Histone Deacetylase Inhibition Regulates Lipid Homeostasis in a Mouse Model of Amyotrophic Lateral Sclerosis
Open accessAbstract
Amyotrophic lateral sclerosis (ALS) is an incurable and fatal neurodegenerative disorder of the motor system. While the etiology is still incompletely understood, defects in metabolism act as a major contributor to the disease progression. Recently, histone deacetylase (HDAC) inhibition using ACY-738 has been shown to restore metabolic alterations in the spinal cord of a FUS mouse model of ALS, which was accompanied by a beneficial effect on the motor phenotype and survival. In this study, we investigated the specific effects of HDAC inhibition on lipid metabolism using untargeted lipidomic analysis combined with transcriptomic analysis in the spinal cord of FUS mice. We discovered that symptomatic FUS mice recapitulate lipid alterations found in ALS patients and in the SOD1 mouse model. Glycerophospholipids, sphingolipids, and cholesterol esters were most affected. Strikingly, HDAC inhibition mitigated lipid homeostasis defects by selectively targeting glycerophospholipid metabolism and reducing cholesteryl esters accumulation. Therefore, our data suggest that HDAC inhibition is a potential new therapeutic strategy to modulate lipid metabolism defects in ALS and potentially other neurodegenerative diseases.
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Genetic knockdown and pharmacological inhibition of HDACs ameliorate ALS pathology in different ALS models.
“Notably, genetic knockdown and pharmacological inhibition of HDACs have been shown to ameliorate ALS pathology in different ALS models.341–344”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [344]
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KEGG as a reference resource for gene and protein annotation
Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M., & Tanabe, M. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkv1070 · Cited by 7,387 · see citing works
Using MetaboAnalyst 4.0 for Comprehensive and Integrative Metabolomics Data Analysis
Chong, J., Wishart, D. S., & Xia, J. (2019) · Current Protocols in Bioinformatics · doi:10.1002/cpbi.86 · Cited by 2,144 · see citing works
Update of the LIPID MAPS comprehensive classification system for lipids
Fahy, E., Subramaniam, S., Murphy, R. C., Nishijima, M., Raetz, C. R. H., Shimizu, T., Spener, F., Gerrit van, M. E. E. R., Wakelam, M. J. O., & Dennis, E. A. (2008) · Journal of Lipid Research · doi:10.1194/jlr.r800095-jlr200 · Cited by 1,766 · see citing works
van der Veen, J. N., Kennelly, J. P., Wan, S., Vance, J. E., Vance, D. E., & Jacobs, R. L. (2017) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2017.04.006 · Cited by 1,514 · see citing works
Marschallinger, J., Iram, T., Zardeneta, M., Lee, S. E., Lehallier, B., Haney, M. S., Pluvinage, J. V., Mathur, V., Hahn, O., Morgens, D. W., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0566-1 · Cited by 1,384 · cited 1× · see citing works
“Although, accumulation of lipid droplets has also been observed in motor neurons and more recently in microglia of aged brains [59,60].”
BackgroundAmyotrophic lateral sclerosis: a clinical review
Masrori, P., & Damme, P. V. (2020) · European Journal of Neurology · doi:10.1111/ene.14393 · Cited by 1,228 · see citing works
Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry
Ejsing, C. S., Sampaio, J. L., Surendranath, V., Duchoslav, E., Ekroos, K., Klemm, R. W., Simons, K., & Shevchenko, A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811700106 · Cited by 1,071 · see citing works
Transcriptional Regulation of Metabolism
Desvergne, B., Michalik, L., & Wahli, W. (2006) · Physiological Reviews · doi:10.1152/physrev.00025.2005 · Cited by 896 · see citing works
MAM (mitochondria-associated membranes) in mammalian cells: Lipids and beyond
Vance, J. E. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2013.11.014 · Cited by 665 · see citing works
Stoica, R., Vos, K. J. D., Paillusson, S., Mueller, S., Sancho, R. M., Lau, K., Vizcay‐Barrena, G., Lin, W.-L., Xu, Y.-F., Lewis, J. M., et al. (2014) · Nature Communications · doi:10.1038/ncomms4996 · Cited by 623 · see citing works
Dyslipidemia is a protective factor in amyotrophic lateral sclerosis
Dupuis, L., Corcia, P., Fergani, A., de Aguilar, J. G., Bonnefont‐Rousselot, D., Bittar, R., Seilhean, D., Hauw, J., Lacomblez, L., Loeffler, J.-P., et al. (2008) · Neurology · doi:10.1212/01.wnl.0000285080.70324.27 · Cited by 551 · see citing works
Membrane lipidome of an epithelial cell line
Sampaio, J. L., Gerl, M. J., Klose, C. D., Ejsing, C. S., Beug, H., Simons, K., & Shevchenko, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019267108 · Cited by 500 · see citing works
Hishikawa, D., Hashidate, T., Shimizu, T., & Shindou, H. (2014) · Journal of Lipid Research · doi:10.1194/jlr.r046094 · Cited by 436 · see citing works
Interaction of FUS and HDAC1 regulates DNA damage response and repair in neurons
Wang, W., Pan, L., Su, S. C., Quinn, E. J., Sasaki, M., Jimenez, J., Mackenzie, I. R., Huang, E. J., & Tsai, L. (2013) · Nature Neuroscience · doi:10.1038/nn.3514 · Cited by 433 · see citing works
LipidXplorer: A Software for Consensual Cross-Platform Lipidomics
Herzog, R., Schuhmann, K., Schwudke, D., Sampaio, J. L., Bornstein, S. R., Schroeder, M., & Shevchenko, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029851 · Cited by 420 · see citing works
Herzog, R., Schwudke, D., Schuhmann, K., Sampaio, J. L., Bornstein, S. R., Schroeder, M., & Shevchenko, A. (2011) · Genome biology · doi:10.1186/gb-2011-12-1-r8 · Cited by 414 · see citing works
Role of histone acetylation in the control of gene expression
Verdone, L., Caserta, M., & Mauro, E. D. (2005) · Biochemistry and Cell Biology · doi:10.1139/o05-041 · Cited by 391 · see citing works
HDAC6 inhibition reverses axonal transport defects in motor neurons derived from FUS-ALS patients
Guo, W., Naujock, M., Fumagalli, L., Vandoorne, T., Baatsen, P., Boon, R., Ordovás, L., Patel, A., Welters, M., Vanwelden, T., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00911-y · Cited by 373 · see citing works
Emerging roles of lysophospholipids in health and disease
Tan, S. T., Ramesh, T., Toh, X. R., & Nguyen, L. N. (2020) · Progress in Lipid Research · doi:10.1016/j.plipres.2020.101068 · Cited by 372 · see citing works
Wang, W., Li, L., Lin, W.-L., Dickson, D. W., Petrucelli, L., Zhang, T., & Wang, X. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt319 · Cited by 340 · see citing works
Giorgi, C., Missiroli, S., Patergnani, S., Duszyński, J., Wieckowski, M. R., & Pinton, P. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.6223 · Cited by 332 · see citing works
Cutler, R. G., Pedersen, W. A., Camandola, S., Rothstein, J. D., & Mattson, M. P. (2002) · Annals of Neurology · doi:10.1002/ana.10312 · Cited by 325 · see citing works
Critical loss of CBP/p300 histone acetylase activity by caspase‐6 during neurodegeneration
Rouaux, C., Jokic, N., Mbebi, C., Boutillier, S., Loeffler, J., & Boutillier, A. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg615 · Cited by 302 · see citing works
LION/web: a web-based ontology enrichment tool for lipidomic data analysis
Molenaar, M. R., Jeucken, A., Wassenaar, T. A., van de Lest, C. H. A., Brouwers, J. F. H. M., & Helms, J. B. (2019) · GigaScience · doi:10.1093/gigascience/giz061 · Cited by 299 · see citing works
Paganoni, S., Deng, J., Jaffa, M., Cudkowicz, M., & Wills, A.-M. A. (2011) · Muscle & Nerve · doi:10.1002/mus.22114 · Cited by 293 · see citing works
Mitchell, J. C., McGoldrick, P., Vance, C. A., Hortobágyi, T., Sreedharan, J., Rogelj, B., Tudor, E. L., Smith, B. N., Klasen, C., Miller, C. C. J., et al. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-1043-z · Cited by 290 · see citing works
Marin, B., Desport, J. C., Kajeu, P., Jésus, P., Nicolaud, B., Nicol, M., Preux, P., & Couratier, P. (2010) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2010.211474 · Cited by 285 · see citing works
Surma, M. A., Herzog, R., Vasilj, A., Klose, C. D., Christinat, N., Morin‐Rivron, D., Simons, K., Masoodi, M., & Sampaio, J. L. (2015) · European Journal of Lipid Science and Technology · doi:10.1002/ejlt.201500145 · Cited by 285 · see citing works
Cardiolipin, Mitochondria, and Neurological Disease
Falabella, M., Vernon, H. J., Hanna, M. G., Claypool, S. M., & Pitceathly, R. D. S. (2021) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2021.01.006 · Cited by 282 · see citing works
Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks
Knutson, S. K., Chyla, B. J., Amann, J. M., Bhaskara, S., Huppert, S. S., & Hiebert, S. W. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.51 · Cited by 271 · see citing works
Stoica, R., Paillusson, S., Gómez‐Suaga, P., Mitchell, J. C., Lau, D. H. W., Gray, E. H., Sancho, R. M., Vizcay‐Barrena, G., Vos, K. J. D., Shaw, C. E., et al. (2016) · EMBO Reports · doi:10.15252/embr.201541726 · Cited by 254 · see citing works
Galmozzi, A., Mitro, N., Ferrari, A., Gers, E., Gilardi, F., Godio, C., Cermenati, G., Gualerzi, A., Donetti, E., Rotili, D., et al. (2012) · Diabetes · doi:10.2337/db12-0548 · Cited by 236 · see citing works
Palamiuc, L., Schlagowski, A.-I., Ngo, S. T., Vernay, A., Dirrig‐Grosch, S., Henriques, A., Boutillier, A., Zoll, J., Echaniz‐Laguna, A., Loeffler, J., et al. (2015) · EMBO Molecular Medicine · doi:10.15252/emmm.201404433 · Cited by 235 · see citing works
Mitochondria‐associated membrane collapse is a common pathomechanism in SIGMAR1‐ and SOD1‐linked ALS
Watanabe, S., Ilieva, H. S., Tamada, H., Nomura, H., Komine, O., Endo, F., Jin, S., Mancías, P., Kiyama, H., & Yamanaka, K. (2016) · EMBO Molecular Medicine · doi:10.15252/emmm.201606403 · Cited by 231 · see citing works
Amyotrophic lateral sclerosis: mechanisms and therapeutics in the epigenomic era
Paez-Colasante, X., Figueroa‐Romero, C., Sakowski, S. A., Goutman, S. A., & Feldman, E. L. (2015) · Nature Reviews Neurology · doi:10.1038/nrneurol.2015.57 · Cited by 224 · see citing works
Jochems, J., Boulden, J., Lee, B. G., Blendy, J. A., Jarpe, M. B., Mazitschek, R., van Duzer, J. H., Jones, S. S., & Berton, O. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.207 · Cited by 168 · see citing works
Single-cell lipidomics with high structural specificity by mass spectrometry
Li, Z., Cheng, S., Lin, Q., Cao, W., Yang, J., Zhang, M., Shen, A., Zhang, W., Xia, Y., Ma, X., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23161-5 · Cited by 161 · see citing works
Lipidomics Reveals Cerebrospinal-Fluid Signatures of ALS
Blasco, H., Veyrat‐Durebex, C., Bocca, C., Patin, F., Vourc’h, P., Nzoughet, J. K., Lenaers, G., Andres, C. R., Simard, G., Corcia, P., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-17389-9 · Cited by 158 · see citing works
Alterations in lipid metabolism of spinal cord linked to amyotrophic lateral sclerosis
Chaves‐Filho, A. B., Pinto, I. F. D., Dantas, L. S., Xavier, A. M., Inague, A., de Faria, R. L., de Medeiros, M. H. G., Glezer, I., Yoshinaga, M. Y., & Miyamoto, S. (2019) · Scientific Reports · doi:10.1038/s41598-019-48059-7 · Cited by 158 · see citing works
Hdac6 deletion delays disease progression in the SOD1G93A mouse model of ALS
Taes, I., Timmers, M., Hersmus, N., Bento‐Abreu, A., Bosch, L. V. D., Damme, P. V., Auwerx, J. H., & Robberecht, W. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt028 · Cited by 139 · see citing works
Bruneteau, G., Simonet, T., Bauché, S., Mandjee, N., Malfatti, E., Girard, E., Tanguy, M., Béhin, A., Khiami, F., Sariali, E., et al. (2013) · Brain · doi:10.1093/brain/awt164 · Cited by 137 · see citing works
Glycosphingolipids are modulators of disease pathogenesis in amyotrophic lateral sclerosis
Dodge, J. C., Treleaven, C. M., Pacheco, J., Cooper, S., Bao, C., Abraham, M., Cromwell, M. A., Sardi, S. P., Chuang, W., Sidman, R. L., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508767112 · Cited by 134 · see citing works
Bennett, S. A., Tanaz, R., Cobos, S. N., & Torrente, M. P. (2018) · Translational research · doi:10.1016/j.trsl.2018.10.002 · Cited by 132 · see citing works
Dissociation of muscle insulin sensitivity from exercise endurance in mice by HDAC3 depletion
Hong, S., Zhou, W., Fang, B., Lu, W., Loro, E., Damle, M., Ding, G., Jager, J., Zhang, S., Zhang, Y., et al. (2016) · Nature Medicine · doi:10.1038/nm.4245 · Cited by 110 · see citing works
Fazal, R., Boeynaems, S., Swijsen, A., De Decker, M., Fumagalli, L., Moisse, M., Vanneste, J., Guo, W., Boon, R., Vercruysse, T., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020106177 · Cited by 108 · see citing works
Self-citationAdipose Tissue Distribution Predicts Survival in Amyotrophic Lateral Sclerosis
Lindauer, E., Dupuis, L., Müller, H., Heiko Neumann, B., Ludolph, A. C., & Kassubek, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067783 · Cited by 102 · see citing works
Inhibition of HDAC3 promotes ligand-independent PPARγ activation by protein acetylation
Jiang, X., Ye, X., Guo, W., Lu, H., & Gao, Z. (2014) · Journal of Molecular Endocrinology · doi:10.1530/jme-14-0066 · Cited by 102 · see citing works
Differential Histone Deacetylase mRNA Expression Patterns in Amyotrophic Lateral Sclerosis
Janssen, C., Schmalbach, S., Boeselt, S., Sarlette, A., Dengler, R., & Petri, S. (2010) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181ddd404 · Cited by 100 · see citing works
Henriques, A., Croixmarie, V., Priestman, D. A., Rosenbohm, A., Dirrig‐Grosch, S., D’Ambra, E., Huebecker, M., Hussain, G., Boursier-Neyret, C., Echaniz‐Laguna, A., et al. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv439 · Cited by 97 · see citing works
Rossaert, E., Pollari, E., Jaspers, T., Van Helleputte, L., Jarpe, M., Van Damme, P., De Bock, K., Moisse, M., & Van Den Bosch, L. (2019) · Acta Neuropathologica Communications · doi:10.1186/s40478-019-0750-2 · Cited by 93 · see citing works
Self-citationBernard‐Marissal, N., Chrast, R., & Schneider, B. L. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0125-1 · Cited by 88 · see citing works
Dittlau, K. S., Krasnow, E. N., Fumagalli, L., Vandoorne, T., Baatsen, P., Kerstens, A., Giacomazzi, G., Pavie, B., Rossaert, E., Beckers, J., et al. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.03.029 · Cited by 85 · see citing works
Self-citationBenoy, V., Berghe, P. V., Jarpe, M. B., Damme, P. V., Robberecht, W., & Bosch, L. V. D. (2016) · Neurotherapeutics · doi:10.1007/s13311-016-0501-z · Cited by 83 · see citing works
Association of Variants in the SPTLC1 Gene With Juvenile Amyotrophic Lateral Sclerosis
Johnson, J. O., Chia, R., Miller, D. E., Li, R., Kumaran, R., Abramzon, Y. A., Alahmady, N. F., Renton, A. E., Topp, S. D., Gibbs, J. R., et al. (2021) · JAMA Neurology · doi:10.1001/jamaneurol.2021.2598 · Cited by 83 · see citing works
Henriques, A., Croixmarie, V., Bouscary, A., Mosbach, A., Keime, C., Boursier-Neyret, C., Walter, B., Spedding, M., & Loeffler, J. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00433 · Cited by 70 · see citing works
Fu, Y., Rusznák, Z., Herculano‐Houzel, S., WATSON, C. R. R., & Paxinos, G. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0462-x · Cited by 66 · see citing works
Área-Gómez, E., Larrea, D., Yun, T., Xu, Y., Hupf, J. C., Zandkarimi, F., Chan, R., & Mitsumoto, H. (2021) · Scientific Reports · doi:10.1038/s41598-021-92112-3 · Cited by 64 · see citing works
Pigna, E., Simonazzi, E., Sanna, K., Bernadzki, K. M., Proszynski, T., Heil, C., Palacios, D., Adamo, S., & Moresi, V. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.01.038 · Cited by 61 · see citing works
HDAC1 inhibition ameliorates TDP-43-induced cell death in vitro and in vivo
Sanna, S., Esposito, S., Masala, A., Sini, P., Nieddu, G., Galioto, M., Fais, M., Iaccarino, C., Cestra, G., & Crosio, C. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-2580-3 · Cited by 61 · see citing works
Majid, T., Griffin, D. M., Criss, Z. K., Jarpe, M. B., & Pautler, R. G. (2015) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1016/j.trci.2015.08.001 · Cited by 60 · see citing works
TDP-43 mediates SREBF2-regulated gene expression required for oligodendrocyte myelination
Ho, W. Y., Chang, J., Lim, K., Cazenave‐Gassiot, A., Nguyen, A. T., Foo, J. C., Muralidharan, S., Viera-Ortiz, A., Ong, S. J. M., Hor, J. H., et al. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.201910213 · Cited by 60 · see citing works
Kuta, R., Larochelle, N., Fernandez, M., Pal, A., Minotti, S., Tibshirani, M., Louis, K. S., Gentil, B. J., Nalbantoglu, J. N., Hermann, A., et al. (2020) · Cell Stress and Chaperones · doi:10.1007/s12192-019-01064-1 · Cited by 57 · see citing works
Tracey, T. J., Kirk, S. E., Steyn, F. J., & Ngo, S. T. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.08.012 · Cited by 54 · see citing works
Neutral Lipid Cacostasis Contributes to Disease Pathogenesis in Amyotrophic Lateral Sclerosis
Dodge, J. C., Jensen, E. H., Yu, J., Sardi, S. P., Bialas, A. R., Taksir, T. V., Bangari, D. S., & Shihabuddin, L. S. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1388-20.2020 · Cited by 54 · see citing works
Sol, J., Jové, M., Povedano, M., Sproviero, W., Domínguez, R., Piñol‐Ripoll, G., Romero‐Guevara, R., Hye, A., Al‐Chalabi, A., Torres, P., et al. (2021) · Brain Communications · doi:10.1093/braincomms/fcab143 · Cited by 53 · see citing works
Valle, C., Salvatori, I., Gerbino, V., Rossi, S., Palamiuc, L., René, F., & Carrı̀, M. T. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.247 · Cited by 52 · see citing works
Arenas, A., Chen, J., Kuang, L., Barnett, K. R., Kasarskis, E. J., Gál, J., & Zhu, H. (2020) · Human Molecular Genetics · doi:10.1093/hmg/ddaa159 · Cited by 51 · see citing works
From Food to Genes: Transcriptional Regulation of Metabolism by Lipids and Carbohydrates
Bravo-Ruiz, I., Medina, M. Á., & Martı́nez-Poveda, B. (2021) · Nutrients · doi:10.3390/nu13051513 · Cited by 51 · see citing works
The HDAC3 enzymatic activity regulates skeletal muscle fuel metabolism
Song, S., Wen, Y., Tong, H. N., Loro, E., Gong, Y., Liu, J., Hong, S., Li, L., Khurana, T. S., Chu, M., et al. (2018) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjy066 · Cited by 44 · see citing works
Bouscary, A., Quessada, C., Mosbach, A., Callizot, N., Spedding, M., Loeffler, J., & Henriques, A. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00883 · Cited by 44 · see citing works
Dysregulation of chromatin remodelling complexes in amyotrophic lateral sclerosis
Tibshirani, M., Zhao, B., Gentil, B. J., Minotti, S., Marques, C., Keith, J., Rogaeva, E., Zinman, L., Rouaux, C., Robertson, J., et al. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx301 · Cited by 42 · see citing works
Veyrat‐Durebex, C., Bris, C., Codron, P., Bocca, C., Chupin, S., Corcia, P., Vourc’h, P., Hergesheimer, R. C., Cassereau, J., Funalot, B., et al. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1484-7 · Cited by 41 · see citing works
GO-PCA: An Unsupervised Method to Explore Gene Expression Data Using Prior Knowledge
Wagner, F. (2015) · PLOS ONE · doi:10.1371/journal.pone.0143196 · Cited by 35 · see citing works
Dodge, J. C. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00356 · Cited by 33 · see citing works
Opportunities for histone deacetylase inhibition in amyotrophic lateral sclerosis
Klingl, Y. E., Pakravan, D., & Bosch, L. V. D. (2020) · British Journal of Pharmacology · doi:10.1111/bph.15217 · Cited by 32 · see citing works
Fernández-Beltrán, L. C., Godoy-Corchuelo, J. M., Losa-Fontangordo, M., Williams, D. J., Matías‐Guiu, J., & Corrochano, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179553 · Cited by 32 · see citing works
HDAC1 and HDAC2 independently regulate common and specific intrinsic responses in murine enteroids
Gonneaud, A., Turgeon, N., Jones, C. M., Couture, C., Lévesque, D., Boisvert, F., Boudreau, F., & Asselin, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-41842-6 · Cited by 27 · see citing works
Potential Therapeutic Role of HDAC Inhibitors in FUS-ALS
Tejido, C., Pakravan, D., & Bosch, L. V. D. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.686995 · Cited by 26 · see citing works
Guzman, K., Brink, L. E., Bey, G. R., Bodnar, R. J., Kuang, L., Xing, B., Sullivan, M. L. G., Park, H. J., Koppes, E., Zhu, H., et al. (2020) · Glia · doi:10.1002/glia.23825 · Cited by 23 · see citing works
Zou, C., Synan, M. J., Li, J., Xiong, S., Manni, M. L., Liu, Y., Chen, B. B., Zhao, Y., Shiva, S., Tyurina, Y. Y., et al. (2015) · Journal of Cell Science · doi:10.1242/jcs.176701 · Cited by 21 · see citing works
Parakh, S., & Atkin, J. D. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.02.002 · Cited by 20 · see citing works
Nuclear lipidome is altered in amyotrophic lateral sclerosis: A pilot study
Ramírez‐Núñez, O., Jové, M., Torres, P., Sol, J., Fontdevila, L., Romero‐Guevara, R., Andrés‐Benito, P., Ayala, V., Rossi, C., Boada, J., et al. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15373 · Cited by 19 · see citing works
Gong, Y., Cao, R., Ding, G., Hong, S., Zhou, W., Lu, W., Damle, M., Fang, B., Wang, C., Qian, J., et al. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.05.024 · Cited by 13 · see citing works
Age and Sex-Related Changes to Gene Expression in the Mouse Spinal Cord
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Wagner, F. (2015) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/018705 · Cited by 4 · see citing works
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Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases
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Current State and Future Directions in the Therapy of ALS
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Labarre, A., Guitard, E., Tossing, G., Forest, A., Bareke, E., Labrecque, M., Tétreault, M., Ruiz, M., & Parker, J. A. (2022) · Communications Biology · doi:10.1038/s42003-022-04295-8 · Cited by 55 · see citing works
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Evidence of Metabolic Dysfunction in Amyotrophic Lateral Sclerosis (ALS) Patients and Animal Models
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Xu, J., Li, C., & Kang, X. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1267456 · Cited by 31 · see citing works
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Self-citationThe Other Side of the Same Coin: Beyond the Coding Region in Amyotrophic Lateral Sclerosis
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Molecular Research on Amyotrophic Lateral Sclerosis
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Wu, Q., Zhao, Y., Yu, Q., Ding, J., Sun, C., Wei, X., Li, S., Wang, K., Zhou, R., Yao, F., et al. (2025) · Cell Biology International · doi:10.1002/cbin.70105 · Cited by 1 · see citing works
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Elimination of senescent cells fails to attenuate disease progression in an ALS mouse model
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FUSDelta14 mutation impairs normal brain development and causes systemic metabolic alterationsPreprint
Godoy-Corchuelo, J. M., Ali, Z., Martins-Bach, A. B., García-Toledo, I., Fernández-Beltrán, L. C., Nair, R., Spring, S., Nieman, B. J., Jiménez-Coca, I., Bains, R. S., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.24.529858
Role of sphingolipids in inflammatory carciongensis
El-Hindi, K. (2022) · doi:10.21248/gups.71949
HDAC6 inhibition as a mechanism to prevent axon degeneration in the mSOD1 G93A mouse model of ALSPreprint
Phipps, A. J., Dwyer, S., Collins, J. M., Kabir, F., Atkinson, R. A. K., Chowdhury, A., Matthews, L., Dixit, D., TERRY, R. S., Smith, J. A., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.28.555025
TDP-43 and ALS - what's wrong with my membranes?
Dahlhaus, R., Yalcin, I., Tischer, J., & Braun, R. J. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107630
- Authors
- Burg, T., Rossaert, E., Moisse, M., Van Damme, P., & Van Den Bosch, L.
- Affiliations
- VIB-KU Leuven Center for Brain & Disease Research (BE)
- Department of Neurosciences, Experimental Neurology, Leuven Brain Institute, KU Leuven—University of Leuven, 3000 Leuven, Belgium
- Venue
- International Journal of Molecular Sciences
- Publisher
- MDPI AG
- Published
- 2021-10-18
- Volume
- 22
- Issue
- 20
- Pages
- 11224
- ISSN
- 1422-0067 (ISSN-L)
- PMC
- PMC8541517
- OpenAlex
- W3207668409
- Cited by
- 50
- References
- 85
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 12 · 2023: 13 · 2022: 10 · 2021: 1
- FWCI
- 4.31
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- International Journal of Molecular Sciences (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Lirias (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Muscular Dystrophy Association (577668)
- Fondation Thierry Latran (00099187)
- Topics
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Genetic Neurodegenerative Diseases
- Keywords
- amyotrophic lateral sclerosis, histone deacetylase inhibition, lipid homeostasis, lipid metabolism, glycerophospholipids, sphingolipids, cholesterol esters, spinal cord, neurodegeneration, treatment options
- MeSH terms
- Lipidomics, Amyotrophic Lateral Sclerosis, Animals, Disease Models, Animal, Female, Hydroxamic Acids, Lipids, Male, Pyrimidines, RNA-Binding Protein FUS, Mice, Histone Deacetylase Inhibitors, Transcriptome
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