Chondroitin sulfate glycan sulfation patterns influence histochemical labeling of perineuronal nets: a comparative study of interregional distribution in human and mouse brain

Author:

Belliveau Claudia12ORCID,Théberge Stéphanie12,Netto Stefanie1,Rahimian Reza1,Fakhfouri Gohar3,Hosdey Clémentine12,Davoli Maria Antonietta1,Hendrickson Aarun4,Hao Kathryn5,Giros Bruno3,Turecki Gustavo123,Alonge Kimberly M4,Mechawar Naguib123

Affiliation:

1. McGill University McGill Group for Suicide Studies, Douglas Mental Health University Institute, , 6875 Blvd LaSalle, H4H 1R3, Montreal, QC, Canada

2. McGill University Integrated Program in Neuroscience, , 1033 Av des Pins Ouest, H3A 1A1, Montreal, QC, Canada

3. McGill University Department of Psychiatry, , 1033 Av des Pins Ouest, H3A 1A1, Montreal, QC, Canada

4. University of Washington Department of Medicinal Chemistry, , 1959 NE Pacific Street, Box 357610, Seattle, WA 98195, United States

5. University of Southern California Health and Human Sciences, , Zonal Avenue, Biggy St, Los Angeles, CA 90033, United States

Abstract

Abstract Perineuronal nets (PNNs) are a condensed subtype of extracellular matrix that form a net-like coverings around certain neurons in the brain. PNNs are primarily composed of chondroitin sulfate (CS) proteoglycans from the lectican family that consist of CS-glycosaminoglycan side chains attached to a core protein. CS disaccharides can exist in various isoforms with different sulfation patterns. Literature suggests that CS disaccharide sulfation patterns can influence the function of PNNs as well as their labeling. This study was conducted to characterize such interregional CS disaccharide sulfation pattern differences in adult human (n = 81) and mouse (n = 19) brains. Liquid chromatography tandem mass spectrometry was used to quantify five different CS disaccharide sulfation patterns, which were then compared to immunolabeling of PNNs using Wisteria Floribunda Lectin (WFL) to identify CS-glycosaminoglycans and anti-aggrecan to identify CS proteoglycans. In healthy brains, significant regional and species-specific differences in CS disaccharide sulfation and single versus double-labeling pattern were identified. A secondary analysis to investigate how early-life stress impacts these PNN features discovered that although early-life stress increases WFL+ PNN density, the CS-glycosaminoglycan sulfation code and single versus double PNN-labeling distributions remained unaffected in both species. These results underscore PNN complexity in traditional research, emphasizing the need to consider their heterogeneity in future experiments.

Funder

National Institutes of Health

Canadian Institutes of Health Research

Publisher

Oxford University Press (OUP)

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