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Article ; Online: Metabolic engineering of Corynebacterium glutamicum for production of scyllo-inositol, a drug candidate against Alzheimer's disease.

Ramp, Paul / Lehnert, Alexander / Matamouros, Susana / Wirtz, Astrid / Baumgart, Meike / Bott, Michael

2021 Volume 67, Page(s) 173–185

Abstract: Scyllo-inositol has been identified as a potential drug for the treatment of Alzheimer's disease. Therefore, cost-efficient processes for the production of this compound are desirable. In this study, we analyzed and engineered Corynebacterium glutamicum ... ...

Abstract	Scyllo-inositol has been identified as a potential drug for the treatment of Alzheimer's disease. Therefore, cost-efficient processes for the production of this compound are desirable. In this study, we analyzed and engineered Corynebacterium glutamicum with the aim to develop competitive scyllo-inositol producer strains. Initial studies revealed that C. glutamicum naturally produces scyllo-inositol when cultured with myo-inositol as carbon source. The conversion involves NAD
MeSH term(s)	Alzheimer Disease/drug therapy ; Alzheimer Disease/genetics ; Bacillus subtilis/genetics ; Corynebacterium glutamicum/genetics ; Humans ; Inositol ; Metabolic Engineering ; Pharmaceutical Preparations
Chemical Substances	Pharmaceutical Preparations ; scyllitol (1VS4X81277) ; Inositol (4L6452S749)
Language	English
Publishing date	2021-07-02
Publishing country	Belgium
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1470383-x
ISSN	1096-7184 ; 1096-7176
ISSN (online)	1096-7184
ISSN	1096-7176
DOI	10.1016/j.ymben.2021.06.011
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Article ; Online: Growth-rate dependency of ribosome abundance and translation elongation rate in Corynebacterium glutamicum differs from that in Escherichia coli.

Matamouros, Susana / Gensch, Thomas / Cerff, Martin / Sachs, Christian C / Abdollahzadeh, Iman / Hendriks, Johnny / Horst, Lucas / Tenhaef, Niklas / Tenhaef, Julia / Noack, Stephan / Graf, Michaela / Takors, Ralf / Nöh, Katharina / Bott, Michael

Nature communications

2023 Volume 14, Issue 1, Page(s) 5611

Abstract: Bacterial growth rate (µ) depends on the protein synthesis capacity of the cell and thus on the number of active ribosomes and their translation elongation rate. The relationship between these fundamental growth parameters have only been described for ... ...

Abstract	Bacterial growth rate (µ) depends on the protein synthesis capacity of the cell and thus on the number of active ribosomes and their translation elongation rate. The relationship between these fundamental growth parameters have only been described for few bacterial species, in particular Escherichia coli. Here, we analyse the growth-rate dependency of ribosome abundance and translation elongation rate for Corynebacterium glutamicum, a gram-positive model species differing from E. coli by a lower growth temperature optimum and a lower maximal growth rate. We show that, unlike in E. coli, there is little change in ribosome abundance for µ <0.4 h
MeSH term(s)	Corynebacterium glutamicum/genetics ; Escherichia coli/genetics ; Ribosomes/genetics ; Polyribosomes ; Temperature
Language	English
Publishing date	2023-09-12
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-41176-y
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Article: S. Typhimurium strategies to resist killing by cationic antimicrobial peptides.

Matamouros, Susana / Miller, Samuel I

Biochimica et biophysica acta

2015 Volume 1848, Issue 11 Pt B, Page(s) 3021–3025

Abstract: S. Typhimurium is a broad host range Gram-negative pathogen that must evade killing by host innate immune systems to colonize, replicate, cause disease, and be transmitted to other hosts. A major pathogenic strategy of Salmonellae is entrance, survival, ... ...

Abstract	S. Typhimurium is a broad host range Gram-negative pathogen that must evade killing by host innate immune systems to colonize, replicate, cause disease, and be transmitted to other hosts. A major pathogenic strategy of Salmonellae is entrance, survival, and replication within eukaryotic cell phagocytic vacuoles. These phagocytic vacuoles and gastrointestinal mucosal surfaces contain multiple cationic antimicrobial peptides (CAMPs) which control invading bacteria. S. Typhimurium possesses several key mechanisms to resist killing by CAMPs which involve sensing CAMPs and membrane damage to activate signaling cascades that result in remodeling of the bacterial envelope to reduce its overall negative charge with an increase in hydrophobicity to decrease binding and effectiveness of CAMPs. Moreover Salmonellae have additional mechanisms to resist killing by CAMPs including an outer membrane protease which targets cationic peptides at the surface, and specific efflux pumps which protect the inner membrane from damage. This article is part of a Special Issue entitled: Bacterial Resistance to Antimicrobial Peptides.
MeSH term(s)	Animals ; Anti-Bacterial Agents/therapeutic use ; Antimicrobial Cationic Peptides/metabolism ; Antimicrobial Cationic Peptides/therapeutic use ; Bacterial Proteins/metabolism ; Drug Resistance, Bacterial ; Host-Pathogen Interactions ; Humans ; Immune Evasion ; Immunity, Innate ; Membrane Fluidity ; Membrane Transport Proteins/metabolism ; Microbial Viability ; O Antigens/immunology ; O Antigens/metabolism ; Proteolysis ; Salmonella Infections/immunology ; Salmonella Infections/metabolism ; Salmonella Infections/microbiology ; Salmonella Infections/prevention & control ; Salmonella typhimurium/drug effects ; Salmonella typhimurium/immunology ; Salmonella typhimurium/metabolism ; Salmonella typhimurium/pathogenicity ; Signal Transduction
Chemical Substances	Anti-Bacterial Agents ; Antimicrobial Cationic Peptides ; Bacterial Proteins ; Membrane Transport Proteins ; O Antigens
Language	English
Publishing date	2015-11
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	60-7
ISSN	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
ISSN (online)	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650
ISSN	0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
DOI	10.1016/j.bbamem.2015.01.013
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Article: Metabolic engineering of Corynebacterium glutamicum for production of scyllo-inositol, a drug candidate against Alzheimer's disease

Ramp, Paul / Lehnert, Alexander / Matamouros, Susana / Wirtz, Astrid / Baumgart, Meike / Bott, Michael

International Metabolic Engineering Society Metabolic engineering. 2021 Sept., v. 67

2021

Abstract	Scyllo-inositol has been identified as a potential drug for the treatment of Alzheimer's disease. Therefore, cost-efficient processes for the production of this compound are desirable. In this study, we analyzed and engineered Corynebacterium glutamicum with the aim to develop competitive scyllo-inositol producer strains. Initial studies revealed that C. glutamicum naturally produces scyllo-inositol when cultured with myo-inositol as carbon source. The conversion involves NAD⁺-dependent oxidation of myo-inositol to 2-keto-myo-inositol followed by NADPH-dependent reduction to scyllo-inositol. Use of myo-inositol for biomass formation was prevented by deletion of a cluster of 16 genes involved in myo-inositol catabolism (strain MB001(DE3)Δiol1). Deletion of a second cluster of four genes (oxiC-cg3390-oxiD-oxiE) related to inositol metabolism prevented conversion of 2-keto-myo-inositol to undesired products causing brown coloration (strain MB001(DE3)Δiol1Δiol2). The two chassis strains were used for plasmid-based overproduction of myo-inositol dehydrogenase (IolG) and scyllo-inositol dehydrogenase (IolW). In BHI medium containing glucose and myo-inositol, a complete conversion of the consumed myo-inositol into scyllo-inositol was achieved with the Δiol1Δiol2 strain. To enable scyllo-inositol production from cheap carbon sources, myo-inositol 1-phosphate synthase (Ino1) and myo-inositol 1-phosphatase (ImpA), which convert glucose 6-phosphate into myo-inositol, were overproduced in addition to IolG and IolW using plasmid pSI. Strain MB001(DE3)Δiol1Δiol2 (pSI) produced 1.8 g/L scyllo-inositol from 20 g/L glucose and even 4.4 g/L scyllo-inositol from 20 g/L sucrose within 72 h. Our results demonstrate that C. glutamicum is an attractive host for the biotechnological production of scyllo-inositol and potentially further myo-inositol-derived products.
Keywords	Alzheimer disease ; Corynebacterium glutamicum ; biomass ; carbon ; catabolism ; color ; cost effectiveness ; drugs ; glucose ; glucose 6-phosphate ; myo-inositol ; oxidation ; oxidoreductases ; plasmids ; sucrose
Language	English
Dates of publication	2021-09
Size	p. 173-185.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	1470383-x
ISSN	1096-7184 ; 1096-7176
ISSN (online)	1096-7184
ISSN	1096-7176
DOI	10.1016/j.ymben.2021.06.011
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Article ; Online: HAMP Domain Rotation and Tilting Movements Associated with Signal Transduction in the PhoQ Sensor Kinase.

Matamouros, Susana / Hager, Kyle R / Miller, Samuel I

mBio

2015 Volume 6, Issue 3, Page(s) e00616–15

Abstract: Unlabelled: HAMP domains are α-helical coiled coils that often transduce signals from extracytoplasmic sensing domains to cytoplasmic domains. Limited structural information has resulted in hypotheses that specific HAMP helix movement changes downstream ...

Abstract	Unlabelled: HAMP domains are α-helical coiled coils that often transduce signals from extracytoplasmic sensing domains to cytoplasmic domains. Limited structural information has resulted in hypotheses that specific HAMP helix movement changes downstream enzymatic activity. These hypotheses were tested by mutagenesis and cysteine cross-linking analysis of the PhoQ histidine kinase, essential for resistance to antimicrobial peptides in a variety of enteric pathogens. These results support a mechanistic model in which periplasmic signals which induce an activation state generate a rotational movement accompanied by a tilt in α-helix 1 which activates kinase activity. Biochemical data and a high-confidence model of the PhoQ cytoplasmic domain indicate a possible physical interaction of the HAMP domain with the catalytic domain as necessary for kinase repression. These results support a model of PhoQ activation in which changes in the periplasmic domain lead to conformational movements in the HAMP domain helices which disrupt interaction between the HAMP and the catalytic domains, thus promoting increased kinase activity. Importance: Most studies on the HAMP domain signaling states have been performed with chemoreceptors or the HAMP domain of Af1503. Full-length structures of the HAMP-containing histidine kinases VicK and CpxA or a hybrid between the HAMP domain of Af1503 and the EnvZ histidine kinase agree with the parallel four-helix bundle structure identified in Af1503 and provide snapshots of structural conformations experienced by HAMP domains. We took advantage of the fact that we can easily regulate the activation state of PhoQ histidine kinase to study its HAMP domain in the context of the full-length protein in living cells and provide biochemical evidence for different conformational states experienced by Salmonella enterica serovar Typhimurium PhoQ HAMP domain upon signaling.
MeSH term(s)	Antimicrobial Cationic Peptides/metabolism ; Bacterial Proteins/chemistry ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Circular Dichroism ; DNA Mutational Analysis ; Histidine Kinase ; Models, Molecular ; Mutant Proteins/chemistry ; Mutant Proteins/genetics ; Mutant Proteins/metabolism ; Protein Binding ; Protein Conformation ; Protein Kinases/chemistry ; Protein Kinases/genetics ; Protein Kinases/metabolism ; Protein Structure, Tertiary ; Salmonella typhimurium/chemistry ; Salmonella typhimurium/metabolism ; Salmonella typhimurium/physiology ; Signal Transduction
Chemical Substances	Antimicrobial Cationic Peptides ; Bacterial Proteins ; Mutant Proteins ; PhoQ protein, Bacteria ; Protein Kinases (EC 2.7.-) ; Histidine Kinase (EC 2.7.13.1)
Language	English
Publishing date	2015-05-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mBio.00616-15
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Article: HAMP Domain Rotation and Tilting Movements Associated with Signal Transduction in the PhoQ Sensor Kinase

Matamouros, Susana / Hager, Kyle R / Miller, Samuel I

mBio. 2015 July 1, v. 6, no. 3

2015

Abstract: ABSTRACT HAMP domains are α-helical coiled coils that often transduce signals from extracytoplasmic sensing domains to cytoplasmic domains. Limited structural information has resulted in hypotheses that specific HAMP helix movement changes downstream ... ...

Abstract	ABSTRACT HAMP domains are α-helical coiled coils that often transduce signals from extracytoplasmic sensing domains to cytoplasmic domains. Limited structural information has resulted in hypotheses that specific HAMP helix movement changes downstream enzymatic activity. These hypotheses were tested by mutagenesis and cysteine cross-linking analysis of the PhoQ histidine kinase, essential for resistance to antimicrobial peptides in a variety of enteric pathogens. These results support a mechanistic model in which periplasmic signals which induce an activation state generate a rotational movement accompanied by a tilt in α-helix 1 which activates kinase activity. Biochemical data and a high-confidence model of the PhoQ cytoplasmic domain indicate a possible physical interaction of the HAMP domain with the catalytic domain as necessary for kinase repression. These results support a model of PhoQ activation in which changes in the periplasmic domain lead to conformational movements in the HAMP domain helices which disrupt interaction between the HAMP and the catalytic domains, thus promoting increased kinase activity.
Keywords	Salmonella Typhimurium ; active sites ; antibiotic resistance ; antimicrobial peptides ; chemoreceptors ; crosslinking ; cysteine ; enzyme activity ; histidine kinase ; models ; mutagenesis ; pathogens ; signal transduction
Language	English
Dates of publication	2015-0701
Size	p. e00616-15.
Publishing place	American Society for Microbiology
Document type	Article
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mBio.00616-15
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Article ; Online: Global mRNA decay and 23S rRNA fragmentation in Gluconobacter oxydans 621H.

Kranz, Angela / Steinmann, Andrea / Degner, Ursula / Mengus-Kaya, Aliye / Matamouros, Susana / Bott, Michael / Polen, Tino

BMC genomics

2018 Volume 19, Issue 1, Page(s) 753

Abstract: Background: Gluconobacter oxydans is a strictly aerobic Gram-negative acetic acid bacterium used industrially for oxidative biotransformations due to its exceptional type of catabolism. It incompletely oxidizes a wide variety of carbohydrates regio- and ...

Abstract	Background: Gluconobacter oxydans is a strictly aerobic Gram-negative acetic acid bacterium used industrially for oxidative biotransformations due to its exceptional type of catabolism. It incompletely oxidizes a wide variety of carbohydrates regio- and stereoselectively in the periplasm using membrane-bound dehydrogenases with accumulation of the products in the medium. As a consequence, only a small fraction of the carbon and energy source enters the cell, resulting in a low biomass yield. Additionally, central carbon metabolism is characterized by the absence of a functional glycolysis and absence of a functional tricarboxylic acid (TCA) cycle. Due to these features, G. oxydans is a highly interesting model organism. Here we analyzed global mRNA decay in G. oxydans to describe its characteristic features and to identify short-lived mRNAs representing potential bottlenecks in the metabolism for further growth improvement by metabolic engineering. Results: Using DNA microarrays we estimated the mRNA half-lives in G. oxydans. Overall, the mRNA half-lives ranged mainly from 3 min to 25 min with a global mean of 5.7 min. The transcripts encoding GroES and GroEL required for proper protein folding ranked at the top among transcripts exhibiting both long half-lives and high abundance. The F-type H Conclusions: The very short mRNA half-lives of the H
MeSH term(s)	Gluconobacter oxydans/genetics ; Half-Life ; RNA Stability ; RNA, Bacterial/chemistry ; RNA, Bacterial/metabolism ; RNA, Messenger/chemistry ; RNA, Messenger/metabolism ; RNA, Ribosomal, 23S/chemistry ; RNA, Ribosomal, 23S/metabolism ; Ribosomes/metabolism
Chemical Substances	RNA, Bacterial ; RNA, Messenger ; RNA, Ribosomal, 23S
Language	English
Publishing date	2018-10-16
Publishing country	England
Document type	Journal Article
ISSN	1471-2164
ISSN (online)	1471-2164
DOI	10.1186/s12864-018-5111-1
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Article: Regulation of toxin and bacteriocin synthesis in Clostridium species by a new subgroup of RNA polymerase sigma-factors.

Dupuy, Bruno / Matamouros, Susana

Research in microbiology

2006 Volume 157, Issue 3, Page(s) 201–205

Abstract: Many Clostridium species are pathogenic for humans and animals, and most of the resulting diseases, such as tetanus, botulism, gas gangrene and pseudomembranous colitis, are due to the production of potent extracellular toxins. The biochemical mechanisms ...

Abstract	Many Clostridium species are pathogenic for humans and animals, and most of the resulting diseases, such as tetanus, botulism, gas gangrene and pseudomembranous colitis, are due to the production of potent extracellular toxins. The biochemical mechanisms of action of Clostridium toxins have been extensively studied in the past ten years. However, detailed information about the regulation of toxin gene expression has only recently emerged. TcdR, BotR, TetR and UviA are now known to be related alternative RNA polymerase sigma factors that drive transcription of toxin A and toxin B genes in C. difficile, the neurotoxin genes in C. botulinum and C. tetani, and a bacteriocin gene in C. perfringens. Although the Clostridium sigma factors have some similarity to members of the ECF sigma factor group, they differ sufficiently in structure and function so that they have been assigned to a new group within the sigma(70)-family.
MeSH term(s)	Amino Acid Sequence ; Bacterial Toxins/biosynthesis ; Bacterial Toxins/genetics ; Bacteriocins/biosynthesis ; Base Sequence ; Clostridium/metabolism ; Clostridium botulinum/metabolism ; Clostridium difficile/metabolism ; Clostridium tetani/metabolism ; DNA-Directed RNA Polymerases/metabolism ; Gene Expression Regulation, Bacterial ; Molecular Sequence Data ; Sigma Factor/metabolism
Chemical Substances	Bacterial Toxins ; Bacteriocins ; Sigma Factor ; DNA-Directed RNA Polymerases (EC 2.7.7.6)
Language	English
Publishing date	2006-04
Publishing country	France
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1004220-9
ISSN	1769-7123 ; 0923-2508
ISSN (online)	1769-7123
ISSN	0923-2508
DOI	10.1016/j.resmic.2005.11.004
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Article ; Online: PhoPQ regulates acidic glycerophospholipid content of the Salmonella Typhimurium outer membrane.

Dalebroux, Zachary D / Matamouros, Susana / Whittington, Dale / Bishop, Russell E / Miller, Samuel I

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

2014 Volume 111, Issue 5, Page(s) 1963–1968

Abstract: Gram-negative bacteria have two lipid membranes separated by a periplasmic space containing peptidoglycan. The surface bilayer, or outer membrane (OM), provides a barrier to toxic molecules, including host cationic antimicrobial peptides (CAMPs). The OM ... ...

Abstract	Gram-negative bacteria have two lipid membranes separated by a periplasmic space containing peptidoglycan. The surface bilayer, or outer membrane (OM), provides a barrier to toxic molecules, including host cationic antimicrobial peptides (CAMPs). The OM comprises an outer leaflet of lipid A, the bioactive component of lipopolysaccharide (LPS), and an inner leaflet of glycerophospholipids (GPLs). The structure of lipid A is environmentally regulated in a manner that can promote bacterial infection by increasing bacterial resistance to CAMP and reducing LPS recognition by the innate immune system. The gastrointestinal pathogen, Salmonella Typhimurium, responds to acidic pH and CAMP through the PhoPQ two-component regulatory system, which stimulates lipid A remodeling, CAMP resistance, and intracellular survival within acidified phagosomes. Work here demonstrates that, in addition to regulating lipid A structure, the S. Typhimurium PhoPQ virulence regulators also regulate acidic GPL by increasing the levels of cardiolipins and palmitoylated acylphosphatidylglycerols within the OM. Triacylated palmitoyl-PG species were diminished in strains deleted for the PhoPQ-regulated OM lipid A palmitoyltransferase enzyme, PagP. Purified PagP transferred palmitate to PG consistent with PagP acylation of both lipid A and PG within the OM. Therefore, PhoPQ coordinately regulates OM acidic GPL with lipid A structure, suggesting that GPLs cooperate with lipid A to form an OM barrier critical for CAMP resistance and intracellular survival of S. Typhimurium.
MeSH term(s)	Alleles ; Antimicrobial Cationic Peptides/pharmacology ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Cardiolipins/chemistry ; Cardiolipins/metabolism ; Cell Membrane/drug effects ; Cell Membrane/metabolism ; Drug Resistance, Bacterial/drug effects ; Drug Resistance, Bacterial/genetics ; Gene Expression Regulation, Bacterial/drug effects ; Glycerophospholipids/chemistry ; Glycerophospholipids/metabolism ; Palmitates/metabolism ; Polymyxin B/pharmacology ; Salmonella typhimurium/cytology ; Salmonella typhimurium/drug effects ; Salmonella typhimurium/genetics ; Salmonella typhimurium/metabolism ; Transcription, Genetic/drug effects
Chemical Substances	Antimicrobial Cationic Peptides ; Bacterial Proteins ; Cardiolipins ; Glycerophospholipids ; Palmitates ; PhoQ protein, Bacteria ; PhoP protein, Bacteria (125360-99-8) ; Polymyxin B (J2VZ07J96K)
Language	English
Publishing date	2014-01-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1316901111
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Article ; Online: Adaptation of commensal proliferating

Matamouros, Susana / Hayden, Hillary S / Hager, Kyle R / Brittnacher, Mitchell J / Lachance, Kristina / Weiss, Eli J / Pope, Christopher E / Imhaus, Anne-Flore / McNally, Colin P / Borenstein, Elhanan / Hoffman, Lucas R / Miller, Samuel I

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

2018 Volume 115, Issue 7, Page(s) 1605–1610

Abstract: The mature human gut microbiota is established during the first years of life, and altered intestinal microbiomes have been associated with several human health disorders. ...

Abstract	The mature human gut microbiota is established during the first years of life, and altered intestinal microbiomes have been associated with several human health disorders.
MeSH term(s)	Case-Control Studies ; Child, Preschool ; Cystic Fibrosis/genetics ; Cystic Fibrosis/microbiology ; Cystic Fibrosis/pathology ; Dietary Fats/metabolism ; Escherichia coli/pathogenicity ; Escherichia coli Infections/genetics ; Escherichia coli Infections/microbiology ; Escherichia coli Infections/pathology ; Feces/microbiology ; Gastrointestinal Microbiome/genetics ; Gene Regulatory Networks ; Glycerol/metabolism ; Humans ; Infant ; Intestines/microbiology ; Phospholipids/metabolism ; Phylogeny ; United States
Chemical Substances	Dietary Fats ; Phospholipids ; Glycerol (PDC6A3C0OX)
Language	English
Publishing date	2018--13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1714373115
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