Neuronal expression of muskelin in the rodent central nervous system
- Nadia Tagnaouti†1,
- Sven Loebrich†1,
- Frank Heisler†1,
- Yvonne Pechmann1,
- Susanne Fehr1,
- Adèle De Arcangelis2,
- Elisabeth Georges-Labouesse2,
- Josephine C Adams3 and
- Matthias Kneussel1Email author
© Tagnaouti et al; licensee BioMed Central Ltd. 2007
Received: 05 January 2007
Accepted: 02 May 2007
Published: 02 May 2007
The kelch repeat protein muskelin mediates cytoskeletal responses to the extracellular matrix protein thrombospondin 1, (TSP1), that is known to promote synaptogenesis in the central nervous system (CNS). Muskelin displays intracellular localization and affects cytoskeletal organization in adherent cells. Muskelin is expressed in adult brain and has been reported to bind the Cdk5 activator p39, which also facilitates the formation of functional synapses. Since little is known about muskelin in neuronal tissues, we here analysed the tissue distribution of muskelin in rodent brain and analysed its subcellular localization using cultured neurons from multiple life stages.
Our data show that muskelin transcripts and polypeptides are expressed throughout the central nervous system with significantly high levels in hippocampus and cerebellum, a finding that resembles the tissue distribution of p39. At the subcellular level, muskelin is found in the soma, in neurite projections and the nucleus with a punctate distribution in both axons and dendrites. Immunostaining and synaptosome preparations identify partial localization of muskelin at synaptic sites. Differential centrifugation further reveals muskelin in membrane-enriched, rather than cytosolic fractions.
Our results suggest that muskelin represents a multifunctional protein associated with membranes and/or large protein complexes in most neurons of the central nervous system. These data are in conclusion with distinct roles of muskelin's functional interaction partners.
Muskelin was originally identified as a molecule required in cellular responses to the extracellular matrix (ECM) component thrombospondin-1 (TSP-1) . Muskelin overexpression promotes cell attachment to the C-terminus of TSP-1 and antisense depletion of muskelin expression leads to reduced cell attachment, cell spreading and cytoskeletal reorganization . TSP-1 is a member of the thrombospondin (TSP) family of widely-expressed, multifunctional ECM proteins [2, 3]. TSPs secreted by immature astrocytes during embryonic development promote central nervous system (CNS) synaptogenesis . Muskelin transcripts are expressed in different tissues of developing mouse embryos  and Northern blot analysis as well as RT-PCR detected muskelin transcripts in many adult tissues including brain [1, 6], however whether the synaptogenic effect of TSPs involves muskelin function is currently unclear.
A reported direct binding partner of muskelin is the cyclin-dependent kinase 5 (Cdk5) activator, p39, that is abundant in the CNS , displays highest expression in cerebellum and hippocampus, and partially localizes to synaptophysin-positive synapses . In COS cells and lens epithelial cells, coexpression of p39 and muskelin recruits intracellular muskelin toward the cell periphery , however whether muskelin also localizes at synaptic sites in neurons is presently unknown. Notably, overexpression of Cdk5 and p39 resulted in significantly higher rates of synapse formation in a neuroblastoma cell/myotube co-culture system , and both the knockout of Cdk5  as well as the double-knockout of p39 and its homologue p35 in mice  lead to widespread disruption of neuronal migration and brain development. Together, these data indicate a critical role for both TSPs and Cdk5/p39 signalling pathways in synapse formation and suggest the hypothesis that muskelin, reported to interact functionally with both systems, might also play a role in synaptogenic mechanisms.
Our study provides the first comprehensive spatio-temporal analysis of muskelin expression in neuronal tissues and at the subcellular level in neurons.
Distribution of muskelin transcripts in the rodent central nervous system
We then performed in situ hybridization around birth using P0 tissue. Here, the analyses revealed that muskelin mRNA transcripts were present in all brain regions, however transcript levels were above average in the hippocampal formation and cerebellum of newborn animals (arrows). Hybridization signals were clearly detectable in the spinal cord at this stage (Figure 2A). Thus, our data indicate that muskelin transcripts are abundant in the second half of mouse embryonic development with a widespread distribution throughout the CNS.
Muskelin has been identified to mediate intracellular responses to thrombospondin-1, however thrombospondins-1 and -2, both identified as synaptogenic proteins, are expressed in the embryonic  and postnatal brain but become downregulated in the adult CNS . In contrast, thrombospondin-4 (TSP-4) is highly expressed in the adult CNS . We therefore also analyzed muskelin transcripts at adult stages and performed in situ hybridization on tissue derived from P42 mice. Muskelin transcripts were prominent throughout the brain and notably displayed significantly strong signals in the adult hippocampal formation and the adult cerebellum (Figure 2B). These data suggest that muskelin might play additional, as yet unidentified, roles in neurons together with other thrombospondins or unrelated proteins.
Distribution of muskelin protein in the adult brain
Subcellular localization of muskelin in cultured hippocampal neurons
Subcellular distribution of muskelin upon differential centrifugation of whole brain extracts
We have analysed the expression of muskelin in brain. Our main findings are: i), muskelin is expressed throughout the central nervous system with highest expression in the adult hippocampus and cerebellum; ii), muskelin localizes to the neuronal nucleus as well as to axonal and dendritic projections, including synaptic sites; iii), muskelin cofractionates with both membrane-enriched fractions and fractions containing protein complexes.
Muskelin was identified as a molecule required in cellular responses to TSP-1. Consistently, during mouse embryonic development, muskelin expression overlaps with the expression pattern of TSP-1 in brain . However, transcripts of TSP-1 and of other TSP family members are strongly downregulated during the late phases of development and early adulthood [28–31], whereas widespread muskelin expression persists. In contrast, TSP-2 was found to be expressed in adult cerebellar Purkinje cells  and TSP-4 was detected in both the adult hippocampus and cerebellum . These observations suggest that, besides a functional interaction of muskelin with TSP-1, muskelin might mediate other roles in neurons, independent of TSP-1 or other TSPs. For instance, the reported muskelin binding partner p39 in combination with its molecular target Cdk5, are candidate proteins that potentially impact on synaptogenesis by promoting rates of synapse formation [8–10].
In accordance with a possible role at neuronal membrane specializations,  our muskelin-specific antibody detected muskelin in a punctate distribution in cell somata, axons and dendrites, many of which were close to the plasma membrane. Confirming this observation, differential centrifugation revealed the presence of muskelin in membrane fractions. Counterstaining with a synapse marker and analysis of synaptosomes showed that a fraction of muskelin associates with synaptic contacts, suggesting that muskelin might participate in synaptogenic actions  and/or the p39/Cdk5 system [6, 8, 11].
Besides a widespread distribution of muskelin puncta in cell somata, axons and dendrites, the protein displayed prominent localization to neuronal nuclei. Interaction of muskelin with RanBPM , a polypeptide that locates to both the nucleus and the cytoplasm [19–21] is in agreement with this observation. Whether muskelin, which is present in both the cytoplasmic and nuclear compartments, is subject of nucleocytoplasmic transport is currently unknown. However, a role for muskelin in transport reactions is not unlikely, as the protein contains the LisH and CTLH domains, that in certain other proteins are known to interact with molecular motors of the dynein family , a microtubule-dependent recruitment system.
In summary, our study provides the first comprehensive spatio-temporal analysis of muskelin expression in neuronal tissue and at the subcellular level in neurons. It reports a newly generated muskelin-specific antibody suitable for immunostaining and western blotting and indicates highest muskelin expression levels in hippocampus and cerebellum. At the subcellular level, muskelin is identified in a punctate distribution throughout the neuron, including synaptic sites, and also displays nuclear localization. Upon cell fractionation, muskelin is further enriched in fractions containing membranes and large protein complexes. The presented data generate an important point of departure to initiate functional studies in neurons in order to understand the role of a protein that appears to be at a critical interface between binding partners that are functionally involved in synaptogenesis, transport and nuclear processes.
Radioactively labeled RNA probes were prepared using the MAXIscript in vitro transcription kit (Ambion, Austin, TX) in the presence of α35S-UTP and α35S-CTP. Probes were purified with ProbeQuant sephadex G-50 microcolumns (Amersham, Buckinghamshire, England). In situ hybridization was performed as previously described [34–36], using five independent muskelin sequences: probe 1 (1–438 bp), probe 2 (450–885 bp), probe 3 (1151–1576 bp), probe 4 (1601–2024 bp) and probe 5 (1–1960 bp). 4 independent experiments with two sets of animals for each timepoint were used for each probe 1–4 (Figure 1B). 3 independent experiments with three sets of animals for each time point were used for probe 5 (Figure 1C).
The N-terminal 280 amino acids of rat muskelin were cloned as an EcoRI/SalI fragment into pGEX-5X1 (Amersham, Buckinghamshire, England) (GST-Muskelin 1–280) and expressed in E. coli BL21. The fusion protein was bound to glutathione-agarose (Amersham, Buckinghamshire, England) and eluted overnight in the cold with 25 mM reduced glutathione (Sigma, Taufkirchen, Germany). The eluate was injected into a guinea pig with boosts every 30 days. The final bleed was taken after the third boost and the whole serum was used for Western blotting. For immunohistochemistry and immunocytochemistry, the immunoglobulins were affinity purified, using the immunogenic GST-fusion immobilized on a Hybond P membrane (Amersham, Buckinghamshire, England). Immunoglobulins were eluted with 250 mM glycine, pH 2.0 for 1 min, buffered with Tris-HCl, pH 8.0, aliquoted and frozen in liquid nitrogen. Preimmune serum was processed under identical conditions. For western blot controls, anti-myc (Sigma) was used at a dilution of 1:4000.
Mice from postnatal stages were perfused with 4% paraformaldehyde through the heart and sagittal vibratome sections were cut from the fixed brain. Sections were permeabilized with 0.4% Triton X-100 (Merck, Darmstadt, Germany) for 10 minutes and blocked with PBS, containing 10% normal goat serum and 1% BSA, for 1 hour at room temperature. Cultured hippocampal neurons were prepared as previously described . Primary antibodies were applied in PBS containing 3% normal goat serum and 1% BSA overnight in the cold, as previously described . The following primary antibodies were used: anti-MAP2 (1:1000; Chemicon, Hampshire, UK); anti-NF-200 (1:300; Sigma); anti-tau (1:5000, DAKO, Glostrup, Denmark); anti-SV2 (1:100; University of Iowa). Application of secondary antibodies and DAB development was carried out according to standard techniques. All secondary antibodies were from Dianova (Hamburg, Germany). For preabsorption controls, muskelin antibodies were incubated with GST-Muskelin 1–280. Antibody-antigen complexes were removed via pulldown with sepharose beads. Supernatant was adjusted to pH 8.0 with Tris-HCl and used for immunochemistry, as described. Fluorescence imaging was carried out with an inverted Leica TCS-SP2 laser scanning confocal microscope (Leica). For simultaneous multichannel fluorescence, images were taken in a sequential channel recording mode.
Neuronal extracts and differential centrifugation
Buffers were supplemented with Complete Mini Protease inhibitor cocktail (Roche, Mannheim, Germany) with or without 1 mM PMSF. Differential centrifugation was performed as previously described . In brief, P10 rats were decapitated and the brains put into buffer 1 (320 mM sucrose, 10 mM HEPES/KOH, pH 7,9, 1 mM DTT, 1 mM EGTA, 1 mM EDTA) and pottered using a glass-teflon-douncer. Extracts were centrifuged at 1000 × g, P1, and the supernatant, S1, further centrifuged at 10,000 × g, P2. The remaining supernatant, S2, was centrifuged at 100,000 × g, P3, with the supernatant referred to as S3. Supernatant S3 was again centrifuged at 400,000 × g, P4, with the final supernatant referred to as S4. Protein content was determined using a BCA protein assay kit (Pierce, Bonn, Germany). For SDS-PAGE, 30 μg of proteins were loaded in each lane. For Western blotting, the antiserum to muskelin was diluted 1:3000 and incubated over night in 5% milk in TBST (10 mM Tris, pH 8.0, 150 mM NaCl, 0.05% Triton-X-100). The preimmuneserum was applied under identical conditions. For controls, anti-actin (Sigma) was used at a dilution of 1:2000 and anti-PSD-95 (BD Biosciences, San Jose, CA) was used at a dilution of 1:250. For neuronal extracts, cultured neurons were prepared as previously described [37, 38]. Cells were harvested in lysis buffer (PBS, 1% Triton-X-100) supplemented with Complete Mini Protease inhibitor cocktail (Roche, Mannheim, Germany) for 30 min on ice. Lysates were centrifuged at 1,000 × g for 5 min at 4°C. Protein concentration was determined using a BCA assay kit (Pierce, Bonn, Germany). Subsequently, protein samples were subjected to SDS PAGE and Western blotting.
Preparation of synaptosomes
Buffers were supplemented with Complete Mini Protease inhibitor cocktail (Roche, Mannheim, Germany) and 1 mM PMSF. Brains of P10 rats were homogenized in sucrose buffer (320 mM sucrose, 1 M NaHCO3, 1 M MgCl2, 500 mM CaCl2, 500 mM EDTA, pH8.0) at 4°C and centrifuged at 1400 × g for 10 min. Pellets were resolved in the same ice cold buffer, homogenized and centrifuged at 700 × g for 10 min at 4°C. Subsequently, supernatants were centrifuged at 13,800 × g for 10 min at 4°C. At this step, pellets were resolved in 2 ml sucrose solution (320 mM sucrose, 1 M NaHCO3) and separated on a discontinous 1.2 M-0.85 M sucrose gradient for 2 h at 82,500 × g at 4°C. Synaptosomal fractions were recovered from the gradient at molarity 1–1.2. For Western blotting, the following antibodies were used: anti-muskelin (1:3000); anti-PSD-95 (1:250; Invitrogen/Zymed Laboratories); anti-gephyrin (BD Biosciences, 1:250).
- The abbreviations used are:
CNS, central nervous system
cyclin-dependent kinase 5
lissencephaly-1 homology, CTLH, C-terminal to LisH
green fluorescent protein
postsynaptic density protein of 95 kDa
synaptic vesicle protein 2.
This work was supported by the University of Hamburg and grants from the Deutsche Forschungsgemeinschaft (KN-556/1-3) to MK; Wellcome Trust SFBBR 038284 and funds from the Cleveland Clinic Foundation to JCA, and funds from the Association pour la Recherche sur le Cancer to EGL. We thank S. Plant for excellent technical assistance.
- Adams JC, Seed B, Lawler J: Muskelin, a novel intracellular mediator of cell adhesive and cytoskeletal responses to thrombospondin-1. Embo J. 1998, 17 (17): 4964-4974. 10.1093/emboj/17.17.4964.PubMedPubMed CentralView ArticleGoogle Scholar
- Adams JC: Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol. 2001, 17: 25-51. 10.1146/annurev.cellbio.17.1.25.PubMedView ArticleGoogle Scholar
- Lawler J: The functions of thrombospondin-1 and-2. Curr Opin Cell Biol. 2000, 12 (5): 634-640. 10.1016/S0955-0674(00)00143-5.PubMedView ArticleGoogle Scholar
- Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA: Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell. 2005, 120 (3): 421-433. 10.1016/j.cell.2004.12.020.PubMedView ArticleGoogle Scholar
- Prag S, De Arcangelis A, Georges-Labouesse E, Adams JC: Regulation of post-translational modifications of muskelin by protein kinase C. Int J Biochem Cell Biol. 2006Google Scholar
- Ledee DR, Gao CY, Seth R, Fariss RN, Tripathi BK, Zelenka PS: A specific interaction between muskelin and the cyclin-dependent kinase 5 activator p39 promotes peripheral localization of muskelin. J Biol Chem. 2005, 280 (22): 21376-21383. 10.1074/jbc.M501215200.PubMedView ArticleGoogle Scholar
- Nilden F, Backstrom A, Bark C: Molecular cloning and characterisation of a mouse gene encoding an isoform of the neuronal cyclin-dependent kinase 5 (CDK5) activator. Biochim Biophys Acta. 1998, 1398 (3): 371-376.PubMedView ArticleGoogle Scholar
- Johansson JU, Lilja L, Chen XL, Higashida H, Meister B, Noda M, Zhong ZG, Yokoyama S, Berggren PO, Bark C: Cyclin-dependent kinase 5 activators p35 and p39 facilitate formation of functional synapses. Brain Res Mol Brain Res. 2005, 138 (2): 215-227. 10.1016/j.molbrainres.2005.04.014.PubMedView ArticleGoogle Scholar
- Ohshima T, Ward JM, Huh CG, Longenecker G, Veeranna, Pant HC, Brady RO, Martin LJ, Kulkarni AB: Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc Natl Acad Sci U S A. 1996, 93 (20): 11173-11178. 10.1073/pnas.93.20.11173.PubMedPubMed CentralView ArticleGoogle Scholar
- Ko J, Humbert S, Bronson RT, Takahashi S, Kulkarni AB, Li E, Tsai LH: p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J Neurosci. 2001, 21 (17): 6758-6771.PubMedGoogle Scholar
- Hasegawa H, Katoh H, Fujita H, Mori K, Negishi M: Receptor isoform-specific interaction of prostaglandin EP3 receptor with muskelin. Biochem Biophys Res Commun. 2000, 276 (1): 350-354. 10.1006/bbrc.2000.3467.PubMedView ArticleGoogle Scholar
- Umeda M, Nishitani H, Nishimoto T: A novel nuclear protein, Twa1, and Muskelin comprise a complex with RanBPM. Gene. 2003, 303: 47-54. 10.1016/S0378-1119(02)01153-8.PubMedView ArticleGoogle Scholar
- Prag S, Collett GD, Adams JC: Molecular analysis of muskelin identifies a conserved discoidin-like domain that contributes to protein self-association. Biochem J. 2004, 381 (Pt 2): 547-559.PubMedPubMed CentralView ArticleGoogle Scholar
- Adams J, Kelso R, Cooley L: The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol. 2000, 10 (1): 17-24. 10.1016/S0962-8924(99)01673-6.PubMedView ArticleGoogle Scholar
- Tooney PA, Sakai T, Sakai K, Aeschlimann D, Mosher DF: Restricted localization of thrombospondin-2 protein during mouse embryogenesis: a comparison to thrombospondin-1. Matrix Biol. 1998, 17 (2): 131-143. 10.1016/S0945-053X(98)90026-9.PubMedView ArticleGoogle Scholar
- Arber S, Caroni P: Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J Cell Biol. 1995, 131 (4): 1083-1094. 10.1083/jcb.131.4.1083.PubMedView ArticleGoogle Scholar
- Dotti CG, Sullivan CA, Banker GA: The establishment of polarity by hippocampal neurons in culture. J Neurosci. 1988, 8 (4): 1454-1468.PubMedGoogle Scholar
- Tsuda M, Tashiro T, Komiya Y: Increased solubility of high-molecular-mass neurofilament subunit by suppression of dephosphorylation: its relation to axonal transport. J Neurochem. 1997, 68 (6): 2558-2565.PubMedView ArticleGoogle Scholar
- Mikolajczyk M, Shi J, Vaillancourt RR, Sachs NA, Nelson M: The cyclin-dependent kinase 11(p46) isoform interacts with RanBPM. Biochem Biophys Res Commun. 2003, 310 (1): 14-18. 10.1016/j.bbrc.2003.08.116.PubMedView ArticleGoogle Scholar
- Kramer S, Ozaki T, Miyazaki K, Kato C, Hanamoto T, Nakagawara A: Protein stability and function of p73 are modulated by a physical interaction with RanBPM in mammalian cultured cells. Oncogene. 2005, 24 (5): 938-944. 10.1038/sj.onc.1208257.PubMedView ArticleGoogle Scholar
- Denti S, Sirri A, Cheli A, Rogge L, Innamorati G, Putignano S, Fabbri M, Pardi R, Bianchi E: RanBPM is a phosphoprotein that associates with the plasma membrane and interacts with the integrin LFA-1. J Biol Chem. 2004, 279 (13): 13027-13034. 10.1074/jbc.M313515200.PubMedView ArticleGoogle Scholar
- Feany MB, Lee S, Edwards RH, Buckley KM: The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell. 1992, 70 (5): 861-867. 10.1016/0092-8674(92)90319-8.PubMedView ArticleGoogle Scholar
- Dabrowski M, Aerts S, Van Hummelen P, Craessaerts K, De Moor B, Annaert W, Moreau Y, De Strooper B: Gene profiling of hippocampal neuronal culture. J Neurochem. 2003, 85 (5): 1279-1288. 10.1046/j.1471-4159.2003.01753.x.PubMedView ArticleGoogle Scholar
- Lee SH, Valtschanoff JG, Kharazia VN, Weinberg R, Sheng M: Biochemical and morphological characterization of an intracellular membrane compartment containing AMPA receptors. Neuropharmacology. 2001, 41 (6): 680-692. 10.1016/S0028-3908(01)00124-1.PubMedView ArticleGoogle Scholar
- Saito N, Okada Y, Noda Y, Kinoshita Y, Kondo S, Hirokawa N: KIFC2 is a novel neuron-specific C-terminal type kinesin superfamily motor for dendritic transport of multivesicular body-like organelles. Neuron. 1997, 18 (3): 425-438. 10.1016/S0896-6273(00)81243-X.PubMedView ArticleGoogle Scholar
- Kennedy MB: The postsynaptic density at glutamatergic synapses. Trends Neurosci. 1997, 20 (6): 264-268. 10.1016/S0166-2236(96)01033-8.PubMedView ArticleGoogle Scholar
- Mok H, Shin H, Kim S, Lee JR, Yoon J, Kim E: Association of the kinesin superfamily motor protein KIF1Balpha with postsynaptic density-95 (PSD-95), synapse-associated protein-97, and synaptic scaffolding molecule PSD-95/discs large/zona occludens-1 proteins. J Neurosci. 2002, 22 (13): 5253-5258.PubMedGoogle Scholar
- O'Shea KS, Dixit VM: Unique distribution of the extracellular matrix component thrombospondin in the developing mouse embryo. J Cell Biol. 1988, 107 (6 Pt 2): 2737-2748. 10.1083/jcb.107.6.2737.PubMedView ArticleGoogle Scholar
- O'Shea KS, Rheinheimer JS, Dixit VM: Deposition and role of thrombospondin in the histogenesis of the cerebellar cortex. J Cell Biol. 1990, 110 (4): 1275-1283. 10.1083/jcb.110.4.1275.PubMedView ArticleGoogle Scholar
- Lawler J, Duquette M, Whittaker CA, Adams JC, McHenry K, DeSimone DW: Identification and characterization of thrombospondin-4, a new member of the thrombospondin gene family. J Cell Biol. 1993, 120 (4): 1059-1067. 10.1083/jcb.120.4.1059.PubMedView ArticleGoogle Scholar
- Qabar AN, Lin Z, Wolf FW, O'Shea KS, Lawler J, Dixit VM: Thrombospondin 3 is a developmentally regulated heparin binding protein. J Biol Chem. 1994, 269 (2): 1262-1269.PubMedGoogle Scholar
- Kyriakides TR, Zhu YH, Yang Z, Bornstein P: The distribution of the matricellular protein thrombospondin 2 in tissues of embryonic and adult mice. J Histochem Cytochem. 1998, 46 (9): 1007-1015.PubMedView ArticleGoogle Scholar
- Gerlitz G, Darhin E, Giorgio G, Franco B, Reiner O: Novel functional features of the Lis-H domain: role in protein dimerization, half-life and cellular localization. Cell Cycle. 2005, 4 (11): 1632-1640.PubMedView ArticleGoogle Scholar
- Fehr S, Ivell R, Koll R, Schams D, Fields M, Richter D: Expression of the oxytocin gene in the large cells of the bovine corpus luteum. FEBS Lett. 1987, 210 (1): 45-50. 10.1016/0014-5793(87)81295-4.PubMedView ArticleGoogle Scholar
- Higgins GA, Schmale H, Bloom FE, Wilson MC, Milner RJ: Cellular localization of 1B236/myelin-associated glycoprotein mRNA during rat brain development. Proc Natl Acad Sci U S A. 1989, 86 (6): 2074-2078. 10.1073/pnas.86.6.2074.PubMedPubMed CentralView ArticleGoogle Scholar
- De Arcangelis A, Georges-Labouesse E, Adams JC: Expression of fascin-1, the gene encoding the actin-bundling protein fascin-1, during mouse embryogenesis. Gene Expr Patterns. 2004, 4 (6): 637-643. 10.1016/j.modgep.2004.04.012.PubMedView ArticleGoogle Scholar
- Maas C, Tagnaouti N, Loebrich S, Behrend B, Lappe-Siefke C, Kneussel M: Neuronal cotransport of glycine receptor and the scaffold protein gephyrin. J Cell Biol. 2006, 172 (3): 441-451. 10.1083/jcb.200506066.PubMedPubMed CentralView ArticleGoogle Scholar
- Loebrich S, Bahring R, Katsuno T, Tsukita S, Kneussel M: Activated radixin is essential for GABAA receptor alpha5 subunit anchoring at the actin cytoskeleton. Embo J. 2006, 25 (5): 987-999. 10.1038/sj.emboj.7600995.PubMedPubMed CentralView ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.