Defective IGF-1 prohormone N-glycosylation and reduced IGF-1 receptor signaling activation in congenital disorders of glycosylation.


Journal

Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402

Informations de publication

Date de publication:
24 Feb 2022
Historique:
received: 14 10 2021
accepted: 31 01 2022
revised: 24 01 2022
entrez: 25 2 2022
pubmed: 26 2 2022
medline: 3 3 2022
Statut: epublish

Résumé

The insulin-like growth factor-1 (IGF-1) signaling pathway is crucial for the regulation of growth and development. The correct processing of the IGF-1Ea prohormone (proIGF-1Ea) and the IGF-1 receptor (IGF-1R) peptide precursor requires proper N-glycosylation. Deficiencies of N-linked glycosylation lead to a clinically heterogeneous group of inherited diseases called Congenital Disorders of Glycosylation (CDG). The impact of N-glycosylation defects on IGF-1/IGF-1R signaling components is largely unknown. In this study, using dermal fibroblasts from patients with different CDG [PMM2-CDG (n = 7); ALG3-CDG (n = 2); ALG8-CDG (n = 1); GMPPB-CDG (n = 1)], we analyzed the glycosylation pattern of the proIGF-1Ea, IGF-1 secretion efficiency and IGF-1R signaling activity. ALG3-CDG, ALG8-CDG, GMPPB-CDG and some PMM2-CDG fibroblasts showed hypoglycosylation of the proIGF-1Ea and lower IGF-1 secretion when compared with control (CTR). Lower IGF-1 serum concentration was observed in ALG3-CDG, ALG8-CDG and in some patients with PMM2-CDG, supporting our in vitro data. Furthermore, reduced IGF-1R expression level was observed in ALG3-CDG, ALG8-CDG and in some PMM2-CDG fibroblasts. IGF-1-induced IGF-1R activation was lower in most PMM2-CDG fibroblasts and was associated with decreased ERK1/2 phosphorylation as compared to CTR. In general, CDG fibroblasts showed a slight upregulation of Endoplasmic Reticulum (ER) stress genes compared with CTR, uncovering mild ER stress in CDG cells. ER-stress-related gene expression negatively correlated with fibroblasts IGF-1 secretion. This study provides new evidence of a direct link between N-glycosylation defects found in CDG and the impairment of IGF-1/IGF-1R signaling components. Further studies are warranted to determine the clinical consequences of reduced systemic IGF-1 availability and local activity in patients with CDG.

Identifiants

pubmed: 35211808
doi: 10.1007/s00018-022-04180-x
pii: 10.1007/s00018-022-04180-x
pmc: PMC8873121
doi:

Substances chimiques

Biomarkers 0
Lectins 0
RNA, Messenger 0
Insulin-Like Growth Factor I 67763-96-6
Receptor, IGF Type 1 EC 2.7.10.1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

150

Informations de copyright

© 2022. The Author(s).

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Auteurs

Laura Di Patria (L)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Via I Maggetti, 26/2, 61029, Urbino, Italy.

Giosuè Annibalini (G)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Via I Maggetti, 26/2, 61029, Urbino, Italy. giosue.annibalini@uniurb.it.

Amelia Morrone (A)

Laboratory of Molecular Biology of Neurometabolic Diseases, Neuroscience Department, Meyer Children's Hospital, Florence, Italy.
Department of NEUROFARBA, University of Florence, Florence, Italy.

Lorenzo Ferri (L)

Laboratory of Molecular Biology of Neurometabolic Diseases, Neuroscience Department, Meyer Children's Hospital, Florence, Italy.

Roberta Saltarelli (R)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Via I Maggetti, 26/2, 61029, Urbino, Italy.

Luca Galluzzi (L)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Via I Maggetti, 26/2, 61029, Urbino, Italy.

Aurora Diotallevi (A)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Via I Maggetti, 26/2, 61029, Urbino, Italy.

Matteo Bocconcelli (M)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Via I Maggetti, 26/2, 61029, Urbino, Italy.

Maria Alice Donati (MA)

Laboratory of Molecular Biology of Neurometabolic Diseases, Neuroscience Department, Meyer Children's Hospital, Florence, Italy.
Department of NEUROFARBA, University of Florence, Florence, Italy.

Rita Barone (R)

Child Neurology and Psychiatry Unit, Department of Clinical and Experimental Medicine, University of Catania, Catania, Italy.
Reseach Unit of Rare Diseases and Neurodevelopmental Disorders, Oasi Research Institute-IRCCS, Troina, Italy.

Renzo Guerrini (R)

Laboratory of Molecular Biology of Neurometabolic Diseases, Neuroscience Department, Meyer Children's Hospital, Florence, Italy.
Department of NEUROFARBA, University of Florence, Florence, Italy.

Jaak Jaeken (J)

Center for Metabolic Diseases, University Hospital Gasthuisberg, KU Leuven, Leuven, Belgium.

Vilberto Stocchi (V)

Department of Human Sciences for the Promotion of Quality of Life, University San Raffaele, Roma, Italy.

Elena Barbieri (E)

Department of Biomolecular Sciences, University of Urbino Carlo Bo, Via I Maggetti, 26/2, 61029, Urbino, Italy.
IIM, Interuniversity Institute of Myology, Perugia, Italy.

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Classifications MeSH