Evaluation and Characterization of Modified K114 Method to Localize Plaques in Rodent and Plaques and Tangles in Human Brain Tissue
- Авторы: Padala S.1, Setti S.1, Raymick J.1, Hanig J.2, Sarkar S.1
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Учреждения:
- Division of Neurotoxicology, National Center for Toxicological Research, U.S. Food & Drug Administration
- Office of Testing & Research, Center for Drug Evaluation Research/FDA
- Выпуск: Том 21, № 1 (2024)
- Страницы: 69-80
- Раздел: Medicine
- URL: https://vietnamjournal.ru/1567-2050/article/view/643715
- DOI: https://doi.org/10.2174/0115672050295561240327055835
- ID: 643715
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Аннотация
Background:A plethora of studies has shown the utility of several chemical dyes due to their affinity to bind Aβ to enable visualization of plaques under light or fluorescence microscope, and some of them showed affinity to bind neurofibrillary tangles (NFT) as well. However, only a few of them have the propensity to bind both senile plaques (SP) and NFT simultaneously.
Objective:In our current study, we aimed to modify the K114 dye and the staining procedure to substantially improve the staining of amyloid plaques in both human and rodent brains and neurofibrillary tangles in the human brain
Methods:We modified the K114 solution and the staining procedure using Sudan Black as a modifier. Additionally, to evaluate the target of the modified K114, we performed double labeling of K114 and increased Aβ against three different epitopes. We used 5 different antibodies to detect phosphorylated tau to understand the specific targets that modified K114 binds.
method:We have modified the K114 solution and the staining procedure using Sudan Black as modifier. Additionally, to evaluate the target of the modified K114, we performed double labeling of K114, and Aβ raised against three different epitopes. We used 5 different antibodies to detect phosphorylated Tau to understand the potential binding targets.
Results:Dual labeling using hyperphosphorylated antibodies against AT8, pTau, and TNT1 revealed that more than 80% hyperphosphorylated tau colocalized with tangles that were positive for modified K114, whereas more than 70% of the hyperphosphorylated tau colocalized with modified K114. On the other hand, more than 80% of the plaques that were stained with Aβ MOAB-2 were colocalized with modified K114.
result:We have found more than 80% hyperphosphorylated Tau against AT8, PTau and TNT1 colocalized with K114 labeled tangles, whereas more than 70% of the hyperphosphorylated Tau colocalized with modified K114. On the other hand, more than 80% of the plaques that were stained with amyloid beta MOAB-2 were colocalized with modified K114.
Conclusion:Our modified method can label amyloid plaques within 5 min in the rat brain and within 20 min in the human brain. Our results indicated that modified K114 could be used as a valuable tool for detecting amyloid plaques and tangles with high contrast and resolution relative to other conventional fluorescence markers.
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Об авторах
Sanjana Padala
Division of Neurotoxicology, National Center for Toxicological Research, U.S. Food & Drug Administration
Email: info@benthamscience.net
Sharay Setti
Division of Neurotoxicology, National Center for Toxicological Research, U.S. Food & Drug Administration
Email: info@benthamscience.net
James Raymick
Division of Neurotoxicology, National Center for Toxicological Research, U.S. Food & Drug Administration
Email: info@benthamscience.net
Joseph Hanig
Office of Testing & Research, Center for Drug Evaluation Research/FDA
Email: info@benthamscience.net
Sumit Sarkar
Division of Neurotoxicology, National Center for Toxicological Research, U.S. Food & Drug Administration
Автор, ответственный за переписку.
Email: info@benthamscience.net
Список литературы
- Alzheimers disease facts and figures. Alzheimers Dement., 2023, 19(4), 1598-1695. doi: 10.1002/alz.13016 PMID: 36918389
- Hardy, J.; Allsop, D. Amyloid deposition as the central event in the aetiology of Alzheimers disease. Trends Pharmacol. Sci., 1991, 12(10), 383-388. doi: 10.1016/0165-6147(91)90609-V PMID: 1763432
- Hardy, J.; Selkoe, D.J. The amyloid hypothesis of Alzheimers disease: Progress and problems on the road to therapeutics. Science, 2002, 297(5580), 353-356. doi: 10.1126/science.1072994 PMID: 12130773
- Hardy, J.A.; Higgins, G.A. Alzheimers disease: The amyloid cascade hypothesis. Science, 1992, 256(5054), 184-185. doi: 10.1126/science.1566067 PMID: 1566067
- Alonso, A.C.; Grundke-Iqbal, I.; Barra, H.S.; Iqbal, K. Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: Sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proc. Natl. Acad. Sci. USA, 1997, 94(1), 298-303. doi: 10.1073/pnas.94.1.298 PMID: 8990203
- Alonso, A.C.; Grundke-Iqbal, I.; Iqbal, K. Alzheimers disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat. Med., 1996, 2(7), 783-787. doi: 10.1038/nm0796-783 PMID: 8673924
- Alonso, A.; Li, B.; Grundke-Iqbal, I.; Iqbal, K. Mechanism of tau-induced neurodegeneration in Alzheimer disease and related tauopathies. Curr. Alzheimer Res., 2008, 5(4), 375-384. doi: 10.2174/156720508785132307 PMID: 18690834
- Iqbal, K.; Alonso, A.C.; Grundke-Iqbal, I. Cytosolic abnormally hyperphosphorylated tau but not paired helical filaments sequester normal MAPs and inhibit microtubule assembly. J. Alzheimers Dis., 2008, 14(4), 365-370. doi: 10.3233/JAD-2008-14402 PMID: 18688085
- Aghourian, M.; Aumont, É.; Grothe, M.J.; Soucy, J.P.; Rosa-Neto, P.; Bedard, M.A. FEOBV-PET to quantify cortical cholinergic denervation in AD: Relationship to basal forebrain volumetry. J. Neuroimaging, 2021, 31(6), 1077-1081. doi: 10.1111/jon.12921 PMID: 34462992
- Aghourian, M.; Legault-Denis, C.; Soucy, J-P.; Rosa-Neto, P.; Gauthier, S.; Kostikov, A.; Gravel, P.; Bédard, M-A. Quantification of brain cholinergic denervation in Alzheimers disease using PET imaging with 18F-FEOBV. Mol. Psychiatry, 2017, 22(11), 1531-1538. doi: 10.1038/mp.2017.183 PMID: 28894304
- Bedard, M.A.; Aghourian, M.; Legault-Denis, C.; Postuma, R.B.; Soucy, J.P.; Gagnon, J.F.; Pelletier, A.; Montplaisir, J. Brain cholinergic alterations in idiopathic REM sleep behaviour disorder: A PET imaging study with 18F-FEOBV. Sleep Med., 2019, 58, 35-41. doi: 10.1016/j.sleep.2018.12.020 PMID: 31078078
- Nejad-Davarani, S.; Koeppe, R.A.; Albin, R.L.; Frey, K.A.; Müller, M.L.T.M.; Bohnen, N.I. Quantification of brain cholinergic denervation in dementia with Lewy bodies using PET imaging with 18F-FEOBV. Mol. Psychiatry, 2019, 24(3), 322-327. doi: 10.1038/s41380-018-0130-5 PMID: 30082840
- de la Torre, J.; Aliev, G.; Perry, G. Drug therapy in Alzheimers disease. N. Engl. J. Med., 2004, 351(18), 1911-1913. doi: 10.1056/NEJM200410283511822 PMID: 15509830
- de La Torre, J.C. Alzheimers disease is a vasocognopathy: A new term to describe its nature. Neurol. Res., 2004, 26(5), 517-524. doi: 10.1179/016164104225016254 PMID: 15265269
- de la Torre, J.C. Is Alzheimers disease a neurodegenrative or vascular disorder? (vol 3, pg 184, 2004). Lancet Neurol., 2004, 3(5), 270-270. PMID: 15099540
- Scheffer, S.; Hermkens, D.M.A.; van der Weerd, L.; de Vries, H.E.; Daemen, M.J.A.P. Vascular hypothesis of Alzheimer disease. Arterioscler. Thromb. Vasc. Biol., 2021, 41(4), 1265-1283. doi: 10.1161/ATVBAHA.120.311911 PMID: 33626911
- Bourgade, K. Anti-viral properties of Amyloid-β Peptides., J Alzheimers Dis., 2016, 54(3), 859-878.
- Bourgade, K.; Garneau, H.; Giroux, G.; Le Page, A.Y.; Bocti, C.; Dupuis, G.; Frost, E.H.; Fülöp, T., Jr β-Amyloid peptides display protective activity against the human Alzheimers disease-associated herpes simplex virus-1. Biogerontology, 2015, 16(1), 85-98. doi: 10.1007/s10522-014-9538-8 PMID: 25376108
- Bourgade, K.; Le Page, A.; Bocti, C.; Witkowski, J.M.; Dupuis, G.; Frost, E.H.; Fülöp, T., Jr Protective effect of Amyloid-β Peptides against Herpes Simplex Virus-1 infection in a neuronal cell culture model. J. Alzheimers Dis., 2016, 50(4), 1227-1241. doi: 10.3233/JAD-150652 PMID: 26836158
- Fulop, T.; Ramassamy, C.; Lévesque, S.; Frost, E.H.; Laurent, B.; Lacombe, G.; Khalil, A.; Larbi, A.; Hirokawa, K.; Desroches, M.; Rodrigues, S.; Bourgade, K.; Cohen, A.A.; Witkowski, J.M. Viruses - a major cause of amyloid deposition in the brain. Expert Rev. Neurother., 2023, 23(9), 775-790. doi: 10.1080/14737175.2023.2244162 PMID: 37551672
- Fulop, T.; Witkowski, J.M.; Bourgade, K.; Khalil, A.; Zerif, E.; Larbi, A.; Hirokawa, K.; Pawelec, G.; Bocti, C.; Lacombe, G.; Dupuis, G.; Frost, E.H. Can an infection hypothesis explain the beta amyloid hypothesis of Alzheimers disease? Front. Aging Neurosci., 2018, 10, 224. doi: 10.3389/fnagi.2018.00224 PMID: 30087609
- Akiyama, H.; Arai, T.; Kondo, H.; Tanno, E.; Haga, C.; Ikeda, K. Cell mediators of inflammation in the Alzheimer disease brain. Alzheimer Dis. Assoc. Disord., 2000, 14(Suppl.), S47-S53. doi: 10.1097/00002093-200000001-00008 PMID: 10850730
- Akiyama, H.; Barger, S.; Barnum, S.; Bradt, B.; Bauer, J.; Cole, G.M.; Cooper, N.R.; Eikelenboom, P.; Emmerling, M.; Fiebich, B.L.; Finch, C.E.; Frautschy, S.; Griffin, W.S.; Hampel, H.; Hull, M.; Landreth, G.; Lue, L.; Mrak, R.; Mackenzie, I.R.; McGeer, P.L.; OBanion, M.K.; Pachter, J.; Pasinetti, G.; Plata-Salaman, C.; Rogers, J.; Rydel, R.; Shen, Y.; Streit, W.; Strohmeyer, R.; Tooyoma, I.; Van Muiswinkel, F.L.; Veerhuis, R.; Walker, D.; Webster, S.; Wegrzyniak, B.; Wenk, G.; Wyss-Coray, T. Inflammation and Alzheimers disease. Neurobiol. Aging, 2000, 21(3), 383-421. doi: 10.1016/S0197-4580(00)00124-X PMID: 10858586
- Pillai, J.A.; Bena, J.; Bebek, G.; Bekris, L.M.; Bonner-Jackson, A.; Kou, L.; Pai, A.; Sørensen, L.; Neilsen, M.; Rao, S.M.; Chance, M.; Lamb, B.T.; Leverenz, J.B. Inflammatory pathway analytes predicting rapid cognitive decline in MCI stage of Alzheimers disease. Ann. Clin. Transl. Neurol., 2020, 7(7), 1225-1239. doi: 10.1002/acn3.51109 PMID: 32634865
- Pillai, J.A.; Maxwell, S.; Bena, J.; Bekris, L.M.; Rao, S.M.; Chance, M.; Lamb, B.T.; Leverenz, J.B. Key inflammatory pathway activations in the MCI stage of Alzheimers disease. Ann. Clin. Transl. Neurol., 2019, 6(7), 1248-1262. doi: 10.1002/acn3.50827 PMID: 31353852
- Cummings, J.; Aisen, P.; Lemere, C.; Atri, A.; Sabbagh, M.; Salloway, S. Aducanumab produced a clinically meaningful benefit in association with amyloid lowering. Alzheimers Res. Ther., 2021, 13(1), 98. doi: 10.1186/s13195-021-00838-z PMID: 33971962
- Padala, S.P.; Yarns, B.C. Under-represented populations left out of alzheimers disease treatment with aducanumab: Commentary on ethics. J. Alzheimers Dis. Rep., 2022, 6(1), 345-348. doi: 10.3233/ADR-220023 PMID: 35891635
- Stepanchuk, A.A.; Heyne, B.; Stys, P.K. Complex photophysical properties of k114 make for a versatile fluorescent probe for amyloid detection. ACS Chem. Neurosci., 2021, 12(7), 1273-1280. doi: 10.1021/acschemneuro.1c00101 PMID: 33705095
- Setti, S.E.; Raymick, J.; Hanig, J.; Sarkar, S. In vivo demonstration of Congo Red labeled amyloid plaques via perfusion in the Alzheimer disease rat model. J. Neurosci. Methods, 2021, 353, 109082. doi: 10.1016/j.jneumeth.2021.109082 PMID: 33508413
- Iadanza, M.G.; Jackson, M.P.; Hewitt, E.W.; Ranson, N.A.; Radford, S.E. A new era for understanding amyloid structures and disease. Nat. Rev. Mol. Cell Biol., 2018, 19(12), 755-773. doi: 10.1038/s41580-018-0060-8 PMID: 30237470
- Selmani, V.; Robbins, K.J.; Ivancic, V.A.; Lazo, N.D. K114 ( trans, trans )-bromo-2,5-bis(4-hydroxystyryl)benzene is an efficient detector of cationic amyloid fibrils. Protein Sci., 2015, 24(3), 420-425. doi: 10.1002/pro.2620 PMID: 25524064
- LeVine, H., III Mechanism of Aβ(1−40) Fibril-Induced Fluorescence of ( trans, trans )-1-Bromo-2,5-bis(4-hydroxystyryl)benzene (K114). Biochemistry, 2005, 44(48), 15937-15943. doi: 10.1021/bi051252l PMID: 16313197
- Crystal, A.S.; Giasson, B.I.; Crowe, A.; Kung, M.P.; Zhuang, Z.P.; Trojanowski, J.Q.; Lee, V.M.Y. A comparison of amyloid fibrillogenesis using the novel fluorescent compound K114. J. Neurochem., 2003, 86(6), 1359-1368. doi: 10.1046/j.1471-4159.2003.01949.x PMID: 12950445
- Stepanchuk, A.A.; Barber, P.A.; Lashley, T.; Joseph, J.T.; Stys, P.K. Quantitative detection of grey and white matter amyloid pathology using a combination of K114 and CRANAD-3 fluorescence. Neurobiol. Dis., 2021, 161, 105540. doi: 10.1016/j.nbd.2021.105540 PMID: 34751140
- Elghetany, M.T.; Saleem, A. Methods for staining amyloid in tissues: A review. Stain Technol., 1988, 63(4), 201-212. doi: 10.3109/10520298809107185 PMID: 2464206
- Glenner, G.G.; Eanes, E.D.; Page, D.L. The relation of the properties of Congo red-stained amyloid fibrils to the -conformation. J. Histochem. Cytochem., 1972, 20(10), 821-826. doi: 10.1177/20.10.821 PMID: 4638557
- Styren, S.D.; Hamilton, R.L.; Styren, G.C.; Klunk, W.E. X-34, a fluorescent derivative of Congo red: A novel histochemical stain for Alzheimers disease pathology. J. Histochem. Cytochem., 2000, 48(9), 1223-1232. doi: 10.1177/002215540004800906 PMID: 10950879
- Skovronsky, D.M.; Zhang, B.; Kung, M.P.; Kung, H.F.; Trojanowski, J.Q.; Lee, V.M.Y. In vivo detection of amyloid plaques in a mouse model of Alzheimers disease. Proc. Natl. Acad. Sci. USA, 2000, 97(13), 7609-7614. doi: 10.1073/pnas.97.13.7609 PMID: 10861023
- Schmidt, M.L.; Schuck, T.; Sheridan, S.; Kung, M.P.; Kung, H.; Zhuang, Z.P.; Bergeron, C.; Lamarche, J.S.; Skovronsky, D.; Giasson, B.I.; Lee, V.M.Y.; Trojanowski, J.Q. The fluorescent Congo red derivative, (trans, trans)-1-bromo-2,5-bis-(3-hydroxycarbonyl-4-hydroxy)styrylbenzene (BSB), labels diverse β-pleated sheet structures in postmortem human neurodegenerative disease brains. Am. J. Pathol., 2001, 159(3), 937-943. doi: 10.1016/S0002-9440(10)61769-5 PMID: 11549586
- Setti, S.E.; Das, N.; Raymick, J.; Hanig, J.; Sarkar, S. Evaluation of Styrylbenzene analog- FSB and its affinity to bind parenchymal plaques and tangles in patients of Alzheimers disease. Metab. Brain Dis., 2022, 37(3), 639-651. doi: 10.1007/s11011-021-00885-3 PMID: 35064472
- Puchtler, H.; Sweat, F. Congo red as a stain for fluorescence microscopy of amyloid. J. Histochem. Cytochem., 1965, 13(8), 693-694. doi: 10.1177/13.8.693 PMID: 4160077
- Kelényi, G. Thioflavin S fluorescent and Congo red anisotropic stainings in the histologic demonstration of amyloid. Acta Neuropathol., 1967, 7(4), 336-348. doi: 10.1007/BF00688089 PMID: 4166287
- Schmued, L.; Raymick, J.; Tolleson, W.; Sarkar, S.; Zhang, Y.H.; Bell-Cohn, A. Introducing Amylo-Glo, a novel fluorescent amyloid specific histochemical tracer especially suited for multiple labeling and large scale quantification studies. J. Neurosci. Methods, 2012, 209(1), 120-126. doi: 10.1016/j.jneumeth.2012.05.019 PMID: 22705750
- Åslund, A.; Sigurdson, C.J.; Klingstedt, T.; Grathwohl, S.; Bolmont, T.; Dickstein, D.L.; Glimsdal, E.; Prokop, S.; Lindgren, M.; Konradsson, P.; Holtzman, D.M.; Hof, P.R.; Heppner, F.L.; Gandy, S.; Jucker, M.; Aguzzi, A.; Hammarström, P.; Nilsson, K.P.R. Novel pentameric thiophene derivatives for in vitro and in vivo optical imaging of a plethora of protein aggregates in cerebral amyloidoses. ACS Chem. Biol., 2009, 4(8), 673-684. doi: 10.1021/cb900112v PMID: 19624097
- Sigurdson, C.J.; Nilsson, K.P.R.; Hornemann, S.; Manco, G.; Polymenidou, M.; Schwarz, P.; Leclerc, M.; Hammarström, P.; Wüthrich, K.; Aguzzi, A. Prion strain discrimination using luminescent conjugated polymers. Nat. Methods, 2007, 4(12), 1023-1030. doi: 10.1038/nmeth1131 PMID: 18026110
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