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Joyce LR, Manzer HS, da C Mendonca J, Villarreal R, Nagao PE, Doran KS, Palmer KL, Guan Z
Identification of a novel cationic glycolipid in Streptococcus agalactiae that contributes to brain entry and meningitis
PLoS Biology 20(2) (2022)
e3001555
Streptococcus agalactiae A909
(NCBI TaxID 205921,
species name lookup)
Streptococcus agalactiae CNCTC 10/84
(NCBI TaxID 1427374,
species name lookup)
Streptococcus agalactiae CJB111
(Ancestor NCBI TaxID 1311,
species name lookup)
Taxonomic group: bacteria / Firmicutes
(Phylum: Firmicutes)
Associated disease: infection due to Streptococcus agalactiae [ICD11:
XN0KC 
]
The structure was elucidated in this paperNCBI PubMed ID: 35180210Publication DOI: 10.1371/journal.pbio.3001555Journal NLM ID: 101183755Publisher: San Francisco, CA: Public Library of Science
Correspondence: K.S. Doran <Kelly.Doran
CUAnschutz.edu>; K.L. PalmerI <Kelli.Palmer
UTDallas.edu>; Z. Guan <Ziqiang.Guan
Duke.edu>
Institutions: Department of Biological Sciences, The University of Texas at Dallas, Richardson, Texas, United States of America, Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, Colorado, United States of America, Rio de Janeiro State University, Roberto Alcantara Gomes Biology Institute, Rio de Janeiro, Rio de Janeiro, Brazil, Department of Biochemistry, Duke University Medical Center, Durham, North Carolina, United States of America
Bacterial membrane lipids are critical for membrane bilayer formation, cell division, protein localization, stress responses, and pathogenesis. Despite their critical roles, membrane lipids have not been fully elucidated for many pathogens. Here, we report the discovery of a novel cationic glycolipid, lysyl-glucosyl-diacylglycerol (Lys-Glc-DAG), which is synthesized in high abundance by the bacterium Streptococcus agalactiae (Group B Streptococcus, GBS). To our knowledge, Lys-Glc-DAG is more positively charged than any other known lipids. Lys-Glc-DAG carries 2 positive net charges per molecule, distinct from the widely described lysylated phospholipid lysyl-phosphatidylglycerol (Lys-PG) that carries one positive net charge due to the presence of a negatively charged phosphate moiety. We use normal phase liquid chromatography (NPLC) coupled with electrospray ionization (ESI) high-resolution tandem mass spectrometry (HRMS/MS) and genetic approaches to determine that Lys-Glc-DAG is synthesized by the enzyme MprF in GBS, which covalently modifies the neutral glycolipid Glc-DAG with the cationic amino acid lysine. GBS is a leading cause of neonatal meningitis, which requires traversal of the endothelial blood-brain barrier (BBB). We demonstrate that GBS strains lacking mprF exhibit a significant decrease in the ability to invade BBB endothelial cells. Further, mice challenged with a GBS?mprF mutant developed bacteremia comparably to wild-type (WT) infected mice yet had less recovered bacteria from brain tissue and a lower incidence of meningitis. Thus, our data suggest that Lys-Glc-DAG may contribute to bacterial uptake into host cells and disease progression. Importantly, our discovery provides a platform for further study of cationic lipids at the host-pathogen interface.
group B Streptococcus, mass spectrometry, Streptococcus agalactiae, lipids, cationic glycolipid
Structure type: monomer ; 884.670
C
49H
92N
2O
11Location inside paper: Fig. 1F, Lys-Glc-DAG
Compound class: glycolipid
Contained glycoepitopes: IEDB_136017,IEDB_141181,IEDB_142488,IEDB_144998,IEDB_146664,IEDB_983931,SB_192
Methods: PCR, DNA techniques, ELISA, MS/MS, radiolabeling, genetic methods, HPLC, LC-ESI-MS, molecular biology techniques, extractions, TIC, hCMEC cell adherence assays, animal experiments, histology
Enzymes that release or process the structure: MprF
Comments, role: Streptococcus agalactiae (Group B Streptococcus, GBS); proposed structure of the lipid
NCBI Taxonomy refs (TaxIDs): 205921,
1427374,
1311
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There is only one chemically distinct structure:
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Lee C, Verma R, Byun S, Jeun E-J, Kim G-C, Lee S, Kang H-J, Kim CJ, Sharma G, Lahiri A, Paul S, Kim KS, Hwang DS, Iwakura Y, Speciale I, Molinaro A, De Castro C, Rudra D, Im S-H
Structural specificities of cell surface β-glucan polysaccharides determine commensal yeast mediated immuno-modulatory activities
Nature Communications 12(1) (2021)
ID 3611
|
a-D-Manp-(1-3)-a-D-Manp-(1-2)-a-D-Manp-(1-2)-+
|
a-D-Manp-(1-2)-a-D-Manp-(1-2)-+ |
| |
a-D-Manp-(1-2)-+ | |
| | |
-6)-a-D-Manp-(1-6)-a-D-Manp-(1-6)-a-D-Manp-(1-6)-a-D-Manp-(1- |
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(fungi)
(NCBI TaxID 4751,
species name lookup)
Taxonomic group: fungi /
NCBI PubMed ID: 34127673Publication DOI: 10.1038/s41467-021-23929-9Journal NLM ID: 101528555Publisher: London: Nature Publishing Group
Correspondence: Rudra D <rudrad
postech.ac.kr>; Im S-H <iimsh
postech.ac.kr>
Institutions: Department of Chemical Sciences, University of Napoli, Napoli, Italy, Task Force on Microbiome Studies, University of Naples Federico II, Naples, Italy, Division of Integrative Biosciences and Biotechnology, Department of Life Sciences, Pohang University of Science and Technology (POSTECH), Pohang, South Korea, Department of Microbiology and Immunology, Yonsei University College of Medicine, Seoul, South Korea, Advanced convergence, Handong Global University, Pohang, South Korea, HEM, Pohang, South Korea, Division of Structural Biology and Bioinformatics, CSIR-Indian Institute of Chemical Biology, Kolkata, India, Division of Environmental Science and Engineering, Pohang University of Science and Technology (POSTECH), Pohang, South Korea, Center for Animal Disease Models, Research Institute for Biomedical Sciences, Tokyo University of Science, Noda-shi, Japan, Center for Experimental Medicine and Systems Biology, Institute of Medical Science, the University of Tokyo, Tokyo, Japan, Department of Agricultural Sciences, University of Napoli, Portici, Italy
Yeast is an integral part of mammalian microbiome, and like commensal bacteria, has the potential of being harnessed to influence immunity in clinical settings. However, functional specificities of yeast-derived immunoregulatory molecules remain elusive. Here we find that while under steady state, β-1,3-glucan-containing polysaccharides potentiate pro-inflammatory properties, a relatively less abundant class of cell surface polysaccharides, dubbed mannan/β-1,6-glucan-containing polysaccharides (MGCP), is capable of exerting potent anti-inflammatory effects to the immune system. MGCP, in contrast to previously identified microbial cell surface polysaccharides, through a Dectin1-Cox2 signaling axis in dendritic cells, facilitates regulatory T (Treg) cell induction from naïve T cells. Furthermore, through a TLR2-dependent mechanism, it restrains Th1 differentiation of effector T cells by suppressing IFN-γ expression. As a result, administration of MGCP display robust suppressive capacity towards experimental inflammatory disease models of colitis and experimental autoimmune encephalomyelitis (EAE) in mice, thereby highlighting its potential therapeutic utility against clinically relevant autoimmune diseases.
polysaccharides, medicine, immunity, β-glucan, yeast
Structure type: structural motif or average structure
Location inside paper: Fig. 2, b
Compound class: polysaccharide, mannan
Contained glycoepitopes: IEDB_130701,IEDB_136104,IEDB_140116,IEDB_141111,IEDB_141793,IEDB_141828,IEDB_141829,IEDB_141830,IEDB_141831,IEDB_141832,IEDB_143632,IEDB_144983,IEDB_152206,IEDB_153220,IEDB_153762,IEDB_153763,IEDB_164174,IEDB_164175,IEDB_164176,IEDB_174840,IEDB_76933,IEDB_857732,IEDB_857735,IEDB_983930,SB_136,SB_191,SB_196,SB_197,SB_198,SB_44,SB_67,SB_72
Methods: 13C NMR, 1H NMR, NMR-2D, methylation, GC-MS, biological assays, HPLC, enzymatic digestion, extraction, EI-MS, acetylation, SEC, reduction, dialysis, RNA sequencing, flow cytometry analysis, RNA extraction, phenol-sulfuric acid assay, centrifugation, qRT-PCR, histology
Related record ID(s): 40996
NCBI Taxonomy refs (TaxIDs): 4751
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There is only one chemically distinct structure:
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Lee C, Verma R, Byun S, Jeun E-J, Kim G-C, Lee S, Kang H-J, Kim CJ, Sharma G, Lahiri A, Paul S, Kim KS, Hwang DS, Iwakura Y, Speciale I, Molinaro A, De Castro C, Rudra D, Im S-H
Structural specificities of cell surface β-glucan polysaccharides determine commensal yeast mediated immuno-modulatory activities
Nature Communications 12(1) (2021)
ID 3611
(fungi)
(NCBI TaxID 4751,
species name lookup)
Taxonomic group: fungi /
NCBI PubMed ID: 34127673Publication DOI: 10.1038/s41467-021-23929-9Journal NLM ID: 101528555Publisher: London: Nature Publishing Group
Correspondence: Rudra D <rudrad
postech.ac.kr>; Im S-H <iimsh
postech.ac.kr>
Institutions: Department of Chemical Sciences, University of Napoli, Napoli, Italy, Task Force on Microbiome Studies, University of Naples Federico II, Naples, Italy, Division of Integrative Biosciences and Biotechnology, Department of Life Sciences, Pohang University of Science and Technology (POSTECH), Pohang, South Korea, Department of Microbiology and Immunology, Yonsei University College of Medicine, Seoul, South Korea, Advanced convergence, Handong Global University, Pohang, South Korea, HEM, Pohang, South Korea, Division of Structural Biology and Bioinformatics, CSIR-Indian Institute of Chemical Biology, Kolkata, India, Division of Environmental Science and Engineering, Pohang University of Science and Technology (POSTECH), Pohang, South Korea, Center for Animal Disease Models, Research Institute for Biomedical Sciences, Tokyo University of Science, Noda-shi, Japan, Center for Experimental Medicine and Systems Biology, Institute of Medical Science, the University of Tokyo, Tokyo, Japan, Department of Agricultural Sciences, University of Napoli, Portici, Italy
Yeast is an integral part of mammalian microbiome, and like commensal bacteria, has the potential of being harnessed to influence immunity in clinical settings. However, functional specificities of yeast-derived immunoregulatory molecules remain elusive. Here we find that while under steady state, β-1,3-glucan-containing polysaccharides potentiate pro-inflammatory properties, a relatively less abundant class of cell surface polysaccharides, dubbed mannan/β-1,6-glucan-containing polysaccharides (MGCP), is capable of exerting potent anti-inflammatory effects to the immune system. MGCP, in contrast to previously identified microbial cell surface polysaccharides, through a Dectin1-Cox2 signaling axis in dendritic cells, facilitates regulatory T (Treg) cell induction from naïve T cells. Furthermore, through a TLR2-dependent mechanism, it restrains Th1 differentiation of effector T cells by suppressing IFN-γ expression. As a result, administration of MGCP display robust suppressive capacity towards experimental inflammatory disease models of colitis and experimental autoimmune encephalomyelitis (EAE) in mice, thereby highlighting its potential therapeutic utility against clinically relevant autoimmune diseases.
polysaccharides, medicine, immunity, β-glucan, yeast
Structure type: structural motif or average structure
Location inside paper: Fig. 2, c
Compound class: glucan, polysaccharide
Contained glycoepitopes: IEDB_135614,IEDB_141806,IEDB_142488,IEDB_146664,IEDB_153543,IEDB_241101,IEDB_983931,SB_192
Methods: 13C NMR, 1H NMR, NMR-2D, methylation, GC-MS, biological assays, HPLC, enzymatic digestion, extraction, EI-MS, acetylation, SEC, reduction, dialysis, RNA sequencing, flow cytometry analysis, RNA extraction, phenol-sulfuric acid assay, centrifugation, qRT-PCR, histology
Related record ID(s): 40995
NCBI Taxonomy refs (TaxIDs): 4751
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