Human-specific features and developmental dynamics of the brain N-glycome

Klarić, Thomas S.; Gudelj, Ivan; Santpere Baró, Gabriel, 1981-; Novokmet, Mislav; Vučković, Frano; Ma, Shaojie; Doll, Hannah; Risgaard, Ryan; Bathla, Shveta; Karger, Amir; Nairn, Angus C.; Luria, Victor; Bečeheli, Ivona; Sherwood, Chet C.; Ely, John J.; Hof, Patrick R.; Sousa, André M. M.; Josić, Djuro; Lauc, Gordan; Sestan, Nenad

Human-specific features and developmental dynamics of the brain N-glycome

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dc.contributor.author Klarić, Thomas S.
dc.contributor.author Gudelj, Ivan
dc.contributor.author Santpere Baró, Gabriel, 1981-
dc.contributor.author Novokmet, Mislav
dc.contributor.author Vučković, Frano
dc.contributor.author Ma, Shaojie
dc.contributor.author Doll, Hannah
dc.contributor.author Risgaard, Ryan
dc.contributor.author Bathla, Shveta
dc.contributor.author Karger, Amir
dc.contributor.author Nairn, Angus C.
dc.contributor.author Luria, Victor
dc.contributor.author Bečeheli, Ivona
dc.contributor.author Sherwood, Chet C.
dc.contributor.author Ely, John J.
dc.contributor.author Hof, Patrick R.
dc.contributor.author Sousa, André M. M.
dc.contributor.author Josić, Djuro
dc.contributor.author Lauc, Gordan
dc.contributor.author Sestan, Nenad
dc.date.accessioned 2024-11-08T08:20:50Z
dc.date.available 2024-11-08T08:20:50Z
dc.date.issued 2023
dc.description.abstract Comparative “omics” studies have revealed unique aspects of human neurobiology, yet an evolutionary perspective of the brain N-glycome is lacking. We performed multiregional characterization of rat, macaque, chimpanzee, and human brain N-glycomes using chromatography and mass spectrometry and then integrated these data with complementary glycotranscriptomic data. We found that, in primates, the brain N-glycome has diverged more rapidly than the underlying transcriptomic framework, providing a means for rapidly generating additional interspecies diversity. Our data suggest that brain N-glycome evolution in hominids has been characterized by an overall increase in complexity coupled with a shift toward increased usage of α(2-6)–linked N-acetylneuraminic acid. Moreover, interspecies differences in the cell type expression pattern of key glycogenes were identified, including some human-specific differences, which may underpin this evolutionary divergence. Last, by comparing the prenatal and adult human brain N-glycomes, we uncovered region-specific neurodevelopmental pathways that lead to distinct spatial N-glycosylation profiles in the mature brain.
dc.description.sponsorship This work was supported by the following funding sources: NIH grant MH124619 (N.S.), NIH grant MH116488 (N.S.), NIH grant DA053628 (N.S.), NIH grant R01HG010898-01 (N.S. and G.S.), Instituto de Salud Carlos III (Spain) grant MS20/00064 (G.S.), Agencia Estatal de Investigación (Spain) grant PID2019-104700GA-I00/AEI/10.13039/501100011033 (G.S.), and the European Union Seventh Framework Programme (FP7 2007 2013) under grant agreement no. 291823 Marie Curie FP7-PEOPLE-2011-COFUND (The New International Fellowship Mobility Programme for Experienced Researchers in Croatia NEWFELPRO). This paper has been written as a part of the project “A spatio-temporal analysis of glycosylation in the human brain (Human Neuroglycome),” which has received funding through NEWFELPRO project under grant agreement no. 34 (T.S.K.). We acknowledge the National Chimpanzee Brain Resource (funded by NIH NS092988) for contributing brain specimens used in this study.
dc.format.mimetype application/pdf
dc.identifier.citation Klarić TS, Gudelj I, Santpere G, Novokmet M, Vučković F, Ma S, et al. Human-specific features and developmental dynamics of the brain N-glycome. Science Advances. 2023;9(49):eadg2615. DOI: 10.1101/2023.01.11.523525
dc.identifier.doi http://dx.doi.org/10.1101/2023.01.11.523525
dc.identifier.issn 2375-2548
dc.identifier.uri http://hdl.handle.net/10230/68466
dc.language.iso eng
dc.publisher American Association for the Advancement of Science (AAAS)
dc.relation.ispartof Science Advances. 2023;9(49):eadg2615
dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/291823
dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PID2019-104700GA-I00
dc.rights © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (http://creativecommons.org/licenses/by-nc/4.0/), which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
dc.rights.accessRights info:eu-repo/semantics/openAccess
dc.rights.uri http://creativecommons.org/licenses/by-nc/4.0/
dc.subject.other Neurobiologia
dc.title Human-specific features and developmental dynamics of the brain N-glycome
dc.type info:eu-repo/semantics/article
dc.type.version info:eu-repo/semantics/publishedVersion

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