17β-estradiol attenuates glutamate-induced apoptosis and preserves electrophysiologic function in primary cortical neurons

Journal of Neuroscience Research

Volumn 76, Issue 5, 2004, Pages 688-696

  Sribnick, Eric Anthony ^a   Ray, Swapan Kumar ^a   Nowak, Mark Walter ^a   Li, Li ^a   Banik, Naren Lal ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Calpain; Caspase; Electrophysiology; Estrogen

Indexed keywords

CALPAIN; CASPASE 3; ESTRADIOL; ESTROGEN; GLUTAMIC ACID; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN BAX; PROTEIN BCL 2; SODIUM CHANNEL; ANTISENSE OLIGONUCLEOTIDE; BAX PROTEIN, RAT; CASP3 PROTEIN, RAT; CASPASE; ONCOPROTEIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CELL; CELL SHAPE; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; IN VITRO STUDY; MEMBRANE POTENTIAL; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SODIUM CURRENT; UPREGULATION; VOLTAGE CLAMP; ANIMAL; BRAIN CORTEX; CELL COUNT; CELL CULTURE; CELL MEMBRANE POTENTIAL; COMPARATIVE STUDY; CYTOLOGY; DRUG INTERACTION; METABOLISM; METHODOLOGY; NERVE CELL; NEWBORN; PATCH CLAMP; PHYSIOLOGY; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CALPAIN; CASPASE 3; CASPASES; CELL COUNT; CELLS, CULTURED; CEREBRAL CORTEX; DRUG INTERACTIONS; ELECTROPHYSIOLOGY; ESTRADIOL; GLUTAMIC ACID; MEMBRANE POTENTIALS; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; PATCH-CLAMP TECHNIQUES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM CHANNELS;

EID: 2542459293     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20124     Document Type: Article

References (59)

1. Adams JM, Cory S. 2001. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 26:61-66.
2. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P. 1995. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973.
3. Ayres S, Abplanalp W, Liu JH, Subbiah MT. 1998. Mechanisms involved in the protective effect of estradiol-17β on lipid peroxidation and DNA damage. Am J Physiol Endocrinol Metab 274:1002-1008.
4. Banik NL, Hogan EL, Jenkins MG, McDonald JK, McAlhaney WW, Sostek MB. 1983. Purification of a calcium-activated neutral proteinase from bovine brain. Neurochem Res 8:1389-1405.
5. Behl C, Moosmann B, Manthey D, Heck S. 2000. The female sex hormone oestrogen as neuroprotectant: activities at various levels. Novartis Found Symp 230:221-234.
6. Bennett MV, Pellegrini-Giampietro DE, GorterJA, Aronica E, Connor JA, Zukin RS. 1996. The GluR2 hypothesis: Ca(++)-permeable AMPA receptors in delayed neurodegeneration. Cold Spring Harb Symp Quant Biol 61:373-384.
7. Benveniste H, Drejer J, Schousboe A, Diemer NH. 1984. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43:1369-1374.
8. Bracken MB, Shepard MJ, Hellenbrand KG, Collins WF, Leo LS, Freeman DF, Wagner FC, Flamm ES, Eisenberg HM, Goodman JH. 1985. Methylprednisolone and neurological function 1 year after spinal cord injury. Results of the National Acute Spinal Cord Injury Study. J Neurosurg 63:704-713.
9. Cain K, Bratton SB, Cohen GM. 2002. The Apaf-1 apoptosome: a large caspase-activating complex. Biochimie 84:203-214.
10. Chin D, Means AR. 2000. Calmodulin: a protorypical calcium sensor. Trends Cell Biol 10:322-328.
11. Clarke CH, Norfleet AM, Clarke MS, Watson CS, Cunningham KA, Thomas ML. 2000. Perimembrane localization of the estrogen receptor α protein in neuronal processes of cultured hippocampal neurons. Neuroendocrinology 71:34-42.
12. Cotran RS, Kumar V, Collins T. 1999. Robbins pathologic basis of disease. Philadelphia: Saunders.
13. Daniel PT. 2000. Dissecting the pathways to death. Leukemia 14:2035-2044.
14. Dubal DB, Zhu H, Yu J, Rau SW, Shughrue PJ, Merchenthaler I, Kindy MS, Wise PM. 2001. Estrogen receptor α, not β, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci USA 98:1952-1957.
15. Duchen MR. 2000. Mitochondria and calcium: from cell signalling to cell death. J Physiol 1:57-68.
16. Dumont RJ, Verma S, Okonkwo DO, Hurlbert RJ, Boulos PT, Ellegala DB, Dumont AS. 2001. Acute spinal cord injury, part II: contemporary pharmacotherapy. Clin Neuropharmacol 24:265-279.
17. Finiels F, Robert JJ, Samolyk ML, Privat A, Mallet J, Revah F. 1995. Induction of neuronal apoptosis by excitotoxins associated with long-lasting increase of 12-O-tetradecanoylphorbol 13-acetate-responsive element-binding activity. J Neurochem 65:1027-1034.
18. Fitzpatrick JL, Mize AL, Wade CB, Harris JA, Shapiro RA, Dorsa DM. 2002. Estrogen-mediated neuroprotection against β-amyloid toxicity requires expression of estrogen receptor α or β and activation of the MAPK pathway. J Neurochem 82:674-682.
19. Gao G, Dou QP. 2000. N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome C release and apoptotic cell death. J Cell Biochem 80:53-72.
20. Globus MY, Alonso O, Dietrich WD, Busto R, Ginsberg MD. 1995. Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia. J Neurochem 65:1704-1711.
21. Goodman Y, Bruce AJ, Cheng B, Mattson MP. 1996. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid β-peptide toxicity in hippocampal neurons. J Neurochem 66:1836-1844.
22. Groswasser Z, Cohen M, Keren O. 1998. Female TBI patients recover better than males. Brain Inj 12:805-808.
23. Gustafsson JA. 2000. An update on estrogen receptors. Semin Perinatol 24:66-69.
24. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85-100.
25. Hisamoto K, Ohmichi M, Kurachi H, Hayakawa J, Kanda Y, Nishio Y, Adachi K, Tasaka K, Miyoshi E, Fujiwara N, Taniguchi N, Murata Y. 2001. Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J Biol Chem 276:3459-3467.
26. Honda K, Shimohama S, Sawada H, Kihara T, Nakamizo T, Shibasaki H, Akaike A. 2001. Nongenomic antiapoptotic signal transduction by estrogen in cultured cortical neurons. J Neurosci Res 64:466-475.
27. Jacobsohn MK, Bauder S, Pine SR, Jacobsohn GM. 1994. Cholesterol limits estrogen uptake by liposomes and erythrocyte membranes. Biochim Biophys Acta 1:131-140.
28. Jover T, Tanaka H, Calderone A, Oguro K, Bennett MV, Etgen AM, Zukin RS. 2002. Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1. J Neurosci 22:2115-2124.
29. Keum YS, Kim J, Lee KH, Park KK, Surh YJ, Lee JM, Lee SS, Yoon JH, Joo SY, Cha IH, Yook JI. 2002. Induction of apoptosis and caspase-3 activation by chemopreventive [6]-paradol and structurally related compounds in KB cells. Cancer Lett 177:41-47.
30. Kim MJ, Jo DG, Hong GS, Kim BJ, Lai M, Cho DH, Kim KW, Bandyopadhyay A, Hong YM, Kim H, Cho C, Liu JO, Snyder SH, Jung YK. 2002. Calpain-dependent cleavage of cain/cabin1 activates calcineurin to mediate calcium-triggered cell death. Proc Natl Acad Sci USA 99:9870-9875.
31. Kim YJ, Hur EM, Park TJ, Kim KT. 2000. Nongenomic inhibition of catecholamine secretion by 17β-estradiol in PC12 cells. J Neurochem 74:2490-2496.
32. Kohli V, Madden JF, Bentley RC, Clavien PA. 1999. Calpain mediates ischemic injury of the liver through modulation of apoptosis and necrosis. Gastroenterology 116:168-178.
33. Levitan IB, Kaczmarek LK. 1997. The neuron: cell and molecular biology. New York: Oxford University Press. 543 p.
34. Lewen A, Matz P, Chan PH. 2000. Free radical pathways in CNS injury. J Neurotrauma 17:871-890.
35. McGarrity TJ, Peiffer LP, Granville DJ, Carthy CM, Levy JG, Khandelwal M, Hunt DW. 2001. Apoptosis associated with esophageal adenocarcinoma: influence of photodynamic therapy. Cancer Lett 163:33-41.
36. Mendelowitsch A, Ritz MF, Ros J, Langemann H, Gratzl O. 2001. 17β-Estradiol reduces cortical lesion size in the glutamate excitotoxicity model by enhancing extracellular lactate: a new neuroprotective pathway. Brain Res 901:230-236.
37. Michaelis EK. 1998. Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog Neurobiol 54:369-415.
38. Mills CD, Xu GY, Johnson KM, McAdoo DJ, Hulsebosch CE. 2000. AIDA reduces glutamate release and attenuates mechanical allodynia after spinal cord injury. Neuroreport 11:3067-3070.
39. Monroe DG, Berger RR, Sanders MM. 2002. Tissue-protective effects of estrogen involve regulation of caspase gene expression. Mol Endocrinol 16:1322-1331.
40. Moosmann B, Behl C. 1999. The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties. Proc Natl Acad Sci USA 96:8867-8872.
41. Murayama A, Fukai F, Murachi T. 1984. Action of calpain on the basic estrogen receptor molecule of porcine uterus. J Biochem 95:1697-1704.
42. Nicoll RA, Malenka RC. 1995. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377:115-118.
43. Nilsen J, Chen SH, Brinton RD. 2002. Dual action of estrogen on glutamate-induced calcium signaling: mechanisms requiring interaction between estrogen receptors and src/mitogen activated protein kinase pathway. Brain Res 930:216-234.
44. Palmer AM, Marion DW, Botscheller ML, Redd EE. 1993. Therapeutic hypothermia is cytoprotective without attenuating the traumatic brain injury-induced elevations in interstitial concentrations of aspartate and glutamate. J Neurotrauma 10:363-372.
45. Patel M, Day BJ, Crapo JD, Fridovich I, McNamara JO. 1996. Requirement for superoxide in excitotoxic cell death. Neuron 16:345-355.
46. Roof RL, Hall ED. 2000. Estrogen-related gender difference in survival rate and cortical blood flow after impact-acceleration head injury in rats. J Neurotrauma 17:1155-1169.
47. Sattler R, Tymianski M. 2000. Molecular mechanisms of calcium-dependent excitotoxicity. J Mol Med 78:3-13.
48. Sattler R, Xiong Z, Lu WY, Hafner M, MacDonald JF, Tymianski M. 1999. Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 284:1845-1848.
49. Shibasaki F, Hallin U, Uchino H. 2002. Calcineurin as a multifunctional regulator. J Biochem 131:1-15.
50. Singer CA, Figueroa-Masot XA, Batchelor RH, Dorsa DM. 1999. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J Neurosci 19:2455-2463.
51. Sorimachi H, Ishiura S, Suzuki K. 1997. Structure and physiological function of calpains. Biochem J 328:721-732.
52. Sribnick EA, Wingrave JM, Matzelle DD, Ray SK, and Banik NL. (2003). Estrogen as a neuroprotective agent in the treatment of spinal cord injury. Ann N Y Acad Sci 993:125-133.
53. Stupka N, Tiidus PM. 2001. Effects of ovariectomy and estrogen on ischemia-reperfusion injury in hindlimbs of female rats. J Appl Physiol 91:1828-1835.
54. Sur P, Sribnick EA, Wingrave JM, Nowak MW, Ray SK, Banik NL. 2003. Estrogen attenuates oxidative stress-induced apoptosis in C6 glial cells. Brain Res 971:178-188.
55. Tiidus PM, Holden D, Bombardier E, Zajchowski S, Enns D, Belcastro A. 2001. Estrogen effect on post-exercise skeletal muscle neutrophil infiltration and calpain activity. Can J Physiol Pharmacol 79:400-406.
56. Wada S, Yone K, Ishidou Y, Nagamine T, Nakahara S, Niiyama T, Sakou T. 1999. Apoptosis following spinal cord injury in rats and preventative effect of N-methyl-D-aspartate receptor antagonist. J Neurosurg 91:98-104.
57. Wang L, Andersson S, Warner M, Gustafsson JA. 2003. Estrogen receptor (Etk)β knockout mice reveal a role for ERβ in migration of cortical neurons in the developing brain. Proc Natl Acad Sci USA 100:703-708.
58. Weaver CE Jr, Park-Chung M, Gibbs TT, Farb DH. 1997. 17β-Estradiol protects against NMDA-induced excitotoxicity by direct inhibition of NMDA receptors. Brain Res 761:338-341.
59. Zimmerman UJ, Boring L, Pak JH, Mukerjee N, Wang KK. 2000. The calpain small subunit gene is essential: its inactivation results in embryonic lethality. IUBMB Life 50:63-68.