Small Aβ1-42 oligomer-induced membrane depolarization of neuronal and microglial cells: Role of N-methyl-D-aspartate receptors

Journal of Neuroscience Research

Volumn 93, Issue 3, 2015, Pages 475-486

  Morkuniene, Ramune ^a   Cizas, Paulius ^a   Jankeviciute, Silvija ^a   Petrolis, Robertas ^a   Arandarcikaite, Odeta ^a   Krisciukaitis, Algimantas ^a   Borutaite, Vilmante ^a  

^a LITHUANIAN UNIVERSITY OF HEALTH SCIENCES   (Lithuania)

Author keywords

A oligomers; Cell death; Membrane potential; Mitochondria; NMDA receptors

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; CALCIUM; DIZOCILPINE; GLUTAMIC ACID; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OLIGOMER; TUMOR NECROSIS FACTOR ALPHA; AMINO ACID RECEPTOR BLOCKING AGENT; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); DIZOCILPINE MALEATE; PEPTIDE FRAGMENT;

ADULT; ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN MITOCHONDRION; CONTROLLED STUDY; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MICROGLIA; NERVE CELL; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL DEATH; CEREBELLUM; DRUG EFFECTS; METABOLISM;

AMYLOID BETA-PEPTIDES; ANIMALS; CELL DEATH; CEREBELLUM; DIZOCILPINE MALEATE; EXCITATORY AMINO ACID ANTAGONISTS; MEMBRANE POTENTIALS; MICROGLIA; NEURONS; PEPTIDE FRAGMENTS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84921000387     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23510     Document Type: Article

References (51)

1. 2+ dysregulation and neuronal death through activation of ionotropic glutamate receptors. Cell Calcium 47:264-272.
2. Arispe N, Rojas E, Pollard HB. 1993. Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc Natl Acad Sci U S A 90:567-571.
3. A receptors and niflumic acid-sensitive chloride channels. Eur J Neurosci 21:103-112.
4. Bal-Price A, Brown GC. 2001. Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J Neurosci 21:6480-6491.
5. Blanchard BJ, Thomas VL, Ingram VM. 2002. Mechanism of membrane depolarization caused by the Alzheimer Abeta1-42 peptide. Biochem Biophys Res Commun 293:197-1203.
6. Boomgard R, Balen R. 1992. Methods for fast morphological image transforms using bitmapped binary images. CVGIP Graphical Models and Image Processing, vol 54.
7. Capone R, Quiroz FG, Prangkio P, Saluja I, Sauer AM, Bautista MR, Turner RS, Yang J, Mayer M. 2009. Amyloid-beta-induced ion flux in artificial lipid bilayers and neuronal cells: resolving a controversy. Neurotox Res 16:1-13.
8. Chen L, Yamada K, Nabeshima T, Sokabe M. 2006. Alpha7 nicotinic acetylcholine receptor as a target to rescue deficit in hippocampal LTP induction in beta-amyloid infused rats. Neuropharmacology 50:254-268.
9. Cizas P, Budvytyte R, Morkuniene R, Moldovan R, Broccio M, Losche M, Niaura G, Valincius G, Borutaite V. 2010. Size-dependent neurotoxicity of beta-amyloid oligomers. Arch Biochem Biophys 496:84-92.
10. Cižas P, Jekabsone A, Borutaite V, Morkūniene R. 2011. Prevention of amyloid-beta oligomer-induced neuronal death by EGTA, estradiol, and endocytosis inhibitor. Medicina (Kaunas) 47:107-112.
11. De Felice FG, Velasco PT, Lambert MP, Viola K, Fernandez SJ, Ferreira ST, Klein WL. 2007. Abeta oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J Biol Chem 282:11590-11601.
12. Decker H, Jurgensen S, Adrover MF, Brito-Moreira J, Bomfim TR, Klein WL, Epstein AL, De Felice FG, Jerusalinsky D, Ferreira ST. 2010. N-methyl-D-aspartate receptors are required for synaptic targeting of Alzheimer's toxic amyloid-β peptide oligomers. J Neurochem 115:1520-1529.
13. Demuro A, Mina E, Kayed R, Milton SC, Parker I, Glabe CG. 2005. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J Biol Chem 280:17294-17300.
14. 42 amyloid pores in Alzheimer's disease pathology. J Cell Biol 195:515-524.
15. Ferreira IL, Bajouco LM, Mota SI, Auberson YP, Oliveira CR, Rego AC. 2012. Amyloid beta peptide 1-42 disturbs intracellular calcium homeostasis through activation of GluN2B-containing N-methyl-D-aspartate receptors in cortical cultures. Cell Calcium 51:95-106.
16. Glenner GG, Wong CW. 1984. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 425:885-890.
17. Godfrey DA, Sun Y, Frisch C, Godfrey MA, Rubin AM. 2012. Depolarization-induced release of amino acids from the vestibular nuclear complex. Neurochem Res 37:732-739.
18. Gornal AG, Bardavill GJ, David MM. 1949. Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751-766.
19. Hardy JA, Higgins GA. 1992. Alzheimer's disease: the amyloid cascade hypothesis. Science 256:184-185.
20. Harkany T, Abraham I, Timmerman W, Laskay G, Tóth B, Sasvari M, Kónya C, Sebens JB, Korf J, Nyakas C, Zarandi M, Penke B, Luiten PG. 2000. Beta-amyloid neurotoxicity is mediated by a glutamate-triggered excitotoxic cascade in rat nucleus basalis. Eur J Neurosci 12:2735-2745.
21. Hung LW, Ciccotosto GD, Giannakis E, Tew DJ, Perez K, Masters CL, Cappai R, Wade JD, Barnham KJ. 2008. Amyloid-beta peptide (Abeta) neurotoxicity is modulated by the rate of peptide aggregation: Abeta dimers and trimers correlate with neurotoxicity. J Neurosci 28:11950-11958.
22. 2 derived from NADPH oxidase: a cell culture study. J Neuroinflammation 7:3-24.
23. Jekabsone A, Neher JJ, Borutaite V, Brown GC. 2007. Nitric oxide from neuronal nitric oxide synthase sensitises neurons to hypoxia-induced death via competitive inhibition of cytochrome oxidase. J Neurochem 103:346-356.
24. 42-induced impairment of synaptic plasticity. J Neurosci 32:3081-3087.
25. Kaindl AM, Degos V, Peineau S, Gouadon E, Chhor V, Loron G, Le Charpentier T, Josserand J, Ali C, Vivien D, Collingridge GL, Lombet A, Issa L, Rene F, Loeffler JP, Kavelaars A, Verney C, Mantz J, Gressens P. 2012. Activation of microglial N-methyl-D-aspartate receptors triggers inflammation and neuronal cell death in the developing and mature brain. Ann Neurol 72:536-549.
26. Kayed R, Sokolov Y, Edmonds B, McIntire TM, Milton SC, Hall JE, Glabe CG. 2004. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J Biol Chem 279:46363-46366.
27. A-receptors. Br J Pharmacol 91:601-608.
28. Koh SH, Noh MY, Kim SH. 2008. Amyloid-beta-induced neurotoxicity is reduced by inhibition of glycogen synthase kinase-3. Brain Res 1188:254-262.
29. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL. 1998. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95:6448-6453.
30. Li S, Hong S, Shepardso NE, Walsh DM, Shankar GM, Selkoe D. 2009. Soluble oligomers of amyloid β-protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 62:788-801.
31. Lin H, Bhatia R, Lal R. 2001. Amyloid beta protein forms ion channels: implications for Alzheimer's disease pathophysiology. FASEB J 15:2433-2444.
32. Lindberg C, Selenica ML, Westlind-Danielsson A, Schultzberg M. 2005. Beta-amyloid protein structure determines the nature of cytokine release from rat microglia. J Mol Neurosci 27:1-12.
33. Lioudyno MI, Broccio M, Sokolov Y, Rasool S, Wu J, Alkire MT, Liu V, Kozak JA, Dennison PR, Glabe CG, Losche M, Hall JE. 2012. Effect of synthetic Aβ peptide oligomers and fluorinated solvents on Kv1.3 channel properties and membrane conductance. PLoS One 7:e35090.
34. Ma QL, Yang F, Rosario ER, Ubeda OJ, Beech W, Gant DJ, Chen PP, Hudspeth B, Chen C, Zhao Y, Vinters HV, Frautschy SA, Cole GM. 2009. Beta-amyloid oligomers induce phosphorylation of tau and inactivation of insulin receptor substrate via c-Jun N-terminal kinase signaling: suppression by omega-3 fatty acids and curcumin. J Neurosci 29:9078-9089.
35. Maezawa I, Zimin PI, Wulff H, Jin LW. 2011. Amyloid-beta protein oligomer at low nanomolar concentrations activates microglia and induces microglial neurotoxicity. J Biol Chem 286:3693-3706.
36. Mairet-Coello G, Courchet J, Pieraut S, Courchet V, Maximov A, Polleux F. 2013. The CAMKK2-AMPK kinase pathway mediates the synaptotoxic effects of Aβ oligomers through Tau phosphorylation. Neuron 78:94-108.
37. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
38. Mukhamedyarov MA, Grishin SN, Yusupova ER, Zefirov AL, Palots A. 2009. Alzheimer's beta-amyloid-induced depolarization of skeletal muscle fibers: implications for motor dysfunctions in dementia. Cell Physiol Biochem 23:109-114.
39. Murugan M, Sivakumar V, Lu J, Ling EA, Kaur C. 2011. Expression of N-methyl D-aspartate receptor subunits in amoeboid microglia mediates production of nitric oxide via NF-κB signaling pathway and oligodendrocyte cell death in hypoxic postnatal rats. Glia 59:521-539.
40. Neniskyte U, Neher JJ, Brown GC. 2011. Neuronal death induced by nanomolar amyloid beta is mediated by primary phagocytosis of neurons by microglia. J Biol Chem 286:39904-39913.
41. - currents regulate steady-state and dynamic membrane potentials in cultured rat microglia. J Physiol 567:869-890.
42. Ono K, Condron MM, Teplow DB. 2009. Structure neurotoxicity relationships of amyloid beta-protein oligomers. Proc Natl Acad Sci U S A 106:14745-14750.
43. Renner M, Lacor PN, Velasco PT, Xu J, Contractor A, Klein WL, Triller A. 2010. Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5. Neuron 66:739-754.
44. Selkoe DJ. 1991. The molecular pathology of Alzheimer's disease. Neuron 6:487-498.
45. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe D. 2008. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14:837-842.
46. Sokolov Y, Kozak JA, Kayed R, Chanturiya A, Glabe C, Hall JE. 2006. Soluble amyloid oligomers increase bilayer conductance by altering dielectric structure. J Gen Physiol 128:637-647.
47. Talantova M, Sanz-Blasco S, Zhang X, Xia P, Akhtar MW. 2013. Aβ induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc Natl Acad Sci U S A 110:E2518-E2527.
48. Vale C, Alfonso A, Sunol C, Vieytes MR, Botana LM. 2006. Modulation of calcium entry and glutamate release in cultured cerebellar granule cells by palytoxin. J Neurosci Res 83:1393-1406.
49. Valincius G, Heinrich F, Budvytyte R, Vanderah DJ, McGillivray DJ, Sokolov Y, Hall JE. 2008. Soluble amyloid beta-oligomers affect dielectric membrane properties by bilayer insertion and domain formation: implications for cell toxicity. Biophys J 95:4845-4861.
50. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ. 2002. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539.
51. Zheng L, Godfrey DA, Waller HJ, Waller HJ, Godfrey TG, Chen K, Sun Y. 2000. Effects of high-potassium-induced depolarization on amino acid chemistry of the dorsal cochlear nucleus in rat brain slices. Neurochem Res 25:823-835.