Medial septal dysfunction by Aβ-induced KCNQ channel-block in glutamatergic neurons

Neurobiology of Aging

Volumn 33, Issue 9, 2012, Pages 2046-2061

  Leão, Richardson N ^a,b   Colom, Luis V ^c   Borgius, Lotta ^a   Kiehn, Ole ^a   Fisahn, André ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF TEXAS AT BROWNSVILLE   (United States)

Author keywords

A current; Amyloid peptide; Cholinergic neurons; GABAergic neurons; Glutamatergic neurons; M current; Medial septum; Theta oscillations

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[25-35]; POTASSIUM CHANNEL KCNQ;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DYSFUNCTION; BRAIN NERVE CELL; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DIAGONAL BAND OF BROCA; FEMALE; GABAERGIC TRANSMISSION; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NEGATIVE FEEDBACK; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEPTUM PELLUCIDUM; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; THETA RHYTHM;

ACTION POTENTIALS; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CHOLINE O-ACETYLTRANSFERASE; FEMALE; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; KCNQ POTASSIUM CHANNELS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEINS; RNA, MESSENGER; SEPTUM OF BRAIN; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84863423626     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.07.013     Document Type: Article

References (46)

1. Abeles M. Corticonics: Neural Circuits of the Cerebral Cortex 1991, Cambridge University Press, Cambridge.
2. Bland B.H., Colom L.V. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog. Neurobiol. 1993, 41:157-208.
3. Bland B.H., Declerck S., Jackson J., Glasgow S., Oddie S. Septohippocampal properties of N-methyl-d-aspartate-induced theta-band oscillation and synchrony. Synapse 2007, 61:185-197.
4. Bland B.H., Oddie S.D., Colom L.V. Mechanisms of neural synchrony in the septohippocampal pathways underlying hippocampal theta generation. J. Neurosci. 1999, 19:3223-3237.
5. Borgius L., Restrepo C.E., Leao R.N., Saleh N., Kiehn O. A transgenic mouse line for molecular genetic analysis of excitatory glutamatergic neurons. Mol. Cell. Neurosci. 2010, 45:245-257.
6. Börjesson A., Karlsson T., Adolfsson R., Rönnlund M., Nilsson L. Li- nopirdine (DUP 996): cholinergic treatment of older adults using successive and non-successive tests. Neuropsychobiology 1999, 40:78-85.
7. Brorson J.R., Bindokas V.P., Iwama T., Marcuccilli C.J., Chisholm J.C., Miller R.J. The Ca2+ influx induced by beta-amyloid peptide 25-35 in cultured hippocampal neurons results from network excitation. J. Neurobiol. 1995, 26:325-338.
8. Carre G.P., Harley C.W. Glutamatergic activation of the medial septum complex: an enhancement of the dentate gyrus population spike and accompanying EEG and unit changes. Brain Res 2000, 861:16-25.
9. Chang Z., Luo Y., Zhang Y., Wei G. Interactions of Aβ25-35 β-barrel-like oligomers with anionic lipid bilayer and resulting membrane leakage: an all-atom molecular dynamics study. J. Phys. Chem. B. 2011, 115:1165-1174.
10. Chen C. Beta-Amyloid increases dendritic Ca2+ influx by inhibiting the A-type K+ current in hippocampal CA1 pyramidal neurons. Biochem. Biophys. Res. Commun. 2005, 338:1913-1919.
11. Chin J.H., Ma L., MacTavish D., Jhamandas J.H. Amyloid beta protein modulates glutamate-mediated neurotransmission in the rat basal forebrain: involvement of presynaptic neuronal nicotinic acetylcholine and metabotropic glutamate receptors. J. Neurosci. 2007, 27:9262-9269.
12. Colom L.V. Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease. J. Neurochem. 2006, 96:609-623.
13. Colom L.V., Bland B.H. Medial septal cell interactions in relation to hippocampal field activity and the effects of atropine. Hippocampus 1991, 1:15-30.
14. Colom L.V., Castañeda M.T., Bañuelos C., Puras G., García-Hernández A., Hernandez S., Mounsey S., Benavidez J., Lehker C. Medial septal beta-amyloid 1-40 injections alter septo-hippocampal anatomy and function. Neurobiol. Aging 2010, 31:46-57.
15. Colom L.V., Castaneda M.T., Reyna T., Hernandez S., Garrido-Sanabria E. Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 2005, 58:151-164.
16. Colom L.V., Diaz M.E., Beers D.R., Neely A., Xie W.J., Appel S.H. Role of potassium channels in amyloid-induced cell death. J. Neurochem. 1998, 70:1925-1934.
17. Colom L.V., García-Hernández A., Castañeda M.T., Perez-Cordova M.G., Garrido-Sanabria E.R. Septo-hippocampal networks in chronically epileptic rats: potential antiepileptic effects of theta rhythm generation. J. Neurophysiol. 2006, 95:3645-3653.
18. Good T.A., Smith D.O., Murphy R.M. Beta-amyloid peptide blocks the fast-inactivating K+ current in rat hippocampal neurons. Biophys. J. 1996, 70:296-304.
19. Goodman D., Brette R. Brian: a simulator for spiking neural networks in Python. Frontiers in Neuroinformatics 2008, 2:1-10.
20. Huh C.Y., Danik M., Manseau F., Trudeau L.E., Williams S. Chronic exposure to nerve growth factor increases acetylcholine and glutamate release from cholinergic neurons of the rat medial septum and diagonal band of Broca via mechanisms mediated by p75NTR. J. Neurosci. 2008, 28:1404-1409.
21. Huh C.Y., Goutagny R., Williams S. Glutamatergic neurons of the mouse medial septum and diagonal band of broca synaptically drive hippocampal pyramidal cells: relevance for hippocampal theta rhythm. J. Neurosci. 2010, 30:15951-15961.
22. Hung L.W., Ciccotosto G.D., Giannakis E., Tew D.J., Perez K., Masters C.L., Cappai R., Wade J.D., Barnham K.J. Amyloid-beta peptide (Abeta) neurotoxicity is modulated by the rate of peptide aggregation: Abeta dimers and trimers correlate with neurotoxicity. J. Neurosci. 2008, 28:11950-11958.
23. Jang H., Arce F.T., Ramachandran S., Capone R., Azimova R., Kagan B.L., Nussinov R., Lal R. Truncated beta-amyloid peptide channels provide an alternative mechanism for Alzheimer's Disease and Down syndrome. Proc. Natl. Acad. Sci. USA 2010, 107:6538-6543.
24. Kerrigan T.L., Atkinson L., Peers C., Pearson H.A. Modulation of 'A'-type K+ current by rodent and human forms of amyloid beta protein. Neuroreport 2008, 19:839-843.
25. Klein W.L., Krafft G.A., Finch C.E. Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum?. Trends Neurosci 2001, 24:219-224.
26. Lamas J.A., Selyanko A.A., Brown D.A. Effects of a cognition-enhancer, linopirdine (DuP 996), on M-type potassium currents (IK(M)) and some other voltage- and ligand-gated membrane currents in rat sympathetic neurons. Eur. J. Neurosci. 1997, 9:605-616.
27. Leao K.E., Leao R.N., Sun H., Fyffe R.E., Walmsley B. Hyperpolarization-activated currents are differentially expressed in mice brainstem auditory nuclei. J. Physiol. 2006, 576:849-864.
28. Leão R.N., Tan H.M., Fisahn A. Kv7/KCNQ channels control action potential phasing of pyramidal neurons during hippocampal gamma oscillations in vitro. J. Neurosci. 2009, 29:13353-13364.
29. Leung L.S., Shen B. Glutamatergic synaptic transmission participates in generating the hippocampal EEG. Hippocampus 2004, 14:510-525.
30. Lue L.F., Kuo Y.M., Roher A.E., Brachova L., Shen Y., Sue L., Beach T., Kurth J.H., Rydel R.E., Rogers J. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 1999, 155:853-862.
31. Millucci L., Ghezzi L., Bernardini G., Santucci A. Conformations and biological activities of amyloid beta peptide 25-35. Curr. Protein Pept. Sci. 2010, 11:54-67.
32. Nerelius C., Sandegren A., Sargsyan H., Raunak R., Leijonmarck H., Chatterjee U., Fisahn A., Imarisio S., Lomas D.A., Crowther D.C., Strömberg R., Johansson J. Alpha-helix targeting reduces amyloid-beta peptide toxicity. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9191-9196.
33. Nevian T., Helmchen F. Calcium indicator loading of neurons using single-cell electroporation. Pflugers Arch 2007, 454:675-688.
34. Nimmrich V., Grimm C., Draguhn A., Barghorn S., Lehmann A., Schoemaker H., Hillen H., Gross G., Ebert U., Bruehl C. Amyloid beta oligomers (A beta(1-42) globulomer) suppress spontaneous synaptic activity by inhibition of P/Q-type calcium currents. J. Neurosci. 2008, 28:788-797.
35. Peña F., Ordaz B., Balleza-Tapia H., Bernal-Pedraza R., Márquez-Ramos A., Carmona-Aparicio L., Giordano M. Beta-amyloid protein (25-35) disrupts hippocampal network activity: role of Fyn-kinase. Hippocampus 2010, 20:78-96.
36. Peters H.C., Hu H., Pongs O., Storm J.F., Isbrandt D. Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat. Neurosci. 2005, 8:51-60.
37. Rockwood K., Beattie B.L., Eastwood M.R., Feldman H., Mohr E., Pryse-Phillips W., Gauthier S. A randomized, controlled trial of linopirdine in the treatment of Alzheimer's disease. Can. J. Neurol. Sci. 1997, 24:140-145.
38. Romero M., Reboreda A., Sánchez E., Lamas J.A. Newly developed blockers of the M-current do not reduce spike frequency adaptation in cultured mouse sympathetic neurons. Eur. J. Neurosci. 2004, 19:2693-2702.
39. Rothman J.S., Manis P.B. Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. J. Neurophysiol. 2003, 89:3083-3096.
40. Ryan D.A., Narrow W.C., Federoff H.J., Bowers W.J. An improved method for generating consistent soluble amyloid-beta oligomer preparations for in vitro neurotoxicity studies. J. Neurosci. Methods 2010, 190:171-179.
41. Santos-Torres J., Fuente A., Criado J.M., Riolobos A.S., Heredia M., Yajeya J. Glutamatergic synaptic depression by synthetic amyloid beta-peptide in the medial septum. J. Neurosci. Res. 2007, 85:634-648.
42. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., Regan C.M., Walsh D.M., Sabatini B.L., Selkoe D.J. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 2008, 14:837-842.
43. Sotty F., Danik M., Manseau F., Laplante F., Quirion R., Williams S. Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J. Physiol. 2003, 551:927-943.
44. Trappenberg T.P. Fundamentals of Computational Neuroscience 2002, Oxford University Press, Oxford.
45. Ujfalussy B., Kiss T. How do glutamatergic and GABAergic cells contribute to synchronization in the medial septum?. J. Comput. Neurosci. 2006, 21:343-357.
46. Vinogradova O.S. Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog. Neurobiol. 1995, 45:523-583.