Quantitative fluorescence microscopy provides high resolution imaging of passive diffusion and P-gp mediated efflux at the in vivo blood-brain barrier

Journal of Neuroscience Methods

Volumn 219, Issue 1, 2013, Pages 188-195

  Mittapalli, Rajendar K ^a   Manda, Vamshi K ^a   Bohn, Kaci A ^a   Adkins, Chris E ^a   Lockman, Paul R ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Alzheimer's; Autoradiography; Blood brain barrier; Drug delivery; Parkinson's; Quantitative fluorescent microscopy; Stroke; Transport

Indexed keywords

MULTIDRUG RESISTANCE PROTEIN; RHODAMINE 123; VERAPAMIL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEACHING; BLOOD BRAIN BARRIER; BRAIN PERFUSION; CONTROLLED STUDY; DIFFUSION; DIFFUSION COEFFICIENT; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MEMBRANE TRANSPORT; NONHUMAN; OPTICAL RESOLUTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; TRANSPORT KINETICS;

ALZHEIMER'S; AUTORADIOGRAPHY; BLOOD-BRAIN BARRIER; DRUG DELIVERY; PARKINSON'S; QUANTITATIVE FLUORESCENT MICROSCOPY; STROKE; TRANSPORT;

ALGORITHMS; ANIMALS; AUTORADIOGRAPHY; BLOOD-BRAIN BARRIER; CALCIUM CHANNEL BLOCKERS; CELLS, CULTURED; DATA INTERPRETATION, STATISTICAL; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; KINETICS; LINEAR MODELS; MALE; MICROSCOPY, FLUORESCENCE; P-GLYCOPROTEIN; PERFUSION; PROPIONATES; QUINOLINES; RATS; RATS, INBRED F344; REFERENCE STANDARDS; RHODAMINE 123; VERAPAMIL; XANTHENES;

EID: 84882981661     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2013.07.001     Document Type: Article

References (64)

1. Allen D.D., Smith Q.R. Characterization of the blood-brain barrier choline transporter using the in situ rat brain perfusion technique. Journal of Neurochemistry 2001, 76:1032-1041.
2. Bachmeier C.J., Miller D.W. A fluorometric screening assay for drug efflux transporter activity in the blood-brain barrier. Pharmaceutical Research 2005, 22:113-121.
3. Bakay L., Ballantine H.T., Hueter T.F., Sosa D. Ultrasonically produced changes in the blood-brain barrier. AMA Archives of Neurology and Psychiatry 1956, 76:457-467.
4. Bauer B., Hartz A.M., Lucking J.R., Yang X., Pollack G.M., Miller D.S. Coordinated nuclear receptor regulation of the efflux transporter, Mrp2, and the phase-II metabolizing enzyme, GSTpi, at the blood-brain barrier. Journal of Cerebral Blood Flow and Metabolism 2008.
5. Baumbach G.L., Heistad D.D. Heterogeneity of brain blood flow and permeability during acute hypertension. American Journal of Physiology 1985, 249:H629-H637.
6. Belayev L., Busto R., Zhao W., Ginsberg M.D. Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Research 1996, 739:88-96.
7. Blasberg R.G., Fenstermacher J.D., Patlak C.S. Transport of alpha-aminoisobutyric acid across brain capillary and cellular membranes. Journal of Cerebral Blood Flow and Metabolism 1983, 3:8-32.
8. Brightman M.W., Reese T.S., Vick N.A., Bigner D.D. A mechanism underlying the lack of a blood-brain barrier to peroxidase in virally induced brain tumors. Journal of Neuropathology and Experimental Neurology 1971, 30:139-140.
9. Brismar H., Ulfhake B. Fluorescence lifetime measurements in confocal microscopy of neurons labeled with multiple fluorophores. Nature Biotechnology 1997, 15:373-377.
10. Brown R.C., Egleton R.D., Davis T.P. Mannitol opening of the blood-brain barrier: regional variation in the permeability of sucrose, but not 86Rb+ or albumin. Brain Research 2004, 1014:221-227.
11. Chikhale E.G., Burton P.S., Borchardt R.T. The effect of verapamil on the transport of peptides across the blood-brain barrier in rats: kinetic evidence for an apically polarized efflux mechanism. Journal of Pharmacology and Experimental Therapeutics 1995, 273:298-303.
12. da Costa J.C. Influence of electroconvulsions on the permeability of the blood-brain barrier to trypan blue. Arquivos de Neuro-Psiquiatria 1972, 30:1-7.
13. Dallas S., Miller D.S., Bendayan R. Multidrug resistance-associated proteins: expression and function in the central nervous system. Pharmacological Reviews 2006, 58:140-161.
14. Dereymaeker A., Claeys L., Sorel L. Experimental study of the blood-brain barrier in the frozen cerebral cortex. European Neurology 1970, 3:293-302.
15. Dorn J.F., Danuser G., Yang G. Computational processing and analysis of dynamic fluorescence image data. Methods in Cell Biology 2008, 85:497-538.
16. Ehrlich P.R. Das Sauerstoff-Bedü rfnis des Organismus. Einefarbenanalytische Studie 1885, Verlag von August Hirschwald, Berlin.
17. Evers R., Kool M., van Deemter L., Janssen H., Calafat J., Oomen L.C., et al. Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. Journal of Clinical Investigation 1998, 101:1310-1319.
18. Fairchild C.R., Moscow J.A., O'Brien E.E., Cowan K.H. Multidrug resistance in cells transfected with human genes encoding a variant P-glycoprotein and glutathione S-transferase-pi. Molecular Pharmacology 1990, 37:801-809.
19. Ferguson M.W., Beaumont S.E., Jones S.E., Navaratnam S., Parsons B.J. Excited state and free radical properties of Rhodamine 123: a laser flash photolysis and radiolysis study. Physical Chemistry Chemical Physics 1999, 1:261-268.
20. Fontaine M., Elmquist W.F., Miller D.W. Use of rhodamine 123 to examine the functional activity of P-glycoprotein in primary cultured brain microvessel endothelial cell monolayers. Life Sciences 1996, 59:1521-1531.
21. Gerk P.M., Vore M. Regulation of expression of the multidrug resistance-associated protein 2 (MRP2) and its role in drug disposition. Journal of Pharmacology and Experimental Therapeutics 2002, 302:407-415.
22. Gleva G.F., Goodglick L.A., Kane A.B. Altered calcium homeostasis in irreversibly injured P388D1 macrophages. American Journal of Pathology 1990, 137:43-57.
23. Goldmann E. Vitalfarbung am zentralnervensystem 1913, 1-60. Abhandl Konigl preuss, Akad Wiss.
24. Hawkins B.T., Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacological Reviews 2005, 57:173-185.
25. Hawkins B.T., Egleton R.D. Fluorescence imaging of blood-brain barrier disruption. Journal of Neuroscience Methods 2006, 151:262-267.
26. Hoffmann K., Gastens A.M., Volk H.A., Loscher W. Expression of the multidrug transporter MRP2 in the blood-brain barrier after pilocarpine-induced seizures in rats. Epilepsy Research 2006, 69:1-14.
27. Janneh O., Owen A., Chandler B., Hartkoorn R.C., Hart C.A., Bray P.G., et al. Modulation of the intracellular accumulation of saquinavir in peripheral blood mononuclear cells by inhibitors of MRP1, MRP2, P-gp and BCRP. AIDS 2005, 19:2097-2102.
28. Janneh O., Jones E., Chandler B., Owen A., Khoo S.H. Inhibition of P-glycoprotein and multidrug resistance-associated proteins modulates the intracellular concentration of lopinavir in cultured CD4T cells and primary human lymphocytes. Journal of Antimicrobial Chemotherapy 2007, 60:987-993.
29. Johansson B., Li C.L., Olsson Y., Klatzo I. The effect of acute arterial hypertension on the blood-brain barrier to protein tracers. Acta Neuropathologica 1970, 16:117-124.
30. Leader J.P., O'Donnell M.J. Transepithelial transport of fluorescent p-glycoprotein and MRP2 substrates by insect Malpighian tubules: confocal microscopic analysis of secreted fluid droplets. Journal of Experimental Biology 2005, 208:4363-4376.
31. Lin S.R., Kormano M. Cerebral circulation after cardiac arrest. Microangiographic and protein tracer studies. Stroke 1977, 8:182-188.
32. Lockman P.R., Roder K.E., Allen D.D. Inhibition of the rat blood-brain barrier choline transporter by manganese chloride. Journal of Neurochemistry 2001, 79:588-594.
33. Lockman P.R., Koziara J., Roder K.E., Paulson J., Abbruscato T.J., Mumper R.J., et al. In vivo and in vitro assessment of baseline blood-brain barrier parameters in the presence of novel nanoparticles. Pharmaceutical Research 2003, 20:705-713.
34. Lockman P.R., Mumper R.J., Allen D.D. Evaluation of blood-brain barrier thiamine efflux using the in situ rat brain perfusion method. Journal of Neurochemistry 2003, 86:627-634.
35. Lockman P.R., Koziara J.M., Mumper R.J., Allen D.D. Nanoparticle surface charges alter blood-brain barrier integrity and permeability. Journal of Drug Targeting 2004, 12:635-641.
36. Lockman P.R., McAfee G., Geldenhuys W.J., Van der Schyf C.J., Abbruscato T.J., Allen D.D. Brain uptake kinetics of nicotine and cotinine after chronic nicotine exposure. Journal of Pharmacology and Experimental Therapeutics 2005, 314:636-642.
37. Lockman P.R., Van der Schyf C.J., Abbruscato T.J., Allen D.D. Chronic nicotine exposure alters blood-brain barrier permeability and diminishes brain uptake of methyllycaconitine. Journal of Neurochemistry 2005, 94:37-44.
38. Lockman P.R., Mittapalli R.K., Taskar K.S., Rudraraju V., Gril B., Bohn K.A., et al. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clinical Cancer Research 2010, 16:5664-5678.
39. Luna-Tortos C., Fedrowitz M., Loscher W. Evaluation of transport of common antiepileptic drugs by human multidrug resistance-associated proteins (MRP1, 2 and 5) that are overexpressed in pharmacoresistant epilepsy. Neuropharmacology 2010, 58:1019-1032.
40. Miller D.S., Nobmann S.N., Gutmann H., Toeroek M., Drewe J., Fricker G. Xenobiotic transport across isolated brain microvessels studied by confocal microscopy. Molecular Pharmacology 2000, 58:1357-1367.
41. Miyagawa T., Oku T., Sasajima T., Dasai R., Beattie B., Finn R., et al. Assessment of treatment response by autoradiography with (14)C-aminocyclopentane carboxylic acid, (67)Ga-DTPA, and (18)F-FDG in a herpes simplex virus thymidine kinase/ganciclovir brain tumor model. Journal of Nuclear Medicine 2003, 44:1845-1854.
42. Narang V.S., Fraga C., Kumar N., Shen J., Throm S., Stewart C.F., et al. Dexamethasone increases expression and activity of multi-drug resistance transporters at the rat blood-brain barrier. American Journal of Physiology, Cell Physiology 2008.
43. Nemeroff C.B., Crisley F.D. Monosodium l-glutamate-induced convulsions: temporary alteration in blood-brain barrier permeability to plasma proteins. Environmental Physiology and Biochemistry 1975, 5:389-395.
44. Neuhaus W., Stessl M., Strizsik E., Bennani-Baiti B., Wirth M., Toegel S., et al. Blood-brain barrier cell line PBMEC/C1-2 possesses functionally active P-glycoprotein. Neuroscience Letters 2010, 469:224-228.
45. Nitsch C., Klatzo I. Regional patterns of blood-brain barrier breakdown during epileptiform seizures induced by various convulsive agents. Journal of the Neurological Sciences 1983, 59:305-322.
46. O'Donnell M.J., Leader J.P. Changes in fluid secretion rate alter net transepithelial transport of MRP2 and P-glycoprotein substrates in Malpighian tubules of Drosophila melanogaster. Archives of Insect Biochemistry and Physiology 2006, 63:123-134.
47. Rao P.S., Mallya K.B., Srivenugopal K.S., Balaji K.C., Rao U.S. RNF2 interacts with the linker region of the human P-glycoprotein. International Journal of Oncology 2006, 29:1413-1419.
48. Reese T.S., Karnovsky M.J. Fine structural localization of a blood-brain barrier to exogenous peroxidase. Journal of Cell Biology 1967, 34:207-217.
49. Reichel V., Miller D.S., Fricker G. Texas Red transport across rat and dogfish shark (Squalus acanthias) choroid plexus. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2008, 295:R1311-R1319.
50. Schettler T., Shealy C.N. Experimental selective alteration of blood-brain barrier by x-irradiation. Journal of Neurosurgery 1970, 32:89-94.
51. Schmidt K.C., Smith C.B. Resolution, sensitivity and precision with autoradiography and small animal positron emission tomography: implications for functional brain imaging in animal research. Nuclear Medicine and Biology 2005, 32:719-725.
52. Sharom F.J., Liu R., Qu Q., Romsicki Y. Exploring the structure and function of the P-glycoprotein multidrug transporter using fluorescence spectroscopic tools. Seminars in Cell & Developmental Biology 2001, 12:257-265.
53. Shealy C.N., Crafts D. Selective alteration of the blood-brain barrier. Journal of Neurosurgery 1965, 23:484-487.
54. Shen F., Chu S., Bence A.K., Bailey B., Xue X., Erickson P.A., et al. Quantitation of doxorubicin uptake, efflux, and modulation of multidrug resistance (MDR) in MDR human cancer cells. Journal of Pharmacology and Experimental Therapeutics 2008, 324:95-102.
55. Smith Q.R. Brain perfusion systems for studies of drug uptake and metabolism in the central nervous system. Pharmaceutical Biotechnology 1996, 8:285-307.
56. Smith Q.R., Takasato Y. Kinetics of amino acid transport at the blood-brain barrier studied using an in situ brain perfusion technique. Annals of the New York Academy of Sciences 1986, 481:186-201.
57. Stopa B., Rybarska J., Drozd A., Konieczny L., Krol M., Lisowski M., et al. Albumin binds self-assembling dyes as specific polymolecular ligands. International Journal of Biological Macromolecules 2006, 40:1-8.
58. Takasato Y., Rapoport S.I., Smith Q.R. An in situ brain perfusion technique to study cerebrovascular transport in the rat. American Journal of Physiology 1984, 247:H484-H493.
59. Tengvar C., Hultstrom D., Olsson Y. An improved Percoll density gradient for measurements of experimental brain edema. Addition of sucrose to an isotonic gradient in an attempt to balance osmotic conditions during density determinations. Acta Neuropathologica 1983, 61:201-206.
60. Uehara H., Miyagawa T., Tjuvajev J., Joshi R., Beattie B., Oku T., et al. Imaging experimental brain tumors with 1-aminocyclopentane carboxylic acid and alpha-aminoisobutyric acid: comparison to fluorodeoxyglucose and diethylenetriaminepentaacetic acid in morphologically defined tumor regions. Journal of Cerebral Blood Flow and Metabolism 1997, 17:1239-1253.
61. Wang Q., Yang H., Miller D.W., Elmquist W.F. Effect of the p-glycoprotein inhibitor, cyclosporin A, on the distribution of rhodamine-123 to the brain: an in vivo microdialysis study in freely moving rats. Biochemical and Biophysical Research Communications 1995, 211:719-726.
62. Yousif S., Marie-Claire C., Roux F., Scherrmann J.M., Decleves X. Expression of drug transporters at the blood-brain barrier using an optimized isolated rat brain microvessel strategy. Brain Research 2007, 1134:1-11.
63. Zastre J.A., Chan G.N., Ronaldson P.T., Ramaswamy M., Couraud P.O., Romero I.A., et al. Up-regulation of P-glycoprotein by HIV protease inhibitors in a human brain microvessel endothelial cell line. Journal of Neuroscience Research 2009, 87:1023-1036.
64. Zhang Y., Han H., Elmquist W.F., Miller D.W. Expression of various multidrug resistance-associated protein (MRP) homologues in brain microvessel endothelial cells. Brain Research 2000, 876:148-153.