Upregulation of calcium binding protein, S100A6, in activated astrocytes is linked to glutamate toxicity

Neuroscience

Volumn 226, Issue , 2012, Pages 119-129

  Yamada, J ^a   Jinno, S ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Aging; Astrocyte; Axotomy; Calcium binding protein; Kainic acid

Indexed keywords

CALCIUM BINDING PROTEIN; CALCYCLIN; CEFTRIAXONE; DIZOCILPINE; GLUTAMIC ACID; KAINIC ACID;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL COUNT; CELL LABELING; CELL SURFACE; CELL TRANSFORMATION; CONTROLLED STUDY; EPILEPSY; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HYPOGLOSSAL NUCLEUS; IMMUNOREACTIVITY; MALE; MOUSE; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE CELL STIMULATION; NERVE FIBER TRANSECTION; NEUROTOXICITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SHAM PROCEDURE; UPREGULATION;

AGING; ANIMALS; ASTROCYTES; AXOTOMY; CA3 REGION, HIPPOCAMPAL; CELL COUNT; CELL CYCLE PROTEINS; DIZOCILPINE MALEATE; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FLUORESCENT ANTIBODY TECHNIQUE; GLUTAMIC ACID; HIPPOCAMPUS; HYPOGLOSSAL NERVE; IMMUNOHISTOCHEMISTRY; KAINIC ACID; MALE; MICE; MICE, INBRED C57BL; NEURONS; RATS; RATS, WISTAR; S100 PROTEINS; TISSUE FIXATION; UP-REGULATION;

EID: 84867315403     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.08.068     Document Type: Article

References (52)

1. Bhatnagar M., Cintra A., Chadi G., Lindberg J., Oitzl M., De Kloet E.R., Möller A., Agnati L.F., Fuxe K. Neurochemical changes in the hippocampus of the brown Norway rat during aging. Neurobiol Aging 1997, 18:319-327.
2. Blackburn D., Sargsyan S., Monk P.N., Shaw P.J. Astrocyte function and role in motor neuron disease: a future therapeutic target?. Glia 2009, 57:1251-1264.
3. Casanovas A., Ribera J., Hukkanen M., Riveros-Moreno V., Esquerda J.E. Prevention by lamotrigine, MK-801 and N omega-nitro-L-arginine methyl ester of motoneuron cell death after neonatal axotomy. Neuroscience 1996, 71:313-325.
4. Clifford D.B., Zorumski C.F., Olney J.W. Ketamine and MK-801 prevent degeneration of thalamic neurons induced by focal cortical seizures. Exp Neurol 1989, 105:272-279.
5. Clineschmidt B.V. Effect of the benzodiazepine receptor antagonist Ro 15-1788 on the anticonvulsant and anticonflict actions of MK-801. Eur J Pharmacol 1982, 84:119-121.
6. de Montigny C., Tardif D. Differential excitatory effects of kainic acid on CA3 and CA1 hippocampal pyramidal neurons: further evidence for the excitotoxic hypothesis and for a receptor-mediated action. Life Sci 1981, 29:2103-2111.
7. During M.J., Spencer D.D. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 1993, 341:1607-1610.
8. Eng L.F., Ghirnikar R.S., Lee Y.L. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem Res 2000, 25:1439-1451.
9. Filipek A., Puzianowska M., Cieślak B., Kuźnicki J. Calcyclin-Ca(2+)-binding protein homologous to glial S-100 beta is present in neurones. Neuroreport 1993, 4:383-386.
10. Freeman G.B., Gibson G.E. Selective alteration of mouse brain neurotransmitter release with age. Neurobiol Aging 1987, 8:147-152.
11. Ganel R., Ho T., Maragakis N.J., Jackson M., Steiner J.P., Rothstein J.D. Selective up-regulation of the glial Na+-dependent glutamate transporter GLT1 by a neuroimmunophilin ligand results in neuroprotection. Neurobiol Dis 2006, 21:556-567.
12. Gill R., Foster A.C., Woodruff G.N. Systemic administration of MK-801 protects against ischemia-induced hippocampal neurodegeneration in the gerbil. J Neurosci 1987, 7:3343-3349.
13. Herman M.A., Nahir B., Jahr C.E. Distribution of extracellular glutamate in the neuropil of hippocampus. PLoS One 2011, 6:e26501.
14. Hosseinzadeh H., Sadeghnia H.R., Rahimi A. Effect of safranal on extracellular hippocampal levels of glutamate and aspartate during kainic acid treatment in anesthetized rats. Planta Med 2008, 74:1441-1445.
15. Hoyaux D., Boom A., Van den Bosch L., Belot N., Martin J.J., Heizmann C.W., Kiss R., Pochet R. S100A6 overexpression within astrocytes associated with impaired axons from both ALS mouse model and human patients. J Neuropathol Exp Neurol 2002, 61:736-744.
16. Jinno S. Regional and laminar differences in antigen profiles and spatial distributions of astrocytes in the mouse hippocampus, with reference to aging. Neuroscience 2011, 180:41-52.
17. Jinno S., Yamada J. Using comparative anatomy in the axotomy model to identify distinct roles for microglia and astrocytes in synaptic stripping. Neuron Glia Biol 2011, 7:55-66.
18. Kawaguchi K., Hickey R.W., Rose M.E., Zhu L., Chen J., Graham S.H. Cyclooxygenase-2 expression is induced in rat brain after kainate-induced seizures and promotes neuronal death in CA3 hippocampus. Brain Res 2005, 1050:130-137.
19. Kiryu-Seo S., Hirayama T., Kato R., Kiyama H. Noxa is a critical mediator of p53-dependent motor neuron death after nerve injury in adult mouse. J Neurosci 2005, 25:1442-1447.
20. Kuźnicki J., Kordowska J., Puzianowska M., Woźniewicz B.M. Calcyclin as a marker of human epithelial cells and fibroblasts. Exp Cell Res 1992, 200:425-430.
21. Langlais P.J., Zhang S.X. Extracellular glutamate is increased in thalamus during thiamine deficiency-induced lesions and is blocked by MK-801. J Neurochem 1993, 61:2175-2182.
22. Leclerc E., Fritz G., Weibel M., Heizmann C.W., Galichet A. S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J Biol Chem 2007, 282:31317-31331.
23. Lepore A.C., Rauck B., Dejea C., Pardo A.C., Rao M.S., Rothstein J.D., Maragakis N.J. Focal transplantation-based astrocyte replacement is neuroprotective in a model of motor neuron disease. Nat Neurosci 2008, 11:1294-1301.
24. Leśniak W., Słomnicki Ł.P., Filipek A. S100A6 - new facts and features. Biochem Biophys Res Commun 2009, 390:1087-1092.
25. Linnemann D., Skarsfelt T. Regional changes in expression of NCAM, GFAP, and S100 in aging rat brain. Neurobiol Aging 1994, 15:651-655.
26. McLin J.P., Steward O. Comparison of seizure phenotype and neurodegeneration induced by systemic kainic acid in inbred, outbred, and hybrid mouse strains. Eur J Neurosci 2006, 24:2191-2202.
27. Nadler J.V., Perry B.W., Cotman C.W. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 1978, 271:676-677.
28. Norton W.T., Aquino D.A., Hozumi I., Chiu F.C., Brosnan C.F. Quantitative aspects of reactive gliosis: a review. Neurochem Res 1992, 17:877-885.
29. Phelps C.H. Neural plasticity in aging and Alzheimer's disease: some selected comments. Prog Brain Res 1990, 86:3-9.
30. Potier B., Billard J.M., Rivière S., Sinet P.M., Denis I., Champeil-Potokar G., Grintal B., Jouvenceau A., Kollen M., Dutar P. Reduction in glutamate uptake is associated with extrasynaptic NMDA and metabotropic glutamate receptor activation at the hippocampal CA1 synapse of aged rats. Aging Cell 2010, 9:722-735.
31. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroenceph Clin Neurophysiol 1972, 32:281-294.
32. Rasmussen B.A., Baron D.A., Kim J.K., Unterwald E.M., Rawls S.M. β-Lactam antibiotic produces a sustained reduction in extracellular glutamate in the nucleus accumbens of rats. Amino Acids 2011, 40:761-764.
33. Rawls S.M., Zielinski M., Patel H., Sacavage S., Baron D.A., Patel D. Betalactam antibiotic reduces morphine analgesic tolerance in rats through GLT-1 transporter activation. Drug Alcohol Depend 2010, 107:261-263.
34. Rickmann M., Wolff J.R. S100 protein expression in subpopulations of neurons of rat brain. Neuroscience 1995, 67:977-991.
35. Rothstein J.D., Van Kammen M., Levey A.I., Martin L.J., Kuncl R.W. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 1995, 38:73-84.
36. Rothstein J.D., Patel S., Regan M.R., Haenggeli C., Huang Y.H., Bergles D.E., Jin L., Dykes Hoberg M., Vidensky S., Chung D.S., Toan S.V., Bruijn L.I., Su Z.Z., Gupta P., Fisher P.B. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 2005, 433:73-77.
37. Rowley H.L., Martin K.F., Marsden C.A. Decreased GABA release following tonic-clonic seizures is associated with an increase in extracellular glutamate in rat hippocampus in vivo. Neuroscience 1995, 68:415-422.
38. Sato K., Morimoto K., Okamoto M. Anticonvulsant action of a non-competitive antagonist of NMDA receptors (MK-801) in the kindling model of epilepsy. Brain Res 1988, 463:12-20.
39. Schauwecker P.E., Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc Natl Acad Sci U S A 1997, 94:4103-4108.
40. Segovia G., Yagüe A.G., García-Verdugo J.M., Mora F. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull 2006, 70:8-14.
41. Shapiro L.A., Wang L., Ribak C.E. Rapid astrocyte and microglial activation following pilocarpine-induced seizures in rats. Epilepsia 2008, 49(Suppl. 2):33-41.
42. Smolders I., Khan G.M., Lindekens H., Prikken S., Marvin C.A., Manil J., Ebinger G., Michotte Y. Effectiveness of vigabatrin against focally evoked pilocarpine-induced seizures and concomitant changes in extracellular hippocampal and cerebellar glutamate, gamma-aminobutyric acid and dopamine levels, a microdialysis-electrocorticography study in freely moving rats. J Pharmacol Exp Ther 1997, 283:1239-1248.
43. Stafstrom C.E., Holmes G.L., Thompson J.L. MK801 pretreatment reduces kainic acid-induced spontaneous seizures in prepubescent rats. Epilepsy Res 1993, 14:41-48.
44. Svensson M., Aldskogius H. Infusion of cytosine-arabinoside into the cerebrospinal fluid of the rat brain inhibits the microglial cell proliferation after hypoglossal nerve injury. Glia 1993, 7:286-298.
45. Ueda Y., Yokoyama H., Nakajima A., Tokumaru J., Doi T., Mitsuyama Y. Glutamate excess and free radical formation during and following kainic acid-induced status epilepticus. Exp Brain Res 2002, 147:219-226.
46. Villarreal A., Aviles Reyes R.X., Angelo M.F., Reines A.G., Ramos A.J. S100B alters neuronal survival and dendrite extension via RAGE-mediated NF-κB signaling. J Neurochem 2011, 117:321-332.
47. Vorwerk C.K., Zurakowski D., McDermott L.M., Mawrin C., Dreyer E.B. Effects of axonal injury on ganglion cell survival and glutamate homeostasis. Brain Res Bull 2004, 62:485-490.
48. Wang Y., Qin Z.H. Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis 2010, 15:1382-1402.
49. Wu Y.W., Grebenyuk S., McHugh T.J., Rusakov D.A., Semyanov A. Backpropagating action potentials enable detection of extrasynaptic glutamate by NMDA receptors. Cell Rep 2012, 1:495-505.
50. Yamada J., Jinno S. Alterations in neuronal survival and glial reactions after axotomy by ceftriaxone and minocycline in the mouse hypoglossal nucleus. Neurosci Lett 2011, 504:295-300.
51. Yamada J., Nakanishi H., Jinno S. Differential involvement of perineuronal astrocytes and microglia in synaptic stripping after hypoglossal axotomy. Neuroscience 2011, 182:1-10.
52. Yamashita N., Ilg E.C., Schäfer B.W., Heizmann C.W., Kosaka T. Distribution of a specific calcium-binding protein of the S100 protein family, S100A6 (calcyclin), in subpopulations of neurons and glial cells of the adult rat nervous system. J Comp Neurol 1999, 404:235-257.