A Defined Glycosylation Regulatory Network Modulates Total Glycome Dynamics During Pluripotency State Transition

Overview

Journal Sci Rep

Specialty Science

Date 2021 Jan 15

PMID 33446700

Citations 8

Authors

Federico Pecori

Ikuko Yokota

Hisatoshi Hanamatsu

Taichi Miura

Chika Ogura

Hayato Ota

Jun-Ichi Furukawa

Shinya Oki

Kazuo Yamamoto

Osamu Yoshie

Shoko Nishihara

Affiliations

Soon will be listed here.

Abstract

Embryonic stem cells (ESCs) and epiblast-like cells (EpiLCs) recapitulate in vitro the epiblast first cell lineage decision, allowing characterization of the molecular mechanisms underlying pluripotent state transition. Here, we performed a comprehensive and comparative analysis of total glycomes of mouse ESCs and EpiLCs, revealing that overall glycosylation undergoes dramatic changes from early stages of development. Remarkably, we showed for the first time the presence of a developmentally regulated network orchestrating glycosylation changes and identified polycomb repressive complex 2 (PRC2) as a key component involved in this process. Collectively, our findings provide novel insights into the naïve-to-primed pluripotent state transition and advance the understanding of glycosylation complex regulation during early mouse embryonic development.

Citing Articles

Switching mechanism from AR to EGFR signaling via 3-O-sulfated heparan sulfate in castration-resistant prostate cancer.

Ota H, Sato H, Mizumoto S, Wakai K, Yoneda K, Yamamoto K Sci Rep. 2023; 13(1):11618.

PMID: 37463954 PMC: 10354070. DOI: 10.1038/s41598-023-38746-x.

Isotopic Tracing of Nucleotide Sugar Metabolism in Human Pluripotent Stem Cells.

Conte F, Noga M, van Scherpenzeel M, Veizaj R, Scharn R, Sam J Cells. 2023; 12(13).

PMID: 37443799 PMC: 10340731. DOI: 10.3390/cells12131765.

PRC2-dependent regulation of ganglioside expression during dedifferentiation contributes to the proliferation and migration of vascular smooth muscle cells.

Sasaki N, Hirano K, Shichi Y, Itakura Y, Ishiwata T, Toyoda M Front Cell Dev Biol. 2022; 10:1003349.

PMID: 36313564 PMC: 9606594. DOI: 10.3389/fcell.2022.1003349.

Bridging Glycomics and Genomics: New Uses of Functional Genetics in the Study of Cellular Glycosylation.

Stewart N, Wisnovsky S Front Mol Biosci. 2022; 9:934584.

PMID: 35782863 PMC: 9243437. DOI: 10.3389/fmolb.2022.934584.

Comprehensive and Comparative Structural Glycome Analysis in Mouse Epiblast-like Cells.

Pecori F, Hanamatsu H, Furukawa J, Nishihara S Methods Mol Biol. 2022; 2490:179-193.

PMID: 35486246 DOI: 10.1007/978-1-0716-2281-0_13.

References

Nishihara S . Glycans in stem cell regulation: from Drosophila tissue stem cells to mammalian pluripotent stem cells. FEBS Lett. 2018; 592(23):3773-3790. DOI: 10.1002/1873-3468.13167. View

He J, Shen L, Wan M, Taranova O, Wu H, Zhang Y . Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes. Nat Cell Biol. 2013; 15(4):373-84. PMC: 4078788. DOI: 10.1038/ncb2702. View

Russo D, Della Ragione F, Rizzo R, Sugiyama E, Scalabri F, Hori K . Glycosphingolipid metabolic reprogramming drives neural differentiation. EMBO J. 2017; 37(7). PMC: 5881633. DOI: 10.15252/embj.201797674. View

Guan F, Handa K, Hakomori S . Specific glycosphingolipids mediate epithelial-to-mesenchymal transition of human and mouse epithelial cell lines. Proc Natl Acad Sci U S A. 2009; 106(18):7461-6. PMC: 2678670. DOI: 10.1073/pnas.0902368106. View

Kurimoto K, Yabuta Y, Hayashi K, Ohta H, Kiyonari H, Mitani T . Quantitative Dynamics of Chromatin Remodeling during Germ Cell Specification from Mouse Embryonic Stem Cells. Cell Stem Cell. 2015; 16(5):517-32. DOI: 10.1016/j.stem.2015.03.002. View

Lanner F, Rossant J . The role of FGF/Erk signaling in pluripotent cells. Development. 2010; 137(20):3351-60. DOI: 10.1242/dev.050146. View

Xia L, Ju T, Westmuckett A, An G, Ivanciu L, McDaniel J . Defective angiogenesis and fatal embryonic hemorrhage in mice lacking core 1-derived O-glycans. J Cell Biol. 2004; 164(3):451-9. PMC: 2172228. DOI: 10.1083/jcb.200311112. View

Hanamatsu H, Nishikaze T, Miura N, Piao J, Okada K, Sekiya S . Sialic Acid Linkage Specific Derivatization of Glycosphingolipid Glycans by Ring-Opening Aminolysis of Lactones. Anal Chem. 2018; 90(22):13193-13199. DOI: 10.1021/acs.analchem.8b02775. View

Pinho S, Seruca R, Gartner F, Yamaguchi Y, Gu J, Taniguchi N . Modulation of E-cadherin function and dysfunction by N-glycosylation. Cell Mol Life Sci. 2010; 68(6):1011-20. PMC: 11114786. DOI: 10.1007/s00018-010-0595-0. View

10.

Niwa H, Ogawa K, Shimosato D, Adachi K . A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature. 2009; 460(7251):118-22. DOI: 10.1038/nature08113. View

11.

Shaanan B, Lis H, Sharon N . Structure of a legume lectin with an ordered N-linked carbohydrate in complex with lactose. Science. 1991; 254(5033):862-6. DOI: 10.1126/science.1948067. View

12.

Nichols J, Smith A . Naive and primed pluripotent states. Cell Stem Cell. 2009; 4(6):487-92. DOI: 10.1016/j.stem.2009.05.015. View

13.

Russo D, Capolupo L, Loomba J, Sticco L, DAngelo G . Glycosphingolipid metabolism in cell fate specification. J Cell Sci. 2018; 131(24). DOI: 10.1242/jcs.219204. View

14.

Torres C, Hart G . Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. Evidence for O-linked GlcNAc. J Biol Chem. 1984; 259(5):3308-17. View

15.

Evans M, Kaufman M . Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981; 292(5819):154-6. DOI: 10.1038/292154a0. View

16.

Bennett E, Mandel U, Clausen H, Gerken T, Fritz T, Tabak L . Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology. 2011; 22(6):736-56. PMC: 3409716. DOI: 10.1093/glycob/cwr182. View

17.

Homan K, Hanamatsu H, Furukawa J, Okada K, Yokota I, Onodera T . Alteration of the Total Cellular Glycome during Late Differentiation of Chondrocytes. Int J Mol Sci. 2019; 20(14). PMC: 6678350. DOI: 10.3390/ijms20143546. View

18.

Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M . Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011; 146(4):519-32. DOI: 10.1016/j.cell.2011.06.052. View

19.

Yamamoto M, Suwa Y, Sugiyama K, Okashita N, Kawaguchi M, Tani N . The PRDM14-CtBP1/2-PRC2 complex regulates transcriptional repression during the transition from primed to naïve pluripotency. J Cell Sci. 2020; 133(15). DOI: 10.1242/jcs.240176. View

20.

Hao Y, Fan X, Shi Y, Zhang C, Sun D, Qin K . Next-generation unnatural monosaccharides reveal that ESRRB O-GlcNAcylation regulates pluripotency of mouse embryonic stem cells. Nat Commun. 2019; 10(1):4065. PMC: 6731260. DOI: 10.1038/s41467-019-11942-y. View