HCN channels are a novel therapeutic target for cognitive dysfunction in Neurofibromatosis type 1

Molecular Psychiatry

Volumn 20, Issue 11, 2015, Pages 1311-1321

  Omrani, A ^a,h   Van Der Vaart, T ^a,b   Mientjes, E ^a   Van Woerden, G M ^a   Hojjati, M R ^a,c   Li, K W ^d   Gutmann, D H ^e   Levelt, C N ^f   Smit, A B ^d   Silva, A J ^g   Kushner, S A ^a   Elgersma, Y ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^c SHAHREKORD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; LAMOTRIGINE; MESSENGER RNA; PICROTOXIN; AMINO ACID RECEPTOR BLOCKING AGENT; HCN1 PROTEIN, MOUSE; ICI D2788; NEUROFIBROMIN; POTASSIUM CHANNEL; PYRIMIDINE DERIVATIVE; TRIAZINE DERIVATIVE;

4 AMINOBUTYRIC ACID RELEASE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL LYSATE; COGNITIVE DEFECT; COMPARATIVE STUDY; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXON; FEMALE; HALF-ACTIVATION VOLTAGE; HETEROLOGOUS EXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SLICE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LEARNING DISORDER; LONG TERM POTENTIATION; MALE; MEMBRANE STEADY POTENTIAL; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROFIBROMATOSIS TYPE 1; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPATIAL LEARNING; SPATIAL MEMORY; SYNAPTIC TRANSMISSION; WESTERN BLOTTING; WHOLE CELL PATCH CLAMP; ANIMAL; C57BL MOUSE; COGNITION DISORDERS; COMPLICATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENETICS; HIPPOCAMPUS; MAZE TEST; METABOLISM; MOTOR ACTIVITY; MUTATION; NERVE CELL; NERVE CELL INHIBITION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; MUTATION; NEURAL INHIBITION; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; NEURONAL PLASTICITY; NEURONS; POTASSIUM CHANNELS; PYRIMIDINES; SIGNAL TRANSDUCTION; TRIAZINES;

EID: 84946489244     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2015.48     Document Type: Article

References (54)

1. Krab LC, Aarsen FK, de Goede-Bolder A, Catsman-Berrevoets CE, Arts WF, Moll HA et al. Impact of neurofibromatosis type 1 on school performance. J Child Neurol 2008; 23: 1002-1010.
2. Hyman SL, Shores A, North KN. The nature and frequency of cognitive deficits in children with neurofibromatosis type 1. Neurology 2005; 65: 1037-1044.
3. Costa RM, Federov NB, Kogan JH, Murphy GG, Stern J, Ohno M et al. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 2002; 415: 526-530.
4. Silva AJ, Frankland PW, Marowitz Z, Friedman E, Laszlo GS, Cioffi D et al. A mouse model for the learning and memory deficits associated with neurofibromatosis type I. Nat Genet 1997; 15: 281-284.
5. van der Vaart T, van Woerden GM, Elgersma Y, de Zeeuw CI, Schonewille M. Motor deficits in neurofibromatosis type 1 mice: The role of the cerebellum. Genes Brain Behav 2011; 10: 404-409.
6. Cui Y, Costa RM, Murphy GG, Elgersma Y, Zhu Y, Gutmann DH et al. Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 2008; 135: 549-560.
7. Ye X, Carew TJ. Small G protein signaling in neuronal plasticity and memory formation: The specific role of ras family proteins. Neuron 2010; 68: 340-361.
8. Krab LC, de Goede-Bolder A, Aarsen FK, Pluijm SM, Bouman MJ, van der Geest JN et al. Effect of simvastatin on cognitive functioning in children with neurofibromatosis type 1: A randomized controlled trial. JAMA 2008; 300: 287-294.
9. van der Vaart T, Plasschaert E, Rietman AB, Renard M, Oostenbrink R, Vogels A et al. Simvastatin for cognitive deficits and behavioural problems in patients with neurofibromatosis type 1 (NF1-SIMCODA): A randomised, placebo-controlled trial. Lancet Neurol 2013; 12: 1076-1083.
10. Geist RT, Gutmann DH. Expression of a developmentally-regulated neuron-specific isoform of the neurofibromatosis 1 (NF1) gene. Neurosci Lett 1996; 211: 85-88.
11. Gutmann DH, Zhang Y, Hirbe A. Developmental regulation of a neuron-specific neurofibromatosis 1 isoform. Ann Neurol 1999; 46: 777-782.
12. Danglot G, Regnier V, Fauvet D, Vassal G, Kujas M, Bernheim A. Neurofibromatosis 1 (NF1) mRNAs expressed in the central nervous system are differentially spliced in the 5' part of the gene. Hum Mole Genet 1995; 4: 915-920.
13. Wahl-Schott C, Biel M. HCN channels: structure, cellular regulation and physiological function. Cell Mol Life Sci 2009; 66: 470-494.
14. Maccaferri G, McBain CJ. The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 1996; 497: 119-130.
15. Lupica CR, Bell JA, Hoffman AF, Watson PL. Contribution of the hyperpolarizationactivated current (I(h)) to membrane potential and GABA release in hippocampal interneurons. J Neurophysiol 2001; 86: 261-268.
16. Magee JC. Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 1999; 2: 848.
17. Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E et al. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 2004; 119: 719-732.
18. Wang M, Ramos BP, Paspalas CD, Shu Y, Simen A, Duque A et al. Alpha2Aadrenoceptors strengthen working memory networks by inhibiting cAMP-HCN channel signaling in prefrontal cortex. Cell 2007; 129: 397-410.
19. Brager DH, Akhavan AR, Johnston D. Impaired dendritic expression and fmr1(-) (/y) plasticity of h-channels in the mouse model of fragile X syndrome. Cell Rep 2012; 1: 225-233.
20. Shah MM, Anderson AE, Leung V, Lin X, Johnston D. Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 2004; 44: 495-508.
21. Fan Y, Fricker D, Brager DH, Chen X, Lu HC, Chitwood RA et al. Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat Neurosci 2005; 8: 1542-1551.
22. Notomi T, Shigemoto R. Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J Comp Neurol 2004; 471: 241-276.
23. Bender RA, Brewster A, Santoro B, Ludwig A, Hofmann F, Biel M et al. Differential and age-dependent expression of hyperpolarization-activated, cyclic nucleotidegated cation channel isoforms 1-4 suggests evolving roles in the developing rat hippocampus. Neuroscience 2001; 106: 689-698.
24. Brewster AL, Chen Y, Bender RA, Yeh A, Shigemoto R, Baram TZ. Quantitative analysis and subcellular distribution of mRNA and protein expression of the hyperpolarization-activated cyclic nucleotide-gated channels throughout development in rat hippocampus. Cereb Cortex 2007; 17: 702-712.
25. Sugino K, Hempel CM, Miller MN, Hattox AM, Shapiro P, Wu C et al. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci 2006; 9: 99-107.
26. Zeng H, Shen EH, Hohmann JG, Oh SW, Bernard A, Royall JJ et al. Large-scale cellular-resolution gene profiling in human neocortex reveals species-specific molecular signatures. Cell 2012; 149: 483-496.
27. van Woerden GM, Harris KD, Hojjati MR, Gustin RM, Qiu S, de Avila Freire R et al. Rescue of neurological deficits in a mouse model for Angelman syndrome by reduction of alphaCaMKII inhibitory phosphorylation. Nat Neurosci 2007; 10: 280-282.
28. Ozonoff S. Cognitive impairment in neurofibromatosis type 1. Am J Med Genet 1999; 89: 45-52.
29. Li W, Cui Y, Kushner SA, Brown RA, Jentsch JD, Frankland PW et al. The HMG-CoA reductase inhibitor lovastatin reverses the learning and attention deficits in a mouse model of neurofibromatosis type 1. Curr Biol 2005; 15: 1961-1967.
30. Larson J, Wong D, Lynch G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 1986; 368: 347-350.
31. Chapman CA, Perez Y, Lacaille JC. Effects of GABA(A) inhibition on the expression of long-term potentiation in CA1 pyramidal cells are dependent on tetanization parameters. Hippocampus 1998; 8: 289-298.
32. Bollag G, McCormick F, Clark R. Characterization of full-length neurofibromin: tubulin inhibits Ras GAP activity. EMBO J 1993; 12: 1923-1927.
33. Gregory PE, Gutmann DH, Mitchell A, Park S, Boguski M, Jacks T et al. Neurofibromatosis type 1 gene product (neurofibromin) associates with microtubules. Somat Cell Mol Genet 1993; 19: 265-274.
34. Poolos NP, Migliore M, Johnston D. Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci 2002; 5: 767-774.
35. Molosh AI, Johnson PL, Spence JP, Arendt D, Federici LM, Bernabe C et al. Social learning and amygdala disruptions in Nf1 mice are rescued by blocking p21-activated kinase. Nat Neurosci 2014; 17: 1583-1590.
36. Shilyansky C, Karlsgodt KH, Cummings DM, Sidiropoulou K, Hardt M, James AS et al. Neurofibromin regulates corticostriatal inhibitory networks during working memory performance. Proc Natl Acad Sci USA 2010; 107: 13141-13146.
37. Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci 2010; 30: 16796-16808.
38. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Deve Neurobiol 2011; 71: 45-61.
39. Pawelzik H, Hughes DI, Thomson AM. Physiological and morphological diversity of immunocytochemically defined parvalbumin-and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol 2002; 443: 346-367.
40. Schuhmacher AJ, Guerra C, Sauzeau V, Canamero M, Bustelo XR, Barbacid M. A mouse model for Costello syndrome reveals an Ang II-mediated hypertensive condition. J Clin Invest 2008; 118: 2169-2179.
41. Poolos NP, Bullis JB, Roth MK. Modulation of h-channels in hippocampal pyramidal neurons by p38 mitogen-activated protein kinase. J Neurosci 2006; 26: 7995-8003.
42. Kuo CC, Lu L. Characterization of lamotrigine inhibition of Na+ channels in rat hippocampal neurones. Br J Pharmacol 1997; 121: 1231-1238.
43. Xie X, Lancaster B, Peakman T, Garthwaite J. Interaction of the antiepileptic drug lamotrigine with recombinant rat brain type IIA Na+ channels and with native Na + channels in rat hippocampal neurones. Pflugers Archiv: Eur J Physiol 1995; 430: 437-446.
44. Krab LC, de Goede-Bolder A, Aarsen FK, Moll HA, De Zeeuw CI, Elgersma Y et al. Motor learning in children with neurofibromatosis type I. Cerebellum 2011; 10: 14-21.
45. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 1996; 16: 815-823.
46. Soltesz I, Smetters DK, Mody I. Tonic inhibition originates from synapses close to the soma. Neuron 1995; 14: 1273-1283.
47. Brager DH, Johnston D. Plasticity of intrinsic excitability during long-term depression is mediated through mGluR-dependent changes in I(h) in hippocampal CA1 pyramidal neurons. J Neurosci 2007; 27: 13926-13937.
48. George MS, Abbott LF, Siegelbaum SA. HCN hyperpolarization-activated cation channels inhibit EPSPs by interactions with M-type K(+) channels. Nat Neurosci 2009; 12: 577-584.
49. Tsay D, Dudman JT, Siegelbaum SA. HCN1 channels constrain synaptically evoked Ca2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron 2007; 56: 1076-1089.
50. Lee YS, Ehninger D, Zhou M, Oh JY, Kang M, Kwak C et al. Mechanism and treatment for learning and memory deficits in mouse models of Noonan syndrome. Nat Neurosci 2014; 17: 1736-1743.
51. Brown JA, Gianino SM, Gutmann DH. Defective cAMP generation underlies the sensitivity of CNS neurons to neurofibromatosis-1 heterozygosity. J Neurosci 2010; 30: 5579-5589.
52. The I, Hannigan GE, Cowley GS, Reginald S, Zhong Y, Gusella JF et al. Rescue of a Drosophila NF1 mutant phenotype by protein kinase A. Science 1997; 276: 791-794.
53. Tong J, Hannan F, Zhu Y, Bernards A, Zhong Y. Neurofibromin regulates G proteinstimulated adenylyl cyclase activity. Nat Neurosci 2002; 5: 95-96.
54. Stowe IB, Mercado EL, Stowe TR, Bell EL, Oses-Prieto JA, Hernandez H et al. A shared molecular mechanism underlies the human rasopathies Legius syndrome and Neurofibromatosis-1. Genes Dev 2012; 26: 1421-1426.