Type 1 diabetes alters astrocytic properties related with neurotransmitter supply, causing abnormal neuronal activities

Brain Research

Volumn 1602, Issue C, 2015, Pages 32-43

  Son, Hyeonwi ^a   Jung, Soonwoong ^a   Kim, Jun Young ^b   Goo, Young Min ^b   Cho, Kye Man ^a   Lee, Dong Hoon ^a   Roh, Gu Seob ^a   Kang, Sang Soo ^a   Cho, Gyeong Jae ^a   Choi, Wan Sung ^a   Kim, Hyun Joon ^a  

^a Gyeongsang National University   (South Korea)

^b Gyeongnam Oriental Medicinal Herb Institute   (South Korea)

Author keywords

Astrocyte; Glu Gln cycle; Glutamate; Glutamine; Glutamine synthetase; Type 1 diabetes

Indexed keywords

4 AMINOBUTYRIC ACID; ADENYLATE KINASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; GLUTAMATE AMMONIA LIGASE; GLUTAMIC ACID; GLUTAMINE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; STREPTOZOCIN; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NERVE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN REGION; CONTROLLED STUDY; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PRIMARY CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CELL CULTURE; EXPERIMENTAL DIABETES MELLITUS; IMMUNOHISTOCHEMISTRY; METABOLISM; WESTERN BLOTTING;

ANIMALIA;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; GAMMA-AMINOBUTYRIC ACID; GLUCOSE; GLUTAMATE-AMMONIA LIGASE; GLUTAMIC ACID; GLUTAMINE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; PREFRONTAL CORTEX; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES;

EID: 84928019817     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.12.055     Document Type: Article

References (63)

1. Ajilore, O., Haroon, E., Kumaran, S., Darwin, C., Binesh, N., Mintz, J., Miller, J., Thomas, M.A., Kumar, A., 2007. Measurement of brain metabolites in patients with type 2 diabetes and major depression using proton magnetic resonance spectroscopy. Neuropsychopharmacology 32, 1224-1231.
2. Barreto, G., White, R.E., Ouyang, Y., Xu, L., Giffard, R.G., 2011. Astrocytes: targets for neuroprotection in stroke. Cent. Nerv. Syst. Agents Med. Chem 11, 164-173.
3. Beauquis, J., Roig, P., Homo-Delarche, F., De Nicola, A., Saravia, F., 2006. Reduced hippocampal neurogenesis and number of hilar neurones in streptozotocin-induced diabetic mice: reversion by antidepressant treatment. Eur. J. Neurosci. 23, 1539-1546.
4. Belanger, M., Allaman, I., Magistretti, P.J., 2011. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14, 724-738.
5. Bobermin, L.D., Quincozes-Santos, A., Guerra, M.C., Leite, M.C., Souza, D.O., Goncalves, C.A., Gottfried, C., 2012. Resveratrol prevents ammonia toxicity in astroglial cells. PLoS One 7, e52164.
6. Boyd-Kimball, D., Sultana, R., Poon, H.F., Lynn, B.C., Casamenti, F., Pepeu, G., Klein, J.B., Butterfield, D.A., 2005. Proteomic identification of proteins specifically oxidized by intracerebral injection of amyloid beta-peptide (1-42) into rat brain: implications for Alzheimer's disease. Neuroscience 132, 313-324.
7. Brosnan, C.F., Raine, C.S., 2013. The astrocyte in multiple sclerosis revisited. Glia 61, 453-465.
8. Butterfield, D.A., Poon St, H.F., Clair, D., Keller, J.N., Pierce, W.M., Klein, J.B., Markesbery, W.R., 2006. Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer's disease. Neurobiol. Dis. 22, 223-232.
9. Castegna, A., Aksenov, M., Aksenova, M., Thongboonkerd, V., Klein, J.B., Pierce, W.M., Booze, R., Markesbery, W.R., Butterfield, D.A., 2002. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic. Biol. Med. 33, 562-571.
10. Castegna, A., Palmieri, L., Spera, I., Porcelli, V., Palmieri, F., Fabis-Pedrini, M.J., Kean, R.B., Barkhouse, D.A., Curtis, M.T., Hooper, D.C., 2011. Oxidative stress and reduced glutamine synthetase activity in the absence of inflammation in the cortex of mice with experimental allergic encephalomyelitis. Neuroscience 185, 97-105.
11. Ceriello, A., Ihnat, M.A., 2010. 'Glycaemic variability': a new therapeutic challenge in diabetes and the critical care setting. Diabet. Med 27, 862-867.
12. Chan, O., Cheng, H., Herzog, R., Czyzyk, D., Zhu, W., Wang, A., McCrimmon, R.J., Seashore, M.R., Sherwin, R.S., 2008. Increased GABAergic tone in the ventromedial hypothalamus contributes to suppression of counterregulatory responses after antecedent hypoglycemia. Diabetes 57, 1363-1370.
13. Chiang, C.Y., Sessle, B.J., Dostrovsky, J.O., 2012. Role of astrocytes in pain. Neurochem. Res. 37, 2419-2431.
14. Coleman, E., Judd, R., Hoe, L., Dennis, J., Posner, P., 2004. Effects of diabetes mellitus on astrocyte GFAP and glutamate transporters in the CNS. Glia 48, 166-178.
15. Coleman, E.S., Dennis, J.C., Braden, T.D., Judd, R.L., Posner, P., 2010. Insulin treatment prevents diabetes-induced alterations in astrocyte glutamate uptake and GFAP content in rats at 4 and 8 weeks of diabetes duration. Brain Res. 1306, 131-141.
16. Coulter, D.A., Eid, T., 2012. Astrocytic regulation of glutamate homeostasis in epilepsy. Glia 60, 1215-1226.
17. dos Santos, A.Q., Nardin, P., Funchal, C., de Almeida, L.M., Jacques-Silva,M.C., Wofchuk, S.T., Goncalves, C.A., Gottfried, C., 2006. Resveratrol increases glutamate uptake and glutamine synthetase activity in C6 glioma cells. Arch. Biochem. Biophys. 453, 161-167.
18. Eid, T., Tu, N., Lee, T.S., Lai, J.C., 2013. Regulation of astrocyte glutamine synthetase in epilepsy. Neurochem. Int. 63, 670-681.
19. Fiechter, G., Pavelescu, D., Mayer, H.K., 2012. UPLC analysis of free amino acids in wines: profiling of on-lees aged wines. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci 879, 1361-1366.
20. Furman, J.L., Sama, D.M., Gant, J.C., Beckett, T.L., Murphy, M.P., Bachstetter, A.D., Van Eldik, L.J., Norris, C.M., 2012. Targeting astrocytes ameliorates neurologic changes in a mouse model of Alzheimer's disease. J. Neurosci. 32, 16129-16140.
21. Gandhi, G.K., Ball, K.K., Cruz, N.F., Dienel, G.A., 2010. Hyperglycaemia and diabetes impair gap junctional communication among astrocytes. ASN Neuro 2, e00030.
22. Garcia-Espinosa, M.A., Rodrigues, T.B., Sierra, A., Benito, M., Fonseca, C., Gray, H.L., Bartnik, B.L., Garcia-Martin, M.L., Ballesteros, P., Cerdan, S., 2004. Cerebral glucose metabolism and the glutamine cycle as detected by in vivo and in vitro 13 C NMR spectroscopy. Neurochem. Int. 45, 297-303.
23. Gawronski, J.D., Benson, D.R., 2004. Microtiter assay for glutamine synthetase biosynthetic activity using inorganic phosphate detection. Anal. Biochem. 327, 114-118.
24. Gispen,W.H., Biessels, G.J., 2000. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci. 23, 542-549.
25. Gruetter, R., Ugurbil, K., Seaquist, E.R., 1998. Steady-state cerebral glucose concentrations and transport in the human brain. J. Neurochem. 70, 397-408.
26. Hardie, D.G., 2011. Sensing of energy and nutrients by AMP-activated protein kinase. Am. J. Clin. Nutr. 93, 891S-896S.
27. Hertz, L., Gibbs, M.E., O'Dowd, B.S., Sedman, G.L., Robinson, S.R., Sykova, E., Hajek, I., Hertz, E., Peng, L., Huang, R., Ng, K.T., 1996. Astrocyte-neuron interaction during one-trial aversive learning in the neonate chick. Neurosci. Biobehav. Rev. 20, 537-551.
28. Hertz, L., Zielke, H.R., 2004. Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci. 27, 735-743.
29. Hughes, E.G., Maguire, J.L., McMinn, M.T., Scholz, R.E., Sutherland, M.L., 2004. Loss of glial fibrillary acidic protein results in decreased glutamate transport and inhibition of PKA-induced EAAT2 cell surface trafficking. Brain Res. Mol. Brain Res. 124, 114-123.
30. Jeon, B.T., Jeong, E.A., Shin, H.J., Lee, Y., Lee, D.H., Kim, H.J., Kang, S.S., Cho, G.J., Choi,W.S., Roh, G.S., 2012. Resveratrol attenuates obesity-associated peripheral and central inflammation and improves memory deficit in mice fed a high-fat diet. Diabetes 61, 1444-1454.
31. Kim, G., Lee, Y., Jeong, E.Y., Jung, S., Son, H., Lee, D.H., Roh, G.S., Kang, S.S., Cho, G.J., Choi, W.S., Kim, H.J., 2010a. Acute stress responsive RGS proteins in the mouse brain. Mol. Cells. 30, 161-165.
32. B receptor associates with regulators of G-protein signaling 4 protein in the mouse prefrontal cortex and hypothalamus. BMB Rep. 47, 324-329.
33. Kim, Y.H., Kim, Y.S., Kang, S.S., Cho, G.J., Choi, W.S., 2010b. Resveratrol inhibits neuronal apoptosis and elevated Ca2+/calmodulin-dependent protein kinase II activity in diabetic mouse retina. Diabetes 59, 1825-1835.
34. Kosenko, E., Llansola, M., Montoliu, C., Monfort, P., Rodrigo, R., Hernandez-Viadel, M., Erceg, S., Sanchez-Perez, A.M., Felipo, V., 2003. Glutamine synthetase activity and glutamine content in brain: modulation by NMDA receptors and nitric oxide. Neurochem. Int. 43, 493-499.
35. Lee, Y., Son, H., Kim, G., Kim, S., Lee, D.H., Roh, G.S., Kang, S.S., Cho, G.J., Choi, W.S., Kim, H.J., 2013. Glutamine deficiency in the prefrontal cortex increases depressive-like behaviours in male mice. J. Psychiatry Neurosci. 37, 120024.
36. Lee, Y.J., Han, S.B., Nam, S.Y., Oh, K.W., Hong, J.T., 2010. Inflammation and Alzheimer's disease. Arch. Pharm. Res 33, 1539-1556.
37. Lieth, E., Barber, A.J., Xu, B., Dice, C., Ratz, M.J., Tanase, D., Strother, J.M., 1998. Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Penn state retina research group. Diabetes 47, 815-820.
38. Lyoo, I.K.,Yoon, S.J.,Musen,G., Simonson,D.C., Weinger, K., Bolo,N., Ryan, C.M., Kim, J.E., Renshaw, P.F., Jacobson, A.M., 2009. Altered prefrontal glutamate-glutamine-gamma-aminobutyric acid levels and relation to low cognitive performance and depressive symptoms in type 1 diabetes mellitus. Arch. Gen. Psychiatry 66, 878-887.
39. Mastrocola, R., Restivo, F., Vercellinatto, I., Danni, O., Brignardello, E., Aragno, M., Boccuzzi, G., 2005. Oxidative and nitrosative stress in brain mitochondria of diabetic rats. J. Endocrinol. 187, 37-44.
40. Matyash, V., Kettenmann, H., 2010. Heterogeneity in astrocyte morphology and physiology. Brain Res. Rev. 63, 2-10.
41. McCarthy, K.D., de Vellis, J., 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902.
42. Miguel-Hidalgo, J.J., Waltzer, R., Whittom, A.A., Austin, M.C., Rajkowska, G., Stockmeier, C.A., 2010. Glial and glutamatergic markers in depression, alcoholism, and their comorbidity. J. Affect Disord. 127, 230-240.
43. Nardin, P., Tramontina, F., Leite, M.C., Tramontina, A.C., Quincozes-Santos, A., de Almeida, L.M., Battastini, A.M., Gottfried, C., Goncalves, C.A., 2007. S100B content and secretion decrease in astrocytes cultured in high-glucose medium. Neurochem. Int. 50, 774-782.
44. Nedergaard, M., Dirnagl, U., 2005. Role of glial cells in cerebral ischemia. Glia 50, 281-286.
45. Nissim, I., 1999. Newer aspects of glutamine/glutamate metabolism: the role of acute pH changes. Am. J. Physiol. 277, F493-F497.
46. Parpura, V., Heneka, M.T., Montana, V., Oliet, S.H., Schousboe, A., Haydon, P.G., Stout Jr., R.F., Spray, D.C., Reichenbach, A., Pannicke, T., Pekny, M., Pekna, M., Zorec, R., Verkhratsky, A., 2012. Glial cells in (patho)physiology. J. Neurochem. 121, 4-27.
47. Qu, J., Chen, W., Luo, G.,Wang, Y., Xiao, S., Ling, Z., Chen, G., 2002. Rapid determination of underivatized pyroglutamic acid, glutamic acid, glutamine and other relevant amino acids in fermentation media by LC-MS-MS. Analyst 127, 66-69.
48. Reagan, L.P., Magarinos, A.M., Lucas, L.R., van Bueren, A.,McCall, A.L., McEwen, B.S., 1999. Regulation of GLUT-3 glucose transporter in the hippocampus of diabetic rats subjected to stress. Am. J. Physiol. 276, E879-E886.
49. Reagan, L.P., 2012. Diabetes as a chronic metabolic stressor: Causes, consequences and clinical complications. Exp. Neurol. 233, 68-78.
50. Robinson, S.R., 2001. Changes in the cellular distribution of glutamine synthetase in Alzheimer's disease. J. Neurosci. Res. 66, 972-980.
51. Rodriguez, J.J., Olabarria, M., Chvatal, A., Verkhratsky, A., 2009. Astroglia in dementia and Alzheimer's disease. Cell Death Differ. 16, 378-385.
52. Sanacora, G., Treccani, G., Popoli, M., 2012. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 62, 63-77.
53. Sanacora, G., Banasr, M., 2013. From pathophysiology to novel antidepressant drugs: glial contributions to the pathology and treatment of mood disorders. Biol. Psychiatry 73, 1172-1179.
54. Schousboe, A., Bak, L.K., Waagepetersen, H.S., 2013. Astrocytic control of biosynthesis and turnover of the neurotransmitters glutamate and GABA. Front Endocrinol (Lausanne) 4, 102.
55. Sibson, N.R., Dhankhar, A., Mason, G.F., Rothman, D.L., Behar, K.L., Shulman, R.G., 1998. Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc. Natl. Acad. Sci. USA 95, 316-321.
56. Swamy, M., Yusof, W.R., Sirajudeen, K.N., Mustapha, Z., Govindasamy, C., 2011. Decreased glutamine synthetase, increased citrulline-nitric oxide cycle activities, and oxidative stress in different regions of brain in epilepsy rat model. J. Physiol. Biochem. 67, 105-113.
57. Swanson, R.A., Ying, W., Kauppinen, T.M., 2004. Astrocyte influences on ischemic neuronal death. Curr. Mol. Med. 4, 193-205.
58. Takahashi, S., Izawa, Y., Suzuki, N., 2012. Astroglial pentose phosphate pathway rates in response to high-glucose environments. ASN Neuro. 4, e00078.
59. Vardimon, L., 2000. Neuroprotection by glutamine synthetase. Isr. Med. Assoc. J 2 (Suppl), 46-51.
60. Verrotti, A., Scaparrotta, A., Olivieri, C., Chiarelli, F., 2012. Mechanisms in endocrinology: seizures and type 1 diabetes mellitus: current state of knowledge. Eur. J. Endocrinol. 167, 749-758.
61. Walton, H.S., Dodd, P.R., 2007. Glutamate-glutamine cycling in Alzheimer's disease. Neurochem. Int. 50, 1052-1066.
62. Ward, M.M., Jobling, A.I., Kalloniatis, M., Fletcher, E.L., 2005. Glutamate uptake in retinal glial cells during diabetes. Diabetologia 48, 351-360.
63. Zhang, Y., Barres, B.A., 2010. Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr. Opin. Neurobiol. 20, 588-594.