The dynamic nature of netrin-1 and the structural basis for glycosaminoglycan fragment-induced filament formation.

Netrin-1 Glycosaminoglycans Heparin Axon Guidance Cell Differentiation Heparan Sulfate Proteoglycans

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
03 03 2023
Historique:
received: 13 10 2021
accepted: 13 02 2023
entrez: 3 3 2023
pubmed: 4 3 2023
medline: 8 3 2023
Statut: epublish

Résumé

Netrin-1 is a bifunctional chemotropic guidance cue that plays key roles in diverse cellular processes including axon pathfinding, cell migration, adhesion, differentiation, and survival. Here, we present a molecular understanding of netrin-1 mediated interactions with glycosaminoglycan chains of diverse heparan sulfate proteoglycans (HSPGs) and short heparin oligosaccharides. Whereas interactions with HSPGs act as platform to co-localise netrin-1 close to the cell surface, heparin oligosaccharides have a significant impact on the highly dynamic behaviour of netrin-1. Remarkably, the monomer-dimer equilibrium of netrin-1 in solution is abolished in the presence of heparin oligosaccharides and replaced with highly hierarchical and distinct super assemblies leading to unique, yet unknown netrin-1 filament formation. In our integrated approach we provide a molecular mechanism for the filament assembly which opens fresh paths towards a molecular understanding of netrin-1 functions.

Identifiants

DOI: 10.1038/s41467-023-36692-w PMID: 36869049 PMC: PMC9984387
pubmed: 36869049
doi: 10.1038/s41467-023-36692-w
pii: 10.1038/s41467-023-36692-w
pmc: PMC9984387
doi:

Substances chimiques

Netrin-1 158651-98-0
Glycosaminoglycans 0
Heparin 9005-49-6
Heparan Sulfate Proteoglycans 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1226

Subventions

Organisme : CIHR
ID : PJT 152935
Pays : Canada

Informations de copyright

© 2023. The Author(s).

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Auteurs

Markus Meier (M)

Department of Chemistry, University of Manitoba, Winnipeg, Canada.
ORCID: 0000-0003-1068-746X

Monika Gupta (M)

Department of Chemistry, University of Manitoba, Winnipeg, Canada.

Serife Akgül (S)

Center for Biochemistry II, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.
Max Planck Institute for Biology of Ageing, Cologne, Germany.
ORCID: 0000-0003-0943-6241

Matthew McDougall (M)

Department of Chemistry, University of Manitoba, Winnipeg, Canada.

Thomas Imhof (T)

Center for Biochemistry II, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany.

Denise Nikodemus (D)

Faculty of Biology, Institute of Biology II, Albert Ludwigs University of Freiburg, Freiburg, Germany.

Raphael Reuten (R)

Institute of Experimental and Clinical Pharmacology and Toxicology, Medical Faculty, University of Freiburg, Freiburg, Germany.
Department of Obsterics and Gynecology, Medical Center, University of Freiburg, Freiburg, Germany.
ORCID: 0000-0002-9434-4108

Aniel Moya-Torres (A)

Department of Chemistry, University of Manitoba, Winnipeg, Canada.

Vu To (V)

Department of Chemistry, University of Manitoba, Winnipeg, Canada.

Fraser Ferens (F)

Department of Chemistry, University of Manitoba, Winnipeg, Canada.
ORCID: 0000-0002-6686-1183

Fabian Heide (F)

Department of Chemistry, University of Manitoba, Winnipeg, Canada.
ORCID: 0000-0002-6849-3177

Gay Pauline Padilla-Meier (GP)

Department of Chemistry, University of Manitoba, Winnipeg, Canada.
ORCID: 0000-0001-8808-9035

Philipp Kukura (P)

Physical and Theoretical Chemistry Laboratory, Department of Chemistry, University of Oxford, South Parks Road, Oxford, OX1 3QZ, UK.
ORCID: 0000-0003-0136-7704

Wenming Huang (W)

Max Planck Institute for Biology of Ageing, Cologne, Germany.

Birgit Gerisch (B)

Max Planck Institute for Biology of Ageing, Cologne, Germany.

Matthias Mörgelin (M)

Colzyx AB, Lund, Sweden.

Kate Poole (K)

Max Delbrück Center for Molecular Medicine, Robert Roessle Str 10, Berlin-Buch, Germany.
EMBL Australia Node in Single Molecule Science, School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, NSW, Australia.

Adam Antebi (A)

Max Planck Institute for Biology of Ageing, Cologne, Germany. aantebi@age.mpg.de.
Cologne Excellence Cluster on Cellular Stress Responses in Aging Associated Diseases, University of Cologne, Cologne, 50931, Germany. aantebi@age.mpg.de.
ORCID: 0000-0002-7241-3029

Manuel Koch (M)

Center for Biochemistry II, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. manuel.koch@uni-koeln.de.
Institute for Dental Research and Oral Musculoskeletal Biology, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. manuel.koch@uni-koeln.de.
Center for Molecular Medicine Cologne, Faculty of Medicine and University Hospital Cologne, University of Cologne, 50931, Cologne, Germany. manuel.koch@uni-koeln.de.
ORCID: 0000-0002-2962-7814

Jörg Stetefeld (J)

Department of Chemistry, University of Manitoba, Winnipeg, Canada. jorg.stetefeld@umanitoba.ca.
ORCID: 0000-0003-1478-3248

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Classifications MeSH

questionsmedicales.fr › Facteurs biologiques › Protéines et peptides de signalisation intercellulaire › Facteurs de croissance nerveuse › Nétrines › Nétrine-1 › The dynamic nature of netrin-1 and the...
questionsmedicales.fr › Glucides › Polyosides › Glycosaminoglycanes › The dynamic nature of netrin-1 and the...
questionsmedicales.fr › Glucides › Polyosides › Glycosaminoglycanes › Héparine › The dynamic nature of netrin-1 and the...
questionsmedicales.fr › Phénomènes physiologiques de l'appareil locomoteur et du système nerveux › Phénomènes physiologiques du système nerveux › Neurogenèse › Excroissance neuronale › Guidage axonal › The dynamic nature of netrin-1 and the...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Différenciation cellulaire › The dynamic nature of netrin-1 and the...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Glycoprotéines › Protéoglycanes › Protéoglycanes à sulfate d'héparane › The dynamic nature of netrin-1 and the...