Delayed increase of astrocytic aquaporin 4 after juvenile traumatic brain injury: Possible role in edema resolution?

Neuroscience

Volumn 222, Issue , 2012, Pages 366-378

  Fukuda, A M ^a   Pop, V ^b   Spagnoli, D ^a,b   Ashwal, S ^b   Obenaus, A ^a,b,c   Badaut, J ^a,b  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOMA LINDA UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aquaporin; Astrocyte; Edema; Juvenile traumatic brain injury

Indexed keywords

AQUAPORIN 1; AQUAPORIN 4; AQUAPORIN 9;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN EDEMA; BRAIN WATER; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; JUVENILE ANIMAL; MALE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; TRAUMATIC BRAIN INJURY; WATER FLOW; WESTERN BLOTTING;

ANIMALS; AQUAPORIN 1; AQUAPORIN 4; AQUAPORINS; ASTROCYTES; BLOTTING, WESTERN; BRAIN EDEMA; BRAIN INJURIES; GLIAL FIBRILLARY ACIDIC PROTEIN; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MALE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84865622420     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.06.033     Document Type: Article

References (64)

1. Adelson P.D., Kochanek P.M. Head injury in children. J Child Neurol 1998, 13:2-15.
2. Adelson P.D., Nemoto E., Colak A., Painter M. The use of near infrared spectroscopy (NIRS) in children after traumatic brain injury: a preliminary report. Acta Neurochir Suppl 1998, 71:250-254.
3. Ajao D, Pop V, Kamper J, Adami A, Rudobeck E, Huang L, Vlkolinsky R, Hartman R, Ashwal S, Obenaus A, Badaut J (2012) Traumatic brain injury in young rats leads to progressive behavioral deficits coincident with altered tissue properties in adulthood. J Neurotrauma [Epub ahead of print].
4. Auguste K.I., Jin S., Uchida K., Yan D., Manley G.T., Papadopoulos M.C., Verkman A.S. Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J 2007, 21:108-116.
5. Badaut J. Aquaglyceroporin 9 in brain pathologies. Neuroscience 2010, 168:1047-1057.
6. Badaut J., Ashwal S., Adami A., Tone B., Recker R., Spagnoli D., Ternon B., Obenaus A. Brain water mobility decreases after astrocytic aquaporin-4 inhibition using RNA interference. J Cereb Blood Flow Metab 2011, 31:819-831.
7. Badaut J., Ashwal S., Obenaus A. Aquaporins in cerebrovascular disease: a target for treatment of brain edema?. Cerebrovasc Dis 2011, 31:521-531.
8. Badaut J., Ashwal S., Tone B., Regli L., Tian H.R., Obenaus A. Temporal and regional evolution of aquaporin-4 expression and magnetic resonance imaging in a rat pup model of neonatal stroke. Pediatr Res 2007, 62:248-254.
9. Badaut J., Petit J.M., Brunet J.F., Magistretti P.J., Charriaut-Marlangue C., Regli L. Distribution of Aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 2004, 128:27-38.
10. Bauer R., Fritz H. Pathophysiology of traumatic injury in the developing brain: an introduction and short update. Exp Toxicol Pathol 2004, 56:65-73.
11. Bertolizio G., Bissonnette B., Mason L., Ashwal S., Hartman R., Marcantonio S., Obenaus A. Effects of hemodilution after traumatic brain injury in juvenile rats. Paediatr Anaesth 2011, 21:1198-1208.
12. Binder D.K., Yao X., Zador Z., Sick T.J., Verkman A.S., Manley G.T. Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 2006, 53:631-636.
13. Borsani E. Aquaporins in sensory and pain transmission. Curr Neuropharmacol 2010, 8:122-127.
14. Borsook D. Neurological diseases and pain. Brain 2012, 135:320-344.
15. Chastain C.A., Oyoyo U.E., Zipperman M., Joo E., Ashwal S., Shutter L.A., Tong K.A. Predicting outcomes of traumatic brain injury by imaging modality and injury distribution. J Neurotrauma 2009, 26:1183-1196.
16. Dibaj P., Kaiser M., Hirrlinger J., Kirchhoff F., Neusch C. Kir4.1 channels regulate swelling of astroglial processes in experimental spinal cord edema. J Neurochem 2007, 103:2620-2628.
17. Ding J.Y., Kreipke C.W., Speirs S.L., Schafer P., Schafer S., Rafols J.A. Hypoxia-inducible factor-1alpha signaling in aquaporin upregulation after traumatic brain injury. Neurosci Lett 2009, 453:68-72.
18. Dobbing J., Sands J. Vulnerability of developing brain not explained by cell number/cell size hypothesis. Early Hum Dev 1981, 5:227-231.
19. Faul M, Xu L, Wald MM, Coronado VG (2010) Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2002-2006. Atlanta (GA): Centers for Disease Control and Prevention, National center for Injury Prevention and Control.
20. Fenton R.A., Moeller H.B., Zelenina M., Snaebjornsson M.T., Holen T., MacAulay N. Differential water permeability and regulation of three aquaporin 4 isoforms. Cell Mol Life Sci 2010, 67:829-840.
21. Gallagher J.P., Zheng F., Hasuo H., Shinnick-Gallagher P. Activities of neurons within the rat dorsolateral septal nucleus (DLSN). Prog Neurobiol 1995, 45:373-395.
22. Gomori E., Pal J., Abraham H., Vajda Z., Sulyok E., Seress L., Doczi T. Fetal development of membrane water channel proteins aquaporin-1 and aquaporin-4 in the human brain. Int J Dev Neurosci 2006, 24:295-305.
23. 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.
24. Higashida T., Kreipke C.W., Rafols J.A., Peng C., Schafer S., Schafer P., Ding J.Y., Dornbos D., Li X., Guthikonda M., Rossi N.F., Ding Y. 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 2011, 114:92-101.
25. Hirt L., Ternon B., Price M., Mastour N., Brunet J.F., Badaut J. Protective role of early aquaporin 4 induction against post ischemic edema formation. J Cereb Blood Flow Metab 2009, 29:423-433.
26. Hsu M.S., Seldin M., Lee D.J., Seifert G., Steinhauser C., Binder D.K. Laminar-specific and developmental expression of aquaporin-4 in the mouse hippocampus. Neuroscience 2011, 178:21-32.
27. Igarashi H., Huber V.J., Tsujita M., Nakada T. Pretreatment with a novel aquaporin 4 inhibitor, TGN-020, significantly reduces ischemic cerebral edema. Neurol Sci 2011, 32:113-116.
28. Ke C., Poon W.S., Ng H.K., Pang J.C., Chan Y. Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats. Neurosci Lett 2001, 301:21-24.
29. Kiening K.L., van Landeghem F.K., Schreiber S., Thomale U.W., von Deimling A., Unterberg A.W., Stover J.F. Decreased hemispheric Aquaporin-4 is linked to evolving brain edema following controlled cortical impact injury in rats. Neurosci Lett 2002, 324:105-108.
30. Kochanek P.M. Pediatric traumatic brain injury: quo vadis?. Dev Neurosci 2006, 28:244-255.
31. Lang D.A., Teasdale G.M., Macpherson P., Lawrence A. Diffuse brain swelling after head injury: more often malignant in adults than children?. J Neurosurg 1994, 80:675-680.
32. Lee D.J., Amini M., Hamamura M.J., Hsu M.S., Seldin M.M., Nalcioglu O., Binder D.K. Aquaporin-4-dependent edema clearance following status epilepticus. Epilepsy Res 2012, 98:264-268.
33. 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.
34. Meng S., Qiao M., Lin L., Del Bigio M.R., Tomanek B., Tuor U.I. Correspondence of AQP4 expression and hypoxic-ischaemic brain oedema monitored by magnetic resonance imaging in the immature and juvenile rat. Eur J Neurosci 2004, 19:2261-2269.
35. Moftakhar P., Lynch M.D., Pomakian J.L., Vinters H.V. Aquaporin expression in the brains of patients with or without cerebral amyloid angiopathy. J Neuropathol Exp Neurol 2010, 69:1201-1209.
36. 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.
37. Nampiaparampil D.E. Prevalence of chronic pain after traumatic brain injury: A systematic review. JAMA 2008, 300:711-719.
38. Nesic O., Guest J.D., Zivadinovic D., Narayana P.A., Herrera J.J., Grill R.J., Mokkapati V.U., Gelman B.B., Lee J. Aquaporins in spinal cord injury: the janus face of aquaporin 4. Neuroscience 2010, 168:1019-1035.
39. Nesic O., Lee J., Unabia G.C., Johnson K., Ye Z., Vergara L., Hulsebosch C.E., Perez-Polo J.R. Aquaporin 1 - a novel player in spinal cord injury. J Neurochem 2008, 105:628-640.
40. Nicchia G.P., Srinivas M., Li W., Brosnan C.F., Frigeri A., Spray D.C. New possible roles for aquaporin-4 in astrocytes: cell cytoskeleton and functional relationship with connexin43. Faseb J 2005, 19:1674-1676.
41. Obenaus A., Ashwal S. Magnetic resonance imaging in cerebral ischemia: focus on neonates. Neuropharmacology 2008, 55:271-280.
42. Oliva A.A., Kang Y., Truettner J.S., Sanchez-Molano J., Furones C., Yool A.J., Atkins C.M. Fluid-percussion brain injury induces changes in aquaporin channel expression. Neuroscience 2011, 180:272-279.
43. Oshio K., Watanabe H., Yan D., Verkman A.S., Manley G.T. Impaired pain sensation in mice lacking Aquaporin-1 water channels. Biochem Biophys Res Commun 2006, 341:1022-1028.
44. Papadopoulos M.C., Saadoun S., Binder D.K., Manley G.T., Krishna S., Verkman A.S. Molecular mechanisms of brain tumor edema. Neuroscience 2004, 129:1011-1020.
45. Papadopoulos M.C., Verkman A.S. Aquaporin-4 gene disruption in mice reduces brain swelling and mortality in pneumococcal meningitis. J Biol Chem 2005, 280:13906-13912.
46. Papadopoulos M.C., Verkman A.S. Aquaporin-4 and brain edema. Pediatr Nephrol 2007, 22:778-784.
47. Pop V., Badaut J. A neurovascular perspective for long-term changes after brain trauma. Transl Stroke Res 2011, 2:533-545.
48. 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.
49. Saadoun S., Bell B.A., Verkman A.S., Papadopoulos M.C. Greatly improved neurological outcome after spinal cord compression injury in AQP4-deficient mice. Brain 2008, 131:1087-1098.
50. Saadoun S., Papadopoulos M.C., Watanabe H., Yan D., Manley G.T., Verkman A.S. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 2005, 118:5691-5698.
51. Schneier A.J., Shields B.J., Hostetler S.G., Xiang H., Smith G.A. Incidence of pediatric traumatic brain injury and associated hospital resource utilization in the United States. Pediatrics 2006, 118:483-492.
52. Singewald G.M., Rjabokon A., Singewald N., Ebner K. The modulatory role of the lateral septum on neuroendocrine and behavioral stress responses. Neuropsychopharmacology 2011, 36:793-804.
53. Skucas V.A., Mathews I.B., Yang J., Cheng Q., Treister A., Duffy A.M., Verkman A.S., Hempstead B.L., Wood M.A., Binder D.K., Scharfman H.E. Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4. J Neurosci 2011, 31:6392-6397.
54. Sun M.C., Honey C.R., Berk C., Wong N.L., Tsui J.K. Regulation of aquaporin-4 in a traumatic brain injury model in rats. J Neurosurg 2003, 98:565-569.
55. Tait M.J., Saadoun S., Bell B.A., Verkman A.S., Papadopoulos M.C. Increased brain edema in aqp4-null mice in an experimental model of subarachnoid hemorrhage. Neuroscience 2010, 167:60-67.
56. Tomura S., Nawashiro H., Otani N., Uozumi Y., Toyooka T., Ohsumi A., Shima K. Effect of decompressive craniectomy on aquaporin-4 expression after lateral fluid percussion injury in rats. J Neurotrauma 2011, 28:237-243.
57. Tourdias T., Dragonu I., Fushimi Y., Deloire M.S., Boiziau C., Brochet B., Moonen C., Petry K.G., Dousset V. Aquaporin 4 correlates with apparent diffusion coefficient and hydrocephalus severity in the rat brain: a combined MRI-histological study. Neuroimage 2009, 47:659-666.
58. Tourdias T., Mori N., Dragonu I., Cassagno N., Boiziau C., Aussudre J., Brochet B., Moonen C., Petry K.G., Dousset V. Differential aquaporin 4 expression during edema build-up and resolution phases of brain inflammation. J Neuroinflammation 2011, 8:143.
59. Tran N.D., Kim S., Vincent H.K., Rodriguez A., Hinton D.R., Bullock M.R., Young H.F. Aquaporin-1-mediated cerebral edema following traumatic brain injury: effects of acidosis and corticosteroid administration. J Neurosurg 2010, 112:1095-1104.
60. Wen H., Nagelhus E.A., Amiry-Moghaddam M., Agre P., Ottersen O.P., Nielsen S. Ontogeny of water transport in rat brain: postnatal expression of the aquaporin-4 water channel. Eur J Neurosci 1999, 11:935-945.
61. Wilcock D.M., Vitek M.P., Colton C.A. Vascular amyloid alters astrocytic water and potassium channels in mouse models and humans with Alzheimer's disease. Neuroscience 2009, 159:1055-1069.
62. Yang J., Lunde L.K., Nuntagij P., Oguchi T., Camassa L.M., Nilsson L.N., Lannfelt L., Xu Y., Amiry-Moghaddam M., Ottersen O.P., Torp R. Loss of astrocyte polarization in the tg-ArcSwe mouse model of Alzheimer's disease. J Alzheimers Dis 2011, 27:711-722.
63. Zhao J., Moore A.N., Clifton G.L., Dash P.K. Sulforaphane enhances aquaporin-4 expression and decreases cerebral edema following traumatic brain injury. J Neurosci Res 2005, 82:499-506.
64. Zheng G.Q., Li Y., Gu Y., Chen X.M., Zhou Y., Zhao S.Z., Shen J. Beyond water channel: aquaporin-4 in adult neurogenesis. Neurochem Int 2010, 56:651-654.