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Article ; Online: Correction: Neuron‑derived extracellular vesicles in blood reveal effects of exercise in Alzheimer's disease.

Delgado-Peraza, Francheska / Nogueras-Ortiz, Carlos / Simonsen, Anja Hviid / Knight, De'Larrian DeAnté / Yao, Pamela J / Goetzl, Edward J / Jensen, Camilla Steen / Høgh, Peter / Gottrup, Hanne / Vestergaard, Karsten / Hasselbalch, Steen Gregers / Kapogiannis, Dimitrios

Alzheimer's research & therapy

2024 Volume 16, Issue 1, Page(s) 18

Language	English
Publishing date	2024-01-23
Publishing country	England
Document type	Published Erratum
ZDB-ID	2506521-X
ISSN	1758-9193 ; 1758-9193
ISSN (online)	1758-9193
ISSN	1758-9193
DOI	10.1186/s13195-023-01371-x
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Article: Comparative assessment of Alzheimer's disease-related biomarkers in plasma and neuron-derived extracellular vesicles: a nested case-control study.

Manolopoulos, Apostolos / Delgado-Peraza, Francheska / Mustapic, Maja / Pucha, Krishna Ananthu / Nogueras-Ortiz, Carlos / Daskalopoulos, Alexander / Knight, De'Larrian DeAnté / Leoutsakos, Jeannie-Marie / Oh, Esther S / Lyketsos, Constantine G / Kapogiannis, Dimitrios

Frontiers in molecular biosciences

2023 Volume 10, Page(s) 1254834

Abstract: Introduction: ...

Abstract	Introduction:
Language	English
Publishing date	2023-09-27
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2814330-9
ISSN	2296-889X
ISSN	2296-889X
DOI	10.3389/fmolb.2023.1254834
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Article ; Online: Neuron-derived extracellular vesicles in blood reveal effects of exercise in Alzheimer's disease.

Alzheimer's research & therapy

2023 Volume 15, Issue 1, Page(s) 156

Abstract: Background: Neuron-derived extracellular vesicles (NDEVs) in blood may be used to derive biomarkers for the effects of exercise in Alzheimer's disease (AD). For this purpose, we studied changes in neuroprotective proteins proBDNF, BDNF, and humanin in ... ...

Abstract	Background: Neuron-derived extracellular vesicles (NDEVs) in blood may be used to derive biomarkers for the effects of exercise in Alzheimer's disease (AD). For this purpose, we studied changes in neuroprotective proteins proBDNF, BDNF, and humanin in plasma NDEVs from patients with mild to moderate AD participating in the randomized controlled trial (RCT) of exercise ADEX. Methods: proBDNF, BDNF, and humanin were quantified in NDEVs immunocaptured from the plasma of 95 ADEX participants, randomized into exercise and control groups, and collected at baseline and 16 weeks. Exploratorily, we also quantified NDEV levels of putative exerkines known to respond to exercise in peripheral tissues. Results: NDEV levels of proBDNF, BDNF, and humanin increased in the exercise group, especially in APOE ε4 carriers, but remained unchanged in the control group. Inter-correlations between NDEV biomarkers observed at baseline were maintained after exercise. NDEV levels of putative exerkines remained unchanged. Conclusions: Findings suggest that the cognitive benefits of exercise could be mediated by the upregulation of neuroprotective factors in NDEVs. Additionally, our results indicate that AD subjects carrying APOE ε4 are more responsive to the neuroprotective effects of physical activity. Unchanged NDEV levels of putative exerkines after physical activity imply that exercise engages different pathways in neurons and peripheral tissues. Future studies should aim to expand upon the effects of exercise duration, intensity, and type in NDEVs from patients with early AD and additional neurodegenerative disorders. Trial registration: The Effect of Physical Exercise in Alzheimer Patients (ADEX) was registered in ClinicalTrials.gov on April 30, 2012 with the identifier NCT01681602.
MeSH term(s)	Humans ; Alzheimer Disease ; Apolipoprotein E4 ; Brain-Derived Neurotrophic Factor ; Exercise ; Extracellular Vesicles ; Neurons
Chemical Substances	Apolipoprotein E4 ; Brain-Derived Neurotrophic Factor
Language	English
Publishing date	2023-09-20
Publishing country	England
Document type	Randomized Controlled Trial ; Journal Article ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2506521-X
ISSN	1758-9193 ; 1758-9193
ISSN (online)	1758-9193
ISSN	1758-9193
DOI	10.1186/s13195-023-01303-9
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Article ; Online: Flow Cytometry of Synaptoneurosomes (FCS) Reveals Increased Ribosomal S6 and Calcineurin Proteins in Activated Medial Prefrontal Cortex to Nucleus Accumbens Synapses.

Rubio, F Javier / Olivares, Daniel E / Dunn, Christopher / Zhang, Shiliang / Hilaire, Elias M / Henry, Akeem / Mejias-Aponte, Carlos / Nogueras-Ortiz, Carlos J / Selvam, Pooja V / Cruz, Fabio C / Madangopal, Rajtarun / Morales, Marisela / Hope, Bruce T

The Journal of neuroscience : the official journal of the Society for Neuroscience

2023 Volume 43, Issue 23, Page(s) 4217–4233

Abstract: Learning and behavior activate cue-specific patterns of sparsely distributed cells and synapses called ensembles that undergo memory-encoding engram alterations. While Fos is often used to label selectively activated cell bodies and identify neuronal ... ...

Abstract	Learning and behavior activate cue-specific patterns of sparsely distributed cells and synapses called ensembles that undergo memory-encoding engram alterations. While Fos is often used to label selectively activated cell bodies and identify neuronal ensembles, there is no comparable endogenous marker to label activated synapses and identify synaptic ensembles. For the purpose of identifying candidate synaptic activity markers, we optimized a flow cytometry of synaptoneurosome (FCS) procedure for assessing protein alterations in activated synapses from male and female rats. After injecting yellow fluorescent protein (YFP)-expressing adeno-associated virus into medial prefrontal cortex (mPFC) to label terminals in nucleus accumbens (NAc) of rats, we injected 20 mg/kg cocaine in a novel context (cocaine+novelty) to activate synapses, and prepared NAc synaptoneurosomes 0-60 min following injections. For FCS, we used commercially available antibodies to label presynaptic and postsynaptic markers synaptophysin and PSD-95 as well as candidate markers of synaptic activity [activity-regulated cytoskeleton protein (Arc), CaMKII and phospho-CaMKII, ribosomal protein S6 (S6) and phospho-S6, and calcineurin and phospho-calcineurin] in YFP-labeled synaptoneurosomes. Cocaine+novelty increased the percentage of S6-positive synaptoneurosomes at 5-60 min and calcineurin-positive synaptoneurosomes at 5-10 min. Electron microscopy verified that S6 and calcineurin levels in synaptoneurosomes were increased 10 min after cocaine+novelty. Pretreatment with the anesthetic chloral hydrate blocked cocaine+novelty-induced S6 and calcineurin increases in synaptoneurosomes, and novel context exposure alone (without cocaine) increased S6, both of which indicate that these increases were due to neural activity per se. Overall, FCS can be used to study protein alterations in activated synapses coming from specifically labeled mPFC projections to NAc.
MeSH term(s)	Female ; Rats ; Male ; Animals ; Rats, Sprague-Dawley ; Calcineurin ; Nucleus Accumbens/physiology ; Calcium-Calmodulin-Dependent Protein Kinase Type 2 ; Flow Cytometry ; Synapses ; Prefrontal Cortex/physiology ; Cocaine/pharmacology
Chemical Substances	Calcineurin (EC 3.1.3.16) ; Calcium-Calmodulin-Dependent Protein Kinase Type 2 (EC 2.7.11.17) ; Cocaine (I5Y540LHVR)
Language	English
Publishing date	2023-05-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.0927-22.2023
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Article ; Online: The Multiple Waves of Cannabinoid 1 Receptor Signaling.

Nogueras-Ortiz, Carlos / Yudowski, Guillermo A

Molecular pharmacology

2016 Volume 90, Issue 5, Page(s) 620–626

Abstract: The cannabinoid 1 receptor ( ... ...

Abstract	The cannabinoid 1 receptor (CB
MeSH term(s)	Animals ; Humans ; Models, Biological ; Receptor, Cannabinoid, CB1/metabolism ; Signal Transduction ; beta-Arrestins/metabolism
Chemical Substances	Receptor, Cannabinoid, CB1 ; beta-Arrestins
Language	English
Publishing date	2016-06-23
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	124034-1
ISSN	1521-0111 ; 0026-895X
ISSN (online)	1521-0111
ISSN	0026-895X
DOI	10.1124/mol.116.104539
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Zs.A 525: Show issues

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Article ; Online: Altered Levels of Toll-Like Receptors in Circulating Extracellular Vesicles in Multiple Sclerosis.

Bhargava, Pavan / Nogueras-Ortiz, Carlos / Chawla, Sahil / Bæk, Rikke / Jørgensen, Malene Møller / Kapogiannis, Dimitrios

Cells

2019 Volume 8, Issue 9

Abstract: Extracellular vesicles (EVs) are involved in inter-cellular communication and their cargo may provide prognostic/diagnostic biomarkers. To discover EV-associated biomarkers for Multiple Sclerosis (MS), we used an immune marker array to identify surface ... ...

Abstract	Extracellular vesicles (EVs) are involved in inter-cellular communication and their cargo may provide prognostic/diagnostic biomarkers. To discover EV-associated biomarkers for Multiple Sclerosis (MS), we used an immune marker array to identify surface proteins on circulating EVs that differ between MS patients and controls (n = 3 each). We identified toll-like receptor-3 (TLR3) as a potential target for further validation. We utilized prospectively collected serum from relapsing-remitting MS patients (n = 18) and controls (n = 16) and confirmed lower concentration of TLR3 and higher concentration of mechanistically related TLR4 in MS EVs compared to controls. Future studies may further evaluate the utility of EV-associated TLRs as MS biomarkers and uncover their mechanistic significance.
MeSH term(s)	Adult ; Biomarkers/blood ; Cell Communication ; Extracellular Vesicles/metabolism ; Extracellular Vesicles/physiology ; Female ; Humans ; Immunity, Innate/immunology ; Immunity, Innate/physiology ; Male ; Membrane Proteins/metabolism ; Middle Aged ; Multiple Sclerosis/metabolism ; Multiple Sclerosis/physiopathology ; Multiple Sclerosis, Relapsing-Remitting/metabolism ; Prognosis ; Toll-Like Receptor 3/analysis ; Toll-Like Receptor 3/metabolism ; Toll-Like Receptor 4/analysis ; Toll-Like Receptor 4/metabolism ; Toll-Like Receptors/metabolism ; Toll-Like Receptors/physiology
Chemical Substances	Biomarkers ; Membrane Proteins ; TLR3 protein, human ; TLR4 protein, human ; Toll-Like Receptor 3 ; Toll-Like Receptor 4 ; Toll-Like Receptors
Language	English
Publishing date	2019-09-10
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells8091058
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Article ; Online: A novel isolation method for spontaneously released extracellular vesicles from brain tissue and its implications for stress-driven brain pathology.

Gomes, Patrícia A / Bodo, Cristian / Nogueras-Ortiz, Carlos / Samiotaki, Martina / Chen, Minghao / Soares-Cunha, Carina / Silva, Joana M / Coimbra, Bárbara / Stamatakis, George / Santos, Liliana / Panayotou, George / Tzouanou, Foteini / Waites, Clarissa L / Gatsogiannis, Christos / Sousa, Nuno / Kapogiannis, Dimitrios / Costa-Silva, Bruno / Sotiropoulos, Ioannis

Cell communication and signaling : CCS

2023 Volume 21, Issue 1, Page(s) 35

Abstract: Background: Extracellular vesicles (EVs), including small EVs (sEVs) such as exosomes, exhibit great potential for the diagnosis and treatment of brain disorders, representing a valuable tool for precision medicine. The latter demands high-quality human ...

Abstract	Background: Extracellular vesicles (EVs), including small EVs (sEVs) such as exosomes, exhibit great potential for the diagnosis and treatment of brain disorders, representing a valuable tool for precision medicine. The latter demands high-quality human biospecimens, especially in complex disorders in which pathological and specimen heterogeneity, as well as diverse individual clinical profile, often complicate the development of precision therapeutic schemes and patient-tailored treatments. Thus, the collection and characterization of physiologically relevant sEVs are of the utmost importance. However, standard brain EV isolation approaches rely on tissue dissociation, which can contaminate EV fractions with intracellular vesicles. Methods: Based on multiscale analytical platforms such as cryo-EM, label-free proteomics, advanced flow cytometry, and ExoView analyses, we compared and characterized the EV fraction isolated with this novel method with a classical digestion-based EV isolation procedure. Moreover, EV biogenesis was pharmacologically manipulated with either GW4869 or picrotoxin to assess the validity of the spontaneous-release method, while the injection of labelled-EVs into the mouse brain further supported the integrity of the isolated vesicles. Results: We hereby present an efficient purification method that captures a sEV-enriched population spontaneously released by mouse and human brain tissue. In addition, we tested the significance of the release method under conditions where biogenesis/secretion of sEVs was pharmacologically manipulated, as well as under animals' exposure to chronic stress, a clinically relevant precipitant of brain pathologies, such as depression and Alzheimer's disease. Our findings show that the released method monitors the drug-evoked inhibition or enhancement of sEVs secretion while chronic stress induces the secretion of brain exosomes accompanied by memory loss and mood deficits suggesting a potential role of sEVs in the brain response to stress and related stress-driven brain pathology. Conclusions: Overall, the spontaneous release method of sEV yield may contribute to the characterization and biomarker profile of physiologically relevant brain-derived sEVs in brain function and pathology. Video Abstract.
MeSH term(s)	Humans ; Animals ; Mice ; Extracellular Vesicles ; Exosomes ; Brain ; Biomarkers ; Alzheimer Disease
Chemical Substances	Biomarkers
Language	English
Publishing date	2023-02-13
Publishing country	England
Document type	Video-Audio Media ; Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2126315-2
ISSN	1478-811X ; 1478-811X
ISSN (online)	1478-811X
ISSN	1478-811X
DOI	10.1186/s12964-023-01045-z
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Article: Inhibiting tau-induced elevated nSMase2 activity and ceramides is therapeutic in an Alzheimer's disease mouse model.

Tallon, Carolyn / Bell, Benjamin J / Malvankar, Medhinee M / Deme, Pragney / Nogueras-Ortiz, Carlos / Eren, Erden / Thomas, Ajit G / Hollinger, Kristen R / Pal, Arindom / Mustapic, Maja / Huang, Meixiang / Coleman, Kaleem / Joe, Tawnjerae R / Rais, Rana / Haughey, Norman J / Kapogiannis, Dimitrios / Slusher, Barbara S

Translational neurodegeneration

2023 Volume 12, Issue 1, Page(s) 56

Abstract: Background: Cognitive decline in Alzheimer's disease (AD) is associated with hyperphosphorylated tau (pTau) propagation between neurons along synaptically connected networks, in part via extracellular vesicles (EVs). EV biogenesis is triggered by ... ...

Abstract	Background: Cognitive decline in Alzheimer's disease (AD) is associated with hyperphosphorylated tau (pTau) propagation between neurons along synaptically connected networks, in part via extracellular vesicles (EVs). EV biogenesis is triggered by ceramide enrichment at the plasma membrane from neutral sphingomyelinase2 (nSMase2)-mediated cleavage of sphingomyelin. We report, for the first time, that human tau expression elevates brain ceramides and nSMase2 activity. Methods: To determine the therapeutic benefit of inhibiting this elevation, we evaluated PDDC, the first potent, selective, orally bioavailable, and brain-penetrable nSMase2 inhibitor in the transgenic PS19 AD mouse model. Additionally, we directly evaluated the effect of PDDC on tau propagation in a mouse model where an adeno-associated virus (AAV) encoding P301L/S320F double mutant human tau was stereotaxically-injected unilaterally into the hippocampus. The contralateral transfer of the double mutant human tau to the dentate gyrus was monitored. We examined ceramide levels, histopathological changes, and pTau content within EVs isolated from the mouse plasma. Results: Similar to human AD, the PS19 mice exhibited increased brain ceramide levels and nSMase2 activity; both were completely normalized by PDDC treatment. The PS19 mice also exhibited elevated tau immunostaining, thinning of hippocampal neuronal cell layers, increased mossy fiber synaptophysin immunostaining, and glial activation, all of which were pathologic features of human AD. PDDC treatment reduced these changes. The plasma of PDDC-treated PS19 mice had reduced levels of neuronal- and microglial-derived EVs, the former carrying lower pTau levels, compared to untreated mice. In the tau propagation model, PDDC normalized the tau-induced increase in brain ceramides and significantly reduced the amount of tau propagation to the contralateral side. Conclusions: PDDC is a first-in-class therapeutic candidate that normalizes elevated brain ceramides and nSMase2 activity, leading to the slowing of tau spread in AD mice.
MeSH term(s)	Animals ; Humans ; Mice ; Alzheimer Disease/drug therapy ; Alzheimer Disease/genetics ; Ceramides/metabolism ; Mice, Transgenic ; Neurons/metabolism
Chemical Substances	Ceramides ; pyrenedodecanoylcarnitine (93255-34-6)
Language	English
Publishing date	2023-12-04
Publishing country	England
Document type	Journal Article
ZDB-ID	2653701-1
ISSN	2047-9158
ISSN	2047-9158
DOI	10.1186/s40035-023-00383-9
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Article: Inhibiting tau-induced elevated nSMase2 activity and ceramides is therapeutic in murine Alzheimer's disease.

Research square

2023

Abstract: Background: Cognitive decline in Alzheimer's disease (AD) is associated with prion-like tau propagation between neurons along synaptically connected networks, in part via extracellular vesicles (EV). EV biogenesis is triggered by ceramide enrichment at ... ...

Abstract	Background: Cognitive decline in Alzheimer's disease (AD) is associated with prion-like tau propagation between neurons along synaptically connected networks, in part via extracellular vesicles (EV). EV biogenesis is triggered by ceramide enrichment at the plasma membrane from neutral sphingomyelinase2(nSMase2)-mediated cleavage of sphingomyelin. We report, for the first time, that tau expression triggers an elevation in brain ceramides and nSMase2 activity. Methods: To determine the therapeutic benefit of inhibiting this elevation, we evaluated the efficacy of PDDC, the first potent, selective, orally bioavailable, and brain-penetrable nSMase2 inhibitor, in the PS19 tau transgenic AD murine model. Changes in brain ceramide and sphingomyelin levels, Tau content, histopathology, and nSMase2 target engagement were monitored, as well as changes in the number of brain-derived EVs in plasma and their Tau content. Additionally, we evaluated the ability of PDDC to impede tau propagation in a murine model where an adeno-associated virus(AAV) encoding for P301L/S320F double mutant human tau was stereotaxically-injected unilaterally into the hippocampus and the contralateral transfer to the dentate gyrus was monitored. Results: Similar to human AD, PS19 mice exhibited increased brain ceramides and nSMase2 activity; both were completely normalized by PDDC treatment. PS19 mice exhibited elevated tau immunostaining, thinning of hippocampal neuronal cell layers, increased mossy fiber synaptophysin immunostaining, and glial activation, all pathologic features of human AD. PDDC treatment significantly attenuated these aberrant changes. Mouse plasma isolated from PDDC-treated PS19 mice exhibited reduced levels of neuron- and microglia-derived EVs, the former carrying lower phosphorylated Tau(pTau) levels, compared to untreated mice. In the AAV tau propagation model, PDDC normalized the tau-induced increase in brain ceramides and significantly decreased tau spreading to the contralateral side. Conclusions: PDDC is a first-in-class therapeutic candidate that normalizes elevated brain ceramides and nSMase2 activity leading to the slowing of tau spread in AD mice.
Language	English
Publishing date	2023-07-18
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-3131295/v1
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Article ; Online: Synaptic and complement markers in extracellular vesicles in multiple sclerosis.

Bhargava, Pavan / Nogueras-Ortiz, Carlos / Kim, Sol / Delgado-Peraza, Francheska / Calabresi, Peter A / Kapogiannis, Dimitrios

Multiple sclerosis (Houndmills, Basingstoke, England)

2020 Volume 27, Issue 4, Page(s) 509–518

Abstract: Background: Synaptic loss is a feature of multiple sclerosis pathology that can be seen even in normal-appearing gray matter. Opsonization of synapses with complement components may underlie pathologic synapse loss.: Objective: We sought to determine ...

Abstract	Background: Synaptic loss is a feature of multiple sclerosis pathology that can be seen even in normal-appearing gray matter. Opsonization of synapses with complement components may underlie pathologic synapse loss. Objective: We sought to determine whether circulating neuronal-enriched and astrocytic-enriched extracellular vesicles (NEVs and AEVs) provide biomarkers reflecting complement-mediated synaptic loss in multiple sclerosis. Methods: From plasma of 61 people with multiple sclerosis (46 relapsing-remitting multiple sclerosis (RRMS) and 15 progressive MS) and 31 healthy controls, we immunocaptured L1CAM + NEVs and GLAST + AEVs. We measured pre- and post-synaptic proteins synaptopodin and synaptophysin in NEVs and complement components (C1q, C3, C3b/iC3b, C4, C5, C5a, C9, Factor B, and Factor H) in AEVs, total circulating EVs, and neat plasma. Results: We found lower levels of NEV synaptopodin and synaptophysin in MS compared to controls ( Conclusion: Circulating EVs could identify synaptic loss in MS and suggest a link between astrocytic complement production and synaptic loss.
MeSH term(s)	Biomarkers ; Complement Activation ; Complement System Proteins ; Extracellular Vesicles ; Humans ; Multiple Sclerosis
Chemical Substances	Biomarkers ; Complement System Proteins (9007-36-7)
Language	English
Publishing date	2020-06-17
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1290669-4
ISSN	1477-0970 ; 1352-4585
ISSN (online)	1477-0970
ISSN	1352-4585
DOI	10.1177/1352458520924590
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