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Article ; Online: Neuropathological stage-dependent proteome mapping of the olfactory tract in Alzheimer's disease: From early olfactory-related omics signatures to computational repurposing of drug candidates.

Cartas-Cejudo, Paz / Cortés, Adriana / Lachén-Montes, Mercedes / Anaya-Cubero, Elena / Puerta, Elena / Solas, Maite / Fernández-Irigoyen, Joaquín / Santamaría, Enrique

Brain pathology (Zurich, Switzerland)

2024 , Page(s) e13252

Abstract: Alzheimer's disease (AD) is the most common form of dementia, characterized by an early olfactory dysfunction, progressive memory loss, and behavioral deterioration. Albeit substantial progress has been made in characterizing AD-associated molecular and ... ...

Abstract	Alzheimer's disease (AD) is the most common form of dementia, characterized by an early olfactory dysfunction, progressive memory loss, and behavioral deterioration. Albeit substantial progress has been made in characterizing AD-associated molecular and cellular events, there is an unmet clinical need for new therapies. In this study, olfactory tract proteotyping performed in controls and AD subjects (n = 17/group) showed a Braak stage-dependent proteostatic impairment accompanied by the progressive modulation of amyloid precursor protein and tau functional interactomes. To implement a computational repurposing of drug candidates with the capacity to reverse early AD-related olfactory omics signatures (OMSs), we generated a consensual OMSs database compiling differential omics datasets obtained by mass-spectrometry or RNA-sequencing derived from initial AD across the olfactory axis. Using the Connectivity Map-based drug repurposing approach, PKC, EGFR, Aurora kinase, Glycogen synthase kinase, and CDK inhibitors were the top pharmacologic classes capable to restore multiple OMSs, whereas compounds with targeted activity to inhibit PI3K, Insulin-like growth factor 1 (IGF-1), microtubules, and Polo-like kinase (PLK) represented a family of drugs with detrimental potential to induce olfactory AD-associated gene expression changes. To validate the potential therapeutic effects of the proposed drugs, in vitro assays were performed. These validation experiments revealed that pretreatment of human neuron-like SH-SY5Y cells with the EGFR inhibitor AG-1478 showed a neuroprotective effect against hydrogen peroxide-induced damage while the pretreatment with the Aurora kinase inhibitor Reversine reduced amyloid-beta (Aβ)-induced neurotoxicity. Taken together, our data pointed out that OMSs may be useful as substrates for drug repurposing to propose novel neuroprotective treatments against AD.
Language	English
Publishing date	2024-03-07
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	1051484-3
ISSN	1750-3639 ; 1015-6305
ISSN (online)	1750-3639
ISSN	1015-6305
DOI	10.1111/bpa.13252
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Article ; Online: Sex-divergent effects on the NAD+-dependent deacetylase sirtuin signaling across the olfactory-entorhinal-amygdaloid axis in Alzheimer's and Parkinson's diseases.

Cartas-Cejudo, Paz / Lachén-Montes, Mercedes / Ferrer, Isidro / Fernández-Irigoyen, Joaquín / Santamaría, Enrique

Biology of sex differences

2023 Volume 14, Issue 1, Page(s) 5

Abstract: Background: Smell impairment is one of the earliest features in Alzheimer's (AD) and Parkinson's diseases (PD). Due to sex differences exist in terms of smell and olfactory structures as well as in the prevalence and manifestation of both neurological ... ...

Abstract	Background: Smell impairment is one of the earliest features in Alzheimer's (AD) and Parkinson's diseases (PD). Due to sex differences exist in terms of smell and olfactory structures as well as in the prevalence and manifestation of both neurological syndromes, we have applied olfactory proteomics to favor the discovery of novel sex-biased physio-pathological mechanisms and potential therapeutic targets associated with olfactory dysfunction. Methods: SWATH-MS (sequential window acquisition of all theoretical fragment ion spectra mass spectrometry) and bioinformatic workflows were applied in 57 post-mortem olfactory tracts (OT) derived from controls with no known neurological history (n = 6F/11M), AD (n = 4F/13M) and PD (n = 7F/16M) subjects. Complementary molecular analyses by Western-blotting were performed in the olfactory bulb (OB), entorhinal cortex (EC) and amygdala areas. Results: 327 and 151 OT differentially expressed proteins (DEPs) were observed in AD women and AD men, respectively (35 DEPs in common). With respect to PD, 198 DEPs were identified in PD women, whereas 95 DEPs were detected in PD men (20 DEPs in common). This proteome dyshomeostasis induced a disruption in OT protein interaction networks and widespread sex-dependent pathway perturbations in a disease-specific manner, among them Sirtuin (SIRT) signaling. SIRT1, SIRT2, SIRT3 and SIRT5 protein levels unveiled a tangled expression profile across the olfactory-entorhinal-amygdaloid axis, evidencing disease-, sex- and brain structure-dependent changes in olfactory protein acetylation. Conclusions: Alteration in the OT proteostasis was more severe in AD than in PD. Moreover, protein expression changes were more abundant in women than men independent of the neurological syndrome. Mechanistically, the tangled SIRT profile observed across the olfactory pathway-associated brain regions in AD and PD indicates differential NAD (+)-dependent deacetylase mechanisms between women and men. All these data shed new light on differential olfactory mechanisms across AD and PD, pointing out that the evaluation of the feasibility of emerging sirtuin-based therapies against neurodegenerative diseases should be considered with caution, including further sex dimension analyses in vivo and in clinical studies.
MeSH term(s)	Humans ; Female ; Male ; Parkinson Disease/pathology ; Alzheimer Disease/pathology ; NAD/metabolism ; Smell ; Signal Transduction
Chemical Substances	NAD (0U46U6E8UK)
Language	English
Publishing date	2023-02-08
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2587352-0
ISSN	2042-6410 ; 2042-6410
ISSN (online)	2042-6410
ISSN	2042-6410
DOI	10.1186/s13293-023-00487-x
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Article ; Online: Sex-divergent effects on the NAD+-dependent deacetylase sirtuin signaling across the olfactory–entorhinal–amygdaloid axis in Alzheimer’s and Parkinson’s diseases

Paz Cartas-Cejudo / Mercedes Lachén-Montes / Isidro Ferrer / Joaquín Fernández-Irigoyen / Enrique Santamaría

Biology of Sex Differences, Vol 14, Iss 1, Pp 1-

2023 Volume 20

Abstract: Highlights Quantitative proteomics is a useful approach to biochemically characterize the pathological neurodegeneration that occurs at the level of olfactory areas. Alteration in the olfactory tract proteostasis is more severe in AD than in PD. Protein ... ...

Abstract	Highlights Quantitative proteomics is a useful approach to biochemically characterize the pathological neurodegeneration that occurs at the level of olfactory areas. Alteration in the olfactory tract proteostasis is more severe in AD than in PD. Protein expression changes are more abundant in women than men independent of the neurological syndrome. Functional enrichment analysis unveiled multiple common biological derangements between both sexes across both pathologies. Significant variations in the NAD+-dependent deacetylase sirtuin (SIRT) signaling, suggest sex, disease- and structure-specific changes in olfactory protein acetylation.
Keywords	Sirtuin ; Olfaction ; Sexual dimorphism ; Alzheimer ; Parkinson ; Proteomics ; Medicine ; R ; Physiology ; QP1-981
Language	English
Publishing date	2023-02-01T00:00:00Z
Publisher	BMC
Document type	Article ; Online
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Article ; Online: Mapping the human brain proteome: opportunities, challenges, and clinical potential.

Cartas-Cejudo, Paz / Cortés, Adriana / Lachén-Montes, Mercedes / Anaya-Cubero, Elena / Peral, Erika / Ausín, Karina / Díaz-Peña, Ramón / Fernández-Irigoyen, Joaquín / Santamaría, Enrique

Expert review of proteomics

2024 Volume 21, Issue 1-3, Page(s) 55–63

Abstract: Introduction: Due to the segmented functions and complexity of the human brain, the characterization of molecular profiles within specific areas such as brain structures and biofluids is essential to unveil the molecular basis for structure ... ...

Abstract	Introduction: Due to the segmented functions and complexity of the human brain, the characterization of molecular profiles within specific areas such as brain structures and biofluids is essential to unveil the molecular basis for structure specialization as well as the molecular imbalance associated with neurodegenerative and psychiatric diseases. Areas covered: Much of our knowledge about brain functionality derives from neurophysiological, anatomical, and transcriptomic approaches. More recently, laser capture and imaging proteomics, technological and computational developments in LC-MS/MS, as well as antibody/aptamer-based platforms have allowed the generation of novel cellular, spatial, and posttranslational dimensions as well as innovative facets in biomarker validation and druggable target identification. Expert opinion: Proteomics is a powerful toolbox to functionally characterize, quantify, and localize the extensive protein catalog of the human brain across physiological and pathological states. Brain function depends on multi-dimensional protein homeostasis, and its elucidation will help us to characterize biological pathways that are essential to properly maintain cognitive functions. In addition, comprehensive human brain pathological proteomes may be the basis in computational drug-repositioning methods as a strategy for unveiling potential new therapies in neurodegenerative and psychiatric disorders.
MeSH term(s)	Humans ; Tandem Mass Spectrometry ; Proteome/genetics ; Proteome/metabolism ; Chromatography, Liquid ; Brain/metabolism ; Biomarkers/metabolism
Chemical Substances	Proteome ; Biomarkers
Language	English
Publishing date	2024-02-05
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2299100-1
ISSN	1744-8387 ; 1478-9450
ISSN (online)	1744-8387
ISSN	1478-9450
DOI	10.1080/14789450.2024.2313073
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Article ; Online: Involvement of Glucosamine 6 Phosphate Isomerase 2 (GNPDA2) Overproduction in β-Amyloid- and Tau P301L-Driven Pathomechanisms.

Lachén-Montes, Mercedes / Cartas-Cejudo, Paz / Cortés, Adriana / Anaya-Cubero, Elena / Peral, Erika / Ausín, Karina / Díaz-Peña, Ramón / Fernández-Irigoyen, Joaquín / Santamaría, Enrique

Biomolecules

2024 Volume 14, Issue 4

Abstract: Alzheimer's disease (AD) is a neurodegenerative olfactory disorder affecting millions of people worldwide. Alterations in the hexosamine- or glucose-related pathways have been described through AD progression. Specifically, an alteration in glucosamine 6 ...

Abstract	Alzheimer's disease (AD) is a neurodegenerative olfactory disorder affecting millions of people worldwide. Alterations in the hexosamine- or glucose-related pathways have been described through AD progression. Specifically, an alteration in glucosamine 6 phosphate isomerase 2 (GNPDA2) protein levels has been observed in olfactory areas of AD subjects. However, the biological role of GNPDA2 in neurodegeneration remains unknown. Using mass spectrometry, multiple GNPDA2 interactors were identified in human nasal epithelial cells (NECs) mainly involved in intraciliary transport. Moreover, GNPDA2 overexpression induced an increment in NEC proliferation rates, accompanied by transcriptomic alterations in Type II interferon signaling or cellular stress responses. In contrast, the presence of beta-amyloid or mutated Tau-P301L in GNPDA2-overexpressing NECs induced a slowdown in the proliferative capacity in parallel with a disruption in protein processing. The proteomic characterization of Tau-P301L transgenic zebrafish embryos demonstrated that GNPDA2 overexpression interfered with collagen biosynthesis and RNA/protein processing, without inducing additional changes in axonal outgrowth defects or neuronal cell death. In humans, a significant increase in serum GNPDA2 levels was observed across multiple neurological proteinopathies (AD, Lewy body dementia, progressive supranuclear palsy, mixed dementia and amyotrophic lateral sclerosis) (
MeSH term(s)	Humans ; Animals ; Zebrafish/metabolism ; Amyloid beta-Peptides/metabolism ; tau Proteins/metabolism ; tau Proteins/genetics ; Alzheimer Disease/metabolism ; Alzheimer Disease/genetics ; Alzheimer Disease/pathology ; Animals, Genetically Modified ; Aldose-Ketose Isomerases/metabolism ; Aldose-Ketose Isomerases/genetics ; Cell Proliferation ; Epithelial Cells/metabolism ; Proteomics
Chemical Substances	Amyloid beta-Peptides ; tau Proteins ; Aldose-Ketose Isomerases (EC 5.3.1.-)
Language	English
Publishing date	2024-03-25
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2701262-1
ISSN	2218-273X ; 2218-273X
ISSN (online)	2218-273X
ISSN	2218-273X
DOI	10.3390/biom14040394
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Article: Olfactory Bulb Proteomics Reveals Widespread Proteostatic Disturbances in Mixed Dementia and Guides for Potential Serum Biomarkers to Discriminate Alzheimer Disease and Mixed Dementia Phenotypes.

Lachén-Montes, Mercedes / Íñigo-Marco, Ignacio / Cartas-Cejudo, Paz / Fernández-Irigoyen, Joaquín / Santamaría, Enrique

Journal of personalized medicine

2021 Volume 11, Issue 6

Abstract: The most common form of mixed dementia (MixD) is constituted by abnormal protein deposits associated with Alzheimer's disease (AD) that coexist with vascular disease. Although olfactory dysfunction is considered a clinical sign of AD-related dementias, ... ...

Abstract	The most common form of mixed dementia (MixD) is constituted by abnormal protein deposits associated with Alzheimer's disease (AD) that coexist with vascular disease. Although olfactory dysfunction is considered a clinical sign of AD-related dementias, little is known about the impact of this sensorial impairment in MixD at the molecular level. To address this gap in knowledge, we assessed olfactory bulb (OB) proteome-wide expression in MixD subjects (
Language	English
Publishing date	2021-06-03
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2662248-8
ISSN	2075-4426
ISSN	2075-4426
DOI	10.3390/jpm11060503
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Article ; Online: Combination of Antibody Arrays to Functionally Characterize Dark Proteins in Human Olfactory Neuroepithelial Cells.

Lachén-Montes, Mercedes / Ausín, Karina / Cartas-Cejudo, Paz / Fernández-Irigoyen, Joaquín / Santamaría, Enrique

Methods in molecular biology (Clifton, N.J.)

2021 Volume 2344, Page(s) 227–238

Abstract: The completion and annotation of the human proteome require the availability of information related to protein function. Currently, more than 1800 human genes constitute the "dark proteome," which include missing proteins, uncharacterized human genes ... ...

Abstract	The completion and annotation of the human proteome require the availability of information related to protein function. Currently, more than 1800 human genes constitute the "dark proteome," which include missing proteins, uncharacterized human genes validated at protein level, smORFs, proteins from lncRNAs, or any uncharacterized transcripts. During the last years, different experimental workflows based on multi-omics analyses, bioinformatics, and in vitro and in vivo studies have been promoted by the Human Proteome Project Consortium to enhance the annotation of dark proteins. In this chapter, we describe a method that utilizes recombinant proteins and antibody arrays to establish a straightforward methodology in order to rapidly characterize potential functional features of dark proteins associated to intracellular signaling dynamics and extracellular immune response in human cell cultures. Further validating the method, this workflow was applied to probe changes in the activation patterns of kinases and transcription factors as well as in cytokine production modulated by the dark C1orf128 (PITHD1) protein in human olfactory neuroepithelial cells.
MeSH term(s)	Antibodies/genetics ; Antibodies/immunology ; Humans ; Neuroepithelial Cells/immunology ; Neuroepithelial Cells/pathology ; Olfactory Bulb/immunology ; Olfactory Bulb/pathology ; Protein Array Analysis ; Proteins/genetics ; Proteins/immunology ; Proteome/genetics ; Proteome/immunology
Chemical Substances	Antibodies ; PITHD1 protein, human ; Proteins ; Proteome
Language	English
Publishing date	2021-06-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-1562-1_16
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Article ; Online: Tackling the Biological Meaning of the Human Olfactory Bulb Dyshomeostatic Proteome across Neurological Disorders: An Integrative Bioinformatic Approach.

Cartas-Cejudo, Paz / Lachén-Montes, Mercedes / Fernández-Irigoyen, Joaquín / Santamaría, Enrique

International journal of molecular sciences

2021 Volume 22, Issue 21

Abstract: Olfactory dysfunction is considered an early prodromal marker of many neurodegenerative diseases. Neuropathological changes and aberrant protein aggregates occur in the olfactory bulb (OB), triggering a tangled cascade of molecular events that is not ... ...

Abstract	Olfactory dysfunction is considered an early prodromal marker of many neurodegenerative diseases. Neuropathological changes and aberrant protein aggregates occur in the olfactory bulb (OB), triggering a tangled cascade of molecular events that is not completely understood across neurological disorders. This study aims to analyze commonalities and differences in the olfactory protein homeostasis across neurological backgrounds with different spectrums of smell dysfunction. For that, an integrative analysis was performed using OB proteomics datasets derived from subjects with Alzheimer's disease (AD), Parkinson's disease (PD), mixed dementia (mixD), dementia with Lewy bodies (DLB), frontotemporal lobar degeneration (FTLD-TDP43), progressive supranuclear palsy (PSP) and amyotrophic lateral sclerosis (ALS) with respect to OB proteome data from neurologically intact controls. A total of 80% of the differential expressed protein products were potentially disease-specific whereas the remaining 20% were commonly altered across two, three or four neurological phenotypes. A multi-level bioinformatic characterization revealed a subset of potential disease-specific transcription factors responsible for the downstream effects detected at the proteome level as well as specific densely connected protein complexes targeted by several neurological phenotypes. Interestingly, common or unique pathways and biofunctions were also identified, providing novel mechanistic clues about each neurological disease at olfactory level. The analysis of olfactory epithelium, olfactory tract and primary olfactory cortical proteotypes in a multi-disease format will functionally complement the OB dyshomeostasis, increasing our knowledge about the neurodegenerative process across the olfactory axis.
MeSH term(s)	Alzheimer Disease/metabolism ; Amyotrophic Lateral Sclerosis/metabolism ; Computational Biology ; Databases, Factual ; Dementia/metabolism ; Gene Expression Regulation ; Humans ; Nervous System Diseases/metabolism ; Neurodegenerative Diseases/metabolism ; Olfactory Bulb/metabolism ; Parkinson Disease/metabolism ; Proteome/analysis ; Proteostasis ; Supranuclear Palsy, Progressive/metabolism ; Synucleinopathies/metabolism ; Transcription Factors/metabolism
Chemical Substances	Proteome ; Transcription Factors
Language	English
Publishing date	2021-10-20
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms222111340
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Article ; Online: Deregulated Transcription and Proteostasis in Adult

Andrés-Benito, Pol / Flores, África / Busquet-Areny, Sara / Carmona, Margarita / Ausín, Karina / Cartas-Cejudo, Paz / Lachén-Montes, Mercedes / Del Rio, José Antonio / Fernández-Irigoyen, Joaquín / Santamaría, Enrique / Ferrer, Isidro

International journal of molecular sciences

2023 Volume 24, Issue 7

Abstract: Transcriptomics and phosphoproteomics were carried out in the cerebral cortex ... ...

Abstract	Transcriptomics and phosphoproteomics were carried out in the cerebral cortex of
MeSH term(s)	Mice ; Animals ; Mice, Knockout ; Proteostasis ; tau Proteins/genetics ; tau Proteins/metabolism ; Neurons/metabolism ; Cerebral Cortex/metabolism ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; Nerve Tissue Proteins/metabolism ; Intracellular Signaling Peptides and Proteins/metabolism
Chemical Substances	tau Proteins ; RNA, Messenger ; Grip2 protein, mouse ; Nerve Tissue Proteins ; Intracellular Signaling Peptides and Proteins ; Mapt protein, mouse
Language	English
Publishing date	2023-03-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms24076559
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Article: Proteomics Insights Into the Molecular Basis of SARS-CoV-2 Infection: What We Can Learn From the Human Olfactory Axis.

Lachén-Montes, Mercedes / Corrales, Fernando J / Fernández-Irigoyen, Joaquín / Santamaría, Enrique

Frontiers in microbiology

2020 Volume 11, Page(s) 2101

Abstract: Like other RNA viruses, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) replicates in host cells, continuously modulating the molecular environment. It encodes 28 multifunctional proteins that induce an imbalance in the metabolic and ... ...

Abstract	Like other RNA viruses, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) replicates in host cells, continuously modulating the molecular environment. It encodes 28 multifunctional proteins that induce an imbalance in the metabolic and proteostatic homeostasis in infected cells. Recently, proteomic approaches have allowed the evaluation of the impact of SARS-CoV-2 infection in human cells. Here, we discuss the current use of proteomics in three major application areas: (i) virus-protein interactomics, (ii) differential proteotyping to map the virus-induced changes in different cell types, and (iii) diagnostic methods for coronavirus infectious disease 2019 (COVID-19). Since the nasal cavity is one of the entry sites for SARS-CoV-2, we will also discuss the potential application of olfactory proteomics to provide novel insights into the olfactory dysfunction triggered by SARS-CoV-2 in patients with COVID-19.
Keywords	covid19
Language	English
Publishing date	2020-09-22
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2587354-4
ISSN	1664-302X
ISSN	1664-302X
DOI	10.3389/fmicb.2020.02101
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