Non-cell autonomous influence of the astrocyte system X-c on hypoglycaemic neuronal cell death

ASN Neuro

Volumn 4, Issue 1, 2012, Pages 23-32

  Jackman, Nicole A ^a   Melchior, Shannon E ^a   Hewett, James A ^b   Hewett, Sandra J ^b  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b SYRACUSE UNIVERSITY   (United States)

Author keywords

Aglycaemia; Astrocyte; Cystine; Glutamate; Neuronal death; Non cell autonomous

Indexed keywords

CYSTEINE; GLUTAMIC ACID; INTERLEUKIN 1BETA; AMINO ACID TRANSPORTER; GLUCOSE; SLC7A11 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EXCITOTOXICITY; FETUS; GENETIC ASSOCIATION; HYPOGLYCEMIA; MOUSE; MUTATOR GENE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NONHUMAN; NULL ALLELE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SLC7A11 GENE; ANIMAL; BRAIN; CELL COMMUNICATION; CELL DEATH; COCULTURE; METABOLISM; MOUSE MUTANT; NERVE CELL; PATHOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; ASTROCYTES; BRAIN; CELL COMMUNICATION; CELL DEATH; COCULTURE TECHNIQUES; GLUCOSE; GLUTAMIC ACID; HYPOGLYCEMIA; MICE; MICE, MUTANT STRAINS; NEURONS; POLYMERASE CHAIN REACTION;

EID: 84857677639     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20110030     Document Type: Article

References (111)

1. Auer RN, Wieloch T, Olsson Y, Siesjo BK (1984) The distribution of hypoglycemic brain damage. Acta Neuropathol 64:177-191.
2. Augustin H, Grosjean Y, Chen K, Featherstone DE (2007) Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. J Neurosci 27:111-123.
3. Backus KH, Kettenmann H, Schachner M (1989) Pharmacological characterization of the glutamate receptor in cultured astrocytes. J Neurosci Res 2:274-282.
4. Baker DA, Madayag A, Kristiansen LV, Meador-Woodruff JH, Haroutunian V, Raju I (2008) Contribution of cystine-glutamate antiporters to the psychotomimetic effects of phencyclidine. Neuropsychopharmacology 33:1760-1772.
5. Baker DA, McFarland K, Lake RW, Shen H, Tang XC, Toda S, Kalivas PW (2003) Neuroadaptations in cystine-glutamate exchange underlie cocaine relapse. Nat Neurosci 6:743-749.
6. Baker DA, Shen H, Kalivas PW (2002a) Cystine/glutamate exchange serves as the source for extracellular glutamate: modifications by repeated cocaine administration. Amino Acids 23:161-162.
7. Baker DA, Xi ZX, Shen H, Swanson CJ, Kalivas PW(2002b) The origin and neuronal function of in vivo nonsynaptic glutamate. J Neurosci 22:9134-9141.
8. Bakken IJ, White LR, Unsgard G, Aasly J, Sonnewald U (1998) [U-13C]glutamate metabolism in astrocytes during hypoglycemia and hypoxia. J Neurosci Res 51:636-645.
9. Bannai S (1984) Transport of cystine and cysteine in mammalian cells. Biochim Biophys Acta 779:289-306.
10. Bannai S, Kitamura E (1980) Transport interaction of L-cystine and L-glutamate in human diploid fibroblasts in culture. J Biol Chem 255:2372-2376.
11. Bannai S, Kitamura E (1982) Adaptive enhancement of cystine and glutamate uptake in human diploid fibroblasts in culture. Biochim Biophys Acta 721:1-10.
12. Bannai S, Sato H, Ishii T, Sugita Y (1989) Induction of cystine transport activity in human fibroblasts by oxygen. J Biol Chem 264:18480-18484.
13. Barbeito LH, Pehar M, Cassina P, Vargas MR, Peluffo H, Viera L, Estevez AG, Beckman JS (2004) A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res Brain Res Rev 47:263-274.
14. Barger SW, Basile AS (2001) Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. J Neurochem 76:846-854.
15. -. Pflugers Arch 442:286-296.
16. Brabet I, Mary S, Bockaert J, Pin JP (1995) Phenylglycine derivatives discriminate between mGluR1- and mGluR5-mediated responses. Neuropharmacology 34:895-903.
17. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum free medium combination. J Neurosci Res 35:567-576.
18. Bridges C, Kekuda R, Wang H, Prasad P, Mehta P, Huang W, Smith S, Ganapathy V (2001) Structure, function, and regulation of human cystine/glutamate transporter in retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 42:47-54.
19. Bridges RJ (2012) System xc - cystine/glutamate antiporter: an update on molecular pharmacology and roles within the CNS. Br J Pharmacol 165:20-34.
20. Brigham MP, Stein WH, Moore S (1960) The Concentrations of cysteine and cystine in human blood plasma. J Clin Invest 39:1633-1638.
21. - in the brain, kidney, and duodenum. J Histochem Cytochem 54:549-557.
22. Cataldo AM, Broadwell RD (1986) Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions: I. Neurons and glia. J Electron Microsc Technol 3:413-437.
23. Cavelier P, Hamann M, Rossi D, Mobbs P, Attwell D (2005) Tonic excitation and inhibition of neurons: ambient transmitter sources and computational consequences. Prog Biophys Mol Biol 87:3-16.
24. Chan PH, Chu L, Chen S (1990) Effects of MK-801 on glutamate-induced swelling of astrocytes in primary cell culture. J Neurosci Res 25:87-93.
25. Chen Y, Swanson RA (2003) Astrocytes and brain injury. J Cereb Blood Flow Metab 23:137-149.
26. Chintala S, Li W, Lamoreux ML, Ito S, Wakamatsu K, Sviderskaya EV, Bennett DC, Park YM, Gahl WA, Huizing M et al. (2005) Slc7a11 gene controls production of pheomelanin pigment and proliferation of cultured cells. Proc Natl Acad Sci USA 102:10964-10969.
27. Choi IY, Lee SP, Kim SG, Gruetter R (2001) In vivo measurements of brain glucose transport using the reversible Michaelis-Menten model and simultaneous measurements of cerebral blood flow changes during hypoglycemia. J Cereb Blood Flow Metab 21:653-663.
28. Choi JW, Shin CY, Choi MS, Yoon SY, Ryu JH, Lee JC, Kim WK, El Kouni MH, Ko KH (2008) Uridine protects cortical neurons from glucose deprivationinduced death: possible role of uridine phosphorylase. J Neurotrauma 25:695-707.
29. Clapp-Lilly KL, Roberts RC, Duffy LK, Irons KP, Hu Y, Drew KL (1999) An ultrastructural analysis of tissue surrounding a microdialysis probe. J Neurosci Methods 90:129-142.
30. Crawhall JC, Lietman PS, Schneider JA, Seegmiller JE (1968) Cystinosis. Plasma cystine and cysteine concentrations and the effect of Dpenicillamine and dietary treatment. Am J Med 44:330-339.
31. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105.
32. - does not induce oxidative stress but decreases extracellular glutamate in hippocampus and influences spatial working memory and limbic seizure susceptibility. J Neurosci 31:5792-5803.
33. Dienel GA, Cruz NF (2006) Astrocyte activation in working brain: energy supplied by minor substrates. Neurochem Int 48:586-595.
34. Dogan Y, Akarsu S, Ustundag B, Yilmaz E, Gurgoze MK (2006) Serum IL-1beta, IL-2, and IL-6 in insulin-dependent diabetic children. Mediators Inflamm 2006:59206.
35. - and glutamate transporter inhibition mediates microglial toxicity to oligodendrocytes. J Immunol 178:6549-6556.
36. Dun Y, Mysona B, Van Ells T, Amarnath L, Ola MS, Ganapathy V, Smith SB (2006) Expression of the cystine-glutamate exchanger (xc2) in retinal ganglion cells and regulation by nitric oxide and oxidative stress. Cell Tissue Res 324:189-202.
37. Eck HP, Gmunder H, Hartmann M, Petzoldt D, Daniel V, Droge W (1989) Low concentrations of acid-soluble thiol (cysteine) in the blood plasma of HIV-1-infected patients. Biol Chem Hoppe Seyler 370:101-108.
38. Erecinska M, Silver IA (1994) Ions and energy in mammalian brain. Prog Neurobiol 43:37-71.
39. Featherstone DE, Shippy SA (2008) Regulation of synaptic transmission by ambient extracellular glutamate. Neuroscientist 14:171-181.
40. Ferraguti F, Pietra C, Valerio E, Corti C, Chiamulera C, Conquet F (1997) Evidence against a permissive role of the metabotropic glutamate receptor 1 in acute excitotoxicity. Neuroscience 79:1-5.
41. Fogal B, Hewett JA, Hewett SJ (2005) Interleukin-1beta potentiates neuronal injury in a variety of injury models involving energy deprivation. J Neuroimmunol 161:93-100.
42. - activity and astrocytes are necessary for interleukin-1b-mediated hypoxic neuronal injury. J Neurosci 27:10094-10105.
43. - subunits. J Neurochem 78:276-286.
44. Goldberg MP, Choi DW (1993) Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J Neurosci 13:3510-3524.
45. Hamby ME, Uliasz TF, Hewett SJ, Hewett JA (2006) Characterization of an improved procedure for the removal of microglia from confluent monolayers of primary astrocytes. J Neurosci Methods 150:128-137.
46. Hewett JA (2009) Determinants of regional and local diversity within the astroglial lineage of the normal central nervous system. J Neurochem 110:1717-1736.
47. Hirrlinger J, Schulz JB, Dringen R (2002) Glutathione release from cultured brain cells: multidrug resistance protein 1 mediates the release of GSH from rat astroglial cells. J Neurosci Res 69:318-326.
48. Hosoya KI, Tomi M, Ohtsuki S, Takanaga H, Saeki S, Kanai Y, Endou H, Naito M, Tsuruo T, Terasaki T (2002) Enhancement of L-cystine transport activity and its relation to xCT gene induction at the blood-brain barrier by diethyl maleate treatment. J Pharmacol Exp Ther 302:225-231.
49. Ichord RN, Johnston MV, Traystman RJ (2001) MK801 decreases glutamate release and oxidative metabolism during hypoglycemic coma in piglets. Brain Res Dev Brain Res 128:139-148.
50. Ichord RN, Northington FJ, van Wylen D, Johnston MV, Kwon C, Traystman RJ (1999) Brain O2 consumption and glutamate release during hypoglycemic coma in piglets are temperature sensitive. Am J Physiol Heart Circ Physiol 276:H2053-H2062.
51. Ikemoto H, Tani E, Matsumoto T, Nakano A, Furuyama J (1995) Apoptosis of human glioma cells in response to calphostin C, a specific protein kinase C inhibitor. J Neurosurg 83:1008-1016.
52. Jabaudon D, Shimamoto K, Yasuda-Kamatani Y, Scanziani M, Gahwiler BH, Gerber U (1999) Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc Natl Acad Sci USA 96:8733-8738.
53. - in hypoglycemia-induced neuronal cell death. Program No. 156.3. 2010 Neuroscience Meeting Planner. Society for Neuroscience, San Diego, CA.
54. Jackman NA, Uliasz TF, Hewett JA, Hewett SJ (2010b) Regulation of system x(c)(-)activity and expression in astrocytes by interleukin-1beta: implications for hypoxic neuronal injury. Glia 58:1806-1815.
55. Jakel RJ, Townsend JA, Kraft AD, Johnson JA (2007) Nrf2-mediated protection against 6-hydroxydopamine. Brain Res 1144:192-201.
56. Janssens N, Lesage AS (2001) Glutamate receptor subunit expression in primary neuronal and secondary glial cultures. J Neurochem 77:1457-1474.
57. Jones DP, Mody VC Jr, Carlson JL, Lynn MJ, Sternberg P Jr, (2002) Redox analysis of human plasma allows separation of pro-oxidant events of aging from decline in antioxidant defenses. Free Radical Biol Med 33:1290-1300.
58. Kau KS, Madayag A, Mantsch JR, Grier MD, Abdulhameed O, Baker DA (2008) Blunted cystine-glutamate antiporter function in the nucleus accumbens promotes cocaine-induced drug seeking. Neuroscience 155: 530-537
59. Kingston AE, Griffey K, Johnson MP, Chamberlain MJ, Kelly G, Tomlinson R, Wright RA, Johnson BG, Schoepp DD, Harris JR et al. (2002) Inhibition of group I metabotropic glutamate receptor responses in vivo in rats by a new generation of carboxyphenylglycine-like amino acid antagonists. Neurosci Lett 330:127-130.
60. Kranich O, Hamprecht B, Dringen R (1996) Different preferences in the utilization of amino acids for glutathione synthesis in cultured neurons and asroglial cells derived from rat brain. Neurosci Lett 219:211-212.
61. La Bella V, Valentino F, Piccoli T, Piccoli F (2007) Expression and developmental regulation of the cystine/glutamate exchanger (xc2) in the rat. Neurochem Res 32:1081-1090.
62. Langan SJ, Deary IJ, Hepburn DA, Frier BM (1991) Cumulative cognitive impairment following recurrent severe hypoglycaemia in adult patients with insulin-treated diabetes mellitus. Diabetologia 34:337-344.
63. Lewerenz J, Albrecht P, Tien ML, Henke N, Karumbayaram S, Kornblum HI, Wiedau-Pazos M, Schubert D, Maher P, Methner A (2009) Induction of Nrf2 and xCT are involved in the action of the neuroprotective antibiotic ceftriaxone in vitro. J Neurochem 111:332-343.
64. Lobsiger CS, Cleveland DW (2007) Glial cells as intrinsic components of noncell-autonomous neurodegenerative disease. Nat Neurosci 10:1355-1360.
65. Lyons SA, Kettenmann H (1998) Oligodendrocytes and microglia are selectively vulnerable to combined hypoxia and hypoglycemia injury in vitro. J Cereb Blood Flow Metab 18:521-530.
66. --deficient mice are highly protected against 6-hydroxydopamine- induced toxicity. FASEB J 25:1359-1369.
67. Matyash V, Kettenmann H (2010) Heterogeneity in astrocyte morphology and physiology. Brain Res Rev 63:2-10.
68. McBean GJ (2002) Cerebral cystine uptake: a tale of two transporters. Trends Pharmacol Sci 23:299-302.
69. Melendez RI, Vuthiganon J, Kalivas PW (2005) Regulation of extracellular glutamate in the prefrontal cortex: focus on the cystine glutamate exchanger and group I metabotropic glutamate receptors. J Pharmacol Exp Ther 314:139-147.
70. Miura K, Ishii T, Sugita Y, Bannai S (1992) Cystine uptake and glutathione level in endothelial cells exposed to oxidative stress. Am J Physiol 262:C50-C58.
71. Monyer H, Choi DW (1988) Morphinans attenuate cortical neuronal injury induced by glucose deprivation in vitro. Brain Res 446:144-148.
72. Monyer H, Giffard RG, Hartley DM, Dugan LL, Goldberg MP, Choi DW (1992) Oxygen or glucose deprivation-induced neuronal injury in cortical cell cultures is reduced by tetanus toxin. Neuron 8:967-973.
73. Monyer H, Goldberg MP, Choi DW (1989) Glucose deprivation neuronal injury in cortical culture. Brain Res 483:347-354.
74. Moroni F, Attucci S, Cozzi A, Meli E, Picca R, Scheideler MA, Pellicciari R, Noe C, Sarichelou I, Pellegrini-Giampietro DE (2002) The novel and systemically active metabotropic glutamate 1 (mGlu1) receptor antagonist 3-MATIDA reduces post-ischemic neuronal death. Neuropharmacology 42:741-751.
75. Nellgard B, Wieloch T (1992) Cerebral protection by AMPA- and NMDAreceptor antagonists administered after severe insulin-induced hypoglycemia. Exp Brain Res 92:259-266.
76. Novelli A, Reilly JA, Lysko PG, Henneberry RC (1988) Glutamate becomes neurotoxic via the N-methyl-D-aspartate receptor when intracellular energy levels are reduced. Brain Res 451:205-212.
77. -: an obligate exchanger of L-glutamate and L-cystine. Neuropharmacology 46:273-284.
78. - in the macrophage-induced glutamate-dependent cytotoxicity to neurons. J Immunol 152:3578-3585.
79. - and apolipoprotein E expressed by microglia have opposite effects on the neurotoxicity of amyloid-beta peptide 1-40. J Neurosci 26:3345-3356.
80. Ryan CM, Atchison J, Puczynski S, Puczynski M, Arslanian S, Becker D (1990) Mild hypoglycemia associated with deterioration of mental efficiency in children with insulin-dependent diabetes mellitus. J Pediatr 117:32-38.
81. Sandberg M, Butcher SP, Hagberg H (1986) Extracellular overflow of neuroactive amino acids during severe insulin-induced hypoglycemia: in vivo dialysis of the rat hippocampus. J Neurochem 47:178-184.
82. Sato H, Fujiwara K, Sagara J, Bannai S (1995) Induction of cystine transport activity in mouse peritoneal macrophages by bacterial lipopolysaccharide. Biochem J 310:547-551.
83. Sato H, Tamba M, Ishii T, Bannai S (1999) Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem 274:11455-11458.
84. Savaskan NE, Heckel A, Hahnen E, Engelhorn T, Doerfler A, Ganslandt O, Nimsky C, Buchfelder M, Eyupoglu IY (2008) Small interfering RNA-mediated Xct silencing in gliomas inhibits neurodegeneration and alleviates brain edema. Nat Med 14:629-632.
85. Shih AY, Erb H, Sun X, Toda S, Kalivas PW, Murphy TH (2006) Cystine/glutamate exchange modulates glutathione supply for neuroprotection from oxidative stress and cell proliferation. J Neurosci 26:10514-10523.
86. Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H, Johnson JA, Murphy TH (2003) Coordinate regulation of glutathione biosynthesis and release by Nrf-2 expressing glia potently protects neurons from oxidative stress. J Neurosci 23:3394-3406.
87. Silverstein FS, Simpson J, Gordon KE (1990) Hypoglycemia alters striatal amino acid efflux in perinatal rats: an in vivo microdialysis study. Ann Neurol 28:516-521.
88. Sontheimer H (2008) A role for glutamate in growth and invasion of primary brain tumors. J Neurochem 105:287-295
89. Steel R, Torrie J (1980) Principles and Procedures of Statistics: A Biometrical Approach, McGraw-Hill Book Co., New York.
90. Suh SW, Bergher JP, Anderson CM, Treadway JL, Fosgerau K, Swanson RA (2007a) Astrocyte glycogen sustains neuronal activity during hypoglycemia: studies with the glycogen phosphorylase inhibitor CP-316,819 ([R-R*,S*]-5-Chloro-N-[2-hydroxy-3-(methoxymethylamino)-3-oxo-1-(phenylmethyl)-propyl]-1H-indole-2-carboxamide). J Pharmacol Exp Ther 321:45-50.
91. Suh SW, Hamby AM, Swanson RA (2007b) Hypoglycemia, brain energetics, and hypoglycemic neuronal death. Glia 55:1280-1286.
92. Swanson RA, Benington JH (1996) Astrocyte glucose metabolism under normal and pathological conditions in vitro. Dev Neurosci 18:515-521.
93. Swanson RA, Yu AC, Chan PH, Sharp FR (1990) Glutamate increases glycogen content and reduces glucose utilization in primary astrocyte culture. J Neurochem 54:490-496.
94. Tanaka J, Toku K, Zhang B, Ishihara K, Sakanaka M, Maeda N (1999) Astrocytes protect neuronal death induced by reactive oxygen and nitrogen species. Glia 28:85-96.
95. Tasker RC, Coyle JT, Vornov JJ (1992) The regional vulnerability to hypoglycemiainduced neurotoxicity in organotypic hippocampal culture: protection by early tetrodotoxin or delayed MK-801. J Neurosci 12:4298-4308.
96. Taylor AL, Hewett SJ (2002) Potassium-evoked glutamate release liberates arachidonic acid from cortical neurons. J Biol Chem 277:43881-43887.
97. Trackey JL, Uliasz TF, Hewett SJ (2001) SIN-1-induced cytotoxicity in mixed cortical cell culture: peroxynitrite-dependent and -independent induction of excitotoxic cell death. J Neurochem 79:445-455.
98. Uliasz TF, Hewett SJ (2000) A microtiter trypan blue absorbance assay for the quantitative determination of excitotoxic neuronal injury in cell culture. J Neurosci Methods 100:157-163.
99. Vitvitsky V, Thomas M, Ghorpade A, Gendelman HE, Banerjee R (2006) A functional transsulfuration pathway in the brain links to glutathione homeostasis. J Biol Chem 281:35785-35793.
100. Walls AB, Heimburger CM, Bouman SD, Schousboe A, Waagepetersen HS (2009) Robust glycogen shunt activity in astrocytes: effects of glutamatergic and adrenergic agents. Neuroscience 158:284-292.
101. Wang XF, Cynader MS (2000) Astrocytes provide cysteine to neurons by releasing glutathione. J Neurochem 74:1434-1442.
102. Warr O, Takahashi M, Attwell D (1999) Modulation of extracellular glutamate concentration in rat brain slices by cystine-glutamate exchange. J Physiol 514:783-793.
103. Watanabe H, Bannai S (1987) Induction of cystine transport activity in mouse peritoneal macrophages. J Exp Med 165:628-640.
104. Watkins J, Collingridge G (1994) Phenylglycine derivatives as antagonists of metabotropic glutamate receptors. Trends Pharmacol Sci 15:333-342.
105. Westergren I, Nystrom B, Hamberger A, Johansson BB (1995) Intracerebral dialysis and the blood-brain barrier. J Neurochem 64:229-234.
106. Wieloch T (1985) Hypoglycemia-induced neuronal damage prevented by an N-methyl-D-aspartate antagonist. Science 230:681-683.
107. Wieloch T, Engelsen B, Westerberg E, Auer R (1985) Lesions of the glutamatergic cortico-striatal projections in the rat ameliorate hypoglycemic brain damage in the striatum. Neurosci Lett 58:25-30.
108. Xu C, Yogaratnam J, Lua R, Khoo CL, Oillai SS, Sim K (2011a) Persistent, severe hypoglycemia-induced organic brain syndrome with neurological sequelae: a case study. Gen Hosp Psychiatry 33:412.e419-412.e411.
109. Xu C, Yogaratnam J, Lua R, Naik S, Khoo CL, Pillai SS, Sim K (2011b) Persistent, severe hypoglycemia-induced organic brain syndrome with neurological sequelae: a case report. Gen Hosp Psychiatry 33:412.e9-412.e11.
110. Ye ZC, Rothstein JD, Sontheimer H (1999) Compromised glutamate transport in human glioma cells: reduction-mislocalization of sodium-dependent glutamate transporters and enhanced activity of cystine-glutamate exchange. J Neurosci 19:10767-10777.
111. Zhang Y, Barres BA (2010) Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr Opin Neurobiol 20:588-594.