Publications

Key publications of the department of the last years:

2021
Moro A, Van Nifterick A, Toonen RF, Verhage M (2021) “Dynamin controls neuropeptide secretion by organizing dense-core vesicle fusion sites” Science Advances (in press, May 2021)
Van Westen R, Poppinga J, Díez Arazola R, Toonen RF, Verhage M (2020) “Neuromodulator release in neurons requires two functionally redundant calcium sensors” Proc Natl Acad Sci USA (in press, April 2021)

2020
Verhage M, Sørensen JB (2020) “SNAREopathies: Diversity in Mechanisms and Symptoms”. Neuron 107(1): 22-37.
Rajewsky N, LifeTime Community Working Groups (2020) “LifeTime and improving European healthcare through cell-based interceptive medicine”. Nature 587(7834): 377-386.
Moro A, van Woerden GM, Toonen RF, Verhage M (2020) “CaMKII controls neuromodulation via neuropeptide gene expression and axonal targeting of neuropeptide vesicles”. PLoS Biol. 18(8): e3000826.
Luo L, ….. Wortel J, … Verhage M, ….. Craig AM. (2020) “Optimizing Nervous System-Specific Gene Targeting with Cre Driver Lines: Prevalence of Germline Recombination and Influencing Factors”. Neuron 106(1): 37-65.
Lammertse HCA, van Berkel AA, Iacomino M, Toonen RF, Striano P, Gambardella A, Verhage M, Zara F. (2020) “Homozygous STXBP1 variant causes encephalopathy and gain-of-function in synaptic transmission”. Brain 143(2): 441-451.

2019
Persoon CM, Hoogstraaten RI, Nassal JP, van Weering JRT, Kaeser PS, Toonen RF, Verhage M (2019) “The RAB3-RIM Pathway Is Essential for the Release of Neuromodulators”. Neuron 104(6): 1065-1080.
Brouwer M, Farzana F, Koopmans F, Chen N, Brunner JW, Oldani S, Li KW, van Weering JR, Smit AB, Toonen RF, Verhage M (2019) “SALM1 controls synapse development by promoting F-actin/PIP2-dependent Neurexin clustering”. EMBO J. 38(17): e101289.
Koopmans F, van Nierop P, … Cornelisse LN, …. Toonen RF, … van Weering J, … Verhage M. (2019) “SynGO: An Evidence-Based, Expert-Curated Knowledge Base for the Synapse”. Neuron 103(2): 217-234.

2018
Persoon C.M., Moro A., Nassal J., Farina M., Broeke J.H., Swati Arora S., Dominguez N., van Weering J.R.T., Toonen R.F.G. and M. Verhage (2018) “Pool size estimations for dense-core vesicles in mammalian CNS neurons”. EMBO J. 37(20): e99672
Emperador-Melero, J., V. Huson, J. van Weering, C. Bollmann, G. Fischer von Mollard, R. F. Toonen and M. Verhage (2018). “Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi.” Nature Commun. 9(1): 3421.
Kovacevic, J., G. Maroteaux, D. Schut, M. Loos, M. Dubey, J. Pitsch, E. Remmelink, B. Koopmans, J. Crowley, L. N. Cornelisse, P. F. Sullivan, S. Schoch, R. F. Toonen, O. Stiedl and M. Verhage (2018). “Protein instability, haploinsufficiency, and cortical hyper-excitability underlie STXBP1 encephalopathy.” Brain 141(5): 1350-1374.
Meijer, M., B. Dorr, H. C. Lammertse, C. Blithikioti, J. R. van Weering, R. F. Toonen, T. H. Sollner and M. Verhage (2018). “Tyrosine phosphorylation of Munc18-1 inhibits synaptic transmission by preventing SNARE assembly.” EMBO J. 37(2): 300-320.

2017
Emperador Melero, J., A. G. Nadadhur, D. Schut, J. V. Weering, V. M. Heine, R. F. Toonen and M. Verhage (2017). “Differential Maturation of the Two Regulated Secretory Pathways in Human iPSC-Derived Neurons.” Stem Cell Reports 8(3): 659-672.
He, E., K. Wierda, R. van Westen, J. H. Broeke, R. F. Toonen, L. N. Cornelisse and M. Verhage (2017). “Munc13-1 and Munc18-1 together prevent NSF-dependent de-priming of synaptic vesicles.” Nature Commun. 8: 15915.

2016
Schmitz, S. K., C. King, C. Kortleven, V. Huson, T. Kroon, J. T. Kevenaar, D. Schut, I. Saarloos, J. P. Hoetjes, H. de Wit, O. Stiedl, S. Spijker, K. W. Li, H. D. Mansvelder, A. B. Smit, L. N. Cornelisse, M. Verhage and R. F. Toonen (2016). “Presynaptic inhibition upon CB1 or mGlu2/3 receptor activation requires ERK/MAPK phosphorylation of Munc18-1.” EMBO J 35(11): 1236-1250.
de Jong, A. P., M. Meijer, I. Saarloos, L. N. Cornelisse, R. F. Toonen, J. B. Sorensen and M. Verhage (2016). “Phosphorylation of synaptotagmin-1 controls a post-priming step in PKC-dependent presynaptic plasticity.” Proc Natl Acad Sci U S A 113(18): 5095-5100.

2015
Farina, M., R. van de Bospoort, E. He, C. M. Persoon, J. R. van Weering, J. H. Broeke, M. Verhage and R. F. Toonen (2015). “CAPS-1 promotes fusion competence of stationary dense-core vesicles in presynaptic terminals of mammalian neurons.” Elife 4 e02722.
Schotten, S., M. Meijer, A. M. Walter, V. Huson, L. Mamer, L. Kalogreades, M. ter Veer, M. Ruiter, N. Brose, C. Rosenmund, J. B. Sorensen, M. Verhage and L. N. Cornelisse (2015). “Additive effects on the energy barrier for synaptic vesicle fusion cause supralinear effects on the vesicle fusion rate.” Elife 4: e05531.

2014
Aarts, E., M. Verhage, J. V. Veenvliet, C. V. Dolan and S. van der Sluis (2014). “A solution to dependency: using multilevel analysis to accommodate nested data.” Nature Neurosci 17(4): 491-496.
Walter, A. M., J. Kurps, H. de Wit, S. Schoning, T. L. Toft-Bertelsen, J. Lauks, I. Ziomkiewicz, A. N. Weiss, A. Schulz, G. Fischer von Mollard, M. Verhage and J. B. Sorensen (2014). “The SNARE protein vti1a functions in dense-core vesicle biogenesis.” EMBO J 33(15): 1681-1697.
Cijsouw, T., J. P. Weber, J. H. Broeke, J. A. Broek, D. Schut, T. Kroon, I. Saarloos, M. Verhage and R. F. Toonen (2014). “Munc18-1 redistributes in nerve terminals in an activity- and PKC-dependent manner.” J Cell Biol 204(5): 759-775.
Genc, O., O. Kochubey, R. F. Toonen, M. Verhage and R. Schneggenburger (2014). “Munc18-1 is a dynamically regulated PKC target during short-term enhancement of transmitter release.” Elife 3: e01715.

2013
Li, H., S. Fertuzinhos, E. Mohns, T. S. Hnasko, M. Verhage, R. Edwards, N. Sestan and M. C. Crair (2013). “Laminar and columnar development of barrel cortex relies on thalamocortical neurotransmission.” Neuron 79(5): 970-986.
Ripke, S., C. O’Dushlaine, K. Chambert, …. D. Posthuma, …. M. Verhage, ….M. C. O’Donovan, K. Stefansson, E. Scolnick, S. Purcell, S. A. McCarroll, P. Sklar, C. M. Hultman and P. F. Sullivan (2013). “Genome-wide association analysis identifies 13 new risk loci for schizophrenia.” Nature Genet 45(10): 1150-1159.
van der Sluis, S., D. Posthuma, M. G. Nivard, M. Verhage and C. V. Dolan (2013). “Power in GWAS: lifting the curse of the clinical cut-off.” Mol Psychiatry 18(1): 2-3.
Nair, R., J. Lauks, S. Jung, N. E. Cooke, H. de Wit, N. Brose, M. W. Kilimann, M. Verhage and J. Rhee (2013). “Neurobeachin regulates neurotransmitter receptor trafficking to synapses.” J Cell Biol 200(1): 61-80.

2012
Heutink, P. and M. Verhage (2012). “Neurodegeneration: new road leads back to the synapse.” Neuron 75(6): 935-938.
Lips, E. S., L. N. Cornelisse, R. F. Toonen, …. M. Verhage, P. F. Sullivan, P. M. Visscher and D. Posthuma (2012). “Functional gene group analysis identifies synaptic gene groups as risk factor for schizophrenia.” Mol Psychiatry 17(10): 996-1006.
Meijer, M., P. Burkhardt, H. de Wit, R. F. Toonen, D. Fasshauer and M. Verhage (2012). “Munc18-1 mutations that strongly impair SNARE-complex binding support normal synaptic transmission.” EMBO J 31(9): 2156-2168.
de Jong, A. P., S. K. Schmitz, R. F. Toonen and M. Verhage (2012). “Dendritic position is a major determinant of presynaptic strength.” J Cell Biol 197(2): 327-337.
van de Bospoort, R., M. Farina, S. K. Schmitz, A. de Jong, H. de Wit, M. Verhage and R. F. Toonen (2012). “Munc13 controls the location and efficiency of dense-core vesicle release in neurons.” J Cell Biol 199(6): 883-891.

2011
Toonen, R. F. and M. Verhage (2011). “Crashpilot underachieves due to acetylation at the nerve terminal.” Neuron 72(5): 679-681.
Liu, Y., D. H. Blackwood, S., ….. Verhage, M. C. O’Donovan, M. J. Owen, B. W. Penninx, S. Purcell, P. Sklar, P. F. Sullivan and C. Wellcome Trust Case-Control (2011). “Meta-analysis of genome-wide association data of bipolar disorder and major depressive disorder.” Mol Psychiatry 16(1): 2-4.

2010
Groffen, A. J., S. Martens, R. Diez Arazola, L. N. Cornelisse, N. Lozovaya, A. P. de Jong, N. A. Goriounova, R. L. Habets, Y. Takai, J. G. Borst, N. Brose, H. T. McMahon and M. Verhage (2010). “Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release.” Science 327(5973): 1614-1618.
Mohrmann, R., H. de Wit, M. Verhage, E. Neher and J. B. Sorensen (2010). “Fast vesicle fusion in living cells requires at least three SNARE complexes.” Science 330(6003): 502-505.

2009
de Wit, H., A. M. Walter, I. Milosevic, A. Gulyas-Kovacs, D. Riedel, J. B. Sorensen and M. Verhage (2009). “Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes.” Cell 138(5): 935-946.
Verhage, M. and G. van Meer (2009). “Synaptobrevin, sphingolipids, and secretion: lube ‘n’ go at the synapse.” Neuron 62(5): 603-605.
Bochdanovits, Z., M. Verhage, A. B. Smit, E. J. de Geus, D. Posthuma, D. I. Boomsma, B. W. Penninx, W. J. Hoogendijk and P. Heutink (2009). “Joint reanalysis of 29 correlated SNPs supports the role of PCLO/Piccolo as a causal risk factor for major depressive disorder.” Mol Psychiatry 14(7): 650-652.
Sullivan, P. F., E. J. de Geus, G. Willemsen, …. Posthuma, ….P. Rizzu, …. M. Verhage, …. Martin, N. R. Wray, D. I. Boomsma and B. W. Penninx (2009). “Genome-wide association for major depressive disorder: a possible role for the presynaptic protein piccolo.” Mol Psychiatry 14(4): 359-375.
Verhage, M. (2009). “Organelle docking: R-SNAREs are late.” Proc Natl Acad Sci U S A 106(47): 19745-19746.

2008
Gerber, S. H., J. C. Rah, S. W. Min, X. Liu, H. de Wit, I. Dulubova, A. C. Meyer, J. Rizo, M. Arancillo, R. E. Hammer, M. Verhage, C. Rosenmund and T. C. Sudhof (2008). “Conformational switch of syntaxin-1 controls synaptic vesicle fusion.” Science 321(5895): 1507-1510.
Wierda, K. D., R. F. Toonen, H. de Wit, A. B. Brussaard and M. Verhage (2008). “Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity.” Neuron 54(2): 275-290.