81326 (Pubitemid 28298738)
4. Bobo R H, Laske D W, Akbasak A, Morrison P F, Dedrick R L and Oldfield E H 1994 Convection-enhanced delivery of macromolecules in the brain Proc. Natl Acad. Sci. USA 91 207680 (Pubitemid 24092045)
5. Boulanger L M and Poo M M 1999 Presynaptic depolarization facilitates neurotrophin-induced synaptic potentiation Nature Neurosci. 2 34651
6. Choi J J, Pernot M, Brown T R, Small S A and Konofagou E E 2007a Spatio-temporal analysis of molecular delivery through the bloodbrain barrier using focused ultrasound Phys. Med. Biol. 52 550930 (Pubitemid 350056681)
7. Choi J J, Pernot M, Small S A and Konofagou E E 2007b Noninvasive, transcranial and localized opening of the bloodbrain barrier using focused ultrasound in mice Ultrasound Med. Biol. 33 95104 (Pubitemid 44959316)
8. Choi J J, Feshitan J A, Baseri B, Wang S, Tung Y S, Borden M A and Konofagou E E 2010a Microbubble-size dependence of focused ultrasound-induced bloodbrain barrier opening in mice in vivo IEEE Trans. Biomed. Eng. 57 14554
9. Choi J J, Wang S, Tung Y S, Morrison B III and Konofagou E E 2010b Molecules of various pharmacologically-relevant sizes can cross the ultrasound-induced bloodbrain barrier opening in vivo Ultrasound Med. Biol. 36 5867
10. Ciammola A, Sassone J, Cannella M, Calza S, Poletti B, Frati L, Squitieri F and Silani V 2007 Low brain-derived neurotrophic factor (BDNF) levels in serum of Huntington's disease patients Am. J. Med. Genet B 144B 5747 (Pubitemid 46983172)
11. Connor B, Young D, Yan Q, Faull R L, Synek B and Dragunow M 1997 Brain-derived neurotrophic factor is reduced in Alzheimer's disease Brain Res. Mol. Brain Res. 49 7181 (Pubitemid 27453116)
12. Deffieux T and Konofagou E E 2010 Numerical study and experimental validation of a simple transcranial focused ultrasound system applied to bloodbrain barrier opening IEEE Trans. Ultrason. Ferroelectr. Freq. Control 57 263753
13. Eisch A J, Bolanos C A, de Wit J, Simonak R D, Pudiak C M, Barrot M, Verhaagen J and Nestler E J 2003 Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: a role in depression Biol. Psychiatry 54 9941005 (Pubitemid 37415034)
14. Hagg T 1998 Neurotrophins prevent death and differentially affect tyrosine hydroxylase of adult rat nigrostriatal neurons in vivo Exp. Neurol. 149 18392 (Pubitemid 28091027)
15. Hofer M, Pagliusi S R, Hohn A, Leibrock J and Barde Y A 1990 Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain EMBO J. 9 245964
16. Howells D W, Porritt M J, Wong J Y, Batchelor P E, Kalnins R, Hughes A J and Donnan G A 2000 Reduced BDNF mRNA expression in the Parkinson's disease substantia nigra Exp. Neurol. 166 12735
17. Huang E J and Reichardt L F 2001 Neurotrophins: roles in neuronal development and function Annu. Rev. Neurosci. 24 677736 (Pubitemid 32695243)
18. Hynynen K, McDannold N, Vykhodtseva N and Jolesz F A 2001 Noninvasive MR imaging-guided focal opening of the bloodbrain barrier in rabbits Radiology 220 6406 (Pubitemid 32799969)
19. Jordao J F, Ayala-Grosso C A, Markham K, Huang Y, Chopra R, McLaurin J, Hynynen K and Aubert I 2010 Antibodies targeted to the brain with image-guided focused ultrasound reduces amyloid-beta plaque load in the TgCRND8 mouse model of Alzheimer's disease PLoS ONE 5 e10549
20. Kinoshita M, McDannold N, Jolesz F A and Hynynen K 2006a Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced bloodbrain barrier disruption Proc. Natl Acad. Sci. USA 103 1171923 (Pubitemid 44182517)
21. Kinoshita M, McDannold N, Jolesz F A and Hynynen K 2006b Targeted delivery of antibodies through the bloodbrain barrier by MRI-guided focused ultrasound Biochem. Biophys. Res. Commun. 340 108590 (Pubitemid 43083389)
22. Koyama R and Ikegaya Y 2005 To BDNF or not to BDNF: that is the epileptic hippocampus Neuroscientist 11 2827 (Pubitemid 41040857)
23. Kroll R A and Neuwelt E A 1998 Outwitting the bloodbrain barrier for therapeutic purposes: osmotic opening and other means Neurosurgery 42 1099100 (discussion) (Pubitemid 28196521)
24. Lee J, Fukumoto H, Orne J, Klucken J, Raju S, Vanderburg C R, Irizarry M C, Hyman B T and Ingelsson M 2005 Decreased levels of BDNF protein in Alzheimer temporal cortex are independent of BDNF polymorphisms Exp. Neurol. 194 916 (Pubitemid 40719746)
25. Liu H L, Wai Y Y, Chen W S, Chen J C, Hsu P H, Wu X Y, Huang W C, Yen T C and Wang J J 2008 Hemorrhage detection during focused-ultrasound induced bloodbrain-barrier opening by using susceptibility-weighted magnetic resonance imaging Ultrasound Med. Biol. 34 598606
26. Lonze B E and Ginty D D 2002 Function and regulation of CREB family transcription factors in the nervous system Neuron 35 60523 (Pubitemid 35229980)
27. Marquet F, Tung Y-S and Konofagou E E 2010 Feasibility study of a clinical bloodbrain opening ultrasound system Nano Life 1 30922
28. Marquet F, Tung Y-S, Teichert T, Ferrera V and Konofagou E E 2011 Noninvasive, transient and selective bloodbrain barrier opening in non-human primates in vivo PLoS ONE 6 e225982011
29. Martinowich K, Manji H and Lu B 2007 New insights into BDNF function in depression and anxiety Nature Neurosci. 10 108993 (Pubitemid 47339961)
30. McDannold N, Vykhodtseva N, Raymond S, Jolesz F A and Hynynen K 2005 MRI-guided targeted bloodbrain barrier disruption with focused ultrasound: histological findings in rabbits Ultrasound Med. Biol. 31 152737 (Pubitemid 41606266)
31. Nagahara A H et al 2009 Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease Nature Med. 15 3317
32. Pardridge W M 2005 The bloodbrain barrier: bottleneck in brain drug development NeuroRx 2 314 (Pubitemid 40128022)
33. Raymond S B, Treat L H, Dewey J D, McDannold N J, Hynynen K and Bacskai B J 2008 Ultrasound enhanced delivery of molecular imaging and therapeutic agents in Alzheimer's disease mouse models PLoS ONE 3 e2175
34. Sakane T and Pardridge W M 1997 Carboxyl-directed pegylation of brain-derived neurotrophic factor markedly reduces systemic clearance with minimal loss of biologic activity Pharm. Res. 14 108591 (Pubitemid 27371411)
35. Samiotaki M, Vlachos F, Tung Y-S, Feshitan J, Borden M and Konofagou E E 2011 A quantitative pressure and microbubble-size dependence study of focused ultrasound-induced bloodbrain barrier opening reversibility in vivo using MRI 19 August, doi: 10.1002/mrm.23063 (Epub ahead of print)
36. Sheikov N, McDannold N, Sharma S and Hynynen K 2008 Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium Ultrasound Med. Biol. 34 1093104 (Pubitemid 351893156)
37. Shirayama Y, Chen A C, Nakagawa S, Russell D S and Duman R S 2002 Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression J. Neurosci. 22 325161 (Pubitemid 35379212)
38. Simmons D A, Rex C S, Palmer L, Pandyarajan V, Fedulov V, Gall C M and Lynch G 2009 Up-regulating BDNF with an ampakine rescues synaptic plasticity and memory in Huntington's disease knockin mice Proc. Natl Acad. Sci. USA 106 490611
39. Treat L H, McDannold N, Vykhodtseva N, Zhang Y, Tam K and Hynynen K 2007 Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound Int. J. Cancer 121 9017 (Pubitemid 47106223)
40. Tung Y, Marquet M, Teichert T, Ferrera V and Konofagou E E 2011 Feasibility of noninvasive cavitation-guided bloodbrain barrier opening using focused ultrasound and microbubbles in nonhuman primates Appl. Phys. Lett. 98
41. Vlachos F, Tung Y S and Konofagou E E 2010 Permeability assessment of the focused ultrasound-induced bloodbrain barrier opening using dynamic contrast-enhanced MRI Phys. Med. Biol. 55 545166
42. Waterhouse E G and Xu B 2009 New insights into the role of brain-derived neurotrophic factor in synaptic plasticity Mol. Cell. Neurosci. 42 819
43. Weaver M and Laske D W 2003 Transferrin receptor ligand-targeted toxin conjugate (Tf-CRM107) for therapy of malignant gliomas J. Neurooncol. 65 313 (Pubitemid 37441310)
44. Yan Q, Rosenfeld R D, Matheson C R, Hawkins N, Lopez O T, Bennett L and Welcher A A 1997 Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system Neuroscience 78 43148 (Pubitemid 27170335)