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Article ; Online: ShapeMetrics: A 3D Cell Segmentation Pipeline for Single-Cell Spatial Morphometric Analysis.

Pajanoja, Ceren / Kerosuo, Laura

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

2023 Volume 2767, Page(s) 263–273

Abstract: There is a growing need for single-cell level data analysis in correlation with the advancements of microscopy techniques. Morphology-based statistics gathered from individual cells are essential for detection and quantification of even subtle changes ... ...

Abstract	There is a growing need for single-cell level data analysis in correlation with the advancements of microscopy techniques. Morphology-based statistics gathered from individual cells are essential for detection and quantification of even subtle changes within the complex tissues, yet the information available from high-resolution imaging is oftentimes sub-optimally utilized due to the lack of proper computational analysis software. Here we present ShapeMetrics, a 3D cell segmentation pipeline that we have developed to identify, analyze, and quantify single cells in an image. This MATLAB-based script enables users to extract morphological parameters, such as ellipticity, longest axis, cell elongation, or the ratio between cell volume and surface area. We have specifically invested in creating a user-friendly pipeline, aimed for biologists with a limited computational background. Our pipeline is presented with detailed stepwise instructions, starting from the establishment of machine learning-based prediction files of immuno-labeled cell membranes followed by the application of 3D cell segmentation and parameter extraction script, leading to the morphometric analysis and spatial visualization of cell clusters defined by their morphometric features.
MeSH term(s)	Imaging, Three-Dimensional/methods ; Software ; Microscopy/methods ; Cell Cycle ; Single-Cell Analysis/methods ; Image Processing, Computer-Assisted/methods
Language	English
Publishing date	2023-05-22
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/7651_2023_489
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Article ; Online: On the road again: Establishment and maintenance of stemness in the neural crest from embryo to adulthood.

Perera, Surangi N / Kerosuo, Laura

Stem cells (Dayton, Ohio)

2020 Volume 39, Issue 1, Page(s) 7–25

Abstract: Unique to vertebrates, the neural crest (NC) is an embryonic stem cell population that contributes to a greatly expanding list of derivatives ranging from neurons and glia of the peripheral nervous system, facial cartilage and bone, pigment cells of the ... ...

Abstract	Unique to vertebrates, the neural crest (NC) is an embryonic stem cell population that contributes to a greatly expanding list of derivatives ranging from neurons and glia of the peripheral nervous system, facial cartilage and bone, pigment cells of the skin to secretory cells of the endocrine system. Here, we focus on what is specifically known about establishment and maintenance of NC stemness and ultimate fate commitment mechanisms, which could help explain its exceptionally high stem cell potential that exceeds the "rules set during gastrulation." In fact, recent discoveries have shed light on the existence of NC cells that coexpress commonly accepted pluripotency factors like Nanog, Oct4/PouV, and Klf4. The coexpression of pluripotency factors together with the exceptional array of diverse NC derivatives encouraged us to propose a new term "pleistopotent" (Greek for abundant, a substantial amount) to be used to reflect the uniqueness of the NC as compared to other post-gastrulation stem cell populations in the vertebrate body, and to differentiate them from multipotent lineage restricted stem cells. We also discuss studies related to the maintenance of NC stemness within the challenging context of being a transient and thus a constantly changing population of stem cells without a permanent niche. The discovery of the stem cell potential of Schwann cell precursors as well as multiple adult NC-derived stem cell reservoirs during the past decade has greatly increased our understanding of how NC cells contribute to tissues formed after its initial migration stage in young embryos.
MeSH term(s)	Animals ; Cell Differentiation ; Embryo, Mammalian/embryology ; Embryonic Development ; Embryonic Stem Cells/metabolism ; Neural Crest/embryology
Language	English
Publishing date	2020-11-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Review
ZDB-ID	1143556-2
ISSN	1549-4918 ; 1066-5099
ISSN (online)	1549-4918
ISSN	1066-5099
DOI	10.1002/stem.3283
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Article ; Online: Spatial Genomic Analysis: A Multiplexed Transcriptional Profiling Method that Reveals Subpopulations of Cells Within Intact Tissues.

Lignell, Antti / Kerosuo, Laura

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

2018 Volume 2002, Page(s) 151–163

Abstract: Here, we present Spatial Genomic Analysis (SGA), a quantitative single-cell transcriptional profiling method that takes advantage of single-molecule imaging of individual transcripts for up to a hundred genes. SGA relies on a machine learning-based image ...

Abstract	Here, we present Spatial Genomic Analysis (SGA), a quantitative single-cell transcriptional profiling method that takes advantage of single-molecule imaging of individual transcripts for up to a hundred genes. SGA relies on a machine learning-based image analysis pipeline that performs cell segmentation and transcript counting in a robust way. SGA is suitable for various in situ applications and was originally developed to address heterogeneity in the neural crest, which is a transient embryonic stem cell population important for formation of various vertebrate body structures. After being specified as multipotent neural crest stem cells in the dorsal neural tube, they go through an epithelial to mesenchymal transition in order to migrate to different destinations around the body, and gradually turn from stem cells to progenitors prior to final commitment. The molecular details of this process remain largely unknown, and upon their emergence, the neural crest cells have been considered as a single homogeneous population. Technical limitations have restricted the possibility to parse the neural crest cell pool into subgroups according to multiplex gene expression properties. By using SGA, we were able to identify subgroups inside the neural crest niche in the dorsal neural tube. The high sensitivity of the method allows detection of low expression levels and we were able to determine factors not previously shown to be present in neural crest stem cells, such as pluripotency or lineage markers. Finally, SGA analysis also provides prediction of gene relationships within individual cells, and thus has broad utility for powerful transcriptome analyses in original biological contexts.
MeSH term(s)	Animals ; Cell Lineage ; Cell Movement ; Chick Embryo ; Embryonic Stem Cells/cytology ; Embryonic Stem Cells/metabolism ; Gene Expression Profiling/methods ; Gene Expression Regulation, Developmental ; Genomics/methods ; Humans ; Neural Crest/cytology ; Neural Crest/metabolism ; Neural Stem Cells/cytology ; Neural Stem Cells/metabolism ; Neural Tube/cytology ; Neural Tube/metabolism
Language	English
Publishing date	2018-09-06
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/7651_2018_188
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Article ; Online: In Vitro Maintenance of Multipotent Neural Crest Stem Cells as Crestospheres.

Mohlin, Sofie / Kerosuo, Laura

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

2018 Volume 2002, Page(s) 1–11

Abstract: Neural crest cells are a critical source of many cell types of the vertebrate body. However, as a stem cell population they are peculiar because of the transient nature of their stem cell niche; soon after the multipotent neural crest cells are specified ...

Abstract	Neural crest cells are a critical source of many cell types of the vertebrate body. However, as a stem cell population they are peculiar because of the transient nature of their stem cell niche; soon after the multipotent neural crest cells are specified in the neuroepithelium, they become mesenchymal cells that migrate into various destinations in early embryos. These rapid in vivo changes during neural crest development complicate the studies on their stem cell properties. Crestospheres are in vitro maintained primary cultures of premigratory neural crest cells that maintain a mixture of neural crest stem and progenitor cells for weeks without spontaneous differentiation, including the multipotent neural crest stem cells. Here, we describe how crestosphere cultures are initiated from either cranial or trunk levels of chick embryos. Alternatively, the same culture conditions can be used to maintain human embryonic stem cell-derived neural crest cells as crestospheres. Thus, crestospheres provide a useful tool for studies on neural crest stemness.
MeSH term(s)	Animals ; Cell Differentiation ; Cells, Cultured ; Chick Embryo ; Embryonic Stem Cells/cytology ; Humans ; In Vitro Techniques ; Multipotent Stem Cells/cytology ; Neural Crest/cytology ; Neural Stem Cells/cytology ; Neurogenesis
Language	English
Publishing date	2018-08-29
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/7651_2018_180
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Article ; Online: cMyc Regulates the Size of the Premigratory Neural Crest Stem Cell Pool.

Kerosuo, Laura / Bronner, Marianne E

Cell reports

2016 Volume 17, Issue 10, Page(s) 2648–2659

Abstract: The neural crest is a transient embryonic population that originates within the central nervous system (CNS) and then migrates into the periphery and differentiates into multiple cell types. The mechanisms that govern neural crest stem-like ... ...

Abstract	The neural crest is a transient embryonic population that originates within the central nervous system (CNS) and then migrates into the periphery and differentiates into multiple cell types. The mechanisms that govern neural crest stem-like characteristics and self-renewal ability are poorly understood. Here, we show that the proto-oncogene cMyc is a critical factor in the chick dorsal neural tube, where it regulates the size of the premigratory neural crest stem cell pool. Loss of cMyc dramatically decreases the number of emigrating neural crest cells due to reduced self-renewal capacity, increased cell death, and shorter duration of the emigration process. Interestingly, rather than via E-Box binding, cMyc acts in the dorsal neural tube by interacting with another transcription factor, Miz1, to promote self-renewal. The finding that cMyc operates in a non-canonical manner in the premigratory neural crest highlights the importance of examining its role at specific time points and in an in vivo context.
MeSH term(s)	Animals ; Cell Adhesion/genetics ; Cell Self Renewal/genetics ; Gene Expression Regulation, Developmental ; Mice ; Neural Crest/growth & development ; Neural Crest/metabolism ; Neural Stem Cells/metabolism ; Neural Tube/growth & development ; Neural Tube/metabolism ; Nuclear Proteins/genetics ; Nuclear Proteins/metabolism ; Protein Inhibitors of Activated STAT/genetics ; Protein Inhibitors of Activated STAT/metabolism ; Proto-Oncogene Proteins c-myc/genetics ; Proto-Oncogene Proteins c-myc/metabolism ; Stem Cells ; Ubiquitin-Protein Ligases
Chemical Substances	Nuclear Proteins ; Protein Inhibitors of Activated STAT ; Proto-Oncogene Proteins c-myc ; Miz1 protein, mouse (EC 2.3.2.27) ; Ubiquitin-Protein Ligases (EC 2.3.2.27)
Language	English
Publishing date	2016-12-29
Publishing country	United States
Document type	Journal Article
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2016.11.025
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Article ; Online: Novel roles of phentolamine in protecting axon myelination, muscle atrophy, and functional recovery following nerve injury.

Zainul, Zarin / Ma, Bo / Koka, Mert / Wilkerson, Jenny L / Ortiz, Yuma T / Kerosuo, Laura / Chandran, Vijayendran

Scientific reports

2022 Volume 12, Issue 1, Page(s) 3344

Abstract: Incomplete functional recovery after peripheral nerve injury (PNI) often results in devastating physical disabilities in human patients. Despite improved progress in surgical and non-surgical approaches, achieving complete functional recovery following ... ...

Abstract	Incomplete functional recovery after peripheral nerve injury (PNI) often results in devastating physical disabilities in human patients. Despite improved progress in surgical and non-surgical approaches, achieving complete functional recovery following PNI remains a challenge. This study demonstrates that phentolamine may hold a significant promise in treating nerve injuries and denervation induced muscle atrophy following PNI. In a sciatic nerve crush injury mouse model, we found that phentolamine treatment enhanced motor and functional recovery, protected axon myelination, and attenuated injury-induced muscle atrophy in mice at 14 days post-injury (dpi) compared to saline treatment. In the soleus of phentolamine treated animals, we observed the downregulation of phosphorylated signal transducer and activator of transcription factor 3 (p-STAT3) as well as muscle atrophy-related genes Myogenin, muscle ring finger 1 (MuRF-1), and Forkhead box O proteins (FoxO1, FoxO3). Our results show that both nerve and muscle recovery are integral components of phentolamine treatment-induced global functional recovery in mice at 14 dpi. Moreover, phentolamine treatment improved locomotor functional recovery in the mice after spinal cord crush (SCC) injury. The fact that phentolamine is an FDA approved non-selective alpha-adrenergic blocker, clinically prescribed for oral anesthesia reversal, hypertension, and erectile dysfunction makes this drug a promising candidate for repurposing in restoring behavioral recovery following PNI and SCC injuries, axonal neuropathy, and muscle wasting disorders.
MeSH term(s)	Animals ; Axons/metabolism ; Humans ; Male ; Mice ; Muscle, Skeletal/pathology ; Muscular Atrophy/pathology ; Nerve Regeneration ; Peripheral Nerve Injuries ; Phentolamine/therapeutic use ; Recovery of Function/physiology ; Sciatic Nerve/injuries ; Sciatic Neuropathy
Chemical Substances	Phentolamine (Z468598HBV)
Language	English
Publishing date	2022-02-28
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-022-07253-w
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Article ; Online: ShapeMetrics: A userfriendly pipeline for 3D cell segmentation and spatial tissue analysis.

Takko, Heli / Pajanoja, Ceren / Kurtzeborn, Kristen / Hsin, Jenny / Kuure, Satu / Kerosuo, Laura

Developmental biology

2020 Volume 462, Issue 1, Page(s) 7–19

Abstract: The demand for single-cell level data is constantly increasing within life sciences. In order to meet this demand, robust cell segmentation methods that can tackle challenging in vivo tissues with complex morphology are required. However, currently ... ...

Abstract	The demand for single-cell level data is constantly increasing within life sciences. In order to meet this demand, robust cell segmentation methods that can tackle challenging in vivo tissues with complex morphology are required. However, currently available cell segmentation and volumetric analysis methods perform poorly on 3D images. Here, we generated ShapeMetrics, a MATLAB-based script that segments cells in 3D and, by performing unbiased clustering using a heatmap, separates the cells into subgroups according to their volumetric and morphological differences. The cells can be accurately segregated according to different biologically meaningful features such as cell ellipticity, longest axis, cell elongation, or the ratio between cell volume and surface area. Our machine learning based script enables dissection of a large amount of novel data from microscope images in addition to the traditional information based on fluorescent biomarkers. Furthermore, the cells in different subgroups can be spatially mapped back to their original locations in the tissue image to help elucidate their roles in their respective morphological contexts. In order to facilitate the transition from bulk analysis to single-cell level accuracy, we emphasize the user-friendliness of our method by providing detailed step-by-step instructions through the pipeline hence aiming to reach users with less experience in computational biology.
MeSH term(s)	Algorithms ; Animals ; Computational Biology ; Humans ; Image Processing, Computer-Assisted/methods ; Imaging, Three-Dimensional/methods ; Microscopy ; Software ; Spatial Analysis
Language	English
Publishing date	2020-02-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2020.02.003
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Article: Maintenance of pluripotency in the entire ectoderm enables neural crest formation.

Pajanoja, Ceren / Hsin, Jenny / Olinger, Bradley / Schiffmacher, Andrew / Abrams, Shaun / Dapkunas, Arvydas / Zainul, Zarin / Doyle, Andrew D / Martin, Daniel / Kerosuo, Laura

Research square

2023

Abstract: The ability of the pluripotent epiblast to contribute progeny to all three germ layers is thought to be lost after gastrulation. The later-forming neural crest (NC) rises from ectoderm and it remains poorly understood how its exceptionally high stem-cell ...

Abstract	The ability of the pluripotent epiblast to contribute progeny to all three germ layers is thought to be lost after gastrulation. The later-forming neural crest (NC) rises from ectoderm and it remains poorly understood how its exceptionally high stem-cell potential to generate mesodermal- and endodermal-like cells is obtained. We monitored transcriptional changes from gastrulation to neurulation using single-cell-Multiplex-Spatial-Transcriptomics (scMST) complemented with RNA-sequencing. Unexpectedly, we find maintenance of undecided Nanog/Oct4-PouV/Klf4-positive pluripotent-like pan-ectodermal stem-cells spanning the entire ectoderm late in the neurulation process with ectodermal patterning completed only at the end of neurulation when pluripotency becomes restricted to NC, challenging our understanding of gastrulation. Furthermore, broad ectodermal pluripotency is found at all axial levels unrelated to the NC lineage the cells later commit to, suggesting a general role in stemness enhancement and proposing a mechanism by which the NC acquires its ability to form derivatives beyond "ectodermal-capacity" in chick and mouse embryos.
Language	English
Publishing date	2023-01-25
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-2285117/v1
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Article ; Online: Maintenance of pluripotency-like signature in the entire ectoderm leads to neural crest stem cell potential.

Pajanoja, Ceren / Hsin, Jenny / Olinger, Bradley / Schiffmacher, Andrew / Yazejian, Rita / Abrams, Shaun / Dapkunas, Arvydas / Zainul, Zarin / Doyle, Andrew D / Martin, Daniel / Kerosuo, Laura

Nature communications

2023 Volume 14, Issue 1, Page(s) 5941

Abstract	The ability of the pluripotent epiblast to contribute progeny to all three germ layers is thought to be lost after gastrulation. The later-forming neural crest (NC) rises from ectoderm and it remains poorly understood how its exceptionally high stem-cell potential to generate mesodermal- and endodermal-like derivatives is obtained. Here, we monitor transcriptional changes from gastrulation to neurulation using single-cell-Multiplex-Spatial-Transcriptomics (scMST) complemented with RNA-sequencing. We show maintenance of pluripotency-like signature (Nanog, Oct4/PouV, Klf4-positive) in undecided pan-ectodermal stem-cells spanning the entire ectoderm late during neurulation with ectodermal patterning completed only at the end of neurulation when the pluripotency-like signature becomes restricted to NC, challenging our understanding of gastrulation. Furthermore, broad ectodermal pluripotency-like signature is found at multiple axial levels unrelated to the NC lineage the cells later commit to, suggesting a general role in stemness enhancement and proposing a mechanism by which the NC acquires its ability to form derivatives beyond "ectodermal-capacity" in chick and mouse embryos.
MeSH term(s)	Animals ; Mice ; Ectoderm ; Neural Crest ; Neural Stem Cells ; Germ Layers ; Chickens
Language	English
Publishing date	2023-09-23
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-41384-6
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Article ; Online: Immunoglobulin superfamily member 3 is required for the vagal neural crest cell migration and enteric neuronal network organization.

Tanjore Ramanathan, Jayendrakishore / Zárybnický, Tomáš / Filppu, Pauliina / Monzo, Hector J / Monni, Outi / Tervonen, Topi A / Klefström, Juha / Kerosuo, Laura / Kuure, Satu / Laakkonen, Pirjo

Scientific reports

2023 Volume 13, Issue 1, Page(s) 17162

Abstract: The immunoglobulin (Ig) superfamily members are involved in cell adhesion and migration, complex multistep processes that play critical roles in embryogenesis, wound healing, tissue formation, and many other processes, but their specific functions during ...

Abstract	The immunoglobulin (Ig) superfamily members are involved in cell adhesion and migration, complex multistep processes that play critical roles in embryogenesis, wound healing, tissue formation, and many other processes, but their specific functions during embryonic development remain unclear. Here, we have studied the function of the immunoglobulin superfamily member 3 (IGSF3) by generating an Igsf3 knockout (KO) mouse model with CRISPR/Cas9-mediated genome engineering. By combining RNA and protein detection methodology, we show that during development, IGSF3 localizes to the neural crest and a subset of its derivatives, suggesting a role in normal embryonic and early postnatal development. Indeed, inactivation of Igsf3 impairs the ability of the vagal neural crest cells to migrate and normally innervate the intestine. The small intestine of Igsf3 KO mice shows reduced thickness of the muscularis externa and diminished number of enteric neurons. Also, misalignment of neurons and smooth muscle cells in the developing intestinal villi is detected. Taken together, our results suggest that IGSF3 functions contribute to the formation of the enteric nervous system. Given the essential role of the enteric nervous system in maintaining normal gastrointestinal function, our study adds to the pool of information required for further understanding the mechanisms of gut innervation and etiology behind bowel motility disorders.
MeSH term(s)	Mice ; Animals ; Neural Crest ; Neurons/physiology ; Gastrointestinal Tract ; Enteric Nervous System/metabolism ; Intestine, Small ; Immunoglobulins/genetics ; Immunoglobulins/metabolism ; Cell Movement/physiology
Chemical Substances	Immunoglobulins
Language	English
Publishing date	2023-10-11
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-44093-8
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