Matthijs Verhage

PROF.DR., (Principal Investigator)

20002019

Research output per year

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2019

A Single-Cell Model for Synaptic Transmission and Plasticity in Human iPSC-Derived Neurons

Meijer, M., Rehbach, K., Brunner, J. W., Classen, J. A., Lammertse, H. C. A., van Linge, L. A., Schut, D., Krutenko, T., Hebisch, M., Cornelisse, L. N., Sullivan, P. F., Peitz, M., Toonen, R. F., Brüstle, O. & Verhage, M., 14 May 2019, In : Cell Reports. 27, 7, p. 2199-2211.e6

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Doc2b Ca2+ binding site mutants enhance synaptic release at rest at the expense of sustained synaptic strength

Bourgeois-Jaarsma, Q., Verhage, M. & Groffen, A. J., 1 Dec 2019, In : Scientific Reports. 9, 1, p. 14408 14408.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Fbxo41 Promotes Disassembly of Neuronal Primary Cilia

King, C. R., A. A. Quadros, A. R., Chazeau, A., Saarloos, I., van der Graaf, A. J., Verhage, M. & Toonen, R. F., 1 Dec 2019, In : Scientific Reports. 9, 1, 8179.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Granulovacuolar degeneration bodies are neuron-selective lysosomal structures induced by intracellular tau pathology

Wiersma, V. I., van Ziel, A. M., Vazquez-Sanchez, S., Nölle, A., Berenjeno-Correa, E., Bonaterra-Pastra, A., Clavaguera, F., Tolnay, M., Musters, R. J. P., van Weering, J. R. T., Verhage, M., Hoozemans, J. J. M. & Scheper, W., 1 Dec 2019, In : Acta Neuropathologica. 138, 6, p. 943-970 28 p.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

MUNC18-1 regulates the submembrane F-actin network, independently of syntaxin1 targeting, via hydrophobicity in β-sheet 10

Pons-Vizcarra, M., Kurps, J., Tawfik, B., Sørensen, J. B., van Weering, J. R. T. & Verhage, M., 2019, In : Journal of Cell Science. 132, 23

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

SALM1 controls synapse development by promoting F-actin/PIP2-dependent Neurexin clustering

Brouwer, M., Farzana, F., Koopmans, F., Chen, N., Brunner, J. W., Oldani, S., Li, K. W., van Weering, J. R. T., Smit, A. B., Toonen, R. F. & Verhage, M., 2 Sep 2019, In : EMBO Journal. 38, 17, e101289.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Synaptotagmin-1 enables frequency coding by suppressing asynchronous release in a temperature dependent manner

Huson, V., van Boven, M. A., Stuefer, A., Verhage, M. & Cornelisse, L. N., 1 Dec 2019, In : Scientific Reports. 9, 1, p. 11341

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

SynGO: An Evidence-Based, Expert-Curated Knowledge Base for the Synapse

Koopmans, F., van Nierop, P., Andres-Alonso, M., Byrnes, A., Cijsouw, T., Coba, M. P., Cornelisse, L. N., Farrell, R. J., Goldschmidt, H. L., Howrigan, D. P., Hussain, N. K., Imig, C., de Jong, A. P. H., Jung, H., Kohansalnodehi, M., Kramarz, B., Lipstein, N., Lovering, R. C., MacGillavry, H., Mariano, V. & 53 others, Mi, H., Ninov, M., Osumi-Sutherland, D., Pielot, R., Smalla, K-H., Tang, H., Tashman, K., Toonen, R. F. G., Verpelli, C., Reig-Viader, R., Watanabe, K., van Weering, J., Achsel, T., Ashrafi, G., Asi, N., Brown, T. C., de Camilli, P., Feuermann, M., Foulger, R. E., Gaudet, P., Joglekar, A., Kanellopoulos, A., Malenka, R., Nicoll, R. A., Pulido, C., de Juan-Sanz, J., Sheng, M., Südhof, T. C., Tilgner, H. U., Bagni, C., Bayés, À., Biederer, T., Brose, N., Chua, J. J. E., Dieterich, D. C., Gundelfinger, E. D., Hoogenraad, C., Huganir, R. L., Jahn, R., Kaeser, P. S., Kim, E., Kreutz, M. R., McPherson, P. S., Neale, B. M., O'Connor, V., Posthuma, D., Ryan, T. A., Sala, C., Feng, G., Hyman, S. E., Thomas, P. D., Smit, A. B. & Verhage, M., 17 Jul 2019, In : Neuron. 103, 2, p. 217-234.e4

Research output: Contribution to journalArticleAcademicpeer-review

Unconventional secretion factor GRASP55 is increased by pharmacological unfolded protein response inducers in neurons

van Ziel, A. M., Largo-Barrientos, P., Wolzak, K., Verhage, M. & Scheper, W., 2019, In : Scientific Reports. 9, 1, 1567.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access
2018

Dense-core vesicle biogenesis and exocytosis in neurons lacking chromogranins A and B

Dominguez, N., van Weering, J. R. T., Borges, R., Toonen, R. F. G. & Verhage, M., 2018, In : Journal of Neurochemistry. 144, 3, p. 241-254

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

MIR137 schizophrenia-associated locus controls synaptic function by regulating synaptogenesis, synapse maturation and synaptic transmission

He, E., Lozano, M. A. G., Stringer, S., Watanabe, K., Sakamoto, K., Oudsten, F. D., Koopmans, F., Giamberardino, S. N., Hammerschlag, A., Niels Cornelisse, L., Li, K. W., van Weering, J., Posthuma, D., Smit, A. B., Sullivan, P. F. & Verhage, M., 2018, In : Human Molecular Genetics. 27, 11, p. 1879-1891

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Pool size estimations for dense-core vesicles in mammalian CNS neurons

Persoon, C. M., Moro, A., Nassal, J. P., Farina, M., Broeke, J. H., Arora, S., Dominguez, N., van Weering, J. R. T., Toonen, R. F. & Verhage, M., 2018, In : EMBO Journal. 37, 20, e99672.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Protein instability, haploinsufficiency, and cortical hyper-excitability underlie STXBP1 encephalopathy

Kovačević, J., Maroteaux, G., Schut, D., Loos, M., Dubey, M., Pitsch, J., Remmelink, E., Koopmans, B., Crowley, J., Cornelisse, L. N., Sullivan, P. F., Schoch, S., Toonen, R. F., Stiedl, O. & Verhage, M., 2018, In : Brain. 141, 5, p. 1350-1374

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Quantifying exosome secretion from single cells reveals a modulatory role for GPCR signaling

Verweij, F. J., Bebelman, M. P., Jimenez, C. R., Garcia-Vallejo, J. J., Janssen, H., Neefjes, J., Knol, J. C., de Goeij-de Haas, R., Piersma, S. R., Baglio, S. R., Verhage, M., Middeldorp, J. M., Zomer, A., van Rheenen, J., Coppolino, M. G., Hurbain, I., Raposo, G., Smit, M. J., Toonen, R. F. G., van Niel, G. & 1 others, Pegtel, D. M., 5 Mar 2018, In : Journal of Cell Biology. 217, 3, p. 1129-1142 14 p.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Secretory vesicle trafficking in awake and anaesthetized mice: differential speeds in axons versus synapses

Knabbe, J., Nassal, J. P., Verhage, M. & Kuner, T., 2018, In : Journal of Physiology. 596, 16, p. 3759-3773

Research output: Contribution to journalArticleAcademicpeer-review

Tyrosine phosphorylation of Munc18-1 inhibits synaptic transmission by preventing SNARE assembly

Meijer, M., Dörr, B., Lammertse, H. C., Blithikioti, C., van Weering, J. R., Toonen, R. F., Söllner, T. H. & Verhage, M., 17 Jan 2018, In : EMBO Journal. 37, 2, p. 300-320 21 p.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access

Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi

Emperador-Melero, J., Huson, V., van Weering, J., Bollmann, C., Fischer von Mollard, G., Toonen, R. F. & Verhage, M., 2018, In : Nature Communications. 9, 1, 3421.

Research output: Contribution to journalArticleAcademicpeer-review

Open Access
2017

Differential Maturation of the Two Regulated Secretory Pathways in Human iPSC-Derived Neurons

Emperador Melero, J., Nadadhur, A. G., Schut, D., Weering, J. V., Heine, V. M., Toonen, R. F. & Verhage, M., 14 Mar 2017, In : Stem Cell Reports. 8, 3, p. 659-672 14 p.

Research output: Contribution to journalArticleAcademicpeer-review

Early golgi abnormalities and neurodegeneration upon loss of presynaptic proteins munc18-1, syntaxin-1, or SNAP-25

Santos, T. C., Wierda, K., Broeke, J. H., Toonen, R. F. & Verhage, M., 26 Apr 2017, In : Journal of Neuroscience. 37, 17, p. 4525-4539 15 p.

Research output: Contribution to journalArticleAcademicpeer-review

Gene-set analysis shows association between FMRP targets and autism spectrum disorder

Jansen, A., Dieleman, G. C., Smit, A. B., Verhage, M., Verhulst, F. C., Polderman, T. J. C. & Posthuma, D., 1 Jun 2017, In : European Journal of Human Genetics. 25, 7, p. 863-868 6 p.

Research output: Contribution to journalArticleAcademicpeer-review

Integrated Bayesian analysis of rare exonic variants to identify risk genes for schizophrenia and neurodevelopmental disorders

Nguyen, H. T., Bryois, J., Kim, A., Dobbyn, A., Huckins, L. M., Munoz-Manchado, A. B., Ruderfer, D. M., Genovese, G., Fromer, M., Xu, X., Pinto, D., Linnarsson, S., Verhage, M., Smit, A. B., Hjerling-Leffler, J., Buxbaum, J. D., Hultman, C., Sklar, P., Purcell, S. M., Lage, K. & 3 others, He, X., Sullivan, P. F. & Stahl, E. A., 20 Dec 2017, In : Genome Medicine. 9, 1, 114.

Research output: Contribution to journalArticleAcademicpeer-review

Multi-level characterization of balanced inhibitory-excitatory cortical neuron network derived from human pluripotent stem cells

Nadadhur, A. G., Melero, J. E., Meijer, M., Schut, D., Jacobs, G., Wan Li, K., Hjorth, J. J. J., Meredith, R. M., Toonen, R. F., Van Kesteren, R. E., Smit, A. B., Verhage, M. & Heine, V. M., 1 Jun 2017, In : PLoS ONE. 12, 6, 0178533.

Research output: Contribution to journalArticleAcademicpeer-review

Munc13-1 and Munc18-1 together prevent NSF-dependent de-priming of synaptic vesicles

He, E., Wierda, K., Van Westen, R., Broeke, J. H., Toonen, R. F., Cornelisse, L. N. & Verhage, M., 21 Jun 2017, In : Nature Communications. 8, 15915.

Research output: Contribution to journalArticleAcademicpeer-review

Tomosyn associates with secretory vesicles in neurons through its N- and C-terminal domains

Geerts, C. J., Mancini, R., Chen, N., Koopmans, F. T. W., Li, K. W., Smit, A. B., Van Weering, J. R. T., Verhage, M. & Groffen, A. J. A., 1 Jul 2017, In : PLoS ONE. 12, 7, e0180912.

Research output: Contribution to journalArticleAcademicpeer-review

2016

Neurobeachin Regulates Glutamate- and GABA-Receptor Targeting to Synapses via Distinct Pathways.

Farzana, F., Zalm, R., Chen, N., Li, K. W., Grant, S. G., Smit, A. B., Toonen, R. F. G. & Verhage, M., 2016, In : Molecular Neurobiology. 53, 4, p. 2112-2123

Research output: Contribution to journalArticleAcademicpeer-review

Normal molecular specification and neurodegenerative disease-like death of spinal neurons lacking the snareassociated synaptic protein Munc18-1

Law, C., Profes, M. S., Levesque, M., Kaltschmidt, J. A., Verhage, M. & Kania, A., 13 Jan 2016, In : Journal of Neuroscience. 36, 2, p. 561-576 16 p.

Research output: Contribution to journalArticleAcademicpeer-review

Phosphorylation of synaptotagmin-1 controls a postpriming step in PKC-dependent presynaptic plasticity

De Jong, A. P. H., Meijer, M., Saarloos, I., Cornelisse, L. N., Toonen, R. F. G., Sorensen, J. B. & Verhage, M., 3 May 2016, In : Proceedings of the National Academy of Sciences of the United States of America. 113, 18, p. 5095-5100 6 p.

Research output: Contribution to journalArticleAcademicpeer-review

Presynaptic inhibition upon CB1 or mGlu2/3 receptor activation requires ERK/MAPK phosphorylation of Munc18-1

Schmitz, S. K., King, C., Kortleven, C., Huson, V., Kroon, T., Kevenaar, J. T., Schut, D., Saarloos, I., Hoetjes, J. P., de Wit, H., Stiedl, O., Spijker, S., Li, K. W., Mansvelder, H. D., Smit, A. B., Cornelisse, L. N., Verhage, M. & Toonen, R. F., 1 Jun 2016, In : EMBO Journal. 35, 11, p. 1236-50 15 p.

Research output: Contribution to journalArticleAcademicpeer-review

2015

A 1-night operant learning task without food-restriction differentiates among mouse strains in an automated home-cage environment

Remmelink, E., Loos, M., Koopmans, B., Aarts, E., van der Sluis, S., Smit, A. B. & Verhage, M., 2015, In : Behavioural Brain Research. 283, p. 53-60

Research output: Contribution to journalArticleAcademicpeer-review

Additive effects on the energy barrier for synaptic vesicle fusion cause supralinear effects on the vesicle fusion rate.

Schotten, S., Meijer, M., Walter, A. M., Huson, V. W. J., Mamer, L., Kalogreades, L., Veer, M. T., Ruiter, M., Brose, N., Rosenmund, C., Sorensen, J. B., Verhage, M. & Cornelisse, L. N., 2015, In : eLife. 4, e05531.

Research output: Contribution to journalArticleAcademicpeer-review

A Post-Docking Role of Synaptotagmin 1-C2B Domain Bottom Residues R398/399 in Mouse Chromaffin Cells.

Kedar, G. H., Munch, A. S., van Weering, J. R. T., Malsam, J., Scheutzow, A., de Wit, H., Houy, S., Tawfik, B., Sollner, T. H., Sorensen, J. B. & Verhage, M., 2015, In : Journal of Neuroscience. 35, 42, p. 14172-14182

Research output: Contribution to journalArticleAcademicpeer-review

CAPS-1 promotes fusion competence of stationary dense-core vesicles in presynaptic terminals of mammalian neurons.

Farina, M., van de Bospoort, R., He, E., Persoon, C. M., van Weering, J. R. T., Broeke, J. H. P., Verhage, M. & Toonen, R. F. G., 2015, In : eLife. 4, e05438.

Research output: Contribution to journalArticleAcademicpeer-review

Functional characterization of the PCLO p.Ser4814Ala variant associated with major depressive disorder reveals cellular but not behavioral differences

Giniatullina, A., Maroteaux, G. P., Geerts, C. J., Koopmans, B., Loos, M., Klaassen, R. V., Chen, N., van der Schors, R. C., van Nierop, P., Li, K. W., de Jong, A. P. H., Altrock, W. D., Cornelisse, L. N., Toonen, R. F. G., van der Sluis, S., Sullivan, P. F., Stiedl, O., Posthuma, D., Smit, A. B., Groffen, A. J. A. & 1 others, Verhage, M., 2015, In : Neuroscience. 300, p. 518-538

Research output: Contribution to journalArticleAcademicpeer-review

Interaction proteomics of canonical Caspr2 (CNTNAP2) reveals the presence of two Caspr2 isoforms with overlapping interactomes

Chen, N., Koopmans, F. T. W., Gordon, A., Paliukhovich, I., Klaassen, R. V., van der Schors, R. C., Peles, E., Verhage, M., Smit, A. B. & Li, K. W., 2015, In : Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics. 1854, 7, p. 827-833

Research output: Contribution to journalArticleAcademicpeer-review

Multilevel analysis quantifies variation in the experimental effect while optimizing power and preventing false positives

Aarts, E., Dolan, C. V., Verhage, M. & van der Sluis, S., 2015, In : BMC Neuroscience. 16, 94.

Research output: Contribution to journalArticleAcademicpeer-review

Synaptic Effects of Munc18-1 Alternative Splicing in Excitatory Hippocampal

Meijer, M., Cijsouw, A., Toonen, R. F. G. & Verhage, M., 2015, In : PLoS ONE. 10, 9, e0138950.

Research output: Contribution to journalArticleAcademicpeer-review

The light spot test: Measuring anxiety in mice in an automated home-cage environment

Aarts, E., Maroteaux, G. P., Loos, M., Koopmans, B., Kovacevic, J., Smit, A. B., Verhage, M. & van der Sluis, S., 2015, In : Behavioural Brain Research. 294, p. 123-130

Research output: Contribution to journalArticleAcademicpeer-review

Tomosyn-2 is required for normal motor performance in mice and sustains neurotransmission at motor endplates.

Geerts, C. J., Plomp, J. J., Koopmans, B., Loos, M., van der Pijl, EM., van der Valk, M. A., Verhage, M. & Groffen, A. J. A., 2015, In : Brain Structure and Function. 220, 4, p. 1971-1982

Research output: Contribution to journalArticleAcademicpeer-review

Within-strain variation in behavior differs consistently between common inbred strains of mice.

Loos, M., Koopmans, B., Aarts, E., van der Sluis, S., Smit, A. B. & Verhage, M., 2015, In : Mammalian Genome. 26, 7-8, p. 348-354

Research output: Contribution to journalArticleAcademicpeer-review

2014

A solution to dependency: using multilevel analysis to accommodate nested data

Aarts, E., Verhage, M., Veenvliet, J. V., Dolan, C. V. & van der Sluis, S., 2014, In : Nature Neuroscience. 17, 4, p. 491-496 6 p.

Research output: Contribution to journalArticleAcademicpeer-review

Display of individuality in avoidance behavior and risk assessment of inbred mice

Hager, T., Jansen, R. F., Pieneman, A. W., Manivannan, S. N., Golani, I., van der Sluis, S., Smit, A. B., Verhage, M. & Stiedl, O., 2014, In : Frontiers in Behavioral Neuroscience. 8, p. 314 314.

Research output: Contribution to journalArticleAcademicpeer-review

DOC2 isoforms play dual roles in insulin secretion and insulin-stimulated glucose uptake

Li, J., Cantley, J., Burchfield, J. G., Meoli, C. C., Stöckli, J., Whitworth, P. T., Pant, H., Chaudhuri, R., Groffen, A. J. A., Verhage, M. & James, D. E., 2014, In : Diabetologia. 57, 10, p. 2173-2182

Research output: Contribution to journalArticleAcademicpeer-review

Functional gene-set analysis does not support a major role for synaptic function in attention deficit/hyperactivity disorder (ADHD).

Hammerschlag, A. R., Polderman, T. J. C., de Leeuw, C. A., Tiemeier, H., White, T., Smit, A. B., Verhage, M. & Posthuma, D., 2014, In : Genes. 5, 3, p. 604-614

Research output: Contribution to journalArticleAcademicpeer-review

Munc18-1 is a dynamically regulated PKC target during short-term enhancement of transmitter release

Genc, O., Kochubey, O., Toonen, R. F. G., Verhage, M. & Schneggenburger, R., 2014, In : eLife. 2014, 3, p. e01715 e01715.

Research output: Contribution to journalArticleAcademicpeer-review

Muncl 8-1 redistributes in nerve terminals in an activity- and PKC-dependent manner

Cijsouw, T., Weber, J. P., Broeke, J. H. P., Broek, J. A., Schut, D., Kroon, T., Saarloos, I., Verhage, M. & Toonen, R. F. G., 2014, In : Journal of Cell Biology. 204, 5, p. 759-775

Research output: Contribution to journalArticleAcademicpeer-review

Sheltering behavior and locomotor activity in 11 genetically diverse common inbred mouse strains using home-cage monitoring

Loos, M., Koopmans, B., Aarts, E., Maroteaux, G. P., van der Sluis, S., Verhage, M. & Smit, A. B., 2014, In : PLoS ONE. 9, 9, p. e108563 e108563.

Research output: Contribution to journalArticleAcademicpeer-review

The BAR Domain Protein PICK1 Controls Vesicle Number and Size in Adrenal Chromaffin Cells

Pinheiro, P. S., Jansen, A. M., de Wit, H., Tawfik, B., Madsen, K. L., Verhage, M., Gether, U. & Sørensen, J. B., 2014, In : Journal of Neuroscience. 34, 32, p. 10688-10700

Research output: Contribution to journalArticleAcademicpeer-review

The SNARE protein vti1a functions in dense-core vesicle biogenesis

Walter, A. M., Kurps, J., de Wit, H., Schöning, S., Toft-Bertelsen, R. L., Lauks, J., Ziomkiewicz, I., Weiss, A. N., Schulz, A., Fischer von Mollard, G., Verhage, M. & Sørensen, J. B., 2014, In : EMBO Journal. 33, 15, p. 1681-1697

Research output: Contribution to journalArticleAcademicpeer-review

Tomosyn Interacts with the SUMO E3 Ligase PIAS gamma

Geerts, C. J., Jacobsen, L., van de Bospoort, R., Verhage, M. & Groffen, A. J. A., 2014, In : PLoS ONE. 9, 3, p. e91697 e91697.

Research output: Contribution to journalArticleAcademicpeer-review

2013

A sequential vesicle pool model with a single release sensor and a ca(2+)-dependent priming catalyst effectively explains ca(2+)-dependent properties of neurosecretion

Walter, A. M., Pinheiro, P. S., Verhage, M. & Sørensen, J. B., 2013, In : PLoS Computational Biology. 9, 12, p. e1003362 e1003362.

Research output: Contribution to journalArticleAcademicpeer-review