Simulated diabetic ketoacidosis therapy in vitro elicits brain cell swelling via sodium-hydrogen exchange and anion transport

American Journal of Physiology - Endocrinology and Metabolism

Volumn 309, Issue 4, 2015, Pages E370-E379

  Rose, Keeley L ^a,b   Watson, Andrew J ^a,b   Drysdale, Thomas A ^a,b   Cepinskas, Gediminas ^c   Chan, Melissa ^b   Fraser, Douglas D ^a,b,c,d  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

^c Centre for Critical Illness Research   (Canada)

^d Translational Research Centre   (Canada)

Author keywords

Anion transport; Cell swelling; Children; Diabetic ketoacidosis; Sodium hydrogen exchangers; Treatment

Indexed keywords

ALLOXAN; AMILORIDE DERIVATIVE; CARIPORIDE; INSULIN; SODIUM PROTON EXCHANGE PROTEIN 1; STREPTOZOCIN; ANION; SODIUM PROTON EXCHANGE PROTEIN;

ALKALINIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANION TRANSPORT; ARTICLE; BRAIN CELL; BRAIN SLICE; BRAIN WATER; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; DIABETIC KETOACIDOSIS; GENOTYPE; IN VITRO STUDY; IN VIVO STUDY; JUVENILE; MOUSE; NONHUMAN; OSMOLALITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REHYDRATION; WATER CONTENT; ADVERSE EFFECTS; ANIMAL; BRAIN; BRAIN EDEMA; COMPLICATION; EXPERIMENTAL DIABETES MELLITUS; FLUID THERAPY; INSULIN DEPENDENT DIABETES MELLITUS; ION TRANSPORT; METABOLISM; ORGAN CULTURE TECHNIQUE; OSMOLARITY; PATHOLOGY; PHYSIOLOGY;

ALLOXAN; ANIMALS; ANIONS; BRAIN; BRAIN EDEMA; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC KETOACIDOSIS; FLUID THERAPY; INSULIN; ION TRANSPORT; MICE; ORGAN CULTURE TECHNIQUES; OSMOLAR CONCENTRATION; SODIUM-HYDROGEN ANTIPORTER; STREPTOZOCIN;

EID: 84939445870     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00107.2015     Document Type: Article

References (56)

1. Aitken PG, Fayuk D, Somjen GG, Turner DA. Use of intrinsic optical signals to monitor physiological changes in brain tissue slices. Methods 18: 91–103, 1999.
2. Alexander RT, Grinstein S. Na+/H+ exchangers and the regulation of volume. Acta Physiol (Oxf) 187: 159–167, 2006.
3. Andrew RD, Jarvis CR, Obeidat AS. Potential sources of intrinsic optical signals imaged in live brain slices. Methods 18: 185–196, 179, 1999.
4. Andrew RD, Labron MW, Boehnke SE, Carnduff L, Kirov SA. Physiological evidence that pyramidal neurons lack functional water channels. Cereb Cortex 17: 787–802, 2007.
5. Andrew RD, Lobinowich ME, Osehobo EP. Evidence against volume regulation by cortical brain cells during acute osmotic stress. Exp Neurol 143: 300–312, 1997.
6. Attaphitaya S, Park K, Melvin JE. Molecular cloning and functional expression of a rat Na+/H+exchanger (NHE5) highly expressed in brain. J Biol Chem 274: 4383–4388, 1999.
7. Baird NR, Orlowski J, Szabo EZ, Zaun HC, Schultheis PJ, Menon AG, Shull GE. Molecular cloning, genomic organization, and functional expression of Na+/H+ exchanger isoform 5 (NHE5) from human brain. J Biol Chem 274: 4377–4382, 1999.
8. Banks WA, Jaspan JB, Kastin AJ. Effect of diabetes mellitus on the permeability of the blood-brain barrier to insulin. Peptides 18: 1577–1584, 1997.
9. Bello FA, Sotos JF. Cerebral oedema in diabetic ketoacidosis in children. Lancet 336: 64, 1990.
10. Bonnet U, Leniger T, Wiemann M. Alteration of intracellular pH and activity of CA3-pyramidal cells in guinea pig hippocampal slices by inhibition of transmembrane acid extrusion. Brain Res 872: 116–124, 2000.
11. Bookstein C, Musch MW, DePaoli A, Xie Y, Rabenau K, Villereal M, Rao MC, Chang EB. Characterization of the rat Na+/H+ exchanger isoform NHE4 and localization in rat hippocampus. Am J Physiol Cell Physiol 271: C1629–C1638, 1996.
12. Cala PM, Maldonado HM. pH regulatory Na/H exchange by Amphiuma red blood cells. J Gen Physiol 103: 1035–1053, 1994.
13. Cameron FJ, Kean MJ, Wellard RM, Werther GA, Neil JJ, Inder TE. Insights into the acute cerebral metabolic changes associated with childhood diabetes. Diabet Med 22: 648–653, 2005.
14. Chatzigeorgiou A, Halapas A, Kalafatakis K, Kamper E. The use of animal models in the study of diabetes mellitus. In Vivo 23: 245–258, 2009.
15. Chesler M. Regulation and modulation of pH in the brain. Physiol Rev 83: 1183–1221, 2003.
16. Close TE, Cepinskas G, Omatsu T, Rose KL, Summers K, Patterson EK, Fraser DD. Diabetic ketoacidosis elicits systemic inflammation associated with cerebrovascular endothelial cell dysfunction. Microcirculation 20: 534–543, 2013.
17. Cox GA, Lutz CM, Yang CL, Biemesderfer D, Bronson RT, Fu A, Aronson PS, Noebels JL, Frankel WN. Sodium/hydrogen exchanger gene defect in slow-wave epilepsy mutant mice. Cell 91: 139–148, 1997.
18. Davies ML, Kirov SA, Andrew RD. Whole isolated neocortical and hippocampal preparations and their use in imaging studies. J Neurosci Methods 166: 203–216, 2007.
19. Dunger DB, Sperling MA, Acerini CL, Bohn DJ, Daneman D, Danne TP, Glaser NS, Hanas R, Hintz RL, Levitsky LL, Savage MO, Tasker RC, Wolfsdorf JI. ESPE/LWPES consensus statement on diabetic ketoacidosis in children and adolescents. Arch Dis Child 89: 188–194, 2004.
20. Edge JA. Cerebral oedema during treatment of diabetic ketoacidosis: are we any nearer finding a cause? Diabetes Metab Res Rev 16: 316–324, 2000.
21. Edge JA, Jakes RW, Roy Y, Hawkins M, Winter D, Ford-Adams ME, Murphy NP, Bergomi A, Widmer B, Dunger DB. The UK case-control study of cerebral oedema complicating diabetic ketoacidosis in children. Diabetologia 49: 2002–2009, 2006.
22. Ferimer HN, Kutina KL, LaManna JC. Methyl isobutyl amiloride delays normalization of brain intracellular pH after cardiac arrest in rats. Crit Care Med 23: 1106–1111, 1995.
23. Figueroa RE, Hoffman WH, Momin Z, Pancholy A, Passmore GG, Allison J. Study of subclinical cerebral edema in diabetic ketoacidosis by magnetic resonance imaging T2 relaxometry and apparent diffusion coefficient maps. Endocr Res 31: 345–355, 2005.
24. Fischer U, Lougheed WD, Albisser AM. In vivo bicarbonate deficiency and insulin dissolution. ASAIO Trans 35: 26–29, 1989.
25. Fliegel L, Murtazina R, Dibrov P, Harris C, Moor A, Fernandez- Rachubinski FA. Regulation and characterization of the Na+/H+ exchanger. Biochem Cell Biol 76: 735–741, 1998.
26. Frelin C, Barbry P, Vigne P, Chassande O, Cragoe EJ Jr, Lazdunski M. Amiloride and its analogs as tools to inhibit Na− transport via the Na+ channel, the Na+/H+ antiport and the Na+/Ca2+ exchanger. Biochimie 70: 1285–1290, 1988.
27. Glaser N, Barnett P, McCaslin I, Nelson D, Trainor J, Louie J, Kaufman F, Quayle K, Roback M, Malley R, Kuppermann N; Pediatric Emergency Medicine Collaborative Research Committee of the American Academy of Pediatrics. Risk factors for cerebral edema in children with diabetic ketoacidosis. The Pediatric Emergency Medicine Collaborative Research Committee of the American Academy of Pediatrics. N Engl J Med 344: 264–269, 2001.
28. Glaser N, Yuen N, Anderson SE, Tancredi DJ, O’Donnell ME. Cerebral metabolic alterations in rats with diabetic ketoacidosis: effects of treatment with insulin and intravenous fluids and effects of bumetanide. Diabetes 59: 702–709, 2010.
29. Glaser NS, Wootton-Gorges SL, Marcin JP, Buonocore MH, Dicarlo J, Neely EK, Barnes P, Bottomly J, Kuppermann N. Mechanism of cerebral edema in children with diabetic ketoacidosis. J Pediatr 145: 164–171, 2004.
30. Hoffmann EK, Dunham PB. Membrane mechanisms and intracellular signalling in cell volume regulation. Int Rev Cytol 161: 173–262, 1995.
31. Jarvis CR, Lilge L, Vipond GJ, Andrew RD. Interpretation of intrinsic optical signals and calcein fluorescence during acute excitotoxic insult in the hippocampal slice. Neuroimage 10: 357–372, 1999.
32. Kim J, Jung YS, Han W, Kim MY, Namkung W, Lee BH, Yi KY, Yoo SE, Lee MG, Kim KH. Pharmacodynamic characteristics and cardioprotective effects of new NHE1 inhibitors. Eur J Pharmacol 567: 131–138, 2007.
33. Koves IH, Russo VC, Higgins S, Mishra A, Pitt J, Cameron FJ, Werther GA. An in vitro paradigm for diabetic cerebral oedema and its therapy: a critical role for taurine and water channels. Neurochem Res 37: 182–192, 2012.
34. Lam TI, Anderson SE, Glaser N, O’Donnell ME. Bumetanide reduces cerebral edema formation in rats with diabetic ketoacidosis. Diabetes 54: 510–516, 2005.
35. Lang F. Mechanisms and significance of cell volume regulation. J Am Coll Nutr 26: 613S–623S, 2007.
36. Lang F, Busch GL, Volkl H. The diversity of volume regulatory mechanisms. Cell Physiol Biochem 8: 1–45, 1998.
37. Lawrence SE, Cummings EA, Gaboury I, Daneman D. Populationbased study of incidence and risk factors for cerebral edema in pediatric diabetic ketoacidosis. J Pediatr 146: 688–692, 2005.
38. Ma E, Haddad GG. Expression and localization of Na+/H+exchangers in rat central nervous system. Neuroscience 79: 591–603, 1997.
39. MacVicar BA, Hochman D. Imaging of synaptically evoked intrinsic optical signals in hippocampal slices. J Neurosci 11: 1458–1469, 1991.
40. Malo ME, Fliegel L. Physiological role and regulation of the Na+/H+ exchanger. Can J Physiol Pharmacol 84: 1081–1095, 2006.
41. Masereel B, Pochet L, Laeckmann D. An overview of inhibitors of Na(+)/H(+) exchanger. Eur J Med Chem 38: 547–554, 2003.
42. McIntyre AK, Porter R. Studies in Neurophysiology: Presented to A. K. McIntyre. Cambridge, UK, and New York: Cambridge University, 1978.
43. Nase G, Helm PJ, Enger R, Ottersen OP. Water entry into astrocytes during brain edema formation. Glia 56: 895–902, 2008.
44. Ohman JL Jr, Marliss EB, Aoki TT, Munichoodappa CS, Khanna VV, Kozak GP. The cerebrospinal fluid in diabetic ketoacidosis. N Engl J Med 284: 283–290, 1971.
45. Omatsu T, Cepinskas G, Clarson C, Patterson EK, Alharfi IM, Summers K, Couraud PO, Romero IA, Weksler B, Fraser DD. CXCL1/CXCL8 (GRα/IL-8) in human diabetic ketoacidosis plasma facilitates leukocyte recruitment to cerebrovascular endothelium in vitro. Am J Physiol Endocrinol Metab 306: E1077–E1084, 2014.
46. Pedersen SF, O’Donnell ME, Anderson SE, Cala PM. Physiology and pathophysiology of Na+/H+ exchange and Na+-K+-2Cl+ cotransport in the heart, brain, and blood. Am J Physiol Regul Integr Comp Physiol 291: R1–R25, 2006.
47. Rieder CV, Fliegel L. Transcriptional regulation of Na+/H+ exchanger expression in the intact mouse. Mol Cell Biochem 243: 87–95, 2003.
48. Risher WC, Andrew RD, Kirov SA. Real-time passive volume responses of astrocytes to acute osmotic and ischemic stress in cortical slices and in vivo revealed by two-photon microscopy. Glia 57: 207–221, 2009.
49. Rose KL, Pin CL, Wang R, Fraser DD. Combined insulin and bicarbonate therapy elicits cerebral edema in a juvenile mouse model of diabetic ketoacidosis. Pediatr Res 61: 301–306, 2007.
50. Sauvage M, Maziere P, Fathallah H, Giraud F. Insulin stimulates NHE1 activity by sequential activation of phosphatidylinositol 3-kinase and protein kinase C zeta in human erythrocytes. Eur J Biochem 267: 955–962, 2000.
51. Van der Meulen JA, Klip A, Grinstein S. Possible mechanism for cerebral oedema in diabetic ketoacidosis. Lancet 2: 306–308, 1987.
52. Ventura R, Harris KM. Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897–6906, 1999.
53. Williams B, Howard RL. Glucose-induced changes in Na+/H+ antiport activity and gene expression in cultured vascular smooth muscle cells. Role of protein kinase. C J Clin Invest 93: 2623–2631, 1994.
54. Wolfsdorf J, Craig ME, Daneman D, Dunger D, Edge J, Lee WR, Rosenbloom A, Sperling MA, Hanas R; International Society for Pediatric and Adolescent Diabetes. Diabetic ketoacidosis. Pediatr Diabetes 8: 28–43, 2007.
55. Wootton-Gorges SL, Buonocore MH, Kuppermann N, Marcin J, Dicarlo J, Neely EK, Barnes PD, Glaser N. Detection of cerebral {beta}-hydroxy butyrate, acetoacetate, and lactate on proton MR spectroscopy in children with diabetic ketoacidosis. AJNR Am J Neuroradiol 26: 1286–1291, 2005.
56. Xue J, Douglas RM, Zhou D, Lim JY, Boron WF, Haddad GG. Expression of Na+/H+ and HCO3+ -dependent transporters in Na+/H+ exchanger isoform 1 null mutant mouse brain. Neuroscience 122: 37–46, 2003.