Brain cell volume regulation in hyponatremia: Role of sex, age, vasopressin, and hypoxia

American Journal of Physiology - Renal Physiology

Volumn 295, Issue 3, 2008, Pages

  Ayus, Juan Carlos ^a   Achinger, Steven G ^b   Arieff, Allen ^c  

^a Renal Consultants of Houston   (United States)

^b San Antonio Center for Clinical Research   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aquaporin; Astrocytes; Cerebral edema

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AQUAPORIN 4; ARGIPRESSIN; ESTROGEN; POTASSIUM ION; SODIUM ION; VASOPRESSIN; VASOPRESSIN DERIVATIVE;

ADAPTATION; AGE; ARTERIAL OXYGEN TENSION; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN CELL; BRAIN DAMAGE; BRAIN DISEASE; BRAIN EDEMA; BRAIN HYPOXIA; BRAIN PERFUSION; BRAIN SIZE; BRAIN WATER; CELL FUNCTION; CELL SWELLING; CELL VOLUME; CHILD; DISEASE ACTIVITY; DISEASE COURSE; GLIA CELL; HIGH RISK PATIENT; HORMONE ACTION; HUMAN; HYPONATREMIA; HYPONATREMIC ENCEPHALOPATHY; HYPOXEMIA; LUNG EDEMA; MOLECULAR DYNAMICS; NONHUMAN; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROGNOSIS; REGULATORY MECHANISM; RESPIRATION CENTER; RESPIRATORY FAILURE; REVIEW; RISK FACTOR; SEX; SEX DIFFERENCE; SODIUM TRANSPORT; TRANSPORT KINETICS; ANOXIA; BRAIN; CELL SIZE; ORGAN SIZE; PATHOLOGY; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; ANOXIA; BLOOD-BRAIN BARRIER; BRAIN; BRAIN EDEMA; CELL SIZE; ESTROGENS; HUMANS; HYPONATREMIA; ORGAN SIZE; SEX FACTORS; VASOPRESSINS;

EID: 54449091151     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00502.2007     Document Type: Review

References (91)

1. Abbott NJ, Ronnback L, Hanson E. Astrocyte-endothelial interactions at the blood brain barrier. Nat Rev Neurosci 7: 41-53, 2006.
2. Achinger SG, Ayus JC. Fluid and electrolytes. In: Critical Care (4th ed.), edited by Civetta D, Taylor A, Kirby JM. Philadelphia, PA: Lippincott, 2006.
3. Adler S, Simplaceanu V. Effect of acute hyponatremia on rat brain pH and rat brain buffering. Am J Physiol Renal Fluid Electrolyte Physiol 256: F113-F119, 1989.
4. Agre P, Preston GM, Smith BL. Aquaporin CHIP: the archtypical molecular water channel. Am J Physiol Renal Fluid Electrolyte Physiol 265: F463-F476, 1993.
5. Akaishi T, Sakuma Y. Estrogen-induced modulation of hypothalamic osmoregulation in female rats. Am J Physiol Regul Integr Comp Physiol 258: R924-R929, 1990.
6. Amiry-Moghaddam M, Ottersen OP. The molecular basis of water transport in the brain. Nat Rev Neurosci 12: 991-1001, 2003.
7. Ang VTY, Jenkins JS. Blood-cerebrospinal fluid barrier to arginine-vasopressin, desmopressin and desglycinamide arginine-vasopressin in the dog. J Endocrinol 93: 319-325, 1982.
8. Arieff AI. Hyponatremia, convulsions, respiratory arrest, and permanent brain damage after elective surgery in healthy women. N Engl J Med 314: 1529-1535, 1986.
9. Arieff AI. Influence of hypoxia and sex on hyponatremic encephalopathy. Am J Med 119: S59-S64, 2006.
10. Arieff AI, Ayus JC. Endometrial ablation complicated by fatal hyponatremic encephalopathy. JAMA 270: 1230-1232, 1993.
11. Arieff AI, Ayus JC, Fraser CL. Hyponatraemia and death or permanent brain damage in healthy children. Br Med J 304: 1218-1222, 1992.
12. Arieff AI, Kozniewska E, Roberts T, Vexler ZS, Ayus JC, Kucharczyk J. Age, gender, and vasopressin affect survival and brain adaptation in rats with metabolic encephalopathy. Am J Physiol Regul Integr Comp Physiol 268: R1143-R1152, 1995.
13. Arieff AI, Kronlund BA. Fatal child abuse by forced water intoxication. Pediatrics 103: 1292-1295, 1999.
14. Ayus JC, Arieff AI. Brain damage and postoperative hyponatremia: role of gender. Neurology 46: 323-328, 1996.
15. Ayus JC, Arieff AI. Chronic hyponatremic encephalopathy in postmenopausal women: association of therapies with morbidity and mortality. JAMA 281: 2299-2304, 1999.
16. Ayus JC, Arieff AI. Glycine-induced hypoosmolar hyponatremia. Arch Intern Med 157: 223-226, 1997.
17. Ayus JC, Arieff AI. Pulmonary complications of hyponatremic encephalopathy: noncardiogenic pulmonary edema and hypercapnic respiratory failure. Chest 107: 517-521, 1995.
18. Ayus JC, Armstrong DL, Arieff AI. Effects of hypernatraemia in the central nervous system and its therapy in rats and rabbits. J Physiol 492.1: 243-255, 1996.
19. Ayus JC, Armstrong DL, Arieff AI. Hyponatremia with hypoxia: effects on brain perfusion, adaptation and histology in rodents. Kidney Int 69: 1319-1325, 2006.
20. Ayus JC, Krothapalli R, Armstrong DL, Norton HJ. Symptomatic hyponatremia in rats: effect of treatment on mortality and brain lesions. Am J Physiol Renal Fluid Electrolyte Physiol 257: F18-F22, 1989.
21. Ayus JC, Krothapalli RK, Arieff AI. Treatment of symptomatic hyponatremia and its relation to brain damage. A prospective study. N Engl J Med 317: 1190-1195, 1987.
22. Ayus JC, Krothapalli RK, Armstrong DL. Rapid correction of severe hyponatremia in the rat: histopathological changes in the brain. Am J Physiol Renal Fluid Electrolyte Physiol 248: F711-F719, 1985.
23. Ayus JC, Varon J, Arieff AI. Hyponatremia, cerebral edema and noncardiogenic pulmonary edema in marathon runners. Ann Intern Med 132: 711-714, 2000.
24. Ayus JC, Wheeler JM, Arieff AI. Postoperative hyponatremic encephalopathy in menstruant women. Ann Intern Med 117: 891-897, 1992.
25. Barron W, Schreiber J, Lindheimer MD. Effect of ovarian sex steroids on osmoregulation and vasopressin secretion in the rat. Am J Physiol Endocrinol Metab 250: E352-E361, 1986.
26. Betz AL. Transport of ions across the blood-brain barrier. Fed Proc 45: 2050-2054, 1986.
27. Bradbury MWB. The structure and function of the blood-brain barrier. Fed Proc 43: 186-190, 1984.
28. Bradley EL, Etheridge MS, Arieff AI. Causes of brain damage in patients with severe symptomatic hyponatremia: analysis of 344 patients over 30 years (Abstract). J Am Soc Nephrol 16: 44A, 2005.
29. +-ATPase) and ouabain/related cardiac glycosides: a new paradigm for development of anti-breast cancer drugs? Breast Cancer Res Treat 96: 1-15, 2006.
30. Cheong JL, Cady EB, Penrice J, Wyatt JS, Cox IJ, Robertson NJ. Proton MR spectroscopy in neonates with perinatal cerebral hypoxic-ischemic injury. Am J Neuroradiol 27: 1546-1554, 2006.
31. de Pasquale M, Patlak CS, Cserr HF. Brain ion and volume regulation during acute hypernatremia in Brattleboro rats. Am J Physiol Renal Fluid Electrolyte Physiol 256: F1059-F1066, 1989.
32. Dekaban AS, Sadowsky D. Changes in brain weights during the span of human life: relation of brain weights to body heights and body weights. Ann Neurol 4: 345-356, 1978.
33. +-transporting adenosine triphosphate related to ovarian function. Brain Res 416: 113-118, 1987.
34. Ell SR. Neurogenic pulmonary edema: a review of the literature and a perspective. Invest Radiol 26: 499-506, 1991.
35. Faraci FM, Mayhan WG, Heistad DD. Effect of vasopressin on production of cerebrospinal fluid: possible role of vasopressin (V1)-receptors. Am J Physiol Regul Integr Comp Physiol 258: R94-R98, 1990.
36. Fraser CL, Arieff AI. Na-K-ATPase activity decreases with aging in female rat brain synaptosomes. Am J Physiol Renal Physiol 281: F674-F678, 2001.
37. Fraser CL, Arieff AI. Epidemiology, pathophysiology and management of hyponatremic encephalopathy. Am J Med 102: 67-77, 1997.
38. Fraser CL, Kucharczyk J, Arieff AI, Rollin C, Sarnacki P, Norman D. Sex differences result in increased morbidity from hyponatremia in female rats. Am J Physiol Regul Integr Comp Physiol 256: R880-R885, 1989.
39. +-ATPase pump function in rat brain synaptosomes is different in males and females. Am J Physiol Endocrinol Metab 257: E284-E289, 1989.
40. Fraser CL, Swanson RA. Female sex hormones inhibit volume regulation in rat brain astrocyte culture. Am J Physiol Cell Physiol 267: C909-C914, 1994.
41. Frydenlund DS, Bhardwai A, Otsuka T. Temporary loss of perivascular aquaporin-4 in neocortex after transient middle cerebral artery occlusion in mice. Proc Natl Acad Sci USA 103: 13532-13536, 2006.
42. Futo J, Shay J, Block S, Holt J, Beach M, Moss J. Estrogen and progesterone withdrawal increases cerebral vasoreactivity to serotonin in rabbit basilar artery. Life Sci 50: 1165-1172, 1992.
43. 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 24: 295-305, 2006.
44. Griggs RC, Arieff AI. Hypoxia and the central nervous system. In: Metabolic Brain Dysfunction in Systemic Disorders, edited by Griggs RC, Arieff AI. Boston, MA: Little, Brown, 1992, p. 39-54.
45. + ATPase activity in male rats. Neurosci Lett 78: 97-100, 1987.
46. Halberthal M, Halperin ML, Bohn D. Acute hyponatremia in children admitted to hospital: retrospective analysis of factors contributing to its development and resolution. Br Med J 322: 780-782, 2001.
47. Hertz L, Schousboe A. Ion and energy metabolism of the brain at the cellular level. Int Rev Neurobiol 18: 141-211, 1975.
48. Hochachka PW, Buck LT, Doll CJ, Land SC. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93: 9493-9498, 1996.
49. Hoorn EJ, Lindermans J, Zietse R. Development of severe hyponatremia in hospitalized patients: treatment-related risk factors and inadequate management. Nephrol Dial Transplant 21: 70-76, 2006.
50. Janzer RC, Raff MC. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325: 253-257, 1987.
51. Kanda F, Arieff AI. Vasopressin inhibits calcium-coupled sodium efflux system in rat brain synaptosomes. Am J Physiol Regul Integr Comp Physiol 266: R1169-R1173, 1994.
52. Keating JP, Schears GJ, Dodge PR. Oral water intoxication in infants. An American epidemic. Am J Dis Child 145: 985-990, 1991.
53. Kim JG, Son YJ, Yun CH, Kim YI, Nam-Goong IS, Park JH, Park SK, Ojeda SR, D'Elia AV, Damante G, Lee BJ. Thyroid transcription factor-1 facilitates cerebrospinal fluid formation by regulating aquaporin-1 synthesis in the brain. J Biol Chem 282: 14923-14931, 2007.
54. Kimelberg HK. Swelling and volume control in brain astroglial cells. In: Advances in Comparative and Environmental Physiology Series, edited by Gilles R. Heidelberg, Germany: Springer, 1991, p. 81-110.
55. Kozniewska E, Roberts TPL, Vexler ZS, Oseka M, Kucharczyk J, Arieff AI. Hormonal dependence of the effects of metabolic encephalopathy on cerebral perfusion and oxygen utilization in the rat. Circ Res 76: 551-558, 1995.
56. Kucharczyk J, Fraser CL, Arieff AI. Central nervous system manifestations of hyponatremia. In: Metabolic Brain Dysfunction in Systemic Disorders (1st ed.), edited by Griggs R, Arieff AI. Boston, MA: Little, Brown, 1992, p. 55-86.
57. Lang F, Busch GL, Volkl H, Haussinger D. Cell volume: a second message in regulation of cellular function. News Physiol Sci 10: 18-22, 1995.
58. Lien YH, Shapiro JI, Chan L. Effects of hypernatremia on organic brain osmoles. J Clin Invest 85: 1427-1435, 1990.
59. Lim ATW, Lolait SJ, Barlow JW, Autelitano DJ, Toh BH, Boublik J, Abrahams J, Johnston CI, Funder JW. Immunoreactive arginine-vasopressin in Brattleboro rat ovary. Nature 310: 61-64, 1984.
60. Malik AB. Mechanisms of neurogenic pulmonary edema. Circ Res 57: 1-18, 1985.
61. Melton JE, Patlak CS, Pettigrew KD, Cserr HF. Volume regulatory loss of Na, Cl, and K from rat brain during acute hyponatremia. Am J Physiol Renal Fluid Electrolyte Physiol 252: F661-F669, 1987.
62. Moritz ML, Ayus JC. The pathophysiology and treatment of hyponatremic encephalopathy: an update. Nephrol Dial Transplant 18: 2486-2491, 2003.
63. Nielsen S, Smith BL, Christensen EI, Agre P. Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc Natl Acad Sci USA 90: 7275-7279, 1993.
64. Nzerue CM, Baffoe-Bonnie H, You W, Falana B, Dai S. Predictors of outcome in hospitalized patients with severe hyponatremia. J Natl Med Assoc 95: 335-343, 2003.
65. +-adenosine triphosphatase on vascular action of vasopressin. J Clin Invest 86: 1241-1248, 1990.
66. Olson JE, Sankar R, Holtzman D, James A, Fleischhacker D. Energy-dependent volume regulation in primary cultured cerebral astrocytes. J Cell Physiol 128: 209-215, 1986.
67. Papadopoulos MC, Verkman AS. Aquaporin-4 and brain edema. Pediatr Nephrol 22: 778-784, 2007.
68. Parker JC. In defense of cell volume? Am J Physiol Cell Physiol 265: C1191-C1200, 1993.
69. Pasantes-Morales H, Lezama RA, Ramos-Mandujano G, Tuz KL. Mechanisms of cell volume regulation in hypo-osmolality. Am J Med 119: S4-S11, 2006.
70. Paulson OB, Newman EA. Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? Science 237: 896-898, 1987.
71. Rollin C, Arieff A, Fraser C, Kucharczyk J, Norman D, Sarnacki P. Gonadal steroid effects on ATP-stimulated sodium transport in pig brain synaptosomes (Abstract). Soc Neurosci Abstr 13: 22.26, 1987.
72. Rosenberg GA, Estrada E, Kyner WT. Vasopressin-induced brain edema is mediated by the V1 receptor. Adv Neurol 52: 149-154, 1990.
73. Sarfaraz D, Fraser CL. Effects of arginine vasopressin on cell volume regulation in brain astrocyte in culture. Am J Physiol Endocrinol Metab 276: E596-E601, 1999.
74. Sarrel PM, Lufkin EG, Oursler MJ, Keefe D. Estrogen actions in arteries, bone, and brain. Sci Am Sci Med 1: 44-53, 1994.
75. +-ATPase activity. Am J Physiol Gastrointest Liver Physiol 254: G687-G694, 1988.
76. Sevick RJ, Kanda F, Mintorovitch J, Arieff AI, Kucharczyk J, Tsuruda JS, Norman D, Moseley ME. Cytotoxic brain edema: assessment using diffusion-weighted MR imaging. Radiology 185: 687-690, 1992.
77. Shimojyo S, Scheinberg P, Kogure K, Reinmuth OM. The effects of graded hypoxia upon transient cerebral blood flow and oxygen consumption. Neurology 18: 127-133, 1968.
78. Simard M, Nedergaard M. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 129: 877-896, 2004.
79. Sun XL, Ding JH, Fan Y. Aquaporin 4 regulates the effects of ovarian hormones on monoamine neurotransmission. Biochem Biophys Res Commun 353: 457-462, 2007.
80. Suzuki R, Okuda M, Asai J, Nagashima G, Itokawa H, Matsunaga A, Fujimoto T, Suzuki T. Astrocytes co-express aquaporin-1, -4, and vascular endothelial growth factor in brain edema tissue associated with brain contusion. Acta Neurochir Suppl (Wien) 96: 398-401, 2006.
81. Tien R, Arieff AI, Kucharczyk W, Wasik A, Kucharczyk J. Hyponatremic encephalopathy: is central pontine myelinolysis a component? Am J Med 92: 513-522, 1992.
82. Van Bree JB, de Boer AG, Verhoef JC, Danhof M, Breimer DD. Transport of vasopressin fragments across the blood-brain barrier: in vitro studies using monolayer cultures of bovine brain endothelial cells. J Pharmacol Exp Ther 249: 901-905, 1989.
83. Verbalis JG. Hyponatremia: epidemiology, pathophysiology, therapy. Curr Opin Nephrol Hypertens 2: 636-652, 1993.
84. Verbalis JG, Gullans SR. Hyponatremia causes large sustained reductions in brain content of multiple organic osmoles in rats. Brain Res 567: 274-282, 1991.
85. Vexler ZS, Ayus JC, Roberts TPL, Kucharczyk J, Fraser CL, Arieff AI. Ischemic or hypoxic hypoxia exacerbates brain injury associated with metabolic encephalopathy in laboratory animals. J Clin Invest 93: 256-264, 1994.
86. Vexler ZS, Roberts TPL, Kucharczyk J, Arieff AI. Severe brain edema associated with cumulative effects of hyponatremic encephalopathy and ischemic hypoxia. In: Brain Edema IX, edited by Ito U, Baethmann A, Hossman KA, Kuroiwa T, Marmarou A, Reulen HJ, Takakura K. Vienna: Springer, 1994, p. 246-249.
87. Videen JS, Michaelis T, Pinto P, Ross BD. Human cerebral osmolytes during chronic hyponatremia. A proton magnetic resonance spectroscopy study. J Clin Invest 95: 788-793, 1995.
88. Vieweg WVR. Special topics in water balance in schizophrenia. In: Water Balance in Schizophrenia, edited by Schnur DB and Kirch DG. Arlington, VA: American Psychiatric Press, 1996, p. 43-52.
89. Widdowson EM, Dickerson JWT. The effect of growth and function on the chemical composition of soft tissues. Biochem J 77: 30-43, 1960.
90. Yamazaki D, Aoyama M, Ohya S. Novel function of small conductance Ca-activated K channel in enhanced cell proliferation by ATP in brain endothelial cells. J Biol Chem 281: 38430-38439, 2006.
91. Zlokovic BV, Hyman S, McComb JG, Lipovac MN, Tang G, Davson H. Kinetics of arginine-vasopressin uptake at the blood-brain barrier. Biochim Biophys Acta 1025: 191-198, 1990.