PIP2-mediated HCN3 channel gating is crucial for rhythmic burst firing in thalamic intergeniculate leaflet neurons

Journal of Neuroscience

Volumn 31, Issue 28, 2011, Pages 10412-10423

  Ying, Shui Wang ^a   Tibbs, Gareth R ^a   Picollo, Alessandra ^a   Abbas, Syed Y ^a   Lea Sanford, R ^a   Accardi, Alessio ^a   Hofmann, Franz ^b   Ludwig, Andreas ^a   Goldstein, Peter A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL 1; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL 2; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL 3; ION CHANNEL; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; ARTICLE; CHANNEL GATING; CIRCADIAN RHYTHM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GENICULATE NUCLEUS; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; ION CURRENT; MOUSE; NERVE CELL EXCITABILITY; NERVE FIBER MEMBRANE POTENTIAL; NONHUMAN; OSCILLATION; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SLEEP; THALAMUS;

ANIMALS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; ION CHANNEL GATING; MEMBRANE POTENTIALS; MICE; NEURONS; PATCH-CLAMP TECHNIQUES; PERIODICITY; PHOSPHOINOSITIDE PHOSPHOLIPASE C; RATS; THALAMUS;

EID: 79960387024     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0021-11.2011     Document Type: Article

References (62)

1. Abbas SY, Ying SW, Goldstein PA (2006) Compartmental distribution of hyperpolarization-activated cyclic-nucleotide-gated channel 2 and hyperpolarization-activated cyclic-nucleotide-gated channel 4 in thalamic reticular and thalamocortical relay neurons. Neuroscience 141:1811-1825.
2. Atherton JF, Kitano K, Baufreton J, Fan K, Wokosin D, Tkatch T, Shigemoto R, Surmeier DJ, Bevan MD (2010) Selective participation of somatodendriticHCNchannels in inhibitory but not excitatory synaptic integration in neurons of the subthalamic nucleus. J Neurosci 30:16025-16040.
3. Bal T, McCormick DA (1997) Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current Ih. J Neurophysiol 77:3145-3156.
4. Balla A, Balla T (2006) Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol 16:351-361.
5. Bessaïh T, Leresche N, Lambert RC (2008) Tcurrent potentiation increases the occurrence and temporal fidelity of synaptically evoked burst firing in sensory thalamic neurons. Proc Natl Acad Sci U S A 105:11376-11381.
6. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarizationactivated cation channels: from genes to function. Physiol Rev 89:847-885.
7. Blasiak A, Blasiak T, Lewandowski MH (2009) Electrophysiology and pharmacology of the optic input to the rat intergeniculate leaflet in vitro. J Physiol Pharmacol 60:171-180.
8. Cain SW, Verwey M, Szybowska M, Ralph MR, Yeomans JS (2007) Carbachol injections into the intergeniculate leaflet induce nonphotic phase shifts. Brain Res 1177:59-65.
9. Card JP, Moore RY (1989) Organization of lateral geniculate-hypothalamic connections in the rat. J Comp Neurol 284:135-147.
10. Chu Z, Takagi H, Moenter SM (2010) Hyperpolarization-activated currents in gonadotropin-releasing hormone (GnRH) neurons contribute to intrinsic excitability and are regulated by gonadal steroid feedback. J Neurosci 30:13373-13383.
11. del Pilar Gomez M, Nasi E (2005) A direct signaling role for phosphatidylinositol 4,5-bisphosphate (PIP2) in the visual excitation process of microvillar receptors. J Biol Chem 280:16784-16789.
12. Dembrow NC, Chitwood RA, Johnston D (2010) Projection-specific neuromodulation of medial prefrontal cortex neurons. J Neurosci 30:16922-16937.
13. Doughman RL, Firestone AJ, Anderson RA (2003) Phosphatidylinositol phosphate kinases put PI4,5P(2) in its place. J Membr Biol 194:77-89.
14. Fogle KJ, Lyashchenko AK, Turbendian HK, Tibbs GR (2007) HCN pacemaker channel activation is controlled by acidic lipids downstream of diacylglycerol kinase and phospholipase A2. J Neurosci 27:2802-2814.
15. Franklin KBJ, Paxinos G (2007) The mouse brain in stereotaxic coordinates, Ed 3. New York: Academic.
16. Frère SG, Lüthi A (2004) Pacemaker channels in mouse thalamocortical neurones are regulated by distinct pathways of cAMP synthesis. J Physiol 554:111-125.
17. Frère SG, Kuisle M, Lüthi A (2004) Regulation of recombinant and native hyperpolarization-activated cation channels. Mol Neurobiol 30:279-305.
18. Gauss R, Seifert R (2000) Pacemaker oscillations in heart and brain: a key role for hyperpolarization-activated cation channels. Chronobiol Int 17:453-469.
19. +channels. Nat Neurosci 12:577-584.
20. Goulding EH, Tibbs GR, Liu D, Siegelbaum SA (1993) Role of H5 domain in determining pore diameter and ion permeation through cyclic nucleotide-gated channels. Nature 364:61-64.
21. Herrmann S, Stieber J, Ludwig A (2007) Pathophysiology ofHCNchannels. Pflugers Arch 454:517-522.
22. + current in rat hippocampal pyramidal cells. J Physiol 545:783-805.
23. Lanzafame AA, Christopoulos A, Mitchelson F (2003) Cellular signaling mechanisms for muscarinic acetylcholine receptors. Receptors Channels 9:241-260.
24. Ludwig A, Budde T, Stieber J, Moosmang S, Wahl C, Holthoff K, Langebartels A, Wotjak C, Munsch T, Zong X, Feil S, Feil R, Lancel M, Chien KR, Konnerth A, Pape HC, Biel M, Hofmann F (2003) Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 22:216-224.
25. Lüthi A, Bal T, McCormick DA (1998) Periodicity of thalamic spindle waves is abolished by ZD7288,a blocker of Ih. J Neurophysiol 79:3284-3289.
26. 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.
27. Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
28. Magee JC (1999) Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2:508-514.
29. McCormick DA, Pape HC (1990) Properties of a hyperpolarizationactivated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol 431:291-318.
30. Meurers BH, Dziewczapolski G, Bittner A, Shi T, Kamme F, Shults CW (2009) Dopamine depletion induced up-regulation of HCN3 enhances rebound excitability of basal ganglia output neurons. Neurobiol Dis 34:178-188.
31. Mistrík P, Mader R, Michalakis S, Weidinger M, Pfeifer A, Biel M (2005) The murine HCN3 gene encodes a hyperpolarization-activated cation channel with slow kinetics and unique response to cyclic nucleotides. J Biol Chem 280:27056-27061.
32. Moore RY, Card JP (1994) Intergeniculate leaflet: an anatomically and functionally distinct subdivision of the lateral geniculate complex. J Comp Neurol 344:403-430.
33. Morin LP, Allen CN (2006) The circadian visual system, 2005. Brain Res Rev 51:1-60.
34. Morin LP, Blanchard J, Moore RY (1992) Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the golden hamster. Vis Neurosci 8:219-230.
35. Much B, Wahl-Schott C, Zong X, Schneider A, Baumann L, Moosmang S, Ludwig A, Biel M (2003) Role of subunit heteromerization andN-linked glycosylation in the formation of functional hyperpolarization-activated cyclic nucleotide-gated channels. J Biol Chem 278:43781-43786.
36. Nakanishi S, Catt KJ, Balla T (1995) A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositolphospholipids. Proc Natl Acad Sci U S A 92:5317-5321.
37. Neuhoff H, Neu A, Liss B, Roeper J (2002) Ih channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22:1290-1302.
38. Nolan MF, Malleret G, Lee KH, Gibbs E, Dudman JT, Santoro B, Yin D, Thompson RF, Siegelbaum SA, Kandel ER, Morozov A (2003) The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell 115:551-564.
39. Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E, Vronskaya S, Buzsáki G, Siegelbaum SA, Kandel ER, Morozov A (2004) A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119:719-732.
40. Notomi T, Shigemoto R (2004) Immunohistochemical localization of Ih channel subunits,HCN1-4, in the rat brain. JCompNeurol 471:241-276.
41. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. New York: Academic.
42. Pian P, Bucchi A, Robinson RB, Siegelbaum SA (2006) Regulation of gating and rundown of HCN hyperpolarization-activated channels by exogenous and endogenous PIP2. J Gen Physiol 128:593-604.
43. Pian P, Bucchi A, Decostanzo A, Robinson RB, Siegelbaum SA (2007) Modulation of cyclic nucleotide-regulated HCN channels by PIP2 and receptors coupled to phospholipase C. Pflügers Arch 455:125-145.
44. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453-480.
45. Saitow F, Konishi S (2000) Excitability increase induced by β-adrenergic receptor-mediated activation of hyperpolarization-activated cation channels in rat cerebellar basket cells. J Neurophysiol 84:2026-2034.
46. Santoro B, Chen S, Lüthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA (2000) Molecular and functional heterogeneity of hyperpolarizationactivated pacemaker channels in the mouse CNS. J Neurosci 20:5264-5275.
47. Sasaki T, Takasuga S, Sasaki J, Kofuji S, Eguchi S, Yamazaki M, Suzuki A (2009) Mammalian phosphoinositide kinases and phosphatases. Prog Lipid Res 48:307-343.
48. Stieber J, Stöckl G, Herrmann S, Hassfurth B, Hofmann F (2005) Functional expression of the human HCN3 channel. J Biol Chem 280:34635-34643.
49. Suh BC, Hille B (2008) PIP2 is a necessary cofactor for ion channel function: how and why? Annu Rev Biophys 37:175-195.
50. Surges R, Freiman TM, Feuerstein TJ (2004) Input resistance is voltage dependent due to activation of Ih channels in rat CA1 pyramidal cells. J Neurosci Res 76:475-480.
51. Szkudlarek HJ, Raastad M (2007) Electrical properties of morphologically characterized neurons in the intergeniculate leaflet of the rat thalamus. Neuroscience 150:309-318.
52. Thankachan S, Rusak B (2005) Juxtacellular recording/labeling analysis of physiological and anatomical characteristics of rat intergeniculate leaflet neurons. J Neurosci 25:9195-9204.
53. Wainger BJ, DeGennaro M, Santoro B, Siegelbaum SA, Tibbs GR (2001) Molecular mechanism of cAMP modulation of HCN pacemaker channels. Nature 411:805-810.
54. Werhun K, Lewandowski MH (2009) The effects of muscarinic cholinergic receptor antagonist on slow bursting neuronal activity in the rat intergeniculate leaflet. Folia Biol (Krakow) 57:187-192.
55. Wicks NL, Wong T, Sun J, Madden Z, Young EC (2011) Cytoplasmic cAMP-sensing domain of hyperpolarization-activated cation (HCN) channels uses two structurally distinct mechanisms to regulate voltage gating. Proc Natl Acad Sci U S A 108:609-614.
56. Williams SR, Stuart GJ (2000) Site independence of EPSP time course is mediated by dendritic Ih in neocortical pyramidal neurons. J Neurophysiol 83:3177-3182.
57. Ying SW, Goldstein PA (2005) Propofol-block of SK channels in reticular thalamic neurons enhances GABAergic inhibition in relay neurons. J Neurophysiol 93:1935-1948.
58. Ying SW, Zhang DX, Rusak B (1993) Effects of serotonin agonists and melatonin on photic responses of hamster intergeniculate leaflet neurons. Brain Res 628:8-16.
59. Ying SW, Abbas SY, Harrison NL, Goldstein PA (2006) Propofol block of Ih contributes to the suppression of neuronal excitability and rhythmic burst firing in thalamocortical neurons. Eur J Neurosci 23:465-480.
60. Ying SW, Abbas SY, Goldstein PA (2007a) HCN3 channels contribute to Ih in thalamic IGL neurons. Soc Neurosci Abstr 33:467.7.
61. Ying SW, Jia F, Abbas SY, Hofmann F, Ludwig A, Goldstein PA (2007b) Dendritic HCN2 channels constrain glutamate-driven excitability in reticular thalamic neurons. J Neurosci 27:8719-8732.
62. Zolles G, Klöcker N, Wenzel D, Weisser-Thomas J, Fleischmann BK, Roeper J, Fakler B (2006) Pacemaking by HCN channels requires interaction with phosphoinositides. Neuron 52:1027-1036.