Sodium influx through cerebral sodium-glucose transporter type 1 exacerbates the development of cerebral ischemic neuronal damage

European Journal of Pharmacology

Volumn 799, Issue , 2017, Pages 103-110

  Yamazaki, Yui ^a   Harada, Shinichi ^a   Wada, Tetsuyuki ^b   Hagiwara, Teruki ^b   Yoshida, Shigeru ^b   Tokuyama, Shogo ^a  

^a KOBE GAKUIN UNIVERSITY   (Japan)

^b KINKI UNIVERSITY   (Japan)

Author keywords

Cerebral ischemia; Hyperglycemia; Neuronal damage; Sodium glucose transporter

Indexed keywords

ALPHA METHYL GLUCOPYRANOSIDE; GLUCOPYRANOSIDE; GLUCOSE; SMALL INTERFERING RNA; SODIUM GLUCOSE COTRANSPORTER 1; UNCLASSIFIED DRUG; METHYLGLUCOSIDE; SLC5A1 PROTEIN, MOUSE; SLC5A4B PROTEIN, MOUSE; SODIUM; SODIUM GLUCOSE COTRANSPORTER;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOASSAY; BRAIN CELL; BRAIN INFARCTION; BRAIN ISCHEMIA; CONTROLLED STUDY; DISEASE EXACERBATION; FEMALE; FLUORESCENCE ANALYSIS; GLUCOSE BLOOD LEVEL; HUMAN; IN VIVO STUDY; MALE; NERVE CELL CULTURE; NERVE CELL LESION; NONHUMAN; PROTEIN EXPRESSION; SODIUM CELL LEVEL; SODIUM TRANSPORT; SURVIVAL RATE; ANIMAL; BRAIN; CELL SURVIVAL; COMPLICATION; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HYPERGLYCEMIA; INTRACELLULAR SPACE; METABOLISM; MOUSE; NERVE CELL; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BRAIN; BRAIN ISCHEMIA; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HYPERGLYCEMIA; INTRACELLULAR SPACE; MALE; METHYLGLUCOSIDES; MICE; NEURONS; RNA, SMALL INTERFERING; SODIUM; SODIUM-GLUCOSE TRANSPORT PROTEINS; SODIUM-GLUCOSE TRANSPORTER 1;

EID: 85011977766     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2017.02.007     Document Type: Article

References (47)

1. Capes, S.E., Hunt, D., Malmberg, K., Pathak, P., Gerstein, H.C., Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: a systematic overview. Stroke 32 (2001), 2426–2432.
2. Cuomo, O., Vinciguerra, A., Cerullo, P., Anzilotti, S., Brancaccio, P., Bilo, L., Scorziello, A., Molinaro, P., Di Renzo, G., Pignataro, G., Ionic homeostasis in brain conditioning. Front. Neurosci., 9, 2015, 277.
3. Doi, Y., Ninomiya, T., Hata, J., Fukuhara, M., Yonemoto, K., Iwase, M., Iida, M., Kiyohara, Y., Impact of glucose tolerance status on development of ischemic stroke and coronary heart disease in a general Japanese population: the Hisayama study. Stroke 41 (2010), 203–209.
4. Dreier, J.P., The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat. Med. 17 (2011), 439–447.
5. Drenckhahn, C., Koch, S.P., Dümmler, J., Kohl-Bareis, M., Steinbrink, J., Dreier, J.P., A validation study of the use of near-infrared spectroscopy imaging in primary and secondary motor areas of the human brain. Epilepsy Behav. 49 (2015), 118–125.
6. Elgendy, I.Y., Mahmoud, A.N., Mansoor, H., Mojadidi, M.K., Bavry, A.A., Evolution of acute ischemic stroke therapy from lysis to thrombectomy: similar or different to acute myocardial infarction?. Int. J. Cardiol. 222 (2016), 441–447.
7. Enger, R., Tang, W., Vindedal, G.F., Jensen, V., Johannes Helm, P., Sprengel, R., Looger, L.L., Nagelhus, E.A., Dynamics of ionic shifts in cortical spreading depression. Cereb. Cortex 25 (2015), 4469–4476.
8. Fujita-Hamabe, W., Tokuyama, S., The involvement of cleavage of neural cell adhesion molecule in neuronal death under oxidative stress conditions in cultured cortical neurons. Biol. Pharm. Bull. 35 (2012), 624–628.
9. Gentile, N.T., Seftchick, M.W., Huynh, T., Kruus, L.K., Gaughan, J., Decreased mortality by normalizing blood glucose after acute ischemic stroke. Acad. Emerg. Med. 13 (2006), 174–180.
10. Gonzàlez, J.A., Reimann, F., Burdakov, D., Dissociation between sensing and metabolism of glucose in sugar sensing neurones. J. Physiol. 587 (2009), 41–48.
11. Gribble, F.M., Williams, L., Simpson, A.K., Reimann, F., A novel glucose-sensing mechanism contributing to glucagon-like peptide-1 secretion from the GLUTag cell line. Diabetes 52 (2003), 1147–1154.
12. Haley, T.J., McCormick, W.G., Pharmacological effects produced by intracerebral injection of drugs in the conscious mouse. Br. J. Pharmacol. Chemother. 12 (1957), 12–15.
13. Harada, S., Fujita, W.H., Shichi, K., Tokuyama, S., The development of glucose intolerance after focal cerebral ischemia participates in subsequent neuronal damage. Brain Res. 1279 (2009), 174–181.
14. Harada, S., Fujita-Hamabe, W., Tokuyama, S., The importance of regulation of blood glucose levels through activation of peripheral 5′-AMP-activated protein kinase on ischemic neuronal damage. Brain Res. 1351 (2010), 254–263.
15. Harada, S., Fujita-Hamabe, W., Tokuyama, S., Effect of orexin-A on post-ischemic glucose intolerance and neuronal damage. J. Pharmacol. Sci. 115 (2011), 155–163.
16. Harada, S., Fujita-Hamabe, W., Tokuyama, S., Ameliorating effect of hypothalamic brain-derived neurotrophic factor against impaired glucose metabolism after cerebral ischemic stress in mice. J. Pharmacol. Sci. 118 (2012), 109–116.
17. Harada, S., Yamazaki, Y., Nishioka, H., Tokuyama, S., Neuroprotective effect through the cerebral sodium-glucose transporter on the development of ischemic damage in global ischemia. Brain Res. 1541 (2013), 61–68.
18. Harada, S., Yamazaki, Y., Tokuyama, S., Orexin-A suppresses postischemic glucose intolerance and neuronal damage through hypothalamic brain-derived neurotrophic factor. J. Pharmacol. Exp. Ther. 344 (2013), 276–285.
19. Matsuoka, T., Nishizaki, T., Kisby, G.E., Na+-dependent and phlorizin-inhibitable transport of glucose and cycasin in brain endothelial cells. J. Neurochem. 70 (1998), 772–777.
20. Matz, K., Keresztes, K., Tatschl, C., Nowotny, M., Dachenhausen, A., Dachenhausenm, A., Brainin, M., Tuomilehto, J., Disorders of glucose metabolism in acute stroke patients: an underrecognized problem. Diabetes Care 29 (2006), 792–797.
21. Murphy, T.H., Li, P., Betts, K., Liu, R., Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J. Neurosci. 28 (2008), 1756–1772.
22. Nicholls, D.G., Mitochondrial calcium function and dysfunction in the central nervous system. Biochim. Biophys. Acta 1787 (2009), 1416–1424.
23. O'Malley, D., Reimann, F., Simpson, A.K., Gribble, F.M., Sodium-coupled glucose cotransporters contribute to hypothalamic glucose sensing. Diabetes 55 (2006), 3381–3386.
24. Oláh, G., Herédi, J., Menyhárt, A., Czinege, Z., Nagy, D., Fuzik, J., Kocsis, K., Knapp, L., Krucsó, E., Gellért, L., Kis, Z., Farkas, T., Fülöp, F., Párdutz, A., Tajti, J., Vécsei, L., Toldi, J., Unexpected effects of peripherally administered kynurenic acid on cortical spreading depression and related blood-brain barrier permeability. Drug Des. Dev. Ther. 7 (2013), 981–987.
25. Olsson, T., Viitanen, M., Asplund, K., Eriksson, S., Hägg, E., Prognosis after stroke in diabetic patients. A controlled prospective study. Diabetologia 33 (1990), 244–249.
26. Orrenius, S., Zhivotovsky, B., Nicotera, P., Regulation of cell death: the calcium-apoptosis link. Nat. Rev. Mol. Cell Biol. 4 (2003), 552–565.
27. Pivovarova, N.B., Stanika, R.I., Kazanina, G., Villanueva, I., Andrews, S.B., The interactive roles of zinc and calcium in mitochondrial dysfunction and neurodegeneration. J. Neurochem. 128 (2014), 592–602.
28. Poppe, R., Karbach, U., Gambaryan, S., Wiesinger, H., Lutzenburg, M., Kraemer, M., Witte, O.W., Koepsell, H., Expression of the Na+-D-glucose cotransporter SGLT1 in neurons. J. Neurochem. 69 (1997), 84–94.
29. Rizk, N.N., Rafols, J.A., Dunbar, J.C., Cerebral ischemia-induced apoptosis and necrosis in normal and diabetic rats: effects of insulin and C-peptide. Brain Res. 1096 (2006), 204–212.
30. Sabino-Silva, R., Mori, R.C., David-Silva, A., Okamoto, M.M., Freitas, H.S., Machado, U.F., The Na+/glucose cotransporters: from genes to therapy. Braz. J. Med. Biol. Res. 43 (2010), 1019–1026.
31. Sarwar, N., Gao, P., Seshasai, S.R.K., Gobin, R., Kaptoge, S., Di Angelantonio, E., Ingelsson, E., Lawlor, D.A., Selvin, E., Stampfer, M., Stehouwer, C.D.A., Lewington, S., Pennells, L., Thompson, A., Sattar, N., White, I.R., Ray, K.K., Danesh, J., Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet 375 (2010), 2215–2222.
32. Scheepers, A., Joost, H.-G., Schürmann, A., The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. JPEN J. Parenter. Enter. Nutr. 28 (2004), 364–371.
33. Shichi, K., Fujita-Hamabe, W., Harada, S., Mizoguchi, H., Yamada, K., Nabeshima, T., Tokuyama, S., Involvement of matrix metalloproteinase-mediated proteolysis of neural cell adhesion molecule in the development of cerebral ischemic neuronal damage. J. Pharmacol. Exp. Ther. 338 (2011), 701–710.
34. Somjen, G.G., Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81 (2001), 1065–1096.
35. Soria, F.N., Pérez-Samartín, A., Martin, A., Gona, K.B., Llop, J., Szczupak, B., Chara, J.C., Matute, C., Domercq, M., Extrasynaptic glutamate release through cystine/glutamate antiporter contributes to ischemic damage. J. Clin. Investig. 124 (2014), 3645–3655.
36. Strong, A.J., Anderson, P.J., Watts, H.R., Virley, D.J., Lloyd, A., Irving, E.A., Nagafuji, T., Ninomiya, M., Nakamura, H., Dunn, A.K., Graf, R., Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex. Brain 130 (2007), 995–1008.
37. Takeda, Y., Zhao, L., Jacewicz, M., Pulsinelli, W.A., Nowak, T.S., Metabolic and perfusion responses to recurrent peri-infarct depolarization during focal ischemia in the Spontaneously Hypertensive Rat: dominant contribution of sporadic CBF decrements to infarct expansion. J. Cereb. Blood Flow. Metab. 31 (2011), 1863–1873.
38. Vijayan, M., Reddy, P.H., Peripheral biomarkers of stroke: focus on circulatory microRNAs. Biochim. Biophys. Acta 1862 (2016), 1984–1993.
39. Wang, X., Ma, Z., Fu, Z., Gao, S., Yang, L., Jin, Y., Sun, H., Wang, C., Fan, W., Chen, L., Zheng, Q.-Y., Bi, G., Ma, C.-L., Hydroxysafflor yellow a protects neurons from excitotoxic death through Inhibition of NMDARs. ASN Neuro, 8, 2016, 10.1177/1759091416642345.
40. Wright, E.M., Loo, D.D.F., Hirayama, B.A., Biology of human sodium glucose transporters. Physiol. Rev. 91 (2011), 733–794.
41. Wright, E.M., Turk, E., The sodium/glucose cotransport family SLC5. Pflug. Arch. 447 (2004), 510–518.
42. Xie, Y., Chen, S., Wu, Y., Murphy, T.H., Prolonged deficits in parvalbumin neuron stimulation-evoked network activity despite recovery of dendritic structure and excitability in the somatosensory cortex following global ischemia in mice. J. Neurosci. 34 (2014), 14890–14900.
43. Yamazaki, Y., Harada, S., Tokuyama, S., Post-ischemic hyperglycemia exacerbates the development of cerebral ischemic neuronal damage through the cerebral sodium-glucose transporter. Brain Res. 1489 (2012), 113–120.
44. Yamazaki, Y., Harada, S., Tokuyama, S., Relationship between cerebral sodium-glucose transporter and hyperglycemia in cerebral ischemia. Neurosci. Lett. 604 (2015), 134–139.
45. Yamazaki, Y., Harada, S., Wada, T., Yoshida, S., Tokuyama, S., Sodium transport through the cerebral sodium-glucose transporter exacerbates neuron damage during cerebral ischaemia. J. Pharm. Pharmacol. 68 (2016), 922–931.
46. Yamazaki, Y., Ogihara, S., Harada, S., Tokuyama, S., Activation of cerebral sodium-glucose transporter type 1 function mediated by post-ischemic hyperglycemia exacerbates the development of cerebral ischemia. Neuroscience 310 (2015), 674–685.
47. Zheng, L.-S., Ishii, Y., Zhao, Q.-L., Kondo, T., Sasahara, M., PDGF suppresses oxidative stress induced Ca2+ overload and calpain activation in neurons. Oxid. Med. Cell. Longev., 2013, 2013, 367206.