Alzheimer's secretases regulate voltage-gated sodium channels

Neuroscience Letters

Volumn 486, Issue 2, 2010, Pages 68-72

  Kovacs, Dora M ^a   Gersbacher, Manuel T ^a   Kim, Doo Yeon ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Secretase; Secretase; Alzheimer's disease; BACE1; Presenilin; Sodium channel 2 subnit; Voltage gated sodium channel

Indexed keywords

BETA SECRETASE 1; PRESENILIN; VOLTAGE GATED SODIUM CHANNEL;

ALZHEIMER DISEASE; BETA CHAIN; ENZYME ACTIVITY; FOLLOW UP; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW;

ALZHEIMER DISEASE; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; BRAIN; HUMANS; ION CHANNEL GATING; MICE; NEURONS; PRESENILINS; SODIUM CHANNELS;

EID: 78049403832     PISSN: 03043940     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neulet.2010.08.048     Document Type: Review

References (72)

1. Assal F., Cummings J. Neuropsychiatric symptoms in the dementias. Curr. Opin. Neurol. 2002, 15:445-450.
2. A.S.Association 2010 Alzheimer's disease facts and figures. Alzheimers Dement. 2010, 6:158-194.
3. Borchelt D., Thinakaran G., Eckman C., Lee M., Davenport F., Ratovitsky T., Prada C., Kim G., Seekins S., Yager D., Slunt H., Wang R., Seeger M., Levey A., Gandy S., Copeland N., Jenkins N., Price D., Younkin S., Sisodia S. Familial Alzheimer's disease-linked presenilin 1 variants elevate Abeta1-42/1-40 ratio in vitro and in vivo. Neuron 1996, 17:1005-1013.
4. + channel beta1 subunit-mediated neurite outgrowth requires Fyn kinase and contributes to postnatal CNS development in vivo. J. Neurosci. 2008, 28:3246-3256.
5. + channels in cellular migration: regulation of central nervous system development and potentiation of invasive cancers. Neuroscientist 2008, 14:571-583.
6. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000, 26:13-25.
7. Catterall W.A. Molecular mechanisms of gating and drug block of sodium channels. Novartis Found Symp. 2002, 241:206-218. discussion 218-232.
8. Chen C., Bharucha V., Chen Y., Westenbroek R., Brown A., Malhotra J., Jones D., Avery C., Gillespie P., Kazen-Gillespie K., Kazarinova-Noyes K., Shrager P., Saunders T., Macdonald R., Ransom B., Scheuer T., Catterall W., Isom L. 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. U.S.A. 2002, 99:17072-17077.
9. Clark D.G, Mendez M.F., Farag E., Vinters H.V. Clinicopathologic case report: progressive aphasia in a 77-year-old man. J. Neuropsych. Clin. Neurosci. 2003, 15:231-238.
10. Davis T., Chen C., Isom L. Sodium channel beta 1 subunits promote neurite outgrowth in cerebellar granule neurons. J. Biol. Chem. 2004.
11. Dominguez D., Tournoy J., Hartmann D., Huth T., Cryns K., Deforce S., Serneels L., Camacho I., Marjaux E., Craessaerts K., Roebroek A., Schwake M., D'Hooge R., Bach P., Kalinke U., Moechars D., Alzheimer C., Reiss K., Saftig P., De Strooper B. Phenotypic and biochemical analyses of BACE1- and BACE2-deficient mice. J. Biol. Chem. 2005, 280:30797-30806.
12. Fukumoto H., Cheung B., Hyman B., Irizarry M. Beta-secretase protein and activity are increased in the neocortex in alzheimer disease. Arch. Neurol. 2002, 59:1381-1389.
13. Guglielmotto M, Aragno M., Autelli R., Giliberto L., Novo E., Colombatto S., Danni O., Parola M., Smith M.A., Perry G., Tamagno E., Tabaton M. The up-regulation of BACE1 mediated by hypoxia and ischemic injury: role of oxidative stress and HIF1alpha. J. Neurochem. 2009, 108:1045-1056.
14. Haass C., Selkoe D.J. Cellular processing of beta-amyloid precursor protein and the genesis of amyloid beta-peptide. Cell 1993, 75:1039-1042.
15. Hains B.C., Waxman S.G. Sodium channel expression and the molecular pathophysiology of pain after SCI. Prog. Brain Res. 2007, 161:195-203.
16. Hardy J., Selkoe D. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
17. Hauser W.A., Morris M.L., Heston L.L., Anderson V.E. Seizures and myoclonus in patients with Alzheimer's disease. Neurology 1986, 36:1226-1230.
18. Hesdorffer D.C., Hauser W.A., Annegers J.F., Kokmen E., Rocca W.A. Dementia and adult-onset unprovoked seizures. Neurology 1996, 46:727-730.
19. Hu X., He W., Diaconu C., Tang X., Kidd G., Macklin W., Trapp B., Yan R. Genetic deletion of BACE1 in mice affects remyelination of sciatic nerves. FASEB J. 2008, 22:2970-2980.
20. Hu X., Hicks C., He W., Wong P., Macklin W., Trapp B., Yan R. Bace1 modulates myelination in the central and peripheral nervous system. Nat. Neurosci. 2006, 9:1520-1525.
21. Hu X., Zhou X., He W., Yang J., Xiong W., Wong P., Wilson C.G., Yan R. BACE1 deficiency causes altered neuronal activity and neurodegeneration. J. Neurosci. 2010, 30:8819-8829.
22. Hussain I., Powell D., Howlett D., Tew D., Meek T., Chapman C., Gloger I., Murphy K., Southan C., Ryan D., Smith T., Simmons D., Walsh F., Dingwall C., Christie G. Identification of a novel aspartic protease (Asp 2) as beta-secretase. Mol. Cell. Neurosci. 1999, 14:419-427.
23. Huth T., Schmidt-Neuenfeldt K., Rittger A., Saftig P., Reiss K., Alzheimer C. Non-proteolytic effect of beta-site APP-cleaving enzyme 1 (BACE1) on sodium channel function. Neurobiol. Dis. 2009, 33:282-289.
24. Isom L. Sodium channel beta subunits: anything but auxiliary. Neuroscientist 2001, 7:42-54.
25. Isom L. The role of sodium channels in cell adhesion. Front. Biosci. 2002, 7:12-23.
26. + channel subunits and Ig domains. Nature 1996, 383:307-308.
27. + channels and increases their functional expression. J. Neurosci. 2001, 21:7517-7525.
28. Kim D., Carey B., Wang H., Ingano L., Binshtok A., Wertz M., Pettingell W., He P., Lee V., Woolf C., Kovacs D. BACE1 regulates voltage-gated sodium channels and neuronal activity. Nat. Cell Biol. 2007, 9:755-764.
29. Kim D., Ingano L., Carey B., Pettingell W., Kovacs D. Presenilin/{gamma}-secretase-mediated cleavage of the voltage-gated sodium channel {beta}2-subunit regulates cell adhesion and migration. J. Biol. Chem. 2005, 280:23251-23261.
30. Laird F., Cai H., Savonenko A., Farah M., He K., Melnikova T., Wen H., Chiang H., Xu G., Koliatsos V., Borchelt D., Price D., Lee H., Wong P. BACE1, a major determinant of selective vulnerability of the brain to amyloid-beta amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J. Neurosci. 2005, 25:11693-11709.
31. Larner A.J, Doran M. Clinical phenotypic heterogeneity of Alzheimer's disease associated with mutations of the presenilin-1 gene. J. Neurol. 2006, 253:139-158.
32. Lee E., Zhang B., Liu K., Greenbaum E., Doms R., Trojanowski J., Lee V. BACE overexpression alters the subcellular processing of APP and inhibits Abeta deposition in vivo. J. Cell Biol. 2005, 168:291-302.
33. Loane D.J., Pocivavsek A., Moussa C.E., Thompson R., Matsuoka Y., Faden A.I., Rebeck G.W., Burns M.P. Amyloid precursor protein secretases as therapeutic targets for traumatic brain injury. Nat. Med. 2009, 15:377-379.
34. Malhotra J., Kazen-Gillespie K., Hortsch M., Isom L. Sodium channel beta subunits mediate homophilic cell adhesion and recruit ankyrin to points of cell-cell contact. J. Biol. Chem. 2000, 275:11383-11388.
35. McCarthy J.V., Twomey C., Wujek P. Presenilin-dependent regulated intramembrane proteolysis and gamma-secretase activity. Cell. Mol. Life Sci. 2009, 66:1534-1555.
36. v1.2 currents and cell surface density is dependent on interactions with contactin and ankyrin. J. Biol. Chem. 2004, 279:16044-16049.
37. Meadows L., Malhotra J., Stetzer A., Isom L., Ragsdale D. The intracellular segment of the sodium channel beta 1 subunit is required for its efficient association with the channel alpha subunit. J. Neurochem. 2001, 76:1871-1878.
38. Miyazaki H., Oyama F., Wong H.-K., Kaneko K., Sakurai T., Tamaoka A., Nukina N. BACE1 modulates filopodia-like protrusions induced by sodium channel beta4 subunit. Biochem. Biophys. Res. Commun. 2007, 361:43-48.
39. O'Connor T., Sadleir K.R., Maus E., Velliquette R.A., Zhao J., Cole S.L., Eimer W.A., Hitt B., Bembinster L.A., Lammich S., Lichtenthaler S.F., Hébert S.S., De Strooper B., Haass C., Bennett D.A., Vassar R. Phosphorylation of the translation initiation factor eIF2alpha increases BACE1 levels and promotes amyloidogenesis. Neuron 2008, 60:988-1009.
40. + channel beta2 subunits is neuroprotective in a mouse model of multiple sclerosis. Mol. Cell. Neurosci. 2009, 40:143-155.
41. Palop J., Chin J., Mucke L. A network dysfunction perspective on neurodegenerative diseases. Nature 2006, 443:768-773.
42. Palop J., Chin J., Roberson E., Wang J., Thwin M., Bien-Ly N., Yoo J., Ho K., Yu G., Kreitzer A., Finkbeiner S., Noebels J., Mucke L. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007, 55:697-711.
43. Palop J., Mucke L. Epilepsy and cognitive impairments in Alzheimer disease. Arch. Neurol. 2009, 66:435-440.
44. Pertin M., Ji R., Berta T., Powell A., Karchewski L., Tate S., Isom L., Woolf C., Gilliard N., Spahn D., Decosterd I. Upregulation of the voltage-gated sodium channel beta2 subunit in neuropathic pain models: characterization of expression in injured and non-injured primary sensory neurons. J. Neurosci. 2005, 25:10970-10980.
45. Saura C., Choi S., Beglopoulos V., Malkani S., Zhang D., Shankaranarayana Rao B., Chattarji S., Kelleher R., Kandel E., Duff K., Kirkwood A., Shen J. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 2004, 42:23-36.
46. Savonenko A., Melnikova T., Laird F., Stewart K., Price D., Wong P. Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1-null mice. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5585-5590.
47. Selkoe D. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
48. Selkoe D., Kopan R., Notch, Presenilin: Regulated intramembrane proteolysis links development and degeneration. Annu. Rev. Neurosci. 2003.
49. Selkoe D., Wolfe M. Presenilin: running with scissors in the membrane. Cell 2007, 131:215-221.
50. Shen J., Bronson R.T., Chen D.F., Xia W., Selkoe D.J., Tonegawa S., Skeletal CNS defects in presenilin-1-deficient mice. Cell 1997, 89:629-639.
51. Sinha S., Anderson J., Barbour R., Basi G., Caccavello R., Davis D., Doan M., Dovey H., Frigon N., Hong J., Jacobson-Croak K., Jewett N., Keim P., Knops J., Lieberburg I., Power M., Tan H., Tatsuno G., Tung J., Schenk D., Seubert P., Suomensaari S., Wang S., Walker D., John V. Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature 1999, 402:537-540.
52. Takao M., Ghetti B., Murrell J.R., Unverzagt F.W., Giaccone G., Tagliavini F., Bugiani O., Piccardo P., Hulette C.M., Crain B.J., Farlow M.R., Heyman A. Ectopic white matter neurons, a developmental abnormality that may be caused by the PSEN1 S169L mutation in a case of familial AD with myoclonus and seizures. J. Neuropathol. Exp. Neurol. 2001, 60:1137-1152.
53. Tesco G, Koh Y.H., Kang E.L., Cameron A.N., Das S., Sena-Esteves M., Hiltunen M., Yang S.H., Zhong Z., Shen Y., Simpkins J.W., Tanzi R.E. Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 2007, 54:721-737.
54. Tiraboschi P., Hansen L.A., Thal L.J., Corey-Bloom J. The importance of neuritic plaques and tangles to the development and evolution of AD. Neurology 2004, 62:1984-1989.
55. Tyler S., Dawbarn D., Wilcock G., Allen S. Alpha- and beta-secretase: profound changes in Alzheimer's disease. Biochem. Biophys. Res. Commun. 2002, 299:373-376.
56. Vassar R., Bennett B., Babu-Khan S., Kahn S., Mendiaz E., Denis P., Teplow D., Ross S., Amarante P., Loeloff R., Luo Y., Fisher S., Fuller J., Edenson S., Lile J., Jarosinski M., Biere A., Curran E., Burgess T., Louis J., Collins F., Treanor J., Rogers G., Citron M. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999, 286:735-741.
57. Vassar R., Kovacs D.M., Yan R., Wong P.C. The beta-secretase enzyme BACE in health and Alzheimer's disease: regulation, cell biology, function, and therapeutic potential. J. Neurosci. 2009, 29:12787-12794.
58. Velez-Pardo C, Arellano J.I., Cardona-Gomez P., Jimenez Del Rio M., Lopera F., De Felipe J. CA1 hippocampal neuronal loss in familial Alzheimer's disease presenilin-1 E280A mutation is related to epilepsy. Epilepsia 2004, 45:751-756.
59. Wang H., Song L., Laird F., Wong P., Lee H. BACE1 knock-outs display deficits in activity-dependent potentiation of synaptic transmission at mossy fiber to CA3 synapses in the hippocampus. J. Neurosci. 2008, 28:8677-8681.
60. Waxman S.G. Acquired channelopathies in nerve injury and MS. Neurology 2001, 56:1621-1627.
61. Waxman S.G. Axonal conduction and injury in multiple sclerosis: the role of sodium channels. Nat. Rev. Neurosci. 2006, 7:932-941.
62. Waxman S.G., Dib-Hajj S., Cummins T.R., Black J.A. Sodium channels and their genes: dynamic expression in the normal nervous system, dysregulation in disease states (1). Brain Res. 2000, 886:5-14.
63. Wen Y, Onyewuchi O., Yang S., Liu R., Simpkins J.W. Increased beta-secretase activity and expression in rats following transient cerebral ischemia. Brain Res. 2004, 1009:1-8.
64. Willem M., Garratt A., Novak B., Citron M., Kaufmann S., Rittger A., Destrooper B., Saftig P., Birchmeier C., Haass C. Control of peripheral nerve myelination by the {beta}-secretase BACE1. Science 2006.
65. Wong H., Sakurai T., Oyama F., Kaneko K., Wada K., Miyazaki H., Kurosawa M., De Strooper B., Saftig P., Nukina N. {Beta} subunits of voltage-gated sodium channels are novel substrates of {beta}-site amyloid precursor protein-cleaving enzyme (BACE1) and {gamma}-secretase. J. Biol. Chem. 2005, 280:23009-23017.
66. Xiao Z., Ragsdale D., Malhotra J., Mattei L., Braun P., Schachner M., Isom L. Tenascin-R is a functional modulator of sodium channel beta subunits. J. Biol. Chem. 1999, 274:26511-26517.
67. Yan R., Bienkowski M., Shuck M., Miao H., Tory M., Pauley A., Brashier J., Stratman N., Mathews W., Buhl A., Carter D., Tomasselli A., Parodi L., Heinrikson R., Gurney M. Membrane-anchored aspartyl protease with Alzheimer's disease beta-secretase activity. Nature 1999, 402:533-537.
68. Yang L., Lindholm K., Yan R., Citron M., Xia W., Yang X., Beach T., Sue L., Wong P., Price D., Li R., Shen Y. Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat. Med. 2003, 9:3-4.
69. Yu H., Saura C., Choi S., Sun L., Yang X., Handler M., Kawarabayashi T., Younkin L., Fedeles B., Wilson M., Younkin S., Kandel E., Kirkwood A., Shen J. APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron 2001, 31:713-726.
70. Zayas E., Grossberg G. Treating the agitated Alzheimer patient. J. Clin. Psychiatry 1996, 7(57 Suppl):46-51. discussion 52-44.
71. Zhang C., Wu B., Beglopoulos V., Wines-Samuelson M., Zhang D., Dragatsis I., Sudhof T., Shen J. Presenilins are essential for regulating neurotransmitter release. Nature 2009, 460:632-636.
72. 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. Beta-site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer's disease pathogenesis. J. Neurosci. 2007, 27:3639-3649.