Brief heat shock affects the permeability and thermotolerance of an in vitro blood-brain barrier model of porcine brain microvascular endothelial cells

Microvascular Research

Volumn 71, Issue 2, 2006, Pages 108-114

  Jeliazkova Mecheva, Valentina V ^a   Hymer, Wes C ^b   Nicholas, Nicholas C ^b   Bobilya, Dennis J ^a  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Blood brain barrier; Brain microvascular endothelial cell; Heat shock; Hyperthermia; Thermotolerance; Transendothelial electrical resistance

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN CORTEX; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; HEAT SHOCK; HEAT TOLERANCE; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; SWINE; TEMPERATURE;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL CULTURE TECHNIQUES; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CEREBRAL CORTEX; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HEAT; SWINE; SWINE, MINIATURE;

ANIMALIA; SUIDAE; SUS SCROFA;

EID: 33646049704     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2005.11.009     Document Type: Article

References (40)

1. Bobilya D.J., D'Amour K., Palmer A., Skeffington C., Therrien N., and Tibaduiza E.C. Isolation and cultivation of porcine brain capillary endothelial cells as an in vitro model of the blood-brain barrier. Methods Cell Sci. 17 (1995) 25-32
2. Bowman P., Schuschereba S., Lawlor D., Gilligan G., Mata J., and DeBaere D. Survival of human epidermal keratinocytes after short-duration high temperature: synthesis of HSP70 and IL-8. Am. J. Physiol. 272 (1997) C1988-C1994
3. Chen Y., Xu R., Huang Q., Xu Z., Jiang X., and Cai Y. Effect of hyperthermia on tight junctions between endothelial cells of the blood-brain barrier model in vitro. Di-Yi Junyi Daxue Xuebao 23 (2003) 21-24
4. Cho C.W., Liu Y., Cobb W.N., Henthorn T.K., Lillehei K., Christians U., and Ng K.Y. Ultrasound-induced mild hyperthermia as a novel approach to increase drug uptake in brain microvessel endothelial cells. Pharm. Res. 19 (2002) 1123-1129
5. Cucullo L., Aumayr B., Rapp E., and Janigro D. Drug delivery and in vitro models of the blood-brain barrier. Curr. Opin. Drug Discovery Dev. 8 (2005) 89-99
6. Diederich C.J., Khail I.S., Stauffer P.R., Sneed P.K., and Phillips T.L. Direct-coupled interstitial ultrasound applicators for simultaneous thermobrachytherapy: a feasibility study. Int. J. Hyperthermia 12 (1996) 401-409
7. Ertl-Wagner B., Jansen O., Schwab S., and Sartor K. Bilateral basal ganglion haemorrhage in diabetic ketoacidotic coma: case report. Neuroradiology 41 (1999) 670-673
8. Garberg P. In vitro models of the blood-brain barrier. ATLA 26 (1998) 821-847
9. Gill J.L. Design and Analysis of Experiments in the Animal and Medical Sciences (1978), Iowa State University Press, Ames, IA
10. Gobbel G.T., Chan T.Y., and Chan P.H. Amelioration of hypoxic and hypoglycemic damage to cerebral endothelial cells. Mol. Chem. Neuropathol. 24 (1995) 107-120
11. Ikeda N., Hayashida O., Kameda H., Ito H., and Matsuda T. Experimental study on thermal damage to dog normal brain. Int. J. Hyperthermia 10 (1994) 553-561
12. Ilbay G., Sahin D., and Ates N. Changes in blood-brain barrier permeability during hot water-induced seizures in rats. Neurol. Sci. 24 (2003) 232-235
13. Kahn E. An examination of the blood-brain barrier in health and disease. Br. J. Nurs. 14 (2005) 509-513
14. Krueger-Naug A., Hopkins D., Armstrong J., Plumier J., and Currie R. Hyperthermic induction of the 27-kDa heat shock protein (Hsp27) in neuroglia and neurons of the rat central nervous system. J. Comp. Neurol. 428 (2000) 495-510
15. Lin J., and Lin M. Microwave hyperthermia-induced blood-brain barrier alterations. Radiat. Res. 89 (1982) 77-87
16. Lin J.C., Yuan P.M.K., and Jung D.T. Enhancement of anticancer drug delivery to the brain by microwave induced hyperthermia. Bioelectrochem. Bioenerg. 47 (1998) 259-264
17. Lindquist S. The heat-shock response. Annu. Rev. Biochem. 55 (1986) 1151-1191
18. Maciag T., Cerundolo J., Ilsley S., Kelley P.R., and Forand R. An endothelial cell growth factor from bovine hypothalamus: identification and partial characterization. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 5674-5678
19. Marcuccilli C., Mathur S., Morimoto R., and Miller R. Regulatory differences in the stress response of hippocampal neurons and glial cells after heat shock. J. Neurosci. 16 (1996) 478-485
20. Mark K.S., and Davis T.P. Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am. J. Physiol.: Heart Circ. Physiol. 282 (2002) H1485-H1494
21. Mizzen l., and Welch W. Characterization of the thermotolerant cell. Effect on protein synthesis activity and the regulation of heat-shock protein expression. J. Cell Biol. 106 (1988) 1105-1116
22. Morita K., Anaka R., Kakinuma K., Takahashi H., and Motoyama H. Combination therapy of rat brain tumours using localized interstitial hyperthermia and intra-arterial chemotherapy. Int. J. Hyperthermia 19 (2003) 204-212
23. Moriyama E., Salcman M., and Brodwell R. Blood-brain barrier alteration after microwave-induced hyperthermia is purely a thermal effect: temperature and power measurements. Surg. Neurol. 35 (1991) 177-182
24. Nagashima T., Ikeda K., Wu S., Kondo T., Yamaguchi M., and Tamaki N. The mechanism of reversible osmotic opening of the blood-brain barrier: role of intracellular calcium ion in capillary endothelial cells. Acta Neurochir., Suppl. 70 (1997) 231-233
25. Nakajima T., Roberts D., Ryan T., Hoopes P., Coughlin C., Trembly B., and Strohbehn J. Pattern of response to interstitial hyperthermia and brachytherapy for malignant intracranial tumour: a CT analysis. Int. J. Hyperthermia 9 (1993) 491-502
26. Ng K., Cho C., Henthorn T., and Tanguay R. Effect of heat preconditioning on the uptake and permeability of R123 in brain microvessel endothelial cells during mild heat treatment. J. Pharm. Sci. 93 (2004) 896-907
27. Ohomoto Y., Fujisawa H., Ishikawa T., Koizumi H., Matsuda T., and Ito H. Sequential changes in cerebral blood flow, early neuropathological consequences and blood-brain barrier disruption following radiofrequency-induced localized hyperthermia in the rat. Int. J. Hyperthermia 12 (1996) 321-324
28. Oztas B., and Kucuk M. Reversible blood-brain barrier dysfunction after intracarotid hyperthermic saline infusion. Int. J. Hyperthermia 14 (1998) 395-401
29. Raaphorst G.P., Mao J., and Ng C.E. Thermotolerance in human glioma cells. Int. J. Hyperthermia 11 (1995) 523-529
30. Rutten M.J., Hoover R.T., and Karnovsky M.J. Electrical resistance and macromolecular permeability of brain endothelial monolayer cultures. Brain Res. 425 (1987) 301-310
31. Sabel M., Rommel F., Kondakci M., Gorol M., Willers R., and Bilzer T. Locoregional opening of the rodent blood-brain barrier for paclitaxel using Nd:YAG laser-induced thermo therapy: a new concept of adjuvant glioma therapy?. Lasers Surg. Med. 33 (2003) 75-80
32. Schulze P., Vitzthum H., Goldammer A., Schneider J., and Schober R. Laser-induced thermotherapy of neoplastic lesions in the brain-underlying tissue alterations, MRI-monitoring and clinical applicability. Acta Neurochir (Wien). 146 (2004) 803-812
33. Sharma H.S. Pathophysiology of blood-brain barrier, brain edema and cell injury following hyperthermia: new role of heat shock protein, nitric oxide and carbon monoxide. Acta Univ. 830 (1999) 1-94
34. Sharma H., and Hoopes P. Hyperthermia induced pathophysiology of the central nervous system. Int. J. Hyperthermia 19 (2003) 325-354
35. Sharma H.S., Westman J., and Nyberg F. Pathophysiology of brain edema and cell changes following hyperthermic brain injury. Prog. Brain Res. 115 (1998) 351-412
36. Sharma H., Drieu K., Alm P., and Westman J. Role of nitric oxide in blood-brain barrier permeability, brain edema and cell damage following hyperthermic brain injury. An experimental study using EGB-761 and Gingkolide B pretreatment in the rat. Acta Neurochir., Suppl. 76 (2000) 81-86
37. Shivers R.R., Pollock M., Bowman P.D., and Atkinson B.G. The effect of heat shock on primary cultures of brain capillary endothelium: inhibition of assembly of zonulae occludentes and the synthesis of heat-shock proteins. Eur. J. Cell Biol. 46 (1988) 181-195
38. Sill H.W., Butler C., Hollis T.M., and Tarbell J.M. Albumin permeability and electrical resistance as means of assessing endothelial monolayer integrity in vitro. J. Tissue Cult. Methods 14 (1992) 253-258
39. Urakawa M., Yamaguchi K., Tsuchida E., Kashiwagi S., Ito H., and Matsuda T. Blood-brain barrier disturbance following localized hyperthermia in rats. Int. J. Hyperthermia 11 (1995) 709-718
40. Wijsman J.A., and Shivers R.R. Heat stress affects blood-brain barrier permeability to horseradish peroxidase in mice. Acta Neuropathol. 86 (1993) 49-54