Effect of Focused Ultrasound Applied With an Ultrasound Contrast Agent on the Tight Junctional Integrity of the Brain Microvascular Endothelium

Ultrasound in Medicine and Biology

Volumn 34, Issue 7, 2008, Pages 1093-1104

  Sheikov, Nickolai ^a   McDannold, Nathan ^a   Sharma, Shipra ^a   Hynynen, Kullervo ^b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Blood brain barrier; Immunoelectron microscopy; Tight junctions; Ultrasound

Indexed keywords

ACOUSTIC WAVES; CHEMOTHERAPY; DRUG DELIVERY; DRUG DOSAGE; LANTHANUM; PLANTS (BOTANY); RELIABILITY; THICKNESS MEASUREMENT; ULTRASONICS;

BLOOD-BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; CLAUDIN; CONTRAST AGENT; FOCUSED ULTRASOUND; HORSE RADISH PEROXIDASE; IMMUNOELECTRON MICROSCOPY; LANTHANUM CHLORIDES; MICROVASCULAR ENDOTHELIUM; OCCLUDIN; OPTISON; POTENTIAL METHODS; PROTEIN EXPRESSIONS; QUANTITATIVE EVALUATION; RAT BRAIN; TARGETED DRUG DELIVERY; TIGHT-JUNCTIONS; TRANS-MEMBRANE PROTEINS; ULTRASOUND; ULTRASOUND CONTRAST AGENT;

ULTRASONIC IMAGING;

ANTIBODY; CLAUDIN 1; CLAUDIN 1 ANTIBODY; CLAUDIN 5; CLAUDIN 5 ANTIBODY; GADOLINIUM PENTETATE; HORSERADISH PEROXIDASE; LANTHANUM CHLORIDE; MEMBRANE PROTEIN; OCCLUDIN; OCCLUDIN ANTIBODY; PERFLUTREN; PROTEIN ZO1; ZO1 PROTEIN ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN MICROCIRCULATION; CELL DENSITY; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG DELIVERY SYSTEM; GENE TARGETING; GENE TRANSFER; IMMUNOELECTRON MICROSCOPY; INTRACELLULAR TRANSPORT; MALE; MEMBRANE DAMAGE; MEMBRANE PERMEABILITY; MICROVASCULATURE; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; TIGHT JUNCTION; TRANSPORT KINETICS; ULTRASOUND; VASCULAR ENDOTHELIUM;

ALBUMINS; ANIMALS; BLOOD-BRAIN BARRIER; CONTRAST MEDIA; ENDOTHELIUM, VASCULAR; FLUOROCARBONS; HORSERADISH PEROXIDASE; MALE; MEMBRANE PROTEINS; MICROCIRCULATION; MICROSCOPY, IMMUNOELECTRON; PERMEABILITY; RATS; RATS, SPRAGUE-DAWLEY; SONICATION; TIGHT JUNCTIONS;

EID: 45949097554     PISSN: 03015629     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2007.12.015     Document Type: Article

References (48)

1. Abramoff M.D., Magelhaes P.J., and Ram S.J. Image processing with ImageJ. Biophotonics Int 11 (2004) 36-1142
2. Andras I.E., Deli M.A., Veszelka S., Hayashi K., Hennig B., and Toborek M. The NMDA and AMPA/KA receptors are involved in glutamate-induced alterations of occludin expression and phosphorylation in brain endothelial cells. J Cereb Blood Flow Metab 27 (2007) 1431-1443
3. Balda M.S., Flores-Maldonado C., Cereijido M., and Matter K. Multiple domains of occludin are involved in the regulation of paracellular permeability. J Cell Biochem 78 (2000) 85-96
4. Bouldin T.W., and Krigman M.R. Differential permeability of cerebral capillary and choroid plexus to lanthanum ion. Brain Res 99 (1975) 444-448
5. Brightman M.W., and Reese T.S. Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40 (1969) 648-677
6. Brightman M.W., Klatzo I., Olsson Y., and Reese T.S. The blood-brain barrier to proteins under normal and pathological conditions. J Neurol Sci 10 (1970) 215-239
7. Choi J.J., Pernot M., Small S.A., and Konofagou E.E. Noninvasive, transcranial and localized opening of the blood-brain barrier using focused ultrasound in mice. Ultrasound Med Biol 33 (2007) 95-104
8. 2-macroglobulin. Mol Cell Proteomics 2 (2003) 234-241
9. Dobrogowska D.H., and Vorbrodt A.W. Immunogold localization of tight junctional proteins in normal and osmotically-affected rat blood-brain barrier. J Mol Histol 35 (2004) 529-539
10. Engelhardt B. Development of the blood-brain barrier interface. From ontogeny to artificial interfaces. Volume 1. In: Dermietzel R., Spray D.C., and Nedregaard M. (Eds). Blood-brain barriers (2006), VCH Verlag GmbH and Co. KGaA, Weinheim 27
11. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonemura S., Tsukita S., and Tsukita S. Occludin-a novel integral membrane-protein localizing at tight junctions. J Cell Biol 123 (1993) 1777-1788
12. Furuse M., Fujita K., Hiiragi T., Fujimoto K., and Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin J. Cell Biol 141 (1998) 1539-1550
13. Gonzales-Mariscal L., Chavez de Ramirez B., and Avila-Flores A. MAGUK proteins: Structure and role in the tight junction. Cell Dev Biol 11 (2000) 315-324
14. Goss S.A., Johnston R.L., and Dunn F. Comprehensive compilation of empirical ultrasonic properties of mammalian tissues. J Acoust Soc Am 64 (1978) 423-457
15. Gurney K.J., Estrada E.Y., and Rosenberg G.A. Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiol Dis 23 (2006) 87-96
16. Harhaj N.S., Felinski E.A., Wolpert E.B., Sundstrom J.M., Gardner T.W., and Antonetti D.A. VEGF activation of protein-kinase C stimulates occludin phosphorylation and contributes to endothelial permeability. Invest Ophthalmol Vis Sci 47 (2006) 5106-5115
17. Heiskala M., Peterson P.A., and Yang Y. The roles of claudin superfamily proteins in paracellular transport. Traffic 2 (2001) 92-98
18. Hirano A., Kawanami T., and Llena J.F. Electron microscopy of the blood-brain barrier in disease. Microsc Res Tech 27 (1994) 543-556
19. Hirase T., Staddon J.M., Saitou M., Ando Akatsuka Y., Itoh M., Furuse M., Fujimoto K., Tsukita S., and Rubin L.L. Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 110 (1997) 1603-1613
20. Hoffstein S., Gennaro D.E., Fox A.C., Hirsch J., Streuli F., and Weissmann G. Colloidal Lanthanum as a marker for impaired plasma membrane permeability in ischemic dog myocardium. Am J Pathol 79 (1975) 207-218
21. Huber D., Balda M.S., and Matter K. Occludin modulates transepithelial migration of neutrophils. J Biol Chem 275 (2000) 5773-5778
22. Hynynen K., Vykhodtseva N.I., Chung A.H., Sorrentino V., Colucci V., and Jolesz F.A. Thermal effects of focused ultrasound on the brain: determination with MR imaging. Radiology 204 (1997) 247-253
23. Hynynen K., McDannold N., Vykhodtseva N., and Jolesz F.A. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 220 (2001) 640-646
24. Hynynen K., McDannold N., Sheikov N.A., Jolesz F.A., and Vykhodtseva N. Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage 24 (2005) 12-20
25. Hynynen K., McDannold N., Vykhodtseva N., Raymond S., Weissleder R., Jolesz F.A., and Sheikov N. Focal disruption of the blood-brain barrier by 260 KHz ultrasound bursts-A method for molecular imaging and targeted drug delivery. J Neurosurg 105 (2006) 445-454
26. Juffermans L.J., Dijkmans P.A., Musters R.J., Visser C.A., and Kamp O. Transient permeabilization of cell membranes by ultrasound-exposed microbubbles is related to formation of hydrogen peroxide. Am J Physiol Heart Circ Physiol 291 (2006) H1595-H1601
27. Kinoshita M., McDannold N., Jolesz F.A., and Hynynen K. Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound. Biochem Biophys Res Commun 340 (2006) 1085-1090
28. Kinoshita M., McDannold N., Jolesz F.A., and Hynynen K. Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption. PNAS 103 (2006) 11719-11723
29. Kroll R.A., and Neuwelt E.A. Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means. Neurosurgery 42 (1998) 1083-1099
30. Liebner S., Fischmann A., Rascher G., Duffner F., Grote E.-H., Kalbacher H., and Wolburg H. Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathol 100 (2000) 323-331
31. Nag S., Robertson D.M., and Dinsdale H.B. Intracerebral arteriolar permeability to lanthanum. Am J Pathol 107 (1982) 336-341
32. Ohtsuki S., Sato S., Yamaguchi H., Kamoi M., Asashima T., and Terasaki T. Exogenous expression of claudin-5 induces barrier properties in cultured rat brain capillary endothelial cells. J Cell Physiol 210 (2006) 81-86
33. Plumb J., McQuaid S., Mirakhur M., and Kirk J. Abnormal endothelial tight junctions in active lesions and normal-appearing white matter in multiple sclerosis. Brain Pathol 12 (2002) 154-169
34. Rapoport S.I. Osmotic opening of the blood-brain barrier: Principles, mechanism, and therapeutic applications. Cell Mol Neurobiol 20 (2000) 217-230
35. Sanovich E., Bartus R.T., Friden P.M., Dean R.L., Le H.Q., and Brightman M.W. Pathway across blood-brain barrier opened by the bradykinin agonist, RMP-4. Brain Res 705 (1995) 125-135
36. Sheikov N., McDannold N., Vykhodtseva N., Jolesz F., and Hynynen K. Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol 30 (2004) 979-989
37. Sheikov N., McDannold N., Jolesz F., Zhang Y.-Z., Tam K., and Hynynen K. Brain arterioles show more active vesicular transport of blood-borne tracer molecules than capillaries and venules after focused ultrasound-evoked opening of the blood-brain barrier. Ultrasound Med Biol 32 (2006) 1399-1409
38. Staddon J.M., Herrenknecht K., Smales C., and Rubin L.L. Evidence that tyrosine phosphorylation may increase tight junction permeability. J Cell Sci 108 (1995) 609-619
39. Stevenson B.R., Anderson J.M., Braun I.D., and Mooseker M.S. Phosphorylation of the tigh-junctions protein ZO-1 in two strains of Madin-Darby canine kidney cells which differ in transepithelial resistance. Biochem J 263 (1989) 597-599
40. Treat L.H., McDannold N., Zhang Y., Vykhodtseva N., and Hynynen K. Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound. Int J Cancer 121 (2007) 901-907
41. Tsukita S., and Furuse M. Occludin and claudins in tight-junction strands: leading or supporting players?. Trends Cell Biol 9 (1999) 268-273
42. Tsukita S., Furuse M., and Itoh M. Multi-functional strands in tight junctions. Nat Rev Mol Cell Biol 2 (2001) 285-293
43. Van Wamel A., Kooiman K., Harteveld M., Emmer M., ten Cate F.J., Versluis M., and de Jong N. Vibrating microbubbles poking individual cells: Drug transfer into cells via sonoporation. J Control Release 112 (2006) 149-155
44. Vykhodtseva N.I., Sorrentino V., Jolesz F.A., Bronson R.T., and Hynynen K. MRI detection of the thermal effects of focused ultrasound on the brain. Ultrasound Med Biol 26 (2000) 871-880
45. Willis C.L., Leach L., Clarke G.J., Nolan C.C., and Ray D.E. Reversible disruption of tight junction complexes in the rat blood-brain barrier, following transitory focal astrocyte loss. Glia 48 (2004) 1-13
46. Wolburg H., Neuhaus J., Kniesel U., Krauss B., Schmid E.M., Ocalan M., Farrell C., and Risau W. Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes. J Cell Sci 107 (1994) 1347-1357
47. Wolburg H., Wolburg-Buchholz K., Kraus J., Rascher-Eggstein G., Liebner S., Hamm S., Duffner F., Grote E.-H., Risau W., and Engelhardt B. Localization of claudin-3 in tight junctions of the blood-brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme. Acta Neuropathol 105 (2003) 586-592
48. Yang F.Y., Fu W.M., Yang R.S., Liou H.C., Kang K.H., and Lin W.L. Quantitative evaluation of focused ultrasound with a contrast agent on blood-brain barrier disruption. Ultrasound Med Biol 33 (2007) 1421-1427