Acidosis leads to neurological disorders through overexciting cortical pyramidal neurons

Biochemical and Biophysical Research Communications

Volumn 415, Issue 2, 2011, Pages 224-228

  Zhao, Hong ^a   Cai, Yan ^a   Yang, Zichao ^a   He, Dandan ^a   Shen, Baozhong ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Acidosis; Action potential; Pyramidal neuron; Sodium channel; Synaptic transmission

Indexed keywords

ACIDOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CEREBROSPINAL FLUID; CONTROLLED STUDY; CORTICAL PYRAMIDAL NEURON; EXCITOTOXICITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NERVE CELL NETWORK; NEUROLOGIC DISEASE; NONHUMAN; PH; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REFRACTORY PERIOD; SIGNAL TRANSDUCTION;

ACIDOSIS; ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; HUMANS; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; MICE; MICE, INBRED STRAINS; NERVOUS SYSTEM DISEASES; PYRAMIDAL CELLS; SODIUM CHANNELS; SYNAPSES;

EID: 84855905187     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2011.08.008     Document Type: Article

References (53)

1. Fricker D., Miles R. Interneuron, spike timing, and perception. Neuron 2001, 32:771-774.
2. Klyachko V.A., Stevens C.F. Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as adaptive filter of neural spike trains. PLoS Biol. 2006, 4.
3. Shepherd G.M. Electronic Properties of Axons and Dendrites 2004, Elsevier Science, New York, USA.
4. Wang J.H., Wei J., Chen X., Yu J., Chen N., Shi J. The gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding. J. Cell Sci. 2008, 121:2951-2960.
5. Avoli M., Louvel J., Pumain R., Kohling R. Cellular and molecular mechanisms of epilepsy in the human brain. Prog. Neurobiol. 2005, 77:166-200.
6. Okuda T., Kurokawa K., Papadakis M.A. Fluid and electrolyte disorders. Current Medical Diagnosis and Treatment 1998, 824-849. Appleton & Lange, Stamford. L.M. Tierney, S.J. McPhee, M.A. Papadakis (Eds.).
7. Nowak T.J., Handford A.G. Fluid and electrolyte imbalances. Pathophysiology 2004, 422-445. Martin J. Lange, Boston. T.J. Nowak, A.G. Handford (Eds.).
8. Amano T., Unal C.T., Pare D. Synaptic correlates of fear extinction in the amygdala. Nat. Neurosci. 2010, 13:489-495.
9. Bishop S.J. Neurocongnitive mechanisms of anxiety: an integrative account. Trends Cognit. Sci. 2007, 11:307-316.
10. DuBios D.W., Floyd P.A.D.W., Weiner J.L., McCool B.A. Distinct functional characteristics of the lateral/basolateral amygdala GABAergic system in C57BL/6J and DBA/2J mice. J. Pharmacol. Exp. Ther. 2006, 318:629-640.
11. Ehrlich I., Humeau Y., Grenier F., Ciocchi S., Herry C., Luthi A. Amygdala inhibitory circuits and the control of fear memory. Neuron 2009, 62:757-771.
12. Arabadzisz D., Freund T.F. Changes in excitatory and inhibitory circuits of the rat hippocampus 12-14months after complete forebrain ischemia. Neuroscience 1999, 92:27-45.
13. Fan Y., Deng P., Wang Y.C., Lu H.C., Xu Z.C., Schulz P.E. Transient cerebral ischemia increases CA1 pyramidal neuron excitability. Exp. Neurol. 2008, 212:415-421.
14. Hamann M., Rossi D.J., Mohr C., Andrade A.L., Attwell D. The electrical response of cerebellar Purkinje neurons to simulated ischemia. Brain 2005, 128:2408-2420.
15. Huang L., Chen N., Ge M., Zhu Y., Guan S., Wang J.H. Ca2+ and acidosis synergistically lead to the dysfunction of cortical GABAergic neurons during ischemia. Biochem. Biophys. Res. Commun. 2010, 394:709-714.
16. Wang J.-H. Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons. Brain Res. Bull. 2003, 60:53-58.
17. 2+. Biochem. Biophys. Res. Commun. 2008, 366:401-407.
18. Li F., Liu X., Su Z., Sun R. Acidosis leads to brain dysfunctions through impairing cortical GABAergic neurons. Biochem. Biophys. Res. Commun. 2011, 410:775-779.
19. Beierlein M., Gibson J.R., Connors B.W. A network of electrical coupled interneurons drives synchronized inhibition in neovcortex. Nat. Neurosci. 2000, 3:904-910.
20. Long M.A., Jutras M.J., Connors B.W., Burwell R.D. Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat. Neurosci. 2005, 8:61-66.
21. Fans E.E., low K.A., Richardson, Connors B.W. Selective state-dependent activation of somatostain-expressing inhibitory interneurons in mouse neocortex. J. Neurophysiol. 2008, 100:2640-2652.
22. McBain C.J., Fisahn A. Interneurons unbound. Nat. Rev. Neurosci. 2001, 2:11-23.
23. Somogyi P., Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. (London) 2005, 562:9-29.
24. Wehr M., Zador A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 2003, 426:442-446.
25. Chen N., Chen S.L., Wu Y.L., Wang J.H. The refractory periods and threshold potentials of sequential spikes measured by whole-cell recordings. Biochem. Biophys. Res. Commun. 2006, 340:151-157.
26. Guan S., Ma S., Yan Z., Ge R., Wang Q., Wang J.H. The intrinsic mechanisms underlying the maturation of programming sequential spikes at cerebellar Purkinje cells. Biochem. Biophys. Res. Commun. 2006, 345:175-180.
27. 2+/CaM signalling pathway up-regulates glutamatergic synaptic function in non-pyramidal fast-spiking neurons of hippocampal CA1. J. Physiol. (London) 2001, 533:407-422.
28. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
29. McKay B.E., Turner R.W. Physiological and morphological development of the rat cerebellar Purkinje cell. J. Physiol. (London) 2005, 567(Pt. 3):829-850.
30. Ni H., Huang L., Chen N., Zhang F., Liu D., Ge M., Guan S., Zhu Y., Wang J.H. Upregulation of barrel GABAergic neurons is associated with cross-modal plasticity in olfactory deficit. PLoS ONE 2010, 5:e13736.
31. Wang Q., Liu X., Ge R., Guan S., Zhu Y., Wang J.H. The postnatal development of intrinsic properties and spike encoding at cortical GABAergic neurons. Biochem. Biophys. Res. Commun. 2009, 378:706-710.
32. Ge R., Chen N., Wang J.H. Real-time neuronal homeostasis by coordinating VGSC intrinsic properties. Biochem. Biophys. Res. Commun. 2009, 387:585-589.
33. Ge R., Qian H., Wang J.H. Physiological synaptic signals initiate sequential spikes at soma of cortical pyramidal neurons. Mol. Brain 2011, 4:19.
34. Chen N., Chen X., Yu J., Wang J.-H. After-hyperpolarization improves spike programming through lowering threshold potentials and refractory periods mediated by voltage-gated sodium channels. Biochem. Biophys. Res. Commun. 2006, 346:938-945.
35. Chen N., Zhu Y., Gao X., Guan S., Wang J.-H. Sodium channel-mediated intrinsic mechanisms underlying the differences of spike programming among GABAergic neurons. Biochem. Biophys. Res. Commun. 2006, 346:281-287.
36. Chen N., Chen X., Wang J.-H. Homeostasis established by coordination of subcellular compartment plasticity improves spike encoding. J. Cell Sci. 2008, 121:2961-2971.
37. Chen N., Yu J., Qian H., Ge R., Wang J.H. Axons amplify somatic incomplete spikes into uniform amplitudes in mouse cortical pyramidal neurons. PLoS ONE 2010, 5(7):e11868.
38. Buzsaki G., Eidelberg E. Direct afferent excitation and long-term potentiation of hippocampal interneurons. J. Neurophysiol. 1982, 48:597-607.
39. Congar P., Khazipov R., Ben-Ari Y. Direct demonstration of functional disconnection by anoxia of inhibitory interneurons from excitatory inputs in rat hippocampus. J. Neurophysiol. 1995, 73:421-426.
40. Frerking M., Malenka R.C., Nicoll R.A. Synaptic activation of kainate receptors on hippocampal interneurons. Nat. Neurosci. 1998, 1:479-486.
41. Wang J., Zhang M. Differential modulation of glutamatergic and cholinergic synapses by calcineurin in hippocampal CA1 fast-spiking interneurons. Brain Res. 2004, 1004:125-135.
42. Wang J.-H., Stelzer A. Shared calcium signaling pathways in the induction of long-term potentiation and synaptic disinhibition in CA1 pyramidal cell dendrites. J. Neurophysiol. 1996, 75:1687-1702.
43. 2+-calmodulin signalling pathway upregulates GABA synaptic transmission through cytoskeleton-mediated mechanisms. Neuroscience 2004, 127:637-647.
44. 2+ and acidosis-mediated neuronal injury by intracellular injury. J. Biol. Chem. 2006, 281:29369-29378.
45. Hodgkin A.L., Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 1952, 117:500-544.
46. Hodgkin A.L., Huxley A.F. The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J. Physiol. 1952, 116:497-506.
47. Regehr W.G., Stevens C.F. Physiology of synaptic transmission and short-term plasticity 2001, The Johns Hopkins University Press, Boltimore and London.
48. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Ann. Rev. Physiol. 2002, 25:355-405.
49. Wemmie J.A., Price M.P., Welsh M.J. Acid-sensing ion channels: advances questions and therapeutic opportunities. Trends Neurosci. 2006, 29:578-586.
50. Xiong Z.G., Chu X.P., Simon R.P. Acid sensing ion channels-novel therapeutic targets for ischemic brain injury. Front Biosci 2007, 12:1376-1386.
51. Zha X.M., Wemmie J.A., Green S.H., Welsh M.J. Acid-sensing ion channel 1a is a postsynaptic proton receptor that affects the density of dendritic spines. Proc. Natl. Acad. Sci. USA 2006, 103:16556-16561.
52. 2+ entry via NCX1 in neuron- and glia-derived cells. Cell. Mol. Neurobiol. 2010, 30:453-460.
53. Klee C.B., Means A.R. Keeping up with calcium: conference on calcium-binding proteins and calcium function in health and disease. EMBO Rep. 2002, 3:823-827.