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Article ; Online: A type VII secretion system in Group B Streptococcus mediates cytotoxicity and virulence.

Spencer, Brady L / Tak, Uday / Mendonça, Jéssica C / Nagao, Prescilla E / Niederweis, Michael / Doran, Kelly S

2021 Volume 17, Issue 12, Page(s) e1010121

Abstract: Type VII secretion systems (T7SS) have been identified in Actinobacteria and Firmicutes and have been shown to secrete effector proteins with functions in virulence, host toxicity, and/or interbacterial killing in a few genera. Bioinformatic analysis ... ...

Abstract	Type VII secretion systems (T7SS) have been identified in Actinobacteria and Firmicutes and have been shown to secrete effector proteins with functions in virulence, host toxicity, and/or interbacterial killing in a few genera. Bioinformatic analysis indicates that isolates of Group B Streptococcus (GBS) encode at least four distinct subtypes of T7SS machinery, three of which encode adjacent putative T7SS effectors with WXG and LXG motifs. However, the function of T7SS in GBS pathogenesis is unknown. Here we assessed the role of the most abundant GBS T7SS subtype during GBS pathogenesis. In a murine model of hematogenous meningitis, mice infected with GBS lacking a functional T7SS or lacking the secreted WXG100 effector EsxA exhibited less mortality, lower bacterial burdens in tissues, and decreased inflammation in the brain compared to mice infected with the parental GBS strain. We further showed that this T7SS induces cytotoxicity in brain endothelium and that EsxA contributes to these cytotoxicity phenotypes in a WXG motif-dependent manner. Finally, we determined that EsxA is a pore-forming protein, thus demonstrating the first role for a non-mycobacterial EsxA homolog in pore formation. This work reveals the importance of a T7SS in host-GBS interactions and has implications for T7SS effector function in other Gram-positive bacteria.
MeSH term(s)	Animals ; Bacterial Proteins/metabolism ; Cells, Cultured ; Humans ; Mice ; Streptococcal Infections/metabolism ; Streptococcus agalactiae/metabolism ; Streptococcus agalactiae/pathogenicity ; Type VII Secretion Systems/metabolism ; Virulence/physiology
Chemical Substances	Bacterial Proteins ; Type VII Secretion Systems
Language	English
Publishing date	2021-12-06
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1010121
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Heterogeneity of the group B streptococcal type VII secretion system and influence on colonization of the female genital tract.

Spencer, Brady L / Job, Alyx M / Robertson, Clare M / Hameed, Zainab A / Serchejian, Camille / Wiafe-Kwakye, Caitlin S / Mendonça, Jéssica C / Apolonio, Morgan A / Nagao, Prescilla E / Neely, Melody N / Korotkova, Natalia / Korotkov, Konstantin V / Patras, Kathryn A / Doran, Kelly S

Molecular microbiology

2023 Volume 120, Issue 2, Page(s) 258–275

Abstract: Type VIIb secretion systems (T7SSb) in Gram-positive bacteria facilitate physiology, interbacterial competition, and/or virulence via EssC ATPase-driven secretion of small ɑ-helical proteins and toxins. Recently, we characterized T7SSb in group B ... ...

Abstract	Type VIIb secretion systems (T7SSb) in Gram-positive bacteria facilitate physiology, interbacterial competition, and/or virulence via EssC ATPase-driven secretion of small ɑ-helical proteins and toxins. Recently, we characterized T7SSb in group B Streptococcus (GBS), a leading cause of infection in newborns and immunocompromised adults. GBS T7SS comprises four subtypes based on variation in the C-terminus of EssC and the repertoire of downstream effectors; however, the intraspecies diversity of GBS T7SS and impact on GBS-host interactions remains unknown. Bioinformatic analysis indicates that GBS T7SS loci encode subtype-specific putative effectors, which have low interspecies and inter-subtype homology but contain similar domains/motifs and therefore may serve similar functions. We further identify orphaned GBS WXG100 proteins. Functionally, we show that GBS T7SS subtype I and III strains secrete EsxA in vitro and that in subtype I strain CJB111, esxA1 appears to be differentially transcribed from the T7SS operon. Furthermore, we observe subtype-specific effects of GBS T7SS on host colonization, as CJB111 subtype I but not CNCTC 10/84 subtype III T7SS promotes GBS vaginal colonization. Finally, we observe that T7SS subtypes I and II are the predominant subtypes in clinical GBS isolates. This study highlights the potential impact of T7SS heterogeneity on host-GBS interactions.
MeSH term(s)	Infant, Newborn ; Female ; Humans ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Type VII Secretion Systems/genetics ; Virulence ; Operon/genetics ; Genitalia, Female/metabolism ; Streptococcal Infections/microbiology ; Streptococcus agalactiae/genetics ; Streptococcus agalactiae/metabolism ; Vagina/metabolism ; Vagina/microbiology
Chemical Substances	Bacterial Proteins ; Type VII Secretion Systems
Language	English
Publishing date	2023-06-26
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	619315-8
ISSN	1365-2958 ; 0950-382X
ISSN (online)	1365-2958
ISSN	0950-382X
DOI	10.1111/mmi.15115
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Article: Heterogeneity of the group B streptococcal type VII secretion system and influence on colonization of the female genital tract.

bioRxiv : the preprint server for biology

2023

Abstract	Type VIIb secretion systems (T7SSb) in Gram-positive bacteria facilitate physiology, interbacterial competition, and/or virulence via EssC ATPase-driven secretion of small ɑ-helical proteins and toxins. Recently, we characterized T7SSb in group B
Language	English
Publishing date	2023-01-25
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.01.25.525443
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Article ; Online: Identification of a novel cationic glycolipid in Streptococcus agalactiae that contributes to brain entry and meningitis.

Joyce, Luke R / Manzer, Haider S / da C Mendonça, Jéssica / Villarreal, Ricardo / Nagao, Prescilla E / Doran, Kelly S / Palmer, Kelli L / Guan, Ziqiang

PLoS biology

2022 Volume 20, Issue 2, Page(s) e3001555

Abstract: 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 ... ...

Abstract	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 GBSΔmprF 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.
MeSH term(s)	Aminoacyltransferases/genetics ; Aminoacyltransferases/metabolism ; Animals ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Biological Transport/genetics ; Blood-Brain Barrier/metabolism ; Brain/metabolism ; Cations/chemistry ; Chromatography, Liquid/methods ; Glycolipids/chemistry ; Glycolipids/metabolism ; Humans ; Male ; Meningitis/metabolism ; Mice ; Mutation ; Spectrometry, Mass, Electrospray Ionization/methods ; Streptococcus agalactiae/genetics ; Streptococcus agalactiae/metabolism ; Tandem Mass Spectrometry/methods
Chemical Substances	Bacterial Proteins ; Cations ; Glycolipids ; Aminoacyltransferases (EC 2.3.2.-)
Language	English
Publishing date	2022-02-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2126776-5
ISSN	1545-7885 ; 1544-9173
ISSN (online)	1545-7885
ISSN	1544-9173
DOI	10.1371/journal.pbio.3001555
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Zs.A 6193: Show issues

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Article: Cas9 Contributes to Group B Streptococcal Colonization and Disease.

Spencer, Brady L / Deng, Liwen / Patras, Kathryn A / Burcham, Zachary M / Sanches, Glenda F / Nagao, Prescilla E / Doran, Kelly S

Frontiers in microbiology

2019 Volume 10, Page(s) 1930

Abstract: ... Group ... ...

Abstract	Group B
Language	English
Publishing date	2019-08-21
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2019.01930
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Article ; Online: Detection and virulence potential of a phospholipase D-negative Corynebacterium ulcerans from a concurrent diphtheria and infectious mononucleosis case.

Simpson-Lourêdo, Liliane / Silva, Cecília M F / Hacker, Elena / Souza, Nadjla F / Santana, Milena M / Antunes, Camila A / Nagao, Prescilla E / Hirata, Raphael / Burkovski, Andreas / Villas Bôas, Maria Helena S / Mattos-Guaraldi, Ana Luíza

Antonie van Leeuwenhoek

2019 Volume 112, Issue 7, Page(s) 1055–1065

Abstract: Diphtheria by Corynebacterium ulcerans is increasingly occurring in children, adolescents and adults. In addition to diphtheria toxin (DT), phospholipase D (PLD) is considered a virulence factor of C. ulcerans. In the present study, a first case of ... ...

Abstract	Diphtheria by Corynebacterium ulcerans is increasingly occurring in children, adolescents and adults. In addition to diphtheria toxin (DT), phospholipase D (PLD) is considered a virulence factor of C. ulcerans. In the present study, a first case of concurrent diphtheria by a PLD-negative C. ulcerans and infectious mononucleosis (IM) was verified. Clinical and microbiological profiles and binding properties to human Fibrinogen (Fbg), Fibronectin (Fn) and type I collagen (col I) biotinylated proteins and virulence to Caenorhabditis elegans were investigated for C. ulcerans strain 2590 (clinical isolate) and two control strains, including PLD-positive BR-AD22 wild type and PLD-negative ELHA-1 PLD mutant strains. MALDI-TOF assays and a multiplex PCR of genes coding for potentially toxigenic corynebacteria identified strain 2590 as non-DT producing. Interestingly, strain 2590 did not express PLD activity in the CAMP test although the presence of the pld gene was verified. PLD-negative 2590 and a PLD-positive 210932 strains showed similar affinity to Fbg, Fn and type I collagen. C. elegans were able to escape from C. ulcerans strains, independent of PLD and DT production. Higher mortality of nematodes was verified for PLD-negative strains. Additional studies concerning multifactorial virulence potential of C. ulcerans, including environmental conditions remain necessary.
MeSH term(s)	Adolescent ; Animals ; Anti-Bacterial Agents/pharmacology ; Caenorhabditis elegans ; Corynebacterium/classification ; Corynebacterium/drug effects ; Corynebacterium/genetics ; Corynebacterium/isolation & purification ; Corynebacterium Infections/microbiology ; Diphtheria/microbiology ; Humans ; Infectious Mononucleosis/microbiology ; Male ; Phospholipase D/analysis ; Phospholipase D/metabolism ; Virulence Factors/analysis ; Virulence Factors/metabolism
Chemical Substances	Anti-Bacterial Agents ; Virulence Factors ; Phospholipase D (EC 3.1.4.4)
Language	English
Publishing date	2019-02-15
Publishing country	Netherlands
Document type	Case Reports ; Journal Article
ZDB-ID	214861-4
ISSN	1572-9699 ; 0003-6072
ISSN (online)	1572-9699
ISSN	0003-6072
DOI	10.1007/s10482-019-01240-4
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Ud II Zs.94: Show issues

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Article: Detection and virulence potential of a phospholipase D-negative Corynebacterium ulcerans from a concurrent diphtheria and infectious mononucleosis case

Simpson-Lourêdo, Liliane / Silva, Cecília M. F / Hacker, Elena / Souza, Nadjla F / Santana, Milena M / Antunes, Camila A / Nagao, Prescilla E / Hirata, Raphael, Jr / Burkovski, Andreas / Villas Bôas, Maria Helena S / Mattos-Guaraldi, Ana Luíza

Antonie van Leeuwenhoek. 2019 July, v. 112, no. 7

2019

Abstract	Diphtheria by Corynebacterium ulcerans is increasingly occurring in children, adolescents and adults. In addition to diphtheria toxin (DT), phospholipase D (PLD) is considered a virulence factor of C. ulcerans. In the present study, a first case of concurrent diphtheria by a PLD-negative C. ulcerans and infectious mononucleosis (IM) was verified. Clinical and microbiological profiles and binding properties to human Fibrinogen (Fbg), Fibronectin (Fn) and type I collagen (col I) biotinylated proteins and virulence to Caenorhabditis elegans were investigated for C. ulcerans strain 2590 (clinical isolate) and two control strains, including PLD-positive BR-AD22 wild type and PLD-negative ELHA-1 PLD mutant strains. MALDI-TOF assays and a multiplex PCR of genes coding for potentially toxigenic corynebacteria identified strain 2590 as non-DT producing. Interestingly, strain 2590 did not express PLD activity in the CAMP test although the presence of the pld gene was verified. PLD-negative 2590 and a PLD-positive 210932 strains showed similar affinity to Fbg, Fn and type I collagen. C. elegans were able to escape from C. ulcerans strains, independent of PLD and DT production. Higher mortality of nematodes was verified for PLD-negative strains. Additional studies concerning multifactorial virulence potential of C. ulcerans, including environmental conditions remain necessary.
Keywords	Caenorhabditis elegans ; Corynebacterium ulcerans ; adolescents ; adults ; binding properties ; children ; collagen ; environmental factors ; fibronectins ; genes ; humans ; matrix-assisted laser desorption-ionization mass spectrometry ; mortality ; mutants ; phospholipase D ; phospholipases ; polymerase chain reaction ; virulence
Language	English
Dates of publication	2019-07
Size	p. 1055-1065.
Publishing place	Springer International Publishing
Document type	Article
ZDB-ID	214861-4
ISSN	1572-9699 ; 0003-6072
ISSN (online)	1572-9699
ISSN	0003-6072
DOI	10.1007/s10482-019-01240-4
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: The Group B Streptococcal surface antigen I/II protein, BspC, interacts with host vimentin to promote adherence to brain endothelium and inflammation during the pathogenesis of meningitis.

Deng, Liwen / Spencer, Brady L / Holmes, Joshua A / Mu, Rong / Rego, Sara / Weston, Thomas A / Hu, Yoonsung / Sanches, Glenda F / Yoon, Sunghyun / Park, Nogi / Nagao, Prescilla E / Jenkinson, Howard F / Thornton, Justin A / Seo, Keun Seok / Nobbs, Angela H / Doran, Kelly S

PLoS pathogens

2019 Volume 15, Issue 6, Page(s) e1007848

Abstract: Streptococcus agalactiae (Group B Streptococcus, GBS) normally colonizes healthy adults but can cause invasive disease, such as meningitis, in the newborn. To gain access to the central nervous system, GBS must interact with and penetrate brain or ... ...

Abstract	Streptococcus agalactiae (Group B Streptococcus, GBS) normally colonizes healthy adults but can cause invasive disease, such as meningitis, in the newborn. To gain access to the central nervous system, GBS must interact with and penetrate brain or meningeal blood vessels; however, the exact mechanisms are still being elucidated. Here, we investigate the contribution of BspC, an antigen I/II family adhesin, to the pathogenesis of GBS meningitis. Disruption of the bspC gene reduced GBS adherence to human cerebral microvascular endothelial cells (hCMEC), while heterologous expression of BspC in non-adherent Lactococcus lactis conferred bacterial attachment. In a murine model of hematogenous meningitis, mice infected with ΔbspC mutants exhibited lower mortality as well as decreased brain bacterial counts and inflammatory infiltrate compared to mice infected with WT GBS strains. Further, BspC was both necessary and sufficient to induce neutrophil chemokine expression. We determined that BspC interacts with the host cytoskeleton component vimentin and confirmed this interaction using a bacterial two-hybrid assay, microscale thermophoresis, immunofluorescent staining, and imaging flow cytometry. Vimentin null mice were protected from WT GBS infection and also exhibited less inflammatory cytokine production in brain tissue. These results suggest that BspC and the vimentin interaction is critical for the pathogenesis of GBS meningitis.
MeSH term(s)	Animals ; Antigens, Bacterial/genetics ; Antigens, Bacterial/metabolism ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Brain/blood supply ; Brain/metabolism ; Brain/microbiology ; Brain/pathology ; Endothelium, Vascular ; HeLa Cells ; Humans ; Male ; Meningitis, Bacterial/genetics ; Meningitis, Bacterial/metabolism ; Meningitis, Bacterial/pathology ; Mice ; Mice, Mutant Strains ; Sheep ; Streptococcal Infections/genetics ; Streptococcal Infections/metabolism ; Streptococcal Infections/pathology ; Streptococcus agalactiae/genetics ; Streptococcus agalactiae/metabolism ; Streptococcus agalactiae/pathogenicity ; Vimentin/genetics ; Vimentin/metabolism
Chemical Substances	Antigens, Bacterial ; Bacterial Proteins ; Vim protein, mouse ; Vimentin
Keywords	covid19
Language	English
Publishing date	2019-06-10
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; 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.1007848
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Article ; Online: Virulent and Avirulent Strains of Group B Streptococci from Rio de Janeiro, Brazil

Nagao Prescilla E / Benchetrit Leslie C

Memórias do Instituto Oswaldo Cruz., Vol 94, Iss 4, Pp 497-

Relationship between Differences in Surface Hydrophobicity, Sialic Acid Content and Macrophage Interaction

1999 Volume 498

Keywords	streptococci ; surface hydrophobicity ; sialic acid ; macrophages ; Rio de Janeiro ; Arctic medicine. Tropical medicine ; RC955-962 ; Microbiology ; QR1-502
Language	English
Publishing date	1999-01-01T00:00:00Z
Publisher	Instituto Oswaldo Cruz, Ministério da Saúde
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article: Signal transduction in human endothelial cells induced by their interaction with group B Streptococci.

Santos, Gabriela S / Lione, Viviane O F / Costa E Silva Filho, Fernando / Nagao, Prescilla E

International journal of molecular medicine

2005 Volume 15, Issue 5, Page(s) 859–863

Abstract: The molecular mechanisms underlying entry of group B Streptococci (GBS) into human endothelial cells are not yet fully understood. This study is centered on the triggering of signaling cascade in human umbilical vein endothelial cells (HUVEC) during ... ...

Abstract	The molecular mechanisms underlying entry of group B Streptococci (GBS) into human endothelial cells are not yet fully understood. This study is centered on the triggering of signaling cascade in human umbilical vein endothelial cells (HUVEC) during their interaction with different GBS serotypes/strains (type III: 80340-vagina and 90356-CSF and type V: 88641-vagina and 90186-blood). We have shown that the analyzed microorganisms adhere to HUVEC, but only those of the strains 90356-CSF, 88641-vagina and 90186-blood presented intracellular viability. Activation of PKC directly increased F-actin content and organization into stress fibers, and increased intracellular viability of GBS-III microorganisms. PKA inhibitor seems to promote surveillance of GBS type V microorganisms within HUVEC. These studies indicate that different molecules present at the cell surface of the GBS might induce different responses to HUVEC, interfering with the recruitment of cortical actin filaments.
MeSH term(s)	Actins/metabolism ; Bacterial Adhesion ; Cells, Cultured ; Cyclic AMP-Dependent Protein Kinases/antagonists & inhibitors ; Cyclic AMP-Dependent Protein Kinases/physiology ; Endothelial Cells/drug effects ; Endothelial Cells/enzymology ; Endothelial Cells/microbiology ; Humans ; Isoquinolines/pharmacology ; Protein Kinase C/antagonists & inhibitors ; Protein Kinase C/physiology ; Signal Transduction ; Sphingosine/pharmacology ; Streptococcus agalactiae/pathogenicity ; Streptococcus agalactiae/physiology ; Stress Fibers/metabolism ; Sulfonamides/pharmacology ; Umbilical Veins/cytology
Chemical Substances	Actins ; Isoquinolines ; Sulfonamides ; N-(2-aminoethyl)-5-isoquinolinesulfonamide (84468-17-7) ; Cyclic AMP-Dependent Protein Kinases (EC 2.7.11.11) ; Protein Kinase C (EC 2.7.11.13) ; Sphingosine (NGZ37HRE42)
Language	English
Publishing date	2005-05
Publishing country	Greece
Document type	Journal Article
ZDB-ID	1444428-8
ISSN	1107-3756
ISSN	1107-3756
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