Epigenetics and Chromatin in Memory and Brain Disorders
Publications
2023
Nicholas Raun, Spencer G Jones, Olivia Kerr, Crystal Keung, Veyan Ibrahim, MacKayla Williams, Deniz Top, Jamie M Kramer (2023) Trithorax regulates long-term memory in Drosophila through epigenetic maintenance of mushroom body metabolic identity and translation capacity. bioRxiv doi: https://doi.org/10.1101/2023.08.08.549887
Rots D*, Jakub TE*, Keung C, Jackson A, Banka S, Pfundt R, de Vries BBA, van Jaarsveld RH, Hopman SMJ, van Binsbergen E, Valenzuela I, Hempel M, Bierhals T, Kortüm F, Lecoquierre F, Goldenberg A, Hertz JM, Andersen CB, Kibæk M, Prijoles EJ, Stevenson RE, Everman DB, Patterson WG, Meng L, Gijavanekar C, De Dios K, Lakhani S, Levy T, Wagner M, Wieczorek D, Benke PJ, Lopez Garcia MS, Perrier R, Sousa SB, Almeida PM, Simões MJ, Isidor B, Deb W, Schmanski AA, Abdul-Rahman O, Philippe C, Bruel AL, Faivre L, Vitobello A, Thauvin C, Smits JJ, Garavelli L, Caraffi SG, Peluso F, Davis-Keppen L, Platt D, Royer E, Leeuwen L, Sinnema M, Stegmann APA, Stumpel CTRM, Tiller GE, Bosch DGM, Potgieter ST, Joss S, Splitt M, Holden S, Prapa M, Foulds N, Douzgou S, Puura K, Waltes R, Chiocchetti AG, Freitag CM, Satterstrom FK, De Rubeis S, Buxbaum J, Gelb BD, Branko A, Kushima I, Howe J, Scherer SW, Arado A, Baldo C, Patat O, Bénédicte D, Lopergolo D, Santorelli FM, Haack TB, Dufke A, Bertrand M, Falb RJ, Rieß A, Krieg P, Spranger S, Bedeschi MF, Iascone M, Josephi-Taylor S, Roscioli T, Buckley MF, Liebelt J, Dagli AI, Aten E, Hurst ACE, Hicks A, Suri M, Aliu E, Naik S, Sidlow R, Coursimault J, Nicolas G, Küpper H, Petit F, Ibrahim V, Top D, Di Cara F; Genomics England Research Consortium; Louie RJ, Stolerman E, Brunner HG, Vissers LELM, Kramer JM*, Kleefstra T.* (2023) The clinical and molecular spectrum of the KDM6B-related neurodevelopmental disorder. Am J Hum Genet. 110(6):963-978. *equal contributions.
2022
Blok LS, Verseput J, Rots D, Venselaar H, Innes AM, Stumpel C, Õunap K, Reinson K, Seaby EG, McKee S, Burton B, Kim K, van Hagen JM, Waisfisz Q, Joset P, Steindl K, Rauch A, Li D, Zackai EH, Sheppard SE, Keena B, Hakonarson H, Roos A, Kohlschmidt N, Cereda A, Iascone M, Rebessi E, Kernohan K, Campeau PM, Millan F, Taylor JA, Lochmüller H, Higgs MR, Goula A, Bernhard B, Velasco DJ, Schmanski
AA, Stark Z, Gallacher L, Pais L, Marcogliese PC, Yamamoto S, Raun N, Jakub TE, Kramer JM, den Hoed J, Fisher SE, Brunner HG, Kleefstra T. 2022. A clustering of heterozygous missense variants in the crucial chromatin modifier WDR5 defines a new neurodevelopmental disorder. Human Genetics and Genomics Advances. 4(1): 100157.
2021
Riahi H, Fenckova M, Goruk K, *Schenck A, *Kramer JM. 2021 The epigenetic regulator G9a attenuates stress-induced resistance and metabolic transcriptional programs across different stressors and species. BMC Biology, 19: 112. *equal contribution.
Raun N.*, Jones S.G.*, Kramer, J.M. (2021) Conditioned courtship suppression in Drosophila melanogaster. Journal of Neurogenetics. 35 (3), 154-167 *equal contribution. Review.
Kummeling J.*, Stremmelaar D.E.*, Raun N.*, Reijnders M, Willemsen MH, Ruiterkamp-Versteeg M, Schepens M, Man CCO, Gilissen C, Cho MT, McWalter K, Sinnema M, Wheless JW, Simon MEH, Genetti CA, Casey AM, Terhal PA, van der Smagt JJ, van Gassen KL, Joset P, Bahr A, Steindl K, Rauch A, Keller A, Raas-Rothschild A, Koolen DA, Agrawal PB, Hoffman TL, Powell-Hamilton NN, Thiffault I, Engleman K, Zhou D, Bodamer O, Hoefele J, Riedhammer KM, Schwaibold EMC, Tasic V, Schubert D, Top D, Pfundt R, *Higgs MR, *Kramer JM, *Kleefstra T (2021). Characterization of SETD1A haploinsufficiency in humans and Drosophila defines a novel neurodevelopmental syndrome. Molecular Psychiatry. 26, 2013-2024. *equal contribution.
2019
Nixon K.C.J.*, Rousseau, J.*, Stone M.H., Sarikahya M., Ehresmann S., Mizuno S., Matsumoto N., Miyake N., DDD study, Baralle D., McKee S., Izumi K., Ritter A., Heide S., Héron D., Depienne C., Titheradge,H., Kramer J.M.*, and Campeau P.M.* (2019) A Syndromic Neurodevelopmental Disorder Caused by Mutations in SMARCD1, a Core SWI/SNF Subunit Needed for Context-Dependent Neuronal Gene Regulation in Flies. American Journal of Human Genetics. 104(4): 596-610. *equal contribution
Chubak M.C., Nixon K.C.J., Stone M.H., Raun N., Rice S.L., Sarikahya M., Jones S.G., Lyons T.A., Jakub T.E., Mainland R.L.M., Knip M.J., Edwards T.N., and Kramer J.M. (2019) Individual components of the SWI/SNF chromatin remodeling complex have distinct roles in memory neurons of the Drosophila mushroom body. Disease Models and Mechanisms. 12(2): dmm037325.
Riahi H., Brekelmans C., Foriel S, Merkling S.H., Lyons T.A., Itskov P.M., Kleefstra T., Ribeiro C., van Rij R.P., Kramer J.M.*, Schenck A.* (2019) The histone methyltransferase G9a regulates tolerance to oxidative stress-induced energy consumption. PLoS Biology. 17(3): e2006146 *equal contribution.
Castells-Nobau A, Eidhof I, Fenckova M, Brenman-Suttner DB, Scheffer-de Gooyert JM, Christine S, Schellevis RL, van der Laan K, Quentin C, van Ninhuijs L, Hofmann F, Ejsmont R, Fisher SE, Kramer JM, Sigrist SJ, Simon AF, Schenck A. (2019) Conserved regulation of neurodevelopmental processes and behavior by FoxP in Drosophila. PLoS One. 14(2): e0211652.
2018
Jones S.G., Nixon K.C.J., and Kramer J.M. (2018) Mushroom body specific transcriptome analysis reveals dynamic regulation of learning and memory genes after acquisition of long-term courtship memory. G3: Genes, Genomes, Genetics, 8(11) 3433-3446.
2017
Mainland R.L., Lyons T.A., Ruth M.M., Kramer J.M. (2017) Optimal RNA isolation method and primer design to detect gene knockdown by qPCR when validating Drosophila transgenic RNAi lines. BMC Research Notes, 10: 647.
Koemans T.S., Kleefstra T., Chubak M.C., Stone M.H., Reijnders M.R.F., Munnik S., Willemsen M.H., Fenckova M., Stumpel C.T.R.M., Bok L.A., Saenz M.S., Byerly K.A., Baughn L.B., Stegmann A.P.A., Pfundt R., Zhou H., Bokhoven H., Schenck A.*, Kramer J.M.* (2017) Functional Convergence of Histone Methyltransferases EHMT1 and KMT2C Involved in Intellectual Disability and Autism Spectrum Disorder. PLoS Genetics, 13(10): e1006864. *equal contribution
Anreiter I., Kramer J.M., Skolowski M.B. (2017) Epigenetic mechanisms modulate differences in Drosophila foraging behavior. PNAS, 114(47): 12518-12523.
Farhan S.M.K, Nixon K.C.J., Everest M., Edwards T.N., Long S., Segal D., Knip M.J., Arts H.H., Chakrabarti R., Wang J., Robinson J.F., Lee D., Mirsattari S.M., Rupar C.A., Siu V.M., FORGE Canada Consortium, Poulter M.O., Hegele R.A., Kramer J.M. (2017) Identification of a novel synaptic protein, TMTC3, involved in periventricular nodular heterotopia with intellectual disability and epilepsy. Human Molecular Genetics, 26(21): 42778-4289.
Koemans TS, Oppitz C, Donders RAT, Bokhoven H, Schenck A, Keleman K, Kramer JM. (2017) Drosophila courtship conditioning as a measure of learning and memory. Journal of Visualized Experiments, 124: e55808.
2016
Kochinke K., Zweier C., Nijhof B., Fenckova M., Cizek P., Honti F., Keerthikumar S., Oortveld M.A.W., Kleefstra T., Kramer J.M., Webber C., Huynen M., Schenck A. (2016) Systematic phenomics analysis deconvolutes intellectual disability genes into biologically coherent modules. American Journal of Human Genetics, 98(1):149-64.
Kramer J.M. (2016) Regulation of cell differentiation and function by the euchromatin histone methyltranserfases G9a and GLP. Biochemistry and Cell Biology, 94(1): 26-32.
2015
Dubos A, Castells-Nobau A, H Meziane, MAW Oortveld, X Houbaert, G Iacono, C Martin, C Mittelhaeuser, V Lalanne, Kramer J.M., C Quentin, J Slabbert, P Verstreken, N Messaddeq, SJ Sigrist, M Birling, M Selloum, HG Stunnenberg, Y Humeau, A Schenck, Y Herrault. (2015) Conditional depletion of intellectual disability and Parkinsonism candidate gene ATP6AP2 in fly and mouse induces cognitive impairment and neurodegeneration. Human Molecular Genetics, 24(23): 6736-55.
Merkling S., Bronkhorst A.W., Kramer J.M., Overheul G.J., Schenck A., van Rij R.P. (2015) The epigenetic regulator G9a mediates tolerance to RNA virus infection in Drosophila. PLoS Pathogens, 11: e1004692.
2014
Gregor A., Kramer J.M., van der Voet M., Schanze I., Uebe S., Donders R., Reis A., Schenck A., Zweier C. (2014) Altered GPM6A/M6 Dosage Impairs Cognition and Causes Phenotypes Responsive to Cholesterol in Human and Drosophila. Human Mutation 35 (12): 1495-1505.
Berube, N.G. and Kramer, J.M. Epigenetics in Intellectual Disability. (2014) In Epigenetics in Psychiatry, ed. Jacob Peedicayil, Dimitri Avramopoulos, and Dennis R. Grayson. Elsevier.
Kleefstra T., Schenck, A., Kramer, J.M., van Bokhoven, H. (2014) The genetics of cognitive epigenetics. Neuropharmacology. 80: 83-94.
2013
Vandewalle J., Langen M., Zschaetzsch M., Nijhof B., Kramer J.M., Brems H., Bauters M., Lauwers E., Srahna M., Marynen P., Verstreken P., Schenck A., Hassan B.A., Froyen G. (2013) Ubiquitin ligase HUWE1 regulates axon branching through the Wnt/beta-catenin pathway in a Drosophila model for intellectual disability. PLoS One, 8(11): e81791.
Gupta V.K., Scheunemann L., Eisenberg T., Mertel S., Bhukel A., Koemans T.S., Kramer J.M., Liu K.S., Schroeder S., Stunnenberg H.G., Sinner F., Magnes C., Pieber T.R., Dipt S., Fiala A., Schenck A., Schwaerzel M., Madeo F., and Sigrist S.J. (2013) Restoration of polyamines protects from age-induced memory impairment in an autophagy-dependent manner. Nature Neuroscience, 16(10):1453-60.
van Bon, B.W.M., Oortveld M.A.W., Nijtmans, L.G., Fenckova, M., Nijhof, B., Besseling, J., Kramer, J.M., de Leeuw, N., Castells Nobau, A., Asztalos, L., Viragh, E., Ruiter, M., Hofmann, F., Eshuis, L., Collavin, L., Huynen, M.A., Asztalos, Z., Verstreken, P., Rodenburg, R.J., Smeitink, J.A., de Vries, B.B.A., and Schenck, A. (2013) CEP89 is required for mitochondrial metabolism and neuronal function in man and fly. Human Molecular Genetics, 22(15): 3138-51.
Iqbal, Z., Vandeweyer, G., van der Voet, M., Waryah, A.M., Zahoor, M.Y., Besseling, J., Tomas Roca, L., Vulto-van Silfhout, A.T., Nijhof, B., Kramer, J.M., van der Aa, N., Ansar, M., Peeters, H., Helsmoortel, C., Gilissen, C., Vissers, L., Veltman, J.A., de Brouwer, A.M.P., Kooy, F.R., Riazuddin, S., Schenck, A., van Bokhoven, H., Rooms, L. (2013) Homozygous and heterozygous disruptions of ANK3: at the crossroads of neurodevelopmental and psychiatric disorders. Human Molecular Genetics, 22(10): 1960-70.
Kramer J.M. (2013) Epigenetic regulation of memory: implications in human cognitive disorders. Biomolecular Concepts. 4(1): 1-12.
2012
Kleefstra, T.*, Kramer, J.M.*, Neveling, K., Willemsen, M.H., Koemans, T., Vissers, L.E., Wissink-Lindhout, W., van den Akker, W., Kasri, N.N., Nillesen, W.M., Prescott, T., Clark, R.D., Devriendt, K., van Reeuwijk, J., de Brouwer, A.P.M., Gilissen, C., Zhou, H., Veltman, J.A., Schenck, A., van Bokhoven, H. (2012) Disruption of an EHMT1-associated chromatin modification module causes intellectual disability. American Journal of Human Genetics, 91(1): 73-82. *equal contribution
Koolen, D.A.*, Kramer, J.M.*, Neveling, K.*, Nillessen, W.M., Moore-Barton, H., Elmslie, F.V., Toutain, A., Amiel, J., Tsai, A.C., Cheung, S.W., Gillissen, C., Verwiel, E., Martens, S., Feuth, T., Bongers, E., de Vries, P., Scheffers, H., Vissers, L.E., de Brouwer, A.P.M., Brunner, H.G., Schenck, A., Veltman, J.A., Yntema, H., de Vries, B.A.B. (2012) Mutations in the chromatin modifier gene KANSL1 cause the 17q21.31 microdeletion syndrome. Nature Genetics, 44(6): 639-41. *equal contribution
2011
Kramer, J.M., Kochinke, K., Oortveld, M.A.W., Marks, H., Kramer, D., de Jong, E.K., Asztalos, Z., Westwood, J.T., Stunnenberg, H.G., Sokolowski, M.B., Keleman, K., Zhou, H., van Bokhoven, H., and Schenck, A. (2011) Epigenetic regulation of learning & memory by Drosophila EHMT/G9a. PLoS Biology, 9(1): e1000569.
2010
Mukhopadhyay, A.*, Kramer, J.M.*, Merkx, G., Lugtenberg, D., Smeets, D., Oortveld, M.A.W., Blokland, E., Agrawal, J., Schenck, A., van Bokhoven, H., Huys, H., Schoenmakers, E., van Kessel, A.G., van Nouhuys, E., and Cremers, F.P.M. (2010) CDK19 is disrupted in a female patient with bilateral congenital retinal folds, microcephaly and mild mental retardation. Human Genetics, 28(3): 281-91. *equal contribution.
van Bokhoven, H. and Kramer, J.M. (2010) Disruption of the Epigenetic Code: A Common Molecular Mechanism in Mental Retardation. Neurobiology of Disease. 39(1): 3-12.
2009
Cliffe, S.T.*, Kramer, J.M.*, Hussain, K.*, Robben, J.H., de Jong, E.K., de Brouwer, A.P., Nibbeling, E., Kamsteeg, E.J., Wong, M., Prendiville, J., James, C., Padidela, R., Becknell, C., van Bokhoven, H., Deen, P.M., Hennekam, R.C., Lindeman, R., Schenck, A., Roscioli, T., Buckley, M.F. (2009) SLC29A3 gene is mutated in pigmented hypertrichosis with insulin-dependent diabetes mellitus syndrome and interacts with the insulin signaling pathway. Human Molecular Genetics, 18(12): 2257-65. *equal contribution.
2008
Kramer J.M. and van Bokhoven H. (2008) Genetic and epigenetic defects in mental retardation. International Journal of Biochemistry and Cell Biology. 41(1): 96-107.
Kramer, J.M., Slade, J.D., and Staveley, B.E. (2008) foxo is required for resistance to amino acid starvation in Drosophila. Genome, 51(8): 668-72.
2003
Kramer, J.M., and Staveley, B.E. (2003) GAL4 causes developmental defects and apoptosis when expressed in the developing eye of Drosophila melanogaster. Genetic and Molecular Research. 2: 43-47.
Kramer, J.M., Davidge, J.T., Lockyer, J.M., Staveley, B.E. (2003) Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Developmental Biology. 3: 5.