Impact of experimental acute hyponatremia on severe traumatic brain injury in rats: Influences on injuries, permeability of blood-brain barrier, ultrastructural features, and aquaporin-4 expression

Experimental Neurology

Volumn 178, Issue 2, 2002, Pages 194-206

  Ke, Changshu ^a   Poon, Wai Sang ^a   Ng, Ho Keung ^a   Lai, Fernand M M ^a   Tang, Nelson L S ^b   Pang, Jesse C S ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Aquaporin 4; Head injury; Hyponatremia; Ultrastructure

Indexed keywords

AQUAPORIN 4; IMMUNOGLOBULIN G; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AXONAL INJURY; BLOOD BRAIN BARRIER; BRAIN CONTUSION; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN MICROCIRCULATION; CELL SWELLING; CELL ULTRASTRUCTURE; CELL VOLUME; CONTROLLED STUDY; CORPUS CALLOSUM; CORRELATION ANALYSIS; DISEASE EXACERBATION; FLUID BALANCE; HOMEOSTASIS; HYPONATREMIA; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR DOWN REGULATION;

EID: 0036935126     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.2002.8037     Document Type: Article

References (46)

1. Abou-Hamden, A., P. C. Blumbergs, G. Scott, J. Manavis, H. Wainwright, N. Jones, and J. McLean. 1997. Axonal injury in falls. J. Neurotrauma 14: 699-713.
2. Adler, S., D. Williams, and J. G. Verbalis. 1993. Effect of acute and chronic hyponatremia on blood-brain barrier function in the rat. NMR Biomed. 6: 119-124.
3. Adler, S., and V. Simplaceanu. 1989. Effect of acute hyponatremia on rat brain pH and rat brain buffering. Am. J. Physiol. 256: F113-F119.
4. Agarwala, S., and R. E. Kalil. 1998. Axotomy-induced neuronal death and reactive astrogliosis in the lateral geniculate nucleus following a lesion of the visual cortex in the rat. J. Comp. Neurol. 392: 252-263.
5. Arieff, A. I. 1987. Hyponatremia associated with permanent brain damage. Adv. Intern. Med. 32: 325-344.
6. Aruoma, O. I., B. Halliwell, B. M. Hoey, and J. Butler. 1988. The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem. J. 256: 251-255.
7. Atchison, J. W., J. Wachendorf, D. Haddock, W. J. Mysiw, M. Gribble, and J. D. Cornigan. 1993. Hyponatraemia-associated cognitive impairment in traumatic brain injury. Brain Inj. 7: 347-352.
8. Balabanov, R., H. Goldman, S. Murphy, G. Pellizon, C. Owen, J. Rafols, and P. Dore-Duffy. 2001. Endothelial cell activation following moderate traumatic brain injury. Neurol. Res. 23: 75-82.
9. Bourke, R. S., H. K. Kimelberg, L. R. Nelson, K. D. Barron, E. L. Auen, A. J. Popp, and J. B. Waldman. 1980. In Biology of Glial Swelling in Experimental Brain Edema. Advances in Neurology. Brain Edema (J. Cervós-Navarro and R. Ferszt, Eds.), Vol. 28, pp. 98-109. Raven Press, New York.
10. Bussmann, C., T. Bast, and D. Rating. 2001. Hyponatraemia in children with acute CNS disease: SIADH or cerebral salt wasting? Childs Nerv. Syst. 17: 58-62.
11. Clark, E. C., D. Thomas, J. Baer, and R. H. Sterns. 1996. Depletion of glutathione from brain cells in hyponatremia. Kidney Int. 49: 470-476.
12. Cluitmans, F. H. M., and A. E. Meinders. 1990. Management of severe hyponatremia: Rapid or slow correction? Am. J. Med. 88: 162-166.
13. Dóczi, T., J. Tarjányi, E. Huszka, and J. Kiss. 1982. Syndrome of inappropriate secretion of antidiuretic hormone (SIADH) after head injury. Neurosurgery 10: 685-688.
14. Dohanics, J., G. E. Hoffman, and J. G. Verbalis. 1996. Chronic hyponatremia reduced survival of magnocellular vasopressin and oxytocin neurons after axonal injury. J. Neurosci. 16: 2373-2380.
15. Dietrich, W. D., O. Alonso, M. Halley, and R. Busto. 1996. Delayed posttraumatic brain hyperthermia worsens outcome after fluid percussion brain injury: A light and electronmicroscopic study in rats. Neurosurgery 38: 533-541.
16. Fox, J. L., J. L. Falik, and R. J. Shaloub. 1971. Neurosurgical hyponatremia: The role of inappropriate antidiuresis. J. Neurosurg. 34: 506-514.
17. Halliwell, B. 1989. Protection against oxidants in biological systems. The superoxide theory of oxygen toxicity. In Free Radicals in Biology and Medicine, 2nd ed. (B. Halliwell, and J. M. C. Gutteridge, Eds.), pp. 86-187. Clarendon Press, London.
18. Hoshino, S., S. Kobayashi, and S. Nakazawa. 1996. Prolonged and extensive IgG immunoreactivity after severe fluid-percussion injury in rat brain. Brain Res. 711: 73-83.
19. Jiang, J. Y., B. G. Lyeth, M. Z. Kapasi, L. W. Jenkins, and J. T. Povlishock. 1992. Moderate hypothermia reduces blood-brain barrier disruption following traumatic brain injury in the rat. Acta Neuropathol. 84: 495-500.
20. Jung, J. S., R. V. Bhat, G. M. Preston, J. M. Baraban, and P. Agre. 1994. Molecular characterization of an aquaporin cDNA from brain: A candidate osmoreceptor and regulator of water balance. Proc. Natl. Acad. Sci. USA 91: 13052-13056.
21. Ke, C., W. S. Poon, H. K. Ng, J. C. S. Pang, and Y. Chan. 2001. Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats. Neurosci. Lett. 301: 21-24.
22. Ke, C., W. S. Poon, H. K. Ng, N. L. S. Tang, Y. Chan, J. Y. Wang, and J. N. K. Hsiang. 2000. The impact of acute hyponatraemia on traumatic brain injury in rats. Acta Neurochir. (Wien) 76: 405-408.
23. Kochanek, P. M., D. W. Marion, W. Zhang, and J. K. Schiding, M. White, A. Palmer, R. S. B. Clark, M. E. O'Malley, S. D. Styren, and C. Ho. 1995. Severe controlled cortical impact in rats: Assessment of cerebral edema, blood flow and contusion volume. J. Neurotrauma 12: 1015-1025.
24. Kroll, M., M. Juhler, and J. Lindholm. 1992. Hyponatraemia in acute brain disease. J. Intern. Med. 232: 291-297.
25. Lammie, G. A., I. R. Piper, D. Thomson, and F. Brannan. 1999. Neuropathologic characterization of a rodent model of closed head injury - Addition of clinically relevant secondary insults does not significantly potentiate brain damage. J. Neurotrauma 16: 603-615.
26. Manley, G. T., M. Fujimura, T. Ma, N. Noshita, F. Filiz, A. W. Bollen, P. Chan, and A. S. Verkman. 2000. Aquaporin-4 deletion in mice reduces brain edema after water intoxication and ischemic stroke. Nat. Med. 6: 159-163.
27. Marmarou, A., A. A. A. Foda, W. Van den Brink, J. Campbell, H. Kita, and K. Demetridou. 1994. A new model of diffuse brain injury in rat: Part I: Pathophysiology and biomechanics. J. Neurosurg. 80: 291-300.
28. Maxwell, W. L., J. T. Povlishock, and D. L. Graham. 1997. A mechanistic analysis of non-disruptive axonal injury: A review. J. Neurotrauma 14: 419-440.
29. Melton, J. E., and E. E. Nattie. 1983. Brain and CSF water and ions during dilutional and isomotic hyponatremia in the rat. Am. J. Physiol. 244: R724-R732.
30. Mitrofanis, J., and L. Mikuletic. 1999. Organisation of the cortical projection to the zona incerta of the thalamus. J. Comp. Neurol. 412: 173-185.
31. Nagelhus, E. A., A. Lehmann, and O. P. Ottersen. 1996. Neuronal and glial handling of glutamate and glutamine during hypoosmotic stress: A biochemical and quantitative immunocytochemical analysis using the rat cerebellum as a model. Neuroscience 72: 743-755.
32. Nagelhus, E. A., Y. Horio, A. Inanobe, A. Fujita, F. M. Huang, S. Nielsen, Y. Kurachi, and O. P. Ottersen. 1999. 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 26: 47-54.
33. Neely, J. D., B. M. Christensen, S. Nielsen, and P. Agre. 1999. Heterotrtrametic composition of aquaporin-4 water channels. Biochemistry 38: 11156-11163.
34. Nielsen, S., E. A. Nagelhus, M. Amiry-Moghaddam, C. Bourque, P. Agre, and O. P. Ottersen. 1997. Specialized membrane domains for water transport in glial cells: High-resolution immunogold cytochemistry of an aquaporins-4 in rat brain. J. Neurosci. 17: 171-180.
35. Petrov, T., and J. A. Rafols. 2001. Acute alterations of endothelin-1 and iNOS expression and control of the brain microcirculation after head trauma. Neurol. Res. 23: 139-143.
36. Pierce, J. E. S., J. Q. Troganowski, D. I. Graham, D. H. Smith, and T. K. McIntosh. 1996. Immunohistochemical characterization of alterations in the distribution of amyloid precursor proteins and β-amyloid peptide after experimental brain injury in rat. J. Neurosci. 16: 1083-1090.
37. Rojiani, A. M., J. W. Prineas, and E. S. Cho. 1994. Electrolyte-induced demyelination in rats. I. role of the blood-brain barrier and edema. Acta Neuropathol. 88: 287-292.
38. Ross, D. T., and F. F. Ebner. 1990. Thalamic retrograde degeneration following cortical injury: An excitotoxic process? Neuroscience 35: 525-550.
39. Schuh-Hofer, S. Lobsien, E. Brodowsky, J. Vogt, J. P. Dreier, R. Klee, U. Dirnagl, and U. Lindauer. 2001. The cerebrovascular response to elevated potassium - Role of nitric oxide in the in vitro model of isolated rat middle cerebral arteries. Neurosci. Lett. 306: 61-64.
40. Soupart, A., R. Penninckx, A. Stenuit, and G. Decaux. 1997. Lack of major hypoxia and significant brain damage in rats despite dramatic hyponatremic encephalopathy. J. Lab. Clin. Med. 130: 226-231.
41. Sterns, R. H., D. J. Thomas, and R. M. Herndon. 1989. Brain dehydration and neurologic deterioration after rapid correction of hyponatremia. Kidney Int. 35: 69-75.
42. Stone, J. R., S. A. Walker, and J. T. Povlishock. 1999. The visualization of a new class of traumatically injured axons through the use of a modified method of microwave antigen retrieval. Acta Neuropathol. 97: 335-345.
43. Stys, P. K. 1998. Anoxic and ischemic injury of myelinated axons in CNS white matter: From mechanistic concepts to therapeutics. J. Cereb. Blood Flow Metab. 18: 2-25.
44. Vajda, Z., D. Promeneur, T. Doczi, E. Sulyok, J. Frokiaer, O. P. Ottersen, and S. Nielsen. 2000. Increased aquaporin-4 immunoreactivity in rat brain in response to systemic hyponatremia. Biochem. Biophys. Res. Commun. 270: 495-503.
45. Verkman, A. S., and A. K. Mitra. 2000. Structure and function of aquaporin water channels. Am. J. Physiol. 278: F13-F28.
46. Vexler, Z. S., J. C. Ayus, T. P. L. Roberts, C. L. Fraser, J. Kucharczk, and A. I. Arieff. 1994. Hypoxic and ischemic hypoxia exacerbate brain injury associated with metabolic encephalopathy in laboratory animals. J. Clin. Invest. 93: 256-264.