Astrocytic gap junctional communication decreases neuronal vulnerability to oxidative stress-induced disruption of Ca2+ homeostasis and cell death

Journal of Neurochemistry

Volumn 70, Issue 3, 1998, Pages 958-970

  Blanc, Emmanuelle M ^a   Bruce Keller, Annadora J ^a   Mattson, Mark P ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Glutamate receptors; Glutathione; Glycyrrhetinic acid; Hydrogen peroxide; Hydroxynonenal; Lipid peroxidation; Mitochondrial impairment

Indexed keywords

18ALPHA GLYCYRRHETINIC ACID; 3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; 4 HYDROXYNONENAL; ANTIOXIDANT; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; FERROUS SULFATE; FLUORESCEIN DERIVATIVE; GALLIC ACID PROPYL ESTER; GLUTAMATE RECEPTOR ANTAGONIST; GLUTATHIONE; KAINIC ACID; LACTATE DEHYDROGENASE; NIMODIPINE; PEROXIDE;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN MITOCHONDRION; BRAIN NERVE CELL; CALCIUM HOMEOSTASIS; CELL COMMUNICATION; CONTROLLED STUDY; EMBRYO; FLUORESCENCE; GAP JUNCTION; HIPPOCAMPUS; NERVE CELL NECROSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0031892134     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70030958.x     Document Type: Article

References (88)

1. Banker G. A. (1980) Trophic interactions between astroglial cells and hippocampal neurons in culture. Science 209, 809-810.
2. 2+ accumulation. Proc. Natl. Acad. Sci. USA 92, 9328-9332.
3. Benveniste E. N., Tang L. P., and Law R. M. (1995) Differential regulation of astrocyte TNF-α expression by the cytokines TGF-β, IL-6 and IL-10. Int. J. Dev. Neurosci. 13, 341-349.
4. Blanc E. M., Toborek M., Mark R. J., Hennig B., and Mattson M. P. (1997) Amyloid β-peptide disrupts barrier and transport functions and induces apoptosis in vascular endothelial cells. J. Neurochem. 68, 1870-1881.
5. Bolaños J. P. and Medina J. M. (1996) Induction of nitric oxide synthase inhibits gap junction permeability in cultured rat astrocytes. J. Neurochem. 66, 2091-2099.
6. Bowling A. C. and Beal M. F. (1995) Bioenergetic and oxidative stress in neurodegenerative diseases. Life Sci. 56, 1151-1171.
7. Bruce A. J., Sakhi S., Schreiber S. S., and Baudry M. (1995) Development of kainic acid and N-methyl-D-aspartic acid toxicity in organotypic hippocampal cultures. Exp. Neurol. 132, 209-219.
8. Bruce A. J., Malfroy B., and Baudry M. (1996) β-Amyloid toxicity in organotypic hippocampal cultures: protection by EUK-8, a synthetic catalytic free radical scavenger. Proc. Natl. Acad. Sci. USA 93, 2312-2316.
9. Buchs P. A., Stoppini L., and Muller D. (1993) Structural modifications associated with synaptic development in area CA1 of rat hippocampal organotypic cultures. Dev. Brain Rex. 71, 81-91.
10. Cheng B. and Mattson M. P. (1991) NGF and bFGF protect rat and human central neurons against hypoglycemic damage by stabilizing calcium homeostasis. Neuron 7, 1031-1041.
11. Cheng B., Christakos S., and Mattson M. P. (1994) Tumor necrosis factors protect neurons against excitotoxic/metabolic insults and promote maintenance of calcium homeostasis. Neuron 12, 139-153.
12. Chiu F. C., Rozental R., Bassalo C., Lyman W. D., and Spray D. C. (1994) Human fetal neurons in culture: intercellular communication and voltage- and ligand-gated responses. J. Neurosci. Res. 38, 687-697.
13. Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., and Smith S. J. (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470-473.
14. D'Andrea P. and Vittur F. (1996) Gap junctions mediate intercellular calcium signalling in cultured articular chondrocytes. Cell Calcium 20, 389-397.
15. Dani J. W. and Smith S. J. (1995) The triggering of astrocytic calcium waves by NMDA-induced neuronal activation. Ciba Found. Symp. 188, 195-205.
16. Dermietzel R. and Spray D. C. (1993) Gap junctions in the brain: where, what type, how many and why? Trends Neurosci. 16, 186-192.
17. Desagher S., Glowinski J., and Premont J. (1996) Astrocytes protect neurons from hydrogen peroxide toxicity. J. Neurosci. 16, 2553-2562.
18. Duffy S. and Mac Vicar B. A. (1995) Adrenergic calcium signaling in astrocyte networks within the hippocampal slice. J. Neurosci. 15, 5535-5550.
19. Eckenstein P.P. (1994) Fibroblast growth factors in the nervous system. J. Neurobiol. 25, 1467-1480.
20. Eichler M. E., Dubinsky J. M., Tong J., and Rich K.M. (1994) The ability of diphenylpiperazines to prevent neuronal death in dorsal root ganglion neurons in vitro after nerve growth factor deprivation and in vivo after axotomy. J Neurochem. 62, 2148-2157.
21. El-Fouhry M. H., Trosko I.E., and Chang C.-C. (1987) Scrape-loading and dye transfer. Exp. Cell Res. 168, 422-430.
22. + concentration. J. Neurochem. 62, 489-495.
23. Giaume C., Marin P., Cordier J., Glowinsky J., and Premont J. (1991) Adrenergic regulation of intercellular communications between cultured striatal astrocytes from the mouse. Proc. Natl. Acad. Sci. USA 88, 5577-5581.
24. Globus M. Y.-T. Alonso O., Dietrich W. D., Busto R., and Ginsberg M. D. (1995) Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia. J. Neurochem. 65, 1704-1711.
25. Goldberg G. S., Moreno A. P., Bechberger J. F., Hearn S. S., Shivers R. R., MacPhee D. J., Zhang Y.-C., and Naus C. C. (1996) Evidence that disruption of connexon particle arrangements in gap junction plaques is associated with inhibition of gap junctional communication by a glycyrrhetinic acid derivative. Exp. Cell Res. 222, 48-53.
26. Goodman Y. and Mattson M. P. (1994) Secreted forms of β-amyloid precursor protein protect hippocampal neurons against amyloid β-peptide-induced oxidative injury. Exp. Neurol. 128, 1-12.
27. Grynkiewicz G., Poenie M., and Tsien R. Y. (1985) A new generation of calcium indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
28. Guan X., Wilson S., Schlender K. K., and Ruch R. J. (1996) Gap-junction disassembly and connexin 43 dephosphorylation induced by 18 beta-glycyrrhetinic acid. Mol. Carcinog. 16, 157-164.
29. Hassinger T. D., Atkinson P. B., Strecker G. J., Whalen L. R., Dudek F. E., Kossel A. H., and Kater S. B. (1995) Evidence for glutamate-mediated activation of hippocampal neurons by glial calcium waves. J. Neurobiol 28, 159-170.
30. Hassinger T. D., Guthrie P. B., Atkinson P. B., Bennett M. V., and Kater S.B. (1996) An extracellular signaling component in propagation of astrocytic calcium waves. Proc. Natl. Acad. Sci. USA 93, 13268-13273.
31. Hewett S. J., Csernansky C. A., and Choi D. W. (1994) Selective potentiation of NMDA-induced neuronal injury following induction of astrocytic iNOS. Neuron 13, 487-494.
32. Hossain M. Z., Peeling J., Sutherland G. R., Hertzberg E. L., and Nagy J.I. (1994) Ischemia-induced cellular redistribution of the astrocytic gap junctional protein connexin 43 in rat brain. Brain Res. 652, 311-322.
33. Jefferys J. G. R. (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions, Physiol. Rev. 75, 689-723.
34. Jesberger J. A. and Richardson J. S. (1991) Oxygen free radicals and brain dysfunction. Int. J. Neurosci. 57, 1-17.
35. Keller J. N., Steiner M. R., Mattson M. P., and Steiner S. M. (1996) Lysophosphatidic acid decreases glutamate and glucose uptake by astrocytes. J. Neurochem. 67, 2300-2305.
36. Kelly J., Furukawa K., Barger S. W., Mark R. J., Rengen M. R., Blanc E. M., Roth G. S., and Mattson M. P. (1996) Amyloid β-peptide disrupts carbachol-induced muscarinic cholinergic signal transduction in cortical neurons. Proc. Natl. Acad. Sci. USA 93, 6753-6758.
37. Kim W. T., Rioult M. G., and Cornell-Bell A. H. (1994) Glutamate-induced calcium signaling in astrocytes. Glia 11, 173-184.
38. Kim Y. S. and Tauber M. G. (1996) Neurotoxicity of glia activated by gram-positive bacterial products depends on nitric oxide production. Infect. Immun. 64, 3148-3153.
39. Koh J. Y. and Chioi D.W. (1987) Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J. Neurosci. Methods 20, 83-90.
40. Kondo Y. and Takano F. (1994) Nitric oxide production in mouse peritoneal macrophages enhanced with glycyrrhizin. Biol. Pharmacol. Bull. 17, 759-761.
41. Koyama S., Haruyama T., Kobatake E., and Aizawa M. (1997) Electrically induced NGF production by astroglial cells. Nat. Biotechnol. 15, 164-166.
42. Kruman I., Bruce-Keller A. J., Bredesen D. E., Waeg G., and Mattson M. P. (1997) Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J. Neurosci. 17, 5097-5108.
43. Kumar N. M. and Gilula N. B. (1996) The gap junction communication channel. Cell 84, 381-388.
44. Lee S. H., Magge S., Spencer D. D., Sontheimer H., and Cornell-Bell A. H. (1995) Human epileptic astrocytes exhibit increased gap junction coupling. Glia 15, 195-202.
45. 2+ homeostasis and cell death. J. Neurosci. 15, 6239-6249.
46. Mark R. J., Lovell M. A., Markesbery W. R., Uchida K., and Mattson M. P. (1997a) A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68, 255-264.
47. Mark R. J., Pang Z., Geddes J. W., Uchida K., and Mattson M. P. (1997b) Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J. Neurosci. 17, 1046-1054.
48. Martin W., Zempel G., Hulser D., and Willecke K. (1991) Growth inhibition of oncogene-transformed rat fibroblasts by cocultured normal cells: relevance of metabolic cooperation mediated by gap junctions. Cancer Res. 51, 5348-5351.
49. Mattson M. P. and Furukawa K. (1996) Programmed cell life: antiapoptotic signaling and therapeutic strategies for neurodegenerative disorders. Restor. Neuro. Neurosci. 9, 191-205.
50. Mattson M. P. and Rychlik B. (1990) Glia protect hippocampal neurons against excitatory amino acid-induced degeneration: involvement of fibroblast growth factor. Int. J. Dev. Neurosci. 8, 399-415.
51. Mattson M. P., Dou P., and Kater S. B. (1988) Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J. Neurosci. 8, 2087-2100.
52. Mattson M. P., Murrain M., Guthrie P. B., and Kater S. B. (1989) Fibroblast growth factor and glutamate: opposing actions in the generation and degeneration of hippocampal neuroarchitecture. J. Neurosci. 9, 3728-3740.
53. Mattson M. P., Tomaselli K., and Rydel R. E. (1993) Calcium-destabilizing and neurodegenerative effects of aggregated β-amyloid peptide are attenuated by basic FGF. Brain Res. 621, 35-49.
54. Mattson M. P., Barger S. W., Begley J. G., and Mark R. J. (1995a) Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol. 46, 187-216.
55. 2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J. Neurochem. 65, 1740-1751.
56. Mattson M. P., Furukawa K., Bruce A. J., Mark R. J., and Blanc E. M. (1996) Calcium homeostasis and free radical metabolism as convergence points in the pathophysiology of dementia, in Molecular Mechanisms of Dementia (Wasco W. and Tanzi R. E., eds). pp. 103-143. Humana Press, Totowa, New Jersey.
57. Mattson M. P., Barger S. W., Furukawa K., Bruce A. J., Wyss-Coray T., Mark R. J., and Mucke L. (1997) Cellular signaling roles of TGFβ, TNFa and βAPP in brain injury responses and Alzheimer's disease. Brain Res. Rev. 23, 47-61.
58. Muller D., Buchs P.A., and Stoppini L. (1993) Time course of synaptic development in hippocampal organotypic cultures. Dev. Brain Res. 71, 93-100.
59. Munari-Silem Y., Lebrethon M. C., Morand I., Rousset B., and Saez J. M. (1995) Gap-junction-mediated cell-to-cell communication in bovine and human adrenal cells. A process whereby cells increase their responsiveness to physiological corticotropin concentrations. J. Clin. Invest. 95, 1429-1439.
60. Murphy T. H., Blatter L. A., Wier W. G., and Baraban J. M. (1993) Rapid communication between neurons and astrocytes in primary cortical cultures. J. Neurosci. 13, 2672-2679.
61. Musser D. A. and Oseroff A. R. (1994) The use of tetrazolium salts to determine sites of damage to the mitochondrial electron transport chain in intact cells following in vitro photodynamic therapy with Photofrin II. Photochem. Photobiol. 59, 621-626.
62. Nedergaard M. (1994) Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science 263, 1768-1771.
63. Nedergaard M., Cooper A. J., and Goldman S. A. (1995) Gap junctions are required for the propagation of spreading depression. J. Neurobiol 28, 433-444.
64. Page B., Page M., and Noel C. (1993) A new fluorometric assay for cytotoxicity measurements in vitro. Int. J. Oncol. 3, 473-476.
65. + in rat astrocytes. Glia 16, 7-15.
66. Paul D. L. (1995) New functions for gap junctions. Curr. Opin. Cell Biol. 7, 665-672.
67. Pereda A. E. and Faber D. S. (1996) Activity-dependent short-term enhancement of intercellular coupling. J. Neurosci. 16, 983-992.
68. Prehn J. H., Bindokas V. P., Jordan J., Galindo M. F., Ghadge G. D., Roos R. P., Boise L. H., Thompson C. B., Krajewski S., Reed J. C., and Miller R. J. (1996) Protective effect of transforming growth factor-β1 on β-amyloid neurotoxicity in rat hippocampal neurons. Mol. Pharmacol. 49, 319-328.
69. Robinson M. B. and Dowd L. A. (1997) Heterogeneity and functional properties of subtypes of sodium-dependent glutamate transporters in the mammalian central nervous system. Adv. Pharmacol. 37, 69-115.
70. Rörig B. and Sutor B. (1996) Nitric oxide-stimulated increase in intracellular cGMP modulates gap junction coupling in rat neocortex. Neuroreport 7, 569-572.
71. Rozental R., Mehler M. F., Morales M., Andrade-Rozental A. F., Kessler J. A., and Spray D. C. (1995) Differentiation of hippocampal progenitor cells in vitro: temporal expression of intercellular coupling and voltage-and ligand-gated responses. Dev. Biol. 167, 350-362.
72. Saez J. C., Spray D. C., Nairn A. C., Hertzberg E., Greengard P., and Bennett V. L. (1986) cAMP increases junctional conductance and stimulates phosphorylation of the 27-kDa principal gap junction polypeptide. Proc. Natl. Acad. Sci. USA 83, 2473-2477.
73. Sawchuk M. A., Hossain M. Z., Hertzberg E. L., and Nagy J. I. (1995) In situ transblot and immunocytochemical comparisons of astrocytic connexin-43 responses to NMDA and kainic acid in rat brain. Brain Res. 683, 153-157.
74. Schwartz J. P., and Nishiyama N. (1994) Neurotrophic factor gene expression in astrocytes during development and following injury. Brain Res. Bull. 35, 403-407.
75. Shearman M. S., Hawtin S. R., and Tailor V. J. (1995) The intracellular component of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction is specifically inhibited by β-amyloid peptides. J. Neurochem. 65, 218-227.
76. Sheen V. L., Dreyer E. B., and Macklis J. D. (1992) Calcium-mediated neuronal degeneration following singlet oxygen production. Neurorepon 3, 705-708.
77. Simonian N. A. and Coyle J. T. (1996) Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 36, 83-106.
78. Spray D. C. and Dermietzel R. (1995) X-linked dominant CharcotMarie-Tooth disease and other potential gap-junction diseases of the nervous system. Trends Neurosci. 18, 256-262.
79. Stoppini L., Buchs P. A., and Muller D. (1991) A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182.
80. Stuiver B. T., Douma B. R., Bakker R., Nyakas C., and Luiten P. G. (1996) In vivo protection against NMDA-induced neurodegeneration by MK-801 and nimodipine: combined therapy and temporal course of protection. Neurodegeneration 5, 153-159.
81. Teranishi T., Neighs K., and Kato S. (1983) Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature 301, 243-246.
82. Tomac A., Lindqvist E., Lin L. F., Ogren S. O., Young D., Hoffer B. J., and Oison L. (1995) Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373, 335-339.
83. Tsacopoulos M. and Magistretti P. J. (1996) Metabolic coupling between glia and neurons. J. Neurosci. 16, 877-885.
84. Venance L., Piomelli D., Glowinski J., and Giaume C. (1995) Inhibition by anandamide of gap junctions and intercellular calcium signalling in striatal astrocytes. Nature 376, 590-594.
85. Verkhratsky A. and Kettenmann H. (1996) Calcium signalling in glial cells. Trends Neurosci. 19, 346-352.
86. Welsh D. K. and Reppert S. M. (1996) Gap junctions couple astrocytes but not neurons in dissociated cultures of rat suprachiasmatic nucleus. Brain Res. 706, 30-36.
87. Whorwood C. B. and Stewart P. M. (1995) Transcriptional regulation of Na/K-ATPase by corticosteroids, glycyrrhetinic acid and second messenger pathways in rat kidney epithelial cells. J. Mol. Endocrinol. 15, 93-103.
88. Zhang Y., Tatsuno T., Carney J., and Mattson M. P. (1993) Basic FGF, NGF, and IGFs protect hippocampal neurons against iron-induced degeneration. J. Cereb. Blood Flow Metab. 13, 378-388.