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Article ; Online: Rspo2 inhibits TCF3 phosphorylation to antagonize Wnt signaling during vertebrate anteroposterior axis specification.

Reis, Alice H / Sokol, Sergei Y

2021 Volume 11, Issue 1, Page(s) 13433

Abstract: The Wnt pathway activates target genes by controlling the β-catenin-T-cell factor (TCF) transcriptional complex during embryonic development and cancer. This pathway can be potentiated by R-spondins, a family of proteins that bind RNF43/ZNRF3 E3 ... ...

Abstract	The Wnt pathway activates target genes by controlling the β-catenin-T-cell factor (TCF) transcriptional complex during embryonic development and cancer. This pathway can be potentiated by R-spondins, a family of proteins that bind RNF43/ZNRF3 E3 ubiquitin ligases and LGR4/5 receptors to prevent Frizzled degradation. Here we demonstrate that, during Xenopus anteroposterior axis specification, Rspo2 functions as a Wnt antagonist, both morphologically and at the level of gene targets and pathway mediators. Unexpectedly, the binding to RNF43/ZNRF3 and LGR4/5 was not required for the Wnt inhibitory activity. Moreover, Rspo2 did not influence Dishevelled phosphorylation in response to Wnt ligands, suggesting that Frizzled activity is not affected. Further analysis indicated that the Wnt antagonism is due to the inhibitory effect of Rspo2 on TCF3/TCF7L1 phosphorylation that normally leads to target gene activation. Consistent with this mechanism, Rspo2 anteriorizing activity has been rescued in TCF3-depleted embryos. These observations suggest that Rspo2 is a context-specific regulator of TCF3 phosphorylation and Wnt signaling.
MeSH term(s)	Animals ; Body Patterning/drug effects ; Body Patterning/physiology ; Embryo, Nonmammalian/abnormalities ; Embryo, Nonmammalian/drug effects ; Embryo, Nonmammalian/metabolism ; Embryonic Development/drug effects ; Gene Expression Regulation, Developmental/drug effects ; Genes, Reporter ; Head/embryology ; Intercellular Signaling Peptides and Proteins/physiology ; Phosphorylation/drug effects ; Protein Processing, Post-Translational/drug effects ; Transcription Factor 3/antagonists & inhibitors ; Transcription Factor 3/metabolism ; Wnt Signaling Pathway/drug effects ; Xenopus Proteins/antagonists & inhibitors ; Xenopus Proteins/biosynthesis ; Xenopus Proteins/genetics ; Xenopus Proteins/metabolism ; Xenopus Proteins/pharmacology ; Xenopus Proteins/physiology ; Xenopus laevis/embryology
Chemical Substances	Intercellular Signaling Peptides and Proteins ; Rspo2 protein, Xenopus ; Tcf3 protein, Xenopus ; Transcription Factor 3 ; Xenopus Proteins
Language	English
Publishing date	2021-06-28
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-92824-6
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Human embryoids: A new strategy of recreating the first steps of embryonic development in vitro.

Zhang, Miaoci / Reis, Alice H / Simunovic, Mijo

Seminars in cell & developmental biology

2022 Volume 141, Page(s) 14–22

Abstract: Molecular mechanisms surrounding early human embryonic events such as blastocyst formation, implantation, and the specification of the body axes are some of the most attractive research questions of developmental biology today. A knowledge on the ... ...

Abstract	Molecular mechanisms surrounding early human embryonic events such as blastocyst formation, implantation, and the specification of the body axes are some of the most attractive research questions of developmental biology today. A knowledge on the detailed signaling landscape underlying these critical events in the human could impact the way we treat early pregnancy disorders and infertility, and considerably advance our abilities to make precise human tissues in a lab. However, owing to ethical, technical, and policy restrictions, research on early human embryo development historically stalled behind animal models. The rapid progress in 3D culture of human embryonic stem cells over the past years created an opportunity to overcome this critical challenge. We review recently developed strategies of making 3D models of the human embryo built from embryonic stem cells, which we refer to as embryoids. We focus on models aimed at reconstituting the 3D epithelial characteristics of the early human embryo, namely the intra/extraembryonic signaling crosstalk, tissue polarity, and embryonic cavities. We identify distinct classes of embryoids based on whether they explicitly include extraembryonic tissues and we argue for the merit of compromising on certain aspects of embryo mimicry in balancing the experimental feasibility with ethical considerations. Human embryoids open gates toward a new field of synthetic human embryology, allowing to study the long inaccessible stages of early human development at unprecedented detail.
MeSH term(s)	Pregnancy ; Animals ; Female ; Humans ; Embryonic Development ; Embryo Implantation ; Embryo, Mammalian ; Embryonic Stem Cells
Language	English
Publishing date	2022-07-21
Publishing country	England
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1016/j.semcdb.2022.07.003
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Article ; Online: Rspo2 antagonizes FGF signaling during vertebrate mesoderm formation and patterning.

Reis, Alice H / Sokol, Sergei Y

Development (Cambridge, England)

2020 Volume 147, Issue 10

Abstract: R-spondins are a family of secreted proteins that play important roles in embryonic development and cancer. R-spondins have been shown to modulate the Wnt pathway; however, their involvement in other developmental signaling processes have remained ... ...

Abstract	R-spondins are a family of secreted proteins that play important roles in embryonic development and cancer. R-spondins have been shown to modulate the Wnt pathway; however, their involvement in other developmental signaling processes have remained largely unstudied. Here, we describe a novel function of Rspo2 in FGF pathway regulation
MeSH term(s)	Animals ; Body Patterning/genetics ; Down-Regulation/genetics ; Ectoderm/embryology ; Ectoderm/metabolism ; Fibroblast Growth Factor 2/metabolism ; Fibroblast Growth Factor 2/pharmacology ; Gastrulation/genetics ; Gene Expression Regulation, Developmental ; Intercellular Signaling Peptides and Proteins ; Mesoderm/embryology ; Mesoderm/metabolism ; Mutagenesis, Site-Directed/methods ; Protein Domains ; Receptor, Fibroblast Growth Factor, Type 1/genetics ; Signal Transduction/genetics ; Wnt Signaling Pathway/genetics ; Xenopus Proteins/genetics ; Xenopus Proteins/metabolism ; Xenopus laevis/embryology ; Xenopus laevis/genetics ; Xenopus laevis/metabolism
Chemical Substances	Intercellular Signaling Peptides and Proteins ; Rspo2 protein, Xenopus ; Xenopus Proteins ; Fibroblast Growth Factor 2 (103107-01-3) ; Receptor, Fibroblast Growth Factor, Type 1 (EC 2.7.10.1)
Language	English
Publishing date	2020-05-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	90607-4
ISSN	1477-9129 ; 0950-1991
ISSN (online)	1477-9129
ISSN	0950-1991
DOI	10.1242/dev.189324
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Article ; Online: Rspo2 inhibits TCF3 phosphorylation to antagonize Wnt signaling during vertebrate anteroposterior axis specification

Alice H. Reis / Sergei Y. Sokol

Scientific Reports, Vol 11, Iss 1, Pp 1-

2021 Volume 11

Abstract: Abstract The Wnt pathway activates target genes by controlling the β-catenin-T-cell factor (TCF) transcriptional complex during embryonic development and cancer. This pathway can be potentiated by R-spondins, a family of proteins that bind RNF43/ZNRF3 E3 ...

Abstract	Abstract The Wnt pathway activates target genes by controlling the β-catenin-T-cell factor (TCF) transcriptional complex during embryonic development and cancer. This pathway can be potentiated by R-spondins, a family of proteins that bind RNF43/ZNRF3 E3 ubiquitin ligases and LGR4/5 receptors to prevent Frizzled degradation. Here we demonstrate that, during Xenopus anteroposterior axis specification, Rspo2 functions as a Wnt antagonist, both morphologically and at the level of gene targets and pathway mediators. Unexpectedly, the binding to RNF43/ZNRF3 and LGR4/5 was not required for the Wnt inhibitory activity. Moreover, Rspo2 did not influence Dishevelled phosphorylation in response to Wnt ligands, suggesting that Frizzled activity is not affected. Further analysis indicated that the Wnt antagonism is due to the inhibitory effect of Rspo2 on TCF3/TCF7L1 phosphorylation that normally leads to target gene activation. Consistent with this mechanism, Rspo2 anteriorizing activity has been rescued in TCF3-depleted embryos. These observations suggest that Rspo2 is a context-specific regulator of TCF3 phosphorylation and Wnt signaling.
Keywords	Medicine ; R ; Science ; Q
Subject code	570
Language	English
Publishing date	2021-06-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Identification of the centrosomal maturation factor SSX2IP as a Wtip-binding partner by targeted proximity biotinylation.

Reis, Alice H / Xiang, Bo / Ossipova, Olga / Itoh, Keiji / Sokol, Sergei Y

PloS one

2021 Volume 16, Issue 10, Page(s) e0259068

Abstract: Wilms tumor-1-interacting protein (Wtip) is a LIM-domain-containing adaptor that links cell junctions with actomyosin complexes and modulates actomyosin contractility and ciliogenesis in Xenopus embryos. The Wtip C-terminus with three LIM domains ... ...

Abstract	Wilms tumor-1-interacting protein (Wtip) is a LIM-domain-containing adaptor that links cell junctions with actomyosin complexes and modulates actomyosin contractility and ciliogenesis in Xenopus embryos. The Wtip C-terminus with three LIM domains associates with the actin-binding protein Shroom3 and modulates Shroom3-induced apical constriction in ectoderm cells. By contrast, the N-terminal domain localizes to apical junctions in the ectoderm and basal bodies in skin multiciliated cells, but its interacting partners remain largely unknown. Targeted proximity biotinylation (TPB) using anti-GFP antibody fused to the biotin ligase BirA identified SSX2IP as a candidate protein that binds GFP-WtipN. SSX2IP, also known as Msd1 or ADIP, is a component of cell junctions, centriolar satellite protein and a targeting factor for ciliary membrane proteins. WtipN physically associated with SSX2IP and the two proteins readily formed mixed aggregates in overexpressing cells. By contrast, we observed only partial colocalization of full length Wtip and SSX2IP, suggesting that Wtip adopts a 'closed' conformation in the cell. Furthermore, the double depletion of Wtip and SSX2IP in early embryos uncovered the functional interaction of the two proteins during neural tube closure. Our results suggest that the association of SSX2IP and Wtip is essential for cell junction remodeling and morphogenetic processes that accompany neurulation. We propose that TPB can be a general approach that is applicable to other GFP-tagged proteins.
MeSH term(s)	Adaptor Proteins, Signal Transducing/metabolism ; Animals ; Biotinylation ; Cytoskeletal Proteins/metabolism ; Mass Spectrometry ; Microtubule-Associated Proteins/metabolism ; Protein Binding ; Transcription Factors/metabolism ; Xenopus Proteins/metabolism ; Xenopus laevis
Chemical Substances	Adaptor Proteins, Signal Transducing ; Cytoskeletal Proteins ; Microtubule-Associated Proteins ; Transcription Factors ; Xenopus Proteins ; wtip protein, Xenopus
Language	English
Publishing date	2021-10-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2267670-3
ISSN	1932-6203 ; 1932-6203
ISSN (online)	1932-6203
ISSN	1932-6203
DOI	10.1371/journal.pone.0259068
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Establishing embryonic territories in the context of Wnt signaling.

Velloso, Ian / Maia, Lorena A / Amado, Nathalia G / Reis, Alice H / He, Xi / Abreu, Jose G

The International journal of developmental biology

2020 Volume 65, Issue 4-5-6, Page(s) 227–233

Abstract: This review highlights the work that my research group has been developing, together with international collaborators, during the last decade. Since we were able to establish ... ...

Abstract	This review highlights the work that my research group has been developing, together with international collaborators, during the last decade. Since we were able to establish the
MeSH term(s)	Animals ; Body Patterning ; Ectoderm/metabolism ; Embryonic Induction ; Gastrula/metabolism ; Gene Expression Regulation, Developmental ; Wnt Signaling Pathway ; Xenopus Proteins/genetics ; Xenopus laevis/metabolism
Chemical Substances	Xenopus Proteins
Language	English
Publishing date	2020-09-09
Publishing country	Spain
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1036070-0
ISSN	1696-3547 ; 0214-6282
ISSN (online)	1696-3547
ISSN	0214-6282
DOI	10.1387/ijdb.200231ja
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Zs.A 3202: Show issues

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Article ; Online: Identification of the centrosomal maturation factor SSX2IP as a Wtip-binding partner by targeted proximity biotinylation.

Alice H Reis / Bo Xiang / Olga Ossipova / Keiji Itoh / Sergei Y Sokol

PLoS ONE, Vol 16, Iss 10, p e

2021 Volume 0259068

Abstract	Wilms tumor-1-interacting protein (Wtip) is a LIM-domain-containing adaptor that links cell junctions with actomyosin complexes and modulates actomyosin contractility and ciliogenesis in Xenopus embryos. The Wtip C-terminus with three LIM domains associates with the actin-binding protein Shroom3 and modulates Shroom3-induced apical constriction in ectoderm cells. By contrast, the N-terminal domain localizes to apical junctions in the ectoderm and basal bodies in skin multiciliated cells, but its interacting partners remain largely unknown. Targeted proximity biotinylation (TPB) using anti-GFP antibody fused to the biotin ligase BirA identified SSX2IP as a candidate protein that binds GFP-WtipN. SSX2IP, also known as Msd1 or ADIP, is a component of cell junctions, centriolar satellite protein and a targeting factor for ciliary membrane proteins. WtipN physically associated with SSX2IP and the two proteins readily formed mixed aggregates in overexpressing cells. By contrast, we observed only partial colocalization of full length Wtip and SSX2IP, suggesting that Wtip adopts a 'closed' conformation in the cell. Furthermore, the double depletion of Wtip and SSX2IP in early embryos uncovered the functional interaction of the two proteins during neural tube closure. Our results suggest that the association of SSX2IP and Wtip is essential for cell junction remodeling and morphogenetic processes that accompany neurulation. We propose that TPB can be a general approach that is applicable to other GFP-tagged proteins.
Keywords	Medicine ; R ; Science ; Q
Subject code	571
Language	English
Publishing date	2021-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Identification of the centrosomal maturation factor SSX2IP as a Wtip-binding partner by targeted proximity biotinylation

Alice H. Reis / Bo Xiang / Olga Ossipova / Keiji Itoh / Sergei Y. Sokol

PLoS ONE, Vol 16, Iss

2021 Volume 10

Abstract	Wilms tumor-1-interacting protein (Wtip) is a LIM-domain-containing adaptor that links cell junctions with actomyosin complexes and modulates actomyosin contractility and ciliogenesis in Xenopus embryos. The Wtip C-terminus with three LIM domains associates with the actin-binding protein Shroom3 and modulates Shroom3-induced apical constriction in ectoderm cells. By contrast, the N-terminal domain localizes to apical junctions in the ectoderm and basal bodies in skin multiciliated cells, but its interacting partners remain largely unknown. Targeted proximity biotinylation (TPB) using anti-GFP antibody fused to the biotin ligase BirA identified SSX2IP as a candidate protein that binds GFP-WtipN. SSX2IP, also known as Msd1 or ADIP, is a component of cell junctions, centriolar satellite protein and a targeting factor for ciliary membrane proteins. WtipN physically associated with SSX2IP and the two proteins readily formed mixed aggregates in overexpressing cells. By contrast, we observed only partial colocalization of full length Wtip and SSX2IP, suggesting that Wtip adopts a ‘closed’ conformation in the cell. Furthermore, the double depletion of Wtip and SSX2IP in early embryos uncovered the functional interaction of the two proteins during neural tube closure. Our results suggest that the association of SSX2IP and Wtip is essential for cell junction remodeling and morphogenetic processes that accompany neurulation. We propose that TPB can be a general approach that is applicable to other GFP-tagged proteins.
Keywords	Medicine ; R ; Science ; Q
Subject code	571
Language	English
Publishing date	2021-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Isolation of nanobodies against Xenopus embryonic antigens using immune and non-immune phage display libraries.

Itoh, Keiji / Reis, Alice H / Hayhurst, Andrew / Sokol, Sergei Y

PloS one

2019 Volume 14, Issue 5, Page(s) e0216083

Abstract: The use of Xenopus laevis as a model for vertebrate developmental biology is limited by a lack of antibodies specific for embryonic antigens. This study evaluated the use of immune and non-immune phage display libraries for the isolation of single domain ...

Abstract	The use of Xenopus laevis as a model for vertebrate developmental biology is limited by a lack of antibodies specific for embryonic antigens. This study evaluated the use of immune and non-immune phage display libraries for the isolation of single domain antibodies, or nanobodies, with specificities for Xenopus embryonic antigens. The immune nanobody library was derived from peripheral blood lymphocyte RNA obtained from a llama immunized with Xenopus gastrula homogenates. Screening this library by immunostaining of embryonic tissues with pooled periplasmic material and sib-selection led to the isolation of several monoclonal phages reactive with the cytoplasm and nuclei of gastrula cells. One antigen recognized by a group of nanobodies was identified using a reverse proteomics approach as nucleoplasmin, an abundant histone chaperone. As an alternative strategy, a semi-synthetic non-immune llama nanobody phage display library was panned on highly purified Xenopus proteins. This proof-of-principle approach isolated monoclonal nanobodies that specifically bind Nuclear distribution element-like 1 (Ndel1) in multiple immunoassays. Our results suggest that immune and non-immune phage display screens on crude and purified embryonic antigens can efficiently identify nanobodies useful to the Xenopus developmental biology community.
MeSH term(s)	Amino Acid Sequence ; Animals ; Antibodies/isolation & purification ; Antibodies/metabolism ; Antigens/immunology ; Cell Surface Display Techniques/methods ; Cytoskeletal Proteins/immunology ; Embryonic Development/immunology ; Gastrula ; Peptide Library ; Single-Domain Antibodies/immunology ; Single-Domain Antibodies/isolation & purification ; Stage-Specific Embryonic Antigens/metabolism ; Xenopus Proteins/genetics ; Xenopus Proteins/immunology ; Xenopus laevis/embryology ; Xenopus laevis/immunology ; Xenopus laevis/metabolism
Chemical Substances	Antibodies ; Antigens ; Cytoskeletal Proteins ; Ndel1 protein, Xenopus ; Peptide Library ; Single-Domain Antibodies ; Stage-Specific Embryonic Antigens ; Xenopus Proteins
Language	English
Publishing date	2019-05-02
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0216083
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Isolation of nanobodies against Xenopus embryonic antigens using immune and non-immune phage display libraries.

Keiji Itoh / Alice H Reis / Andrew Hayhurst / Sergei Y Sokol

PLoS ONE, Vol 14, Iss 5, p e

2019 Volume 0216083

Abstract	The use of Xenopus laevis as a model for vertebrate developmental biology is limited by a lack of antibodies specific for embryonic antigens. This study evaluated the use of immune and non-immune phage display libraries for the isolation of single domain antibodies, or nanobodies, with specificities for Xenopus embryonic antigens. The immune nanobody library was derived from peripheral blood lymphocyte RNA obtained from a llama immunized with Xenopus gastrula homogenates. Screening this library by immunostaining of embryonic tissues with pooled periplasmic material and sib-selection led to the isolation of several monoclonal phages reactive with the cytoplasm and nuclei of gastrula cells. One antigen recognized by a group of nanobodies was identified using a reverse proteomics approach as nucleoplasmin, an abundant histone chaperone. As an alternative strategy, a semi-synthetic non-immune llama nanobody phage display library was panned on highly purified Xenopus proteins. This proof-of-principle approach isolated monoclonal nanobodies that specifically bind Nuclear distribution element-like 1 (Ndel1) in multiple immunoassays. Our results suggest that immune and non-immune phage display screens on crude and purified embryonic antigens can efficiently identify nanobodies useful to the Xenopus developmental biology community.
Keywords	Medicine ; R ; Science ; Q
Subject code	570
Language	English
Publishing date	2019-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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