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Article ; Online: Bisulphite Sequencing of Chromatin Immunoprecipitated DNA (BisChIP-seq).

Stirzaker, Clare / Song, Jenny Z / Statham, Aaron L / Clark, Susan J

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

2017 Volume 1708, Page(s) 285–302

Abstract: Epigenetic regulation plays a critical role in gene expression, cellular differentiation, and disease. There is a complex interplay between the different layers of epigenetic information, including DNA methylation, nucleosome positions, histone ... ...

Abstract	Epigenetic regulation plays a critical role in gene expression, cellular differentiation, and disease. There is a complex interplay between the different layers of epigenetic information, including DNA methylation, nucleosome positions, histone modifications, histone variants, and other important epigenetic regulators. The different modifications do not act independently of each other and their relationship plays an important role in governing the regulation of the epigenome. Of these, DNA methylation is the best-studied epigenetic modification in mammals. However, the direct relationship between DNA methylation and chromatin modifications has been difficult to unravel with existing technologies, with epigenome-wide integration studies still based on "overlaying" independent chromatin modification and DNA methylation maps. Bisulphite sequencing enables the methylation state of every cytosine residue to be analyzed across a given molecule in a strand-specific context. Here, we describe a direct approach to interrogating the DNA methylation status of specific chromatin-marked DNA, using high-throughput sequencing of bisulphite-treated chromatin immunoprecipitated DNA (BisChIP-seq). This combined approach enables the exquisite relationship between chromatin-modified DNA or transcription factor-associated DNA and the methylation state of each targeted allele to be directly interrogated. BisChIP-Seq can now be widely applied genome-wide to further understand the molecular relationship between DNA methylation and other important epigenetic regulators.
MeSH term(s)	Alleles ; Animals ; Cell Line ; Chromatin Immunoprecipitation/methods ; DNA Methylation ; Epigenesis, Genetic ; High-Throughput Nucleotide Sequencing/methods ; Humans ; Mammals/genetics ; Sequence Analysis, DNA/methods ; Sulfites
Chemical Substances	Sulfites ; hydrogen sulfite (OJ9787WBLU)
Language	English
Publishing date	2017-12-06
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-7481-8_15
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Article: Mining cancer methylomes: prospects and challenges.

Stirzaker, Clare / Taberlay, Phillippa C / Statham, Aaron L / Clark, Susan J

Trends in genetics : TIG

2014 Volume 30, Issue 2, Page(s) 75–84

Abstract: There are over 28 million CpG sites in the human genome. Assessing the methylation status of each of these sites will be required to understand fully the role of DNA methylation in health and disease. Genome-wide analysis, using arrays and high- ... ...

Abstract	There are over 28 million CpG sites in the human genome. Assessing the methylation status of each of these sites will be required to understand fully the role of DNA methylation in health and disease. Genome-wide analysis, using arrays and high-throughput sequencing, has enabled assessment of large fractions of the methylome, but each protocol comes with unique advantages and disadvantages. Notably, except for whole-genome bisulfite sequencing, most commonly used genome-wide methods detect <5% of all CpG sites. Here, we discuss approaches for methylome studies and compare genome coverage of promoters, genes, and intergenic regions, and capacity to quantitate individual CpG methylation states. Finally, we examine the extent of published cancer methylomes that have been generated using genome-wide approaches.
MeSH term(s)	Animals ; Computational Biology/methods ; DNA Methylation ; Databases, Genetic ; Epigenesis, Genetic ; Epigenomics/methods ; Genome-Wide Association Study/methods ; High-Throughput Nucleotide Sequencing ; Humans ; Internet ; Neoplasms/genetics ; Transcriptome
Language	English
Publishing date	2014-02
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	619240-3
ISSN	1362-4555 ; 0168-9525 ; 0168-9479
ISSN (online)	1362-4555
ISSN	0168-9525 ; 0168-9479
DOI	10.1016/j.tig.2013.11.004
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Article: COBRA-Seq: Sensitive and Quantitative Methylome Profiling.

Varinli, Hilal / Statham, Aaron L / Clark, Susan J / Molloy, Peter L / Ross, Jason P

Genes

2015 Volume 6, Issue 4, Page(s) 1140–1163

Abstract: Combined Bisulfite Restriction Analysis (COBRA) quantifies DNA methylation at a specific locus. It does so via digestion of PCR amplicons produced from bisulfite-treated DNA, using a restriction enzyme that contains a cytosine within its recognition ... ...

Abstract	Combined Bisulfite Restriction Analysis (COBRA) quantifies DNA methylation at a specific locus. It does so via digestion of PCR amplicons produced from bisulfite-treated DNA, using a restriction enzyme that contains a cytosine within its recognition sequence, such as TaqI. Here, we introduce COBRA-seq, a genome wide reduced methylome method that requires minimal DNA input (0.1-1.0 mg) and can either use PCR or linear amplification to amplify the sequencing library. Variants of COBRA-seq can be used to explore CpG-depleted as well as CpG-rich regions in vertebrate DNA. The choice of enzyme influences enrichment for specific genomic features, such as CpG-rich promoters and CpG islands, or enrichment for less CpG dense regions such as enhancers. COBRA-seq coupled with linear amplification has the additional advantage of reduced PCR bias by producing full length fragments at high abundance. Unlike other reduced representative methylome methods, COBRA-seq has great flexibility in the choice of enzyme and can be multiplexed and tuned, to reduce sequencing costs and to interrogate different numbers of sites. Moreover, COBRA-seq is applicable to non-model organisms without the reference genome and compatible with the investigation of non-CpG methylation by using restriction enzymes containing CpA, CpT, and CpC in their recognition site.
Language	English
Publishing date	2015-10-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527218-4
ISSN	2073-4425
ISSN	2073-4425
DOI	10.3390/genes6041140
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Article: Genome-wide nucleosome occupancy and DNA methylation profiling of four human cell lines.

Statham, Aaron L / Taberlay, Phillippa C / Kelly, Theresa K / Jones, Peter A / Clark, Susan J

Genomics data

2014 Volume 3, Page(s) 94–96

Abstract: DNA methylation and nucleosome positioning are two key mechanisms that contribute to the epigenetic control of gene expression. During carcinogenesis, the expression of many genes is altered alongside extensive changes in the epigenome, with repressed ... ...

Abstract	DNA methylation and nucleosome positioning are two key mechanisms that contribute to the epigenetic control of gene expression. During carcinogenesis, the expression of many genes is altered alongside extensive changes in the epigenome, with repressed genes often being associated with local DNA hypermethylation and gain of nucleosomes at their promoters. However the spectrum of alterations that occur at distal regulatory regions has not been extensively studied. To address this we used Nucleosome Occupancy and Methylation sequencing (NOMe-seq) to compare the genome-wide DNA methylation and nucleosome occupancy profiles between normal and cancer cell line models of the breast and prostate. Here we describe the bioinformatic pipeline and methods that we developed for the processing and analysis of the NOMe-seq data published by (Taberlay et al., 2014 [1]) and deposited in the Gene Expression Omnibus with accession GSE57498.
Language	English
Publishing date	2014-12-08
Publishing country	United States
Document type	Journal Article
ZDB-ID	2751131-5
ISSN	2213-5960
ISSN	2213-5960
DOI	10.1016/j.gdata.2014.11.012
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Article ; Online: Reconfiguration of nucleosome-depleted regions at distal regulatory elements accompanies DNA methylation of enhancers and insulators in cancer.

Taberlay, Phillippa C / Statham, Aaron L / Kelly, Theresa K / Clark, Susan J / Jones, Peter A

Genome research

2014 Volume 24, Issue 9, Page(s) 1421–1432

Abstract: It is well established that cancer-associated epigenetic repression occurs concomitant with CpG island hypermethylation and loss of nucleosomes at promoters, but the role of nucleosome occupancy and epigenetic reprogramming at distal regulatory elements ... ...

Abstract	It is well established that cancer-associated epigenetic repression occurs concomitant with CpG island hypermethylation and loss of nucleosomes at promoters, but the role of nucleosome occupancy and epigenetic reprogramming at distal regulatory elements in cancer is still poorly understood. Here, we evaluate the scope of global epigenetic alterations at enhancers and insulator elements in prostate and breast cancer cells using simultaneous genome-wide mapping of DNA methylation and nucleosome occupancy (NOMe-seq). We find that the genomic location of nucleosome-depleted regions (NDRs) is mostly cell type specific and preferentially found at enhancers in normal cells. In cancer cells, however, we observe a global reconfiguration of NDRs at distal regulatory elements coupled with a substantial reorganization of the cancer methylome. Aberrant acquisition of nucleosomes at enhancer-associated NDRs is associated with hypermethylation and epigenetic silencing marks, and conversely, loss of nucleosomes with demethylation and epigenetic activation. Remarkably, we show that nucleosomes remain strongly organized and phased at many facultative distal regulatory elements, even in the absence of a NDR as an anchor. Finally, we find that key transcription factor (TF) binding sites also show extensive peripheral nucleosome phasing, suggesting the potential for TFs to organize NDRs genome-wide and contribute to deregulation of cancer epigenomes. Together, our findings suggest that "decommissioning" of NDRs and TFs at distal regulatory elements in cancer cells is accompanied by DNA hypermethylation susceptibility of enhancers and insulator elements, which in turn may contribute to an altered genome-wide architecture and epigenetic deregulation in malignancy.
MeSH term(s)	DNA Methylation ; Enhancer Elements, Genetic ; Epigenesis, Genetic ; Gene Expression Regulation, Neoplastic ; Humans ; Insulator Elements ; MCF-7 Cells ; Nucleosomes/genetics ; Nucleosomes/metabolism
Chemical Substances	Nucleosomes
Language	English
Publishing date	2014-06-10
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1284872-4
ISSN	1549-5469 ; 1088-9051 ; 1054-9803
ISSN (online)	1549-5469
ISSN	1088-9051 ; 1054-9803
DOI	10.1101/gr.163485.113
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Article ; Online: Evaluation of cross-platform and interlaboratory concordance via consensus modelling of genomic measurements

Peters, Timothy J. / French, Hugh J. / Bradford, Stephen T. / Pidsley, Ruth / Stirzaker, Clare / Varinli, Hilal / Nair, Shalima / Qu, Wenjia / Song, Jenny / Giles, Katherine A. / Statham, Aaron L. / Speirs, Helen / Speed, Terence P. / Clark, Susan J.

Bioinformatics. 2019 Feb. 15, v. 35, no. 4, p. 560-570

2019 , Page(s) 560–570

Abstract: A synoptic view of the human genome benefits chiefly from the application of nucleic acid sequencing and microarray technologies. These platforms allow interrogation of patterns such as gene expression and DNA methylation at the vast majority of ... ...

Abstract	A synoptic view of the human genome benefits chiefly from the application of nucleic acid sequencing and microarray technologies. These platforms allow interrogation of patterns such as gene expression and DNA methylation at the vast majority of canonical loci, allowing granular insights and opportunities for validation of original findings. However, problems arise when validating against a “gold standard” measurement, since this immediately biases all subsequent measurements towards that particular technology or protocol. Since all genomic measurements are estimates, in the absence of a ”gold standard” we instead empirically assess the measurement precision and sensitivity of a large suite of genomic technologies via a consensus modelling method called the row-linear model. This method is an application of the American Society for Testing and Materials Standard E691 for assessing interlaboratory precision and sources of variability across multiple testing sites. Both cross-platform and cross-locus comparisons can be made across all common loci, allowing identification of technology- and locus-specific tendencies. We assess technologies including the Infinium MethylationEPIC BeadChip, whole genome bisulfite sequencing (WGBS), two different RNA-Seq protocols (PolyA+ and Ribo-Zero) and five different gene expression array platforms. Each technology thus is characterised herein, relative to the consensus. We showcase a number of applications of the row-linear model, including correlation with known interfering traits. We demonstrate a clear effect of cross-hybridisation on the sensitivity of Infinium methylation arrays. Additionally, we perform a true interlaboratory test on a set of samples interrogated on the same platform across twenty-one separate testing laboratories. A full implementation of the row-linear model, plus extra functions for visualisation, are found in the R package consensus at https://github.com/timpeters82/consensus. Supplementary data are available at Bioinformatics online.
Keywords	DNA methylation ; bioinformatics ; bisulfites ; gene expression ; genome ; genomics ; humans ; microarray technology ; models ; nucleic acids ; sequence analysis
Language	English
Dates of publication	2019-0215
Size	p. 560-570
Publishing place	Oxford University Press
Document type	Article ; Online
Note	Use and reproduction
ZDB-ID	1468345-3
ISSN	1367-4811 ; 1460-2059
ISSN	1367-4811 ; 1460-2059
DOI	10.1093/bioinformatics/bty675
Database	NAL-Catalogue (AGRICOLA)

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Article: Genome-wide nucleosome occupancy and DNA methylation profiling of four human cell lines

Statham, Aaron L / Taberlay, Phillippa C / Kelly, Theresa K / Jones, Peter A / Clark, Susan J

Genomics Data. 2015 Mar., v. 3

2015

Abstract	DNA methylation and nucleosome positioning are two key mechanisms that contribute to the epigenetic control of gene expression. During carcinogenesis, the expression of many genes is altered alongside extensive changes in the epigenome, with repressed genes often being associated with local DNA hypermethylation and gain of nucleosomes at their promoters. However the spectrum of alterations that occur at distal regulatory regions has not been extensively studied. To address this we used Nucleosome Occupancy and Methylation sequencing (NOMe-seq) to compare the genome-wide DNA methylation and nucleosome occupancy profiles between normal and cancer cell line models of the breast and prostate. Here we describe the bioinformatic pipeline and methods that we developed for the processing and analysis of the NOMe-seq data published by (Taberlay et al., 2014 [1]) and deposited in the Gene Expression Omnibus with accession GSE57498.
Keywords	DNA ; DNA methylation ; bioinformatics ; breasts ; carcinogenesis ; epigenetics ; gene expression ; genes ; human cell lines ; models ; neoplasms ; nucleosomes
Language	English
Dates of publication	2015-03
Size	p. 94-96.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	2751131-5
ISSN	2213-5960
ISSN	2213-5960
DOI	10.1016/j.gdata.2014.11.012
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Article ; Online: Protocol matters: which methylome are you actually studying?

Robinson, Mark D / Statham, Aaron L / Speed, Terence P / Clark, Susan J

Epigenomics

2011 Volume 2, Issue 4, Page(s) 587–598

Abstract: The field of epigenetics is now capitalizing on the vast number of emerging technologies, largely based on second-generation sequencing, which interrogate DNA methylation status and histone modifications genome-wide. However, getting an exhaustive and ... ...

Abstract	The field of epigenetics is now capitalizing on the vast number of emerging technologies, largely based on second-generation sequencing, which interrogate DNA methylation status and histone modifications genome-wide. However, getting an exhaustive and unbiased view of a methylome at a reasonable cost is proving to be a significant challenge. In this article, we take a closer look at the impact of the DNA sequence and bias effects introduced to datasets by genome-wide DNA methylation technologies and where possible, explore the bioinformatics tools that deconvolve them. There remains much to be learned about the performance of genome-wide technologies, the data we mine from these assays and how it reflects the actual biology. While there are several methods to interrogate the DNA methylation status genome-wide, our opinion is that no single technique suitably covers the minimum criteria of high coverage and, high resolution at a reasonable cost. In fact, the fraction of the methylome that is studied currently depends entirely on the inherent biases of the protocol employed. There is promise for this to change, as the third generation of sequencing technologies is expected to again 'revolutionize' the way that we study genomes and epigenomes.
MeSH term(s)	Base Composition ; Computational Biology/methods ; CpG Islands/genetics ; DNA Methylation/genetics ; Gene Dosage ; Genome/genetics ; Histones/genetics ; Histones/metabolism ; Humans ; Sequence Analysis, DNA/methods
Chemical Substances	Histones
Language	English
Publishing date	2011-03-07
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1750-192X
ISSN (online)	1750-192X
DOI	10.2217/epi.10.36
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Article ; Online: Constitutively bound CTCF sites maintain 3D chromatin architecture and long-range epigenetically regulated domains.

Khoury, Amanda / Achinger-Kawecka, Joanna / Bert, Saul A / Smith, Grady C / French, Hugh J / Luu, Phuc-Loi / Peters, Timothy J / Du, Qian / Parry, Aled J / Valdes-Mora, Fatima / Taberlay, Phillippa C / Stirzaker, Clare / Statham, Aaron L / Clark, Susan J

Nature communications

2020 Volume 11, Issue 1, Page(s) 54

Abstract: The architectural protein CTCF is a mediator of chromatin conformation, but how CTCF binding to DNA is orchestrated to maintain long-range gene expression is poorly understood. Here we perform RNAi knockdown to reduce CTCF levels and reveal a shared ... ...

Abstract	The architectural protein CTCF is a mediator of chromatin conformation, but how CTCF binding to DNA is orchestrated to maintain long-range gene expression is poorly understood. Here we perform RNAi knockdown to reduce CTCF levels and reveal a shared subset of CTCF-bound sites are robustly resistant to protein depletion. The 'persistent' CTCF sites are enriched at domain boundaries and chromatin loops constitutive to all cell types. CRISPR-Cas9 deletion of 2 persistent CTCF sites at the boundary between a long-range epigenetically active (LREA) and silenced (LRES) region, within the Kallikrein (KLK) locus, results in concordant activation of all 8 KLK genes within the LRES region. CTCF genome-wide depletion results in alteration in Topologically Associating Domain (TAD) structure, including the merging of TADs, whereas TAD boundaries are not altered where persistent sites are maintained. We propose that the subset of essential CTCF sites are involved in cell-type constitutive, higher order chromatin architecture.
MeSH term(s)	Binding Sites ; CCCTC-Binding Factor/genetics ; CCCTC-Binding Factor/metabolism ; Chromatin/chemistry ; Chromatin/genetics ; Chromatin/metabolism ; DNA/genetics ; DNA/metabolism ; Epigenesis, Genetic ; Humans ; Promoter Regions, Genetic ; Protein Binding ; Protein Domains
Chemical Substances	CCCTC-Binding Factor ; Chromatin ; DNA (9007-49-2)
Language	English
Publishing date	2020-01-07
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/s41467-019-13753-7
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Article ; Online: Evaluation of cross-platform and interlaboratory concordance via consensus modelling of genomic measurements.

Peters, Timothy J / French, Hugh J / Bradford, Stephen T / Pidsley, Ruth / Stirzaker, Clare / Varinli, Hilal / Nair, Shalima / Qu, Wenjia / Song, Jenny / Giles, Katherine A / Statham, Aaron L / Speirs, Helen / Speed, Terence P / Clark, Susan J

Bioinformatics (Oxford, England)

2018 Volume 35, Issue 4, Page(s) 560–570

Abstract: Motivation: A synoptic view of the human genome benefits chiefly from the application of nucleic acid sequencing and microarray technologies. These platforms allow interrogation of patterns such as gene expression and DNA methylation at the vast ... ...

Abstract	Motivation: A synoptic view of the human genome benefits chiefly from the application of nucleic acid sequencing and microarray technologies. These platforms allow interrogation of patterns such as gene expression and DNA methylation at the vast majority of canonical loci, allowing granular insights and opportunities for validation of original findings. However, problems arise when validating against a "gold standard" measurement, since this immediately biases all subsequent measurements towards that particular technology or protocol. Since all genomic measurements are estimates, in the absence of a "gold standard" we instead empirically assess the measurement precision and sensitivity of a large suite of genomic technologies via a consensus modelling method called the row-linear model. This method is an application of the American Society for Testing and Materials Standard E691 for assessing interlaboratory precision and sources of variability across multiple testing sites. Both cross-platform and cross-locus comparisons can be made across all common loci, allowing identification of technology- and locus-specific tendencies. Results: We assess technologies including the Infinium MethylationEPIC BeadChip, whole genome bisulfite sequencing (WGBS), two different RNA-Seq protocols (PolyA+ and Ribo-Zero) and five different gene expression array platforms. Each technology thus is characterised herein, relative to the consensus. We showcase a number of applications of the row-linear model, including correlation with known interfering traits. We demonstrate a clear effect of cross-hybridisation on the sensitivity of Infinium methylation arrays. Additionally, we perform a true interlaboratory test on a set of samples interrogated on the same platform across twenty-one separate testing laboratories. Availability and implementation: A full implementation of the row-linear model, plus extra functions for visualisation, are found in the R package consensus at https://github.com/timpeters82/consensus. Supplementary information: Supplementary data are available at Bioinformatics online.
MeSH term(s)	Computational Biology ; DNA Methylation ; Genome, Human ; Genomics ; Humans ; Oligonucleotide Array Sequence Analysis ; Software
Language	English
Publishing date	2018-07-03
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1422668-6
ISSN	1367-4811 ; 1367-4803
ISSN (online)	1367-4811
ISSN	1367-4803
DOI	10.1093/bioinformatics/bty675
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