• Cell Biology - Department of Biology - Faculty of Science - Utrecht University
  • Cell Biology - Department of Biology - Faculty of Science - Utrecht University
  • Cell Biology - Department of Biology - Faculty of Science - Utrecht University
Cell Biology

Casper Hoogenraad: Cell Biology of the Neuron

CV - Research - Projects - Lab members - Publications

 


casper_hoogenraadProf. dr. Casper Hoogenraad
Cell Biology, Faculty of Science, Utrecht University
Kruytgebouw, room N501
Padualaan 8, 3584CH Utrecht
The Netherlands
Tel. +31-(0)30-2534585
Fax. +31-(0)30-2532837
E-mail This email address is being protected from spambots. You need JavaScript enabled to view it.

 


 Curriculum Vitae

PhD, Erasmus University Rotterdam (1996-2001)
Postdoc, Massachusetts Institute of Technology (2002-2005)
Associate professor, Erasmus Medical Center (2006-2010)
Full professor, Utrecht University (2011-present)

Casper Hoogenraad is recipient of ZonMW-VIDI (2004), ESF-EURYI (2005) and NWO-ALW VICI (2011) grants.

A pdf of a short CV can be downloaded here.

dejongeakademieCasper Hoogenraad is a member of “De Jonge Akademie (DJA)”, which is part of the Royal Academy of Arts and Sciences (KNAW). DJA focuses on three themes - interdisciplinarity within science and scholarship, science policy and science and society. See short introduction video (in Dutch). For more information about De Jonge Akademie, please see their website.

 

emboCasper Hoogenraad is member of the European Molecular Biology Organization (EMBO) - Young Investigator Program (YIP). EMBO-YIP selects independent scientists throughout their member states, thereby creating a European network of outstanding life scientists. See website EMBO-YIP.  

 


 Research summary

The primary goal of the lab is to understand how intracellular protein trafficking underlies neuronal development and function. This work is significant because neurons are dependent upon very precise localization of proteins to support their ability to send and receive information.

Neuronal cells represent a unique model for addressing fundamental questions in molecular and cellular biology. The size, shape and specialized functions of neurons permit analyses of neuronal migration, axon and dendrite outgrowth, and synapse formation and function. By understanding the basic cellular mechanisms and development of individual neurons, we can better understand how the nervous system develops and functions in an entire animal.

We particularly focus on the areas of microtubule cytoskeleton, synaptic cargo trafficking and synaptic plasticity. The research in the lab can roughly be divided in three themes:

  • Cytoskeleton dynamics during neurodevelopment and synaptic plasticity
  • Motor proteins and adaptors as regulators of synaptic transport
  • Neuropsychiatric disorders linked to intracellular transport

Our research relies on combining different genetics, biochemistry, molecular, and cellular biology methods in in vitro (neuron cultures), ex vivo (brain slices), and in vivo (mice) systems. In addition we employ immunofluorescent confocal microscopy, high-resolution live cell imaging (spinning disc microscopy and total internal reflection fluorescence microscopy, TIRF) and quantitative analysis using advanced high-resolution microscopy (photo-activated localization microscopy, PALM).

 


 Projects

- Cytoskeleton dynamics during neurodevelopment and synaptic plasticity

spineDendritic spines are small protrusions on neuronal dendrites that constitute the postsynaptic component of most excitatory (glutamatergic) synapses in the brain. Ever since their discovery at the turn of the 19th century by Ramon y Cajal, spines are assumed to serve as determinants of synaptic strength and major sites of information processing and storage in the brain. There is now strong experimental evidence that changes in dendritic spine morphology play an important role in the cognitive processes in brain.

We have recently shown that dynamic microtubules enter dendritic spines, are temporal and spatial regulators of spine actin dynamics and cause transient morphological spine alterations. Now we focus on i) the molecular mechanism by which dynamic microtubules enter dendritic spines and regulate actin dynamics ii) the relation between cytoskeletal organization and cargo transport in spines iii) the effect of synaptic activity on the microtubule cytoskeleton.

 

- Motor proteins and adaptors as regulators of synaptic transport

pex1In order to form new synapses and alter the strength of synaptic transmission, neurons need a regulatory mechanism to deliver and remove synaptic proteins at synaptic sites. Neurons make use of active transport driven by molecular motor proteins to move synaptic cargo over either microtubules (kinesin, dynein) or actin filaments (myosin) to their specific site of action. These mechanisms are crucial for the initial establishment of synaptic specializations during synaptogenesis and for activity-dependent changes in synaptic strength during plasticity.

Research in the lab focuses on synaptic cargo sorting and trafficking into axons and dendrites and the spatial and temporal regulation of motor protein-based transport. We recently developed an inducible cargo trafficking assay to probe motor protein activity in neuronal cells.

 

- Psychiatric and neurologic disease disorders linked to intracellular transport

neuron1The relationship between the cytoskeleton, motor protein transport and synaptic signaling is immediately clear when the brain becomes dysfunctional. Recent genetic, neuropathological, functional imaging, and pharmacological evidence implicate synapses are key sites for the pathogenesis of neurological and mental diseases, including Alzheimer’s disease (AD), schizophrenia, and autism spectrum disorders (ASD).

Moreover, hampering neuronal trafficking may underlie several adult-onset neurodegenerative diseases, such as Huntington’s disease (HD) and the motor neuron degenerative disease Amyotrophic Lateral Sclerosis (ALS) or be involved in the inflammatory disease Multiple Sclerosis (MS).

 

Understanding the molecular link between neuronal transport and synaptic pathology may provide essential insight into the pathogenesis of these disorders, and can reveal novel drug targets to treat these mental and neurological disorders. We focus on the role of the cytoskeleton and neuronal transport routes in several psychiatric and neurological disorders.

 


 Lab members

Technicians:  
Phebe Wulf This email address is being protected from spambots. You need JavaScript enabled to view it.
Bart de Haan This email address is being protected from spambots. You need JavaScript enabled to view it.
   
Postdocs:  
Karin Boekhoorn This email address is being protected from spambots. You need JavaScript enabled to view it.
Ines Cunha Ferreira This email address is being protected from spambots. You need JavaScript enabled to view it.
Amélie Fréal This email address is being protected from spambots. You need JavaScript enabled to view it.
Laura Gumy This email address is being protected from spambots. You need JavaScript enabled to view it.
Martin Harterink This email address is being protected from spambots. You need JavaScript enabled to view it.
Marina Mikhaylova This email address is being protected from spambots. You need JavaScript enabled to view it.
Philipp Schätzle This email address is being protected from spambots. You need JavaScript enabled to view it.
Elena Tortosa This email address is being protected from spambots. You need JavaScript enabled to view it.
Lena Will This email address is being protected from spambots. You need JavaScript enabled to view it.
   
PhD students:  
Kah Wai Yau This email address is being protected from spambots. You need JavaScript enabled to view it.
Robert van den Berg This email address is being protected from spambots. You need JavaScript enabled to view it.
Marta Silva This email address is being protected from spambots. You need JavaScript enabled to view it.
Mariella Franker This email address is being protected from spambots. You need JavaScript enabled to view it.
Joanna Lipka This email address is being protected from spambots. You need JavaScript enabled to view it.
Sam van Beuningen This email address is being protected from spambots. You need JavaScript enabled to view it.
Petra van Bergeijk This email address is being protected from spambots. You need JavaScript enabled to view it.
Josta Kevenaar This email address is being protected from spambots. You need JavaScript enabled to view it.
Catia Frias This email address is being protected from spambots. You need JavaScript enabled to view it.
Michael Dumbacher This email address is being protected from spambots. You need JavaScript enabled to view it.
Riccardo Stucchi This email address is being protected from spambots. You need JavaScript enabled to view it.
Dieudonnée van de Willige This email address is being protected from spambots. You need JavaScript enabled to view it.

 


 Publications

Research paper - Review - Book chapter

Research paper

2013

Schwenk BM, Lang CM, Hogl S, Tahirovic S, Orozco D, Rentzsch K, Lichtenthaler SF, Hoogenraad CC, Capell A, Haass C, and Edbauer D. The FTLD risk factor TMEM106B and MAP6 control dendritic trafficking of lysosomes. EMBO J. 2013 Dec 19 PMID: 24357581.

Kusters R, Kapitein LC, Hoogenraad CC, and Storm C. Shape-induced asymmetric diffusion in dendritic spines allows efficient synaptic AMPA receptor trapping. Biophys J. 2013 Dec 17, 105(12): 2743-50. PMID: 24359746.

Benoit RM, Frey D, Hilbert M, Kevenaar JT, Wieser MM, Stirnimann CU, McMillan D, Ceska T, Lebon F, Jaussi R, Steinmetz MO, Schertler GF, Hoogenraad CC, Capitani G, and Kammerer RA. Structural basis for recognition of synaptic vesicle protein 2C by botulinum neurotoxin A. Nature. 2013 Nov 17 PMID: 24240280.

van der Vaart B, van Riel WE, Doodhi H, Kevenaar JT, Katrukha EA, Gumy L, Bouchet BP, Grigoriev I, Spangler SA, Yu KL, Wulf PS, Wu J, Lansbergen G, van Battum EY, Pasterkamp RJ, Mimori-Kiyosue Y, Demmers J, Olieric N, Maly IV, Hoogenraad CC, and Akhmanova A. CFEOM1-associated kinesin KIF21A is a cortical microtubule growth inhibitor. Dev Cell. 2013 Oct 28, 27(2): 145-60. PMID: 24120883.

van Spronsen M, van Battum EY, Kuijpers M, Vangoor VR, Rietman ML, Pothof J, Gumy LF, van Ijcken WF, Akhmanova A, Pasterkamp RJ, and Hoogenraad CC. Developmental and activity-dependent miRNA expression profiling in primary hippocampal neuron cultures. PLoS One. 2013, 8(10): e74907. PMID: 24098357.

Kuijpers M, Yu KL, Teuling E, Akhmanova A, Jaarsma D, and Hoogenraad CC. The ALS8 protein VAPB interacts with the ER-Golgi recycling protein YIF1A and regulates membrane delivery into dendrites. EMBO J. 2013 Jul 17, 32(14): 2056-72. PMID: 23736259.

Gumy LF, Chew DJ, Tortosa E, Katrukha EA, Kapitein LC, Tolkovsky AM, Hoogenraad CC, and Fawcett JW. The kinesin-2 family member KIF3C regulates microtubule dynamics and is required for axon growth and regeneration. J Neurosci. 2013 Jul 10, 33(28): 11329-45. PMID: 23843507.

Kuijpers M, van Dis V, Haasdijk ED, Harterink M, Vocking K, Post JA, Scheper W, Hoogenraad CC, and Jaarsma D. Amyotrophic lateral sclerosis (ALS)-associated VAPB-P56S inclusions represent an ER quality control compartment. Acta Neuropathol Commun. 2013, Jun 12,1(1): 24. PMID: 24252306.

Spangler SA, Schmitz SK, Kevenaar JT, de Graaff E, de Wit H, Demmers J, Toonen RF, and Hoogenraad CC. Liprin-alpha2 promotes the presynaptic recruitment and turnover of RIM1/CASK to facilitate synaptic transmission. J Cell Biol. 2013 Jun 10, 201(6): 915-28. PMID: 23751498.

de Graaf EL, Vermeij WP, de Waard MC, Rijksen Y, van der Pluijm I, Hoogenraad CC, Hoeijmakers JH, Altelaar AF, and Heck AJ. Spatio-temporal analysis of molecular determinants of neuronal degeneration in the aging mouse cerebellum. Mol Cell Proteomics. 2013 May, 12(5): 1350-62. PMID: 23399551.

Kapitein LC, van Bergeijk P, Lipka J, Keijzer N, Wulf PS, Katrukha EA, Akhmanova A, and Hoogenraad CC. Myosin-V opposes microtubule-based cargo transport and drives directional motility on cortical actin. Curr Biol. 2013 May 6, 23(9): 828-34. PMID: 23602478.

van Spronsen M, Mikhaylova M, Lipka J, Schlager MA, van den Heuvel DJ, Kuijpers M, Wulf PS, Keijzer N, Demmers J, Kapitein LC, Jaarsma D, Gerritsen HC, Akhmanova A, and Hoogenraad CC. TRAK/Milton motor-adaptor proteins steer mitochondrial trafficking to axons and dendrites. Neuron. 2013 Feb 6, 77(3): 485-502. PMID: 23395375.

Prota AE, Magiera MM, Kuijpers M, Bargsten K, Frey D, Wieser M, Jaussi R, Hoogenraad CC, Kammerer RA, Janke C, and Steinmetz MO. Structural basis of tubulin tyrosination by tubulin tyrosine ligase. J Cell Biol. 2013 Feb 4, 200(3): 259-70. PMID: 23358242.

2012

van der Vaart B, Franker MA, Kuijpers M, Hua S, Bouchet BP, Jiang K, Grigoriev I, Hoogenraad CC, and Akhmanova A. Microtubule plus-end tracking proteins SLAIN1/2 and ch-TOG promote axonal development. J Neurosci. 2012 Oct 17, 32(42): 14722-8. PMID: 23077057.

Splinter D, Razafsky DS, Schlager MA, Serra-Marques A, Grigoriev I, Demmers J, Keijzer N, Jiang K, Poser I, Hyman AA, Hoogenraad CC, King SJ, Akhmanova A. BICD2, dynactin and LIS1 cooperate in regulating dynein recruitment to cellular structures. Mol Biol Cell. 2012 Sep 5. PMID: 22956769

de Graaff E, Maat P, Hulsenboom E, van den Berg R, van den Bent M, Demmers J, Lugtenburg PJ, Hoogenraad CC, Sillevis Smitt P. Identification of delta/notch-like epidermal growth factor-related receptor as the Tr antigen in paraneoplastic cerebellar degeneration. Ann Neurol. 2012 Jun;71(6):815-24. doi: 10.1002/ana.23550. PMID: 22447725 

Zhou M, Hoogenraad CC, Joëls M, Krugers HJ. Combined β-adrenergic and corticosteroid receptor activation regulates AMPA receptor function in hippocampal neurons. J Psychopharmacol. 2012 Apr;26(4):516-24. Epub 2011 Oct 2. PMID: 21965192

2011

Hayashi K, Suzuki A, Hirai S, Kurihara Y, Hoogenraad CC, Ohno S. Maintenance of dendritic spine morphology by partitioning-defective 1b through regulation of microtubule growth. J Neurosci. 2011 Aug 24;31(34):12094-103. PMID: 21865452

Wei Z, Zheng S, Spangler SA, Yu C, Hoogenraad CC, Zhang M. Liprin-mediated large signaling complex organization revealed by the liprin-α/CASK and liprin-α/liprin-β complex structures. Mol Cell. 2011 Aug 19;43(4):586-98.PMID: 21855798

Kapitein LC, Yau KW, Gouveia SM, van der Zwan WA, Wulf PS, Keijzer N, Demmers J, Jaworski J, Akhmanova A, Hoogenraad CC.NMDA receptor activation suppresses microtubule growth and spine entry. J Neurosci. 2011 Jun 1;31(22):8194-209.PMID:21632941

Spangler SA, Jaarsma D, de Graaff E, Wulf PS, Akhmanova A, Hoogenraad CC.
Differential expression of liprin-α family proteins in the brain suggests functional diversification. J Comp Neurol. 2011 May 25. doi: 10.1002/cne.22665. PMID:21618222

van der Vaart B, Manatschal C, Grigoriev I, Olieric V, Gouveia SM, Bjelic S, Demmers J, Vorobjev I, Hoogenraad CC, Steinmetz MO, Akhmanova A. SLAIN2 links microtubule plus end-tracking proteins and controls microtubule growth in interphase. J Cell Biol. 2011 Jun 13;193(6):1083-99. Epub 2011 Jun 6.PMID: 21646404

Grigoriev I, Yu KL, Martinez-Sanchez E, Serra-Marques A, Smal I, Meijering E, Demmers J, Peränen J, Pasterkamp RJ, van der Sluijs P, Hoogenraad CC, Akhmanova A.Rab6, Rab8, and MICAL3 cooperate in controlling docking and fusion of exocytotic carriers. Curr Biol. 2011 Jun 7;21(11):967-74. Epub 2011 May 19. PMID: 21596566

Bralten LB, Nouwens S, Kockx C, Erdem L, Hoogenraad CC, Kros JM, Moorhouse MJ, Sillevis Smitt PA, van der Spek P, van Ijcken W, Stubbs A, French PJ. Absence of common somatic alterations in genes on 1p and 19q in oligodendrogliomas. PLoS One. 2011;6(7):e22000. Epub 2011 Jul 7.PMID:21760942

Hossaini M, Cano SC, van Dis V, Haasdijk ED, Hoogenraad CC, Holstege JC, Jaarsma D. Spinal Inhibitory Interneuron Pathology Follows Motor Neuron Degeneration Independent of Glial Mutant Superoxide Dismutase 1 Expression in SOD1-ALS Mice. J Neuropathol Exp Neurol. 2011 Aug;70(8):662-77.PMID:21760539

Borgesius NZ, van Woerden GM, Buitendijk GH, Keijzer N, Jaarsma D, Hoogenraad CC, Elgersma Y. {beta}CaMKII Plays a Nonenzymatic Role in Hippocampal Synaptic Plasticity and Learning by Targeting {alpha}CaMKII to Synapses. J Neurosci. 2011 Jul 13;31(28):10141-8. PMID:21752990

Swiech L, Blazejczyk M, Urbanska M, Pietruszka P, Dortland BR, Malik AR, Wulf PS, Hoogenraad CC, Jaworski J. CLIP-170 and IQGAP1 cooperatively regulate dendrite morphology. J Neurosci. 2011 Mar 23;31(12):4555-68.PMID:21430156

Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, Umlauf M, Kapitein LC, Strikis D, Lemmon V, Bixby J, Hoogenraad CC, Bradke F. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science. 2011 Feb 18;331(6019):928-31. PMID: 21273450

2010

Stiess M, Maghelli N, Kapitein LC, Gomis-Rüth S, Wilsch-Bräuninger M, Hoogenraad CC, Tolić-Nørrelykke IM, Bradke F. Axon extension occurs independently of centrosomal microtubule nucleation. Science. 2010 Feb 5;327(5966):704-7. PMID: 20056854

Kapitein LC, Schlager MA, Kuijpers M, Wulf PS, van Spronsen M, MacKintosh FC, Hoogenraad CC. Mixed microtubules steer dynein-driven cargo transport into dendrites. Curr Biol. 2010 Feb 23;20(4):290-9. PMID: 20137950

Schlager MA, Kapitein LC, Grigoriev I, Burzynski GM, Wulf PS, Keijzer N, de Graaff E, Fukuda M, Shepherd IT, Akhmanova A, Hoogenraad CC. Pericentrosomal targeting of Rab6 secretory vesicles by Bicaudal-D-related protein 1 (BICDR-1) regulates neuritogenesis. EMBO J. 2010 May 19;29(10):1637-51. PMID: 20360680

Hoogenraad CC, Popa I, Futai K, Martinez-Sanchez E, Wulf PS, van Vlijmen T, Dortland BR, Oorschot V, Govers R, Monti M, Heck AJ, Sheng M, Klumperman J, Rehmann H, Jaarsma D, Kapitein LC, van der Sluijs P. Neuron specific Rab4 effector GRASP-1 coordinates membrane specialization and maturation of recycling endosomes. PLoS Biol. 2010 Jan 19;8(1):e1000283. PMID: 20098723

Kapitein LC, Schlager MA, van der Zwan WA, Wulf PS, Keijzer N, Hoogenraad CC. Probing intracellular motor protein activity using an inducible cargo trafficking assay. Biophys J. 2010 Oct 6;99(7):2143-52. PMID: 2092364

Montenegro Gouveia S, Leslie K, Kapitein LC, Buey RM, Grigoriev I, Wagenbach M, Smal I, Meijering E, Hoogenraad CC, Wordeman L, Steinmetz MO, Akhmanova A. In vitro reconstitution of the functional interplay between MCAK and EB3 at microtubule plus ends. Curr Biol. 2010 Oct 12;20(19):1717-22. PMID: 20850319

Bralten LB, Gravendeel AM, Kloosterhof NK, Sacchetti A, Vrijenhoek T, Veltman JA, van den Bent MJ, Kros JM, Hoogenraad CC, Sillevis Smitt PA, French PJ. The CASPR2 cell adhesion molecule functions as a tumor suppressor gene in glioma. Oncogene. 2010 Nov 18;29(46):6138-48. PMID: 20711234

Splinter D, Tanenbaum ME, Lindqvist A, Jaarsma D, Flotho A, Yu KL, Grigoriev I, Engelsma D, Haasdijk ED, Keijzer N, Demmers J, Fornerod M, Melchior F, Hoogenraad CC, Medema RH, Akhmanova A. Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol. 2010 Apr 6;8(4):e1000350. PMID: 20386726

Fasana E, Fossati M, Ruggiano A, Brambillasca S, Hoogenraad CC, Navone F, Francolini M, Borgese N. A VAPB mutant linked to amyotrophic lateral sclerosis generates a novel form of organized smooth endoplasmic reticulum. FASEB J. 2010 May;24(5):1419-30. PMID: 20008544

Bralten LB, Kloosterhof NK, Gravendeel LA, Sacchetti A, Duijm EJ, Kros JM, van den Bent MJ, Hoogenraad CC, Sillevis Smitt PA, French PJ. Integrated genomic profiling identifies candidate genes implicated in glioma-genesis and a novel LEO1-SLC12A1 fusion gene. Genes Chromosomes Cancer. 2010 Jun;49(6):509-17. PMID: 20196086

Gravendeel LA, Kloosterhof NK, Bralten LB, van Marion R, Dubbink HJ, Dinjens W, Bleeker FE, Hoogenraad CC, Michiels E, Kros JM, van den Bent M, Smitt PA, French PJ. Segregation of non-p.R132H mutations in IDH1 in distinct molecular subtypes of glioma. Hum Mutat. 2010 Mar;31(3):E1186-99. PMID: 20077503

2009

Jaworski J, Kapitein LC, Gouveia SM, Dortland BR, Wulf PS, Grigoriev I, Camera P, Spangler SA, Di Stefano P, Demmers J, Krugers H, Defilippi P, Akhmanova A, Hoogenraad CC. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron. 2009 Jan 15;61(1):85-100. PMID: 19146815

van Woerden GM, Hoebeek FE, Gao Z, Nagaraja RY, Hoogenraad CC, Kushner SA, Hansel C, De Zeeuw CI, Elgersma Y. betaCaMKII controls the direction of plasticity at parallel fiber-Purkinje cell synapses. Nat Neurosci. 2009 Jul;12(7):823-5. PMID: 19503086

Martin S, Henley JM, Holman D, Zhou M, Wiegert O, van Spronsen M, Joëls M, Hoogenraad CC, Krugers HJ. Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS One. 2009;4(3):e4714. PMID: 19305644

Komarova Y, De Groot CO, Grigoriev I, Gouveia SM, Munteanu EL, Schober JM, Honnappa S, Buey RM, Hoogenraad CC, Dogterom M, Borisy GG, Steinmetz MO, Akhmanova A. Mammalian end binding proteins control persistent microtubule growth. J Cell Biol. 2009 Mar 9;184(5):691-706. PMID: 19255245

2008

Jaarsma D, Teuling E, Haasdijk ED, De Zeeuw CI, Hoogenraad CC. Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J Neurosci. 2008 Feb 27;28(9):2075-88. PMID: 18305242

Kapitein LC, Janson ME, van den Wildenberg SM, Hoogenraad CC, Schmidt CF, Peterman EJ. Microtubule-driven multimerization recruits ase1p onto overlapping microtubules. Curr Biol. 2008 Nov 11;18(21):1713-7. PMID: 18976915

van Vlijmen T, Vleugel M, Evers M, Mohammed S, Wulf PS, Heck AJ, Hoogenraad CC, van der Sluijs P. A unique residue in rab3c determines the interaction with novel binding protein Zwint-1. FEBS Lett. 2008 Aug 20;582(19):2838-42. PMID: 18625232

Teuling E, van Dis V, Wulf PS, Haasdijk ED, Akhmanova A, Hoogenraad CC, Jaarsma D. A novel mouse model with impaired dynein/dynactin function develops amyotrophic lateral sclerosis (ALS)-like features in motor neurons and improves lifespan in SOD1-ALS mice. Hum Mol Genet. 2008 Sep 15;17(18):2849-62. PMID: 18579581

Grigoriev I, Gouveia SM, van der Vaart B, Demmers J, Smyth JT, Honnappa S, Splinter D, Steinmetz MO, Putney JW Jr, Hoogenraad CC, Akhmanova A. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr Biol. 2008 Feb 12;18(3):177-82. PMID: 18249114

2007

Teuling E, Ahmed S, Haasdijk E, Demmers J, Steinmetz MO, Akhmanova A, Jaarsma D, Hoogenraad CC. Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. J Neurosci. 2007 Sep 5;27(36):9801-15. PMID: 17804640

Wanschers BF, van de Vorstenbosch R, Schlager MA, Splinter D, Akhmanova A, Hoogenraad CC, Wieringa B, Fransen JA. A role for the Rab6B Bicaudal-D1 interaction in retrograde transport in neuronal cells. Exp Cell Res. 2007 Oct 1;313(16):3408-20. PMID: 17707369

Grigoriev I, Splinter D, Keijzer N, Wulf PS, Demmers J, Ohtsuka T, Modesti M, Maly IV, Grosveld F, Hoogenraad CC, Akhmanova A. Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell. 2007 Aug;13(2):305-14. PMID: 17681140

Hoogenraad CC, Feliu-Mojer MI, Spangler SA, Milstein AD, Dunah AW, Hung AY, Sheng M. Liprinalpha1 degradation by calcium/calmodulin-dependent protein kinase II regulates LAR receptor tyrosine phosphatase distribution and dendrite development. Dev Cell. 2007 Apr;12(4):587-602. PMID: 17419996

Erez H, Malkinson G, Prager-Khoutorsky M, De Zeeuw CI, Hoogenraad CC, Spira ME. Formation of microtubule-based traps controls the sorting and concentration of vesicles to restricted sites of regenerating neurons after axotomy. J Cell Biol. 2007 Feb 12;176(4):497-507. PMID: 17283182

Scheper W, Hoozemans JJ, Hoogenraad CC, Rozemuller AJ, Eikelenboom P, Baas F.
Rab6 is increased in Alzheimer's disease brain and correlates with endoplasmic reticulum stress. Neuropathol Appl Neurobiol. 2007 Oct;33(5):523-32. PMID: 17573808

van Hagen JM, van der Geest JN, van der Giessen RS, Lagers-van Haselen GC, Eussen HJ, Gille JJ, Govaerts LC, Wouters CH, de Coo IF, Hoogenraad CC, Koekkoek SK, Frens MA, van Camp N, van der Linden A, Jansweijer MC, Thorgeirsson SS, De Zeeuw CI. Contribution of CYLN2 and GTF2IRD1 to neurological and cognitive symptoms in Williams Syndrome. Neurobiol Dis. 2007 Apr;26(1):112-24. PMID: 17270452

2006

Fumoto K, Hoogenraad CC, Kikuchi A. GSK-3beta-regulated interaction of BICD with dynein is involved in microtubule anchorage at centrosome. EMBO J. 2006 Dec 13;25(24):5670-82. PMID: 17139249

Cheng D, Hoogenraad CC, Rush J, Ramm E, Schlager MA, Duong DM, Xu P, Wijayawardana SR, Hanfelt J, Nakagawa T, Sheng M, Peng J. Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol Cell Proteomics. 2006 Jun;5(6):1158-70. PMID: 16507876

Nakagawa T, Feliu-Mojer MI, Wulf P, Lois C, Sheng M, Hoogenraad CC. Generation of lentiviral transgenic rats expressing glutamate receptor interacting protein 1 (GRIP1) in brain, spinal cord and testis. J Neurosci Methods. 2006 Apr 15;152(1-2):1-9. PMID: 16157387

2005

Hoogenraad CC, Milstein AD, Ethell IM, Henkemeyer M, Sheng M. GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat Neurosci. 2005 Jul;8(7):906-15. PMID: 15965473

Jaworski J, Spangler S, Seeburg DP, Hoogenraad CC, Sheng M. Control of dendritic arborization by the phosphoinositide-3'-kinase-Akt-mammalian target of rapamycin pathway. J Neurosci. 2005 Dec 7;25(49):11300-12. PMID: 16339025

Dunah AW, Hueske E, Wyszynski M, Hoogenraad CC, Jaworski J, Pak DT, Simonetta A, Liu G, Sheng M. LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci. 2005 Apr;8(4):458-67. PMID: 15750591

Akhmanova A, Mausset-Bonnefont AL, van Cappellen W, Keijzer N, Hoogenraad CC, Stepanova T, Drabek K, van der Wees J, Mommaas M, Onderwater J, van der Meulen H, Tanenbaum ME, Medema RH, Hoogerbrugge J, Vreeburg J, Uringa EJ, Grootegoed JA, Grosveld F, Galjart N. The microtubule plus-end-tracking protein CLIP-170 associates with the spermatid manchette and is essential for spermatogenesis. Genes Dev. 2005 Oct 15;19(20):2501-15. PMID: 16230537

Vlug AS, Teuling E, Haasdijk ED, French P, Hoogenraad CC, Jaarsma D. ATF3 expression precedes death of spinal motoneurons in amyotrophic lateral sclerosis-SOD1 transgenic mice and correlates with c-Jun phosphorylation, CHOP expression, somato-dendritic ubiquitination and Golgi fragmentation. Eur J Neurosci. 2005 Oct;22(8):1881-94. PMID: 16262628


2004

Lansbergen G, Komarova Y, Modesti M, Wyman C, Hoogenraad CC, Goodson HV, Lemaitre RP, Drechsel DN, van Munster E, Gadella TW Jr, Grosveld F, Galjart N, Borisy GG, Akhmanova A. Conformational changes in CLIP-170 regulate its binding to microtubules and dynactin localization. J Cell Biol. 2004 Sep 27;166(7):1003-14. Epub 2004 Sep 20. PMID: 15381688

2003

Hoogenraad CC, Wulf P, Schiefermeier N, Stepanova T, Galjart N, Small JV, Grosveld F, de Zeeuw CI, Akhmanova A. Bicaudal D induces selective dynein-mediated microtubule minus end-directed transport. EMBO J. 2003 Nov 17;22(22):6004-15. PMID: 14609947

Stepanova T, Slemmer J, Hoogenraad CC, Lansbergen G, Dortland B, De Zeeuw CI, Grosveld F, van Cappellen G, Akhmanova A, Galjart N. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J Neurosci. 2003 Apr 1;23(7):2655-64. PMID: 12684451

De Zeeuw CI, Chorev E, Devor A, Manor Y, Van Der Giessen RS, De Jeu MT, Hoogenraad CC, Bijman J, Ruigrok TJ, French P, Jaarsma D, Kistler WM, Meier C, Petrasch-Parwez E, Dermietzel R, Sohl G, Gueldenagel M, Willecke K, Yarom Y. Deformation of network connectivity in the inferior olive of connexin 36-deficient mice is compensated by morphological and electrophysiological changes at the single neuron level. J Neurosci. 2003 Jun 1;23(11):4700-11. PMID: 12805309

2002

Matanis T, Akhmanova A, Wulf P, Del Nery E, Weide T, Stepanova T, Galjart N, Grosveld F, Goud B, De Zeeuw CI, Barnekow A, Hoogenraad CC. Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat Cell Biol. 2002 Dec;4(12):986-92. PMID: 12447383

Hoogenraad CC, Koekkoek B, Akhmanova A, Krugers H, Dortland B, Miedema M, van Alphen A, Kistler WM, Jaegle M, Koutsourakis M, Van Camp N, Verhoye M, van der Linden A, Kaverina I, Grosveld F, De Zeeuw CI, Galjart N. Targeted mutation of Cyln2 in the Williams syndrome critical region links CLIP-115 haploinsufficiency to neurodevelopmental abnormalities in mice. Nat Genet. 2002 Sep;32(1):116-27. PMID: 12195424

Kistler WM, De Jeu MT, Elgersma Y, Van Der Giessen RS, Hensbroek R, Luo C, Koekkoek SK, Hoogenraad CC, Hamers FP, Gueldenagel M, Sohl G, Willecke K, De Zeeuw CI. Analysis of Cx36 knockout does not support tenet that olivary gap junctions are required for complex spike synchronization and normal motor performance. Ann N Y Acad Sci. 2002 Dec;978:391-404. PMID: 12582068

Coquelle FM, Caspi M, Cordelières FP, Dompierre JP, Dujardin DL, Koifman C, Martin P, Hoogenraad CC, Akhmanova A, Galjart N, De Mey JR, Reiner O. LIS1, CLIP-170's key to the dynein/dynactin pathway. Mol Cell Biol. 2002 May;22(9):3089-102. PMID: 11940666

2001

Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, Verkerk T, Vermeulen W, Burgering BM, De Zeeuw CI, Grosveld F, Galjart N. Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell. 2001 Mar 23;104(6):923-35. PMID: 11290329

Sun JC, Van Alphen AM, Wagenaar M, Huygen P, Hoogenraad CC, Hasson T, Koekkoek SK, Bohne BA, De Zeeuw CI. Hereditary familial vestibular degenerative diseases. Ann N Y Acad Sci. 2001 Oct;942:493-6. PMID: 11710498

Hoogenraad CC, Akhmanova A, Howell SA, Dortland BR, De Zeeuw CI, Willemsen R, Visser P, Grosveld F, Galjart N. Mammalian Golgi-associated Bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J. 2001 Aug 1;20(15):4041-54. PMID: 11483508

Sun JC, van Alphen AM, Wagenaar M, Huygen P, Hoogenraad CC, Hasson T, Koekkoek SK, Bohne BA, De Zeeuw CI. Origin of vestibular dysfunction in Usher syndrome type 1B. Neurobiol Dis. 2001 Feb;8(1):69-77. PMID: 11162241

2000

Hoogenraad CC, Akhmanova A, Grosveld F, De Zeeuw CI, Galjart N. Functional analysis of CLIP-115 and its binding to microtubules. J Cell Sci. 2000 Jun;113 ( Pt 12):2285-97. PMID: 10825300

 

 Review

2013

Lipka J, Kuijpers M, Jaworski J, and Hoogenraad CC. Mutations in cytoplasmic dynein and its regulators cause malformations of cortical development and neurodegenerative diseases. Biochem Soc Trans. 2013 Dec 1, 41(6): 1605-12. PMID: 24256262.

van Coevorden-Hameete MH, de Graaff E, Titulaer MJ, Hoogenraad CC, and Sillevis Smitt PA. Molecular and cellular mechanisms underlying anti-neuronal antibody mediated disorders of the central nervous system. Autoimmun Rev. 2013 Nov 10 PMID: 24225076.

Timmermans W, Xiong H, Hoogenraad CC, and Krugers HJ. Stress and excitatory synapses: from health to disease. Neuroscience. 2013 Sep 17, 248: 626-36. PMID: 23727506.

Harterink M and Hoogenraad CC. Slide to the left and slide to the right: motor coordination in neurons. Dev Cell. 2013 Aug 26, 26(4): 326-8. PMID: 23987508. 

Gumy LF, Katrukha EA, Kapitein LC, and Hoogenraad CC. New insights into mRNA trafficking in axons. Dev Neurobiol. 2013 Aug 19 PMID: 23959656.

Franker MA and Hoogenraad CC. Microtubule-based transport - basic mechanisms, traffic rules and role in neurological pathogenesis. J Cell Sci. 2013 Jun 1, 126(Pt 11): 2319-29. PMID: 23729742.

Gumy LF and Hoogenraad CC. Off the rails: axonal cargoes on the road to nowhere. EMBO J. 2013 May 15, 32(10): 1345-7. PMID: 23612610.

2012

van den Berg R and Hoogenraad CC. Molecular motors in cargo trafficking and synapse assembly. Adv Exp Med Biol. 2012, 970: 173-96. PMID: 22351056.

2011

van der Sluijs P, Hoogenraad CC. New insights in endosomal dynamics and AMPA receptor trafficking. Semin Cell Dev Biol. 2011 Jul;22(5):499-505. PMID: 21843653

Kuijpers M, Hoogenraad CC. Centrosomes, microtubules and neuronal development. Mol Cell Neurosci. 2011 May 23. PMID:21722732

Kapitein LC, Hoogenraad CC. Which way to go? Cytoskeletal organization and polarized transport in neurons. Mol Cell Neurosci. 2011 Jan;46(1):9-20. PMID: 20817096

2010

Krugers HJ, Hoogenraad CC, Groc L. Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nat Rev Neurosci. 2010 Oct;11(10):675-81. PMID: 20820185

Hoogenraad CC, Akhmanova A. Dendritic spine plasticity: new regulatory roles of dynamic microtubules. Neuroscientist. 2010 Dec;16(6):650-61. PMID: 21239729

Hoogenraad CC, van der Sluijs P. GRASP-1 regulates endocytic receptor recycling and synaptic plasticity. Commun Integr Biol. 2010 Sep;3(5):433-5. PMID: 2105763

Hotulainen P, Hoogenraad CC. Actin in dendritic spines: connecting dynamics to function. J Cell Biol. 2010 May 17;189(4):619-29. PMID: 20457765

van Spronsen M, Hoogenraad CC. Synapse pathology in psychiatric and neurologic disease. Curr Neurol Neurosci Rep. 2010 May;10(3):207-14. PMID: 20425036

2009

Hoogenraad CC, Bradke F. Control of neuronal polarity and plasticity--a renaissance for microtubules? Trends Cell Biol. 2009 Dec;19(12):669-76. PMID: 19801190

Schlager MA, Hoogenraad CC. Basic mechanisms for recognition and transport of synaptic cargos. Mol Brain. 2009 Aug 4;2:25. PMID: 19653898

2008

Jaworski J, Hoogenraad CC, Akhmanova A. Microtubule plus-end tracking proteins in differentiated mammalian cells. Int J Biochem Cell Biol. 2008;40(4):619-37. PMID: 18023603

2007

Sheng M, Hoogenraad CC. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem. 2007;76:823-47. PMID: 1724389

Spangler SA, Hoogenraad CC. Liprin-alpha proteins: scaffold molecules for synapse maturation. Biochem Soc Trans. 2007 Nov;35(Pt 5):1278-82. PMID: 17956329

2005

Akhmanova A, Hoogenraad CC. Microtubule plus-end-tracking proteins: mechanisms and functions. Curr Opin Cell Biol. 2005 Feb;17(1):47-54. PMID: 15661518

2004

Hoogenraad CC, Akhmanova A, Galjart N, De Zeeuw CI. LIMK1 and CLIP-115: linking cytoskeletal defects to Williams syndrome. Bioessays. 2004 Feb;26(2):141-50. PMID: 14745832

2003

Hoogenraad CC, Sheng M. The return of the exocyst. Nat Cell Biol. 2003 Jun;5(6):493-5. PMID: 12776120

 

 Book chapter

2011

Yu KL, Keijzer N, Hoogenraad CC, Akhmanova A. Isolation of Novel +TIPs and Their Binding Partners Using Affinity Purification Techniques. Methods Mol Biol. 2011;777:293-316. PMID:21773937

Nakagawa T, Hoogenraad CC. Lentiviral transgenesis. Methods Mol Biol. 2011;693:117-42. PMID: 21080278

2010

Kapitein LC, Yau KW, Hoogenraad CC. Microtubule dynamics in dendritic spines. Methods Cell Biol. 2010;97:111-32. PMID: 20719268