Conserved aquaporin 4 levels associated with reduction of brain edema are mediated by estrogen in the ischemic brain after experimental stroke

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1812, Issue 9, 2011, Pages 1154-1163

  Shin, Jin A ^a   Choi, Ji Ha ^a   Choi, Youn Hee ^a   Park, Eun Mi ^a,b  

^a Ewha Womans University School of Medicine   (South Korea)

^b Ewha Womans University   (South Korea)

Author keywords

Aquaporin 4; Brain edema; Estrogen; Estrogen receptor; Ischemic stroke; Sex difference

Indexed keywords

AQUAPORIN 4; CYCLOPHILIN; ESTROGEN RECEPTOR; FULVESTRANT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN EDEMA; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; ESTROGEN THERAPY; FEMALE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; STROKE;

ANIMALS; AQUAPORIN 4; BRAIN EDEMA; BRAIN INFARCTION; BRAIN ISCHEMIA; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROGENS; FEMALE; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, ESTROGEN; SEX FACTORS; STROKE;

MUS;

EID: 79960562989     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.05.004     Document Type: Article

References (39)

1. Bardutzky J., Schwab S. Antiedema therapy in ischemic stroke. Stroke 2007, 38:3084-3094.
2. Ropper A.H., Shafran B. Brain edema after stroke. Clinical syndrome and intracranial pressure. Arch. Neurol. 1984, 41:26-29.
3. Nielsen S., Nagelhus E.A., Amiry-Moghaddam M., Bourque C., Agre P., Ottersen O.P. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 1997, 17:171-180.
4. Kobayashi H., Yanagita T., Yokoo H., Wada A. Molecular mechanisms and drug development in aquaporin water channel diseases: aquaporins in the brain. J. Pharmacol. Sci. 2004, 96:264-270.
5. Tait M.J., Saadoun S., Bell B.A., Papadopoulos M.C. Water movements in the brain: role of aquaporins. Trends Neurosci. 2008, 31:37-43.
6. Manley G.T., Fujimura M., Ma T., Noshita N., Filiz F., Bollen A.W., Chan P., Verkman A.S. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 2000, 6:159-163.
7. Papadopoulos M.C., Manley G.T., Krishna S., Verkman A.S. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 2004, 18:1291-1293.
8. Amiry-Moghaddam M., Otsuka T., Hurn P.D., Traystman R.J., Haug F.M., Froehner S.C., Adams M.E., Neely J.D., Agre P., Ottersen O.P., Bhardwaj A. An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:2106-2111.
9. Taniguchi M., Yamashita T., Kumura E., Tamatani M., Kobayashi A., Yokawa T., Maruno M., Kato A., Ohnishi T., Kohmura E., Tohyama M., Yoshimine T. Induction of aquaporin-4 water channel mRNA after focal cerebral ischemia in rat. Brain. Res. Mol. Brain. Res. 2000, 78:131-137.
10. Frydenlund D.S., Bhardwaj A., Otsuka T., Mylonakou M.N., Yasumura T., Davidson K.G., Zeynalov E., Skare O., Laake P., Haug F.M., Rash J.E., Agre P., Ottersen O.P., 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. 2006, 103:13532-13536.
11. Suzuki S., Brown C.M., Wise P.M. Neuroprotective effects of estrogens following ischemic stroke. Front. Neuroendocrinol. 2009, 30:201-211.
12. Liu X., Zhang W., Alkayed N.J., Froehner S.C., Adams M.E., Amiry-Moghaddam M., Ottersen O.P., Hurn P.D., Bhardwaj A. Lack of sex-linked differences in cerebral edema and aquaporin-4 expression after experimental stroke. J. Cereb. Blood Flow Metab. 2008, 28:1898-1906.
13. Liu F., Yuan R., Benashski S.E., McCullough L.D. Changes in experimental stroke outcome across the life span. J. Cereb. Blood Flow Metab. 2009, 29:792-802.
14. O'Donnell M.E., Lam T.I., Tran L.Q., Foroutan S., Anderson S.E. 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. 2006, 26:1234-1249.
15. Shi J., Bui J.D., Yang S.H., He Z., Lucas T.H., Buckley D.L., Blackband S.J., King M.A., Day A.L., Simpkins J.W. Estrogens decrease reperfusion-associated cortical ischemic damage: an MRI analysis in a transient focal ischemia model. Stroke 2001, 32:987-992.
16. Shahrokhi N., Khaksari M., Soltani Z., Mahmoodi M., Nakhaee N. Effect of sex steroid hormones on brain edema, intracranial pressure, and neurologic outcomes after traumatic brain injury. Can. J. Physiol. Pharmacol. 2010, 88:414-421.
17. O'Connor C.A., Cernak I., Vink R. Both estrogen and progesterone attenuate edema formation following diffuse traumatic brain injury in rats. Brain Res. 2005, 1062:171-174.
18. Guo Q., Sayeed I., Baronne L.M., Hoffman S.W., Guennoun R., Stein D.G. Progesterone administration modulates AQP4 expression and edema after traumatic brain injury in male rats. Exp. Neurol. 2006, 198:469-478.
19. Gu F., Hata R., Toku K., Yang L., Ma Y.J., Maeda N., Sakanaka M., Tanaka J. Testosterone up-regulates aquaporin-4 expression in cultured astrocytes. J. Neurosci. Res. 2003, 72:709-715.
20. Tomas-Camardiel M., Venero J.L., Herrera A.J., De Pablos R.M., Pintor-Toro J.A., 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. 2005, 80:235-246.
21. Park E.M., Cho S., Frys K., Glickstein S., Zhou P., Anrather J., Ross M., Iadecola C. Inducible nitric oxide synthase contributes to gender differences in ischemic brain injury. J. Cereb. Blood Flow Metab. 2006, 26:392-401.
22. Shin J.A., Park E.M., Choi J.S., Seo S.M., Kang J.L., Lee K.E., Cho S. Ischemic preconditioning-induced neuroprotection is associated with differential expression of IL-1beta and IL-1 receptor antagonist in the ischemic cortex. J. Neuroimmunol. 2009, 217:14-19.
23. Sawada M., Alkayed N.J., Goto S., Crain B.J., Traystman R.J., Shaivitz A., Nelson R.J., Hurn P.D. Estrogen receptor antagonist ICI182,780 exacerbates ischemic injury in female mouse. J. Cereb. Blood Flow Metab. 2000, 20:112-118.
24. Lin T.N., He Y.Y., Wu G., Khan M., Hsu C.Y. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 1993, 24:117-121.
25. Kondo T., Reaume A.G., Huang T.T., Carlson E., Murakami K., Chen S.F., Hoffman E.K., Scott R.W., Epstein C.J., Chan P.H. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J. Neurosci. 1997, 17:4180-4189.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
27. Hayashi S., Ueyama T., Kajimoto T., Yagi K., Kohmura E., Saito N. Involvement of gamma protein kinase C in estrogen-induced neuroprotection against focal brain ischemia through G protein-coupled estrogen receptor. J. Neurochem. 2005, 93:883-891.
28. Hirt L., Ternon B., Price M., Mastour N., Brunet J.F., Badaut J. Protective role of early aquaporin 4 induction against postischemic edema formation. J. Cereb. Blood Flow Metab. 2009, 29:423-433.
29. Nagelhus E.A., Horio Y., Inanobe A., Fujita A., Haug F.M., Nielsen S., Kurachi Y., Ottersen O.P. Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Muller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia 1999, 26:47-54.
30. Nagelhus E.A., Mathiisen T.M., Ottersen O.P. Aquaporin-4 in the central nervous system: cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 2004, 129:905-913.
31. Ribeiro Mde C., Hirt L., Bogousslavsky J., Regli L., Badaut J. Time course of aquaporin expression after transient focal cerebral ischemia in mice. J. Neurosci. Res. 2006, 83:1231-1240.
32. Yang M., Gao F., Liu H., Yu W.H., Sun S.Q. Temporal changes in expression of aquaporin-3, -4, -5 and -8 in rat brains after permanent focal cerebral ischemia. Brain Res.. 2009, 1290:121-132.
33. Zheng Y.Y., Lan Y.P., Tang H.F., Zhu S.M. Propofol pretreatment attenuates aquaporin-4 over-expression and alleviates cerebral edema after transient focal brain ischemia reperfusion in rats. Anesth. Analg. 2008, 107:2009-2016.
34. Kikuchi K., Tancharoen S., Matsuda F., Biswas K.K., Ito T., Morimoto Y., Oyama Y., Takenouchi K., Miura N., Arimura N., Nawa Y., Meng X., Shrestha B., Arimura S., Iwata M., Mera K., Sameshima H., Ohno Y., Maenosono R., Tajima Y., Uchikado H., Kuramoto T., Nakayama K., Shigemori M., Yoshida Y., Hashiguchi T., Maruyama I., Kawahara K. Edaravone attenuates cerebral ischemic injury by suppressing aquaporin-4. Biochem. Biophys. Res. Commun. 2009, 390:1121-1125.
35. Zeng H.K., Wang Q.S., Deng Y.Y., Fang M., Chen C.B., Fu Y.H., Jiang W.Q., Jiang X. Hypertonic saline ameliorates cerebral edema through downregulation of aquaporin-4 expression in the astrocytes. Neuroscience 2010, 166:878-885.
36. Migliati E.R., Amiry-Moghaddam M., Froehner S.C., Adams M.E., Ottersen O.P., Bhardwaj A. Na(+)-K(+)-2Cl(-) cotransport inhibitor attenuates cerebral edema following experimental stroke via the perivascular pool of aquaporin-4. Neurocrit. Care 2010, 13:123-131.
37. Liu X., Nakayama S., Amiry-Moghaddam M., Ottersen O.P., Bhardwaj A. Arginine-vasopressin V1 but not V2 receptor antagonism modulates infarct volume, brain water content, and aquaporin-4 expression following experimental stroke. Neurocrit. Care 2010, 12:124-131.
38. Gunnarson E., Zelenina M., Aperia A. Regulation of brain aquaporins. Neuroscience 2004, 129:947-955.
39. Vasudevan N., Pfaff D.W. Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front. Neuroendocrinol. 2008, 29:238-257.