Short-term episodes of hypoxia induce posthypoxic hyperexcitability and selective death of GABAergic hippocampal neurons

Experimental Neurology

Volumn 250, Issue , 2013, Pages 1-7

  Turovsky, Egor A ^a   Turovskaya, Maria V ^a   Kononov, Alex V ^a   Zinchenko, Valery P ^a  

^a INSTITUTE OF CELL BIOPHYSICS   (Russian Federation)

Author keywords

Brief hypoxia; Ca2+ imaging; Fura 2; GABAergic neurons; Hippocampus; Interleukin 10; NMDA receptors; Posthypoxic hyperexcitability; Precondition

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM BINDING PROTEIN; INTERLEUKIN 10; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CALCIUM SIGNALING; CELL DEATH; CELL FUNCTION; CELL POPULATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; GABAERGIC SYSTEM; HIPPOCAMPUS; HYPOXIA; NERVE CELL EXCITABILITY; NONHUMAN; POSTHYPOXIC HYPEREXCITABILITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RAT; REOXYGENATION; SIGNAL TRANSDUCTION;

BRIEF HYPOXIA; CA(2+) IMAGING; FURA-2; GABAERGIC NEURONS; HIPPOCAMPUS; INTERLEUKIN-10; NMDA RECEPTORS; POSTHYPOXIC HYPEREXCITABILITY; PRECONDITION;

ANIMALS; ANOXIA; APOPTOSIS; CALCIUM; CELL HYPOXIA; CELL SURVIVAL; EXCITATORY AMINO ACIDS; GABAERGIC NEURONS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; ISCHEMIC PRECONDITIONING; N-METHYLASPARTATE; RATS; SIGNAL TRANSDUCTION;

EID: 84885359200     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.09.006     Document Type: Article

References (41)

1. Alexi T., Borlongan C.V., Faull R.L.M., Williams C.E., Clark R.G., Gluckman P.D., Hughes P.E. Neuroprotective strategies for basal ganglia degeneration: Parkinson's and Huntington's diseases. Prog. Neurobiol. 2000, 60:409-470.
2. Bachis A., Colangelo A.M., Vicini S., Doe P.P., De Bernardi M.A., Brooker G., Mocchetti I. Interleukin-10 prevents glutamate-mediated cerebellar granule cell death by blocking caspase-3-like activity. J. Neurosci. 2001, 21(9):3104-3112.
3. Bergeron M., Gidday J.M., Yu A.Y., Semenza G.L., Ferriero D.M., Sharp F.R. Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann. Neurol. 2000, 48:285-296.
4. Bernaudin M., Tang Y., Reilly M., Petit E., Sharp F.R. Brain genomic response following hypoxia and re-oxygenation in the neonatal rat. Identification of genes that might contribute to hypoxia-induced ischemic tolerance. J. Biol. Chem. 2002, 277:39728-39738.
5. Bond A., Lodge D., Hicks C.A., Ward M.A., O'Neill M.J. NMDA receptor antagonism, but not AMPA receptor antagonism attenuates induced ischaemic tolerance in the gerbil hippocampus. Eur. J. Pharmacol. 1999, 380:91-99.
6. Bonde C., Noraberg J., Noer H., Zimmer J. Ionotropic glutamate receptors and glutamate transporters are involved in necrotic neuronal cell death induced by oxygen-glucose deprivation of hippocampal slice cultures. Neuroscience 2005, 136(3):779-794.
7. Cassarino D.S., Bennett J.P. An evaluation of the role of mitochondria in neurodegenerative diseases: mitochondrial mutations and oxidative pathology, protective nuclear responses, and cell death in neurodegeneration. Brain Res. Rev. 1999, 29(1):1-25.
8. Castro-Alamancos M.A. Origin of synchronized oscillations induced by neocortical disinhibition in vivo. J. Neurosci. 2000, 20(24):9195-9206.
9. Choi D.W., Peters S., Viseskul V. Dextrorphan and levorphanol selectively block N-methyl-D-aspartate receptor-mediated neurotoxicity on cortical neurons. J. Pharmacol. Exp. Ther. 1987, 242(2):713-720.
10. 2+ signaling. J. Neurosci. 2005, 25(1):96-107.
11. Earls L.R., Hacker M.L., Watson J.D., Miller D.M. Coenzyme Q protects caenorhabditis elegans GABA neurons from calcium-dependent degeneration. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(32):14460-14465.
12. 2+ channels. Neuropharmacology 2002, 42:459-466.
13. Gonzalez-Burgos G., Lewis D.A. GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. Schizophr. Bull. 2008, 34(5):944-961.
14. Ha K.S., Kim K.M., Kwon Y.G., Bai S.K., Nam W.D., Yoo Y.M., Kim P.K., Chung H.T., Billiar T.R., Kim Y.M. Nitric oxide prevents 6-hydroxydopamine-induced apoptosis in PC12 cells through cGMP-dependent PI3 kinase/Akt activation. FASEB J. 2003, 17:1036-1047.
15. + channels in cerebral ischemic preconditioning. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:4666-4670.
16. Jeong H.Y., Gutkin B. Synchrony of neuronal oscillations controlled by GABAergic reversal potentials. Neural Comput. 2007, 19(3):706-729.
17. Kitagawa K., Matsumoto M., Tagaya M., Hata R., Ueda H., Niinobe M., Handa N., Fukunaga R., Kimura K., Mikoshiba K. "Ischemic tolerance" phenomenon found in the brain. Brain Res. 1990, 528:21-24.
18. Kolch W. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. J. Biochem. 2000, 351:289-305.
19. 2+ oscillations in hippocampal neurons by GABAergic interneurons with desensitization-free kainate receptors. Biol. Membr. (Moscow) 2012, 29(1-2):133-138.
20. Kristian T., Siesjo B.K. Calcium in ischemic cell death. Stroke 1998, 29:705-718.
21. Kruman I., Bruce-Keller A.J., Bredesen D., Waeg G., Mattson M.P. Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J. Neurosci. 1997, 17(13):5089-5100.
22. Kumral A., Baskin H., Gokmen N., Yilmaz O., Genc K., Genc S., Tatli M.M., Duman N., Ozer E., Ozkan H. Selective inhibition of nitric oxide in hypoxic-ischemic brain model in newborn rats: is it an explanation for the protective role of erythropoietin?. Biol. Neonate 2004, 85:51-54.
23. + channels in posthypoxic hyperexcitability and rapid hypoxic preconditioning in hippocampal CA1 pyramidal neurons in vitro. Neurosci. Lett. 2009, 461:90-94.
24. Liu J., Ginis I., Spatz M., Hallenbeck J.M. Hypoxic preconditioning protects cultured neurons against hypoxic stress via TNF-α and ceramide. Am. J. Physiol. Cell Physiol. 2000, 278(1):144-153.
25. 2+ release and apoptosis. Cell Death Dis. 2012, 3(5):304.
26. 2+ and short-term facilitation. J. Neurosci. 2007, 27(9):2261-2271.
27. Murry C.E., Jennings R.B., Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986, 74:1124-1136.
28. Nandagopal K., Dawson T.M., Dawson V.L. Critical role for nitric oxide signaling in cardiac and neuronal ischemic preconditioning and tolerance. J. Pharmacol. Exp. Ther. 2001, 297(2):474-478.
29. Nitsch C., Scotti A., Sommacal A., Kalt G. GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2(+)-binding protein parvalbumin. Neurosci. Lett. 1989, 105(3):263-268.
30. Perez-Pinzon M.A., Mumford P.L., Rosenthal M., Sick T.J. Anoxic preconditioning in hippocampal slices: role of adenosine. Neuroscience 1996, 75:687-694.
31. Rivollier A., Perrin-Cocon L., Luche S., Diemer H., Strub J.M., Hanau D., van Dorsselaer A., Lotteau V., Rabourdin-Combe C., Rabilloud T., Servet-Delprat C. High expression of antioxidant proteins in dendritic cells: possible implications in atherosclerosis. Mol. Cell. Proteomics 2006, 5(4):726-736.
32. Romijn H.J. Preferential loss of GABAergic neurons in hypoxia-exposed neocortex slab cultures is attenuated by the NMDA receptor blocker D-2-amino-7-phosphonoheptanoate. Brain Res. 1989, 501(1):100-104.
33. Romijn H.J., Ruijter J.M., Wolters P.S. Hypoxia preferentially destroys GABAergic neurons in developing rat neocortex explants in culture. Exp. Neurol. 1988, 100(2):332-340.
34. Semenov D.G., Belyakov A.V., Samoilov M.O. Moderate hypobaric hypoxia modifies Ca2+-mediated glutamatergic signal transduction in rat cerebral cortex. Neurosci. Behav. Physiol. 2002, 40(9):1012-1016.
35. Sharma S., Yang B., Xi X., Grotta J.C., Aronowski J., Savitz S.I. IL-10 directly protects cortical neurons by activating PI-3 kinase and STAT-3 pathways. Brain Res. 2011, 1373:189-194.
36. Simonian N.A., Coyle J.T. Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 1996, 36:83-106.
37. Stuart M., Rothwell A., Rothwell N. Cytokines and acute neurodegeneration. Nature 2001, 2:734-744.
38. Tremblay R., Chakravarthy B., Hewitt K., Tauskela J., Morley P., Atkinson T., Durkin J.P. Transient NMDA receptor inactivation provides long-term protection to cultured cortical neurons from a variety of death signals. J. Neurosci. 2000, 20(19):7183-7192.
39. Turovskaya M.V., Turovsky E.A., Zinchenko V.P., Levin S.G., Shamsutdinova A.A., Godukhin O.V. Repeated brief episodes of hypoxia modulate the calcium responses of ionotropic glutamate receptors in hippocampal neurons. Neurosci. Lett. 2011, 496:11-14.
40. i response induced by repeated NMDA receptor activation with brief hypoxia through inhibition of InsP(3)-sensitive internal stores in hippocampal neurons. Neurosci. Lett. 2012, 516(1):151-155.
41. Wu L.Y., Ding A.S., Zhao T., Ma Z.M., Wang F.Z., Fan M. Underlying mechanism of hypoxic preconditioning decreasing apoptosis induced by anoxia in cultured hippocampal neurons. Neurosignals 2005, 14(3):109-116.