Noninvasive and Targeted Gene Delivery into the Brain Using Microbubble-Facilitated Focused Ultrasound

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Hsu, Po Hung ^a   Wei, Kuo Chen ^a   Huang, Chiung Yin ^a   Wen, Chih Jen ^a   Yen, Tzu Chen ^a   Liu, Chao Lin ^b   Lin, Ya Tin ^a   Chen, Jin Chung ^a   Shen, Chia Rui ^a   Liu, Hao Li ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b MING CHI UNIVERSITY OF TECHNOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; GREEN FLUORESCENT PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN REGION; CELL INFILTRATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; HEMISPHERE; IMMUNOFLUORESCENCE TEST; INTRACELLULAR SIGNALING; MALE; MICROBUBBLE FACILITATED FOCUSED ULTRASOUND; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCESS OPTIMIZATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ULTRASOUND; VIRAL GENE DELIVERY SYSTEM; VIRUS GENOME; VIRUS RECOMBINANT; WESTERN BLOTTING;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; CONTRAST MEDIA; DEPENDOVIRUS; FLUORESCENT ANTIBODY TECHNIQUE; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED ICR; MICROBUBBLES; REPRODUCIBILITY OF RESULTS; TRANSDUCTION, GENETIC; ULTRASONICS;

EID: 84874529633     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057682     Document Type: Article

References (55)

1. Mingozzi F, High KA, (2011) Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 12: 341-355.
2. McPhee SW, Janson CG, Li C, Samulski RJ, Camp AS, et al. (2006) Immune responses to AAV in a phase I study for Canavan disease. J Gene Med 8: 577-588.
3. Worgall S, Sondhi D, Hackett NR, Kosofsky B, Kekatpure MV, et al. (2008) Treatment of late infantile neuronal ceroid lipofuscinosis by CNS administration of a serotype 2 adeno-associated virus expressing CLN2 cDNA. Hum Gene Ther 19: 463-474.
4. Christine CW, Starr PA, Larson PS, Eberling JL, Jagust WJ, et al. (2009) Safety and tolerability of putaminal AADC gene therapy for Parkinson disease. Neurology 73: 1662-1669.
5. Mandel RJ, (2010) CERE-110, an adeno-associated virus-based gene delivery vector expressing human nerve growth factor for the treatment of Alzheimer's disease. Curr Opin Mol Ther 12: 240-247.
6. Rapoport SI (1976) Blood-brain barrier in physiology and medicine. New York: Raven Press. xii, 316 p.
7. LeWitt PA, Rezai AR, Leehey MA, Ojemann SG, Flaherty AW, et al. (2011) AAV2-GAD gene therapy for advanced Parkinson's disease: a double-blind, sham-surgery controlled, randomised trial. Lancet Neurol 10: 309-319.
8. Carty N, Lee D, Dickey C, Ceballos-Diaz C, Jansen-West K,et al. Convection-enhanced delivery and systemic mannitol increase gene product distribution of AAV vectors 5, 8, and 9 and increase gene product in the adult mouse brain. J Neurosci Methods 194: 144-153.
9. Bankiewicz KS, Eberling JL, Kohutnicka M, Jagust W, Pivirotto P, et al. (2000) Convection-enhanced delivery of AAV vector in parkinsonian monkeys; in vivo detection of gene expression and restoration of dopaminergic function using pro-drug approach. Exp Neurol 164: 2-14.
10. Carty N, Lee D, Dickey C, Ceballos-Diaz C, Jansen-West K, et al. (2010) Convection-enhanced delivery and systemic mannitol increase gene product distribution of AAV vectors 5, 8, and 9 and increase gene product in the adult mouse brain. J Neurosci Methods 194: 144-153.
11. Burger C, Gorbatyuk OS, Velardo MJ, Peden CS, Williams P, et al. (2004) Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 10: 302-317.
12. Fu H, Muenzer J, Samulski RJ, Breese G, Sifford J, et al. (2003) Self-complementary adeno-associated virus serotype 2 vector: global distribution and broad dispersion of AAV-mediated transgene expression in mouse brain. Mol Ther 8: 911-917.
13. Doran SE, Ren XD, Betz AL, Pagel MA, Neuwelt EA, et al. (1995) Gene expression from recombinant viral vectors in the central nervous system after blood-brain barrier disruption. Neurosurgery 36: 965-970.
14. Duque S, Joussemet B, Riviere C, Marais T, Dubreil L, et al. (2009) Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol Ther 17: 1187-1196.
15. Gray SJ, Matagne V, Bachaboina L, Yadav S, Ojeda SR, et al. (2011) Preclinical differences of intravascular AAV9 delivery to neurons and glia: a comparative study of adult mice and nonhuman primates. Mol Ther 19: 1058-1069.
16. Hynynen K, McDannold N, Sheikov NA, Jolesz FA, Vykhodtseva N, (2005) Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage 24: 12-20.
17. Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA, (2001) Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 220: 640-646.
18. Kinoshita M, McDannold N, Jolesz FA, Hynynen K, (2006) Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound. Biochem Biophys Res Commun 340: 1085-1090.
19. Kinoshita M, McDannold N, Jolesz FA, Hynynen K, (2006) Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption. Proc Natl Acad Sci U S A 103: 11719-11723.
20. Hynynen K, McDannold N, Vykhodtseva N, Raymond S, Weissleder R, et al. (2006) Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery. J Neurosurg 105: 445-454.
21. McDannold N, Clement GT, Black P, Jolesz F, Hynynen K, (2010) Transcranial magnetic resonance imaging- guided focused ultrasound surgery of brain tumors: initial findings in 3 patients. Neurosurgery 66: 323-332 discussion 332.
22. Treat LH, McDannold N, Vykhodtseva N, Zhang Y, Tam K, et al. (2007) Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound. Int J Cancer 121: 901-907.
23. Liu HL, Hua MY, Chen PY, Chu PC, Pan CH, et al. (2010) Blood-brain barrier disruption with focused ultrasound enhances delivery of chemotherapeutic drugs for glioblastoma treatment. Radiology 255: 415-425.
24. Chen PY, Liu HL, Hua MY, Yang HW, Huang CY, et al. (2010) Novel magnetic/ultrasound focusing system enhances nanoparticle drug delivery for glioma treatment. Neuro Oncol 12: 1050-1060.
25. Liu HL, Hua MY, Yang HW, Huang CY, Chu PC, et al. (2010) Magnetic resonance monitoring of focused ultrasound/magnetic nanoparticle targeting delivery of therapeutic agents to the brain. Proc Natl Acad Sci U S A 107: 15205-15210.
26. Huang Q, Deng J, Wang F, Chen S, Liu Y, et al. (2011) Targeted gene delivery to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption. Exp Neurol 233: 350-356.
27. Wu CJ, Huang WC, Chen LC, Shen CR, Kuo ML (2012) Pseudotyped Adeno-Associated Virus 2/9-Delivered CCL11 shRNA Alleviates Lung Inflammation in an Allergen-Sensitized Mouse Model. Hum Gene Ther.
28. Yang CJ, Liu YK, Liu CL, Shen CN, Kuo ML, et al. (2009) Inhibition of acidic mammalian chitinase by RNA interference suppresses ovalbumin-sensitized allergic asthma. Hum Gene Ther 20: 1597-1606.
29. Hu C, Busuttil RW, Lipshutz GS, (2010) RH10 provides superior transgene expression in mice when compared with natural AAV serotypes for neonatal gene therapy. J Gene Med 12: 766-778.
30. Ponnazhagan S, Mukherjee P, Yoder MC, Wang XS, Zhou SZ, et al. (1997) Adeno-associated virus 2-mediated gene transfer in vivo: organ-tropism and expression of transduced sequences in mice. Gene 190: 203-210.
31. Wu Z, Asokan A, Samulski RJ, (2006) Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 14: 316-327.
32. Royo NC, Vandenberghe LH, Ma JY, Hauspurg A, Yu L, et al. (2008) Specific AAV serotypes stably transduce primary hippocampal and cortical cultures with high efficiency and low toxicity. Brain Res 1190: 15-22.
33. Howard DB, Powers K, Wang Y, Harvey BK, (2008) Tropism and toxicity of adeno-associated viral vector serotypes 1, 2, 5, 6, 7, 8, and 9 in rat neurons and glia in vitro. Virology 372: 24-34.
34. Lawlor PA, Bland RJ, Mouravlev A, Young D, During MJ, (2009) Efficient gene delivery and selective transduction of glial cells in the mammalian brain by AAV serotypes isolated from nonhuman primates. Mol Ther 17: 1692-1702.
35. Sheikov N, McDannold N, Vykhodtseva N, Jolesz F, Hynynen K, (2004) Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol 30: 979-989.
36. Liu HL, Wai YY, Chen WS, Chen JC, Hsu PH, et al. (2008) Hemorrhage detection during focused-ultrasound induced blood-brain-barrier opening by using susceptibility-weighted magnetic resonance imaging. Ultrasound Med Biol 34: 598-606.
37. Favre D, Provost N, Blouin V, Blancho G, Cherel Y, et al. (2001) Immediate and long-term safety of recombinant adeno-associated virus injection into the nonhuman primate muscle. Mol Ther 4: 559-566.
38. Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, et al. (2007) Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 369: 2097-2105.
39. Toromanoff A, Cherel Y, Guilbaud M, Penaud-Budloo M, Snyder RO, et al. (2008) Safety and efficacy of regional intravenous (r.i.) versus intramuscular (i.m.) delivery of rAAV1 and rAAV8 to nonhuman primate skeletal muscle. Mol Ther 16: 1291-1299.
40. Ryals RC, Boye SL, Dinculescu A, Hauswirth WW, Boye SE, (2011) Quantifying transduction efficiencies of unmodified and tyrosine capsid mutant AAV vectors in vitro using two ocular cell lines. Mol Vis 17: 1090-1102.
41. Sarra GM, Stephens C, Schlichtenbrede FC, Bainbridge JW, Thrasher AJ, et al. (2002) Kinetics of transgene expression in mouse retina following sub-retinal injection of recombinant adeno-associated virus. Vision Res 42: 541-549.
42. Bennett J, Maguire AM, Cideciyan AV, Schnell M, Glover E, et al. (1999) Stable transgene expression in rod photoreceptors after recombinant adeno-associated virus-mediated gene transfer to monkey retina. Proc Natl Acad Sci U S A 96: 9920-9925.
43. Shevtsova Z, Malik JM, Michel U, Bahr M, Kugler S, (2005) Promoters and serotypes: targeting of adeno-associated virus vectors for gene transfer in the rat central nervous system in vitro and in vivo. Exp Physiol 90: 53-59.
44. Thévenot E JJ, O'Reilly MA, Markham K, Weng YQ, Foust KD, et al. (2012) Targeted Delivery of Self-Complementary Adeno-Associated Virus Serotype 9 to the Brain, Using Magnetic Resonance Imaging-Guided Focused Ultrasound. Hum Gene Ther.
45. Meijer DH, Maguire CA, LeRoy SG, Sena-Esteves M, (2009) Controlling brain tumor growth by intraventricular administration of an AAV vector encoding IFN-beta. Cancer Gene Ther 16: 664-671.
46. Kaplitt MG, Leone P, Samulski RJ, Xiao X, Pfaff DW, et al. (1994) Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet 8: 148-154.
47. McCown TJ, Xiao X, Li J, Breese GR, Samulski RJ, (1996) Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res 713: 99-107.
48. Davidson BL, Stein CS, Heth JA, Martins I, Kotin RM, et al. (2000) Recombinant adeno-associated virus type 2, 4, and 5 vectors: transduction of variant cell types and regions in the mammalian central nervous system. Proc Natl Acad Sci U S A 97: 3428-3432.
49. Summerford C, Samulski RJ, (1998) Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72: 1438-1445.
50. Properzi F, Lin R, Kwok J, Naidu M, van Kuppevelt TH, et al. (2008) Heparan sulphate proteoglycans in glia and in the normal and injured CNS: expression of sulphotransferases and changes in sulphation. Eur J Neurosci 27: 593-604.
51. Chen H, McCarty DM, Bruce AT, Suzuki K, (1998) Gene transfer and expression in oligodendrocytes under the control of myelin basic protein transcriptional control region mediated by adeno-associated virus. Gene Ther 5: 50-58.
52. Chen H, McCarty DM, Bruce AT, Suzuki K, (1999) Oligodendrocyte-specific gene expression in mouse brain: use of a myelin-forming cell type-specific promoter in an adeno-associated virus. J Neurosci Res 55: 504-513.
53. Xing X, Zhang S, Chang JY, Tucker SD, Chen H, et al. (1998) Safety study and characterization of E1A-liposome complex gene-delivery protocol in an ovarian cancer model. Gene Ther 5: 1538-1544.
54. Alisky JM, Hughes SM, Sauter SL, Jolly D, Dubensky TW Jr, et al. (2000) Transduction of murine cerebellar neurons with recombinant FIV and AAV5 vectors. Neuroreport 11: 2669-2673.
55. Klein RL, Dayton RD, Tatom JB, Diaczynsky CG, Salvatore MF, (2008) Tau expression levels from various adeno-associated virus vector serotypes produce graded neurodegenerative disease states. Eur J Neurosci 27: 1615-1625.