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Gangliosides in the differentiation process of primary neurons: the specific role of GM1-oligosaccharide

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Abstract

It has been recently reported by our group that GM1-oligosaccharide added to neuroblastoma cells or administered to mouse experimental model mimics the neurotrophic and neuroprotective properties of GM1 ganglioside. In addition to this, differently from GM1, GM1-oligosaccharide is not taken up by the cells, remaining solubilized into the extracellular environment interacting with cell surface proteins. Those characteristics make GM1-oligosaccharide a good tool to study the properties of the endogenous GM1, avoiding to interfere with the ganglioside natural metabolic pathway. In this study, we show that GM1-oligosaccharide administered to mice cerebellar granule neurons by interacting with cell surface induces TrkA-MAP kinase pathway activation enhancing neuron clustering, arborization and networking. Accordingly, in the presence of GM1-oligosaccharide, neurons show a higher phosphorylation rate of FAK and Src proteins, the intracellular key regulators of neuronal motility. Moreover, treated cells express increased level of specific neuronal markers, suggesting an advanced stage of maturation compared to controls. In parallel, we found that in the presence of GM1-oligosaccharide, neurons accelerate the expression of complex gangliosides and reduce the level of the simplest ones, displaying the typical ganglioside pattern of mature neurons. Our data confirms the specific role of GM1 in neuronal differentiation and maturation, determined by its oligosaccharide portion. GM1-oligosacchairide interaction with cell surface receptors triggers the activation of intracellular biochemical pathways responsible for neuronal migration, dendrites emission and axon growth.

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Abbreviations

CGN:

cerebellar granule neurons

Ctx-B:

cholera toxin-subunit B

CTRL:

control

ERK1/2:

extracellular signal-regulated protein kinases 1 and 2

FBS:

fetal bovine serum

GM1:

II3Neu5Ac-Gg4Cer, β-Gal-(1–3)-β-GalNAc-(1–4)-[α-Neu5Ac-(2–3)]-β-Gal-(1–4)-β-Glc-Cer

HPTLC:

high-performance silica gel thin-layer chromatography

MAPK:

mitogen-activated protein kinase

NGF:

nerve growth factor

OligoGM1:

GM1-oligosaccharide, II3Neu5Ac-Gg4.

PBS:

phosphate-buffered saline

P-ERK1/2:

phosphorylated ERK1/2

P-TrkA:

phosphorylated TrkA

PM:

plasma membrane

PVDF:

polyvinylidene difluoride

RRID:

Research Resource Identifiers

Trk:

neurotrophin tyrosin kinase receptor

Tyr490:

tyrosine 490

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Acknowledgments

This work was supported by the 2015-2016 contract from FIDIA s.p.a in favor to S.S. and by University of Milan departmental funds Fond PSR2017_RONDELLI-CHIRICOZZI to E.C.

The authors acknowledge Euro-BioImaging (www.eurobioimaging.eu) for providing access to imaging technologies and services via the Italian Node (ALEMBIC, Milano, Italy).

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  1. Department of Medical Biotechnology and Translational Medicine, University of Milano, Via Fratelli Cervi 93, 20090, Segrate, MI, Italy

    Erika Di Biase, Giulia Lunghi, Maria Fazzari, Margherita Maggioni, Diego Yuri Pomè, Manuela Valsecchi, Maura Samarani, Pamela Fato, Maria Grazia Ciampa, Simona Prioni, Laura Mauri, Sandro Sonnino & Elena Chiricozzi

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  1. Erika Di Biase
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ESM 1

This figure shows the contrast phase images of one week of OligoGM1 treated or not CGN. This figure shows the frame images of the time laps acquisition of OligoGM1 treated or not CGN. (PDF 1185 kb)

ESM 2

Video clip shows the entire video of 24 h time laps analysis of untreated CGN (CTRL). (MP4 8965 kb)

ESM 3

Video clip shows the entire video of 24 h time laps analysis of OligoGM1 treated CGN. (MP4 9257 kb)

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Di Biase, E., Lunghi, G., Fazzari, M. et al. Gangliosides in the differentiation process of primary neurons: the specific role of GM1-oligosaccharide. Glycoconj J 37, 329–343 (2020). https://doi.org/10.1007/s10719-020-09919-x

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