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Research Paper

A method for the efficient evaluation of substrate-based cholinesterase imaging probes for Alzheimer’s disease

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Article: 2225797 | Received 24 Mar 2023, Accepted 10 Jun 2023, Published online: 26 Jun 2023

References

  • Ferrari C, Sorbi S. The complexity of Alzheimer’s disease: an evolving puzzle. Physiol Rev. 2021;101(3):1047–1081. doi:10.1152/physrev.00015.2020
  • Alzheimer’s Association. Alzheimer’s disease facts and figures. Alzheimers Dement. 2022; 18(4):700–789.
  • Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, Bergström M, Savitcheva I, Huan G-F, Estrada S, et al. Imaging brain amyloid in Alzheimer’s disease with Pittsburgh compound-B. Ann Neurol. 2004;55(3):306–319. doi:10.1002/ana.20009
  • Chapleau M, Iaccarino L, Soleimani-Meigooni D, Rabinovici GD. The role of amyloid PET in imaging neurodegenerative disorders: a review. J Nucl Med. 2022;63(Suppl 1):13S–19S. doi:10.2967/jnumed.121.263195
  • Leuzy A, Chiotis K, Lemoine L, Gillberg PG, Almkvist O, Rodriguez-Vieitez E, Nordberg A. Tau PET imaging in neurodegenerative tauopathies-still a challenge. Mol Psychiatry. 2019;24(8):1112–1134. doi:10.1038/s41380-018-0342-8
  • Bischof GN, Dodich A, Boccardi M, van Eimeren T, Festari C, Barthel H, Hansson O, Nordberg A, Ossenkoppele R, Sabri O, et al. Clinical validity of second-generation tau PET tracers as biomarkers for Alzheimer’s disease in the context of a structured 5-phase development framework. Eur J Nucl Med Mol Imaging. 2021;48(7):2110–2120. doi:10.1007/s00259-020-05156-4
  • Gouras GK, Olsson TT, Hansson O. β-Amyloid peptides and amyloid plaques in Alzheimer’s disease. Neurotherapeutics. 2015;12(1):3–11. doi:10.1007/s13311-014-0313-y
  • Puzzo D, Gulisano W, Arancio O, Palmeri A. The keystone of Alzheimer pathogenesis might be sought in Aβ physiology. Neuroscience. 2015;307:26–36. doi:10.1016/j.neuroscience.2015.08.039
  • Jansen WJ, Ossenkoppele R, Knol DL, Tijms BM, Scheltens P, Verhey FRJ, Visser PJ, Aalten P, Aarsland D, Alcolea D, et al. Prevalence of cerebral amyloid pathology in persons without dementia: a meta-analysis. JAMA. 2015;313(19):1924–1938. doi:10.1001/jama.2015.4668
  • Maxwell SP, Cash MK, Darvesh S. Neuropathology and cholinesterase expression in the brains of octogenarians and older. Chem Biol Interact. 2022;364:110065. doi:10.1016/j.cbi.2022.110065
  • Mortimer JA. The Nun study: risk factors for pathology and clinical-pathologic correlations. Curr Alzheimer Res. 2012;9(6):621–627.
  • Bennett DA, Schneider JA, Arvanitakis Z, Kelly JF, Aggarwal NT, Shah RC, Wilson RS. Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology. 2006;66(12):1837–1844. doi:10.1212/01.wnl.0000219668.47116.e6
  • Ziontz J, Bilgel M, Shafer AT, Moghekar A, Elkins W, Helphrey J, Gomez G, June D, McDonald MA, Dannals RF, et al. Tau pathology in cognitively normal older adults. Alzheimers Dement). 2019; 11:637–645. doi:10.1016/j.dadm.2019.07.007
  • Aizenstein HJ, Nebes RD, Saxton JA, Price JC, Mathis CA, Tsopelas ND, Ziolko SC, James JA, Snitz BE, Houck PR, et al. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch Neurol. 2008;65(11):1509–1517. doi:10.1001/archneur.65.11.1509
  • Davies P, Maloney AJ. Selective loss of central cholinergic neurons in Alzheimer’s disease. Lancet. 1976;2(8000):1403. doi:10.1016/s0140-6736(76)91936-x
  • Friede RL. A comparative histochemical mapping of the distribution of butyryl cholinesterase in the brains of four species of mammals, including man. Acta Anat). 1967;66(2):161–177. doi:10.1159/000142920
  • Mesulam MM, Geula C. Acetylcholinesterase-rich neurons of the human cerebral cortex: cytoarchitectonic and ontogenetic patterns of distribution. J Comp Neurol. 1991;306(2):193–220. doi:10.1002/cne.903060202
  • Darvesh S, Grantham DL, Hopkins DA. Distribution of butyrylcholinesterase in the human amygdala and hippocampal formation. J Comp Neurol. 1998;393(3):374–390. doi:10.1002/(SICI)1096-9861(19980413)393:3<374::AID-CNE8>3.0.CO;2-Z
  • Darvesh S, Hopkins DA. Differential distribution of butyrylcholinesterase and acetylcholinesterase in the human thalamus. J Comp Neurol. 2003;463(1):25–43. doi:10.1002/cne.10751
  • Darvesh S, Hopkins DA, Geula C. Neurobiology of butyrylcholinesterase. Nat Rev Neurosci. 2003;4(2):131–138. doi:10.1038/nrn1035
  • Friede RL. Enzyme histochemical studies of senile plaques. J Neuropathol Exp Neurol. 1965;24(3):477–491. doi:10.1097/00005072-196507000-00008
  • Geula C, Mesulam MM. Special properties of cholinesterases in the cerebral cortex of Alzheimer’s disease. Brain Res. 1989;498(1):185–189. doi:10.1016/0006-8993(89)90419-8
  • Mesulam MM, Geula C. Butyrylcholinesterase reactivity differentiates the amyloid plaques of aging from those of dementia. Ann Neurol. 1994;36(5):722–727. doi:10.1002/ana.410360506
  • Geula C, Mesulam MM. Cholinesterases and the pathology of Alzheimer disease. Alzheimer Dis Assoc Disord. 1995;9(Suppl 2):23–28. doi:10.1097/00002093-199501002-00005
  • Guillozet AL, Smiley JF, Mash DC, Mesulam MM. Butyrylcholinesterase in the life cycle of amyloid plaques. Ann Neurol. 1997;42(6):909–918. doi:10.1002/ana.410420613
  • Darvesh S, Reid GA, Martin E. Biochemical and histochemical comparison of cholinesterases in normal and Alzheimer brain tissues. Curr Alzheimer Res. 2010;7(5):386–400. doi:10.2174/156720510791383868
  • Perry EK, Perry RH, Blessed G, Tomlinson BE. Changes in brain cholinesterases in senile dementia of Alzheimer type. Neuropathol Appl Neurobiol. 1978;4(4):273–277. doi:10.1111/j.1365-2990.1978.tb00545.x
  • Macdonald IR, Maxwell SP, Reid GA, Cash MK, DeBay DR, Darvesh S. Quantification of butyrylcholinesterase activity as a sensitive and specific biomarker of Alzheimer’s disease. J Alzheimers Dis. 2017;58(2):491–505. doi:10.3233/JAD-170164
  • Irie T, Fukushi K, Akimoto Y, Tamagami H, Nozaki T. Design and evaluation of radioactive acetylcholine analogs for mapping brain acetylcholinesterase (AchE) in vivo. Nucl Med Biol. 1994;21(6):801–808. doi:10.1016/0969-8051(94)90159-7
  • Kilbourn MR, Snyder SE, Sherman PS, Kuhl DE. In vivo studies of acetylcholinesterase activity using a labeled substrate, N-[11C]methylpiperdin-4-yl propionate ([11C]PMP). Synapse. 1996;22(2):123–131. doi:10.1002/(SICI)1098-2396(199602)22:2<123::AID-SYN5>3.0.CO;2-F
  • Irie T, Fukushi K, Namba H, Iyo M, Tamagami H, Nagatsuka S, Ikota N. Brain acetylcholinesterase activity: validation of a PET tracer in a rat model of Alzheimer’s disease. J Nucl Med. 1996;37(4):649–655.
  • Iyo M, Namba H, Fukushi K, Shinotoh H, Nagatsuka S, Suhara T, Sudo Y, Suzuki K, Irie T. Measurement of acetylcholinesterase by positron emission tomography in the brains of healthy controls and patients with Alzheimer’s disease. Lancet. 1997;349(9068):1805–1809. doi:10.1016/S0140-6736(96)09124-6
  • Kuhl DE, Koeppe RA, Minoshima S, Snyder SE, Ficaro EP, Foster NL, Frey KA, Kilbourn MR. In vivo mapping of cerebral acetylcholinesterase activity in aging and Alzheimer’s disease. Neurology. 1999;52(4):691–699. doi:10.1212/wnl.52.4.691
  • Kikuchi T, Okamura T, Fukushi K, Takahashi K, Toyohara J, Okada M, Zhang MR, Irie T. Cerebral acetylcholinesterase imaging: development of the radioprobes. Curr Top Med Chem. 2007;7(18):1790–1799. doi:10.2174/156802607782507466
  • Kikuchi T, Okamura T, Zhang MR, Irie T. PET probes for imaging brain acetylcholinesterase. J Labelled Comp Radiopharm. 2013;56(3-4):172–179. doi:10.1002/jlcr.3002
  • Herholz K, Bauer B, Wienhard K, Kracht L, Mielke R, Lenz MO, Strotmann T, Heiss WD. In-vivo measurements of regional acetylcholine esterase activity in degenerative dementia: comparison with blood flow and glucose metabolism. J Neural Transm. 2000;107(12):1457–1468. doi:10.1007/s007020070009
  • Bohnen NI, Kaufer DI, Hendrickson R, Ivanco LS, Lopresti B, Davis JG, Constantine G, Mathis CA, Moore RY, DeKosky ST. Cognitive correlates of alterations in acetylcholinesterase in Alzheimer’s disease. Neurosci Lett. 2005;380(1–2):127–132. doi:10.1016/j.neulet.2005.01.031
  • Eggers C, Herholz K, Kalbe E, Heiss WD. Cortical acetylcholine esterase activity and ApoE4-genotype in Alzheimer disease. Neurosci Lett. 2006;408(1):46–50. doi:10.1016/j.neulet.2006.08.061
  • Hirano S, Shinotoh H, Shimada H, Ota T, Sato K, Tanaka N, Zhang MR, Higuchi M, Fukushi K, Irie T, et al. Voxel-based acetylcholinesterase PET study in early and late onset Alzheimer’s disease. J Alzheimers Dis. 2018;62(4):1539–1548. doi:10.3233/JAD-170749
  • Silver A. The Biology of Cholinesterases. Amsterdam (Netherlands): Elsevier; 1974.
  • Snyder SE, Gunupudi N, Sherman PS, Butch ER, Skaddan MB, Kilbourn MR, Koeppe RA, Kuhl DE. Radiolabeled cholinesterase substrates: in vitro methods for determining structure-activity relationships and identification of a positron emission tomography radiopharmaceutical for in vivo measurement of butyrylcholinesterase activity. J Cereb Blood Flow Metab. 2001;21(2):132–143. doi:10.1097/00004647-200102000-00004
  • Roivainen A, Rinne J, Virta J, Järvenpää T, Salomäki S, Yu M, Någren K. Biodistribution and blood metabolism of 1-11C-methyl-4-piperidinyl n-butyrate in humans: an imaging agent for in vivo assessment of butyrylcholinesterase activity with PET. J Nucl Med. 2004;45(12):2032–2039.
  • Kuhl DE, Koeppe RA, Snyder SE, Minoshima S, Frey KA, Kilbourn MR. In vivo butyrylcholinesterase activity is not increased in Alzheimer’s disease synapses. Ann Neurol. 2006;59(1):13–20. doi:10.1002/ana.20672
  • Bormans G, Sherman P, Snyder SE, Kilbourn MR. Synthesis of carbon-11- and fluorine-18-labeled 1-methyl-4-piperidyl-4’-fluorobenzoate and their biodistribution in mice. Nucl Med Biol. 1996;23(4):513–517. doi:10.1016/0969-8051(96)00033-9
  • Macdonald IR, Reid GA, Joy EE, Pottie IR, Matte G, Burrell S, Mawko G, Martin E, Darvesh S. Synthesis and preliminary evaluation of piperidinyl and pyrrolidinyl iodobenzoates as imaging agents for butyrylcholinesterase. Mol Imaging Biol. 2011;13(6):1250–1261. doi:10.1007/s11307-010-0448-0
  • Brimijoin S, Hammond P. Butyrylcholinesterase in human brain and acetylcholinesterase in human plasma: trace enzymes measured by two-site immunoassay. J Neurochem. 1988;51(4):1227–1231. doi:10.1111/j.1471-4159.1988.tb03091.x
  • Reid GA, Chilukuri N, Darvesh S. Butyrylcholinesterase and the cholinergic system. Neuroscience. 2013;234:53–68. doi:10.1016/j.neuroscience.2012.12.054
  • Wright CI, Guela C, Mesulam MM. Protease inhibitors and indoleamines selectively inhibit cholinesterases in the histopathologic structures of Alzheimer disease. Proc Natl Acad Sci U S A. 1993;90(2):683–686. doi:10.1073/pnas.90.2.683
  • Macdonald IR, Jollymore CT, Reid GA, Pottie IR, Martin E, Darvesh S. Thioesters for the in vitro evaluation of agents to image brain cholinesterases. J Enzyme Inhib Med Chem. 2013;28(3):447–455. doi:10.3109/14756366.2011.647008
  • Karnovsky MJ, Roots L. A ‘direct-coloring’ thiocholine method for cholinesterases. J Histochem Cytochem. 1964;12:219–221. doi:10.1177/12.3.219
  • Ivanov IP, Miteva HJ, Yomtova VM. A simplified equation allowing the determination of kinetic constants of ‘invisible’ substrates. Anal Biochem. 2003;323(2):247–248. doi:10.1016/j.ab.2003.07.025
  • Mukhametgalieva AR, Aglyamova AR, Lushchekina SV, Goličnik M, Masson P. Time-course of human cholinesterases-catalyzed competing substrate kinetics. Chem Biol Interact. 2019; 310:108702. doi:10.1016/j.cbi.2019.06.015
  • Goličnik M, Masson P. Time-course of enzyme-catalyzed competing substrate degradation for michaelian behavior and for enzymes showing activation/inhibition by excess substrate. Chem Biol Interact. 2019;309:108704. doi:10.1016/j.cbi.2019.06.017
  • Darvesh S, McDonald RS, Darvesh KV, Mataija D, Mothana S, Cook H, Carneiro KM, Richard N, Walsh R, Martin E. On the active site for hydrolysis of aryl amides and choline esters by human cholinesterases. Bioorg Med Chem. 2006;14(13):4586–4599. doi:10.1016/j.bmc.2006.02.021
  • Kaplan D, Ordentlich A, Barak D, Ariel N, Kronman C, Velan B, Shafferman A. Does ‘butyrylization’ of acetylcholinesterase through substitution of the six divergent aromatic amino acids in the active center gorge generate an enzyme mimic of butyrylcholinesterase? Biochemistry. 2001;40(25):7433–7445. doi:10.1021/bi010181x
  • Lockridge O. Genetic variants of human serum cholinesterase influence metabolism of the muscle relaxant succinylcholine. Pharmacol Ther. 1990;47(1):35–60. doi:10.1016/0163-7258(90)90044-3
  • Masson P, Froment MT, Gillon E, Nachon F, Darvesh S, Schopfer LM. Kinetic analysis of butyrylcholinesterase-catalyzed hydrolysis of acetanilides. Biochim Biophys Acta. 2007;1774(9):1139–1147. doi:10.1016/j.bbapap.2007.06.004
  • Montine TJ, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Dickson DW, Duyckaerts C, Frosch MP, Masliah E, Mirra SS, Alzheimer’s Association, et al. National Institute on aging-Alzheimer’s association guidelines for the neuropathologic assessment of Alzheimer’s disease: a practical approach. Acta Neuropathol. 2012;123(1):1–11. doi:10.1007/s00401-011-0910-3
  • Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, et al. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: potential factors in amyloid plaque formation. J Neurosci. 2006;26(40):10129–10140. doi:10.1523/JNEUROSCI.1202-06.2006
  • Reid GA, Darvesh S. Butyrylcholinesterase-knockout reduces brain deposition of fibrillar β-amyloid in an Alzheimer mouse model. Neuroscience. 2015;298:424–435. doi:10.1016/j.neuroscience.2015.04.039
  • Saxena A, Redman AM, Jiang X, Lockridge O, Doctor BP. Differences in active-site gorge dimensions of cholinesterases revealed by binding of inhibitors to human butyrylcholinesterase. Chem Biol Interact. 1999;119-120:61–69. doi:10.1016/s0009-2797(99)00014-9
  • Roy R, Niccolini F, Pagano G, Politis M. Cholinergic imaging in dementia spectrum disorders. Eur J Nucl Med Mol Imaging. 2016;43(7):1376–1386. doi:10.1007/s00259-016-3349-x
  • Barros L. A simple spectrophotometric method to be used in kinetics studies when substrates and products absorb at the same wavelength. Med Sci Res. 1990;18:527–529.
  • Reid GA, Darvesh S. Interaction of exogenous butyrylcholinesterase with β-amyloid plaques in 5XFAD/butyrylcholinesterase-knockout mouse brain. Curr Alzheimer Res. 2021;18(6):470–481. doi:10.2174/1567205018666210827122704
  • Green RC, Mesulam MM. Acetylcholinesterase fiber staining in the human hippocampus and parahippocampal gyrus. J Comp Neurol. 1988;273(4):488–499. doi:10.1002/cne.902730405