Hypoxia effects on cell volume and ion uptake of cerebral microvascular endothelial cells

American Journal of Physiology - Cell Physiology

Volumn 294, Issue 1, 2008, Pages

  Brillault, Julien ^a,b   Lam, Tina I ^a   Rutkowsky, Jennifer M ^a   Foroutan, Shahin ^a   O'Donnell, Martha E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITÉ DE POITIERS   (France)

Author keywords

Brain microvessels; Bumetanide; Cerebral edema; Cerebral ischemia; Cotransport

Indexed keywords

3 METHYLGLUCOSE; BUMETANIDE; CARIPORIDE; ESTRADIOL; GLUCOSE; POTASSIUM ION; SODIUM ION; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SUCROSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CELL; BRAIN EDEMA; BRAIN ISCHEMIA; CELL HYPOXIA; CELL SWELLING; CONTROLLED STUDY; COW; ENDOTHELIUM CELL; EXTRACELLULAR FLUID; FEMALE; HUMAN; HUMAN CELL; ION PAIR CHROMATOGRAPHY; ION TRANSPORT; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SODIUM TRANSPORT; STROKE; VASCULAR ENDOTHELIUM;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN EDEMA; BUMETANIDE; CATTLE; CELL HYPOXIA; CELL SIZE; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; EXTRACELLULAR FLUID; GLUCOSE; GUANIDINES; INFARCTION, MIDDLE CEREBRAL ARTERY; INTRACELLULAR FLUID; MICROCIRCULATION; POTASSIUM; RATS; SODIUM; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; SODIUM-HYDROGEN ANTIPORTER; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SULFONES; TIME FACTORS; VASOPRESSINS;

EID: 38349169844     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00148.2007     Document Type: Article

References (48)

1. Abbruscato TA, Davis TP. Combination of hypoxia/aglycemia compromises in vitro blood-brain barrier integrity. J Pharmacol Exp Ther 289: 668-675, 1999.
2. Atwal KS, O'Neil SV, Ahmad S, Doweyko L, Kirby M, Corso CR, Chandrasena G, Chen BC, Zhao R, Zahler R. Synthesis and biological activity of r-aryl-4-(4-(5-methyl-1H-imidazol-4-yl)piperidin-1-yl)pyrimidine analogs as potent, highly selective, and orally bioavailable NHE-1 inhibitors. Bioorgan Med Chem Lett 16: 4796-4799, 2006.
3. + influx. J Neurosci Res 52: 307-321, 1998.
4. Betz AL. Alterations in cerebral endothelial cell function in ischemia. Adv Neurol 71: 301-313, 1996.
5. Betz AL, Keep RF, Beer ME, Ren X. Blood-brain barrier permeability and brain concentration of sodium, potassium, and chloride during focal ischemia. J Cereb Blood Flow Metab 14: 29-37, 1994.
6. Bourke RS, Kimelberg HK, Nelson LR, Barron KD, Auen EL, Popp AJ, Waldman JB. Biology of glial swelling in experimental brain edema. Adv Neurol Brain Edema 28: 99-109, 1980.
7. Brillault J, Berezowski V, Cecchelli R, Dehouck MP. Intercommunications between brain capillary endothelial c ells and glial cells increase the transcellular permeability of the blood-brain barrier during ischaemia. J Neurochem 83: 807-817, 2002.
8. Dharmsathaphorn K, Mandel KG, Masui H, McRoberts JA. Vasoactive intestinal polypeptide-induced chloride secretion by a colonic epithelial cell line. J Clin Invest 75: 462-471, 1985.
9. Dickinson LD, Betz AL. Attenuated development of ischemic brain edema in vasopressin-deficient rats. J Cereb Blood Flow Metab 12: 681-690, 1992.
10. Dóczi T, Szerdahelyi P, Gulya K, Kiss J. Brain water accumulation after the central administration of vasopressin. Neurosurgery 11: 402-407, 1982.
11. Fischer H, Illek B, Finkbeiner WE, Widdicombe JH. Basolateral Cl channels in primary airway epithelial cultures. Am J Physiol Lung Cell Mol Physiol 292: L1432-L1443, 2007.
12. Foroutan S, Brillault J, Forbush B, O'Donnell ME. Moderate to severe ischemic conditions increase activity and phosphorylation of the cerebral microvascular endothelial cell Na-K-Cl cotransporter. Am J Physiol Cell Physiol 289: C1492-C1501, 2005.
13. Golshani P, Liu XB, Jones EG. Differences in quantal amplitude reflect GLUR4-subunit number at corticothalamic synapses on two populations of thalamic neurons. Proc Natl Acad Sci USA 98: 4172-4177, 2001.
14. Gotoh O, Asano T, Koide T, Takakura K. Ischemic brain edema following occlusion of the middle cerebral artery in the rat. I: The time course of the brain water, sodium and potassium contents and blood-brain barrier permeability to 125I-albumin. Stroke 16: 101-109, 1985.
15. Haas M. Properties and diversity of (Na-K-Cl) cotransporters. Annu Rev Physiol 51: 443-457, 1989.
16. Haas M, Forbush B. The Na-K-Cl cotransporter of secretory epithelia. Annu Rev Physiol 62: 515-534, 2000.
17. Haas M, McBrayer DG. Na-K-Cl cotransport in nystatin-treated tracheal cells: regulation by isoproterenol, apical UTP, and [Cl]i. Am J Physiol Cell Physiol 266: C1440-C1452, 1994.
18. Hatashita S, Hoff J. Brain edema and cerebrovascular permeability during cerebral ischemia in rats. Stroke 21: 582-588, 1990.
19. Iadecola C. Mechanisms of Cerebral Ischemic Damage. In: Cerebral Ischemia: Molecular and Cellular Pathophysiology, edited by Walz W. Totowa, NJ: Humana, 1999, p. 3-34.
20. Jójárt I, Joó F, Siklós L, László FA. Immunoelectronhistochemical evidence for innervation of brain microvessels by vasopressin-immunoreactive neurons in the rat. Neurosci Lett 51: 259-264, 1984.
21. Kalaria RN, Premkumar DR, Lin CW, Kroon SN, Bae JY, Sayre LM, LaManna JC. Identification and expression of the Na+/H+ exchanger in mammalian cerebrovascular and choroidal tissues: characterization by amiloride-sensitive [3H]MIA binding and RT-PCR analysis. Brain Res Mol Brain Res 58: 178-187, 1998.
22. -- cotransport in cultured brain capillary endothelial cells of the rat. J Neurochem 66: 2572-2579, 1996.
23. Kawai N, McCarron RM, Spatz M. The effect of endothelins on ion transport systems in cultured rat brain capillary endothelial cells. Acta Neurochir (Wien) 70: 138-140, 1997.
24. A receptors and protein kinase C-dependent pathway in cerebral capillary endothelium. J Neurochem 65: 1588-1596, 1995.
25. Kempski O, Rosen Sv Weight H, Staub F, Peters J, Baethmann A. Glial ion transport and volume control. In: Glial-Neuronal Interaction, edited by Abbott NJ. New York: New York Acad Sci, 1991, p. 306-317.
26. Kimelberg HK. Current concepts of brain edema. Rev Lab Invest J Neurosurg 83: 1051-1059, 1995.
27. Kletzien RF, Pariza MW, Becker JE, Potter VR. A method using 3-O-methyl-D-glucose and phloretin for the determination of intracellular water space of cells in monolayer culture. Anal Biochem 68: 5370544, 1975.
28. Lam TI, Wise PM, O'Donnell ME. Na/H exchange of cerebral microvascular endothelial cells: evidence for the presence of NHE1 and NHE2 isoforms and stimulation by ischemic conditions. Soc Neurosci, Atlanta GA, 2006, p. Program No. 8318.
29. Landgraf R. Central release of vasopressin: stimuli, dynamics, consequences. Prog Brain Res 91: 29-39, 1992.
30. Liu KF, Li F, Tatlisumak T, Garcia JH, Sotak CH, Fisher M, Fenstermacher JD. Regional variations in the apparent diffusion coefficient and the intracellular distribution of water in rat brain during acute focal ischemia. Stroke 32: 1897-1905, 2001.
31. + exchanger. Eur J Med Chem 38: 547-554, 2003.
32. Menzies SA, Betz AL, Hoff JT. Contributions of ions and albumin to the formation and resolution of ischemic brain edema. J Neurosurg 78: 257-266, 1993.
33. O'Donnell ME. Role of Na-K-Cl cotransport in vascular endothelial cell volume regulation. Am J Physiol Cell Physiol 264: C1316-C1326, 1993.
34. O'Donnell ME, Duong V, Suvatne S, Foroutan S, Johnson DM. Arginine vasopressin stimulation of cerebral microvascular endothelial cell Na-K-Cl cotransport activity is V1 receptor- and [Ca]-dependent. Am J Physiol Cell Physiol 289: C283-C292, 2005.
35. O'Donnell ME, Lam TI, Tran LQ, Foroutan S, Anderson SE. Estradiol reduces activity of the blood-brain barrier Na-K-Cl cotransporter and decreases edema formation in permanent middle cerebral artery occlusion. J Cereb Blood Flow Metab 26: 1234-1249, 2006.
36. O'Donnell ME, Martinez A, Sun D. Cerebral microvascular endothelial cell Na-K-Cl cotransport: regulation by astrocyte-conditioned medium. Am J Physiol Cell Physiol 268: C747-C754, 1995.
37. O'Donnell ME, Tran L, Lam T, Liu XB, Anderson SE. Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke. J Cereb Blood Flow Metab 24: 1046-1056, 2004.
38. - cotransporter in the heart, brain and blood. Am J Physiol Regul Integr Comp Physiol 291: R1-R25, 2006.
39. Rosenberg GA, Estrada E, Kyner WT. Vasopressin-induced brain edema is mediated by the V1 receptor. Adv Neurol 52: 149-154, 1990.
40. Russell JM. Sodium-potassium-chloride cotransport. Physiol Rev 80: 211-276, 2000.
41. Schielke GP, Moises HC, Betz AL. Blood to brain sodium transport and interstitial fluid potassium concentration during focal ischemia in the rat. J Cereb Blood Flow Metab 11: 466-471, 1991.
42. Scholz W, Jessel A, Albus U. Development of the Na+/H+ exchange inhibitor cariporide as a cardioprotective drug: from the laboratory to the GUARDIAN trial. J Thromb Thrombolysis 8: 61-70, 1999.
43. Sipos H, Törocsik B, Tretter L, Adam-Vizi V. Impaired regulation of pH homeostasis by oxidative stress in rat brain capillary endothelial cells. Cell Mol Neurobiol 25: 141-151, 2005.
44. Sorensen PS, Gjerris A, Hammer M. Cerebrospinal fluid vasopressin in neurological and psychiatric disorders. J Neurol Neurosurg Psychiatry 48: 50-57, 1985.
45. Sun D, Lytle C, O'Donnell ME. Astroglial cell-induced expression of Na-K-Cl cotransporter in brain microvascular endothelial cells. Am J Physiol Cell Physiol 269: C1506-C1512, 1995.
46. Vigne P, Champigny G, Marsault R, Barbry P, Frelin C, Lazdunski M. A new type of amiloride-sensitive cationic channel in endothelial cells of brain microvessels. J Biol Chem 264: 7663-7668, 1989.
47. von Weikersthal SF, Barrand MA, Hladky SB. Functional and molecular characterization of a volume-sensitive chloride current in rat brain endothelial cells. J Physiol 516: 75-84, 1999.
48. Young W, Rappaport ZH, Chalif DJ, Flamm ES. Regional brain sodium, potassium, and water changes in the rat middle cerebral artery occlusion model of ischemia. Stroke 18: 751-759, 1987.