Role of HCN channels in neuronal hyperexcitability after subarachnoid hemorrhage in rats

Journal of Neuroscience

Volumn 32, Issue 9, 2012, Pages 3164-3175

  Li, Bo ^a   Luo, Chunxia ^a   Tang, Weihua ^a   Chen, Zhi ^a   Li, Qiang ^a   Hu, Bo ^a   Lin, Jiangkai ^a   Zhu, Gang ^a   Zhang, John H ^b   Feng, Hua ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b LOMA LINDA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC NUCLEOTIDE GATED CHANNEL; HEMOGLOBIN; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; MESSENGER RNA; N (G) NITROARGININE; NITRIC OXIDE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE POTENTIAL; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPIKE; SUBARACHNOID HEMORRHAGE; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; MALE; NEURONS; ORGAN CULTURE TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SUBARACHNOID HEMORRHAGE;

EID: 84863279803     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5143-11.2012     Document Type: Article

References (53)

1. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarizationactivated cation channels: from genes to function. Physiol Rev 89:847-885.
2. Bosche B, Graf R, Ernestus RI, Dohmen C, Reithmeier T, Brinker G, Strong AJ, Dreier JP, Woitzik J (2010) Recurrent spreading depolarizations after subarachnoid hemorrhage decreases oxygen availability in human cerebral cortex. Ann Neurol 67:607-617.
3. Cahill J, Calvert JW, Zhang JH (2006) Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 26:1341-1353.
4. Canals S, Makarova I, López-Aguado L, Largo C, Ibarz JM, Herreras O (2005) Longitudinal depolarization gradients along the somatodendritic axis of CA1 pyramidal cells: a novel feature of spreading depression. J Neurophysiol 94:943-951.
5. Chen S, Wang J, Siegelbaum SA (2001) Properties of hyperpolarizationactivated pacemaker current defined by coassembly of HCN1 and HCN2 subunits and basal modulation by cyclic nucleotide. J Gen Physiol 117:491-504.
6. Day M, Carr DB, Ulrich S, Ilijic E, Tkatch T, Surmeier DJ (2005) Dendritic excitability of mouse frontal cortex pyramidal neurons is shaped by the interaction among HCN, Kir2, and Kleak channels. J Neurosci 25:8776-8787.
7. Destexhe A, Contreras D, Steriade M, Sejnowski TJ, Huguenard JR (1996) In vivo, in vitro, and computational analysis of dendritic calcium currents in thalamic reticular neurons. J Neurosci 16:169-185.
8. Dreier JP (2011) The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 17:439-447.
9. Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Lehmann TN, Sarrafzadeh A, Willumsen L, Hartings JA, Sakowitz OW, Seemann JH, Thieme A, Lauritzen M, Strong AJ (2006) Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 129:3224-3237.
10. Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn C, Steinbrink J, Tolias C, Oliveira-Ferreira AI, Fabricius M, Hartings JA, Vajkoczy P, Lauritzen M, Dirnagl U, Bohner G, Strong AJ (2009) Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 132:1866-1881.
11. Fan Y, Deng P, Wang YC, Lu HC, Xu ZC, Schulz PE (2008) Transient cerebral ischemia increases CA1 pyramidal neuron excitability. Exp Neurol 212:415-421.
12. George MS, Abbott LF, Siegelbaum SA (2009) HCN hyperpolarizationactivated cation channels inhibit EPSPs by interactions with M-type K(+) channels. Nat Neurosci 12:577-584.
13. Henning EC, Meng X, Fisher M, Sotak CH (2005) Visualization of cortical spreading depression using manganese-enhanced magnetic resonance imaging. Magn Reson Med 53:851-857.
14. Iadecola C (2009) Bleeding in the brain: Killer waves of depolarization in subarachnoid bleed. Nat Med 15:1131-1132.
15. Jung S, Jones TD, Lugo JN Jr, Sheerin AH, Miller JW, D'Ambrosio R, Anderson AE, Poolos NP (2007) Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy. J Neurosci 27:13012-13021.
16. Koźniewska E, Michalik R, Rafałowska J, Gadamski R, Walski M, Frontczak-Baniewicz M, Piotrowski P, Czernicki Z (2006) Mechanisms of vascular dysfunction after subarachnoid hemorrhage. J Physiol Pharmacol 57 [Suppl 11]:145-160.
17. Kusaka G, Ishikawa M, Nanda A, Granger DN, Zhang JH (2004) Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 24:916-925.
18. Leão AAP (1944) Spreading depression of activity in the cerebral cortex. J Neurophysiol 7:359-390.
19. Lee JY, Sagher O, Keep R, Hua Y, Xi G (2009) Comparison of experimental rat models of early brain injury after subarachnoid hemorrhage. Neurosurgery 65:331-343.
20. Li B, Chen F, Ye J, Chen X, Yan J, Li Y, Xiong Y, Zhou Z, Xia J, Hu Z (2010) The modulation of orexin A on HCN currents of pyramidal neurons in mouse prelimbic cortex. Cereb Cortex 20:1756-1767.
21. Lörincz A, Notomi T, Tamás G, Shigemoto R, Nusser Z (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5:1185-1193.
22. Lovelock CE, Rinkel GJ, Rothwell PM (2010) Time trends in outcome of subarachnoid hemorrhage: population-based study and systematic review. Neurology 74:1494-1501.
23. Luo C, Yi B, Tao G, Li M, Chen Z, Tang W, Zhang JH, Feng H (2010) Adenosine A3 receptor agonist reduces early brain injury in subarachnoid haemorrhage. Neuroreport 21:892-896.
24. Macdonald RL, Weir BK (1991) A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke 22:971-982.
25. Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
26. Magee JC (1999) Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2:508-514.
27. Martin W, Villani GM, Jothiananda D, Furchgott RF (1985) Blockade of endothelium-dependent and glyceryl trinitrate-induced relaxation of rabbit aorta by certain ferrous hemoproteins. J Pharmacol Exp Ther 233:679-685.
28. McCormick WF, Nofzinger JD (1965) Saccular intracranial aneurysms: an autopsy study. J Neurosurg 22:155-159.
29. Neitz A, Mergia E, Eysel UT, Koesling D, Mittmann T (2011) Presynaptic nitric oxide/cGMP facilitates glutamate release via hyperpolarizationactivated cyclic nucleotide-gated channels in the hippocampus. Eur J Neurosci 33:1611-1621.
30. Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ (2009) Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 8:635-642.
31. Notomi T, Shigemoto R (2004) Immunohistochemical localization of Ih channel subunits,HCN1-4, in the rat brain. JCompNeurol 471:241-276.
32. Nusser Z (2009) Variability in the subcellular distribution of ion channels increases neuronal diversity. Trends Neurosci 32:267-274.
33. Oviedo H, Reyes AD (2005) Variation of input-output properties along the somatodendritic axis of pyramidal neurons. J Neurosci 25:4985-4995.
34. Pape HC, Mager R (1992) Nitric oxide controls oscillatory activity in thalamocortical neurons. Neuron 9:441-448.
35. Petzold GC, Haack S, von Bohlen Und Halbach O, Priller J, Lehmann TN, Heinemann U, Dirnagl U, Dreier JP (2008) Nitric oxide modulates spreading depolarization threshold in the human and rodent cortex. Stroke 39:1292-1299.
36. Pluta RM, Hansen-Schwartz J, Dreier J, Vajkoczy P, Macdonald RL, Nishizawa S, Kasuya H, Wellman G, Keller E, Zauner A, Dorsch N, Clark J, Ono S, Kiris T, Leroux P, Zhang JH (2009) Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res 31:151-158.
37. Poolos NP, Migliore M, Johnston D (2002) Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci 5:767-774.
38. Pose I, Sampogna S, Chase MH, Morales FR (2003) Mesencephalic trigeminal neurons are innervated by nitric oxide synthase-containing fibers and respond to nitric oxide. Brain Res 960:81-89.
39. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453-480.
40. Schievink WI, Riedinger M, Jhutty TK, Simon P (2004) Racial disparities in subarachnoid hemorrhage mortality: Los Angeles County, California, 1985-1998. Neuroepidemiology 23:299-305.
41. Sehba FA, Schwartz AY, Chereshnev I, Bederson JB (2000) Acute decrease in cerebral nitric oxide levels after subarachnoid hemorrhage. J Cereb Blood Flow Metab 20:604-611.
42. Shin M, Chetkovich DM (2007) Activity-dependent regulation of h channel distribution in hippocampal CA1 pyramidal neurons. J Biol Chem 282:33168-33180.
43. Somjen GG (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81:1065-1096.
44. Sugawara T, Ayer R, Jadhav V, Zhang JH (2008) A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J Neurosci Methods 167:327-334.
45. Suzuki H, Hasegawa Y, Kanamaru K, Zhang JH (2010) Mechanisms of osteopontin-induced stabilization of blood-brain barrier disruption after subarachnoid hemorrhage in rats. Stroke 41:1783-1790.
46. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M (2007) Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10:754-762.
47. 2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron 56:1076-1089.
48. Turner CP, Bergeron M, Matz P, Zegna A, Noble LJ, Panter SS, Sharp FR (1998) Heme oxygenase-1 (HO-1) is induced in glia throughout the brain by subarachnoid hemoglobin. J Cereb Blood Flow Metab 18:257-273.
49. Vajkoczy P, Meyer B, Weidauer S, Raabe A, Thome C, Ringel F, Breu V, Schmiedek P (2005) Clazosentan (AXV-034343), a selective endothelin A receptor antagonist, in the prevention of cerebral vasospasm following severe aneurysmal subarachnoid hemorrhage: results of a randomized, double-blind, placebo-controlled, multicenter phase IIa study. J Neurosurg 103:9-17.
50. Wang M, Ramos BP, Paspalas CD, Shu Y, Simen A, Duque A, Vijayraghavan S, Brennan A, Dudley A, Nou E, Mazer JA, McCormick DA, Arnsten AF (2007) a2A-Adrenoceptors strengthen working memory networks by inhibiting cAMP HCN channel signaling in prefrontal cortex. Cell 129:397-410.
51. Wickman G, Lan C, Vollrath B (2003) Functional roles of the rho/rho kinase pathway and protein kinase C in the regulation of cerebrovascular constriction mediated by hemoglobin: relevance to subarachnoid hemorrhage and vasospasm. Circ Res 92:809-816.
52. Williams SR, Stuart GJ (2003) Role of dendritic synapse location in the control of action potential output. Trends Neurosci 26:147-154.
53. Wilson GW, Garthwaite J (2010) Hyperpolarization-activated ion channels as targets for nitric oxide signalling in deep cerebellar nuclei. Eur J Neurosci 31:1935-1945.