Evidence map›Paper›PMID 26731579›Full record

ArticleACS chemical biology2016

Expanding the 3-O-Sulfate Proteome--Enhanced Binding of Neuropilin-1 to 3-O-Sulfated Heparan Sulfate Modulates Its Activity.

Bryan E Thacker, Emylie Seamen, Roger Lawrence, Matthew W Parker, Yongmei Xu, Jian Liu, Craig W Vander Kooi, Jeffrey D Esko

Open access · greenAbstract read
In one paragraph

Article in ACS chemical biology, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 49 papers.

0numbers the graph read from it
0cells of the map it votes in
49citing papers in PubMed
4.4field-weighted citation impact, top 6% 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

49 citing papers in PubMed, 68 citations in OpenAlex.

  1. Review
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  11. Increased 3-Science advances · 2023
    Article
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  15. Review
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  17. Article
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  19. Global analyses of mRNA expression in human sensory neurons reveal eIF5A as a conserved target for inflammatory pain.FASEB journal : official publication of the Federation of American Societies for Experimental Biology · 2022
    Article
  20. Emerging chemical and biochemical tools for studying 3-American journal of physiology. Cell physiology · 2022
    Review
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

8 authors at 3 institutions in 1 country.

Bryan E Thacker
Emylie Seamen
Roger Lawrence
Matthew W ParkerCenter for Structural Biology, Department of Molecular and Cellular Biochemistry, University of Kentucky , Lexington, Kentucky 40536, United States.
Yongmei XuDivision of Chemical Biology and Medicinal Chemistry, Eshelman School of Pharmacy, University of North Carolina , Chapel Hill, North Carolina 27599, United States.
Jian LiuDivision of Chemical Biology and Medicinal Chemistry, Eshelman School of Pharmacy, University of North Carolina , Chapel Hill, North Carolina 27599, United States.
Craig W Vander KooiCenter for Structural Biology, Department of Molecular and Cellular Biochemistry, University of Kentucky , Lexington, Kentucky 40536, United States.
Jeffrey D Esko
University of California, San Diego · USUniversity of Kentucky · USUniversity of North Carolina at Chapel Hill · US

Funding

Siglec Modulation of Inflammatory ResponsesP01HL107150 · NHLBI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI LE, DZUNG T · 2011 to 2017
$18.0M
Predoctoral and Postdoctoral Training in Cancer Cell BiologyT32CA067754 · NCI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI JEAN Y.J. WANG · 1995 to 2026
$6.5M
In vitro synthesis of recombinant heparan sulfateR01HL094463 · NHLBI · UNIV OF NORTH CAROLINA CHAPEL HILL · PI LIU, JIAN, PAWLINSKI, RAFAL L · 2009 to 2021
$5.2M
Mechanism of Neuropilin Dependent AngiogenesisR01GM094155 · NIGMS · UNIVERSITY OF KENTUCKY · PI VANDER KOOI, CRAIG · 2010 to 2014
$1.3M
Structure and Function of 3-O-sulfation in Heparan SulfateR01GM093131 · NIGMS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI ESKO, JEFFREY D · 2010 to 2013
$1.2M
Searching for Novel Genes in Heparan Sulfate BiosynthesisF32CA156987 · NCI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI SEAMEN, EMYLIE · 2011 to 2013
$161k
NCI NIH HHS F32 CA156987NCI NIH HHS F32CA156987NCI NIH HHS T32 CA067754NCI NIH HHS T32CA067754NHLBI NIH HHS HL107150NHLBI NIH HHS P01 HL107150NHLBI NIH HHS R01 HL094463NIGMS NIH HHS GM094155NIGMS NIH HHS GM93131NIGMS NIH HHS R01 GM093131NIGMS NIH HHS R01 GM094155
6 · The paper itself

Abstract

Binding of proteins to heparan sulfate is driven predominantly by electrostatic interactions between positively charged amino acid residues in the protein and negatively charged sulfate groups located at various positions along the polysaccharide chain. Although many heparin/heparan-sulfate-binding proteins have been described, few exhibit preferential binding for heparan sulfates containing relatively rare 3-O-sulfated glucosamine residues. To expand the "3-O-sulfate proteome," affinity matrices were created from Chinese hamster ovary (CHO) cell heparan sulfate engineered in vitro with and without 3-O-sulfate groups. Fractionation of different animal sera yielded several proteins that bound specifically to columns containing 3-O-sulfated heparan sulfate modified by two members of the heparan sulfate 3-O-sulfotransferase superfamily, Hs3st1 and Hs3st2. Neuropilin-1 was analyzed in detail because it has been implicated in angiogenesis and axon guidance. We show that 3-O-sulfation enhanced the binding of neuropilin-1 to heparan sulfate immobilized on plastic plates and to heparan sulfate present on cultured cells. Chemoenzymatically synthesized 3-O-sulfated heparan sulfate dodecamers protected neuropilin-1 from thermal denaturation and inhibited neuropilin-1-dependent, semaphorin-3a-induced growth cone collapse of neurons derived from murine dorsal root ganglia. The effect of 3-O-sulfation was cell autonomous and specific to Hs3st2 based on collapse assays of neurons derived from Hs3st1- and Hs3st2-deficient mice. Finally, 3-O-sulfated heparan sulfate enhanced the inhibition of endothelial cell sprouting by exogenous heparan sulfate. These findings demonstrate a reliable method to identify members of the 3-O-sulfate proteome and that 3-O-sulfation of heparan sulfate can modulate axonal growth cone collapse and endothelial cell sprouting.

Indexed as

ProteomeAnimalsCarbohydrate SequenceCattleHeparan SulfateHumansMiceNeuropilin-1OligosaccharidesSulfatesHeparan SulfateNeuropilin-1OligosaccharidesProteomeSulfates

Identifiers

PMID26731579
PMCPMC5450942
OpenAlexW2231907166

What OpenQuestion holds

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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.