Tau-dependent Kv4.2 depletion and dendritic hyperexcitability in a mouse model of Alzheimer’s disease

Journal of Neuroscience

Volumn 35, Issue 15, 2015, Pages 6221-6230

  Hall, Alicia M ^a,b   Throesch, Benjamin T ^c   Buckingham, Susan C ^b   Markwardt, Sean J ^b   Peng, Yin ^b   Wang, Qin ^b   Hoffman, Dax A ^c   Roberson, Erik D ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Alzheimer; Amyloid beta; Dendrites; Excitability; Kv4.2; Tau

Indexed keywords

AMYLOID BETA PROTEIN; CALBINDIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; COMPLEMENTARY DNA; ETIRACETAM; LIGAND GATED ION CHANNEL; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV4.2; TAU PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL; AMYLOID PRECURSOR PROTEIN; NOOTROPIC AGENT; PIRACETAM; SHAL POTASSIUM CHANNEL;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN PERFUSION; CONTROLLED STUDY; DENDRITIC SPINE; ELECTROENCEPHALOGRAPHY; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; GENOTYPE; HIPPOCAMPAL CA1 REGION; HYPERPOLARIZATION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; OSMOTIC MINIPUMP; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PROTEIN DEPLETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SOMATOSENSORY CORTEX; TRANSGENIC MOUSE; ACTION POTENTIAL; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DEFICIENCY; DENDRITE; DRUG EFFECTS; ELECTROENCEPHALOGRAM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IN VITRO STUDY; MUTATION; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN WAVES; CA1 REGION, HIPPOCAMPAL; DENDRITES; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IN VITRO TECHNIQUES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEURONS; NOOTROPIC AGENTS; PIRACETAM; SHAL POTASSIUM CHANNELS; TAU PROTEINS;

EID: 84929260607     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2552-14.2015     Document Type: Article

References (52)

1. Andrásfalvy BK, Makara JK, Johnston D, Magee JC (2008) Altered synaptic and non-synaptic properties of CA1 pyramidal neurons in Kv4.2 knockout mice. J Physiol 586:3881-3892. CrossRef Medline
2. Aronica E, Boer K, Doom KJ, Zurolo E, Spliet WG, van Rijen PC, Baayen JC, Gorter JA, Jeromin A (2009) Expression and localization of voltage dependent potassium channel Kv4.2 in epilepsy associated focal lesions. Neurobiol Dis 36:81-95. CrossRef Medline
3. Bernard C, Anderson A, Becker A, Poolos NP, Beck H, Johnston D (2004) Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305: 532-535. CrossRef Medline
4. Brager DH, Johnston D (2014) Channelopathies and dendritic dysfunction in fragile X syndrome. Brain Res Bull 103:11-17. CrossRef Medline
5. Busche MA, Chen X, Henning HA, Reichwald J, Staufenbiel M, Sakmann B, Konnerth A (2012) Critical role of soluble amyloid-β for early hippocampal hyperactivity in a mouse model of Alzheimer’s disease. Proc Natl Acad Sci U S A 109:8740-8745. CrossRef Medline
6. + current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J Neurosci 26:12143-12151. CrossRef Medline
7. Chin J, Palop JJ, Puoliväli J, Massaro C, Bien-LyN, Gerstein H, Scearce-Levie K, Masliah E, Mucke L (2005) Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer’s disease. J Neurosci 25:9694-9703. CrossRef Medline
8. Cochran JN, Hall AM, Roberson ED (2014) The dendritic hypothesis for Alzheimer’s disease pathophysiology. Brain Res Bull 103:18-28. CrossRef Medline
9. Dawson HN, Ferreira A, Eyster MV, Ghoshal N, Binder LI, Vitek MP (2001) Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 114:1179-1187. Medline
10. DeVos SL, Goncharoff DK, Chen G, Kebodeaux CS, Yamada K, Stewart FR, Schuler DR, Maloney SE, Wozniak DF, Rigo F, Bennett CF, Cirrito JR, Holtzman DM, Miller TM (2013) Antisense reduction of tau in adult mice protects against seizures. J Neurosci 33:12887-12897. CrossRef Medline
11. Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, Rentz DM, Bertram L, Mullin K, Tanzi RE, Blacker D, Albert MS, Sperling RA (2005) Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 65:404-411. CrossRef Medline
12. Farris W, Schütz SG, Cirrito JR, Shankar GM, Sun X, George A, Leissring MA, Walsh DM, Qiu WQ, Holtzman DM, Selkoe DJ (2007) Loss of neprilysin function promotes amyloid plaque formation and causes cerebral amyloid angiopathy. Am J Pathol 171:241-251. CrossRef Medline
13. Frandemiche ML, De Seranno S, Rush T, Borel E, Elie A, Arnal I, Lanté F, Buisson A (2014) Activity-dependent tau protein translocation to excitatory synapse is disrupted by exposure to amyloid-beta oligomers. J Neurosci 34:6084-6097. CrossRef Medline
14. Frick A, Johnston D (2005) Plasticity of dendritic excitability. J Neurobiol 64:100-115. CrossRef Medline
15. Gross C, Yao X, Pong DL, Jeromin A, Bassell GJ (2011) Fragile X mental retardation protein regulates protein expression and mRNA translation of the potassium channel Kv4.2. J Neurosci 31:5693-5698. CrossRef Medline
16. to f and results in electrical and molecular remodeling, with no evidence of ventricular hypertrophy or myocardial dysfunction. Circ Res 97:1342-1350. CrossRef Medline
17. Hall AM, Roberson ED (2012) Mouse models of Alzheimer’s disease. Brain Res Bull 88:3-12. CrossRef Medline
18. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wolfing H, Chieng BC, Christie MJ, Napier IA, Eckert A, Staufenbiel M, Hardeman E, Götz J (2010) Dendritic function of tau mediates amyloid-β toxicity in Alzheimer’s disease mouse models. Cell 142:387-397. CrossRef Medline
19. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, Borchelt DR (2001) Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng 17:157-165. CrossRef Medline
20. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR (2004) Mutant presenilins specifically elevate the levels of the 42 residue β-amyloid peptide in vivo: evidence for augmentation of a 42-specific y secretase. Hum Mol Genet 13:159-170. CrossRef Medline
21. Jinno S, Jeromin A, Kosaka T (2005) Postsynaptic and extrasynaptic localization of Kv4.2 channels in the mouse hippocampal region, with special reference to targeted clustering at GABAergic synapses. Neuroscience 134:483-494. CrossRef Medline
22. Kim J, Wei DS, Hoffman DA (2005) Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol 569:41-57. CrossRef Medline
23. Kuchibhotla KV, Goldman ST, Lattarulo CR, Wu HY, Hyman BT, Bacskai BJ (2008) Aβ plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron 59:214-225. CrossRef Medline
24. Lee HY, Ge WP, Huang W, He Y, Wang GX, Rowson-Baldwin A, Smith SJ, Jan YN, Jan LY (2011) Bidirectional regulation of dendritic voltage-gated potassium channels by the fragile X mental retardation protein. Neuron 72:630-642. CrossRef Medline
25. Lei Z, Deng P, Li J, Xu ZC (2012) Alterations of A-type potassium channels in hippocampal neurons after traumatic brain injury. J Neurotrauma 29:235-245. CrossRef Medline
26. Lugo JN, Barnwell LF, Ren Y, Lee WL, Johnston LD, Kim R, Hrachovy RA, Sweatt JD, Anderson AE (2008) Altered phosphorylation and localization of the A-type channel, Kv4.2 in status epilepticus. J Neurochem 106:1929-1940. CrossRef Medline
27. Lugo JN, Brewster AL, Spencer CM, Anderson AE (2012) Kv4.2 knockout mice have hippocampal-dependent learning and memory deficits. Learn Mem 19:182-189. CrossRef Medline
28. Magee J, Hoffman D, Colbert C, Johnston D (1998) Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60:327-346. CrossRef Medline
29. + conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J Comput Neurosci 7:5-15. CrossRef Medline
30. Moolman DL, Vitolo OV, Vonsattel JP, Shelanski ML (2004) Dendrite and dendritic spine alterations in Alzheimer models. J Neurocytol 33:377-387. CrossRef Medline
31. 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20:4050-4058. Medline
32. Nestor MW, Hoffman DA (2012) Aberrant dendritic excitability: a common pathophysiology in CNS disorders affecting memory? Mol Neurobiol 45:478-487. CrossRef Medline
33. Olazarán J, Prieto J, Cruz I, Esteban A (2010) Cortical excitability in very mild Alzheimer’s disease: a long-term follow-up study. J Neurol 257: 2078-2085. CrossRef Medline
34. Palop JJ, Mucke L (2009) Epilepsy and cognitive impairments in Alzheimer disease. Arch Neurol 66:435-440. CrossRef Medline
35. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L (2003) Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer’s disease-related cognitive deficits. Proc Natl Acad Sci U S A 100:9572-9577. CrossRef Medline
36. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-LyN, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer’s disease. Neuron 55:697-711. CrossRef Medline
37. Palop JJ, Mucke L, Roberson ED (2011) Quantifying biomarkers of cognitive dysfunction and neuronal network hyperexcitability in mouse models of Alzheimer’s disease: depletion of calcium-dependent proteins and inhibitory hippocampal remodeling. Methods Mol Biol 670:245-262. CrossRef Medline
38. Pei Q, Burnet PW, Grahame-Smith DG, Zetterström TS (1997) Differential effects of acute and chronic electroconvulsive shock on the abundance of messenger RNAs for voltage-dependent potassium channel subunits in the rat brain. Neuroscience 78:343-350. CrossRef Medline
39. + current modulated by arachidonic acid regulates synaptic integration and threshold for LTP induction in hippocampal pyramidal cells. Proc Natl Acad Sci USA 99:10144-10149. CrossRef Medline
40. Reiman EM, Quiroz YT, Fleisher AS, Chen K, Velez-Pardo C, Jimenez-Del-Rio M, Fagan AM, Shah AR, Alvarez S, Arbelaez A, Giraldo M, Acosta-Baena N, Sperling RA, Dickerson B, Stern CE, Tirado V, Munoz C, Reiman RA, Huentelman MJ, Alexander GE, et al. (2012) Brain imaging and fluid biomarker analysis in young adults at genetic risk for autosomal dominant Alzheimer’s disease in the presenilin 1 E280A kindred: a case-control study. Lancet Neurol 11:1048-1056. CrossRef Medline
41. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T, Gerstein H, Yu GQ, Mucke L (2007) Reducing endogenous tau ameliorates amyloid /3-induced deficits in an Alzheimer’s disease mouse model. Science 316: 750-754. CrossRef Medline
42. Roberson ED, Halabisky B, Yoo JW, Yao J, Chin J, Yan F, Wu T, Ham to P, Devidze N, Yu GQ, Palop JJ, Noebels JL, Mucke L (2011) Amyloid-β/ Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer’s disease. J Neurosci 31:700-711. CrossRef Medline
43. + currents in hippocampal granule cells of control and chronically epileptic rats. Eur J Neurosci 23:675-685. CrossRef Medline
44. Sanchez PE, Zhu L, Verret L, Vossel KA, Orr AG, Cirrito JR, Devidze N, Ho K, Yu GQ, Palop JJ, Mucke L (2012) Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer’s disease model. Proc Natl Acad Sci U S A 109:E2895-E2903. CrossRef Medline
45. Sišková Z, Justus D, Kaneko H, Friedrichs D, Henneberg N, Beutel T, Pitsch J, Schoch S, Becker A, von der Kammer H, Remy S (2014) Dendritic structural degeneration is functionally linked to cellular hyperexcitability in a mouse model of Alzheimer’s disease. Neuron 84:1023-1033. CrossRef Medline
46. + channel mRNAs in the rat brain and down-regulation in the hippocampus following seizures. Neuron 8:1055-1067. CrossRef Medline
47. Verret L, Mann EO, Hang GB, Barth AM, Cobos I, Ho K, Devidze N, Masliah E, Kreitzer AC, Mody I, Mucke L, Palop JJ (2012) Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149:708-721. CrossRef Medline
48. Vetter P, Roth A, Häusser M (2001) Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 85:926-937. Medline
49. Vossel KA, Beagle AJ, Rabinovici GD, Shu H, Lee SE, Naasan G, Hegde M, Cornes SB, Henry ML, Nelson AB, Seeley WW, Geschwind MD, Gorno-Tempini ML, Shih T, Kirsch HE, Garcia PA, Miller BL, Mucke L (2013) Seizures and epileptiform activity in the early stages of Alzheimer disease. JAMA Neurol 70:1158-1166. CrossRef Medline
50. + channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 99:8366-8371. CrossRef Medline
51. A in pyramidal neurons in (rat) primary visual cortex. J Neurosci 25:9185-9194. CrossRef Medline
52. Zempel H, Luedtke J, Kumar Y, Biernat J, Dawson H, Mandelkow E, Mandelkow EM (2013) Amyloid-β oligomers induce synaptic damage via Tau-dependent microtubule severing by TTLL6 and spastin. EMBO J 32:2920-2937. CrossRef Medline