Evidence map›Paper›PMID 30100184›Full record

ArticleCell2018

Heparan Sulfate Organizes Neuronal Synapses through Neurexin Partnerships.

Peng Zhang, Hong Lu, Rui T Peixoto, Mary K Pines, Yuan Ge, Shinichiro Oku, Tabrez J Siddiqui, Yicheng Xie, Wenlan Wu, Stephanie Archer-Hartmann and 8 more

Open access · hybridAbstract read
In one paragraph

Article in Cell, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 110 papers.

0numbers the graph read from it
0cells of the map it votes in
110citing papers in PubMed
9.6field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

110 citing papers in PubMed, 162 citations in OpenAlex.

  1. Article
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  7. Review
  8. Heparan sulfate is essential for Drosophila FGF export.bioRxiv : the preprint server for biology · 2026
    Article
  9. Article
  10. Article
  11. GalNAc-T13 maintains neurite architecture and memory retention via O-GalNAc glycosylation of seizure protein 6.Proceedings of the National Academy of Sciences of the United States of America · 2026
    Article
  12. Review
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  14. Article
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  18. Article
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50 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

18 authors at 7 institutions in 6 countries.

Peng ZhangDjavad Mowafaghian Centre for Brain Health and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada. Electronic address: peng.pengzhang@gmail.com.
Hong LuDjavad Mowafaghian Centre for Brain Health and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada.
Rui T PeixotoHoward Hughes Medical Institute, Harvard Medical School, Department of Neurobiology, Boston, MA 02115, USA; Istituto Italiano di Tecnologia, Genova 16163, Italy.
Mary K PinesDepartment of Zoology and Life Sciences Institute, University of British Columbia, Vancouver, BC V6T 1Z3, Canada.
Yuan GeDjavad Mowafaghian Centre for Brain Health and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada.
Shinichiro OkuDjavad Mowafaghian Centre for Brain Health and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada.
Tabrez J SiddiquiDjavad Mowafaghian Centre for Brain Health and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada.
Yicheng XieDjavad Mowafaghian Centre for Brain Health and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada.
Wenlan WuDjavad Mowafaghian Centre for Brain Health and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada; Medical School, Henan University of Science and Technology, Luoyang 471023, China.
Stephanie Archer-HartmannComplex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, USA.
Keitaro YoshidaDepartment of Neuropsychiatry, Keio University School of Medicine, Tokyo 160-8582, Japan.
Kenji F TanakaDepartment of Neuropsychiatry, Keio University School of Medicine, Tokyo 160-8582, Japan.
A Radu AricescuMRC Laboratory of Molecular Biology, Cambridge Biomedical Campus, Cambridge CB2 0QH, UK.
Parastoo AzadiComplex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, USA.
Michael D GordonDepartment of Zoology and Life Sciences Institute, University of British Columbia, Vancouver, BC V6T 1Z3, Canada.
Bernardo L SabatiniHoward Hughes Medical Institute, Harvard Medical School, Department of Neurobiology, Boston, MA 02115, USA.
Rachel O L WongDepartment of Biological Structure, University of Washington, Seattle, WA 98195, USA.
Ann Marie CraigDjavad Mowafaghian Centre for Brain Health and Department of Psychiatry, University of British Columbia, Vancouver, BC V6T 2B5, Canada. Electronic address: acraig@mail.ubc.ca.
University of British Columbia · CAKeio University · JPUniversity of Georgia · USHarvard University · USHoward Hughes Medical Institute · USMRC Laboratory of Molecular Biology · GBUniversity of Washington · US

Funding

TR&D3. Approaches to Proteoglycan Function at Biochemical and Cellular LevelsP41GM103390 · NIGMS · UNIVERSITY OF GEORGIA · PI MOREMEN, KELLEY W. · 2012 to 2019
$14.5M
Action and interaction of ionotropic and metabotropic neurotransmissionR37NS046579 · NINDS · HARVARD MEDICAL SCHOOL · PI SABATINI, BERNARDO L · 2018 to 2024
$4.6M
Mechanisms of Central Neuron SynaptogenesisR01MH070860 · NIMH · UNIVERSITY OF BRITISH COLUMBIA · PI CRAIG, ANN M · 2005 to 2015
$2.3M
Orbitrap Fusion Tribrid Mass SpectrometerS10OD018530 · OD · UNIVERSITY OF GEORGIA · PI AZADI, PARASTOO · 2014 to 2014
$750k
CIHR FDN-143206CIHR MOP-11934Howard Hughes Medical InstituteMedical Research Council G0700232Medical Research Council MC_EX_MR/L009609/2Medical Research Council MC_UP_1201/15Medical Research Council MR/L009609/1NIGMS NIH HHS P41 GM103390NIH HHS S10 OD018530NIMH NIH HHS R01 MH070860NINDS NIH HHS R37 NS046579
6 · The paper itself

Abstract

Synapses are fundamental units of communication in the brain. The prototypical synapse-organizing complex neurexin-neuroligin mediates synapse development and function and is central to a shared genetic risk pathway in autism and schizophrenia. Neurexin's role in synapse development is thought to be mediated purely by its protein domains, but we reveal a requirement for a rare glycan modification. Mice lacking heparan sulfate (HS) on neurexin-1 show reduced survival, as well as structural and functional deficits at central synapses. HS directly binds postsynaptic partners neuroligins and LRRTMs, revealing a dual binding mode involving intrinsic glycan and protein domains for canonical synapse-organizing complexes. Neurexin HS chains also bind novel ligands, potentially expanding the neurexin interactome to hundreds of HS-binding proteins. Because HS structure is heterogeneous, our findings indicate an additional dimension to neurexin diversity, provide a molecular basis for fine-tuning synaptic function, and open therapeutic directions targeting glycan-binding motifs critical for brain development.

Indexed as

Amino Acid SequenceAnimalsCalcium-Binding ProteinsCell Adhesion Molecules, NeuronalDrosophilaDrosophila ProteinsFemaleGlycopeptidesHeparan SulfateHumansMembrane ProteinsMiceMice, Inbred C57BLNerve Tissue ProteinsNeural Cell Adhesion MoleculesNeuronsCalcium-Binding ProteinsCell Adhesion Molecules, NeuronalDrosophila ProteinsGlycopeptidesHeparan SulfateLRRTM2 protein, mouseMembrane ProteinsNerve Tissue ProteinsNeural Cell Adhesion Moleculesneuroligin 1Nrxn1 protein, mouseRNA, Small Interferingheparan sulphateLRRTMmossy fiberneurexinneuroliginproteoglycansynaptic adhesion proteinsynaptic transmissionsynaptogenesisthorny excrescence

Identifiers

PMID30100184
PMCPMC6173057
OpenAlexW2885963228

What OpenQuestion holds

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LicenceCC BY
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.