Effects of estradiol on ischemic factor-induced astrocyte swelling and AQP4 protein abundance

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 1, 2011, Pages

  Rutkowsky, Jennifer M ^a   Wallace, Breanna K ^a   Wise, Phyllis M ^a   O'Donnell, Martha E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aquaporin 4; Astrocytes; Cerebral ischemia; Cytotoxic edema

Indexed keywords

3 METHYLGLUCOSE; AQUAPORIN 4; ARGIPRESSIN; BUMETANIDE; CARIPORIDE; ESTRADIOL; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM PROTON EXCHANGE PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE SWELLING; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; EDEMA; ENZYME INHIBITION; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; AQUAPORIN 4; ARGININE VASOPRESSIN; ASTROCYTES; BLOTTING, FAR-WESTERN; BRAIN EDEMA; BUMETANIDE; CELL HYPOXIA; CELL SIZE; CELLS, CULTURED; ESTRADIOL; GLUCOSE; GUANIDINES; RATS; RATS, SPRAGUE-DAWLEY; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; SODIUM-HYDROGEN ANTIPORTER; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SULFONES;

RATTUS;

EID: 79959834906     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00399.2010     Document Type: Article

References (69)

1. Amiry-Moghaddam M, Frydenlund DS, Ottersen OP. Anchoring of aquaporin-4 in brain: molecular mechanisms and implications for the physiology and pathophysiology of water transport. Neuroscience 129: 999-1010, 2004.
2. Amiry-Moghaddam M, Xue R, Haug FM, Neely JD, Bhardwaj A,Agre P, Adams ME, Froehner SC, Mori S, Ottersen OP. Alphasyntrophin deletion removes the perivascular but not endothelial pool of aquaporin-4 at the blood-brain barrier and delays the development of brain edema in an experimental model of acute hyponatremia. FASEB J 18: 542-544, 2004.
3. Badaut J, Ashwal S, Tone B, Regli L, Tian HR, Obenaus A. Temporal and regional evolution of aquaporin-4 expression and magnetic resonance imaging in a rat pup model of neonatal stroke. Pediatr Res 62: 248-254, 2007.
4. Badaut J, Lasbennes F, Magistretti PJ, Regli L. Aquaporins in brain: distribution, physiology, and pathophysiology. J Cereb Blood Flow Metab 22: 367-378, 2002.
5. Baringa M. Finding new drugs to treat stroke. Science 272: 646-666, 1996.
6. + influx. J Neurosci Res 52: 307-321, 1998.
7. Betz AL. Alterations in cerebral endothelial cell function in ischemia. Adv Neurol 71: 301-313, 1996.
8. Betz AL, Iannotti F, Hoff JT. Brain edema: a classification based on blood-brain barrier integrity. Cerebrovasc Brain Metab Rev 1: 133-154, 1989.
9. Betz AL, Keep RF, Beer ME, Ren XD. Blood-brain barrier permeability and brain concentration of sodium, potassium, and chloride during focal ischemia. J Cereb Blood Flow Metab 14: 29-37, 1994.
10. Bevensee MO, Boron WF. Effects of acute hypoxia on intracellular-pH regulation in astrocytes cultured from rat hippocampus. Brain Res 1193: 143-152, 2008.
11. Bourke RS, Kimelberg HK, Nelson LR, Barron KD, Auen EL, Popp AJ, Waldman JB. Biology of glial swelling in experimental brain edema. Adv Neurol 28: 99-109, 1980.
12. Brillault J, Lam TI, Rutkowsky JM, Foroutan S, O'Donnell ME. Hypoxia effects on cell volume and ion uptake of cerebral microvascular endothelial cells. Am J Physiol Cell Physiol 294: C88-C96, 2008.
13. Brown AM, Ransom BR. Astrocyte glycogen and brain energy metabolism. Glia 55: 1263-1271, 2007.
14. Chang E, O'Donnell ME, Barakat AI. Shear stress and 17beta-estradiol modulate cerebral microvascular endothelial Na-K-Cl cotransporter and Na/H exchanger protein levels. Am J Physiol Cell Physiol 294: C363-C371, 2008.
15. Chen YJ, Anderson SE, O'Donnell ME. Bumetanide and HOE642 administered after initiation of middle cerebral artery occlusion effectively reduce rat brain Na uptake and infarct (Abstract). FASEB J 23: A614.613, 2009.
16. Chen YJ, Lam TI, Anderson SE, Walton JH, O'Donnell ME. Bloodbrain barrier Na-K-Cl cotransporter and Na/H exchanger: therapeutic targets for ischemia-induced brain Na uptake and edema formation (Abstract). J Cereb Blood Flow Metab 29: S489, 2009.
17. Del Bigio MR, Fedoroff S, Qualtiere LF. Morphology of astroglia in colony cultures following transient exposure to potassium ion, hypoosmolarity and vasopressin. J Neurocytol 21: 7-18, 1992.
18. Dóczi T. Volume regulation of the brain tissue-a survey. Acta Neurochir (Wien) 121: 1-8, 1992.
19. Dubal DB, Kashon ML, Pettigrew LC, Ren JM, Finklestein SP, Rau SW, Wise PM. Estradiol protects against ischemic injury. J Cereb Blood Flow Metab 18: 1253-1258, 1998.
20. Dubal DB, Wise PM. Neuroprotective effects of estradiol in middle-aged female rats. Endocrinology 142: 43-48, 2001.
21. - cotransporter. Am J Physiol Cell Physiol 289: C1492-C1501, 2005.
22. Frydenlund DS, Bhardwaj A, Otsuka T, Mylonakou MN, Yasumura T, Davidson KG, Zeynalov E, Skare O, Laake P, Haug FM, Rash JE,Agre P, Ottersen OP, Amiry-Moghaddam M. Temporary loss of perivascular aquaporin-4 in neocortex after transient middle cerebral artery occlusion in mice. Proc Natl Acad Sci U S A 103: 13532-13536, 2006.
23. Garcia-Segura LM, Azcoitia I, DonCarlos LL. Neuroprotection by estradiol. Prog Neurobiol 63: 29-60, 2001.
24. Gartshore G, Patterson J, Macrae IM. Influence of ischemia and reperfusion on the course of brain tissue swelling and blood-brain barrier permeability in a rodent model of transient focal cerebral ischemia. Exp Neurol 147: 353-360, 1997.
25. 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.
26. Gunnarson E, Song Y, Kowalewski JM, Brismar H, Brines M, Cerami A, Andersson U, Zelenina M, Aperia A. Erythropoietin modulation of astrocyte water permeability as a component of neuroprotection. Proc Natl Acad Sci U S A 106: 1602-1607, 2009.
27. Hurn PD, Macrae IM. Estrogen as a neuroprotectant in stroke. J Cereb Blood Flow Metab 20: 631-652, 2000.
28. + exchange. Brain Res 485: 215-224, 1989.
29. Jójárt I, Joo F, Siklos L, Laszlo FA. Immunoelectronhistochemical evidence for innervation of brain microvessels by vasopressin-immunoreactive neurons in the rat. Neurosci Lett 51: 259-264, 1984.
30. Katay L, Latzkovits L, Fonagy A, Janka Z, Lajtha A. Effects of arginine vasopressin and atriopeptin on chloride uptake in cultured astroglia. Neurochem Res 23: 831-836, 1998.
31. Kimelberg HK. Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy. Glia 50: 389-397, 2005.
32. Kimelberg HK. Current concepts of brain edema. Review of laboratory investigations. J Neurosurg 83: 1051-1059, 1995.
33. Kimelberg HK, Barron KD, Bourke RS, Nelson LR, Cragoe EJ. Brain anti-cytoxic edema agents. Prog Clin Biol Res 361: 363-385, 1990.
34. + exchanger isoform 1 null mice. Am J Physiol Cell Physiol 287: C12-C21, 2004.
35. 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: 537-544, 1975.
36. Kuroiwa T, Miyasaka N, Fengyo Z, Yamada I, Nakane M, Nagaoka T,Tamura A, Ohno K. Experimental ischemic brain edema: morphological and magnetic resonance imaging findings. Neurosurg Focus 22: E11, 2007.
37. Lam TI, Wise PM, O'Donnell ME. Cerebral microvascular endothelial cell Na/H exchange: evidence for the presence of NHE1 and NHE2 isoforms and regulation by arginine vasopressin. Am J Physiol Cell Physiol 297: C278-C289, 2009.
38. Landgraf R. Central release of vasopressin: stimuli, dynamics, consequences. Prog Brain Res 91: 29-39, 1992.
39. Latzkovits L, Cserr HF, Park JT, Patlak CS, Pettigrew KD,Rimanoczy A. Effects of arginine vasopressin and atriopeptin on glial cell volume measured as 3-MG space. Am J Physiol Cell Physiol 264: C603-C608, 1993.
40. Lehmann GL, Gradilone SA, Marinelli RA. Aquaporin water channels in central nervous system. Curr Neurovasc Res 1: 293-303, 2004.
41. + signaling in astrocytes in an in vitro ischemic model. J Neurosci 24: 9585-9597, 2004.
42. Liang D, Bhatta S, Gerzanich V, Simard JM. Cytotoxic edema: mechanisms of pathological cell swelling. Neurosurg Focus 22: E2, 2007.
43. Liu KF, Li F, Tatlisumak T, Garcia JH, Sotak CH, Fisher M,Fenstermacher MD. 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.
44. Liu X, Nakayama S, Amiry-Moghaddam M, Ottersen OP, Bhardwaj A. Arginine-vasopressin V1 but not V2 receptor antagonism modulated infarct volume brain water content, and aquaporin-4 expression following experimental stroke. Neurocrit Care 12: 124-131, 2010.
45. MacVicar BA, Feighan D, Brown A, Ransom B. Intrinsic optical signals in the rat optic nerve: role for K(+) uptake via NKCC1 and swelling of astrocytes. Glia 37: 114-123, 2002.
46. McCarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85: 890-902, 1980.
47. 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.
48. O'Donnell ME, Duong V, Suvatne J, Foroutan S, Johnson DM. Arginine vasopressin stimulation of cerebral microvascular endothelial cell Na-K-Cl cotransporter activity is V1 receptor and [Ca] dependent. Am J Physiol Cell Physiol 289: C283-C292, 2005.
49. O'Donnell ME, Lam TI, Tran L, Anderson SE. The role of the blood-brain barrier Na-K-2Cl cotransporter in stroke. Adv Exp Med Biol 559: 67-75, 2004.
50. 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.
51. O'Donnell ME, Tran L, Lam TI, 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.
52. Okuno K, Taya K, Marmarou CR, Ozisik P, Fazzina G, Kleindienst A, Gulsen S, Marmarou A. The modulation of aquaporin-4 by using PKC-activator (phorbol myristate acetate) and V1a receptor antagonist (SR49059) following middle cerebral artery occlusion/reperfusion in the rat. Acta Neurochir Suppl (Wien) 102: 431-436, 2008.
53. Park CK, Jun SS, Cho SH, Kang JK. Assessment of the relationship between ischemic damage and brain swelling in frozen brain slices. Acta Neurochir Suppl (Wien) 70: 17-19, 1997.
54. Pasantes-Morales H, Cruz-Rangel S. Brain volume regulation: osmolytes and aquaporin perspectives. Neuroscience 168: 871-884, 2010.
55. Ribeiro Md Hirt L, Bogousslavsky J, Regli L, Badaut J. Time course of aquaporin expression after transient focal cerebral ischemia in mice. J Neurosci Res 83: 1231-1240, 2006.
56. Schielke GP, Moises HC, Betz AL. Blood to brain sodium transport and interstitial fluid potassium concentration during early focal ischemia in the rat. J Cereb Blood Flow Metab 11: 466-471, 1991.
57. Shi J, Bui JD, Yang SH, He Z, Lucas TH, Buckley DL, Blackband SJ,King MA, Day AL, Simpkins JW. Estrogens decrease reperfusionassociated cortical ischemic damage: an MRI analysis in a transient focal ischemia model. Stroke 32: 987-992, 2001.
58. Silberstein C, Bouley R, Huang Y, Fang P, Pastor-Soler N, Brown D, Van Hoek AN. Membrane organization and function of M1 and M23 isoforms of aquaporin-4 in epithelial cells. Am J Physiol Renal Physiol 287: F501-F511, 2004.
59. Simpkins JW, Rajakumar G, Zhang YQ, Simpkins CE, Greenwald D,Yu CJ, Bodor N, Day AL. Estrogens may reduce mortality and ischemic damage cau\sed by middle cerebral artery occlusion in the female rat. J Neurosurg 87: 724-730, 1997.
60. Sorensen PS, Gjerris A, Hammer M. Cerebrospinal fluid vasopressin in neurological and psychiatric disorders. J Neurol Neurosurg Psychiatry 48: 50-57, 1985.
61. Staub F, Peters J, Kempski O, Schneider GH, Schurer L, Baethmann A. Swelling of glial cells in lactacidosis and by glutamate: significance of Cl(-)-transport. Brain Res 610: 69-74, 1993.
62. +]o-induced swelling and EAA release in astrocytes. Am J Physiol Cell Physiol 282: C1136-C1146, 2002.
63. Suzuki S, Brown CM, Wise PM. Mechanisms of neuroprotection by estrogen. Endocrine 29: 209-215, 2006.
64. Tomas-Camardiel M, Venero JL, Herrera AJ, De Pablos RM, Pintor-Toro JA, Machado A, Cano J. Blood-brain barrier disruption highly induces aquaporin-4 mRNA and protein in perivascular and parenchymal astrocytes: protective effect by estradiol treatment in ovariectomized animals. J Neurosci Res 80: 235-246, 2005.
65. Toung TJ, Traystman RJ, Hurn PD. Estrogen-mediated neuroprotection after experimental stroke in male rats. Stroke 29: 1666-1670, 1998.
66. Vakill A, Kataoka H, Plesnilla N. Role of arginine vasopressin V1 and V2 receptors for brain damage after transient focal ischemia. J Cereb Blood Flow Metab 25: 1012-1019, 2005.
67. Walls AB, Sickmann HM, Brown A, Bouman SD, Ransom B, Schousboe A, Waagepetersen HS. Characterization of 1.4-dideoxy-1, 4-imino- D-arabinitol. (DAB) as an inhibitor of brain glycogen shunt activity. J Neurochem 105: 1462-1470, 2008.
68. Wise PM, Dubal DB. Estradiol protects against ischemic brain injury in middle-aged rats. Biol Reprod 63: 982-985, 2000.
69. Wise PM, Dubal DB, Wilson ME, Rau SW, Bottner M, Rosewell KL. Estradiol is a protective factor in the adult and aging brain: understanding of mechanisms derived from in vivo and in vitro studies. Brain Res Brain Res Rev 37: 313-319, 2001.