Sodium channel cleavage is associated with aberrant neuronal activity and cognitive deficits in a mouse model of alzheimer's disease

Journal of Neuroscience

Volumn 33, Issue 16, 2013, Pages 7020-7026

  Corbett, Brian F ^a,b   Leiser, Steven C ^c   Ling, Huai Ping ^c   Nagy, Reka ^c   Breysse, Nathalie ^c   Zhang, Xiaohong ^a,b   Hazra, Anupam ^a,b   Brown, Jon T ^d   Randall, Andrew D ^d   Wood, Andrew ^c   Chin, Jeannie ^a,b,c   Reinhart, Peter H ^c  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c PFIZER INC   (United States)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; CALBINDIN; SODIUM CHANNEL NAV1.1; VOLTAGE GATED SODIUM CHANNEL BETA 2 SUBUNIT;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; COGNITIVE DEFECT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; IMMUNOHISTOCHEMISTRY; MALE; MAZE TEST; MOUSE; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANSGENIC MOUSE; WESTERN BLOTTING;

EID: 84876261166     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2325-12.2013     Document Type: Article

References (60)

1. Amatniek JC, Hauser WA, DelCastillo-Castaneda C, Jacobs DM, Marder K, Bell K, Albert M, Brandt J, Stern Y (2006) Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 47:867-872.
2. Bakker A, Krauss GL, Albert MS, Speck CL, Jones LR, Stark CE, Yassa MA, Bassett SS, Shelton AL, Gallagher M (2012) Reduction of hippocampal hyperactivity improves cognition inamnestic mild cognitive impairment. Neuron 74:467-474.
3. Bertram L, Lill CM, Tanzi RE (2010) The genetics of Alzheimer disease: back to the future. Neuron 68:270-281.
4. Blennow K, de Leon MJ, Zetterberg H (2006) Alzheimer's disease. Lancet 368:387-403.
5. Bourne KZ, Ferrari DC, Lange-Dohna C, Rossner S, Wood TG, Perez-Polo JR (2007) Differential regulation of BACE1 promoter activity by nuclear factor-kappaB in neurons and glia upon exposure to beta-amyloid pep-tides. J Neurosci Res 85:1194-1204.
6. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, Staufenbiel M, Konnerth A, Garaschuk O (2008) Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321:1686-1689.
7. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.
8. Catterall WA (2010) Ion channel voltage sensors: structure, function, and pathophysiology. Neuron 67:915-928.
9. Chen C, Bharucha V, Chen Y, Westenbroek RE, Brown A, Malhotra JD, Jones D, Avery C, Gillespie PJ 3rd, Kazen-Gillespie KA, Kazarinova-Noyes K, Shrager P, Saunders TL, Macdonald RL, Ransom BR, Scheuer T, Catterall WA, Isom LL (2002) Reduced sodium channel density, altered voltage dependence of inactivation, and increased susceptibility to seizures in mice lacking sodium channel beta 2-subunits. Proc Natl Acad Sci USA 99:17072-17077.
10. Chin J, Palop JJ, Puolivali J, Massaro C, Bien-Ly N, 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 Neu-rosci 25:9694-9703.
11. Derdikman D, Moser EI (2010) A manifold of spatial maps in the brain. Trends CognSci 14:561-569.
12. Fukumoto H, Cheung BS, Hyman BT, Irizarry MC (2002) Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 59:1381-1389.
13. Gersbacher MT, Kim DY, Bhattacharyya R, Kovacs DM (2010) Identification of BACE1 cleavage sites in human voltage-gated sodium channel beta 2 subunit. Mol Neurodegener 5:61.
14. Gong B, Rhodes KJ, Bekele-Arcuri Z, Trimmer JS (1999) Type I and type II Na(+) channel alpha-subunit polypeptides exhibit distinct spatial and temporal patterning, and association with auxiliary subunits in rat brain. J Comp Neurol 412:342-352.
15. Gordon JA (2011) Oscillations and hippocampal-prefrontal synchrony. Curr Opin Neurobiol 21:486-491.
16. Harris JA, Devidze N, Verret L, Ho K, Halabisky B, Thwin MT, Kim D, Hamto P, Lo I, Yu GQ, Palop JJ, Masliah E, Mucke L (2010) Transsynaptic progression of amyloid-beta-induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron 68:428-441.
17. Hebert SS, Horré K, Nicolaï L, Papadopoulou AS, Mandemakers W, Si-lahtaroglu AN, Kauppinen S, Delacourte A, De Strooper B (2008) Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc Natl Acad Sci USA 105:6415-6420.
18. Hitt BD, Jaramillo TC, Chetkovich DM, Vassar R (2010) BACE1 mice exhibit seizure activity that does not correlate with sodium channel level or axonal localization. Mol Neurodegener 5:31.
19. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4:97-100.
20. Holsinger RM, McLean CA, Beyreuther K, Masters CL, Evin G (2002) Increased expression of the amyloid precursor β-secretase in Alzheimer's disease. Ann Neurol 51:783-786.
21. Hsiao KK, Borchelt DR, Olson K, Johannsdottir R, Kitt C, Yunis W, Xu S, Eckman C, Younkin S, Price D (1995) Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron 15:1203-1218.
22. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
23. Hu X, Zhou X, He W, Yang J, Xiong W, Wong P, Wilson CG, Yan R (2010) BACE1 deficiency causes altered neuronal activity and neurodegenera-tion. J Neurosci 30:8819-8829.
24. Kim DY, Gersbacher MT, Inquimbert P, Kovacs DM (2011) Reduced sodium channel Nav1.1 levels in BACE1-null mice. J Biol Chem 286:8106-8116.
25. Kim DY, Carey BW, Wang H, Ingano LA, Binshtok AM, Wertz MH, Pettin-gell WH, He P, Lee VM, Woolf CJ, Kovacs DM (2007) BACE1 regulates voltage-gated sodium channels and neuronal activity. Nat Cell Biol 9:755-764.
26. Kobayashi D, Zeller M, Cole T, Buttini M, McConlogue L, Sinha S, Freedman S, Morris RG, Chen KS (2008) BACE1 gene deletion: impact on behavioral function in a model of Alzheimer's disease. Neurobiol Aging 29:861-873.
27. Kovacs DM, Gersbacher MT, Kim DY (2010) Alzheimer's secretases regulate voltage-gated sodium channels. Neurosci Lett 486:68-72.
28. LaFerla FM, Tinkle BT, Bieberich CJ, Haudenschild CC, Jay G (1995) The Alzheimer's Abeta peptide induces neurodegeneration and apoptotic cell death in transgenic mice. Nat Genet 9:21-30.
29. Lai HC, Jan LY (2006) The distribution and targeting of neuronal voltage-gated ion channels. Nat Rev Neurosci 7:548-562.
30. Lalonde R, Dumont M, Staufenbiel M, Strazielle C (2005) Neurobehavioral characterization of APP23 transgenic mice with the SHIRPA primary screen. Behav Brain Res 157:91-98.
31. Li R, Lindholm K, Yang LB, Yue X, Citron M, Yan R, Beach T, Sue L, Sabbagh M, Cai H, Wong P, Price D, Shen Y (2004) Amyloid beta peptide load is correlated with increased beta-secretase activity in sporadic Alzheimer's disease patients. Proc Natl Acad Sci USA 101:3632-3637.
32. Lopez-Santiago LF, Pertin M, Morisod X, Chen C, Hong S, Wiley J, Decosterd I, Isom LL (2006) Sodium channel beta2 subunits regulate tetrodotoxin-sensitive sodium channels in small dorsal root ganglion neurons and modulate the response to pain. J Neurosci 26:7984-7994.
33. Lozsadi DA, Larner AJ (2006) Prevalence and causes of seizures at the time of diagnosis of probable Alzheimer's disease. Dement Geriatr Cogn Disord 22:121-124.
34. Messner DJ, Catterall WA (1985) The sodium channel from rat brain: separation and characterization of subunits. J Biol Chem 260:10597-10604.
35. Minkeviciene R, Rheims S, Dobszay MB, Zilberter M, Hartikainen J, Fülop L, Penke B, Zilberter Y, Harkany T, Pitkanen A, Tanila H (2009) Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. J Neurosci 29:3453-3462.
36. Moechars D, Lorent K, Van Leuven F (1999) Premature death in transgenic mice that overexpress a mutant amyloid precursor protein is preceded by severe neurodegeneration and apoptosis. Neuroscience 91:819-830.
37. Molinari S, Battini R, Ferrari S, Pozzi L, Killcross AS, Robbins TW, Jou-venceau A, Billard JM, Dutar P, Lamour Y, Baker WA, Cox H, Emson P (1996) Deficits in memory and hippocampal long-term potentiation in mice with reduced calbindin D28K expression. Proc Natl Acad Sci USA 93:8028-8033.
38. Mucke L, Selkoe DJ (2012) Neurotoxicity of amyloid beta-protein: synaptic and network dysfunction. Cold Spring Harb Perspect Med 2:a006338.
39. Muzzio IA, Kentros C, Kandel E (2009) What is remembered? Role of attention on the encoding and retrieval of hippocampal representations. J Physiol 587:2837-2854.
40. 2+ influx because of a loss of calbindin-D28K in temporal lobe epilepsy. J Neurosci 20:1831-1836.
41. Oberheim NA, Tian GF, Han X, Peng W, Takano T, Ransom B, Nedergaard M (2008) Loss of astrocytic domain organization in the epileptic brain. J Neurosci 28:3264-3276.
42. Ogiwara I, Miyamoto H, Morita N, Atapour N, Mazaki E, Inoue I, Takeuchi T, Itohara S, Yanagawa Y, Obata K, Furuichi T, Hensch TK, Yamakawa K (2007) Na(v)1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. J Neurosci 27:5903-5914.
43. Ohno M, Sametsky EA, Younkin LH, Oakley H, Younkin SG, Citron M, Vassar R, Disterhoft JF (2004) BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease. Neuron 41:27-33.
44. 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 USA 100:9572-9577.
45. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, 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.
46. 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 beta-induced deficits in an Alzheimer's disease mouse model. Science 316:750-754.
47. Roberson ED, Halabisky B, Yoo JW, Yao J, Chin J, Yan F, Wu T, Hamto 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.
48. Rockenstein E, Mante M, Alford M, Adame A, Crews L, Hashimoto M, Esposito L, Mucke L, Masliah E (2005) High β-secretase activity elicits neurodegeneration in transgenic mice despite reductions in amyloid-jS levels: implications for the treatment of Alzheimer's disease. J Biol Chem 280:32957-32967.
49. Rudy B, Fishell G, Lee S, Hjerling-Leffler J (2011) Three groups of interneu-rons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71:45-61.
50. 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 USA 109:E2895-2903.
51. Shimmyo Y, Kihara T, Akaike A, Niidome T, Sugimoto H (2008) Epigallocat-echin-3-gallate and curcumin suppress amyloid beta-induced beta-site APP cleaving enzyme-1 upregulation. Neuroreport 19:1329-1333.
52. Sun A, Koelsch G, Tang J, Bing G (2002) Localization of beta-secretase me-mapsin 2 in the brain of Alzheimer's patients and normal aged controls. Exp Neurol 175:10-22.
53. Tesco G, Koh YH, Kang EL, Cameron AN, Das S, Sena-Esteves M, Hiltunen M, Yang SH, Zhong Z, Shen Y, Simpkins JW, Tanzi RE (2007) Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 54:721-737.
54. Vann SD, Albasser MM (2011) Hippocampus and neocortex: recognition and spatial memory. Curr Opin Neurobiol 21:440-445.
55. 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 interneu-ron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149:708-721.
56. Vezzani A, Sperk G, Colmers WF (1999) Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci 22:25-30.
57. Vogt DL, Thomas D, Galvan V, Bredesen DE, Lamb BT, Pimplikar SW (2011) Abnormal neuronal networks and seizure susceptibility in mice overexpressing the APP intracellular domain. Neurobiol Aging 32:1725-1729.
58. Wong HK, Sakurai T, Oyama F, Kaneko K, Wada K, Miyazaki H, Kurosawa M, De Strooper B, Saftig P, Nukina S (2005) β Subunits of voltage-gated sodium channels are novel substrates of beta-site amyloid precursor protein-cleaving enzyme (BACE1) and gamma-secretase. J Biol Chem 280:23009-23017.
59. Yang LB, Lindholm K, Yan R, Citron M, Xia W, Yang XL, Beach T, Sue L, Wong P, Price D, Li R, Shen Y (2003) Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 9:3-4.
60. Zhao J, Fu Y, Yasvoina M, Shao P, Hitt B, O'Connor T, Logan S, Maus E, Citron M, Berry R, Binder L, Vassar R (2007) Beta-site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer's disease pathogenesis. J Neurosci 27:3639-3649.