Deciphering mouse brain spatial diversity via glyco-lipidomic mapping.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
07 Oct 2024
07 Oct 2024
Historique:
received:
07
04
2024
accepted:
30
09
2024
medline:
8
10
2024
pubmed:
8
10
2024
entrez:
7
10
2024
Statut:
epublish
Résumé
Gangliosides in the brain play a crucial role in modulating the integrity of vertebrate central nervous system in a region-specific manner. However, to date, a comprehensive structural elucidation of complex intact ganglioside isomers has not been achieved, resulting in the elusiveness into related molecular mechanism. Here, we present a glycolipidomic approach for isomer-specific and brain region-specific profiling of the mouse brain. Considerable region-specificity and commonality in specific group of regions are highlighted. Notably, we observe a similarity in the abundance of major isomers, GD1a and GD1b, within certain regions, which provides significant biological implications with interpretation through the lens of a theoretical retrosynthetic state-transition network. Furthermore, A glycocentric-omics approaches using gangliosides and N-glycans reveal a remarkable convergence in spatial dynamics, providing valuable insight into molecular interaction network. Collectively, this study uncovers the spatial dynamics of intact glyco-conjugates in the brain, which are relevant to regional function and accelerates the discovery of potential therapeutic targets for brain diseases.
Identifiants
pubmed: 39375371
doi: 10.1038/s41467-024-53032-8
pii: 10.1038/s41467-024-53032-8
doi:
Substances chimiques
Gangliosides
0
Polysaccharides
0
ganglioside, GD1a
12707-58-3
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8689Informations de copyright
© 2024. The Author(s).
Références
Mlinac, K. et al. Structural analysis of brain ganglioside acetylation patterns in mice with altered ganglioside biosynthesis. Carbohydr. Res. 382, 1–8 (2013).
doi: 10.1016/j.carres.2013.09.007
Ariga, T. & McDonald, M. P. Robert KY. Thematic review series: sphingolipids. Role of ganglioside metabolism in the pathogenesis of Alzheimer’s disease—a review. J. Lipid Res. 49, 1157–1175 (2008).
doi: 10.1194/jlr.R800007-JLR200
Svennerholm L. Gangliosides and synaptic transmission. In: Structure and function of gangliosides. Springer (1980).
Mocchetti, I. Exogenous gangliosides, neuronal plasticity and repair, and the neurotrophins. Cell Mol. Life Sci. 62, 2283–2294 (2005).
doi: 10.1007/s00018-005-5188-y
She, J. Q., Wang, M., Zhu, D. M., Sun, L. G. & Ruan, D. Y. Effect of ganglioside on synaptic plasticity of hippocampus in lead-exposed rats in vivo. Brain Res. 1060, 162–169 (2005).
doi: 10.1016/j.brainres.2005.08.044
Palmano, K., Rowan, A., Guillermo, R., Guan, J. & McJarrow, P. The role of gangliosides in neurodevelopment. Nutrients 7, 3891–3913 (2015).
doi: 10.3390/nu7053891
Sugiura, Y. et al. Sensory nerve-dominant nerve degeneration and remodeling in the mutant mice lacking complex gangliosides. Neuroscience 135, 1167–1178 (2005).
doi: 10.1016/j.neuroscience.2005.07.035
Sántha, P., Dobos, I., Kis, G. & Jancsó, G. Role of gangliosides in peripheral pain mechanisms. Int. J. Mol. Sci. 21, 1005 (2020).
doi: 10.3390/ijms21031005
Ariga, T. The pathogenic role of ganglioside metabolism in Alzheimer’s disease-cholinergic neuron-specific gangliosides and neurogenesis. Mol. Neurobiol. 54, 623–638 (2017).
doi: 10.1007/s12035-015-9641-0
Rahmann, H. Brain gangliosides and memory formation. Behav. Brain Res. 66, 105–116 (1995).
doi: 10.1016/0166-4328(94)00131-X
Yoon, J. H. et al. Brain lipidomics: from functional landscape to clinical significance. Sci. Adv. 8, eadc9317 (2022).
doi: 10.1126/sciadv.adc9317
Schneider J. Gangliosides and glycolipids in neurodegenerative disorders. In: Glycobiology of the Nervous System. Springer (2014).
Ariga, T. Pathogenic role of ganglioside metabolism in neurodegenerative diseases. J. Neurosci. Res. 92, 1227–1242 (2014).
doi: 10.1002/jnr.23411
Han, X., MH, D., McKeel, D. W. Jr., Kelley, J. & Morris, J. C. Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer’s disease: potential role in disease pathogenesis. J. Neurochem. 82, 809–818 (2002).
doi: 10.1046/j.1471-4159.2002.00997.x
Mabe, N. W. et al. Transition to a mesenchymal state in neuroblastoma confers resistance to anti-GD2 antibody via reduced expression of ST8SIA1. Nat. Cancer 3, 976–993 (2022).
doi: 10.1038/s43018-022-00405-x
Huebecker, M. et al. Reduced sphingolipid hydrolase activities, substrate accumulation and ganglioside decline in Parkinson’s disease. Mol. Neurodegener. 14, 40 (2019).
doi: 10.1186/s13024-019-0339-z
Kracun, I., Kalanj, S., Talan-Hranilovic, J. & Cosovic, C. Cortical distribution of gangliosides in Alzheimer’s disease. Neurochem. Int. 20, 433–438 (1992).
doi: 10.1016/0197-0186(92)90058-Y
Svennerholm, L. & Gottfries, C. G. Membrane-lipids, selectively diminished in Alzheimer brains, suggest synapse loss as a primary event in early-onset form (type-I) and demyelination in late-onset form (type-Ii). J. Neurochem. 62, 1039–1047 (1994).
doi: 10.1046/j.1471-4159.1994.62031039.x
Kalanj, S., Kracun, I., Rosner, H. & Cosovic, C. Regional distribution of brain gangliosides in Alzheimer’s disease. Neurol. Croat. 40, 269–281 (1991).
Jana, A. & Pahan, K. Sphingolipids in multiple sclerosis. Neuromol. Med. 12, 351–361 (2010).
doi: 10.1007/s12017-010-8128-4
Lee, J. et al. Spatial and temporal diversity of glycome expression in mammalian brain. Proc. Natl. Acad. Sci. USA 117, 28743–28753 (2020).
doi: 10.1073/pnas.2014207117
Sharma, K. et al. Cell type- and brain region-resolved mouse brain proteome. Nat. Neurosci. 18, 1819–1831 (2015).
doi: 10.1038/nn.4160
Ivanisevic, J. et al. Brain region mapping using global metabolomics. Chem. Biol. 21, 1575–1584 (2014).
doi: 10.1016/j.chembiol.2014.09.016
Hawrylycz, M. J. et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489, 391–399 (2012).
doi: 10.1038/nature11405
Ng, L. et al. An anatomic gene expression atlas of the adult mouse brain. Nat. Neurosci. 12, 356–362 (2009).
doi: 10.1038/nn.2281
Lee, B. & An, H. J. Small but big leaps towards neuroglycomics: exploring N-glycome in the brain to advance the understanding of brain development and function. Neural Regen. Res. 19, 489–490 (2023).
De Baecque, C., Johnson, A. B., Naiki, M., Schwarting, G. & Marcus, D. M. Ganglioside localization in cerebellar cortex: an immunoperoxidase study with antibody to GM1 ganglioside. Brain Res. 114, 117–122 (1976).
doi: 10.1016/0006-8993(76)91011-8
Byers, D. M., Irwin, L. N. & Cabeza, R. Ganglioside patterns mature at different rates in functionally related subregions of the rat pons. Dev. Neurosci. 24, 478–484 (2002).
doi: 10.1159/000069358
Laev, H., Rapport, M. M., Mahadik, S. P. & Silverman, A.-J. Immunohistological localization of ganglioside in rat cerebellum. Brain Res. 157, 136–141 (1978).
doi: 10.1016/0006-8993(78)91002-8
Molander, M., Berthold, C. H., Persson, H. & Fredman, P. Immunostaining of ganglioside GD1b, GD3 and GM1 in rat cerebellum: cellular layer and cell type specific associations. J. Neurosci. Res. 60, 531–542 (2000).
doi: 10.1002/(SICI)1097-4547(20000515)60:4<531::AID-JNR12>3.0.CO;2-6
Goto-Inoue, N. et al. The detection of glycosphingolipids in brain tissue sections by imaging mass spectrometry using gold nanoparticles. J. Am. Soc. Mass Spectrom. 21, 1940–1943 (2010).
doi: 10.1016/j.jasms.2010.08.002
Colsch, B. & Woods, A. S. Localization and imaging of sialylated glycosphingolipids in brain tissue sections by MALDI mass spectrometry. Glycobiology 20, 661–667 (2010).
doi: 10.1093/glycob/cwq031
Li, Z. & Zhang, Q. Ganglioside isomer analysis using ion polarity switching liquid chromatography-tandem mass spectrometry. Anal. Bioanal. Chem. 413, 3269–3279 (2021).
doi: 10.1007/s00216-021-03262-2
Wojcik, R. et al. Lipid and glycolipid isomer analyses using ultra-high resolution ion mobility spectrometry separations. Int. J. Mol. Sci. 18, 183 (2017).
doi: 10.3390/ijms18010183
Hu, T., Jia, Z. X. & Zhang, J. L. Strategy for comprehensive profiling and identification of acidic glycosphingolipids using ultra-high-performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry. Anal. Chem. 89, 7808–7816 (2017).
doi: 10.1021/acs.analchem.7b02023
Kirschbaum, C. et al. Unravelling the structural complexity of glycolipids with cryogenic infrared spectroscopy. Nat. Commun. 12, 1–7 (2021).
doi: 10.1038/s41467-021-21480-1
Lee, J. et al. Comprehensive profiling of surface gangliosides extracted from various cell lines by LC-MS/MS. Cells 8, 1323 (2019).
doi: 10.3390/cells8111323
Sturgill, E. R. et al. Biosynthesis of the major brain gangliosides GD1a and GT1b. Glycobiology 22, 1289–1301 (2012).
doi: 10.1093/glycob/cws103
Vajn, K., Viljetic, B., Degmecic, I. V., Schnaar, R. L. & Heffer, M. Differential distribution of major brain gangliosides in the adult mouse central nervous system. Plos One 8, e75720 (2013).
doi: 10.1371/journal.pone.0075720
Kohla, G., Stockfleth, E. & Schauer, R. Gangliosides with O-acetylated sialic acids in tumors of neuroectodermal origin. Neurochem. Res. 27, 583–592 (2002).
doi: 10.1023/A:1020211714104
Mandal, C., Schwartz-Albiez, R. & Vlasak, R. Functions and biosynthesis of O-acetylated sialic acids. Top. Curr. Chem. 366, 1–30 (2012).
doi: 10.1007/128_2011_310
Siebert, H.-C. et al. Molecular dynamics-derived conformation and intramolecular interaction analysis of the N-acetyl-9-O-acetylneuraminic acid-containing ganglioside GD1a and NMR-based analysis of its binding to a human polyclonal inununoglobulin G fraction with selectivity for O-acetylated sialic acids. Glycobiology 6, 561–571 (1996).
doi: 10.1093/glycob/6.6.561-b
Varki, N. M. & Varki, A. Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab. Invest. 87, 851–857 (2007).
doi: 10.1038/labinvest.3700656
Hájek, R., Jirásko, R., Lísa, M., Cifková, E. & Holcapek, M. Hydrophilic interaction liquid chromatography-mass spectrometry characterization of gangliosides in biological samples. Anal. Chem. 89, 12425–12432 (2017).
doi: 10.1021/acs.analchem.7b03523
Todeschini, A. R. & Hakomori, S. I. Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochem. Biophys. Acta 1780, 421–433 (2008).
doi: 10.1016/j.bbagen.2007.10.008
Itokazu, Y., Wang, J. & Yu, R. K. Gangliosides in nerve cell specification. Prog. Mol. Biol. Transl. 156, 241–263 (2018).
doi: 10.1016/bs.pmbts.2017.12.008
Ngamukote, S., Yanagisawa, M., Ariga, T., Ando, S. & Yu, R. K. Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J. Neurochem. 103, 2327–2341 (2007).
doi: 10.1111/j.1471-4159.2007.04910.x
Kronewitter, S. R. et al. The development of retrosynthetic glycan libraries to profile and classify the human serum N‐linked glycome. Proteomics 9, 2986–2994 (2009).
doi: 10.1002/pmic.200800760
Kolter, T. Ganglioside biochemistry. ISRN Biochem. 2012, 506160 (2012).
doi: 10.5402/2012/506160
Bieberich, E. et al. Regulation of ganglioside biosynthesis by enzyme complex formation of glycosyltransferases. Biochemistry 41, 11479–11487 (2002).
doi: 10.1021/bi0259958
Giraudo, C. G., Daniotti, J. L. & Maccioni, H. J. F. Physical and functional association of glycolipid -acetyl-galactosaminyl and galactosyl transferases in the Golgi apparatus. Proc. Natl. Acad. Sci. USA 98, 1625–1630 (2001).
doi: 10.1073/pnas.98.4.1625
Giraudo, C. G. & Maccioni, H. J. Ganglioside glycosyltransferases organize in distinct multienzyme complexes in CHO-K1 cells. J. Biol. Chem. 278, 40262–40271 (2003).
doi: 10.1074/jbc.M305455200
Bieberich E. Synthesis, processing, and function of N-glycans in N-glycoproteins. In: Glycobiology of the nervous system. Springer (2014).
Bieberich, E., Freischutz, B., Liour, S. S. & Yu, R. K. Regulation of ganglioside metabolism by phosphorylation and dephosphorylation. J. Neurochem. 71, 972–979 (1998).
doi: 10.1046/j.1471-4159.1998.71030972.x
Katoh, T. et al. Deficiency of α-glucosidase I alters glycoprotein glycosylation and lifespan in Caenorhabditis elegans. Glycobiology 23, 1142–1151 (2013).
doi: 10.1093/glycob/cwt051
Barone, R. et al. CSF N‐glycan profile reveals sialylation deficiency in a patient with GM2 gangliosidosis presenting as childhood disintegrative disorder. Autism Res. 9, 423–428 (2016).
doi: 10.1002/aur.1541
Lawrence, R. et al. Characterization of glycan substrates accumulating in GM1 Gangliosidosis. Mol. Genet. Metab. Rep. 21, 100524 (2019).
doi: 10.1016/j.ymgmr.2019.100524
Cavender, C. et al. Natural history study of glycan accumulation in large animal models of GM2 gangliosidoses. Plos One 15, e0243006 (2020).
doi: 10.1371/journal.pone.0243006
Hakomori, S. I. Structure and function of glycosphingolipids and sphingolipids: recollections and future trends. Biochim. Biophys. Acta 1780, 325–346 (2008).
doi: 10.1016/j.bbagen.2007.08.015
Veillon, L. et al. Characterization of isomeric glycan structures by LC-MS/MS. Electrophoresis 38, 2100–2114 (2017).
doi: 10.1002/elps.201700042
Ikeda, K. & Taguchi, R. Highly sensitive localization analysis of gangliosides and sulfatides including structural isomers in mouse cerebellum sections by combination of laser microdissection and hydrophilic interaction liquid chromatography/electrospray ionization mass spectrometry with theoretically expanded multiple reaction monitoring. Rapid Commun. Mass Spectrom 24, 2957–2965 (2010).
doi: 10.1002/rcm.4716
Albrecht, S. et al. Comprehensive profiling of glycosphingolipid glycans using a novel broad specificity endoglycoceramidase in a high-throughput workflow. Anal. Chem. 88, 4795–4802 (2016).
doi: 10.1021/acs.analchem.6b00259
Tettamanti G., Ledeen R., Sandhoff K., Nagai Y., Toffano G. Gangliosides and neuronal plasticity. In: Springer Science & Business Media (2013).
Maglione, V. et al. Impaired ganglioside metabolism in Huntington’s disease and neuroprotective role of GM1. J. Neurosci. 30, 4072–4080 (2010).
doi: 10.1523/JNEUROSCI.6348-09.2010
Barrier, L. et al. Genotype-related changes of ganglioside composition in brain regions of transgenic mouse models of Alzheimer’s disease. Neurobiol. Aging 28, 1863–1872 (2007).
doi: 10.1016/j.neurobiolaging.2006.08.002
Schnaar, R. L. & Lopez, P. H. Myelin‐associated glycoprotein and its axonal receptors. J. Neurosci. Res. 87, 3267–3276 (2009).
doi: 10.1002/jnr.21992
Vasques, J. F. et al. Gangliosides in nervous system development, regeneration, and pathologies. Neural Regen. Res. 18, 81–86 (2023).
doi: 10.4103/1673-5374.343890
Thomas, P. D. & Brewer, G. J. Gangliosides and synaptic transmission. Biochim. Biophys. Acta 1031, 277–289 (1990).
doi: 10.1016/0304-4157(90)90013-3
Fujii, S. et al. Effects of the mono-and tetrasialogangliosides GM1 and GQ1b on ATP-induced long-term potentiation in hippocampal CA1 neurons. Glycobiology 12, 339–344 (2002).
doi: 10.1093/glycob/12.5.339
Zhang, Z. et al. Ganglioside GQ1b induces dopamine release through the activation of Pyk2. Mol. Cell. Neurosci. 71, 102–113 (2016).
doi: 10.1016/j.mcn.2015.12.009
Manan H. A., Yahya N., Han P., Hummel T. A systematic review of olfactory-related brain structural changes in patients with congenital or acquired anosmia. Brain Struct. Funct. 227, 177–202 (2022).
Seyfried, T. N., el-Abbadi, M. & Roy, M. L. Ganglioside distribution in murine neural tumors. Mol. Chem. Neuropathol. 17, 147–167 (1992).
doi: 10.1007/BF03159989
Tena, J. et al. Regio-specific N-glycome and N-glycoproteome map of the elderly human brain with and without Alzheimer’s disease. Mol. Cell Proteom. 21, 100427 (2022).
doi: 10.1016/j.mcpro.2022.100427
Frenkel-Pinter, M. et al. Interplay between protein glycosylation pathways in Alzheimer’s disease. Sci. Adv. 3, e1601576 (2017).
doi: 10.1126/sciadv.1601576
Rebelo A. L., Drake R., Marchetti-Deschmann M., Saldova R., Pandit A. Changes in tissue protein N-glycosylation and associated molecular signature occur in the human parkinsonian brain in a region-specific manner. PNAS nexus 3, pgad439 (2022).
Spijker S. Dissection of rodent brain regions. In: Neuroproteomics (ed. Li K. W.). Humana Press (2011).
Folch, J., Lees, M. & Stanley, G. S. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497–509 (1957).
doi: 10.1016/S0021-9258(18)64849-5
Li Q., Xie Y., Wong M., Barboza M., Lebrilla C. B. Comprehensive structural glycomic characterization of the glycocalyxes of cells and tissues. Nat. Protoc. 15, 2668–2704 (2020).