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Article ; Online: IL-6/STAT3 Signaling Axis Enhances and Prolongs Pdcd1 Expression in Murine CD8 T Cells.

Powell, Michael D / Lu, Peiyuan / Neeld, Dennis K / Kania, Anna K / George-Alexander, Lou-Ella M M / Bally, Alexander P R / Scharer, Christopher D / Boss, Jeremy M

ImmunoHorizons

2022 Volume 6, Issue 12, Page(s) 872–882

Abstract: CD8 cytotoxic T cells are a potent line of defense against invading pathogens. To aid in curtailing aberrant immune responses, the activation status of CD8 T cells is highly regulated. One mechanism in which CD8 T cell responses are dampened is via ... ...

Abstract	CD8 cytotoxic T cells are a potent line of defense against invading pathogens. To aid in curtailing aberrant immune responses, the activation status of CD8 T cells is highly regulated. One mechanism in which CD8 T cell responses are dampened is via signaling through the immune-inhibitory receptor Programmed Cell Death Protein-1, encoded by Pdcd1. Pdcd1 expression is regulated through engagement of the TCR, as well as by signaling from extracellular cytokines. Understanding such pathways has influenced the development of numerous clinical treatments. In this study, we showed that signals from the cytokine IL-6 enhanced Pdcd1 expression when paired with TCR stimulation in murine CD8 T cells. Mechanistically, signals from IL-6 were propagated through activation of the transcription factor STAT3, resulting in IL-6-dependent binding of STAT3 to Pdcd1 cis-regulatory elements. Intriguingly, IL-6 stimulation overcame B Lymphocyte Maturation Protein 1-mediated epigenetic repression of Pdcd1, which resulted in a transcriptionally permissive landscape marked by heightened histone acetylation. Furthermore, in vivo-activated CD8 T cells derived from lymphocytic choriomeningitis virus infection required STAT3 for optimal Programmed Cell Death Protein-1 surface expression. Importantly, STAT3 was the only member of the STAT family present at Pdcd1 regulatory elements in lymphocytic choriomeningitis virus Ag-specific CD8 T cells. Collectively, these data define mechanisms by which the IL-6/STAT3 signaling axis can enhance and prolong Pdcd1 expression in murine CD8 T cells.
MeSH term(s)	Animals ; Mice ; CD8-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/virology ; Interleukin-6/metabolism ; Lymphocytic Choriomeningitis/immunology ; Lymphocytic Choriomeningitis/virology ; Programmed Cell Death 1 Receptor/metabolism ; Receptors, Antigen, T-Cell/metabolism ; Signal Transduction ; Lymphocytic choriomeningitis virus/immunology
Chemical Substances	Interleukin-6 ; Pdcd1 protein, mouse ; Programmed Cell Death 1 Receptor ; Receptors, Antigen, T-Cell
Language	English
Publishing date	2022-12-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	2573-7732
ISSN (online)	2573-7732
DOI	10.4049/immunohorizons.2100112
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Article ; Online: The Murine MHC Class II Super Enhancer

Majumder, Parimal / Lee, Joshua T / Barwick, Benjamin G / Patterson, Dillon G / Bally, Alexander P R / Scharer, Christopher D / Boss, Jeremy M

Journal of immunology (Baltimore, Md. : 1950)

2021 Volume 206, Issue 9, Page(s) 2221–2232

Abstract: In both humans and mice, CTCF-binding elements form a series of interacting loops across the MHC class II (MHC-II) locus, and CTCF is required for maximal MHC-II gene expression. In humans, a CTCF-bound chromatin insulator ... ...

Abstract	In both humans and mice, CTCF-binding elements form a series of interacting loops across the MHC class II (MHC-II) locus, and CTCF is required for maximal MHC-II gene expression. In humans, a CTCF-bound chromatin insulator termed
MeSH term(s)	Animals ; CCCTC-Binding Factor/genetics ; CCCTC-Binding Factor/immunology ; Genes, MHC Class II/genetics ; Genes, MHC Class II/immunology ; HLA-DQ alpha-Chains/genetics ; HLA-DQ alpha-Chains/immunology ; HLA-DRB1 Chains/genetics ; HLA-DRB1 Chains/immunology ; Mice ; Mice, Inbred C57BL ; Mice, Knockout
Chemical Substances	CCCTC-Binding Factor ; HLA-DQ alpha-Chains ; HLA-DQA1 antigen ; HLA-DRB1 Chains
Language	English
Publishing date	2021-04-16
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2001089
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Article ; Online: Genetic and Epigenetic Regulation of PD-1 Expression.

Bally, Alexander P R / Austin, James W / Boss, Jeremy M

Journal of immunology (Baltimore, Md. : 1950)

2016 Volume 196, Issue 6, Page(s) 2431–2437

Abstract: The inhibitory immune receptor programmed cell death-1 (PD-1) is intricately regulated. In T cells, PD-1 is expressed in response to most immune challenges, but it is rapidly downregulated in acute settings, allowing for normal immune responses. On ... ...

Abstract	The inhibitory immune receptor programmed cell death-1 (PD-1) is intricately regulated. In T cells, PD-1 is expressed in response to most immune challenges, but it is rapidly downregulated in acute settings, allowing for normal immune responses. On chronically stimulated Ag-specific T cells, PD-1 expression remains high, leading to an impaired response to stimuli. Ab blockade of PD-1 interactions during chronic Ag settings partially restores immune function and is now used clinically to treat a variety of devastating cancers. Understanding the regulation of PD-1 expression may be useful for developing novel immune-based therapies. In this review, the molecular mechanisms that drive dynamic PD-1 expression during acute and chronic antigenic stimuli are discussed. An array of cis-DNA elements, transcription factors, and epigenetic components, including DNA methylation and histone modifications, control PD-1 expression. The interplay between these regulators fine-tunes PD-1 expression in different inflammatory environments and across numerous cell types to modulate immune responses.
MeSH term(s)	Animals ; Epigenesis, Genetic/immunology ; Gene Expression Regulation/immunology ; Humans ; Programmed Cell Death 1 Receptor/biosynthesis ; Programmed Cell Death 1 Receptor/genetics ; Programmed Cell Death 1 Receptor/immunology
Chemical Substances	Programmed Cell Death 1 Receptor
Language	English
Publishing date	2016-03-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.1502643
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Article ; Online: Cutting Edge: Chromatin Accessibility Programs CD8 T Cell Memory.

Scharer, Christopher D / Bally, Alexander P R / Gandham, Bhanu / Boss, Jeremy M

Journal of immunology (Baltimore, Md. : 1950)

2017 Volume 198, Issue 6, Page(s) 2238–2243

Abstract: CD8 T cell memory is characterized by rapid recall of effector function, increased proliferation, and reduced activation requirements. Despite the extensive functional characterization, the molecular mechanisms that facilitate these enhanced properties ... ...

Abstract	CD8 T cell memory is characterized by rapid recall of effector function, increased proliferation, and reduced activation requirements. Despite the extensive functional characterization, the molecular mechanisms that facilitate these enhanced properties are not well characterized. In this study, the assay for transposase-accessible chromatin sequencing was employed to map the
MeSH term(s)	Animals ; CD8-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/virology ; Cell Proliferation ; Cells, Cultured ; Chromatin/immunology ; Chromatin Assembly and Disassembly ; Immunologic Memory/genetics ; Lymphocyte Activation ; Lymphocytic Choriomeningitis/immunology ; Lymphocytic choriomeningitis virus/immunology ; Mice ; Mice, Inbred C57BL ; Sequence Analysis, DNA ; T-Lymphocyte Subsets/immunology ; T-Lymphocyte Subsets/virology ; Transposases/metabolism
Chemical Substances	Chromatin ; Transposases (EC 2.7.7.-)
Language	English
Publishing date	2017-03-15
Publishing country	United States
Document type	Journal Article
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.1602086
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Article ; Online: Plasma cell differentiation is controlled by multiple cell division-coupled epigenetic programs.

Scharer, Christopher D / Barwick, Benjamin G / Guo, Muyao / Bally, Alexander P R / Boss, Jeremy M

Nature communications

2018 Volume 9, Issue 1, Page(s) 1698

Abstract: The genomic loci associated with B cell differentiation that are subject to transcriptional and epigenetic regulation in vivo are not well defined, leaving a gap in our understanding of the development of humoral immune responses. Here, using an in vivo ... ...

Abstract	The genomic loci associated with B cell differentiation that are subject to transcriptional and epigenetic regulation in vivo are not well defined, leaving a gap in our understanding of the development of humoral immune responses. Here, using an in vivo T cell independent B cell differentiation model, we define a cellular division-dependent cis-regulatory element road map using ATAC-seq. Chromatin accessibility changes correlate with gene expression and reveal the reprogramming of transcriptional networks and the genes they regulate at specific cell divisions. A subset of genes in naive B cells display accessible promoters in the absence of transcription and are marked by H3K27me3, an EZH2 catalyzed repressive modification. Such genes encode regulators of cell division and metabolism and include the essential plasma cell transcription factor Blimp-1. Chemical inhibition of EZH2 results in enhanced plasma cell formation, increased expression of the above gene set, and premature expression of Blimp-1 ex vivo. These data provide insights into cell-division coupled epigenetic and transcriptional processes that program plasma cells.
MeSH term(s)	Animals ; Cell Differentiation/genetics ; Cell Division/genetics ; Cell Line, Tumor ; DNA Methylation/genetics ; Enhancer of Zeste Homolog 2 Protein/antagonists & inhibitors ; Enhancer of Zeste Homolog 2 Protein/genetics ; Enhancer of Zeste Homolog 2 Protein/metabolism ; Epigenesis, Genetic/genetics ; Histones/metabolism ; Immunity, Humoral/genetics ; Mice, Inbred C57BL ; Mice, Transgenic ; Plasma Cells/physiology ; Positive Regulatory Domain I-Binding Factor 1/genetics ; Positive Regulatory Domain I-Binding Factor 1/metabolism ; Primary Cell Culture ; Promoter Regions, Genetic/genetics
Chemical Substances	Histones ; Prdm1 protein, mouse ; Positive Regulatory Domain I-Binding Factor 1 (EC 2.1.1.-) ; Enhancer of Zeste Homolog 2 Protein (EC 2.1.1.43) ; Ezh2 protein, mouse (EC 2.1.1.43)
Language	English
Publishing date	2018-04-27
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-018-04125-8
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Article ; Online: PD-1 Expression during Acute Infection Is Repressed through an LSD1-Blimp-1 Axis.

Bally, Alexander P R / Neeld, Dennis K / Lu, Peiyuan / Majumder, Parimal / Tang, Yan / Barwick, Benjamin G / Wang, Qing / Boss, Jeremy M

Journal of immunology (Baltimore, Md. : 1950)

2019 Volume 204, Issue 2, Page(s) 449–458

Abstract: During prolonged exposure to Ags, such as chronic viral infections, sustained TCR signaling can result in T cell exhaustion mediated in part by expression of programmed cell death-1 (PD-1) encoded by ... ...

Abstract	During prolonged exposure to Ags, such as chronic viral infections, sustained TCR signaling can result in T cell exhaustion mediated in part by expression of programmed cell death-1 (PD-1) encoded by the
MeSH term(s)	Acetylation ; Acute Disease ; Animals ; CD8-Positive T-Lymphocytes/immunology ; Chronic Disease ; Gene Expression Regulation ; Histone Demethylases/genetics ; Histone Demethylases/metabolism ; Histones/metabolism ; Lymphocyte Activation/genetics ; Lymphocytic Choriomeningitis/metabolism ; Lymphocytic choriomeningitis virus/physiology ; Melanoma/metabolism ; Melanoma, Experimental ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Neoplasms, Experimental ; Positive Regulatory Domain I-Binding Factor 1/metabolism ; Programmed Cell Death 1 Receptor/genetics ; Programmed Cell Death 1 Receptor/metabolism ; Signal Transduction
Chemical Substances	Histones ; PDCD1 protein, human ; Prdm1 protein, mouse ; Programmed Cell Death 1 Receptor ; Histone Demethylases (EC 1.14.11.-) ; KDM1a protein, mouse (EC 1.14.11.-) ; Positive Regulatory Domain I-Binding Factor 1 (EC 2.1.1.-)
Language	English
Publishing date	2019-12-06
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.1900601
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Article ; Online: Plasma cell differentiation is coupled to division-dependent DNA hypomethylation and gene regulation.

Barwick, Benjamin G / Scharer, Christopher D / Bally, Alexander P R / Boss, Jeremy M

Nature immunology

2016 Volume 17, Issue 10, Page(s) 1216–1225

Abstract: The epigenetic processes that regulate antibody-secreting plasma cells are not well understood. Here, analysis of plasma cell differentiation revealed DNA hypomethylation of 10% of CpG loci that were overrepresented at enhancers. Inhibition of DNA ... ...

Abstract	The epigenetic processes that regulate antibody-secreting plasma cells are not well understood. Here, analysis of plasma cell differentiation revealed DNA hypomethylation of 10% of CpG loci that were overrepresented at enhancers. Inhibition of DNA methylation enhanced plasma cell commitment in a cell-division-dependent manner. Analysis of B cells differentiating in vivo stratified by cell division revealed a fivefold increase in mRNA transcription coupled to DNA hypomethylation. Demethylation occurred first at binding motifs for the transcription factors NF-κB and AP-1 and later at those for the transcription factors IRF and Oct-2 and was coincident with activation and differentiation gene-expression programs in a cell-division-dependent manner. These data provide mechanistic insight into cell-division-coupled transcriptional and epigenetic reprogramming and suggest that DNA hypomethylation reflects the cis-regulatory history of plasma cell differentiation.
MeSH term(s)	Animals ; B-Lymphocytes/physiology ; Binding Sites/genetics ; Cell Differentiation/genetics ; Cell Division/genetics ; Cells, Cultured ; CpG Islands/genetics ; DNA Methylation ; Epigenesis, Genetic ; Female ; Gene Expression Regulation ; Immunity, Humoral/genetics ; Interferon Regulatory Factors/genetics ; Interferon Regulatory Factors/metabolism ; Male ; Mice ; Mice, Inbred C57BL ; NF-kappa B/genetics ; NF-kappa B/metabolism ; Octamer Transcription Factor-2/genetics ; Octamer Transcription Factor-2/metabolism ; Plasma Cells/physiology ; Transcription Factor AP-1/genetics ; Transcription Factor AP-1/metabolism
Chemical Substances	Interferon Regulatory Factors ; NF-kappa B ; Octamer Transcription Factor-2 ; Transcription Factor AP-1
Language	English
Publishing date	2016-10
Publishing country	United States
Document type	Journal Article
ZDB-ID	2016987-5
ISSN	1529-2916 ; 1529-2908
ISSN (online)	1529-2916
ISSN	1529-2908
DOI	10.1038/ni.3519
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Article ; Online: Plasma cell differentiation is controlled by multiple cell division-coupled epigenetic programs

Christopher D. Scharer / Benjamin G. Barwick / Muyao Guo / Alexander P. R. Bally / Jeremy M. Boss

Nature Communications, Vol 9, Iss 1, Pp 1-

2018 Volume 14

Abstract: During B cell differentiation, the role of different genomic loci in transcriptional and epigenetic regulation in vivo is not well defined. Here the authors use an in vivo B cell differentiation model to map cellular division-dependent cis-regulatory ... ...

Abstract	During B cell differentiation, the role of different genomic loci in transcriptional and epigenetic regulation in vivo is not well defined. Here the authors use an in vivo B cell differentiation model to map cellular division-dependent cis-regulatory element road map with ATAC-seq.
Keywords	Science ; Q
Language	English
Publishing date	2018-04-01T00:00:00Z
Publisher	Nature Publishing Group
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Plasma cell differentiation is controlled by multiple cell division-coupled epigenetic programs

Christopher D. Scharer / Benjamin G. Barwick / Muyao Guo / Alexander P. R. Bally / Jeremy M. Boss

Nature Communications, Vol 9, Iss 1, Pp 1-

2018 Volume 14

Abstract	During B cell differentiation, the role of different genomic loci in transcriptional and epigenetic regulation in vivo is not well defined. Here the authors use an in vivo B cell differentiation model to map cellular division-dependent cis-regulatory element road map with ATAC-seq.
Keywords	Science ; Q
Language	English
Publishing date	2018-04-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: B cell activation and plasma cell differentiation are inhibited by de novo DNA methylation.

Barwick, Benjamin G / Scharer, Christopher D / Martinez, Ryan J / Price, Madeline J / Wein, Alexander N / Haines, Robert R / Bally, Alexander P R / Kohlmeier, Jacob E / Boss, Jeremy M

Nature communications

2018 Volume 9, Issue 1, Page(s) 1900

Abstract: B cells provide humoral immunity by differentiating into antibody-secreting plasma cells, a process that requires cellular division and is linked to DNA hypomethylation. Conversely, little is known about how de novo deposition of DNA methylation affects ... ...

Abstract	B cells provide humoral immunity by differentiating into antibody-secreting plasma cells, a process that requires cellular division and is linked to DNA hypomethylation. Conversely, little is known about how de novo deposition of DNA methylation affects B cell fate and function. Here we show that genetic deletion of the de novo DNA methyltransferases Dnmt3a and Dnmt3b (Dnmt3-deficient) in mouse B cells results in normal B cell development and maturation, but increased cell activation and expansion of the germinal center B cell and plasma cell populations upon immunization. Gene expression is mostly unaltered in naive and germinal center B cells, but dysregulated in Dnmt3-deficient plasma cells. Differences in gene expression are proximal to Dnmt3-dependent DNA methylation and chromatin changes, both of which coincide with E2A and PU.1-IRF composite-binding motifs. Thus, de novo DNA methylation limits B cell activation, represses the plasma cell chromatin state, and regulates plasma cell differentiation.
MeSH term(s)	Animals ; B-Lymphocytes/cytology ; B-Lymphocytes/immunology ; B-Lymphocytes/metabolism ; Cell Differentiation ; Chromatin/genetics ; Chromatin/metabolism ; DNA (Cytosine-5-)-Methyltransferases/genetics ; DNA (Cytosine-5-)-Methyltransferases/immunology ; DNA Methylation ; DNA Methyltransferase 3A ; Female ; Gene Deletion ; Lymphocyte Activation ; Male ; Mice ; Plasma Cells/cytology ; Plasma Cells/immunology ; Plasma Cells/metabolism ; DNA Methyltransferase 3B
Chemical Substances	Chromatin ; Dnmt3a protein, mouse ; DNA (Cytosine-5-)-Methyltransferases (EC 2.1.1.37) ; DNA Methyltransferase 3A (EC 2.1.1.37)
Language	English
Publishing date	2018-05-15
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; 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/s41467-018-04234-4
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