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Article ; Online: Time-Lapse Imaging of Inflammasome-Dependent Cell Death and Extrusion in Enteroid-Derived Intestinal Epithelial Monolayers.

Geiser, Petra / van Rijn, Jorik M / Sellin, Mikael E

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

2023 Volume 2641, Page(s) 203–221

Abstract: Inflammasome-induced cell death is an epithelium-intrinsic innate immune response to pathogenic onslaught on epithelial barriers, caused by invasive microbes such as Salmonella Typhimurium (S.Tm). Pattern recognition receptors detect pathogen- or damage- ... ...

Abstract	Inflammasome-induced cell death is an epithelium-intrinsic innate immune response to pathogenic onslaught on epithelial barriers, caused by invasive microbes such as Salmonella Typhimurium (S.Tm). Pattern recognition receptors detect pathogen- or damage-associated ligands and elicit inflammasome formation. This ultimately restricts bacterial loads within the epithelium, limits breaching of the barrier, and prevents detrimental inflammatory tissue damage. Pathogen restriction is mediated via the specific extrusion of dying intestinal epithelial cells (IECs) from the epithelial tissue, accompanied by membrane permeabilization at some stage of the process. These inflammasome-dependent mechanisms can be studied in real time in intestinal epithelial organoids (enteroids), which allow imaging at high temporal and spatial resolution in a stable focal plane when seeded as 2D monolayers. The protocols described here involve the establishment of murine and human enteroid-derived monolayers, as well as time-lapse imaging of IEC extrusion and membrane permeabilization following inflammasome activation by S.Tm infection. The protocols can be adapted to also study other pathogenic insults or combined with genetic and pharmacological manipulation of the involved pathways.
MeSH term(s)	Mice ; Animals ; Humans ; Inflammasomes/metabolism ; Intestinal Mucosa/metabolism ; Time-Lapse Imaging ; Intestines ; Epithelial Cells ; Cell Death
Chemical Substances	Inflammasomes
Language	English
Publishing date	2023-04-19
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-3040-2_17
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Article ; Online: High-Definition DIC Imaging Uncovers Transient Stages of Pathogen Infection Cycles on the Surface of Human Adult Stem Cell-Derived Intestinal Epithelium.

van Rijn, Jorik M / Eriksson, Jens / Grüttner, Jana / Sundbom, Magnus / Webb, Dominic-Luc / Hellström, Per M / Svärd, Staffan G / Sellin, Mikael E

mBio

2022 Volume 13, Issue 1, Page(s) e0002222

Abstract: Interactions between individual pathogenic microbes and host tissues involve fast and dynamic processes that ultimately impact the outcome of infection. Using live-cell microscopy, these dynamics can be visualized to study, e.g., microbe motility, ... ...

Abstract	Interactions between individual pathogenic microbes and host tissues involve fast and dynamic processes that ultimately impact the outcome of infection. Using live-cell microscopy, these dynamics can be visualized to study, e.g., microbe motility, binding and invasion of host cells, and intrahost-cell survival. Such methodology typically employs confocal imaging of fluorescent tags in tumor-derived cell line infections on glass. This allows high-definition imaging but poorly reflects the host tissue's physiological architecture and may result in artifacts. We developed a method for live-cell imaging of microbial infection dynamics on human adult stem cell-derived intestinal epithelial cell (IEC) layers. These IEC layers are grown in apical imaging chambers, optimized for physiological cell arrangement and fast, but gentle, differential interference contrast (DIC) imaging. This allows subsecond visualization of both microbial and epithelial surface ultrastructure at high resolution without using fluorescent reporters. We employed this technology to probe the behavior of two model pathogens, Salmonella enterica serovar Typhimurium and Giardia intestinalis, at the intestinal epithelial surface. Our results reveal pathogen-specific swimming patterns on the epithelium and show that Salmonella lingers on the IEC surface for prolonged periods before host cell invasion, while Giardia uses circular swimming with intermittent attachments to scout for stable adhesion sites. The method even permits tracking of individual Giardia flagella, demonstrating that active flagellar beating and attachment to the IEC surface are not mutually exclusive. This work describes a generalizable and relatively inexpensive approach to resolving dynamic pathogen-IEC layer interactions, applicable even to genetically nontractable microorganisms.
MeSH term(s)	Humans ; Intestinal Mucosa ; Epithelial Cells ; Intestines ; Epithelium ; Salmonella typhimurium
Language	English
Publishing date	2022-02-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mbio.00022-22
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Article ; Online: Trophozoite fitness dictates the intestinal epithelial cell response to Giardia intestinalis infection.

Grüttner, Jana / van Rijn, Jorik M / Geiser, Petra / Florbrant, Alexandra / Webb, Dominic-Luc / Hellström, Per M / Sundbom, Magnus / Sellin, Mikael E / Svärd, Staffan G

PLoS pathogens

2023 Volume 19, Issue 5, Page(s) e1011372

Abstract: Giardia intestinalis is a non-invasive, protozoan parasite infecting the upper small intestine of most mammals. Symptomatic infections cause the diarrhoeal disease giardiasis in humans and animals, but at least half of the infections are asymptomatic. ... ...

Abstract	Giardia intestinalis is a non-invasive, protozoan parasite infecting the upper small intestine of most mammals. Symptomatic infections cause the diarrhoeal disease giardiasis in humans and animals, but at least half of the infections are asymptomatic. However, the molecular underpinnings of these different outcomes of the infection are still poorly defined. Here, we studied the early transcriptional response to G. intestinalis trophozoites, the disease-causing life-cycle stage, in human enteroid-derived, 2-dimensional intestinal epithelial cell (IEC) monolayers. Trophozoites preconditioned in media that maximise parasite fitness triggered only neglectable inflammatory transcription in the IECs during the first hours of co-incubation. By sharp contrast, "non-fit" or lysed trophozoites induced a vigorous IEC transcriptional response, including high up-regulation of many inflammatory cytokines and chemokines. Furthermore, "fit" trophozoites could even suppress the stimulatory effect of lysed trophozoites in mixed infections, suggesting active G. intestinalis suppression of the IEC response. By dual-species RNA-sequencing, we defined the IEC and G. intestinalis gene expression programs associated with these differential outcomes of the infection. Taken together, our results inform on how G. intestinalis infection can lead to such highly variable effects on the host, and pinpoints trophozoite fitness as a key determinant of the IEC response to this common parasite.
MeSH term(s)	Animals ; Humans ; Giardiasis/metabolism ; Trophozoites/metabolism ; Intestines ; Giardia lamblia/metabolism ; Epithelial Cells/metabolism ; Mammals
Language	English
Publishing date	2023-05-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1011372
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Article ; Online: A Fluorescence-based Assay for Characterization and Quantification of Lipid Droplet Formation in Human Intestinal Organoids.

van Rijn, Jorik M / van Hoesel, Marliek / Middendorp, Sabine

Journal of visualized experiments : JoVE

2019 , Issue 152

Abstract: Dietary lipids are taken up as free fatty acids (FAs) by the intestinal epithelium. These FAs are intracellularly converted into triglyceride (TG) molecules, before they are packaged into chylomicrons for transport to the lymph or into cytosolic lipid ... ...

Abstract	Dietary lipids are taken up as free fatty acids (FAs) by the intestinal epithelium. These FAs are intracellularly converted into triglyceride (TG) molecules, before they are packaged into chylomicrons for transport to the lymph or into cytosolic lipid droplets (LDs) for intracellular storage. A crucial step for the formation of LDs is the catalytic activity of diacylglycerol acyltransferases (DGAT) in the final step of TG synthesis. LDs are important to buffer toxic lipid species and regulate cellular metabolism in different cell types. Since the human intestinal epithelium is regularly confronted with high concentrations of lipids, LD formation is of great importance to regulate homeostasis. Here we describe a simple assay for the characterization and quantification of LD formation (LDF) upon stimulation with the most common unsaturated fatty acid, oleic acid, in human intestinal organoids. The LDF assay is based on the LD-specific fluorescent dye LD540, which allows for quantification of LDs by confocal microscopy, fluorescent plate reader, or flow cytometry. The LDF assay can be used to characterize LD formation in human intestinal epithelial cells, or to study human (genetic) disorders that affect LD metabolism, such as DGAT1 deficiency. Furthermore, this assay can also be used in a high-throughput pipeline to test novel therapeutic compounds, which restore defects in LD formation in intestinal or other types of organoids.
MeSH term(s)	Cells, Cultured ; Fluorescence ; Fluorescent Dyes/analysis ; Humans ; Intestinal Mucosa/chemistry ; Intestinal Mucosa/metabolism ; Intestine, Small/chemistry ; Intestine, Small/cytology ; Lipid Droplets/chemistry ; Lipid Droplets/metabolism ; Lipid Metabolism/physiology ; Organoids/chemistry ; Organoids/metabolism
Chemical Substances	Fluorescent Dyes
Language	English
Publishing date	2019-10-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Video-Audio Media
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/60150
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Article ; Online: Erratum: DGAT2 partially compensates for lipid-induced ER stress in human DGAT1-deficient intestinal stem cells.

van Rijn, Jorik M / van Hoesel, Marliek / de Heus, Cecilia / van Vugt, Anke H M / Klumperman, Judith / Nieuwenhuis, Edward E S / Houwen, Roderick H J / Middendorp, Sabine

Journal of lipid research

2021 Volume 62, Page(s) 100126

Language	English
Publishing date	2021-10-06
Publishing country	United States
Document type	Published Erratum
ZDB-ID	80154-9
ISSN	1539-7262 ; 0022-2275
ISSN (online)	1539-7262
ISSN	0022-2275
DOI	10.1016/j.jlr.2021.100126
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Article ; Online: Targeting pediatric cancers via T-cell recognition of the monomorphic MHC class I-related protein MR1.

Cornel, Annelisa M / van der Sman, Loutje / van Dinter, Jip T / Arrabito, Marta / Dunnebach, Ester / van Hoesel, Marliek / Kluiver, Thomas A / Lopes, Ana P / Dautzenberg, Noël M M / Dekker, Linde / van Rijn, Jorik M / van den Beemt, Denise A M H / Buhl, Juliane L / du Chatinier, Aimee / Barneh, Farnaz / Lu, Yuyan / Lo Nigro, Luca / Krippner-Heidenreich, Anja / Sebestyén, Zsolt /

Kuball, Jurgen / Hulleman, Esther / Drost, Jarno / van Heesch, Sebastiaan / Heidenreich, Olaf T / Peng, Weng Chuan / Nierkens, Stefan

Journal for immunotherapy of cancer

2024 Volume 12, Issue 3

Abstract: Human leukocyte antigen (HLA) restriction of conventional T-cell targeting introduces complexity in generating T-cell therapy strategies for patients with cancer with diverse HLA-backgrounds. A subpopulation of atypical, major histocompatibility complex- ... ...

Abstract	Human leukocyte antigen (HLA) restriction of conventional T-cell targeting introduces complexity in generating T-cell therapy strategies for patients with cancer with diverse HLA-backgrounds. A subpopulation of atypical, major histocompatibility complex-I related protein 1 (MR1)-restricted T-cells, distinctive from mucosal-associated invariant T-cells (MAITs), was recently identified recognizing currently unidentified MR1-presented cancer-specific metabolites. It is hypothesized that the MC.7.G5 MR1T-clone has potential as a pan-cancer, pan-population T-cell immunotherapy approach. These cells are irresponsive to healthy tissue while conferring T-cell receptor(TCR) dependent, HLA-independent cytotoxicity to a wide range of adult cancers. Studies so far are limited to adult malignancies. Here, we investigated the potential of MR1-targeting cellular therapy strategies in pediatric cancer. Bulk RNA sequencing data of primary pediatric tumors were analyzed to assess
MeSH term(s)	Humans ; Child ; Histocompatibility Antigens Class I ; Receptors, Antigen, T-Cell ; Histocompatibility Antigens Class II ; Leukemia ; Neoplasms, Germ Cell and Embryonal ; Glioma ; Minor Histocompatibility Antigens
Chemical Substances	Histocompatibility Antigens Class I ; Receptors, Antigen, T-Cell ; Histocompatibility Antigens Class II ; MR1 protein, human ; Minor Histocompatibility Antigens
Language	English
Publishing date	2024-03-21
Publishing country	England
Document type	Journal Article
ZDB-ID	2719863-7
ISSN	2051-1426 ; 2051-1426
ISSN (online)	2051-1426
ISSN	2051-1426
DOI	10.1136/jitc-2023-007538
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Article: A fluorescence-based assay for characterization and quantification of lipid droplet formation in human intestinal organoids

van Rijn, Jorik M / Middendorp, Sabine / van Hoesel, Marliek

Journal of visualized experiments. 2019 Oct. 13, , no. 152

2019

Abstract	Dietary lipids are taken up as free fatty acids (FAs) by the intestinal epithelium. These FAs are intracellularly converted into triglyceride (TG) molecules, before they are packaged into chylomicrons for transport to the lymph or into cytosolic lipid droplets (LDs) for intracellular storage. A crucial step for the formation of LDs is the catalytic activity of diacylglycerol acyltransferases (DGAT) in the final step of TG synthesis. LDs are important to buffer toxic lipid species and regulate cellular metabolism in different cell types. Since the human intestinal epithelium is regularly confronted with high concentrations of lipids, LD formation is of great importance to regulate homeostasis. Here we describe a simple assay for the characterization and quantification of LD formation (LDF) upon stimulation with the most common unsaturated fatty acid, oleic acid, in human intestinal organoids. The LDF assay is based on the LD-specific fluorescent dye LD540, which allows for quantification of LDs by confocal microscopy, fluorescent plate reader, or flow cytometry. The LDF assay can be used to characterize LD formation in human intestinal epithelial cells, or to study human (genetic) disorders that affect LD metabolism, such as DGAT1 deficiency. Furthermore, this assay can also be used in a high-throughput pipeline to test novel therapeutic compounds, which restore defects in LD formation in intestinal or other types of organoids.
Keywords	catalytic activity ; chylomicrons ; confocal microscopy ; diacylglycerol acyltransferase ; dietary fat ; droplets ; flow cytometry ; fluorescence ; fluorescent dyes ; free fatty acids ; homeostasis ; humans ; intestinal mucosa ; lymph ; metabolism ; oleic acid ; therapeutics ; toxicity ; triacylglycerols
Language	English
Dates of publication	2019-1013
Size	p. e60150.
Publishing place	Journal of Visualized Experiments
Document type	Article
ZDB-ID	2259946-0
ISSN	1940-087X
ISSN	1940-087X
DOI	10.3791/60150
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Novel approaches: Tissue engineering and stem cells--In vitro modelling of the gut.

van Rijn, Jorik M / Schneeberger, Kerstin / Wiegerinck, Caroline L / Nieuwenhuis, Edward E S / Middendorp, Sabine

Best practice & research. Clinical gastroenterology

2016 Volume 30, Issue 2, Page(s) 281–293

Abstract: In many intestinal diseases, the function of the epithelial lining is impaired. In this review, we describe the recent developments of in vitro intestinal stem cell cultures. When these stem cells are grown in 3D structures (organoids), they provide a ... ...

Abstract	In many intestinal diseases, the function of the epithelial lining is impaired. In this review, we describe the recent developments of in vitro intestinal stem cell cultures. When these stem cells are grown in 3D structures (organoids), they provide a model of the intestinal epithelium, which is closely similar to the growth and development of the in vivo gut. This model provides a new tool to study various diseases of malabsorption in functional detail and therapeutic applications, which could not be achieved with traditional cell lines. First, we describe the organization and function of the healthy small intestinal epithelium. Then, we discuss the establishment of organoid cultures and how these structures represent the healthy epithelium. Finally, we discuss organoid cultures as a tool for studying intrinsic properties of the epithelium, as a model for intestinal disease, and as a possible source for stem cell transplantations.
MeSH term(s)	Cell Differentiation ; Cell Proliferation ; Humans ; Intestinal Mucosa/cytology ; Mechanotransduction, Cellular/physiology ; Models, Biological ; Organoids/metabolism ; Stem Cell Transplantation ; Tissue Engineering/methods
Language	English
Publishing date	2016-04
Publishing country	Netherlands
Document type	Journal Article ; Review
ZDB-ID	2048181-0
ISSN	1532-1916 ; 1521-6918
ISSN (online)	1532-1916
ISSN	1521-6918
DOI	10.1016/j.bpg.2016.03.005
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Article ; Online: Type I interferon promotes cell-to-cell spread of Listeria monocytogenes.

Osborne, Suzanne E / Sit, Brandon / Shaker, Andrew / Currie, Elissa / Tan, Joël M J / van Rijn, Jorik / Higgins, Darren E / Brumell, John H

Cellular microbiology

2017 Volume 19, Issue 3

Abstract: Type I interferons (IFNs) play a critical role in antiviral immune responses, but can be deleterious to the host during some bacterial infections. Listeria monocytogenes (Lm) induces a type I IFN response by activating cytosolic antiviral surveillance ... ...

Abstract	Type I interferons (IFNs) play a critical role in antiviral immune responses, but can be deleterious to the host during some bacterial infections. Listeria monocytogenes (Lm) induces a type I IFN response by activating cytosolic antiviral surveillance pathways. This is beneficial to the bacteria as mice lacking the type I IFN receptor (IFNAR1
MeSH term(s)	Animals ; Disease Models, Animal ; Host-Pathogen Interactions ; Interferon Type I/metabolism ; Listeria monocytogenes/growth & development ; Listeriosis/microbiology ; Listeriosis/pathology ; Liver/microbiology ; Liver/pathology ; Macrophages/microbiology ; Mice ; Receptor, Interferon alpha-beta/metabolism
Chemical Substances	Ifnar1 protein, mouse ; Interferon Type I ; Receptor, Interferon alpha-beta (156986-95-7)
Language	English
Publishing date	2017-03
Publishing country	England
Document type	Journal Article
ZDB-ID	1468320-9
ISSN	1462-5822 ; 1462-5814
ISSN (online)	1462-5822
ISSN	1462-5814
DOI	10.1111/cmi.12660
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Article ; Online: DGAT2 partially compensates for lipid-induced ER stress in human DGAT1-deficient intestinal stem cells.

van Rijn, Jorik M / van Hoesel, Marliek / de Heus, Cecilia / van Vugt, Anke H M / Klumperman, Judith / Nieuwenhuis, Edward E S / Houwen, Roderick H J / Middendorp, Sabine

Journal of lipid research

2019 Volume 60, Issue 10, Page(s) 1787–1800

Abstract: Dietary lipids are taken up as FAs by the intestinal epithelium and converted by diacylglycerol acyltransferase (DGAT) enzymes into triglycerides, which are packaged in chylomicrons or stored in cytoplasmic lipid droplets (LDs). DGAT1-deficient patients ... ...

Abstract	Dietary lipids are taken up as FAs by the intestinal epithelium and converted by diacylglycerol acyltransferase (DGAT) enzymes into triglycerides, which are packaged in chylomicrons or stored in cytoplasmic lipid droplets (LDs). DGAT1-deficient patients suffer from vomiting, diarrhea, and protein losing enteropathy, illustrating the importance of this process to intestinal homeostasis. Previously, we have shown that DGAT1 deficiency causes decreased LD formation and resistance to unsaturated FA lipotoxicity in patient-derived intestinal organoids. However, LD formation was not completely abolished in patient-derived organoids, suggesting the presence of an alternative mechanism for LD formation. Here, we show an unexpected role for DGAT2 in lipid metabolism, as DGAT2 partially compensates for LD formation and lipotoxicity in DGAT1-deficient intestinal stem cells. Furthermore, we show that (un)saturated FA-induced lipotoxicity is mediated by ER stress. More importantly, we demonstrate that overexpression of DGAT2 fully compensates for the loss of DGAT1 in organoids, indicating that induced DGAT2 expression in patient cells may serve as a therapeutic target in the future.
MeSH term(s)	Child, Preschool ; Diacylglycerol O-Acyltransferase/deficiency ; Diacylglycerol O-Acyltransferase/metabolism ; Endoplasmic Reticulum Stress/drug effects ; Female ; Humans ; Intestines/cytology ; Lipid Droplets/drug effects ; Lipid Droplets/metabolism ; Lipids/adverse effects ; Male ; Stem Cells/drug effects ; Stem Cells/metabolism
Chemical Substances	Lipids ; DGAT1 protein, human (EC 2.3.1.20) ; DGAT2 protein, human (EC 2.3.1.20) ; Diacylglycerol O-Acyltransferase (EC 2.3.1.20)
Language	English
Publishing date	2019-07-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80154-9
ISSN	1539-7262 ; 0022-2275
ISSN (online)	1539-7262
ISSN	0022-2275
DOI	10.1194/jlr.M094201
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