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Article ; Online: Lysosomal storage, impaired autophagy and innate immunity in Gaucher and Parkinson's diseases: insights for drug discovery.

Hull, Alexander / Atilano, Magda L / Gergi, Laith / Kinghorn, Kerri J

Philosophical transactions of the Royal Society of London. Series B, Biological sciences

2024 Volume 379, Issue 1899, Page(s) 20220381

Abstract: Impairment of autophagic-lysosomal pathways is increasingly being implicated in Parkinson's disease (PD). ...

Abstract	Impairment of autophagic-lysosomal pathways is increasingly being implicated in Parkinson's disease (PD).
MeSH term(s)	Animals ; Mice ; Parkinson Disease/drug therapy ; Parkinson Disease/genetics ; Parkinson Disease/metabolism ; Gaucher Disease/drug therapy ; Gaucher Disease/genetics ; Gaucher Disease/metabolism ; Autophagy/genetics ; Lysosomes/genetics ; Lysosomes/metabolism ; Lysosomes/pathology ; Drug Discovery ; Immunity, Innate
Language	English
Publishing date	2024-02-19
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	208382-6
ISSN	1471-2970 ; 0080-4622 ; 0264-3839 ; 0962-8436
ISSN (online)	1471-2970
ISSN	0080-4622 ; 0264-3839 ; 0962-8436
DOI	10.1098/rstb.2022.0381
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Article ; Online: Trametinib ameliorates aging-associated gut pathology in

Ureña, Enric / Xu, Bowen / Regan, Jennifer C / Atilano, Magda L / Minkley, Lucy J / Filer, Danny / Lu, Yu-Xuan / Bolukbasi, Ekin / Khericha, Mobina / Alic, Nazif / Partridge, Linda

Proceedings of the National Academy of Sciences of the United States of America

2024 Volume 121, Issue 4, Page(s) e2311313121

Abstract: Pharmacological therapies are promising interventions to slow down aging and reduce multimorbidity in the elderly. Studies in animal models are the first step toward translation of candidate molecules into human therapies, as they aim to elucidate the ... ...

Abstract	Pharmacological therapies are promising interventions to slow down aging and reduce multimorbidity in the elderly. Studies in animal models are the first step toward translation of candidate molecules into human therapies, as they aim to elucidate the molecular pathways, cellular mechanisms, and tissue pathologies involved in the anti-aging effects. Trametinib, an allosteric inhibitor of MEK within the Ras/MAPK (Ras/Mitogen-Activated Protein Kinase) pathway and currently used as an anti-cancer treatment, emerged as a geroprotector candidate because it extended lifespan in the fruit fly
MeSH term(s)	Animals ; Male ; Humans ; Female ; Aged ; Drosophila ; Drosophila melanogaster/genetics ; Aging/physiology ; Stem Cells/metabolism ; Mammals ; Pyridones ; Pyrimidinones
Chemical Substances	trametinib (33E86K87QN) ; Pyridones ; Pyrimidinones
Language	English
Publishing date	2024-01-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2311313121
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Article ; Online: Autophagic dysfunction and gut microbiota dysbiosis cause chronic immune activation in a Drosophila model of Gaucher disease.

Atilano, Magda L / Hull, Alexander / Romila, Catalina-Andreea / Adams, Mirjam L / Wildfire, Jacob / Ureña, Enric / Dyson, Miranda / Ivan-Castillo-Quan, Jorge / Partridge, Linda / Kinghorn, Kerri J

PLoS genetics

2023 Volume 19, Issue 12, Page(s) e1011063

Abstract: Mutations in the GBA1 gene cause the lysosomal storage disorder Gaucher disease (GD) and are the greatest known genetic risk factors for Parkinson's disease (PD). Communication between the gut and brain and immune dysregulation are increasingly being ... ...

Abstract	Mutations in the GBA1 gene cause the lysosomal storage disorder Gaucher disease (GD) and are the greatest known genetic risk factors for Parkinson's disease (PD). Communication between the gut and brain and immune dysregulation are increasingly being implicated in neurodegenerative disorders such as PD. Here, we show that flies lacking the Gba1b gene, the main fly orthologue of GBA1, display widespread NF-kB signalling activation, including gut inflammation, and brain glial activation. We also demonstrate intestinal autophagic defects, gut dysfunction, and microbiome dysbiosis. Remarkably, modulating the microbiome of Gba1b knockout flies, by raising them under germ-free conditions, partially ameliorates lifespan, locomotor and immune phenotypes. Moreover, we show that modulation of the immune deficiency (IMD) pathway is detrimental to the survival of Gba1 deficient flies. We also reveal that direct stimulation of autophagy by rapamycin treatment achieves similar benefits to germ-free conditions independent of gut bacterial load. Consistent with this, we show that pharmacologically blocking autophagosomal-lysosomal fusion, mimicking the autophagy defects of Gba1 depleted cells, is sufficient to stimulate intestinal immune activation. Overall, our data elucidate a mechanism whereby an altered microbiome, coupled with defects in autophagy, drive chronic activation of NF-kB signaling in a Gba1 loss-of-function model. It also highlights that elimination of the microbiota or stimulation of autophagy to remove immune mediators, rather than prolonged immunosuppression, may represent effective therapeutic avenues for GBA1-associated disorders.
MeSH term(s)	Animals ; Gaucher Disease/genetics ; Gaucher Disease/metabolism ; Glucosylceramidase/genetics ; Drosophila/genetics ; Drosophila/metabolism ; Gastrointestinal Microbiome/genetics ; NF-kappa B/genetics ; Dysbiosis/genetics ; Parkinson Disease/genetics ; Autophagy/genetics
Chemical Substances	Glucosylceramidase (EC 3.2.1.45) ; NF-kappa B
Language	English
Publishing date	2023-12-21
Publishing country	United States
Document type	Journal Article
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1011063
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Article ; Online: Protein retention in the endoplasmic reticulum rescues Aβ toxicity in Drosophila.

Catterson, James H / Minkley, Lucy / Aspe, Salomé / Judd-Mole, Sebastian / Moura, Sofia / Dyson, Miranda C / Rajasingam, Arjunan / Woodling, Nathaniel S / Atilano, Magda L / Ahmad, Mumtaz / Durrant, Claire S / Spires-Jones, Tara L / Partridge, Linda

Neurobiology of aging

2023 Volume 132, Page(s) 154–174

Abstract: Amyloid β (Aβ) accumulation is a hallmark of Alzheimer's disease. In adult Drosophila brains, human Aβ overexpression harms climbing and lifespan. It's uncertain whether Aβ is intrinsically toxic or activates downstream neurodegeneration pathways. Our ... ...

Abstract	Amyloid β (Aβ) accumulation is a hallmark of Alzheimer's disease. In adult Drosophila brains, human Aβ overexpression harms climbing and lifespan. It's uncertain whether Aβ is intrinsically toxic or activates downstream neurodegeneration pathways. Our study uncovers a novel protective role against Aβ toxicity: intra-endoplasmic reticulum (ER) protein accumulation with a focus on laminin and collagen subunits. Despite high Aβ, laminin B1 (LanB1) overexpression robustly counters toxicity, suggesting a potential Aβ resistance mechanism. Other laminin subunits and collagen IV also alleviate Aβ toxicity; combining them with LanB1 augments the effect. Imaging reveals ER retention of LanB1 without altering Aβ secretion. LanB1's rescue function operates independently of the IRE1α/XBP1 ER stress response. ER-targeted GFP overexpression also mitigates Aβ toxicity, highlighting broader ER protein retention advantages. Proof-of-principle tests in murine hippocampal slices using mouse Lamb1 demonstrate ER retention in transduced cells, indicating a conserved mechanism. Though ER protein retention generally harms, it could paradoxically counter neuronal Aβ toxicity, offering a new therapeutic avenue for Alzheimer's disease.
MeSH term(s)	Animals ; Mice ; Humans ; Amyloid beta-Peptides/toxicity ; Amyloid beta-Peptides/metabolism ; Drosophila ; Alzheimer Disease/genetics ; Alzheimer Disease/metabolism ; Endoribonucleases/metabolism ; Laminin/metabolism ; Protein Serine-Threonine Kinases/metabolism ; Endoplasmic Reticulum Stress ; Endoplasmic Reticulum/metabolism ; Collagen/metabolism
Chemical Substances	Amyloid beta-Peptides ; Endoribonucleases (EC 3.1.-) ; Laminin ; Protein Serine-Threonine Kinases (EC 2.7.11.1) ; Collagen (9007-34-5)
Language	English
Publishing date	2023-09-21
Publishing country	United States
Document type	Journal Article
ZDB-ID	604505-4
ISSN	1558-1497 ; 0197-4580
ISSN (online)	1558-1497
ISSN	0197-4580
DOI	10.1016/j.neurobiolaging.2023.09.008
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Article ; Online: A monocarboxylate transporter rescues frontotemporal dementia and Alzheimer's disease models.

Xu, Dongwei / Vincent, Alec / González-Gutiérrez, Andrés / Aleyakpo, Benjamin / Anoar, Sharifah / Giblin, Ashling / Atilano, Magda L / Adams, Mirjam / Shen, Dunxin / Thoeng, Annora / Tsintzas, Elli / Maeland, Marie / Isaacs, Adrian M / Sierralta, Jimena / Niccoli, Teresa

PLoS genetics

2023 Volume 19, Issue 9, Page(s) e1010893

Abstract: Brains are highly metabolically active organs, consuming 20% of a person's energy at resting state. A decline in glucose metabolism is a common feature across a number of neurodegenerative diseases. Another common feature is the progressive accumulation ... ...

Abstract	Brains are highly metabolically active organs, consuming 20% of a person's energy at resting state. A decline in glucose metabolism is a common feature across a number of neurodegenerative diseases. Another common feature is the progressive accumulation of insoluble protein deposits, it's unclear if the two are linked. Glucose metabolism in the brain is highly coupled between neurons and glia, with glucose taken up by glia and metabolised to lactate, which is then shuttled via transporters to neurons, where it is converted back to pyruvate and fed into the TCA cycle for ATP production. Monocarboxylates are also involved in signalling, and play broad ranging roles in brain homeostasis and metabolic reprogramming. However, the role of monocarboxylates in dementia has not been tested. Here, we find that increasing pyruvate import in Drosophila neurons by over-expression of the transporter bumpel, leads to a rescue of lifespan and behavioural phenotypes in fly models of both frontotemporal dementia and Alzheimer's disease. The rescue is linked to a clearance of late stage autolysosomes, leading to degradation of toxic peptides associated with disease. We propose upregulation of pyruvate import into neurons as potentially a broad-scope therapeutic approach to increase neuronal autophagy, which could be beneficial for multiple dementias.
MeSH term(s)	Humans ; Animals ; Frontotemporal Dementia/genetics ; Alzheimer Disease/genetics ; Neuroglia ; Pyruvic Acid ; Drosophila ; Glucose
Chemical Substances	Pyruvic Acid (8558G7RUTR) ; Glucose (IY9XDZ35W2)
Language	English
Publishing date	2023-09-21
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1010893
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Article ; Online: MicroRNAs That Contribute to Coordinating the Immune Response in

Atilano, Magda L / Glittenberg, Marcus / Monteiro, Annabel / Copley, Richard R / Ligoxygakis, Petros

Genetics

2017 Volume 207, Issue 1, Page(s) 163–178

Abstract: Small noncoding RNAs called microRNAs (miRNAs) have emerged as post-transcriptional regulators of gene expression related to host defenses. Here, we have ... ...

Abstract	Small noncoding RNAs called microRNAs (miRNAs) have emerged as post-transcriptional regulators of gene expression related to host defenses. Here, we have used
MeSH term(s)	Animals ; Candida albicans/pathogenicity ; Candidiasis/immunology ; DNA-Binding Proteins/genetics ; DNA-Binding Proteins/metabolism ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Drosophila melanogaster/genetics ; Drosophila melanogaster/immunology ; Drosophila melanogaster/microbiology ; Immunity, Innate/genetics ; MicroRNAs/genetics ; Signal Transduction ; Transcription Factors/genetics ; Transcription Factors/metabolism
Chemical Substances	DNA-Binding Proteins ; Dif protein, Drosophila ; Drosophila Proteins ; MicroRNAs ; Transcription Factors ; DRS protein, Drosophila (159522-55-1)
Language	English
Publishing date	2017-07-13
Publishing country	United States
Document type	Journal Article
ZDB-ID	2167-2
ISSN	1943-2631 ; 0016-6731
ISSN (online)	1943-2631
ISSN	0016-6731
DOI	10.1534/genetics.116.196584
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Article ; Online: Enhanced insulin signalling ameliorates C9orf72 hexanucleotide repeat expansion toxicity in

Atilano, Magda L / Grönke, Sebastian / Niccoli, Teresa / Kempthorne, Liam / Hahn, Oliver / Morón-Oset, Javier / Hendrich, Oliver / Dyson, Miranda / Adams, Mirjam Lisette / Hull, Alexander / Salcher-Konrad, Marie-Therese / Monaghan, Amy / Bictash, Magda / Glaria, Idoia / Isaacs, Adrian M / Partridge, Linda

eLife

2021 Volume 10

Abstract: G4C2 repeat expansions within ... ...

Abstract	G4C2 repeat expansions within the
MeSH term(s)	Amyotrophic Lateral Sclerosis/genetics ; Animals ; C9orf72 Protein/genetics ; C9orf72 Protein/toxicity ; DNA Repeat Expansion ; Drosophila melanogaster/physiology ; Female ; Frontotemporal Dementia/genetics ; Insulin/physiology ; Signal Transduction
Chemical Substances	C9orf72 Protein ; Insulin
Language	English
Publishing date	2021-03-19
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.58565
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Article ; Online: L-Rhamnosylation of Listeria monocytogenes Wall Teichoic Acids Promotes Resistance to Antimicrobial Peptides by Delaying Interaction with the Membrane.

Carvalho, Filipe / Atilano, Magda L / Pombinho, Rita / Covas, Gonçalo / Gallo, Richard L / Filipe, Sérgio R / Sousa, Sandra / Cabanes, Didier

PLoS pathogens

2015 Volume 11, Issue 5, Page(s) e1004919

Abstract: Listeria monocytogenes is an opportunistic Gram-positive bacterial pathogen responsible for listeriosis, a human foodborne disease. Its cell wall is densely decorated with wall teichoic acids (WTAs), a class of anionic glycopolymers that play key roles ... ...

Abstract	Listeria monocytogenes is an opportunistic Gram-positive bacterial pathogen responsible for listeriosis, a human foodborne disease. Its cell wall is densely decorated with wall teichoic acids (WTAs), a class of anionic glycopolymers that play key roles in bacterial physiology, including protection against the activity of antimicrobial peptides (AMPs). In other Gram-positive pathogens, WTA modification by amine-containing groups such as D-alanine was largely correlated with resistance to AMPs. However, in L. monocytogenes, where WTA modification is achieved solely via glycosylation, WTA-associated mechanisms of AMP resistance were unknown. Here, we show that the L-rhamnosylation of L. monocytogenes WTAs relies not only on the rmlACBD locus, which encodes the biosynthetic pathway for L-rhamnose, but also on rmlT encoding a putative rhamnosyltransferase. We demonstrate that this WTA tailoring mechanism promotes resistance to AMPs, unveiling a novel link between WTA glycosylation and bacterial resistance to host defense peptides. Using in vitro binding assays, fluorescence-based techniques and electron microscopy, we show that the presence of L-rhamnosylated WTAs at the surface of L. monocytogenes delays the crossing of the cell wall by AMPs and postpones their contact with the listerial membrane. We propose that WTA L-rhamnosylation promotes L. monocytogenes survival by decreasing the cell wall permeability to AMPs, thus hindering their access and detrimental interaction with the plasma membrane. Strikingly, we reveal a key contribution of WTA L-rhamnosylation for L. monocytogenes virulence in a mouse model of infection.
MeSH term(s)	Animals ; Anti-Infective Agents/pharmacology ; Antimicrobial Cationic Peptides/pharmacology ; Cell Membrane/metabolism ; Cell Wall/metabolism ; Cells, Cultured ; Drug Resistance, Bacterial/drug effects ; Glycosylation ; Humans ; Listeria monocytogenes/physiology ; Listeriosis/drug therapy ; Listeriosis/microbiology ; Macrophages/drug effects ; Macrophages/microbiology ; Mice ; Mice, Inbred BALB C ; Rhamnose/chemistry ; Teichoic Acids/pharmacology ; Virulence
Chemical Substances	Anti-Infective Agents ; Antimicrobial Cationic Peptides ; Teichoic Acids ; Rhamnose (QN34XC755A)
Language	English
Publishing date	2015-05-22
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1004919
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Article ; Online: Wall teichoic acids of Staphylococcus aureus limit recognition by the drosophila peptidoglycan recognition protein-SA to promote pathogenicity.

Atilano, Magda L / Yates, James / Glittenberg, Marcus / Filipe, Sergio R / Ligoxygakis, Petros

PLoS pathogens

2011 Volume 7, Issue 12, Page(s) e1002421

Abstract: The cell wall of gram-positive bacteria is a complex network of surface proteins, capsular polysaccharides and wall teichoic acids (WTA) covalently linked to Peptidoglycan (PG). The absence of WTA has been associated with a reduced pathogenicity of ... ...

Abstract	The cell wall of gram-positive bacteria is a complex network of surface proteins, capsular polysaccharides and wall teichoic acids (WTA) covalently linked to Peptidoglycan (PG). The absence of WTA has been associated with a reduced pathogenicity of Staphylococcus aureus (S. aureus). Here, we assessed whether this was due to increased detection of PG, an important target of innate immune receptors. Antibiotic-mediated or genetic inhibition of WTA production in S. aureus led to increased binding of the non-lytic PG Recognition Protein-SA (PGRP-SA), and this was associated with a reduction in host susceptibility to infection. Moreover, PGRP-SD, another innate sensor required to control wild type S. aureus infection, became redundant. Our data imply that by using WTA to limit access of innate immune receptors to PG, under-detected bacteria are able to establish an infection and ultimately overwhelm the host. We propose that different PGRPs work in concert to counter this strategy.
MeSH term(s)	Animals ; Anti-Bacterial Agents/pharmacology ; Carrier Proteins/genetics ; Carrier Proteins/metabolism ; Cell Wall/genetics ; Cell Wall/metabolism ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Drosophila melanogaster ; Immunity, Innate/drug effects ; Immunity, Innate/genetics ; Peptidoglycan/genetics ; Peptidoglycan/metabolism ; Staphylococcal Infections/genetics ; Staphylococcal Infections/metabolism ; Staphylococcus aureus/genetics ; Staphylococcus aureus/metabolism ; Staphylococcus aureus/pathogenicity ; Teichoic Acids/genetics ; Teichoic Acids/metabolism
Chemical Substances	Anti-Bacterial Agents ; Carrier Proteins ; Drosophila Proteins ; Peptidoglycan ; Teichoic Acids ; peptidoglycan recognition protein
Language	English
Publishing date	2011-12-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1002421
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Article ; Online: Thioridazine induces major changes in global gene expression and cell wall composition in methicillin-resistant Staphylococcus aureus USA300.

Thorsing, Mette / Klitgaard, Janne K / Atilano, Magda L / Skov, Marianne N / Kolmos, Hans Jørn / Filipe, Sérgio R / Kallipolitis, Birgitte H

PloS one

2013 Volume 8, Issue 5, Page(s) e64518

Abstract: Subinhibitory concentrations of the neuroleptic drug thioridazine (TDZ) are well-known to enhance the killing of methicillin-resistant Staphylococcus aureus (MRSA) by β-lactam antibiotics, however, the mechanism underlying the synergy between TDZ and β- ... ...

Abstract	Subinhibitory concentrations of the neuroleptic drug thioridazine (TDZ) are well-known to enhance the killing of methicillin-resistant Staphylococcus aureus (MRSA) by β-lactam antibiotics, however, the mechanism underlying the synergy between TDZ and β-lactams is not fully understood. In the present study, we have examined the effect of a subinhibitory concentration of TDZ on antimicrobial resistance, the global transcriptome, and the cell wall composition of MRSA USA300. We show that TDZ is able to sensitize the bacteria to several classes of antimicrobials targeting the late stages of peptidoglycan (PGN) synthesis. Furthermore, our microarray analysis demonstrates that TDZ modulates the expression of genes encoding membrane and surface proteins, transporters, and enzymes involved in amino acid biosynthesis. Interestingly, resemblance between the transcriptional profile of TDZ treatment and the transcriptomic response of S. aureus to known inhibitors of cell wall synthesis suggests that TDZ disturbs PGN biosynthesis at a stage that precedes transpeptidation by penicillin-binding proteins (PBPs). In support of this notion, dramatic changes in the muropeptide profile of USA300 were observed following growth in the presence of TDZ, indicating that TDZ can interfere with the formation of the pentaglycine branches. Strikingly, the addition of glycine to the growth medium relieved the effect of TDZ on the muropeptide profile. Furthermore, exogenous glycine offered a modest protective effect against TDZ-induced β-lactam sensitivity. We propose that TDZ exposure leads to a shortage of intracellular amino acids, including glycine, which is required for the production of normal PGN precursors with pentaglycine branches, the correct substrate of S. aureus PBPs. Collectively, this work demonstrates that TDZ has a major impact on the cell wall biosynthesis pathway in S. aureus and provides new insights into how MRSA may be sensitized towards β-lactam antibiotics.
MeSH term(s)	Antipsychotic Agents/pharmacology ; Cell Wall/drug effects ; Cell Wall/metabolism ; Gene Expression Regulation, Bacterial/drug effects ; Glycine/pharmacology ; Linear Models ; Methicillin-Resistant Staphylococcus aureus/genetics ; Methicillin-Resistant Staphylococcus aureus/metabolism ; Microarray Analysis ; Microbial Sensitivity Tests ; Penicillin-Binding Proteins/metabolism ; Peptidoglycan/biosynthesis ; Thioridazine/pharmacology ; beta-Lactam Resistance/drug effects
Chemical Substances	Antipsychotic Agents ; Penicillin-Binding Proteins ; Peptidoglycan ; Thioridazine (N3D6TG58NI) ; Glycine (TE7660XO1C)
Language	English
Publishing date	2013-05-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0064518
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