Interaction of metal chelators with different molecular forms of acetylcholinesterase and its significance in Alzheimer's disease treatment

Proteins: Structure, Function and Bioinformatics

Volumn 81, Issue 7, 2013, Pages 1179-1191

  Chitra, Loganathan ^a   Kumar, Chinnadurai Raj ^a   Basha, Haleema M ^a   Ponne, Saravanaraman ^a   Boopathy, Rathanam ^a  

^a BHARATHIAR UNIVERSITY   (India)

Author keywords

1,10 phenanthroline; Amyloid beta peptide; Aryl acylamidase; Hydrophobic interaction; Peripheral anionic site

Indexed keywords

1,10 PHENANTHROLINE; ACETYLCHOLINESTERASE; ARYL ACYLAMIDASE; CHELATING AGENT; ESTERASE; HYDROGEN; TRYPTOPHAN; TYROSINE;

ALZHEIMER DISEASE; ARTICLE; BINDING AFFINITY; CHELATION; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROGEN BOND; HYDROPHOBICITY; IC 50; INHIBITION KINETICS; MOLECULAR BIOLOGY; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PERIPHERAL ANIONIC SITE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION;

ACETYLCHOLINESTERASE; ALZHEIMER DISEASE; AMIDOHYDROLASES; AMYLOID BETA-PEPTIDES; CHELATING AGENTS; CHOLINESTERASE INHIBITORS; ESTERASES; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; METALS; MOLECULAR DYNAMICS SIMULATION; PHENANTHROLINES;

EID: 84879419961     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24267     Document Type: Article

References (59)

1. Taylor P.The cholinesterases. J Biol Chem 1991;266:4025-4028.
2. Soreq H, Seidman S. Acetylcholinesterase-new roles for an old actor. Nat Rev Neurosci 2001;2:294-302.
3. Small DH, Michaelson S, Sberna G. Non-classical actions of cholinesterases: role in cellular differentiation, tumorigenesis and Alzheimer's disease. Neurochem Int 1996;28:453-483.
4. Balasubramanian AS, Bhanumathy CD. Noncholinergic functions of cholinesterases. FASEB J 1993;7:1354-1358.
5. George ST, Balasubramanian AS. The identity of the serotonin-sensitive aryl acylamidase with acetylcholinesterase from human erythrocytes, sheep basal ganglia and electric eel. Eur J Biochem 1980;111:511-524.
6. Soto C, Branes MC, Alvarez J, Inestrosa NC. Structural determinants of the Alzheimer's amyloid beta-peptide. J Neurochem 1994;63:1191-1198.
7. Selkoe DJ. Amyloid beta-protein and the genetics of Alzheimer's disease. J Biol Chem 1996;271:18295-18298.
8. Ulrich J, Meier-Ruge W, Probst A, Meier E, Ipsen S. Senile plaques: staining for acetylcholinesterase and A4 protein: a comparative study in the hippocampus and entorhinal cortex. Acta Neuropathol 1990;80:624-628.
9. Geula C, Mesulam M. Special properties of cholinesterases in the cerebral cortex of Alzheimer's disease. Brain Res 1989;498:185-189.
10. Moran MA, Mufson EJ, Gomez-Ramos P. Colocalization of cholinesterases with beta amyloid protein in aged and Alzheimer's brains. Acta Neuropathol 1993;85:362-369.
11. Inestrosa NC, Alvarez A, Perez CA, Moreno RD, Vicente M, Linker C, Casanueva OI, Soto C, Garrido J. Acetylcholinesterase accelerates assembly of amyloid-beta-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron 1996;16:881-891.
12. Alvarez A, Bronfman F, Perez CA, Vicente M, Garrido J, Inestrosa NC. Acetylcholinesterase, a senile plaque component, affects the fibrillogenesis of amyloid-beta-peptides. Neurosci Lett 1995;201:49-52.
13. Alvarez A, Alarcon R, Opazo C, Campos EO, Munoz FJ, Calderon FH, Dajas F, Gentry MK, Doctor BP, De Mello FG, Inestrosa NC. Stable complexes involving acetylcholinesterase and amyloid-beta peptide change the biochemical properties of the enzyme and increase the neurotoxicity of Alzheimer's fibrils. J Neurosci 1998;18:3213-3223.
14. Munoz FJ, Inestrosa NC. Neurotoxicity of acetylcholinesterase amyloid beta-peptide aggregates is dependent on the type of Abeta peptide and the AChE concentration present in the complexes. FEBS Lett 1999;450:205-209.
15. Dinamarca MC, Arrazola M, Toledo E, Cerpa WF, Hancke J, Inestrosa NC. Release of acetylcholinesterase (AChE) from beta-amyloid plaques assemblies improves the spatial memory impairments in APP-transgenic mice. Chemico-biological interactions 2008;175:142-149.
16. Fishman EB, Siek GC, MacCallum RD, Bird ED, Volicer L, Marquis JK. Distribution of the molecular forms of acetylcholinesterase in human brain: alterations in dementia of the Alzheimer type. Ann Neurol 1986;19:246-252.
17. Saez-Valero J, Sberna G, McLean CA, Small DH. Molecular isoform distribution and glycosylation of acetylcholinesterase are altered in brain and cerebrospinal fluid of patients with Alzheimer's disease. J Neurochem 1999;72:1600-1608.
18. Arendt T, Bruckner MK, Lange M, Bigl V. Changes in acetylcholinesterase and butyrylcholinesterase in Alzheimer's disease resemble embryonic development-a study of molecular forms. Neurochem Int 1992;21:381-396.
19. Wright CI, Guela C, Mesulam MM. Protease inhibitors and indoleamines selectively inhibit cholinesterases in the histopathologic structures of Alzheimer disease. Proc Natl Acad Sci USA 1993;90:683-686.
20. Boopathy R, Layer PG. Aryl acylamidase activity on acetylcholinesterase is high during early chicken brain development. Protein J 2004;23:325-333.
21. Rajesh RV, Chitra L, Layer PG, Boopathy R. The aryl acylamidase activity is much more sensitive to Alzheimer drugs than the esterase activity of acetylcholinesterase in chicken embryonic brain. Biochimie 2009;91:1087-1094.
22. Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR. Copper, iron and zinc in Alzheimer's disease senile plaques. J Neurol Sci 1998;158:47-52.
23. Huang X, Atwood CS, Moir RD, Hartshorn MA, Vonsattel JP, Tanzi RE, Bush AI. Zinc-induced Alzheimer's Abeta1-40 aggregation is mediated by conformational factors. J Biol Chem 1997;272:26464-26470.
24. Cherny RA, Atwood CS, Xilinas ME, Gray DN, Jones WD, McLean CA, Barnham KJ, Volitakis I, Fraser FW, Kim Y, Huang X, Goldstein LE, Moir RD, Lim JT, Beyreuther K, Zheng H, Tanzi RE, Masters CL, Bush AI. Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 2001;30:665-676.
25. +2-binding site in acetylcholinesterase. Biochimie 2009;91:526-532.
26. Karnovsky MJ, Roots L. A 'direct-coloring' thiocholine method for cholinesterases. J Histochem Cytochem 1964;12:219-221.
27. Ellman GL, Courtney KD, Andres V, Jr., Feather-Stone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961;7:88-95.
28. Hoagland RE, Graf G. Nitroacetanilides as chromogenic substrates for assaying de-acetylating activity: the isolation and partial purification of aryl acylamidases from erepsin and tulip. Enzymologia 1971;41:313-319.
29. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
30. Lineweaver H, Burk D. The determination of enzyme dissociation constants. J Am Chem Soc 1934;56:658-666.
31. Dixon M. The determination of enzyme inhibitor constants. Biochem J 1953;55:170-171.
32. Kryger G, Harel M, Giles K, Toker L, Velan B, Lazar A, Kronman C, Barak D, Ariel N, Shafferman A, Silman I, Sussman JL. Structures of recombinant native and E202Q mutant human acetylcholinesterase complexed with the snake-venom toxin fasciculin-II. Acta Crystallogr D Biol Crystallogr 2000;56:1385-1394.
33. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A. Comparative protein structure modeling using MODELLER. Curr Protoc Protein Sci 2007; Chapter 2:Unit 2. 9.
34. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr26:283-291.
35. Wallace AC, Laskowski RA, Thornton JM. LIGPLOT:a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 1995;8:127-134.
36. Berk Hess CK, David van der Spoel, Erik Lindahl. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 2008;4:13.
37. Bon S, Vigny M, Massoulie J. Asymmetric and globular forms of acetylcholinesterase in mammals and birds. Proc Natl Acad Sci USA 1979;76:2546-2550.
38. Rajesh RV, Layer PG, Boopathy R. High aryl acylamidase activity associated with cobra venom acetylcholinesterase: biological significance. Biochimie 2009;91:1450-1456.
39. Bush AI, Pettingell WH, Multhaup GD, Paradis M, Vonsattel JP, Gusella JF, Beyreuther K, Masters CL, Tanzi RE. Rapid induction of Alzheimer A beta amyloid formation by zinc. Science 1994;265:1464-1467.
40. Talmard C, Yona RL, Faller P. Mechanism of zinc(II)-promoted amyloid formation: zinc(II) binding facilitates the transition from the partially α-helical conformer to aggregates of amyloid β protein(1-28). J Biol Inorg Chem 2009;14:449-455.
41. Cherny RA, Legg JT, McLean CA, Fairlie DP, Huang X, Atwood CS, Beyreuther K, Tanzi RE, Masters CL, Bush AI. Aqueous dissolution of Alzheimer's disease Abeta amyloid deposits by biometal depletion. J Biol Chem 1999;274:23223-23228.
42. Wermuth B, Brodbeck U. Inhibition of acetylcholinesterase activity by aromatic chelating agents. Eur J Biochem 1973;35:499-506.
43. Barak D, Ordentlich A, Stein D, Yu QS, Greig NH, Shafferman A. Accommodation of physostigmine and its analogues by acetylcholinesterase is dominated by hydrophobic interactions. Biochem J 2009;417:213-222.
44. Gerber E, Bredy A, Kahl R. Ortho-phenanthroline modulates enzymes of cellular energy metabolism. Toxicology 1996;110:85-93.
45. Mazumder A, Gupta M, Perrin DM, Sigman DS, Rabinovitz M, Pommier Y. Inhibition of human immunodeficiency virus type 1 integrase by a hydrophobic cation: the phenanthroline-cuprous complex. AIDS Res Hum Retroviruses 1995;11:115-125.
46. Harel M, Schalk I, Ehret-Sabatier L, Bouet F, Goeldner M, Hirth C, Axelsen PH, Silman I, Sussman JL. Quaternary ligand binding to aromatic residues in the active-site gorge of acetylcholinesterase. Proc Natl Acad Sci USA 1993;90:9031-9035.
47. Felder CE, Harel M, Silman I, Sussman JL. Structure of a complex of the potent and specific inhibitor BW284C51 with Torpedo californica acetylcholinesterase. Acta Crystallogr D Biol Crystallogr 2002;58:1765-1771.
48. Moore DE, Hess GP. Acetylcholinesterase-catalyzed hydrolysis of an amide. Biochemistry 1975;14:2386-2389.
49. Majumdar R, Balasubramanian AS. Chemical modification of acetylcholinesterase from eel and basal ganglia: effect on the acetylcholinesterase and aryl acylamidase activities. Biochemistry 1984;23:4088-4093.
50. Costagli C, Galli A. Inhibition of cholinesterase-associated aryl acylamidase activity by anticholinesterase agents: focus on drugs potentially effective in Alzheimer's disease. Biochem Pharmacol 1998;55:1733-1737.
51. Wiesner J, Kriz Z, Kuca K, Jun D, Koca J. Influence of the acetylcholinesterase active site protonation on omega loop and active site dynamics. J Biomol Struct Dyn 2010;28:393-403.
52. Bourne Y, Taylor P, Radic Z, Marchot P. Structural insights into ligand interactions at the acetylcholinesterase peripheral anionic site. EMBO J 2003;22:1-12.
53. Barak D, Ordentlich A, Bromberg A, Kronman C, Marcus D, Lazar A, Ariel N, Velan B, Shafferman A. Allosteric modulation of acetylcholinesterase activity by peripheral ligands involves a conformational transition of the anionic subsite. Biochemistry 1995;34:15444-15452.
54. Cavalli A, Bottegoni G, Raco C, De Vivo M, Recanatini M. A computational study of the binding of propidium to the peripheral anionic site of human acetylcholinesterase. J Med Chem 2004;47:3991-3999.
55. Reyes AE, Perez DR, Alvarez A, Garrido J, Gentry MK, Doctor BP, Inestrosa NC. A monoclonal antibody against acetylcholinesterase inhibits the formation of amyloid fibrils induced by the enzyme. Biochem Biophys Res Commun 1997;232:652-655.
56. Bartolini M, Bertucci C, Cavrini V, Andrisano V. beta-Amyloid aggregation induced by human acetylcholinesterase: inhibition studies. Biochem Pharmacol 2003;65:407-416.
57. Caragounis A, Du T, Filiz G, Laughton KM, Volitakis I, Sharples RA, Cherny RA, Masters CL, Drew SC, Hill AF, Li QX, Crouch PJ, Barnham KJ, White AR. Differential modulation of Alzheimer's disease amyloid beta-peptide accumulation by diverse classes of metal ligands. Biochem J 2007;407:435-450.
58. Zheng H, Youdim MB, Fridkin M. Site-activated multifunctional chelator with acetylcholinesterase and neuroprotective-neurorestorative moieties for Alzheimer's therapy. J Med Chem 2009;52:4095-4098.
59. Zheng H, Youdim MB, Fridkin M. Site-activated chelators targeting acetylcholinesterase and monoamine oxidase for Alzheimer's therapy. ACS Chem Biol 2010;5:603-610.