Ih current is necessary to maintain normal dopamine fluctuations and sleep consolidation in drosophila

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Gonzalo Gomez, Alicia ^a   Turiegano, Enrique ^a   León, Yolanda ^a   Molina, Isabel ^a   Torroja, Laura ^a   Canal, Inmaculada ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC NUCLEOTIDE GATED CHANNEL; DOPAMINE; DROSOPHILA PROTEIN; ION CHANNEL;

ARTICLE; CIRCADIAN RHYTHM; DMLH GENE; DOPAMINE METABOLISM; DROSOPHILA MELANOGASTER; GENE; GENETIC CODE; HEART ELECTROPHYSIOLOGY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LH CURRENT; LIGHT DARK CYCLE; MAMMAL; MUTANT; NONHUMAN; SLEEP CONSOLIDATION; SLEEP PARAMETERS; WILD TYPE; ANIMAL; ANIMAL BEHAVIOR; DARKNESS; GENE DELETION; GENETICS; METABOLISM; PHYSIOLOGY; RADIATION EXPOSURE; SLEEP;

DROSOPHILA MELANOGASTER; MAMMALIA;

ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; DARKNESS; DOPAMINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE DELETION; ION CHANNELS; SLEEP;

EID: 84860531905     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036477     Document Type: Article

References (73)

1. Thollon C, Vilaine J-P, (2010) I(f) inhibition in cardiovascular diseases. Adv Pharmacol 59: 53-92 doi:10.1016/S1054-3589(10)59003-3.
2. Baruscotti M, Bottelli G, Milanesi R, DiFrancesco JC, DiFrancesco D, (2010) HCN-related channelopathies. Pflugers Arch 460: 405-415 doi:10.1007/s00424-010-0810-8.
3. Lewis AS, Chetkovich DM, (2011) HCN channels in behavior and neurological disease: too hyper or not active enough? Mol Cell Neurosci 46: 357-367 doi:10.1016/j.mcn.2010.11.007.
4. Shi W, Wymore R, Yu H, Wu J, Wymore RT, et al. (1999) Distribution and prevalence of hyperpolarization-activated cation channel (HCN) mRNA expression in cardiac tissues. Circ Res 85: e1-6.
5. Herrmann S, Stieber J, Ludwig A, (2007) Pathophysiology of HCN channels. Pflugers Arch 454: 517-522 doi:10.1007/s00424-007-0224-4.
6. Stieber J, Wieland K, Stöckl G, Ludwig A, Hofmann F, (2006) Bradycardic and proarrhythmic properties of sinus node inhibitors. Mol Pharmacol 69: 1328-1337 doi:10.1124/mol.105.020701.
7. Gisselmann G, Gamerschlag B, Sonnenfeld R, Marx T, Neuhaus EM, et al. (2005) Variants of the Drosophila melanogaster Ih-channel are generated by different splicing. Insect Biochem Mol Biol 35: 505-514 doi:10.1016/j.ibmb.2005.02.001.
8. Neuhoff H, Neu A, Liss B, Roeper J, (2002) I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 22: 1290-1302.
9. Puopolo M, Raviola E, Bean BP, (2007) Roles of subthreshold calcium current and sodium current in spontaneous firing of mouse midbrain dopamine neurons. J Neurosci 27: 645-656 doi:10.1523/JNEUROSCI.4341-06.2007.
10. Zolles G, Klöcker N, Wenzel D, Weisser-Thomas J, Fleischmann BK, et al. (2006) Pacemaking by HCN channels requires interaction with phosphoinositides. Neuron 52: 1027-1036 doi:10.1016/j.neuron.2006.12.005.
11. Seutin V, Massotte L, Renette MF, Dresse A, (2001) Evidence for a modulatory role of Ih on the firing of a subgroup of midbrain dopamine neurons. Neuroreport 12: 255-258.
12. Chan CS, Shigemoto R, Mercer JN, Surmeier DJ, (2004) HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J Neurosci 24: 9921-9932 doi:10.1523/JNEUROSCI.2162-04.2004.
13. Arencibia-Albite F, Paladini C, Williams JT, Jiménez-Rivera CA, (2007) Noradrenergic modulation of the hyperpolarization-activated cation current (Ih) in dopamine neurons of the ventral tegmental area. Neuroscience 149: 303-314 doi:10.1016/j.neuroscience.2007.08.009.
14. Liu Z, Bunney EB, Appel SB, Brodie MS, (2003) Serotonin reduces the hyperpolarization-activated current (Ih) in ventral tegmental area dopamine neurons: involvement of 5-HT2 receptors and protein kinase C. J Neurophysiol 90: 3201-3212 doi:10.1152/jn.00281.2003.
15. Vandecasteele M, Glowinski J, Deniau J-M, Venance L, (2008) Chemical transmission between dopaminergic neuron pairs. Proc Natl Acad Sci U S A 105: 4904-4909 doi:10.1073/pnas.0703121105.
16. Cathala L, Paupardin-Tritsch D, (1999) Effect of catecholamines on the hyperpolarization-activated cationic Ih and the inwardly rectifying potassium I(Kir) currents in the rat substantia nigra pars compacta. Eur J Neurosci 11: 398-406.
17. Cathala L, Paupardin-Tritsch D, (1997) Neurotensin inhibition of the hyperpolarization-activated cation current (Ih) in the rat substantia nigra pars compacta implicates the protein kinase C pathway. J Physiol (Lond) 503 (Pt 1): 87-97.
18. Okamoto T, Harnett MT, Morikawa H, (2006) Hyperpolarization-activated cation current (Ih) is an ethanol target in midbrain dopamine neurons of mice. J Neurophysiol 95: 619-626 doi:10.1152/jn.00682.2005.
19. Brodie MS, Appel SB, (1998) The effects of ethanol on dopaminergic neurons of the ventral tegmental area studied with intracellular recording in brain slices. Alcohol Clin Exp Res 22: 236-244.
20. Arnsten AFT, (2007) Catecholamine and second messenger influences on prefrontal cortical networks of "representational knowledge": a rational bridge between genetics and the symptoms of mental illness. Cereb Cortex 17 (Suppl 1): i6-15 doi:10.1093/cercor/bhm033.
21. Chan CS, Glajch KE, Gertler TS, Guzman JN, Mercer JN, et al. (2011) HCN channelopathy in external globus pallidus neurons in models of Parkinson's disease. Nat Neurosci 14: 85-92 doi:10.1038/nn.2692.
22. Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, et al. (2007) "Rejuvenation" protects neurons in mouse models of Parkinson's disease. Nature 447: 1081-1086 doi:10.1038/nature05865.
23. Chu H, Zhen X, (2010) Hyperpolarization-activated, cyclic nucleotide-gated (HCN) channels in the regulation of midbrain dopamine systems. Acta Pharmacol Sin 31: 1036-1043 doi:10.1038/aps.2010.105.
24. Marx T, Gisselmann G, Störtkuhl KF, Hovemann BT, Hatt H, (1999) Molecular cloning of a putative voltage- and cyclic nucleotide-gated ion channel present in the antennae and eyes of Drosophila melanogaster. Invert Neurosci 4: 55-63 doi:10.1007/s101589900006.
25. Dzirasa K, Ribeiro S, Costa R, Santos LM, Lin S-C, et al. (2006) Dopaminergic control of sleep-wake states. J Neurosci 26: 10577-10589 doi:10.1523/JNEUROSCI.1767-06.2006.
26. Kume K, Kume S, Park SK, Hirsh J, Jackson FR, (2005) Dopamine is a regulator of arousal in the fruit fly. J Neurosci 25: 7377-7384 doi:25/32/7377.
27. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, et al. (2004) Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36: 288-292 doi:10.1038/ng1312.
28. Borycz J, Borycz JA, Kubów A, Lloyd V, Meinertzhagen IA, (2008) Drosophila ABC transporter mutants white, brown and scarlet have altered contents and distribution of biogenic amines in the brain. J Exp Biol 211: 3454-3466 doi:10.1242/jeb.021162.
29. Castañeda TR, de Prado BM, Prieto D, Mora F, (2004) Circadian rhythms of dopamine, glutamate and GABA in the striatum and nucleus accumbens of the awake rat: modulation by light. J Pineal Res 36: 177-185.
30. Sleipness EP, Jansen HT, Schenk JO, Sorg BA, (2008) Time-of-day differences in dopamine clearance in the rat medial prefrontal cortex and nucleus accumbens. Synapse 62: 877-885 doi:10.1002/syn.20552.
31. Ceriani MF, Hogenesch JB, Yanovsky M, Panda S, Straume M, et al. (2002) Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J Neurosci 22: 9305-9319.
32. Keegan KP, Pradhan S, Wang J-P, Allada R, (2007) Meta-analysis of Drosophila circadian microarray studies identifies a novel set of rhythmically expressed genes. PLoS Comput Biol 3: e208 doi:10.1371/journal.pcbi.0030208.
33. Andretic R, Hirsh J, (2000) Circadian modulation of dopamine receptor responsiveness in Drosophila melanogaster. Proc Natl Acad Sci U S A 97: 1873-1878 doi:PMC26529.
34. Hirsh J, Riemensperger T, Coulom H, Iché M, Coupar J, et al. (2010) Roles of dopamine in circadian rhythmicity and extreme light sensitivity of circadian entrainment. Curr Biol 20: 209-214 doi:10.1016/j.cub.2009.11.037.
35. Hood S, Cassidy P, Cossette M-P, Weigl Y, Verwey M, et al. (2010) Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J Neurosci 30: 14046-14058 doi:10.1523/JNEUROSCI.2128-10.2010.
36. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, et al. (2000) Rest in Drosophila is a sleep-like state. Neuron 25: 129-138.
37. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G, (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287: 1834-1837.
38. Andretic R, Kim Y-C, Jones FS, Han K-A, Greenspan RJ, (2008) Drosophila D1 dopamine receptor mediates caffeine-induced arousal. Proc Natl Acad Sci USA 105: 20392-20397 doi:10.1073/pnas.0806776105.
39. Zhang YQ, Friedman DB, Wang Z, Woodruff E, Pan L, et al. (2005) Protein expression profiling of the drosophila fragile X mutant brain reveals up-regulation of monoamine synthesis. Mol Cell Proteomics 4: 278-290 doi:10.1074/mcp.M400174-MCP200.
40. Bushey D, Tononi G, Cirelli C, (2009) The Drosophila fragile X mental retardation gene regulates sleep need. J Neurosci 29: 1948-1961 doi:10.1523/JNEUROSCI.4830-08.2009.
41. Lebestky T, Chang J-SC, Dankert H, Zelnik L, Kim Y-C, et al. (2009) Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64: 522-536 doi:10.1016/j.neuron.2009.09.031.
42. Andretic R, van Swinderen B, Greenspan RJ, (2005) Dopaminergic modulation of arousal in Drosophila. Curr Biol 12;15 (13): 1165-7543 doi:10.1016/j.cub.2005.05.025.
43. Bainton RJ, Tsai LT, Singh CM, Moore MS, Neckameyer WS, et al. (2000) Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr Biol 10: 187-194 doi:10704411.
44. Koh K, Evans JM, Hendricks JC, Sehgal A, (2006) A Drosophila model for age-associated changes in sleep:wake cycles. Proc Natl Acad Sci USA 103: 13843-13847 doi:10.1073/pnas.0605903103.
45. Parashar V, Frankel S, Lurie AG, Rogina B, (2008) The effects of age on radiation resistance and oxidative stress in adult Drosophila melanogaster. Radiat Res 169: 707-711 doi:10.1667/RR1225.1.
46. Chung WK, Shin M, Jaramillo TC, Leibel RL, LeDuc CA, et al. (2009) Absence epilepsy in apathetic, a spontaneous mutant mouse lacking the h channel subunit, HCN2. Neurobiol Dis 33: 499-508 doi:10.1016/j.nbd.2008.12.004.
47. Fernández MP, Berni J, Ceriani MF, (2008) Circadian remodeling of neuronal circuits involved in rhythmic behavior. PLoS Biol 6: e69 doi:10.1371/journal.pbio.0060069.
48. Dubruille R, Emery P, (2008) A plastic clock: how circadian rhythms respond to environmental cues in Drosophila. Mol Neurobiol 38: 129-145 doi:10.1007/s12035-008-8035-y.
49. Ruan G-X, Allen GC, Yamazaki S, McMahon DG, (2008) An autonomous circadian clock in the inner mouse retina regulated by dopamine and GABA. PLoS Biol 6: e249 doi:PMC2567003.
50. Tosini G, Pozdeyev N, Sakamoto K, Iuvone PM, (2008) The circadian clock system in the mammalian retina. Bioessays 30: 624-633 doi:10.1002/bies.20777.
51. Cervetto L, Demontis GC, Gargini C, (2007) Cellular mechanisms underlying the pharmacological induction of phosphenes. Br J Pharmacol 150: 383-390 doi:10.1038/sj.bjp.0706998.
52. Demontis GC, Cervetto L, (2002) Vision: how to catch fast signals with slow detectors. News Physiol Sci 17: 110-114.
53. Cangiano L, Gargini C, Della Santina L, Demontis GC, Cervetto L, (2007) High-pass filtering of input signals by the Ih current in a non-spiking neuron, the retinal rod bipolar cell. PLoS ONE 2: e1327 doi:10.1371/journal.pone.0001327.
54. George MS, Abbott LF, Siegelbaum SA, (2009) HCN hyperpolarization-activated cation channels inhibit EPSPs by interactions with M-type K(+) channels. Nat Neurosci 12: 577-584 doi:10.1038/nn.2307.
55. Magee JC, (2001) Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons. J Neurophysiol 86: 528-532.
56. Lee KH, McCormick DA, (1996) Abolition of spindle oscillations by serotonin and norepinephrine in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuron 17: 309-321.
57. Draper I, Kurshan PT, McBride E, Jackson FR, Kopin AS, (2007) Locomotor activity is regulated by D2-like receptors in Drosophila: an anatomic and functional analysis. Dev Neurobiol 67: 378-393 doi:10.1002/dneu.20355.
58. Zhou QY, Palmiter RD, (1995) Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 83: 1197-1209.
59. Vermeulen CJ, Cremers TIFH, Westerink BHC, Van De Zande L, Bijlsma R, (2006) Changes in dopamine levels and locomotor activity in response to selection on virgin lifespan in Drosophila melanogaster. Mech Ageing Dev 127: 610-617 doi:10.1016/j.mad.2006.02.004.
60. Lima SQ, Miesenböck G, (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121: 141-152 doi:10.1016/j.cell.2005.02.004.
61. Van Swinderen B, Andretic R, (2011) Dopamine in Drosophila: setting arousal thresholds in a miniature brain. Proc Biol Sci 278: 906-913 doi:10.1098/rspb.2010.2564.
62. Lu B, Liu W, Guo F, Guo A, (2008) Circadian modulation of light-induced locomotion responses in Drosophila melanogaster. Genes Brain Behav 7: 730-739 doi:10.1111/j.1601-183X.2008.00411.x.
63. Zhou X, Yuan C, Guo A, (2005) Drosophila olfactory response rhythms require clock genes but not pigment dispersing factor or lateral neurons. J Biol Rhythms 20: 237-244 doi:10.1177/0748730405274451.
64. Lyons LC, Roman G, (2009) Circadian modulation of short-term memory in Drosophila. Learn Mem 16: 19-27 doi:10.1101/lm.1146009.
65. Sakai T, Ishida N, (2001) Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci USA 98: 9221-9225 doi:10.1073/pnas.151443298.
66. Fujii S, Krishnan P, Hardin P, Amrein H, (2007) Nocturnal male sex drive in Drosophila. Curr Biol 17: 244-251 doi:10.1016/j.cub.2006.11.049.
67. Grima B, Chélot E, Xia R, Rouyer F, (2004) Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431: 869-873 doi:10.1038/nature02935.
68. Suh J, Jackson FR, (2007) Drosophila ebony activity is required in glia for the circadian regulation of locomotor activity. Neuron 55: 435-447 doi:PMC2034310.
69. Cahill GM, Besharse JC, (1991) Resetting the circadian clock in cultured Xenopus eyecups: regulation of retinal melatonin rhythms by light and D2 dopamine receptors. J Neurosci 11: 2959-2971.
70. Gravotta L, Gavrila AM, Hood S, Amir S, (2011) Global depletion of dopamine using intracerebroventricular 6-hydroxydopamine injection disrupts normal circadian wheel-running patterns and PERIOD2 expression in the rat forebrain. J Mol Neurosci 45: 162-171 doi:10.1007/s12031-011-9520-8.
71. Dibner C, Schibler U, Albrecht U, (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72: 517-549 doi:10.1146/annurev-physiol-021909-135821.
72. Sicaeros B, Campusano JM, O'Dowd DK, (2007) Primary neuronal cultures from the brains of late stage Drosophila pupae. J Vis Exp pp. 200 doi:10.3791/200.
73. Sorribes A, Armendariz BG, Lopez-Pigozzi D, Murga C, de Polavieja GG, (2011) The origin of behavioral bursts in decision-making circuitry. PLoS Comput Biol 7: e1002075 doi:10.1371/journal.pcbi.1002075.