Preclinical validation of a novel brain-penetrant PET ligand for visualization of histone deacetylase 6: a potential imaging target for neurodegenerative diseases

Barneda-Zahonero B, Parra M. Histone deacetylases and cancer. Mol Oncol. 2012;6:579–89. https://doi.org/10.1016/j.molonc.2012.07.003.

Article  CAS  PubMed Central  Google Scholar 

Batchu SN, Brijmohan AS, Advani A. The therapeutic hope for HDAC6 inhibitors in malignancy and chronic disease. Clin Sci (Lond). 2016;130:987–1003. https://doi.org/10.1042/CS20160084.

Article  CAS  Google Scholar 

Bertos NR, Gilquin B, Chan GK, Yen TJ, Khochbin S, Yang XJ. Role of the tetradecapeptide repeat domain of human histone deacetylase 6 in cytoplasmic retention. J Biol Chem. 2004;279:48246–54. https://doi.org/10.1074/jbc.M408583200.

Article  CAS  Google Scholar 

Li Y, Shin D, Kwon SH. Histone deacetylase 6 plays a role as a distinct regulator of diverse cellular processes. FEBS J. 2013;280:775–93. https://doi.org/10.1111/febs.12079.

Article  CAS  Google Scholar 

Cohen TJ, Guo JL, Hurtado DE, Kwong LK, Mills IP, Trojanowski JQ, et al. The acetylation of tau inhibits its function and promotes pathological tau aggregation. Nat Commun. 2011;2:252. https://doi.org/10.1038/ncomms1255.

Article  Google Scholar 

Miki Y, Mori F, Tanji K, Kakita A, Takahashi H, Wakabayashi K. Accumulation of histone deacetylase 6, an aggresome-related protein, is specific to Lewy bodies and glial cytoplasmic inclusions. Neuropathology. 2011;31:561–8. https://doi.org/10.1111/j.1440-1789.2011.01200.x.

Article  Google Scholar 

Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell. 2003;115:727–38.

Article  CAS  Google Scholar 

Simoes-Pires C, Zwick V, Nurisso A, Schenker E, Carrupt PA, Cuendet M. HDAC6 as a target for neurodegenerative diseases: what makes it different from the other HDACs? Mol Neurodegener. 2013;8:7. https://doi.org/10.1186/1750-1326-8-7.

Article  CAS  PubMed Central  Google Scholar 

Ding H, Dolan PJ, Johnson GV. Histone deacetylase 6 interacts with the microtubule-associated protein tau. J Neurochem. 2008;106:2119–30. https://doi.org/10.1111/j.1471-4159.2008.05564.x.

Article  CAS  PubMed Central  Google Scholar 

Odagiri S, Tanji K, Mori F, Miki Y, Kakita A, Takahashi H, et al. Brain expression level and activity of HDAC6 protein in neurodegenerative dementia. Biochem Biophys Res Commun. 2013;430:394–9. https://doi.org/10.1016/j.bbrc.2012.11.034.

Article  CAS  Google Scholar 

Guo W, Naujock M, Fumagalli L, Vandoorne T, Baatsen P, Boon R, et al. HDAC6 inhibition reverses axonal transport defects in motor neurons derived from FUS-ALS patients. Nat Commun. 2017;8:861. https://doi.org/10.1038/s41467-017-00911-y.

Article  CAS  PubMed Central  Google Scholar 

Onishi T, Maeda R, Terada M, Sato S, Fujii T, Ito M, et al. A novel orally active HDAC6 inhibitor T-518 shows a therapeutic potential for Alzheimer’s disease and tauopathy in mice. Sci Rep. 2021;11:15423. https://doi.org/10.1038/s41598-021-94923-w.

Article  CAS  PubMed Central  Google Scholar 

Tago T, Toyohara J. Advances in the development of PET ligands targeting histone deacetylases for the assessment of neurodegenerative diseases. Molecules. 2018;23. https://doi.org/10.3390/molecules23020300.

Schroeder FA, Wang C, Van de Bittner GC, Neelamegam R, Takakura WR, Karunakaran A, et al. PET imaging demonstrates histone deacetylase target engagement and clarifies brain penetrance of known and novel small molecule inhibitors in rat. ACS Chem Neurosci. 2014;5:1055–62. https://doi.org/10.1021/cn500162j.

Article  CAS  Google Scholar 

Del Rosso G, Carlomagno Y, Todd TW, Jones CY, Prudencio M, Daughrity LM, et al. HDAC6 interacts with poly (GA) and modulates its accumulation in c9FTD/ALS. Front Cell Dev Biol. 2021;9: 809942. https://doi.org/10.3389/fcell.2021.809942.

Article  Google Scholar 

Strebl MG, Campbell AJ, Zhao WN, Schroeder FA, Riley MM, Chindavong PS, et al. HDAC6 brain mapping with [18F]bavarostat enabled by a Ru-mediated deoxyfluorination. ACS Cent Sci. 2017;3:1006–14. https://doi.org/10.1021/acscentsci.7b00274.

Article  CAS  PubMed Central  Google Scholar 

Koole M, Van Weehaeghe D, Serdons K, Herbots M, Cawthorne C, Celen S, et al. Clinical validation of the novel HDAC6 radiotracer [18F]EKZ-001 in the human brain. Eur J Nucl Med Mol Imaging. 2021;48:596–611. https://doi.org/10.1007/s00259-020-04891-y.

Article  CAS  Google Scholar 

Bai P, Mondal P, Bagdasarian FA, Rani N, Liu Y, Gomm A, et al. Development of a potential PET probe for HDAC6 imaging in Alzheimer’s disease. Acta Pharm Sin B. 2022;12:3891–904. https://doi.org/10.1016/j.apsb.2022.05.017.

Article  CAS  PubMed Central  Google Scholar 

Kozikowski AP, Shen S, Pardo M, Tavares MT, Szarics D, Benoy V, et al. Brain penetrable histone deacetylase 6 inhibitor SW-100 ameliorates memory and learning impairments in a mouse model of fragile X syndrome. ACS Chem Neurosci. 2019;10:1679–95. https://doi.org/10.1021/acschemneuro.8b00600.

Article  CAS  Google Scholar 

Tago T, Toyohara J, Ishii K. Preclinical evaluation of an 18F-labeled SW-100 derivative for PET imaging of histone deacetylase 6 in the brain. ACS Chem Neurosci. 2021;12:746–55. https://doi.org/10.1021/acschemneuro.0c00774.

Article  CAS  Google Scholar 

Onoe H, Inoue O, Suzuki K, Tsukada H, Itoh T, Mataga N, et al. Ketamine increases the striatal N-[11C]methylspiperone binding in vivo: positron emission tomography study using conscious rhesus monkey. Brain Res. 1994;663:191–8. https://doi.org/10.1016/0006-8993(94)91263-7.

Article  CAS  Google Scholar 

Logan J, Fowler JS, Volkow ND, Wolf AP, Dewey SL, Schlyer DJ, et al. Graphical analysis of reversible radioligand binding from time-activity measurements applied to [N-11C-methyl]-(-)-cocaine PET studies in human subjects. J Cereb Blood Flow Metab. 1990;10:740–7. https://doi.org/10.1038/jcbfm.1990.127.

Article  CAS  Google Scholar 

Varga J, Szabo Z. Modified regression model for the Logan plot. J Cereb Blood Flow Metab. 2002;22:240–4. https://doi.org/10.1097/00004647-200202000-00012.

Article  Google Scholar 

Lassen NA, Bartenstein PA, Lammertsma AA, Prevett MC, Turton DR, Luthra SK, et al. Benzodiazepine receptor quantification in vivo in humans using [11C]flumazenil and PET: application of the steady-state principle. J Cereb Blood Flow Metab. 1995;15:152–65. https://doi.org/10.1038/jcbfm.1995.17.

Article  CAS  Google Scholar 

Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008;22:659–61. https://doi.org/10.1096/fj.07-9574LSF.

Article  CAS  Google Scholar 

Jochems J, Boulden J, Lee BG, Blendy JA, Jarpe M, Mazitschek R, et al. Antidepressant-like properties of novel HDAC6-selective inhibitors with improved brain bioavailability. Neuropsychopharmacology. 2014;39:389–400. https://doi.org/10.1038/npp.2013.207.

Article  CAS  Google Scholar 

Toyohara J, Nishino K, Sakai M, Tago T, Oda T. Automated production of [18F]MK-6240 on CFN-MPS200. Appl Radiat Isot. 2020;168: 109468. https://doi.org/10.1016/j.apradiso.2020.109468.

Article  CAS  Google Scholar 

Tetrabutylammonium in radiopharmaceutical preparations. European Pharmacopoeia. 10.5 ed: European Directorate for the Quality of Medicines & HealthCare. 2021, pp.5661.

Bogni A, Laera L, Cucchi C, Seregni E, Pascali C. Tetrabutylammonium HPLC analysis: shortcomings in the Ph. Eur method J Labelled Comp Radiopharm. 2020;63:203–8. https://doi.org/10.1002/jlcr.3822.

Article  CAS  Google Scholar 

ICH Guideline Q3D(R2) Guideline for elemental impurities. https://database.ich.org/sites/default/files/Q3D-R2_Guideline_Step4_2022_0308.pdf. Accessed 20 Sep 2023.

Shen S, Kozikowski AP. Why hydroxamates may not be the best histone deacetylase inhibitors–what some may have forgotten or would rather forget? ChemMedChem. 2016;11:15–21. https://doi.org/10.1002/cmdc.201500486.

Article  CAS  Google Scholar 

Shen S, Picci C, Ustinova K, Benoy V, Kutil Z, Zhang G, et al. Tetrahydroquinoline-capped histone deacetylase 6 inhibitor SW-101 ameliorates pathological phenotypes in a charcot-marie-tooth type 2A mouse model. J Med Chem. 2021;64:4810–40. https://doi.org/10.1021/acs.jmedchem.0c02210.

Article  CAS  Google Scholar 

Koziorowski J, Behe M, Decristoforo C, Ballinger J, Elsinga P, Ferrari V, et al. Position paper on requirements for toxicological studies in the specific case of radiopharmaceuticals. EJNMMI Radiopharm Chem. 2017;1:1. https://doi.org/10.1186/s41181-016-0004-6.

Article  CAS  Google Scholar 

Dietz KC, Casaccia P. HDAC inhibitors and neurodegeneration: at the edge between protection and damage. Pharmacol Res. 2010;62:11–7. https://doi.org/10.1016/j.phrs.2010.01.011.

Article  CAS  PubMed Central  Google Scholar 

Anderson KW, Chen J, Wang M, Mast N, Pikuleva IA, Turko IV. Quantification of histone deacetylase isoforms in human frontal cortex, human retina, and mouse brain. PLoS ONE. 2015;10: e0126592. https://doi.org/10.1371/journal.pone.0126592.

Article  CAS  PubMed Central  Google Scholar 

Guidance for Industry and Researchers. The radioactive drug research committee: human research without an investigational new drug application: US Food and Drug Administration. 2010.

Zanotti-Fregonara P, Lammertsma AA, Innis RB. 11C dosimetry scans should be abandoned. J Nucl Med. 2021;62:158–9. https://doi.org/10.2967/jnumed.120.257402.

Article  PubMed Central  Google Scholar 

Radiological Protection in Biomedical Research. ICRP Publication 62. Ann ICRP. 1992;22.

Zanotti-Fregonara P, Lammertsma AA, Innis RB. Suggested pathway to assess radiation safety of 18F-labeled PET tracers for first-in-human studies. Eur J Nucl Med Mol Imaging. 2013;40:1781–3. https://doi.org/10.1007/s00259-013-2512-x.

Article  Google Scholar 

Celen S, Rokka J, Gilbert TM, Koole M, Vermeulen I, Serdons K, et al. Translation of HDAC6 PET imaging using [18F]EKZ-001-cGMP production and measurement of HDAC6 target occupancy in nonhuman primates. ACS Chem Neurosci. 2020;11:1093–101. https://doi.org/10.1021/acschemneuro.0c00074.

Article  CAS  Google Scholar 

Lechner S, Malgapo MIP, Gratz C, Steimbach RR, Baron A, Ruther P, et al. Target deconvolution of HDAC pharmacopoeia reveals MBLAC2 as common off-target. Nat Chem Biol. 2022;18:812–20. https://doi.org/10.1038/s41589-022-01015-5.

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