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The Neuroprotective Role of the GM1 Oligosaccharide, II3Neu5Ac-Gg4, in Neuroblastoma Cells

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Abstract

Recently, we demonstrated that the GM1 oligosaccharide, II3Neu5Ac-Gg4 (OligoGM1), administered to cultured murine Neuro2a neuroblastoma cells interacts with the NGF receptor TrkA, leading to the activation of the ERK1/2 downstream pathway and to cell differentiation. To understand how the activation of the TrkA pathway is able to trigger key biochemical signaling, we performed a proteomic analysis on Neuro2a cells treated with 50 μM OligoGM1 for 24 h. Over 3000 proteins were identified. Among these, 324 proteins were exclusively expressed in OligoGM1-treated cells. Interestingly, several proteins expressed only in OligoGM1-treated cells are involved in biochemical mechanisms with a neuroprotective potential, reflecting the GM1 neuroprotective effect. In addition, we found that the exogenous administration of OligoGM1 reduced the cellular oxidative stress in Neuro2a cells and conferred protection against MPTP neurotoxicity. These results confirm and reinforce the idea that the molecular mechanisms underlying the GM1 neurotrophic and neuroprotective effects depend on its oligosaccharide chain, suggesting the activation of a positive signaling starting at plasma membrane level.

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Abbreviations

Ganglioside nomenclature:

is in accordance with IUPAC-IUBB recommendations [1]

GM1:

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

OligoGM1:

GM1 oligosaccharide, II3Neu5Ac-Gg4

Ctrl:

Control

DMEM:

Dulbecco’s modified Eagle’s medium

ERK1/2:

Extracellular signal-regulated protein kinases 1 and 2

FBS:

Fetal bovine serum

HPTLC:

High-performance silica gel thin-layer chromatography

IPA:

Ingenuity Pathway Analysis

MAPK:

Mitogen-activated protein kinase

MPP+ :

1-Methyl-4-phenylpyridinium

MPTP:

1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine hydrochloride

MS:

Mass spectrometry

N2a:

Neuro2a cells

NGF:

Nerve growth factor

PBS:

Phosphate-buffered saline

p-ERK1/2:

Phosphorylated ERK1/2

p-TrkA:

Phosphorylated TrkA

PM:

Plasma membrane

PVDF:

Polyvinylidene difluoride

RA:

Retinoic acid

ROS:

Reactive oxygen species

RRID:

Research resource identifiers

Trk:

Neurotrophin tyrosine kinase receptor

Tyr490:

Tyrosine 490

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Author notes

  1. Elena Chiricozzi and Margherita Maggioni contributed equally to this work.

Authors and Affiliations

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

    Elena Chiricozzi, Margherita Maggioni, Erika di Biase, Giulia Lunghi, Maria Fazzari, Nicoletta Loberto & Sandro Sonnino

  2. Department of Veterinary Medicine, University of Milan, via Celoria 10, 20133, Milan, Italy

    Maffioli Elisa, Francesca Grassi Scalvini & Gabriella Tedeschi

  3. Fondazione Unimi, v.le Ortles 22/4, 20139, Milan, Italy

    Gabriella Tedeschi

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  1. Elena Chiricozzi
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Chiricozzi, E., Maggioni, M., di Biase, E. et al. The Neuroprotective Role of the GM1 Oligosaccharide, II3Neu5Ac-Gg4, in Neuroblastoma Cells. Mol Neurobiol 56, 6673–6702 (2019). https://doi.org/10.1007/s12035-019-1556-8

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