Nicotine blocks the hyperpolarization-activated current Ih and severely impairs the oscillatory behavior of oriens-lacunosum moleculare interneurons

Journal of Neuroscience

Volumn 30, Issue 32, 2010, Pages 10773-10783

  Griguoli, Marilena ^a   Maul, Alena ^a   Nguyen, Chuong ^b   Giorgetti, Alejandro ^c   Carloni, Paolo ^b   Cherubini, Enrico ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b SISSA   (Italy)

^c UNIVERSITY OF VERONA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; ENHANCED GREEN FLUORESCENT PROTEIN; EPIBATIDINE; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT IH; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; SOMATOSTATIN; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; 8 BROMO CYCLIC AMP; AMINO ACID RECEPTOR BLOCKING AGENT; CARDIOVASCULAR AGENT; CYCLIC NUCLEOTIDE GATED CHANNEL; DIHYDRO BETA ERYTHROIDINE; FORSKOLIN; GREEN FLUORESCENT PROTEIN; HYPERPOLARIZATION ACTIVATED CATION CHANNEL; HYPERPOLARIZATION-ACTIVATED CATION CHANNEL; ICI D2788; MECAMYLAMINE; NICOTINIC AGENT; POTASSIUM CHANNEL; PYRIMIDINE DERIVATIVE;

ANIMAL TISSUE; ARTICLE; BRAIN; COGNITION; CONTROLLED STUDY; DENDRITE; DEPOLARIZATION; DRUG PROTEIN BINDING; FEMALE; HYPERPOLARIZATION; INTERNEURON; MALE; MOLECULAR MODEL; MOUSE; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SMOKING; SPIKE; TOBACCO; TRANSGENIC MOUSE; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; CHEMICAL STRUCTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; ELECTROSTIMULATION; GENETICS; HIPPOCAMPUS; IN VITRO STUDY; METABOLISM; METHODOLOGY; NERVE CELL INHIBITION; PATCH CLAMP; PHYSIOLOGY;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; BIOLOGICAL CLOCKS; CARDIOVASCULAR AGENTS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DIHYDRO-BETA-ERYTHROIDINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; FORSKOLIN; GAMMA-AMINOBUTYRIC ACID; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; INTERNEURONS; MALE; MECAMYLAMINE; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MODELS, MOLECULAR; NEURAL INHIBITION; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; PYRIMIDINES; SOMATOSTATIN;

EID: 77956217435     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2446-10.2010     Document Type: Article

References (61)

1. Ali AB, Thomson AM (1998) Facilitating pyramid to horizontal oriensalveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol 507:185-199.
2. Badio B, Daly JW (1994) Epibatidine, a potent analgetic and nicotinic agonist. Mol Pharmacol 45:563-569.
3. Benowitz NL, Jacob P 3rd, Yu L (1989) Daily use of smokeless tobacco: systemic effects. Ann Intern Med 111:112-116.
4. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarization- activated cation channels: from genes to function. Physiol Rev 89:847-885.
5. BoSmith RE, Briggs I, Sturgess NC (1993) Inhibitory actions of ZENECA ZD 7288 on whole-cell hyperpolarization activated inward current (If) in guinea-pig dissociated sino atrial node cells. Br J Pharmacol 110:343-349.
6. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.
7. Carryl OR, Gallardo-Carpentier A, Carpentier RG (1992) Effects of nicotine and ethanol on rat atrial membrane potentials. Alcohol 9:87-92.
8. Cheng L, Kinard K, Rajamani R, Sanguinetti MC (2007) Molecular mapping of the binding site for a blocker of hyperpolarization-activated, cyclic nucleotide-modulated pacemaker channels. J Pharmacol Exp Ther 322:931-939.
9. Cossart R, Petanjek Z, Dumitriu D, Hirsch JC, Ben-Ari Y, Esclapez M, Bernard C (2006) Interneurons targeting similar layers receive synaptic inputs with similar kinetics. Hippocampus 16:408-420.
10. Dugladze T, Vida I, Tort AB, Gross A, Otahal J, Heinemann U, Kopell NJ, Gloveli T (2007) Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc Natl Acad Sci U S A 104:17530-17535.
11. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
12. Frotscher M, Léránth C (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J Comp Neurol 239:237-246.
13. h) in rat CA1 hippocampal neurons. Eur J Neurosci 11:3093-3100.
14. Gillies MJ, Traub RD, LeBeau FE, Davies CH, Gloveli T, Buhl EH, Whittington MA (2002) A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol 543:779-793.
15. Giorgetti A, Carloni P, Mistrik P, Torre V (2005) A homology model of the pore region of HCN channels. Biophys J 89:932-944.
16. Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD, Whittington MA, Buhl EH (2005) Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol 562:131-147.
17. Goldin M, Epsztein J, Jorquera I, Represa A, Ben-Ari Y, Crépel V, Cossart R (2007) Synaptic kainate receptors tune oriens-lacunosum moleculare interneurons to operate at theta frequency. J Neurosci 27:9560-9572.
18. Good CH, Bay KD, Buchanan RA, McKeon KA, Skinner RD, Garcia-Rill E (2006) Prenatal exposure to cigarette smoke affects the physiology of pedunculopontine nucleus (PPN) neurons in development. Neurotoxicol Teratol 28:210-219.
19. Greenspan K, Edmands RE, Knoebel SB, Fisch C (1969) Some effects of nicotine on cardiac automaticity, conduction, and inotropy. Arch Intern Med 123:707-712.
20. Griguoli M, Scuri R, Ragozzino D, Cherubini E (2009) Activation of nicotinic acetylcholine receptors enhances a slow calcium-dependent potassium conductance and reduces the firing of stratum oriens interneurons. Eur J Neurosci 30:1011-1022.
21. Hájos N, Pálhalmi J, Mann EO, Németh B, Paulsen O, Freund TF (2004) Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J Neurosci 24:9127-9137.
22. Hestrin S, Galarreta M (2005) Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci 28:304-309.
23. + current in rat hippocampal pyramidal cells. J Physiol 545:783-805.
24. Hutcheon B, Yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23:216-222.
25. Janigro D, Martenson ME, Baumann TK (1997) Preferential inhibition of Ih in rat trigeminal ganglion neurons by an organic blocker. J Membr Biol 160:101-109.
26. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002) Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417:515-522.
27. Kanyshkova T, Pawlowski M, Meuth P, Dubé C, Bender RA, Brewster AL, Baumann A, Baram TZ, Pape HC, Budde T (2009) Postnatal expression pattern of HCN channel isoforms in thalamic neurons: relationship to maturation of thalamocortical oscillations. J Neurosci 29:8847-8857.
28. Kilb W, Luhmann HJ (2000) Characterization of a hyperpolarization- activated inward current in Cajal-Retzius cells in rat neonatal neocortex. J Neurophysiol 84:1681-1691.
29. Klausberger T, Magill PJ, Márton LF, Roberts JD, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-848.
30. Klausberger T, Márton LF, Baude A, Roberts JD, Magill PJ, Somogyi P (2004) Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7:41-47.
31. Lacaille JC, Mueller AL, Kunkel DD, Schwartzkroin PA (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7:1979-1993.
32. Lawrence JJ, Grinspan ZM, Statland JM, McBain CJ (2006) Muscarinic receptor activation tunes mouse stratum oriens interneurones to amplify spike reliability. J Physiol 571:555-562.
33. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsáki G (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033-1047.
34. Levey AI, Edmunds SM, Koliatsos V, Wiley RG, Heilman CJ (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 15:4077-4092.
35. Lupica CR, Bell JA, Hoffman AF, Watson PL (2001) Contribution of the hyperpolarization-activated current I(h) to membrane potential and GABA release in hippocampal interneurons. J Neurophysiol 86:261-268.
36. Maccaferri G (2005) Stratum oriens horizontal interneurone diversity and hippocampal network dynamics. J Physiol 562:73-80.
37. Maccaferri G, McBain CJ (1996) The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497:119-130.
38. Maccaferri G, Roberts JD, Szucs P, Cottingham CA, Somogyi P (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J Physiol 524:91-116.
39. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11-23.
40. McBain CJ, DiChiara TJ, Kauer JA (1994) Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14:4433-4445.
41. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
42. Minneci F, Janahmadi M, Migliore M, Dragicevic N, Avossa D, Cherubini E (2007) Signaling properties of stratum oriens interneurons in the hippocampus of transgenic mice expressing EGFP in a subset of somatostatin-containing cells. Hippocampus 17:538-553.
43. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 19:1639-1662.
44. Narayanan R, Johnston D (2007) Long-term potentiation in rat hippocampal neurons is accompanied by spatially widespread changes in intrinsic oscillatory dynamics and excitability. Neuron 56:1061-1075.
45. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20:3354-3368.
46. Pappano AJ, Rembish RA (1970) Nicotine-induced restoration of action potentials to cardiac tissue depolarized by potassium. Life Sci I 9:1381-1388.
47. Pedarzani P, Storm JF (1995) Protein kinase A-independent modulation of ion channels in the brain by cyclic AMP. Proc Natl Acad Sci U S A 92:11716-11720.
48. Pike FG, Goddard RS, Suckling JM, Ganter P, Kasthuri N, Paulsen O (2000) Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents. J Physiol 529:205-213.
49. Puil E, Gimbarzevsky B, Miura RM (1986) Quantification of membrane properties of trigeminal root ganglion neurons in guinea pigs. J Neurophysiol 55:995-1016.
50. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453-480.
51. Santoro B, Liu DT, Yao H, Bartsch D, Kandel ER, Siegelbaum SA, Tibbs GR (1998) Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain. Cell 93:717-729.
52. Satoh H (1997) Effects of nicotine on spontaneous activity and underlying ionic currents in rabbit sinoatrial nodal cells. Gen Pharmacol 28:39-44.
53. Somogyi P, Klausberger T (2005) Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol 562:9-26.
54. + channel currents in vascular smooth muscle cells from rat tail arteries. Eur J Pharmacol 364:247-254.
55. Tribollet E, Bertrand D, Marguerat A, Raggenbass M (2004) Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain. Neuroscience 124:405-420.
56. Varanda WA, Aracava Y, Sherby SM, VanMeter WG, Eldefrawi ME, Albuquerque EX (1985) The acetylcholine receptor of the neuromuscular junction recognizes mecamylamine as a noncompetitive antagonist. Mol Pharmacol 28:128-137.
57. + channels. Effects on cloned Kv4.3 channels and native transient outward current. Circulation 102:1165-1171.
58. Wang H, Yang B, Zhang L, Xu D, Wang Z (2000b) Direct block of inward rectifier potassium channels by nicotine. Toxicol Appl Pharmacol 164:97-101.
59. Whittington MA, Traub RD (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676-682.
60. Zemankovics R, Káli S, Paulsen O, Freund TF, Hájos N (2010) Differences in subthreshold resonance of hippocampal pyramidal cells and interneurons: the role of h-current and passive membrane characteristics. J Physiol 588:2109-2132.
61. Zsiros V, Maccaferri G (2005) Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J Neurosci 25:8686-8695.