Aquaporins and blood-brain barrier permeability in early edema development after traumatic brain injury

Brain Research

Volumn 1611, Issue , 2015, Pages 18-28

  Blixt, Jonas ^a,b   Svensson, Mikael ^b   Gunnarson, Eli ^b   Wanecek, Michael ^b  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Aquaporin; Blood brain barrier; Brain edema; Brain injury; Brain trauma; Rat

Indexed keywords

AQUAPORIN 4; IMMUNOGLOBULIN G; PROTEIN ZO1; TIGHT JUNCTION PROTEIN; TJP1 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN EDEMA; CONTROLLED STUDY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE PERMEABILITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURY; COMPLICATION; METABOLISM; PATHOLOGY; PERMEABILITY; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ANIMALS; AQUAPORIN 4; BLOOD-BRAIN BARRIER; BRAIN EDEMA; BRAIN INJURIES; IMMUNOGLOBULIN G; PERMEABILITY; RATS; RATS, SPRAGUE-DAWLEY; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84929606047     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.03.004     Document Type: Article

References (64)

1. P. Agre, L.S. King, M. Yasui, W.B. Guggino, O.P. Ottersen, Y. Fujiyoshi, A. Engel, and S. Nielsen Aquaporin water channels - from atomic structure to clinical medicine J. Physiol. 542 2002 3 16
2. M. Amiry-Moghaddam, T. Otsuka, P.D. Hurn, R.J. Traystman, F.M. Haug, S.C. Froehner, M.E. Adams, J.D. Neely, P. Agre, O.P. Ottersen, and A. Bhardwaj 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. 100 2003 2106 2111
3. M. Amiry-Moghaddam, R. Xue, F.M. Haug, J.D. Neely, A. Bhardwaj, P. Agre, M.E. Adams, S.C. Froehner, S. Mori, and O.P. Ottersen Alpha-syntrophin 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 2004 542 544
4. J. Badaut, F. Lasbennes, P.J. Magistretti, and L. Regli Aquaporins in brain: distribution, physiology, and pathophysiology J. Cereb. Blood Flow Metab. 22 2002 367 378
5. P. Barzo, A. Marmarou, P. Fatouros, K. Hayasaki, and F. Corwin Contribution of vasogenic and cellular edema to traumatic brain swelling measured by diffusion-weighted imaging J. Neurosurg. 87 1997 900 907
6. B.M. Bellander, S.K. Singhrao, M. Ohlsson, P. Mattsson, and M. Svensson Complement activation in the human brain after traumatic head injury J. Neurotrauma 18 2001 1295 1311
7. T. Broman On basic aspects of the blood-brain barrier Acta Psychiatr. Neurol. Scand. 30 1955 115 124
8. E. Candelario-Jalil, Y. Yang, and G.A. Rosenberg Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia Neuroscience 158 2009 983 994
9. O.J. Castejon Electron microscopic analysis of cortical biopsies in patients with traumatic brain injuries and dysfunction of neurobehavioural system J. Submicrosc. Cytol. Pathol. 30 1998 145 156
10. A. Chodobski, B.J. Zink, and J. Szmydynger-Chodobska Blood-brain barrier pathophysiology in traumatic brain injury Transl. Stroke Res. 2 2011 492 516
11. T. Clausen, and R. Bullock Medical treatment and neuroprotection in traumatic brain injury Curr. Pharm. Des. 7 2001 1517 1532
12. 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
13. R. Diaz-Arrastia, P.M. Kochanek, P. Bergold, K. Kenney, C.E. Marx, C.J. Grimes, L.T. Loh, L.T. Adam, D. Oskvig, K.C. Curley, and 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
14. H.M. Eisenberg, H.E. Gary Jr., E.F. Aldrich, C. Saydjari, B. Turner, M.A. Foulkes, J.A. Jane, A. Marmarou, L.F. Marshall, and H.F. Young Initial CT findings in 753 patients with severe head injury. A report from the NIH Traumatic Coma Data Bank J. Neurosurg 73 1990 688 698
15. 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 theBrain Trauma Foundation guidelines for the treatment of severe traumatic brain injury J. Trauma 63 2007 1271 1278
16. D.M. Feeney, M.G. Boyeson, R.T. Linn, H.M. Murray, and W.G. Dail Responses to cortical injury: I. Methodology and local effects of contusions in the rat Brain Res. 211 1981 67 77
17. S.R. Gullans, and J.G. Verbalis Control of brain volume during hyperosmolar and hypoosmolar conditions Annu. Rev. Med. 44 1993 289 301
18. J. Hennig, A. Nauerth, and H. Friedburg RARE imaging: a fast imaging method for clinical MR Magn. Reson. Med. 3 1986 823 833
19. T. Higashida, C.W. Kreipke, J.A. Rafols, C. Peng, S. Schafer, P. Schafer, J.Y. Ding, D. Dornbos 3rd, X. Li, M. Guthikonda, N.F. Rossi, and Y. Ding The role of hypoxia-inducible factor-1alpha, aquaporin-4, and matrix metalloproteinase-9 in blood-brain barrier disruption and brain edema after traumatic brain injury J. Neurosurg. 114 2011 92 101
20. S. Holmin, T. Mathiesen, J. Shetye, and P. Biberfeld Intracerebral inflammatory response to experimental brain contusion Acta Neurochir. (Wien) 132 1995 110 119
21. S. Honeybul An update on the management of traumatic brain injury J. Neurosurg. Sci. 55 2011 343 355
22. A.M. Hudak, L. Peng, C. Marquez de la Plata, J. Thottakara, C. Moore, C. Harper, R. McColl, E. Babcock, and R. Diaz-Arrastia Cytotoxic and vasogenic cerebral oedema in traumatic brain injury: assessment with FLAIR and DWI imaging Brain Injury: [BI] 28 2014 1602 1609
23. B. Jacobs, T. Beems, T.M. van der Vliet, R.R. Diaz-Arrastia, G.F. Borm, and P.E. Vos Computed tomography and outcome in moderate and severe traumatic brain injury: hematoma volume and midline shift revisited J. Neurotrauma 28 2011 203 215
24. I.M. Jou, Y.T. Tsai, C.L. Tsai, M.H. Wu, H.Y. Chang, and N.S. Wang Simplified rat intubation using a new oropharyngeal intubation wedge J. Appl. Physiol. 89 2000 1766 1770
25. C. Ke, W.S. Poon, H.K. Ng, J.C. Pang, and Y. Chan Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats Neurosci. Lett. 301 2001 21 24
26. O. Kempski, M. Zimmer, A. Neu, F. von Rosen, M. Jansen, and A. Baethmann Control of glial cell volume in anoxia. In vitro studies on ischemic cell swelling Stroke 18 1987 623 628
27. K.L. Kiening, F.K. van Landeghem, S. Schreiber, U.W. Thomale, A. von Deimling, A.W. Unterberg, and J.F. Stover Decreased hemispheric Aquaporin-4 is linked to evolving brain edema following controlled cortical impact injury in rats Neurosci. Lett. 324 2002 105 108
28. H.K. Kimelberg Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy Glia 50 2005 389 397
29. I. Klatzo Pathophysiological aspects of brain edema Acta Neuropathol. 72 1987 236 239
30. I. Klatzo, A. Piraux, and E.J. Laskowski The relationship between edema, blood-brain-barrier and tissue elements in a local brain injury J. Neuropathol. Exp. Neurol. 17 1958 548 564
31. 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. (Wien) 155 2013 151 164
32. J. Koyama, S. Miyake, T. Sasayama, T. Kondoh, and E. Kohmura Effect of VEGF receptor antagonist (VGA1155) on brain edema in the rat cold injury model Kobe J. Med. Sci. 53 2007 199 207
33. M.F. Lythgoe, A.L. Busza, F. Calamante, C.H. Sotak, M.D. King, A.C. Bingham, S.R. Williams, and D.G. Gadian Effects of diffusion anisotropy on lesion delineation in a rat model of cerebral ischemia Magn. Reson. Med. 38 1997 662 668
34. 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
35. K.S. Mark, and T.P. Davis Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation Am. J. Physiol. Hear. Circ. Physiol. 282 2002 H1485 H1494
36. N. Marklund, A. Bakshi, D.J. Castelbuono, V. Conte, and T.K. McIntosh Evaluation of pharmacological treatment strategies in traumatic brain injury Curr. Pharm. Des. 12 2006 1645 1680
37. A. Marmarou A review of progress in understanding the pathophysiology and treatment of brain edema Neurosurg. Focus 22 2007 E1
38. 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
39. F. Masson, M. Thicoipe, P. Aye, T. Mokni, P. Senjean, V. Schmitt, P.H. Dessalles, M. Cazaugade, P. Labadens Aquitaine Group for Severe Brain Injuries S Epidemiology of severe brain injuries: a prospective population-based study J. Trauma 51 2001 481 489
40. E.A. Nagelhus, and O.P. Ottersen Physiological roles of aquaporin-4 in brain Physiol. Rev. 93 2013 1543 1562
41. 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
42. 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
43. A.A. Oliva Jr., Y. Kang, J.S. Truettner, J. Sanchez-Molano, C. Furones, A.J. Yool, and C.M. Atkins Fluid-percussion brain injury induces changes in aquaporin channel expression Neuroscience 180 2011 272 279
44. M.C. Papadopoulos, G.T. Manley, S. Krishna, and A.S. Verkman Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema FASEB J. 18 2004 1291 1293
45. M.C. Papadopoulos, and A.S. Verkman Aquaporin-4 gene disruption in mice reduces brain swelling and mortality in pneumococcal meningitis J. Biol. Chem. 280 2005 13906 13912
46. M.C. Papadopoulos, and A.S. Verkman Aquaporin-4 and brain edema Pediatr. Nephrol. 22 2007 778 784
47. K.V. Rama Rao, and M.D. Norenberg Aquaporin-4 in hepatic encephalopathy Metab. Brain Dis. 22 2007 265 275
48. 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
49. M. Reinert, B. Hoelper, E. Doppenberg, A. Zauner, and R. Bullock Substrate delivery and ionic balance disturbance after severe human head injury Acta Neurochir. Suppl. 76 2000 439 444
50. Z. Ren, J.J. Iliff, L. Yang, J. Yang, X. Chen, M.J. Chen, R.N. Giese, B. Wang, X. Shi, and M. Nedergaard 'Hit & Run' model of closed-skull traumatic brain injury (TBI) reveals complex patterns of post-traumatic AQP4 dysregulation J. Cereb. Blood Flow Metab. 33 2013 834 845
51. D. Shlosberg, M. Benifla, D. Kaufer, and A. Friedman Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury Nat. Rev. Neurol. 6 2010 393 403
52. S. Signoretti, A. Marmarou, B. Tavazzi, G. Lazzarino, A. Beaumont, and R. Vagnozzi N-acetylaspartate reduction as a measure of injury severity and mitochondrial dysfunction following diffuse traumatic brain injury J. Neurotrauma 18 2001 977 991
53. 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
54. J. Sword, T. Masuda, D. Croom, and S.A. Kirov Evolution of neuronal and astroglial disruption in the peri-contusional cortex of mice revealed by in vivo two-photon imaging Brain 136 2013 1446 1461
55. F. Tagliaferri, C. Compagnone, M. Korsic, F. Servadei, and J. Kraus A systematic review of brain injury epidemiology in Europe Acta Neurochir. (Wien) 148 2006 255 268 (discussion 268)
56. H. Tanno, R.P. Nockels, L.H. Pitts, and L.J. Noble Breakdown of the blood-brain barrier after fluid percussive brain injury in the rat. Part 1: Distribution and time course of protein extravasation J. Neurotrauma 9 1992 21 32
57. 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
58. T. Tourdias, N. Mori, I. Dragonu, N. Cassagno, C. Boiziau, J. Aussudre, B. Brochet, C. Moonen, K.G. Petry, and V. Dousset Differential aquaporin 4 expression during edema build-up and resolution phases of brain inflammation J. Neuroinflamm. 8 2011 143
59. K. Umeda, J. Ikenouchi, S. Katahira-Tayama, K. Furuse, H. Sasaki, M. Nakayama, T. Matsui, S. Tsukita, M. Furuse, and S. Tsukita ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation Cell 126 2006 741 754
60. A.W. Unterberg, J. Stover, B. Kress, and K.L. Kiening Edema and brain trauma Neuroscience 129 2004 1021 1029
61. Z. Vajda, M. Pedersen, E.M. Fuchtbauer, K. Wertz, H. Stodkilde-Jorgensen, E. Sulyok, T. Doczi, J.D. Neely, P. Agre, J. Frokiaer, and S. Nielsen Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice Proc. Natl. Acad. Sci. U. S. A. 99 2002 13131 13136
62. H.P. Van Putten, M.G. Bouwhuis, J.P. Muizelaar, B.G. Lyeth, and R.F. Berman Diffusion-weighted imaging of edema following traumatic brain injury in rats: effects of secondary hypoxia J. Neurotrauma 22 2005 857 872
63. K.K. Wang, S.F. Larner, G. Robinson, and R.L. Hayes Neuroprotection targets after traumatic brain injury Curr. Opin. Neurol. 19 2006 514 519
64. J. Wen, S. Qian, Q. Yang, L. Deng, Y. Mo, and Y. Yu Overexpression of netrin-1 increases the expression of tight junction-associated proteins, claudin-5, occludin, and ZO-1, following traumatic brain injury in rats Exp. Ther. Med. 8 2014 881 886