Acetylcholinesterase induces the expression of the β-amyloid precursor protein in glia and activates glial cells in culture

Neurobiology of Disease

Volumn 14, Issue 3, 2003, Pages 447-457

  Von Bernhardi, Rommy ^a,b   Ramírez, Gigliola ^a,b   De Ferrari, Giancarlo V ^a   Inestrosa, Nibaldo C ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD DE LOS ANDES   (Chile)

Author keywords

Acetylcholinesterase; AChE inhibitors; Alzheimer's disease; Glia; iNOS; APP

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN; NITRIC OXIDE SYNTHASE; PROTEIN PRECURSOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BINDING AFFINITY; CELL ACTIVATION; CELL METABOLISM; CONTROLLED STUDY; GLIA CELL; IMMUNOCYTOCHEMISTRY; MICROGLIA; NEWBORN; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; RAT; REDUCTION; TISSUE CULTURE;

EID: 0347479362     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2003.08.014     Document Type: Article

References (70)

1. Alvarez A., Alarcón R., Opazo C., Campos E.O., Muñoz F.J., Calderón F.H., Dajas F., Gentry M.K., Doctor B.P., De Mello F.G., Inestrosa N.C. Stable complexes involving acetylcholinesterase and amyloid-b peptide change the biochemical properties of the enzyme and increase the neurotoxicity of Alzheimer's fibrils. J Neurosci. 18:1998;3113-3223.
2. Alvarez A., Opazo C., Alarcón R., Garrido J., Inestrosa N.C. Acetylcholinesterase promotes the aggregation of amyloid-β-peptide fragments by forming a complex with the growing fibrils. J. Mol. Biol. 272:1997;348-361.
3. Araki W., Nakamura S., Tanaka S., Kimura J., Ueda K. Separation of protease activity from acetylcholinesterase of electric eel. Neurochem. Int. 19:1991;537-541.
4. Banati R.B., Gehrmann J., Caech C., Mönning V., Jones L.L., König G., Beyreuther K., Kreutzberg G.W. Early and rapid de novo synthesis of Alzheimer βA4-amyloid precursor protein (APP) in activated microglia. Glia. 9:1993;199-210.
5. Banati R.B., Gehrmann J., Schubert P., Kreutzberg G.W. Cytotoxicity of microglia. Glia. 7:1993;111-118.
6. Barron K.D. The microglial cell. A historical review. J. Neurol. Sci. 134:1995;57-68.
7. Bartoli M., Bertucci C., Cavrini V., Andrisano V. Beta-amyloid aggregation induced by human acetylcholinesterase inhibition studies . Biochem. Pharmacol. 65:2003;407-416.
8. Beeri R., Le Novere N., Mervis R., Huberman T., Grauer E., Changeux J.P., Soreq H. Enhanced hemicholinium binding and attenuated dendrite branching in cognitively impaired acetylcholinesterase-transgenic mice. J. Neurochem. 69:1997;2441-2451.
9. Beyreuther K., Multhaup G., Mönning U., Sandbrink R., Beher D., Hesse L., Small D.H., Masters C.L. Regulation of APP expression, biogenesis and metabolism by extracellular matrix and cytokines. Ann. N.Y. Acad. Sci. 777:1996;74-76.
10. Birikh K.R., Sklan E.H., Shoham S., Soreq H. Interaction of "readthrough" acetylcholinesterase with RACK1 and PKCβII correlates with intensified fear-induced conflict behavior. Proc. Natl. Acad. Sci. USA. 100:2003;283-288.
11. Bois R.T., Hummel R.G., Dettbarn W.D., Laskowski M.B. Presynaptic and postsynaptic neuromuscular effects of a specific inhibitor of acetylcholinesterase. J. Pharmacol. Exp. Ther. 215:1980;53-59.
12. Bronfman F.C., Fernández H.L., Inestrosa N.C. Amyloid precursor protein fragment and acetylcholinesterase increase with cell confluence and differentiation in a neuronal cell line. Exp. Cell Res. 229:1996;93-99.
13. Bronfman F.C., Soto C., Tapia L., Tapia V., Inestrosa N.C. Extracellular Matrix regulates the amount of the β-amyloid precursor protein and its amyloidogenic fragments. J. Cell. Physiol. 166:1996;360-369.
14. Calderón F., von Bernhardi R., De Ferrari G., Luza S., Inestrosa N.C. Toxic effects of acetylcholinesterase on neuronal and glial-like cells in vitro. Mol. Psychatry. 3:1998;247-255.
15. Campos E.O., Alvarez A., Inestrosa N.C. Brain acetylcholinesterase promotes amyloid-beta-peptide aggregation but does not hydrolize amyloid precursor protein peptides. Neurochem. Res. 23:1998;135-140.
16. Carroll R., Emmerling M.R. Identification of trypsin-like activity in commercial preparations of eel acetylcholinesterase. Biochem. Biophys. Res. Commun. 181:1991;358-362.
17. Checler F., Grassi J., Vincent J.-P. Cholinesterase display genuine arylacylamidasa activity but are totally devoid of intrinsic peptidase activities. J. Neurochem. 62:1994;756-763.
18. Checler F., Vincent J.-P. Peptidasic activities associated with acetylcholinesterase are due to contaminating enzymes. J. Neurochem. 53:1989;924-928.
19. Chen J.-W., Lou Y.-L., Hwang M.-Y., Peng F.-C., Ling K.-H. Territrem B, a tremogenic mycotoxin that inhibits acetylcholinesterase with a noncovalent yet irreversible binding mechanism. J. Biol. Chem. 274:1999;34916-34923.
20. Chong Y.H., Suh Y.H. Amyloidogenic processing of alzheimer's amyloid precursor protein in vitro and its modulation by metal ions and tacrine. Life Sci. 59:1996;545-557.
21. Darreh-Shori T., Almkvist O., Guan Z.Z., Garlind A., Strandberg B., Svensson A.L., Soreq H., Hellstrom-Lindahl E., Nordberg A. Sustained cholinesterase inhibition in AD patients receiving rivastigmine for 12 months. Neurology. 59:2002;563-572.
22. De Ferrari G.V., Canales M.A., Shin I., Weiner L.M., Silman I., Inestrosa N.C. A structural motif of acetylcholinesterase that promotes amyloid-β-peptide fibril formation. Biochemistry. 40:2001;10447-10457.
23. De la Hoz D., Doctor B.P., Ralston J.S., Rush R.S., Wolfe A.D. A simplified procedure for the purification of large quantities of fetal bovine serum acetylcholinesterase. Life Sci. 39:1986;195-199.
24. Dickson D.W., Lee S.C., Mattiace L.A., Yen S.H., Brosnan C. Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia. 7:1993;75-83.
25. Doctor B.P., Chapman T.C., Christner C.E., Deal C.D., De La Hoz D.M., Gentry M.K., Ogert R.A., Rush R.S., Smyth K.K., Wolfe A.D. Complete amino acid sequence of fetal bovine serum acetylcholinesterase and its comparison in various regions with other cholinesterases. FEBS Letk. 266:1990;123-127.
26. Geula C., Mesulam M.M. Cholinergic systems in Alzheimer's disease. Terry R.D., Katzman R., Bick K.L., Sisodia S.S. Alzheimer Disease. 1999;269-292 Lippincott Williams & Wilkins, Philadelphia.
27. Giulian D. Amoeboid microglia as effectors of inflammation in the central nervous system. J. Neurosci. Res. 18:1987;155-171.
28. Giulian D., Baker T.J. Characterization of amoeboid microglia isolated from developing mammalian brain. J. Neurosci. 6:1986;2163-2178.
29. Goodwin J.L., Uemura E., Cunnick J.E. Microglial release of nitric oxide by the synergistic action of beta-amyloid and IFN-gamma. Brain. Res. 692:1995;207-214.
30. Gray C.W., Patel A.J. Regulation of β-amyloid precursor protein isoform mRNAs by transforming growth factor-β1 and interleukin-1β in astrocytes. Mol. Brain. Res. 19:1993;251-256.
31. Griffin W.S.T., Sheng J.G., Roberts G.W., Mark R.E. Interleukin-1 expression is different plaque types in Alzheimer's disease significance in plaque evolution . J. Neuropathol. Exp. Neurol. 54:1995;276-281.
32. Hu J., Akama K.T., Krafft G.A., Chromy B.A., Van Eldik L.J. Amyloid-b peptide activates cultured astrocytes morphological alterations, cytokine induction and nitric oxide release . Brain Res. 785:1998;195-206.
33. Inestrosa N.C., Alvarez A., Pérez C., Moreno D., Vicente M., Linker C., et al. Acetylcholinesterase accelerates assembly of amyloid-β peptides into Alzheimer's fibrils possible role of the peripheral site of the enzyme . Neuron. 16:1996;881-891.
34. Inestrosa N.C., Roberts W.L., Marshall T.L., Rosenberry T.L. Acetylcholinesterase from bovine caudate nucleus is attached to membranes by a novel subunit distinct from those of acetylcholinesterases in other tissues. J. Biol. Chem. 262:1987;4441-4444.
35. Kaufer D., Friedman A., Seidman S., Soreq H. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature. 393:1998;373-377.
36. Kreimer D.I., Shnyrov V.L., Villar E., Silman I., Weiner L. Irreversible thermal denaturation of Torpedo californica acetylcholinesterase. Protein Sci. 4:1995;2349-2357.
37. Klegeris A., Walker D.G., McGeer P.L. Activation of macrophages by Alzheimer beta amyloid peptide. Biochem. Biophys. Res. Commun. 199:1994;984-991.
38. Leanza G. Chronic elevation of amyloid precursor protein expression in the neocortex and hippocampus of rats with selective cholinergic lesions. Neurosci. Lett. 257:1998;53-56.
39. Lee S.C., Liu W., Brosnan C.F., Dickson D.W. GM-CSF promotes proliferation of human fetal and adult microglia in primary cultures. Glia. 12:1994;309-318.
40. Lemere C.A., Blustzjan J.K., Yamaguchi H., Wisniewski T., Saido T.C., Selkoe D.J. Sequence of deposition of heterogeneous amyloid β-peptides and Apo E in Down syndrome implications for initial events in amyloid plaque formation . Neurobiol. Dis. 3:1996;16-32.
41. Li Y., Liu L., Kang J., Sheng J.G., Barger S.W., Mrak R.E., Griffin W.S.T. Neuronal-glial interactions mediated by interleukin-1 enhance neuronal acetylcholinesterase activity and mRNA expression. J. Neurosci. 20:2000;149-155.
42. Lin L., LeBlanc C.J., Deacon T.W., Isacson O. Chronic cognitive deficits and amyloid precursor protein elevation after selective immunotoxin lesions of the basal forebrain cholinergic system. NeuroReport. 9:1998;547-552.
43. Liu Y., Peterson D.A., Kimura H., Schubert D. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J. Neurochem. 69:1997;2285-2293.
44. Lyons C.R., Orloff G.J., Cunningham J.M. Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J. Biol. Chem. 267:1992;6370-6374.
45. Mallerder W.D., Szegletes T., Rosenberry T.L. Organophosphorylation of acetylcholinesterase in the presence of peripheral site ligands. Distinct effects of propidium and fasciculin. J. Biol. Chem. 274:1999;8491-8499.
46. Marzolo M.P., von Bernhardi R., Inestrosa N.C. Mannose receptor is present in a functional state in rat microglial cells. J. Neurosci. Res. 58:1999;387-395.
47. Meda L., Cassatella M.A., Szendrei G.I., Otvos J.L., Baron P., Villalba M., Ferrari D., Rossi F. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature. 374:1995;647-650.
48. Meshorer E., Erb C., Gazit R., Pavlovsky L., Kaufer D., Friedman A., Glick D., Ben-Arie N., Soreq H. Alternative splicing and neuritic mRNA translocation under long-term neuronal hypersensitivity. Science. 295:2002;508-512.
49. Mönning U., Sandbrink R., Banati R.B., Masters C.L., Beyreuther K. Transforming growth factor β mediates increase of mature transmembrane amyloid precursor protein in microglial cells. FEBS. Lett. 342:1994;267-272.
50. Morán M.A., Mufson E.J., Gómez-Ramos P. Colocalization of cholinesterases with β-amyloid protein in aged and Alzheimer's brain. Acta Neuropathol. 85:1993;362-369.
51. Mori F., Lai C.C., Fusi F., Giacobini E. Cholinesterase inhibitors increase secretion of APPs in rat brain cortex. NeuroReport. 6:1995;633-636.
52. Mrak R.E., Griffin W.S. Interleukin-1, neuroinflammation, and Alzheimer's disease. Neurobiol. Aging. 22:2001;903-908.
53. Nitsch R.M., Slacke B.E., Farber S.A., Schluz J.G., Deng M., Kim C., Borghesani P.R., Korver W., Wurtman R.J., Growdon J.H. Regulation of proteolytic processing of the amyloid beta-protein precursor of Alzheimer's disease in transfected cell lines and in brain slices. J. Neural Transm. Suppl. 44:1994;21-27.
54. Paresce D., Ghosh R., Maxfield F. Microglial cells internalize aggregates of the Alzheimer disease amyloid-β protein via a scavenger receptor. Neuron. 17:1996;553-565.
55. Ralston J.S., Rush R.S., Doctor B.P., Wolfe A.D. Acetylcholinesterase from fetal bovine serum. Purification and characterization of soluble G4 enzyme. J. Biol. Chem. 260:1984;4312-4318.
56. Rees, T., Hammond, O., Soreq, H., Younkin, S., Brimijoin, S., 2003. Acetylcholinesterase promotes beta-amyloid plaques in cerebral cortex. Neurobiol. Aging, in press.
57. Sastry B.V., Singh G., Loo P., Janson V.E. Evaluation of the nature of rat retinal acetylcholinesterase using a specific substrate and a specific inhibitor. J. Ocul. Pharmacol. Ther. 11:1995;401-409.
58. Sberna G., Saez-Valero J., Beyreuther K., Masters C.L., Small D.H. The amyloid beta-protein of alzheimer's disease increases acetylcholinesterase expression by increasing intracellular calcium in embryonal carcinoma P19 cells. J. Neurochem. 69:1997;1177-1184.
59. Sberna G., Saez-Valero J., Li Q.X., Czech C., Beyreuther K., Masters C.L., McLean C.A., Small D.H. Acetylcholinesterase is increased in the brains of transgenic mice expressing the C-terminal fragment (CT100) of the β-amyloid protein precursor of Alzheimer's disease. J. Neurochem. 71:1998;723-731.
60. Schubert D., Jin L., Saitoh T., Cole G.M. The regulation of amyloid β protein precursor secretion and its modulatory role in cell adhesion. Neuron. 3:1989;689-694.
61. Seidman S., Sternfeld M., Ben Aziz-Aloya R., Timberg R., Kaufer-Nachum D., Soreq H. Synaptic and epidermal accumulations of human acetylcholinesterase are encoded by alternative 3′-terminal exons. Mol. Cell. Biol. 15:1995;2993-3002.
62. Shi J., Xiang Y., Simpkins J.W. Hypoglycemia enhances the expression of mRNA encoding β-amyloid precursor protein in rat primary cortical astroglial cells. Brain Res. 772:1997;247-251.
63. Shohami E., Kaufer D., Chen Y., Seidman S., Cohen O., Ginzberg D., Melamed-Book N., Yirmiya R., Soreq H. Antisense prevention of neuronal damages following head injury in mice. J. Mol. Med. 78:2000;228-236.
64. Sternfeld M., Shoham S., Klein O., Flores-Flores C., Evron T., Idelson G.H., Kitsberg D., Patrick J.W., Soreq H. Excess "read-through" acetylcholinesterase attenuates but the "synaptic" variant intensifies neurodeterioration correlates. Proc. Natl. Acad. Sci. USA. 97:2000;8647-8652.
65. Szegletes T., Mallender W.D., Rosenberry T.L. Nonequilibrium analysis alters the mechanistic interpretation of inhibition of acetylcholinesterase by peripheral site ligand. Biochemistry. 37:1998;4206-4216.
66. Taylor P., Lappi S. Interaction of fluorescence probes with acetycholinesterase. The site and specificity of propidium binding. Biochemistry. 14:1975;1989-1997.
67. von Bernhardi R., Ramírez G. Microglia-astrocyte interaction in Alzheimer's disease friends or foes for the nervous system? Biol. Res. 34:2001;123-128.
68. von Bernhardi R., Ramírez G., Matile H., Döbeli H. Immobilized amyloid precursor protein constructs a tool for the in vitro screening of glial cell reactivity . Eur. J. Neurosci. 14:2001;946-956.
69. Weldon D.T., Rogers S.D., Ghilardi J.R., Finke M.P., Clearly J.P., O'Hare E., Esler W.P., Maggio J.E., Mantyh P.W. Fibrillar β-amyloid induces microglial phagocytosis, expression of inducible nitric oxide synthase, and loss of a select population of neurons in the rat CNS in vivo. J. Neurosci. 18:1998;2161-2173.
70. Wright C.I., Geula C., Mesulam M.M. Neurological cholinesterases in the normal brain and in Alzheimer's disease relationship to plaques, tangles, and patterns of selective vulnerability . Ann. Neurol. 34:1993;373-384.