Fluorescent GD2 analog for single-molecule imaging.

Single Molecule Imaging Gangliosides / metabolism Cell Membrane / metabolism Membrane Microdomains / metabolism
GD2 Ganglioside Lipid raft Single-molecule imaging

Journal

Glycoconjugate journal
ISSN: 1573-4986
Titre abrégé: Glycoconj J
Pays: United States
ID NLM: 8603310

Informations de publication

Date de publication:
04 2023
Historique:
received: 30 11 2022
accepted: 13 01 2023
revised: 06 01 2023
pubmed: 27 1 2023
medline: 23 3 2023
entrez: 26 1 2023
Statut: ppublish

Résumé

Ganglioside GD2 is associated with the proliferation and migration of breast cancer cells. However, the precise role of GD2 is unclear because its tendency to form dynamic and transient domains in cell plasma membranes (PMs), called lipid rafts, makes it difficult to observe. Previously, we developed fluorescent analogs of gangliosides (e.g., GM3 and GM1), which enabled the observation of lipid raft formation for the first time using single-molecule imaging. In this report, we describe the first chemical synthesis of a fluorescent ganglioside, GD2. A biophysical analysis of the synthesized analog revealed its raft-philic character, suggesting its potential to aid single-molecule imaging-based investigations into raft-associated interactions.

Identifiants

DOI: 10.1007/s10719-023-10102-1 PMID: 36701103
pubmed: 36701103
doi: 10.1007/s10719-023-10102-1
pii: 10.1007/s10719-023-10102-1
doi:

Substances chimiques

ganglioside, GD2 65988-71-8
Gangliosides 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

247-257

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Lopez, P.H., Schnaar, R.L.: Gangliosides in cell recognition and membrane protein regulation. Curr. Opin. Struct. Biol 19, 549–557 (2009). https://doi.org/10.1016/j.sbi.2009.06.001
doi: 10.1016/j.sbi.2009.06.001 pubmed: 19608407 pmcid: 2763983
Haselhorst, T., Fleming, F.E., Dyason, J.C., Hartnell, R.D., Yu, X., Holloway, G., Santegoets, K., Kiefel, M.J., Blanchard, H., Coulson, B.S., von Itzstein, M.: Sialic acid dependence in rotavirus host cell invasion. Nat. Chem. Biol 5, 91–93 (2009). https://doi.org/10.1038/nchembio.134
doi: 10.1038/nchembio.134 pubmed: 19109595
Stencel-Baerenwald, J.E., Reiss, K., Reiter, D.M., Stehle, T., Dermody, T.S.: The sweet spot: defining virus–sialic acid interactions. Nat. Rev. Microbiol 12, 739–749 (2014). https://doi.org/10.1038/nrmicro3346
doi: 10.1038/nrmicro3346 pubmed: 25263223 pmcid: 4791167
Simons, K., Ikonen, E.: Functional rafts in cell membranes. Nature 387, 569–572 (1997). https://doi.org/10.1038/42408
doi: 10.1038/42408 pubmed: 9177342
Simons, K., Gerl, M.J.: Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell. Biol 11, 688–699 (2010). https://doi.org/10.1038/nrm2977
doi: 10.1038/nrm2977 pubmed: 20861879
Suzuki, K.G.N., Kasai, R.S., Hirosawa, K.M., Nemoto, Y.L., Ishibashi, M., Miwa, Y., Fujiwara, T.K., Kusumi, A.: Transient GPI-anchored protein homodimers are units for raft organization and function. Nat. Chem. Biol 8, 774–783 (2012). https://doi.org/10.1038/nchembio.1028
doi: 10.1038/nchembio.1028 pubmed: 22820419
Komura, N., Suzuki, K.G.N., Ando, H., Konishi, M., Koikeda, M., Imamura, A., Chadda, R., Fujiwara, T.K., Tsuboi, H., Sheng, R., Cho, W., Furukawa, K., Furukawa, K., Yamauchi, Y., Ishida, H., Kusumi, A., Kiso, M.: Raft-based interactions of gangliosides with a GPI-anchored receptor. Nat. Chem. Biol 12, 402–410 (2016). https://doi.org/10.1038/nchembio.2059
doi: 10.1038/nchembio.2059 pubmed: 27043189
Konishi, M., Komura, N., Hirose, Y., Suganuma, Y., Tanaka, H.-N., Imamura, A., Ishida, H., Suzuki, K.G.N., Ando, H.: Development of fluorescent ganglioside GD3 and GQ1b analogs for elucidation of raft-associated interactions. J. Org. Chem 85, 15998–16013 (2020). https://doi.org/10.1021/acs.joc.0c01493
doi: 10.1021/acs.joc.0c01493 pubmed: 32951428
Takahashi, M., Komura, N., Yoshida, Y., Yamaguchi, E., Hasegawa, A., Tanaka, H.-N., Imamura, A., Ishida, H., Suzuki, K.G.N., Ando, H.: Development of lacto-series ganglioside fluorescent probe using late-stage sialylation and behavior analysis with single-molecule imaging. RSC Chem. Biol 3, 868–885 (2022). https://doi.org/10.1039/D2CB00083K
doi: 10.1039/D2CB00083K pubmed: 35866169 pmcid: 9257605
Battula, V.L., Shi, Y., Evans, K.W., Wang, R.Y., Spaeth, E.L., Jacamo, R.O., Guerra, R., Sahin, A.A., Marini, F.C., Hortobagyi, G., Mani, S.A., Andreeff, M.: Ganglioside GD2 identifies breast cancer stem cells and promotes tumorigenesis. J. Clin. Invest 122, 2066–2078 (2012). https://doi.org/10.1172/JCI59735
doi: 10.1172/JCI59735 pubmed: 22585577 pmcid: 3591166
Nazha, B., Inal, C., Owonikoko, T.K.: Disialoganglioside GD2 expression in solid tumors and role as a target for cancer therapy. Front. Oncol 10, 1000 (2020). https://doi.org/10.3389/fonc.2020.01000
doi: 10.3389/fonc.2020.01000 pubmed: 32733795 pmcid: 7358363
Koikeda, M., Komura, N., Tanaka, H.-N., Imamura, A., Ishida, H., Kiso, M., Ando, H.: Synthesis of ganglioside analogs containing fluorescently labeled GalNAc for single-molecule imaging. J. Carbohydr. Chem 38, 509–527 (2019). https://doi.org/10.1080/07328303.2019.1609019
doi: 10.1080/07328303.2019.1609019
Imamura, A., Ando, H., Ishida, H., Kiso, M.: Ganglioside GQ1b: efficient total synthesis and the expansion to synthetic derivatives to elucidate its biological roles. J. Org. Chem 74, 3009–3023 (2009). https://doi.org/10.1021/jo8027888
doi: 10.1021/jo8027888 pubmed: 19296672
Tamai, H., Ando, H., Tanaka, H.-N., Hosoda-Yabe, R., Yabe, T., Ishida, H., Kiso, M.: The total synthesis of the neurogenic ganglioside LLG-3 isolated from the starfish Linckia laevigata Angew Chem. Int. Ed 50, 2330–2333 (2011). https://doi.org/10.1002/anie.201006035
doi: 10.1002/anie.201006035
Nakashima, S., Ando, H., Saito, R., Tamai, H., Ishida, H., Kiso, M.: Efficiently synthesizing lacto-ganglio-series gangliosides by using a glucosyl ceramide cassette approach: the total synthesis of ganglioside X2. Chem Asian J 7, 1041–1051 (2012). https://doi.org/10.1002/asia.201100928
doi: 10.1002/asia.201100928 pubmed: 22334413
Asano, S., Tanaka, H.-N., Imamura, A., Ishida, H., Ando, H.: p-tert-butyl groups improve the utility of aromatic protecting groups in carbohydrate synthesis. Org. Lett. 21, 4197–4200 (2019). https://doi.org/10.1021/acs.orglett.9b01372
doi: 10.1021/acs.orglett.9b01372 pubmed: 31145627
Ishida, H., Ohta, Y., Tsukada, Y., Kiso, M., Hasegawa, A.: A synthetic approach to polysialogangliosides containing α-sialyl-(2→8)-sialic acid: total synthesis of ganglioside GD3. Carbohydr. Res 246, 75–88 (1993). https://doi.org/10.1016/0008-6215(93)84025-2
doi: 10.1016/0008-6215(93)84025-2 pubmed: 8370046
Kenworthy, A.K., Nichols, B.J., Remmert, C.L., Hendirix, G.M., Kumar, M., Zimmerberg, J., Lippincott-Schwartz, J.: Dynamics of putative raft-associated proteins at the cell surface. J. Cell. Biol 165, 735–746 (2004). https://doi.org/10.1083/jcb.200312170
doi: 10.1083/jcb.200312170 pubmed: 15173190 pmcid: 2172371
Asano, S., Pal, R., Tanaka, H.-N., Imamura, A., Ishida, H., Suzuki, K.G.N., Ando, H.: Development of fluorescently labeled SSEA-3, SSEA-4, and Globo-H glycosphingolipids for elucidating molecular interactions in the cell membrane. Int. J. Mol. Sci 20, 6187 (2019). https://doi.org/10.3390/ijms20246187
doi: 10.3390/ijms20246187 pubmed: 31817926 pmcid: 6941013
Tanaka, K.A.K., Suzuki, K.G.N., Shirai, Y.M., Shibutani, S.T., Miyahara, M.S.H., Tsuboi, H., Yahara, M., Yoshimura, A., Mayor, S., Fujiwara, T.K., Kusumi, A.: Membrane molecules mobile even after chemical fixation. Nat. Methods 7, 865–866 (2010). https://doi.org/10.1038/nmeth.f.314
doi: 10.1038/nmeth.f.314 pubmed: 20881966

Auteurs

Eriko Yamaguchi (E)

Institute for Glyco-core Research (iGCORE), Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan.

Naoko Komura (N)

Institute for Glyco-core Research (iGCORE), Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan. komura@gifu-u.ac.jp.

Hide-Nori Tanaka (HN)

Institute for Glyco-core Research (iGCORE), Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan.

Akihiro Imamura (A)

Institute for Glyco-core Research (iGCORE), Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan.
Department of Applied Bioorganic Chemistry, Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan.

Hideharu Ishida (H)

Institute for Glyco-core Research (iGCORE), Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan.
Department of Applied Bioorganic Chemistry, Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan.

Sophie Groux-Degroote (S)

UMR 8576-UGSF-Unité de Glycobiologie Structurale et Fonctionnelle, CNRS, Université de Lille, F-59000, Lille, France.

Martina Mühlenhoff (M)

Institute of Clinical Biochemistry, Hannover Medical School, 30623, Hannover, Germany.

Kenichi G N Suzuki (KGN)

Institute for Glyco-core Research (iGCORE), Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan. kgsuzuki@gifu-u.ac.jp.

Hiromune Ando (H)

Institute for Glyco-core Research (iGCORE), Gifu University, 1-1 Yanagido, 501-1193, Gifu, Japan. hando@gifu-u.ac.jp.

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Classifications MeSH

questionsmedicales.fr › Techniques d'investigation › Techniques de sonde moléculaire › Imagerie moléculaire › Imagerie de molécules uniques › Fluorescent GD2 analog for single-molecule imaging.
questionsmedicales.fr › Lipides › Lipides membranaires › Sphingolipides › Glycosphingolipides › Glycosphingolipides acides › Gangliosides › Fluorescent GD2 analog for single-molecule imaging.
questionsmedicales.fr › Cellules › Structures cellulaires › Membrane cellulaire › Fluorescent GD2 analog for single-molecule imaging.
questionsmedicales.fr › Cellules › Structures cellulaires › Membrane cellulaire › Structures de la membrane cellulaire › Microdomaines membranaires › Fluorescent GD2 analog for single-molecule imaging.