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

Author:

Klarić Thomas S.12ORCID,Gudelj Ivan123ORCID,Santpere Gabriel14ORCID,Novokmet Mislav2,Vučković Frano2ORCID,Ma Shaojie1ORCID,Doll Hannah M.56ORCID,Risgaard Ryan56ORCID,Bathla Shveta7,Karger Amir8ORCID,Nairn Angus C.7ORCID,Luria Victor19ORCID,Bečeheli Ivona2,Sherwood Chet C.10ORCID,Ely John J.1112,Hof Patrick R.13ORCID,Sousa André M. M.56ORCID,Josić Djuro314,Lauc Gordan215ORCID,Sestan Nenad1716ORCID

Affiliation:

1. Department of Neuroscience, Yale School of Medicine, New Haven, CT, USA.

2. Genos Glycoscience Research Laboratory, Zagreb, Croatia.

3. Department of Biotechnology, University of Rijeka, Rijeka, Croatia.

4. Hospital del Mar Research Institute, Barcelona, Catalonia, Spain.

5. Waisman Center and Department of Neuroscience, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI, USA.

6. Department of Neuroscience, University of Wisconsin-Madison, Madison, WI, USA.

7. Department of Psychiatry, Yale School of Medicine, New Haven, CT, USA.

8. IT Research Computing, Harvard Medical School, Boston, MA, USA.

9. Division of Genetics and Genomics, Boston Children’s Hospital, Harvard Medical School, Boston, USA.

10. Department of Anthropology, The George Washington University, Washington, DC, USA.

11. Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC, USA.

12. MAEBIOS, Alamogordo, NM, USA.

13. Nash Family Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

14. Warren Alpert Medical School, Brown University, Providence, RI, USA.

15. University of Zagreb Faculty of Pharmacy and Biochemistry, Zagreb, Croatia.

16. Departments of Genetics and Comparative Medicine, Kavli Institute for Neuroscience, Program in Cellular Neuroscience, Neurodegeneration and Repair, and Yale Child Study Center, Yale School of Medicine, New Haven, CT, USA.

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.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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