Modulation of intracellular ca2+ concentration in brain microvascular endothelial cells in vitro by acoustic cavitation

Ultrasound in Medicine and Biology

Volumn 36, Issue 7, 2010, Pages 1176-1187

  Park, Juyoung ^a   Fan, Zhenzhen ^a   Kumon, Ronald E ^a   El Sayed, Mohamed E H ^a   Deng, Cheri X ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Blood brain barrier; Brain endothelial cells; Calcium imaging; Fast frame photography; Microbubble contrast agents; Propidium iodide; Sonoporation; Ultrasound

Indexed keywords

BLOOD-BRAIN BARRIER; CALCIUM IMAGING; FAST-FRAME PHOTOGRAPHY; MICROBUBBLE CONTRAST AGENTS; PROPIDIUM IODIDE; SONOPORATION;

BLOOD; BLOOD VESSEL PROSTHESES; CALCIUM; CELL MEMBRANES; CYTOLOGY; ENZYME ACTIVITY; PHOTOGRAPHY; SELF ASSEMBLY; ULTRASONICS;

ENDOTHELIAL CELLS;

CALCIUM ION; FURA 2; PROPIDIUM IODIDE; CALCIUM;

ACOUSTIC STRESS; ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRIGHT FIELD MICROSCOPY; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DAMAGE; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR CALCIUM; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; MICROBUBBLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; ULTRASOUND; ANIMAL; BRAIN CIRCULATION; CELL LINE; DRUG EFFECT; METABOLISM; MICROCIRCULATION; PHYSIOLOGY; RADIATION DOSE; RADIATION EXPOSURE; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CELL LINE; CEREBROVASCULAR CIRCULATION; ENDOTHELIAL CELLS; MICE; MICROCIRCULATION; RADIATION DOSAGE; SIGNAL TRANSDUCTION; SONICATION;

EID: 77953881020     PISSN: 03015629     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2010.04.006     Document Type: Article

References (67)

1. Abbott N.J. Role of intracellular calcium in regulation of brain endothelial permeability. Introduction to the blood-brain barrier: Methodology, biology and pathology. New York 1998, 345-351. Cambridge University Press. W.M. Pardridge (Ed.).
2. Abbott N.J. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell Mol Neurobiol 2000, 20:131-147.
3. Abbott N.J., Rönnbäck L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006, 7:41-53.
4. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003, 4:517-529.
5. Boitano S., Dirksen E., Sanderson M. Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science 1992, 258:292-295.
6. Bradbury M.W. The blood-brain barrier. Exp Physiol 1993, 78:453-472.
7. Brown R.C., Davis T.P. Calcium modulation of adherens and tight junction function: A potential mechanism for blood-brain barrier disruption after stroke. Stroke 2002, 33:1706-1711.
8. Choi J.J., Pernot M., Small S.A., Konofagou E.E. Noninvasive, transcranial and localized opening of the blood-brain barrier using focused ultrasound in mice. Ultrasound Med Biol 2007, 33:95-104.
9. Cotrina M.L., Lin J.H.C., Nedergaard M. Cytoskeletal assembly and ATP release regulate astrocytic calcium signaling. J Neurosci 1998, 18:8794-8804.
10. Deng C., Sieling F., Pan H., Cui J. Ultrasound-induced cell membrane porosity. Ultrasound Med Biol 2004, 30:519-526.
11. Desai S.Y., Marroni M., Cucullo L., Krizanac-Bengez L., Mayberg M.R., Hossain M.T., Grant G.G., Janigro D. Mechanisms of endothelial survival under shear stress. Endothelium 2002, 9:89-102.
12. Doolittle N.D., Petrillo A., Bell S., Cummings P., Eriksen S. Blood-brain barrier disruption for the treatment of malignant brain tumors: The National Program. J Neurosci Nurs 1998, 30:81-90.
13. Fan Z., Kumon R.E., Park J., Deng C.X. Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles. J Control Release 2010, 142:31-39.
14. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985, 260:3440-3450.
15. Gumbiner B.M. Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 1996, 84:345-357.
16. Gumerlock M.K., Belshe B.D., Madsen R., Watts C. Osmotic blood-brain barrier disruption and chemotherapy in the treatment of high grade malignant glioma: Patient series and literature review. J Neurooncol 1992, 12:33-46.
17. Hariri R. Cerebral oedema. Neurosurg Clin North Am 1994, 5:687-706.
18. Honda H., Kondo T., Zhao Q.-L., Feril L.B., Kitagawa H. Role of intracellular calcium ions and reactive oxygen species in apoptosis induced by ultrasound. Ultrasound Med Biol 2004, 30:683-692.
19. Hynynen K., McDannold N., Sheikov N.A., Jolesz F.A., Vykhodtseva N. Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage 2005, 24:12-20.
20. Hynynen K., McDannold N., Vykhodtseva N., Jolesz F.A. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 2001, 220:640-646.
21. Juffermans L.J., Dijkmans P.A., Musters R.J., Visser C.A., Kamp O. Transient permeabilization of cell membranes by ultrasound-exposed microbubbles is related to formation of hydrogen peroxide. Am J Physiol Heart Circ Physiol 2006, 291. H1595-HH601.
22. Kinoshita M., McDannold N., Jolesz F.A., Hynynen K. 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 2006, 103:11719-11723.
23. Kinoshita M., McDannold N., Jolesz F.A., Hynynen K. Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound. Biochem Biophys Res Commun 2006, 340:1085-1090.
24. Krizanac-Bengez L., Mayberg M.R., Janigro D. The cerebral vasculature as a therapeutic target for neurological disorders and the role of shear stress in vascular homeostatis and pathophysiology. Neurol Res 2004, 26:846-853.
25. Kroll R.A., Neuwelt E.A. Outwitting the blood-brain barrier for therapeutic purposes: Osmotic opening and other means. Neurosurgery 1998, 42:1083-1099. discussion 99-100.
26. Kumon R.E., Aehle M., Sabens D., Parikh P., Han Y.W., Kourennyi D., Deng C.X. Spatiotemporal effects of sonoporation measured by real-time calcium imaging. Ultrasound Med Biol 2009, 35:494-506.
27. Kumon R.E., Aehle M., Sabens D., Parikh P., Kourennyi D., Deng C.X. Ultrasound-induced calcium oscillations and waves in Chinese hamster ovary cells in the presence of microbubbles. Biophys J 2007, 93:L29-L31.
28. McDannold N., Vykhodtseva N., Hynynen K. Blood-brain barrier disruption induced by focused ultrasound and circulating preformed microbubbles appears to be characterized by the mechanical index. Ultrasound Med Biol 2008, 34:834-840.
29. Montesano R., Pepper M.S., Mohle-Steinlein U., Risau W., Wagner E.F., Orci L. Increased proteolytic activity is responsible for the aberrant morphogenetic behavior of endothelial cells expressing the middle T oncogene. Cell 1990, 62:435-445.
30. 2+ mobilization to mechanical stretch in endothelial cells. Am J Physiol Cell Physiol 1993, 264:C1037-C1044.
31. Neuwelt E.A., Frenkel E.P., Diehl J., Vu L.H., Rapoport S., Hill S. Reversible osmotic blood-brain barrier disruption in humans: Implications for the chemotherapy of malignant brain tumors. Neurosurgery 1980, 7:44-52.
32. Ng K.Y., Liu Y. Therapeutic ultrasound: Its application in drug delivery. Med Res Rev 2002, 22:204-223.
33. Nigam S.K., Rodriguez-Boulan E., Silver R.B. Changes in intracellular calcium during the development of epithelial polarity and junctions. Proc Natl Acad Sci U S A 1992, 89:6162-6166.
34. Olesen S. An electrophysiological study of microvascular permeability and its modulation by chemical mediators. Acta Physiol Scand 1989, 136(Suppl. 579):1-28.
35. Osipchuk Y., Cahalan M. Cell-to-cell spread of calcium signals mediated by ATP receptors in mast cells. Nature 1992, 359:241-244.
36. Paemeleire K., de Hemptinne A., Leybaert L. Chemically, mechanically, and hyperosmolarity-induced calcium responses of rat cortical capillary endothelial cells in culture. Exp Brain Res 1999, 126:473-481.
37. Pardridge W.M. Drug and gene delivery to the brain: The vascular route. Neuron 2002, 36:555-558.
38. Pardridge W.M. The blood-brain barrier: Bottleneck in brain drug development. NeuroRx 2005, 2:3-14.
39. Pardridge W.M. Introduction to the blood-brain barrier: Methodology, biology and pathology 2006, Cambridge University Press, Cambridge.
40. Petty H.R. Spatiotemporal chemical dynamics in living cells: From information trafficking to cell physiology. Biosystems 2006, 83:217-224.
41. Popp R., Hoyer J., Meyer J., Galla H.J., Gögelein H. Stretch-activated nonselective cation channels in the antiluminal membrane of porcine cerebral capillaries. J Physiol 1992, 454:435-449.
42. Prentice P., Cuschieri A., Dholakia K., Prausnitz M., Campbell P. Membrane disruption by optically controlled microbubble cavitation. Nat Phys 2005, 1:107-110.
43. Puka-Sundvall M., Hagberg H., Andin P. Changes in extracellular calcium concentration in the immature rat cerebral cortex during anoxia are not influenced by MK-801. Develop Brain Res 1994, 77:146-150.
44. Rapoport S.I., Bachman D.S., Thompson H.K. Chronic effects of osmotic opening of the blood-brain barrier in the monkey. Science 1972, 176:1243-1245.
45. Revest P., Abbott N., Gillespie J. Receptor-mediated changes in intracellular [Ca2+] in cultured rat brain capillary endothelial cells. Brain Res 1991, 549:159-161.
46. Roman-Goldstein S., Clunie D.A., Stevens J., Hogan R., Monard J., Ramsey F., Neuwelt E.A. Osmotic blood-brain barrier disruption: CT and radionuclide imaging. AJNR Am J Neuroradiol 1994, 15:581-590.
47. Ross J.P., Cai X., Chiu J.F., Yang J., Wu J.R. Optical and atomic force microscopic studies on sonoporation. J Acoust Soc Am 2002, 111:1161-1164.
48. Sanderson M. Intercellular waves of communication. Nes Physiol Sci 1996, 11:262-269.
49. Sanderson M., Charles A., Boitano S., Dirksen E. Mechanisms and function of intercellular calcium signaling. Mol Cell Endocrinol 1994, 98:173-187.
50. Schlicher R.K., Radhakrishna H., Tolentino T.P., Apkarian R.P., Zarnitsyn V., Prausnitz M.R. Mechanism of intracellular delivery by acoustic cavitation. Ultrasound Med Biol 2006, 32:915-924.
51. Shasby D.M., Shasby S.S. Effects of calcium on transendothelial albumin transfer and electrical resistance. J Appl Physiol 1986, 60:71-79.
52. Sheikov N., McDannold N., Jolesz F., Zhang Y.Z., Tam K., 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 2006, 32:1399-1409.
53. Sheikov N., McDannold N., Sharma S., Hynynen K. Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium. Ultrasound Med Biol 2008, 34:1093-1104.
54. Sheikov N., McDannold N., Vykhodtseva N., Jolesz F., Hynynen K. Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med Biol 2004, 30:979-989.
55. Sipido K.R., Marban E. L-type calcium channels, potassium channels, and novel nonspecific cation channels in a clonal muscle cell line derived from embryonic rat ventricle. Circ Res 1991, 69:1487-1499.
56. Stewart P.A., Tuor U.I. Blood-eye barriers in the rat: Correlation of ultrastructure with function. J Comp Neurol 1994, 340:566-576.
57. Stokes B.T., Fox P., Hollinden G. Extracellular calcium activity in the injured spinal cord. Exp Neurol 1983, 80:561-572.
58. Stuart R.O., Sun A., Bush K.T., Nigam S.K. Dependence of epithelial intercellular junction biogenesis on thapsigargin-sensitive intracellular calcium stores. J Biol Chem 1996, 271:13636-13641.
59. Stuart R.O., Sun A., Panichas M., Hebert S.C., Brenner B.M., Nigam S.K. Critical role for intracellular calcium in tight junction biogenesis. J Cell Physiol 1994, 159:423-433.
60. Tachibana K., Tachibana S. The use of ultrasound for drug delivery. Echocardiography 2001, 18:323-328.
61. Tran T.A., Le Guennec J.Y., Bougnoux P., Tranquart F., Bouakaz A. Characterization of cell membrane response to ultrasound activated microbubbles. IEEE Trans Ultrason Ferroelectr Freq Control 2008, 55:43-44.
62. Tran T.A., Roger S., Le Guennec J.Y., Tranquart F., Bouakaz A. Effect of ultrasound-activated microbubbles on the cell electrophysiological properties. Ultrasound Med Biol 2007, 33. 158-16.
63. Tsukamoto A., Yasui N., Watanabe Y., Furukawa K., Ushida T. Real-time imaging of interaction between microbubble and cell under therapeutic ultrasound radiation. Sixth IASTED International Conference 2008, 334-337. Acta Press, Innsbruck, Austria. A. Hierlemann (Ed.).
64. Yanga F., Gua N., Chenb D., Xic X., Zhangc D., Lia Y., Wu J. Experimental study on cell self-sealing during sonoporation. J Control Release 2008, 131:205-210.
65. Zhao Y.-Z., Luo Y.-K., Lu C.-T., Xu J.-F., Tang J., Zhang M., Zhang Y., Liang H-D. Phospholipids-based microbubbles sonoporation pore size and reseal of cell membrane cultured in vitro. J Drug Target 2008, 16:18-25.
66. Zhou Y., Kumon R.E., Cui J., Deng C.X. The size of sonoporation pores on the cell membrane. Ultrasound Med Biol 2009, 35:1756-1760.
67. Zunkeler B., Carson R.E., Olson J., Blasberg R.G., DeVroom H., Lutz R.J., Saris S.C., Wright D.C., Kammerer W., Patronas N.J., Dedrick R.L., Herscovitch P., Oldfield E.H. Quantification and pharmacokinetics of blood-brain barrier disruption in humans. J Neurosurg 1996, 85:1056-1065.