Selective vasopressin-1a receptor antagonist prevents brain edema, reduces astrocytic cell swelling and GFAP, V1aR and AQP4 expression after focal traumatic brain injury

Brain Research

Volumn 1581, Issue , 2014, Pages 89-102

  Marmarou, Christina R ^a   Liang, Xiuyin ^a   Abidi, Naqeeb H ^a   Parveen, Shanaz ^a   Taya, Keisuke ^a   Henderson, Scott C ^a   Young, Harold F ^a   Filippidis, Aristotelis S ^a   Baumgarten, Clive M ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aquaporin 4; Astrocyte; Edema; SR49059; Traumatic brain injury; Vasopressin

Indexed keywords

AQUAPORIN 4 ANTIBODY; GLIAL FIBRILLARY ACIDIC PROTEIN; RELCOVAPTAN; VASOPRESSIN V1A RECEPTOR; AQP4 PROTEIN, RAT; AQUAPORIN 4; INDOLE DERIVATIVE; NEUROPROTECTIVE AGENT; PYRROLIDINE DERIVATIVE; V1A VASOPRESSIN RECEPTOR, RAT; VASOPRESSIN RECEPTOR; VASOPRESSIN RECEPTOR ANTAGONIST;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN EDEMA; BRAIN WATER; CELL SWELLING; COMPARATIVE STUDY; CONTINUOUS INFUSION; CONTROLLED STUDY; CORTICAL CONTUSION INJURY; DENSITOMETRY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; NEUROPROTECTION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; TRAUMATIC BRAIN INJURY; TRIPLE LABEL FLUORESCENCE IMMUNOHISTOCHEMISTRY; UPREGULATION; WATER CONTENT; WESTERN BLOTTING; ANIMAL; BRAIN INJURIES; COMPLICATION; CONFOCAL MICROSCOPY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIDIURETIC HORMONE RECEPTOR ANTAGONISTS; AQUAPORIN 4; ASTROCYTES; BRAIN EDEMA; BRAIN INJURIES; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; INDOLES; MALE; MICROSCOPY, CONFOCAL; NEUROPROTECTIVE AGENTS; PYRROLIDINES; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, VASOPRESSIN;

EID: 84907653286     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.06.005     Document Type: Article

References (78)

1. M. Amiry-Moghaddam, and O.P. Ottersen The molecular basis of water transport in the brain Nat. Rev. Neurosci. 4 2003 991 1001
2. A.M. Amorini, J.G. Dunbar, and A. Marmarou Modulation of aquaporin-4 water transport in a model of TBI Acta Neurochir. 86 Suppl. 2003 S261 S263
3. M. Bagheri, A. Rezakhani, S. Nystrom, M.V. Turkina, M. Roghani, P. Hammarstrom, and S. Mohseni Amyloid beta(1-40)-induced astrogliosis and the effect of genistein treatment in rat: a three-dimensional confocal morphometric and proteomic study PLoS One 8 2013 e76526
4. I. Bemana, and S. Nagao Treatment of brain edema with a nonpeptide arginine vasopressin V1 receptor antagonist OPC-21268 in rats Neurosurgery 44 1999 148 154
5. R. Bullock, W.L. Maxwell, D.I. Graham, G.M. Teasdale, and J.H. Adams Glial swelling following human cerebral contusion: an ultrastructural study J. Neurol. Neurosurg. Psychiatry 54 1991 427 434
6. E. Carrasco, C. Hernandez, A. Miralles, P. Huguet, J. Farres, and R. Simo Lower somatostatin expression is an early event in diabetic retinopathy and is associated with retinal neurodegeneration Diabetes Care 30 2007 2902 2908
7. V.G. Coronado, L. Xu, S.V. Basavaraju, L.C. McGuire, M.M. Wald, M.D. Faul, B.R. Guzman, and J.D. Hemphill Surveillance for traumatic brain injury-related deaths - United States, 1997-2007 MMWR Surveill. Summ. 60 2011 1 32
8. H.F. Cserr, and L. Latzkovits A role for centrally-released vasopressin in brain ion and volume regulation: a hypothesis Prog. Brain Res. 91 1992 3 6
9. R. Diaz-Arrastia, P.M. Kochanek, P. Bergold, K. Kenney, C.E. Marx, C.J. Grimes, L.Y. Loh, L.G. Adam, D. Oskvig, K.C. Curley, and C.W. Salzer Pharmacotherapy of traumatic brain injury: state of the science and the road forward: report of the department of defense neurotrauma pharmacology workgroup J. Neurotrauma 31 2014 135 158
10. L.D. Dickinson, and A.L. Betz Attenuated development of ischemic brain edema in vasopressin-deficient rats J. Cereb. Blood Flow Metab. 12 1992 681 690
11. W.D. Dietrich, J. Truettner, W. Zhao, O.F. Alonso, R. Busto, and M.D. Ginsberg Sequential changes in glial fibrillary acidic protein and gene expression following parasagittal fluid-percussion brain injury in rats J. Neurotrauma 16 1999 567 581
12. C.E. Dixon, B.G. Lyeth, J.T. Povlishock, R.L. Findling, R.J. Hamm, A. Marmarou, H.F. Young, and R.L. Hayes A fluid percussion model of experimental brain injury in the rat J. Neurosurg. 67 1987 110 119
13. T. Doczi, F.A. Laszlo, P. Szerdahelyi, and F. Joo Involvement of vasopressin in brain edema formation: further evidence obtained from the Brattleboro diabetes insipidus rat with experimental subarachnoid hemorrhage Neurosurgery 14 1984 436 441
14. T. Doczi, P. Szerdahelyi, K. Gulya, and J. Kiss Brain water accumulation after the central administration of vasopressin Neurosurgery 11 1982 402 407
15. L.F. Eng, and R.S. Ghirnikar GFAP and astrogliosis Brain Pathol. 4 1994 229 237
16. L.F. Eng, R.S. Ghirnikar, and Y.L. Lee Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000) Neurochem. Res. 25 2000 1439 1451
17. L. Fattore, M.C. Puddu, S. Picciau, A. Cappai, W. Fratta, G.P. Serra, and S. Spiga Astroglial in vivo response to cocaine in mouse dentate gyrus: a quantitative and qualitative analysis by confocal microscopy Neuroscience 110 2002 1 6
18. M. Faul, M.M. Wald, W. Rutland-Brown, E.E. Sullivent, and R.W. Sattin Using a cost-benefit analysis to estimate outcomes of a clinical treatment guideline: testing the Brain Trauma Foundation guidelines for the treatment of severe traumatic brain injury J. Trauma 63 2007 1271 1278
19. G. Fazzina, A.M. Amorini, C.R. Marmarou, S. Fukui, K. Okuno, J.G. Dunbar, R. Glisson, A. Marmarou, and A. Kleindienst The protein kinase C activator phorbol myristate acetate decreases brain edema by aquaporin 4 downregulation after middle cerebral artery occlusion in the rat J. Neurotrauma 27 2010 453 461
20. A.S. Filippidis, X. Liang, W. Wang, S. Parveen, C.M. Baumgarten, and C. Marmarou Real-time monitoring of changes in brain extracellular sodium and potassium concentrations and intracranial pressure after selective vasopressin-1a receptor (V1aR) inhibition following focal traumatic brain injury in rats J. Neurotrauma 2014 10.1089/neu.2013.3063
21. C.L. Floyd, and B.G. Lyeth Astroglia: important mediators of traumatic brain injury Prog. Brain Res. 161 2007 61 79
22. E. Girardi, A.J. Ramos, G. Vanore, and A. Brusco Astrocytic response in hippocampus and cerebral cortex in an experimental epilepsy model Neurochem. Res. 29 2004 371 377
23. Q. Guo, I. Sayeed, L.M. Baronne, S.W. Hoffman, R. Guennoun, and D.G. Stein Progesterone administration modulates AQP4 expression and edema after traumatic brain injury in male rats Exp. Neurol. 198 2006 469 478
24. N.N. Haj-Yasein, G.F. Vindedal, M. Eilert-Olsen, G.A. Gundersen, O. Skare, P. Laake, A. Klungland, A.E. Thoren, J.M. Burkhardt, O.P. Ottersen, and E.A. Nagelhus Glial-conditional deletion of aquaporin-4 (Aqp4) reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet Proc. Natl. Acad. Sci. USA 108 2011 17815 17820
25. M.E. Hamby, and M.V. Sofroniew Reactive astrocytes as therapeutic targets for CNS disorders Neurotherapeutics 7 2010 494 506
26. F. Hernando, O. Schoots, S.J. Lolait, and J.P. Burbach Immunohistochemical localization of the vasopressin V1b receptor in the rat brain and pituitary gland: anatomical support for its involvement in the central effects of vasopressin Endocrinology 142 2001 1659 1668
27. W.D. Huang, J. Pan, M. Xu, W. Su, Y.Q. Lu, Z.J. Chen, T.Y. Jiang, and Y.M. Yang Changes and effects of plasma arginine vasopressin in traumatic brain injury J. Endocrinol. Invest. 31 2008 996 1000
28. J. Ito, A. Marmarou, P. Barzo, P. Fatouros, and F. Corwin Characterization of edema by diffusion-weighted imaging in experimental traumatic brain injury J. Neurosurg. 84 1996 97 103
29. M. Kagawa, S. Nagao, and I. Bemana Arginine vasopressin receptor antagonists for treatment of vasogenic brain edema: an experimental study J. Neurotrauma 13 1996 273 279
30. I. Klatzo Pathophysiological aspects of brain edema Acta Neuropathol. 72 1987 236 239
31. A. Kleindienst, G. Brabant, N.G. Morgenthaler, K.C. Dixit, H. Parsch, and M. Buchfelder Following brain trauma, copeptin, a stable peptide derived from the AVP precusor, does not reflect osmoregulation but correlates with injury severity Acta Neurochir. 106 Suppl. 2010 S221 S224
32. A. Kleindienst, J.G. Dunbar, R. Glisson, and A. Marmarou The role of vasopressin V1A receptors in cytotoxic brain edema formation following brain injury Acta Neurochir. 155 2013 151 164
33. A. Kleindienst, G. Fazzina, A.M. Amorini, J.G. Dunbar, R. Glisson, and A. Marmarou Modulation of AQP4 expression by the protein kinase C activator, phorbol myristate acetate, decreases ischemia-induced brain edema Acta Neurochir. 96 Suppl. 2006 S393 S397
34. A. Kleindienst, G. Fazzina, J.G. Dunbar, R. Glisson, and A. Marmarou Protective effect of the V1a receptor antagonist SR49059 on brain edema formation following middle cerebral artery occlusion in the rat Acta Neurochir. 96 Suppl. 2006 S303 S306
35. R. Landgraf Central release of vasopressin: stimuli, dynamics, consequences Prog. Brain Res. 91 1992 29 39
36. J.A. Langlois, W. Rutland-Brown, and M.M. Wald The epidemiology and impact of traumatic brain injury: a brief overview J. Head Trauma Rehabil. 21 2006 375 378
37. L. Latzkovits, H.F. Cserr, J.T. Park, C.S. Patlak, K.D. Pettigrew, and A. Rimanoczy Effects of arginine vasopressin and atriopeptin on glial cell volume measured as 3-MG space Am. J. Physiol. 264 1993 C603 C608
38. X. Liu, S. Nakayama, M. Amiry-Moghaddam, O.P. Ottersen, and A. Bhardwaj Arginine-vasopressin V1 but not V2 receptor antagonism modulates infarct volume, brain water content, and aquaporin-4 expression following experimental stroke Neurocrit. Care 12 2010 124 131
39. M. Lo Pizzo, G. Schiera, I. Di Liegro, C.M. Di Liegro, J. Pal, E. Czeiter, E. Sulyok, and T. Doczi Aquaporin-4 distribution in control and stressed astrocytes in culture and in the cerebrospinal fluid of patients with traumatic brain injuries Neurol. Sci. 34 2013 1309 1314
40. A. Manaenko, N. Fathali, N.H. Khatibi, T. Lekic, Y. Hasegawa, R. Martin, J. Tang, and J.H. Zhang Arginine-vasopressin V1a receptor inhibition improves neurologic outcomes following an intracerebral hemorrhagic brain injury Neurochem. Int. 58 2011 542 548
41. A. Manaenko, N. Fathali, N.H. Khatibi, T. Lekic, K.J. Shum, R. Martin, J.H. Zhang, and J. Tang Post-treatment with SR49059 improves outcomes following an intracerebral hemorrhagic stroke in mice Acta Neurochir. 111 Suppl. 2011 S191 S196
42. G.T. Manley, M. Fujimura, T. Ma, N. Noshita, F. Filiz, A.W. Bollen, P. Chan, and A.S. Verkman Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke Nat. Med. 6 2000 159 163
43. A. Marmarou A review of progress in understanding the pathophysiology and treatment of brain edema Neurosurg. Focus 22 2007 E1
44. A. Marmarou, G. Hochwald, T. Nakamura, K. Tanaka, J. Weaver, and J. Dunbar Brain edema resolution by CSF pathways and brain vasculature in cats Am. J. Physiol. 267 1994 H514 H520
45. A. Marmarou, S. Signoretti, P.P. Fatouros, G. Portella, G.A. Aygok, and M.R. Bullock Predominance of cellular edema in traumatic brain swelling in patients with severe head injuries J. Neurosurg. 104 2006 720 730
46. F. Masson, M. Thicoipe, P. Aye, T. Mokni, P. Senjean, V. Schmitt, P.H. Dessalles, M. Cazaugade, and P. Labadens Epidemiology of severe brain injuries: a prospective population-based study J. Trauma 51 2001 481 489
47. C.J. Neal, E.Y. Lee, A. Gyorgy, J.M. Ecklund, D.V. Agoston, and G.S. Ling Effect of penetrating brain injury on aquaporin-4 expression using a rat model J. Neurotrauma 24 2007 1609 1617
48. S. Nielsen, E.A. Nagelhus, M. Amiry-Moghaddam, C. Bourque, P. Agre, and O.P. Ottersen Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain J. Neurosci. 17 1997 171 180
49. H. Niermann, M. Amiry-Moghaddam, K. Holthoff, O.W. Witte, and O.P. Ottersen A novel role of vasopressin in the brain: modulation of activity-dependent water flux in the neocortex J. Neurosci. 21 2001 3045 3051
50. K. Okuno, K. Taya, C.R. Marmarou, P. Ozisik, G. Fazzina, A. Kleindienst, S. Gulsen, and A. Marmarou 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. 102 Suppl. 2008 S431 S436
51. N.L. Ostrowski, S.J. Lolait, and W.S. Young III Cellular localization of vasopressin V1a receptor messenger ribonucleic acid in adult male rat brain, pineal, and brain vasculature Endocrinology 135 1994 1511 1528
52. C.L. Pascale, J. Szmydynger-Chodobska, J.E. Sarri, and A. Chodobski Traumatic brain injury results in a concomitant increase in neocortical expression of vasopressin and its V1a receptor J. Physiol. Pharmacol. 57 Suppl. 11 2006 S161 S167
53. G. Paxinos, and C. Watson Rat brain in Stereotaxic Coordinates 6th edition 2007 Elsevier Amsterdam
54. M.E. Raichle, and R.L. Grubb Jr. Regulation of brain water permeability by centrally-released vasopressin Brain Res. 143 1978 191 194
55. K.V. Rao, P.V. Reddy, K.M. Curtis, and M.D. Norenberg Aquaporin-4 expression in cultured astrocytes after fluid percussion injury J. Neurotrauma 28 2011 371 381
56. K. Rauen, R. Trabold, C. Brem, N.A. Terpolilli, and N. Plesnila Arginine vasopressin V1a receptor-deficient mice have reduced brain edema and secondary brain damage following traumatic brain injury J. Neurotrauma 30 2013 1442 1448
57. G.A. Rosenberg, O. Scremin, E. Estrada, and W.T. Kyner Arginine vasopressin V1-antagonist and atrial natriuretic peptide reduce hemorrhagic brain edema in rats Stroke 23 1992 1767 1773
58. G.C. Serradeil-Le, J. Wagnon, C. Garcia, C. Lacour, P. Guiraudou, B. Christophe, G. Villanova, D. Nisato, J.P. Maffrand, and F.G. Le Biochemical and pharmacological properties of SR 49059, a new, potent, nonpeptide antagonist of rat and human vasopressin V1a receptors J. Clin. Invest. 92 1993 224 231
59. A. Shuaib, W.C. Xu, T. Yang, and R. Noor Effects of nonpeptide V(1) vasopressin receptor antagonist SR-49059 on infarction volume and recovery of function in a focal embolic stroke model Stroke 33 2002 3033 3037
60. E. Solenov, H. Watanabe, G.T. Manley, and A.S. Verkman Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method Am. J. Physiol Cell Physiol. 286 2004 C426 C432
61. P.S. Sorensen, A. Gjerris, and M. Hammer Cerebrospinal fluid vasopressin in neurological and psychiatric disorders J. Neurol. Neurosurg. Psychiatry 48 1985 50 57
62. S.C. Stein, P. Georgoff, S. Meghan, K. Mizra, and S.S. Sonnad 150 years of treating severe traumatic brain injury: a systematic review of progress in mortality J. Neurotrauma 27 2010 1343 1353
63. M.C. Sun, C.R. Honey, C. Berk, N.L. Wong, and J.K. Tsui Regulation of aquaporin-4 in a traumatic brain injury model in rats J. Neurosurg. 98 2003 565 569
64. R. Suzuki, M. Okuda, J. Asai, G. Nagashima, H. Itokawa, A. Matsunaga, T. Fujimoto, and T. Suzuki Astrocytes co-express aquaporin-1, -4, and vascular endothelial growth factor in brain edema tissue associated with brain contusion Acta Neurochir. 96 Suppl. 2006 S398 S401
65. J. Szmydynger-Chodobska, I. Chung, E. Kozniewska, B. Tran, F.J. Harrington, J.A. Duncan, and A. Chodobski Increased expression of vasopressin v1a receptors after traumatic brain injury J. Neurotrauma 21 2004 1090 1102
66. J. Szmydynger-Chodobska, L.M. Fox, K.M. Lynch, B.J. Zink, and A. Chodobski Vasopressin amplifies the production of proinflammatory mediators in traumatic brain injury J. Neurotrauma 27 2010 1449 1461
67. J. Szmydynger-Chodobska, B.J. Zink, and A. Chodobski Multiple sites of vasopressin synthesis in the injured brain J. Cereb. Blood Flow Metab. 31 2011 47 51
68. P. Szot, T.L. Bale, and D.M. Dorsa Distribution of messenger RNA for the vasopressin V1a receptor in the CNS of male and female rats Brain Res. Mol. Brain Res. 24 1994 1 10
69. K. Taya, S. Gulsen, K. Okuno, R. Prieto, C.R. Marmarou, and A. Marmarou Modulation of AQP4 expression by the selective V1a receptor antagonist, SR49059, decreases trauma-induced brain edema Acta Neurochir. 102 Suppl. 2008 S425 S429
70. K. Taya, C.R. Marmarou, K. Okuno, R. Prieto, and A. Marmarou Effect of secondary insults upon aquaporin-4 water channels following experimental cortical contusion in rats J. Neurotrauma 27 2010 229 239
71. M. Thibonnier, L.N. Berti-Mattera, N. Dulin, D.M. Conarty, and R. Mattera Signal transduction pathways of the human V1-vascular, V2-renal, V3-pituitary vasopressin and oxytocin receptors Prog. Brain Res. 119 1998 147 161
72. D. Thurman, and J. Guerrero Trends in hospitalization associated with traumatic brain injury J. Am. Med. Assoc. 282 1999 954 957
73. R. Trabold, S. Krieg, K. Scholler, and N. Plesnila Role of vasopressin V(1a) and V2 receptors for the development of secondary brain damage after traumatic brain injury in mice J. Neurotrauma 25 2008 1459 1465
74. Z. Vajda, M. Pedersen, T. Doczi, E. Sulyok, H. Stodkilde-Jorgensen, J. Frokiaer, and S. Nielsen Effects of centrally administered arginine vasopressin and atrial natriuretic peptide on the development of brain edema in hyponatremic rats Neurosurgery 49 2001 697 704
75. A. Vakili, H. Kataoka, and N. Plesnila Role of arginine vasopressin V1 and V2 receptors for brain damage after transient focal cerebral ischemia J. Cereb. Blood Flow Metab. 25 2005 1012 1019
76. A.S. Verkman Aquaporins: translating bench research to human disease J. Exp. Biol. 212 2009 1707 1715
77. V.K. Vijayan, Y.L. Lee, and L.F. Eng Increase in glial fibrillary acidic protein following neural trauma Mol. Chem. Neuropathol. 13 1990 107 118
78. M. Zelenina, S. Zelenin, A.A. Bondar, H. Brismar, and A. Aperia Water permeability of aquaporin-4 is decreased by protein kinase C and dopamine Am. J. Physiol. Renal Physiol. 283 2002 F309 F318