Activation of cerebral sodium-glucose transporter type 1 function mediated by post-ischemic hyperglycemia exacerbates the development of cerebral ischemia

Neuroscience

Volumn 310, Issue , 2015, Pages 674-685

  Yamazaki, Y ^a   Ogihara, S ^a   Harada, S ^a   Tokuyama, S ^a  

^a KOBE GAKUIN UNIVERSITY   (Japan)

Author keywords

5' adenosine monophosphate activated protein kinase; Cerebral ischemia; Glucose transporter; Hyperglycemia; Sodium glucose transporter type 1

Indexed keywords

GLUCOSE; HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NEURON SPECIFIC NUCLEAR PROTEIN; SODIUM GLUCOSE COTRANSPORTER 1; SLC5A1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE EXACERBATION; ENZYME ACTIVATION; ENZYME MECHANISM; FEMALE; FETUS; HYPERGLYCEMIA; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION; ANIMAL; ASTROCYTE; BRAIN; CEREBRAL ARTERY DISEASE; METABOLISM; NERVE CELL;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ASTROCYTES; BRAIN; BRAIN ISCHEMIA; HYPERGLYCEMIA; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE; NEURONS; SODIUM-GLUCOSE TRANSPORTER 1;

EID: 84944718007     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.10.005     Document Type: Article

References (68)

1. Banerjee S.K., Wang D.W., Alzamora R., Huang X.N., Pastor-Soler N.M., Hallows K.R., McGaffin K.R., Ahmad F. SGLT1, a novel cardiac glucose transporter, mediates increased glucose uptake in PRKAG2 cardiomyopathy. J Mol Cell Cardiol 2010, 49:683-692.
2. Barcelona S., Menegaz D., Díez-Sampedro A. Mouse SGLT3a generates proton-activated currents but does not transport sugar. Am J Physiol Cell Physiol 2012, 302:1073-1082.
3. Bruno A., Liebeskind D., Hao Q., Raychev R. Diabetes mellitus, acute hyperglycemia, and ischemic stroke. Curr Treat Options Neurol 2010, 12:492-503.
4. Burdakov D., Luckman S.M., Verkhratsky A. Glucose-sensing neurons of the hypothalamus. Philos Trans R Soc Lond B Biol Sci 2005, 360:2227-2235.
5. 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 2001, 32:2426-2432.
6. Chen J., Guo Y., Cheng W., Chen R., Liu T., Chen Z., Tan S. High glucose induces apoptosis and suppresses proliferation of adult rat neural stem cells following in vitro ischemia. BMC Neurosci 2013, 14:24.
7. Chen J.-H., Kuo H.-C., Lee K.-F., Tsai T.-H. Global proteomic analysis of brain tissues in transient ischemia brain damage in rats. Int J Mol Sci 2015, 16:11873-11891.
8. Costa G.N., Vindeirinho J., Cavadas C., Ambrósio A.F., Santos P.F. Contribution of TNF receptor 1 to retinal neural cell death induced by elevated glucose. Mol Cell Neurosci 2012, 50:113-123.
9. + affinity and transport stoichiometry in mouse sodium/glucose cotransporter type 3B. J Biol Chem 2011, 286:7975-7982.
10. Diez-Sampedro A., Hirayama B.A., Osswald C., Gorboulev V., Baumgarten K., Volk C., Wright E.M., Koepsell H. A glucose sensor hiding in a family of transporters. Proc Natl Acad Sci U S A 2003, 100:11753-11758.
11. Ding S. Dynamic reactive astrocytes after focal ischemia. Neural Regen Res 2014, 9:2048-2052.
12. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 1999, 22:391-397.
13. 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 2010, 41:203-209.
14. Dreier J.P. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011, 17:439-447.
15. 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 2015, 49:118-125.
16. 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 2015, 10.1093/cercor/bhv054.
17. 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 2012, 35:624-628.
18. 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 2006, 13:174-180.
19. Grell A.-S., Thigarajah R., Edvinsson L., Samraj A.K. Regulatory mechanism of endothelin receptor B in the cerebral arteries after focal cerebral ischemia. PLoS ONE 2014, 9:e113624.
20. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., Turk B.E., Shaw R.J. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 2008, 30:214-226.
21. Hahn S.S., Tang Q., Zheng F., Zhao S., Wu J., Chen J. Repression of integrin-linked kinase by antidiabetes drugs through cross-talk of PPARγ- and AMPKα-dependent signaling: role of AP-2α and Sp1. Cell Signal 2014, 26:639-647.
22. Haley T.J., Mccormick W.G. Pharmacological effects produced by intracerebral injection of drugs in the conscious mouse. Br J Pharmacol Chemother 1957, 12:12-15.
23. 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 2009, 1279:174-181.
24. 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 2010, 1351:254-263.
25. Harada S., Fujita-Hamabe W., Tokuyama S. Effect of orexin-A on post-ischemic glucose intolerance and neuronal damage. J Pharmacol Sci 2011, 115:155-163.
26. 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 2013, 1541:61-68.
27. 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 2013, 344:276-285.
28. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 2007, 8:774-785.
29. He Huang, Kang R., Zhao Z. Hepatitis C virus infection and risk of stroke: a systematic review and meta-analysis. PLoS One 2013, 8:e81305.
30. Hertz L., Xu J., Chen Y., Gibbs M.E., Du T. Antagonists of the vasopressin V1 receptor and of the β(1)-adrenoceptor inhibit cytotoxic brain edema in stroke by effects on astrocytes - but the mechanisms Differ. Curr Neuropharmacol 2014, 12:308-323.
31. Jiang M., Li J., Peng Q., Liu Y., Liu W., Luo C., Peng J., Li J., Yung K.K.L., Mo Z. Neuroprotective effects of bilobalide on cerebral ischemia and reperfusion injury are associated with inhibition of pro-inflammatory mediator production and down-regulation of JNK1/2 and p38 MAPK activation. J Neuroinflammation 2014, 11:167.
32. Kiss K., Baghy K., Spisák S., Szanyi S., Tulassay Z., Zalatnai A., Löhr J.-M., Jesenofsky R., Kovalszky I., Firneisz G. Chronic hyperglycemia induces trans-differentiation of human pancreatic stellate cells and enhances the malignant molecular communication with human pancreatic cancer cells. PLoS ONE 2015, 10:e0128059.
33. Krajewska M., Xu L., Xu W., Krajewski S., Kress C.L., Cui J., Yang L., Irie F., Yamaguchi Y., Lipton S.A., Reed J.C. Endoplasmic reticulum protein BI-1 modulates unfolded protein response signaling and protects against stroke and traumatic brain injury. Brain Res 2011, 1370:227-237.
34. Krimi R.B., Letteron P., Chedid P., Nazaret C., Ducroc R., Marie J.-C. Resistin-like molecule-beta inhibits SGLT-1 activity and enhances GLUT2-dependent jejunal glucose transport. Diabetes 2009, 58:2032-2038.
35. LeComte M.D., Shimada I.S., Sherwin C., Spees J.L. Notch1-STAT3-ETBR signaling axis controls reactive astrocyte proliferation after brain injury. Proc Natl Acad Sci U S A 2015, 112:8726-8731.
36. Lee M., Bikram M., Oh S., Bull D.A., Kim S.W. Sp1-dependent regulation of the RTP801 promoter and its application to hypoxia-inducible VEGF plasmid for ischemic disease. Pharm Res 2004, 21:736-741.
37. Lee J., Kosaras B., Aleyasin H., Han J.A., Park D.S., Ratan R.R., Kowall N.W., Ferrante R.J., Lee S.W., Ryu H. Role of cyclooxygenase-2 induction by transcription factor Sp1 and Sp3 in neuronal oxidative and DNA damage response. FASEB J 2006, 20:2375-2377.
38. Lee Y.J., Suh H.N., Han H.J. Effect of BSA-induced ER stress on SGLT protein expression levels and alpha-MG uptake in renal proximal tubule cells. Am J Physiol Renal Physiol 2009, 296:1405-1416.
39. Li J., McCullough L.D. Effects of AMP-activated protein kinase in cerebral ischemia. J Cereb Blood Flow Metab 2010, 30:480-492.
40. Li J., Zeng Z., Viollet B., Ronnett G.V., McCullough L.D. Neuroprotective effects of adenosine monophosphate-activated protein kinase inhibition and gene deletion in stroke. Stroke 2007, 38:2992-2999.
41. +-coupled cotransporters GAT1 and SGLT1. J Biol Chem 2000, 275:37414-37422.
42. Malatiali S., Francis I., Barac-Nieto M. Phlorizin prevents glomerular hyperfiltration but not hypertrophy in diabetic rats. Exp Diabetes Res 2008, 305403.
43. +-glucose cotransporter gene, SGLT1, by HNF-1 and Sp1. Am J Physiol Gastrointest Liver Physiol 2000, 278:591-603.
44. +-dependent and phlorizin-inhibitable transport of glucose and cycasin in brain endothelial cells. J Neurochem 1998, 70:772-777.
45. McDonald J.W., Althomsons S.P., Hyrc K.L., Choi D.W., Goldberg M.P. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat Med 1998, 4:291-297.
46. Miki N., Ikuta M., Matsui T. Hypoxia-induced activation of the retinoic acid receptor-related orphan receptor alpha4 gene by an interaction between hypoxia-inducible factor-1 and Sp1. J Biol Chem 2004, 279:15025-15031.
47. Morikawa E., Mori H., Kiyama Y., Mishina M., Asano T., Kirino T. Attenuation of focal ischemic brain injury in mice deficient in the epsilon1 (NR2A) subunit of NMDA receptor. J Neurosci 1998, 18:9727-9732.
48. Nicholls D.G. Mitochondrial calcium function and dysfunction in the central nervous system. Biochim Biophys Acta 2009, 1787:1416-1424.
49. O'Malley D., Reimann F., Simpson A.K., Gribble F.M. Sodium-coupled glucose cotransporters contribute to hypothalamic glucose sensing. Diabetes 2006, 55:3381-3386.
50. +-D-glucose cotransporter SGLT1 in neurons. J Neurochem 1997, 69:84-94.
51. Ryu H., Lee J., Zaman K., Kubilis J., Ferrante R.J., Ross B.D., Neve R., Ratan R.R. Sp1 and Sp3 are oxidative stress-inducible, antideath transcription factors in cortical neurons. J Neurosci 2003, 23:3597-3606.
52. Saito I. Epidemiological evidence of type 2 diabetes mellitus, metabolic syndrome, and cardiovascular disease in Japan. Circ J 2012, 76:1066-1073.
53. Scheepers A., Joost H.-G., Schürmann A. The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. JPEN J Parenter Enteral Nutr 2004, 28:364-371.
54. Serra-Pérez A., Verdaguer E., Planas A.M., Santalucía T. Glucose promotes caspase-dependent delayed cell death after a transient episode of oxygen and glucose deprivation in SH-SY5Y cells. J Neurochem 2008, 106:1237-1247.
55. Siniscalchi A., Gallelli L., Malferrari G., Pirritano D., Serra R., Santangelo E., De Sarro G. Cerebral stroke injury: the role of cytokines and brain inflammation. J Basic Clin Physiol Pharmacol 2014, 25:131-137.
56. +-coupled glucose carrier SGLT1 by AMP-activated protein kinase. Mol Membr Biol 2010, 27:137-144.
57. Stöllberger C., Exner I., Finsterer J., Slany J., Steger C. Stroke in diabetic and non-diabetic patients: course and prognostic value of admission serum glucose. Ann Med 2005, 37:357-364.
58. Takano T., Oberheim N., Cotrina M.L., Nedergaard M. Astrocytes and ischemic injury. Stroke 2009, 40:8-12.
59. Wong J.K., Chen L., Huang Y., Sehba F.A., Friedel R.H., Zou H. Attenuation of cerebral ischemic injury in Smad1 deficient mice. PLoS ONE 2015, 10:e0136967.
60. Wright E.M., Turk E. The sodium/glucose cotransport family SLC5. Pflugers Arch 2004, 447:510-518.
61. Wright E.M., Loo D.D.F., Hirayama B.A. Biology of human sodium glucose transporters. Physiol Rev 2011, 91:733-794.
62. Xu C., Bailly-Maitre B., Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005, 115:2656-2664.
63. 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 2012, 1489:113-120.
64. Yamazaki Y., Harada S., Tokuyama S. Sodium-glucose transporter type 3-mediated neuroprotective effect of acetylcholine suppresses the development of cerebral ischemic neuronal damage. Neuroscience 2014, 269:134-142.
65. Yamazaki Y., Harada S., Tokuyama S. Relationship between cerebral sodium-glucose transporter and hyperglycemia in cerebral ischemia. Neurosci Lett 2015, 604:134-139.
66. Yeh S.H., Yang W.Bin, Gean P.W., Hsu C.Y., Tseng J.T., Su T.P., Chang W.C., Hung J.J. Translational and transcriptional control of Sp1 against ischaemia through a hydrogen peroxide-activated internal ribosomal entry site pathway. Nucleic Acids Res 2011, 39:5412-5423.
67. +-glucose cotransporter SGLT1 from humans and rabbit. J Physiol 2001, 531:631-644.
68. 2+ overload and calpain activation in neurons. Oxid Med Cell Longev 2013, 367206.