Cited by 482Neuroscience and Neuropharmacology ResearchCellular transport and secretionGenetics and Neurodevelopmental Disorders

Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals

Open access
Dieck, Susannetom, Sanmartí-Vila, Lydia, Langnaese, Kristina, Richter, Karin, Kindler, Stefan, Soyke, Antje, Wex, Heike, Smalla, Karl-Heinz +5 more·1998·The Journal of Cell Biology

Abstract

The molecular architecture of the cytomatrix of presynaptic nerve terminals is poorly understood. Here we show that Bassoon, a novel protein of >400,000 Mr, is a new component of the presynaptic cytoskeleton. The murine bassoon gene maps to chromosome 9F. A comparison with the corresponding rat cDNA identified 10 exons within its protein-coding region. The Bassoon protein is predicted to contain two double-zinc fingers, several coiled-coil domains, and a stretch of polyglutamines (24 and 11 residues in rat and mouse, respectively). In some human proteins, e.g., Huntingtin, abnormal amplification of such poly-glutamine regions causes late-onset neurodegeneration. Bassoon is highly enriched in synaptic protein preparations. In cultured hippocampal neurons, Bassoon colocalizes with the synaptic vesicle protein synaptophysin and Piccolo, a presynaptic cytomatrix component. At the ultrastructural level, Bassoon is detected in axon terminals of hippocampal neurons where it is highly concentrated in the vicinity of the active zone. Immunogold labeling of synaptosomes revealed that Bassoon is associated with material interspersed between clear synaptic vesicles, and biochemical studies suggest a tight association with cytoskeletal structures. These data indicate that Bassoon is a strong candidate to be involved in cytomatrix organization at the site of neurotransmitter release.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1083/jcb.142.2.499

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Piccolo and bassoon are associated with active zones in vertebrates.

    “In addition to these five core active zone proteins, piccolo and bassoon (two large homologous proteins) are associated in vertebrates with active zones (tom Dieck et al., 1998; Wang et al., 1999; Fenster et al., 2000; Limbach et al., 2011), and proteins related to C. elegans SYD-1 are important for the assembly of active zones in invertebrates (Hallam et al., 2002; Patel et al., 2006; Owald et al”

    From The Presynaptic Active Zone (2012) · cites this paper as tom Dieck et al., 1998

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 53

  1. Amaral, D.G., and M.P. Witter. 1994. Hippocampal Formation. In The Rat Nervous System. G. Paxinos, editor. Academic Press Limited, London, United Kingdom. 443–494.
  2. Budnik V Koh YH Guan B Hartmann B Hough C Woods D Gorczyca M Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg Neuron 1996 17 627 640 8893021 PMC4661176
  3. Burns ME Augustine GJ Synaptic structure and function: dynamic organization yields architectural precision Cell 1995 83 187 194 7585936
  4. Carlin RK Grab DJ Cohen RS Siekevitz P Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities J Cell Biol 1980 86 831 843 7410481 PMC2110694
  5. Cases-Langhoff C Voss B Garner AM Appeltauer U Takei K Kindler S Veh RW De Camilli P Gundelfinger ED Garner CC Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix Eur J Cell Biol 1996 69 214 223 8900486
  6. Cohen P The search for physiological substrates of MAP and SAP kinases in mammalian cells Trends Cell Biol 1997 7 353 361 17708980
  7. De Camilli P Cameron R Greengard P Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections J Cell Biol 1983a 96 1337 1354 6404910 PMC2112636
  8. De Camilli P Harris SM Huttner WB Greengard P Synapsin I (protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes J Cell Biol 1983b 96 1355 1373 6404911 PMC2112643
  9. De Camilli P Takei K Molecular mechanisms in synaptic vesicle endocytosis and recycling Neuron 1996 16 481 486 8785046
  10. Froehner SC The submembrane machinery for nicotinic acetylcholine receptor clustering J Cell Biol 1991 114 1 7 2050736 PMC2289056
  11. Garcia EP McPherson PS Chilcote TJ Takei K De Camilli P rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin J Cell Biol 1995 129 105 120 7698978 PMC2120371
  12. Garner, C.C., A. Garner, B. Voss, U. Appeltauer, and E.D. Gundelfinger. 1993. Identifying novel synapse associated proteins. In Neuronal Cytoskeleton– Morphogenesis, Transport and Synaptic Transmission. N. Hirokawa, editor. Japan Scientific Societies Press, Tokyo, Japan. 317–329.
  13. Garner CC Kindler S Synaptic proteins and the assembly of synaptic junctions Trends Cell Biol 1996 6 429 433 15157514
  14. Giasson BI Mushynski WE Study of proline-directed protein kinases involved in phosphorylation of the heavy neurofilament subunit J Neurosci 1997 17 9466 9472 9391002 PMC6573415
  15. Goslin, K., and G. Banker. 1991. Rat hippocampal neurons in low-density culture. In Culturing Nerve Cells. G. Banker and K. Goslin, editors. MIT Press, Cambridge, MA. 251–281.
  16. Hall, Z.W., and J.R. Sanes. 1993. Synaptic structure and development: the neuromuscular junction. Cell. 72 (Suppl):99–121. 8428377
  17. Hayes NVL Rayner DA Baines AJ Purification and properties of p103, a novel 103-kDa component of postsynaptic densities J Neurochem 1991 57 397 405 2072092
  18. Hirokawa N Sobue K Kanda K Harada A Yorifuji H The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1 J Cell Biol 1989 108 111 126 2536030 PMC2115350
  19. Huttner WB Schiebler W Greengard P De Camilli P Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation J Cell Biol 1983 96 1374 1388 6404912 PMC2112660
  20. Kagotani Y Picart R Barret A Wiedenmann B Huttner WB Tixier-Vidal A Subcellular localization of secretogranin II and synaptophysin by immunoelectron microscopy in differentiated hypothalamic neurons in culture J Histochem Cytochem 1991 39 1507 1518 1918927
  21. Kennedy M The postsynaptic density at glutamatergic synapses Trends Neurosci 1997 20 264 268 9185308
  22. Kim E Niethammer M Rothschild A Jan YN Sheng M Clustering of shaker-type K+ channels by interaction with a family of membrane-associated guanylate kinases Nature 1995 378 85 88 7477295
  23. Kim E Cho K Rothschild A Sheng M Heteromultimerization and NMDA receptor-clustering activity of chapsyn-110, a member of the PSD-95 family of proteins Neuron 1996 17 103 113 8755482
  24. Kirsch J Meyer G Betz H Synaptic targeting of ionotropic neurotransmitter receptors Mol Cell Neurosci 1996 8 93 98 8954624
  25. Kistner U Wenzel BM Veh RW Cases-Langhoff C Garner AM Appeltauer U Voss B Gundelfinger ED Garner CC SAP90, a rat presynaptic protein related to the product of the Drosophilatumor suppressor gene dlg-A J Biol Chem 1993 268 4580 4583 7680343
  26. Kotake K Ozaki N Mizuta M Sekiya S Inagaki N Seino S Noc2, a putative zinc-finger protein involved in exocytosis in endocrine cells J Biol Chem 1997 272 29407 29410 9367993
  27. Kozak M An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs Nucl Acids Res 1987 15 8125 8148 3313277 PMC306349
  28. Laemmli UK Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 1970 227 680 685 5432063
  29. Langnaese K Beesley PW Gundelfinger ED Synaptic membrane glycoproteins gp65 and gp55 are new members of the immunoglobulin superfamily J Biol Chem 1997 272 821 827 8995369
  30. Langnaese K Seidenbecher C Wex H Seidel B Hartung K Appeltauer U Garner A Voss B Mueller B Garner CC Gundelfinger ED Protein components of a rat brain synaptic junctional protein preparation Mol Brain Res 1996 42 118 122 8915587
  31. Lichter, P., and T. Cremer. 1992. Chromosome analysis by non-isotopic in situ hybridization. In Human Cytogenetics: A Practical Approach. 2nd ed., Vol. 1. D.E. Rooney, and B.H. Czepulkowski, editors. IRL Press at Oxford University Press, Oxford, United Kingdom. 157–192.
  32. Llinás, R.R., and K.D. Walton. 1990. Cerebellum. In The Synaptic Organization of the Brain. G.M. Shepherd, editor. Oxford University Press, New York.
  33. Lupas A Coiled coils: new structures and new functions Trends Biochem Sci 1996 21 375 382 8918191
  34. Lupas A Van Dyke M Stock J Predicting coiled coils from protein sequences Science 1991 252 1162 1164 2031185
  35. Müller BM Kistner U Veh RW Cases-Langhoff C Becker B Gundelfinger ED Garner CC Molecular characterization and spatial distribution of SAP 97, a novel presynaptic protein homologous to SAP 90 and the Drosophiladiscs-large tumor suppressor protein J Neurosci 1995 15 2354 2366 7891172 PMC6578138
  36. Müller BM Kistner U Kindler S Chung WJ Kuhlendahl S Fenster SD Lau LF Veh RW Huganir RL Gundelfinger ED Garner CC SAP102, a novel postsynaptic protein that interacts with NMDA Receptor complexes in vivo Neuron 1996 17 255 265 8780649
  37. Pieribone VA Shupliakov O Brodin L Hilfiker-Rothenfluh S Czernik AJ Greengard P Distinct pools of synaptic vesicles in neurotransmitter release Nature 1995 375 493 497 7777058
  38. Reddy SP Housman DE The complex pathology of trinucleotide repeats Curr Opin Cell Biol 1997 9 364 372 9159084
  39. Richter K Hamprecht B Scheich H Ultrastructural localization of glycogen phosphorylase predominantly in astrocytes of the gerbil brain Glia 1996 17 263 273 8856323
  40. Rosahl TW Spillane D Missler M Herz J Selig DK Wolff JR Hammer RE Malenka RC Südhof TC Essential functions of synapsins I and II in synaptic vesicle regulation Nature 1995 375 488 493 7777057
  41. Ross C Intranuclear neuronal inclusions: a common pathogenic mechanism for glutamine-repeat neurodegenerative diseases? Neuron 1997 19 1147 1150 9427237
  42. Sánchez-García I The LIM domain: a new structural motif found in zinc-finger-like proteins Trends Genet 1994 10 315 320 7974745
  43. Seidenbecher CI Richter K Rauch U Fässler R Garner CC Gundelfinger ED Brevican, a chondroitin sulfate proteoglycan of rat brain, occurs as secreted and cell surface glycosylphosphatidylinositol- anchored isoforms J Biol Chem 1995 270 27206 27212 7592978
  44. Shirataki H Kaibuchi K Sakoda T Kishida S Yamaguchi T Wada K Miyazaki M Takai Y Rabphilin-3A, a putative target protein for smg p25A/rab3A p25 small GTP-binding protein related to synaptotagmin Mol Cell Biol 1993 13 2061 2068 8384302 PMC359527
  45. Sikorski AF Terlecki G Zagon IS Goodman SR Synapsin I-mediated interaction of brain spectrin with synaptic vesicles J Cell Biol 1991 114 313 318 1906474 PMC2289068
  46. Südhof TC The synaptic vesicle cycle: a cascade of protein-protein interactions Nature 1995 375 645 653 7791897
  47. Südhof TC Function of Rab3 GDP-GTP exchange Neuron 1997 18 519 522 9136761
  48. Takei Y Harada A Takeda S Kobayashi K Terada S Noda T Takahashi T Hirokawa N Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system J Cell Biol 1995 131 1789 1800 8557745 PMC2120677
  49. Thomas U Phannavong B Müller B Garner CC Gundelfinger ED Functional expression of rat synapse-associated proteins SAP97 and SAP102 in Drosophiladlg-1 mutants: effects on tumor suppression and synaptic bouton structure Mech Dev 1997a 62 161 174 9152008
  50. Thomas U Kim E Kuhlendahl S Koh YH Gundelfinger ED Sheng M Garner CC Budnik V Synaptic clustering of the cell adhesion molecule fasciclin II by discs- large and its role in the regulation of presynaptic structure Neuron 1997b 19 787 799 9354326 PMC4658217
  51. Wang Y Okamoto M Schmitz F Hofmann K Südhof TC Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion Nature 1997 388 593 598 9252191
  52. Wiedenmann B Franke WW Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr38.000 characteristic of presynaptic vesicles Cell 1985 41 1017 1028 3924408
  53. Ziff EB Enlightening the postsynaptic density Neuron 1997 19 1163 1174 9427241

Cited by

Sorted by citations

Authors
Dieck, S., Sanmartí-Vila, L., Langnaese, K., Richter, K., Kindler, S., Soyke, A., Wex, H., Smalla, K.-H., Kämpf, U., Fränzer, J.-T., Stumm, M., Garner, C. C., & Gundelfinger, E. D.
Affiliations
  • *Leibniz Institute for Neurobiology, D-39118 Magdeburg, Germany; ‡Institute for Cellular Biochemistry and Clinical Neurobiology, University of Hamburg, D-20246 Hamburg, Germany; §Institute for Human Genetics, Medical Faculty, Otto von Guericke University, D-39120 Magdeburg, Germany; ‖Institute for Pharmacology and Toxicology, Medical Faculty, Otto von Guericke University, D-39120 Magdeburg, Germany; and ¶Department of Neurobiology, University of Alabama at Birmingham, South Birmingham, Alabama 35213-0021
  • Universität Hamburg (DE)
Venue
The Journal of Cell Biology
Published
1998-07-27
Volume
142
Issue
2
Pages
499-509
ISSN
  • 0021-9525 (ISSN-L)
  • 1540-8140
OpenAlex
W1944633888
Cited by
482
References
1
Citations by year
2026: 9 · 2025: 9 · 2024: 13 · 2023: 18 · 2022: 19 · 2021: 14 · 2020: 11 · 2019: 16 · 2018: 5 · 2017: 14 · 2016: 18 · 2015: 16 · 2014: 21 · 2013: 17 · 2012: 36
FWCI
6.33
Type
journal article
Language
en
Open access
Locations
  • The Journal of Cell Biology (publishedVersion)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • W. M. Keck Foundation
  • Deutsche Forschungsgemeinschaft (SFB 426)
  • National Institutes of Health (5p50hd032901-05, P50 HD32901)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (P50 HD32901)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords
bassoon, active zone, presynaptic terminals, zinc finger proteins, polyglutamine repeat, coiled-coil domain, synaptophysin, piccolo, synaptic vesicles, neurotransmitter release, hippocampal neurons, gene mapping, huntingtin
MeSH terms
Amino Acid Sequence, Animals, Base Sequence, Chromosome Mapping, Cloning, Molecular, Exons, Hippocampus, Humans, Molecular Sequence Data, Molecular Weight, Nerve Tissue Proteins, Peptides, Microscopy, Immunoelectron, Zinc Fingers, Sequence Homology, Amino Acid, Presynaptic Terminals, DNA, Complementary, Trinucleotide Repeats, Mice, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review