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Article ; Online: A mutation in Themis contributes to anaphylaxis severity following oral peanut challenge in CC027 mice.

Risemberg, Ellen L / Smeekens, Johanna M / Cruz Cisneros, Marta C / Hampton, Brea K / Hock, Pablo / Linnertz, Colton L / Miller, Darla R / Orgel, Kelly / Shaw, Ginger D / Manuel de Villena, Fernando Pardo / Burks, A Wesley / Valdar, William / Kulis, Michael D / Ferris, Martin T

The Journal of allergy and clinical immunology

2024

Abstract: Background: The development of peanut allergy is due to a combination of genetic and environmental factors, although specific genes have proven difficult to identify. Previously, we reported that peanut-sensitized CC027/GeniUnc (CC027) mice develop ... ...

Abstract	Background: The development of peanut allergy is due to a combination of genetic and environmental factors, although specific genes have proven difficult to identify. Previously, we reported that peanut-sensitized CC027/GeniUnc (CC027) mice develop anaphylaxis upon oral challenge to peanut, unlike C3H/HeJ (C3H) mice. Objective: To determine the genetic basis of orally-induced anaphylaxis to peanut in CC027 mice. Methods: A genetic mapping population between CC027 and C3H mice was designed to identify the genetic factors that drive oral anaphylaxis. A total of 356 CC027xC3H backcrossed mice were generated, sensitized to peanut, then challenged to peanut by oral gavage. Anaphylaxis and peanut-specific IgE were quantified for all mice. T-cell phenotyping was conducted on CC027 and five additional CC strains. Results: Anaphylaxis to peanut was absent in 77% of backcrossed mice, with 19% showing moderate anaphylaxis, and 4% having severe anaphylaxis. A total of eight genetic loci were associated with variation in response to peanut challenge, six associated with anaphylaxis (temperature decrease) and two associated with peanut-specific IgE levels. There were two major loci that impacted multiple aspects of the severity of acute anaphylaxis, at which the CC027 allele was associated with worse outcome. At one of these loci, CC027 has a private genetic variant in the Themis (thymocyte-expressed molecule involved in selection) gene. Consistent with Themis' described functions, we found that CC027 have more immature T cells with fewer CD8+, CD4+, and CD4+CD25+CD127- regulatory T cells. Conclusion: Our results demonstrate a key role for Themis in the orally-reactive CC027 mouse model of peanut allergy.
Language	English
Publishing date	2024-04-24
Publishing country	United States
Document type	Journal Article
ZDB-ID	121011-7
ISSN	1097-6825 ; 1085-8725 ; 0091-6749
ISSN (online)	1097-6825 ; 1085-8725
ISSN	0091-6749
DOI	10.1016/j.jaci.2024.03.027
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Article: Host Genetic Variation Impacts SARS-CoV-2 Vaccination Response in the Diversity Outbred Mouse Population.

Vaccines

2024 Volume 12, Issue 1

Abstract: The COVID-19 pandemic led to the rapid and worldwide development of highly effective vaccines against SARS-CoV-2. However, there is significant individual-to-individual variation in vaccine efficacy due to factors including viral variants, host age, ... ...

Abstract	The COVID-19 pandemic led to the rapid and worldwide development of highly effective vaccines against SARS-CoV-2. However, there is significant individual-to-individual variation in vaccine efficacy due to factors including viral variants, host age, immune status, environmental and host genetic factors. Understanding those determinants driving this variation may inform the development of more broadly protective vaccine strategies. While host genetic factors are known to impact vaccine efficacy for respiratory pathogens such as influenza and tuberculosis, the impact of host genetic variation on vaccine efficacy against COVID-19 is not well understood. To model the impact of host genetic variation on SARS-CoV-2 vaccine efficacy, while controlling for the impact of non-genetic factors, we used the Diversity Outbred (DO) mouse model. We found that DO mice immunized against SARS-CoV-2 exhibited high levels of variation in vaccine-induced neutralizing antibody responses. While the majority of the vaccinated mice were protected from virus-induced disease, similar to human populations, we observed vaccine breakthrough in a subset of mice. Importantly, we found that this variation in neutralizing antibody, virus-induced disease, and viral titer is heritable, indicating that the DO serves as a useful model system for studying the contribution of genetic variation of both vaccines and disease outcomes.
Language	English
Publishing date	2024-01-20
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2703319-3
ISSN	2076-393X
ISSN	2076-393X
DOI	10.3390/vaccines12010103
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Article: A mutation in

Risemberg, Ellen L / Smeekens, Johanna M / Cisneros, Marta C Cruz / Hampton, Brea K / Hock, Pablo / Linnertz, Colton L / Miller, Darla R / Orgel, Kelly / Shaw, Ginger D / de Villena, Fernando Pardo Manuel / Burks, A Wesley / Valdar, William / Kulis, Michael D / Ferris, Martin T

bioRxiv : the preprint server for biology

2023

Abstract	Background: The development of peanut allergy is due to a combination of genetic and environmental factors, although specific genes have proven difficult to identify. Previously, we reported that peanut-sensitized CC027/GeniUnc (CC027) mice develop anaphylaxis upon oral challenge to peanut, unlike C3H/HeJ (C3H) mice. Objective: To determine the genetic basis of orally-induced anaphylaxis to peanut in CC027 mice. Methods: A genetic mapping population between CC027 and C3H mice was designed to identify the genetic factors that drive oral anaphylaxis. A total of 356 CC027xC3H backcrossed mice were generated, sensitized to peanut, then challenged to peanut by oral gavage. Anaphylaxis and peanut-specific IgE were quantified for all mice. T-cell phenotyping was conducted on CC027 and five additional CC strains. Results: Anaphylaxis to peanut was absent in 77% of backcrossed mice, with 19% showing moderate anaphylaxis, and 4% having severe anaphylaxis. A total of eight genetic loci were associated with variation in response to peanut challenge, six associated with anaphylaxis (temperature decrease) and two associated with peanut-specific IgE levels. There were two major loci that impacted multiple aspects of the severity of acute anaphylaxis, at which the CC027 allele was associated with worse outcome. At one of these loci, CC027 has a private genetic variant in the Conclusion: Our results demonstrate a key role for
Language	English
Publishing date	2023-09-13
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.13.557467
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Article ; Online: Forward genetic screen of homeostatic antibody levels in the Collaborative Cross identifies MBD1 as a novel regulator of B cell homeostasis.

Hampton, Brea K / Plante, Kenneth S / Whitmore, Alan C / Linnertz, Colton L / Madden, Emily A / Noll, Kelsey E / Boyson, Samuel P / Parotti, Breantie / Xenakis, James G / Bell, Timothy A / Hock, Pablo / Shaw, Ginger D / de Villena, Fernando Pardo-Manuel / Ferris, Martin T / Heise, Mark T

PLoS genetics

2022 Volume 18, Issue 12, Page(s) e1010548

Abstract: Variation in immune homeostasis, the state in which the immune system is maintained in the absence of stimulation, is highly variable across populations. This variation is attributed to both genetic and environmental factors. However, the identity and ... ...

Abstract	Variation in immune homeostasis, the state in which the immune system is maintained in the absence of stimulation, is highly variable across populations. This variation is attributed to both genetic and environmental factors. However, the identity and function of specific regulators have been difficult to identify in humans. We evaluated homeostatic antibody levels in the serum of the Collaborative Cross (CC) mouse genetic reference population. We found heritable variation in all antibody isotypes and subtypes measured. We identified 4 quantitative trait loci (QTL) associated with 3 IgG subtypes: IgG1, IgG2b, and IgG2c. While 3 of these QTL map to genome regions of known immunological significance (major histocompatibility and immunoglobulin heavy chain locus), Qih1 (associated with variation in IgG1) mapped to a novel locus on Chromosome 18. We further associated this locus with B cell proportions in the spleen and identify Methyl-CpG binding domain protein 1 under this locus as a novel regulator of homeostatic IgG1 levels in the serum and marginal zone B cells (MZB) in the spleen, consistent with a role in MZB differentiation to antibody secreting cells.
MeSH term(s)	Mice ; Humans ; Animals ; Quantitative Trait Loci/genetics ; Collaborative Cross Mice/genetics ; Lymphocyte Activation ; Immunoglobulin G/genetics ; Homeostasis/genetics ; DNA-Binding Proteins/genetics ; Transcription Factors/genetics
Chemical Substances	Immunoglobulin G ; MBD1 protein, human ; DNA-Binding Proteins ; Transcription Factors ; Mbd1 protein, mouse
Language	English
Publishing date	2022-12-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1010548
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Article ; Online: Genetic loci regulate Sarbecovirus pathogenesis: A comparison across mice and humans.

Schäfer, Alexandra / Gralinski, Lisa E / Leist, Sarah R / Hampton, Brea K / Mooney, Michael A / Jensen, Kara L / Graham, Rachel L / Agnihothram, Sudhakar / Jeng, Sophia / Chamberlin, Steven / Bell, Timothy A / Scobey, D Trevor / Linnertz, Colton L / VanBlargan, Laura A / Thackray, Larissa B / Hock, Pablo / Miller, Darla R / Shaw, Ginger D / Diamond, Michael S /

de Villena, Fernando Pardo Manuel / McWeeney, Shannon K / Heise, Mark T / Menachery, Vineet D / Ferris, Martin T / Baric, Ralph S

Virus research

2024 Volume 344, Page(s) 199357

Abstract: Coronavirus (CoV) cause considerable morbidity and mortality in humans and other mammals, as evidenced by the emergence of Severe Acute Respiratory CoV (SARS-CoV) in 2003, Middle East Respiratory CoV (MERS-CoV) in 2012, and SARS-CoV-2 in 2019. Although ... ...

Abstract	Coronavirus (CoV) cause considerable morbidity and mortality in humans and other mammals, as evidenced by the emergence of Severe Acute Respiratory CoV (SARS-CoV) in 2003, Middle East Respiratory CoV (MERS-CoV) in 2012, and SARS-CoV-2 in 2019. Although poorly characterized, natural genetic variation in human and other mammals modulate virus pathogenesis, as reflected by the spectrum of clinical outcomes ranging from asymptomatic infections to lethal disease. Using multiple human epidemic and zoonotic Sarbecoviruses, coupled with murine Collaborative Cross genetic reference populations, we identify several dozen quantitative trait loci that regulate SARS-like group-2B CoV pathogenesis and replication. Under a Chr4 QTL, we deleted a candidate interferon stimulated gene, Trim14 which resulted in enhanced SARS-CoV titers and clinical disease, suggesting an antiviral role during infection. Importantly, about 60 % of the murine QTL encode susceptibility genes identified as priority candidates from human genome-wide association studies (GWAS) studies after SARS-CoV-2 infection, suggesting that similar selective forces have targeted analogous genes and pathways to regulate Sarbecovirus disease across diverse mammalian hosts. These studies provide an experimental platform in rodents to investigate the molecular-genetic mechanisms by which potential cross mammalian susceptibility loci and genes regulate type-specific and cross-SARS-like group 2B CoV replication, immunity, and pathogenesis in rodent models. Our study also provides a paradigm for identifying susceptibility loci for other highly heterogeneous and virulent viruses that sporadically emerge from zoonotic reservoirs to plague human and animal populations.
MeSH term(s)	Animals ; Humans ; Mice ; Quantitative Trait Loci ; SARS-CoV-2/genetics ; Virus Replication ; Genome-Wide Association Study ; COVID-19/virology ; Tripartite Motif Proteins/genetics ; Coronavirus Infections/virology ; Coronavirus Infections/genetics ; Disease Models, Animal
Chemical Substances	Tripartite Motif Proteins
Language	English
Publishing date	2024-03-23
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Comparative Study
ZDB-ID	605780-9
ISSN	1872-7492 ; 0168-1702
ISSN (online)	1872-7492
ISSN	0168-1702
DOI	10.1016/j.virusres.2024.199357
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Article ; Online: Fc-mediated pan-sarbecovirus protection after alphavirus vector vaccination.

Adams, Lily E / Leist, Sarah R / Dinnon, Kenneth H / West, Ande / Gully, Kendra L / Anderson, Elizabeth J / Loome, Jennifer F / Madden, Emily A / Powers, John M / Schäfer, Alexandra / Sarkar, Sanjay / Castillo, Izabella N / Maron, Jenny S / McNamara, Ryan P / Bertera, Harry L / Zweigert, Mark R / Higgins, Jaclyn S / Hampton, Brea K / Premkumar, Lakshmanane /

Alter, Galit / Montgomery, Stephanie A / Baxter, Victoria K / Heise, Mark T / Baric, Ralph S

Cell reports

2023 Volume 42, Issue 4, Page(s) 112326

Abstract: Group 2B β-coronaviruses (sarbecoviruses) have caused regional and global epidemics in modern history. Here, we evaluate the mechanisms of cross-sarbecovirus protective immunity, currently less clear yet important for pan-sarbecovirus vaccine development, ...

Abstract	Group 2B β-coronaviruses (sarbecoviruses) have caused regional and global epidemics in modern history. Here, we evaluate the mechanisms of cross-sarbecovirus protective immunity, currently less clear yet important for pan-sarbecovirus vaccine development, using a panel of alphavirus-vectored vaccines covering bat to human strains. While vaccination does not prevent virus replication, it protects against lethal heterologous disease outcomes in both severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and clade 2 bat sarbecovirus challenge models. The spike vaccines tested primarily elicit a highly S1-specific homologous neutralizing antibody response with no detectable cross-virus neutralization. Rather, non-neutralizing antibody functions, mechanistically linked to FcgR4 and spike S2, mediate cross-protection in wild-type mice. Protection is lost in FcR knockout mice, further supporting a model for non-neutralizing, protective antibodies. These data highlight the importance of FcR-mediated cross-protective immune responses in universal pan-sarbecovirus vaccine designs.
MeSH term(s)	Humans ; Animals ; Mice ; Viral Vaccines ; Antibodies, Viral ; Alphavirus ; Severe acute respiratory syndrome-related coronavirus ; Chiroptera ; SARS-CoV-2 ; COVID-19/prevention & control ; Antibodies, Neutralizing ; Vaccination
Chemical Substances	Viral Vaccines ; Antibodies, Viral ; Antibodies, Neutralizing
Language	English
Publishing date	2023-03-30
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2023.112326
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Article: Fc mediated pan-sarbecovirus protection after alphavirus vector vaccination.

Alter, Galit / Montgomery, Stephanie A / Baxter, Victoria K / Heise, Mark T / Baric, Ralph S

bioRxiv : the preprint server for biology

2022

Abstract: Two group 2B β-coronaviruses (sarbecoviruses) have caused regional and global epidemics in modern history. The mechanisms of cross protection driven by the sarbecovirus spike, a dominant immunogen, are less clear yet critically important for pan- ... ...

Abstract	Two group 2B β-coronaviruses (sarbecoviruses) have caused regional and global epidemics in modern history. The mechanisms of cross protection driven by the sarbecovirus spike, a dominant immunogen, are less clear yet critically important for pan-sarbecovirus vaccine development. We evaluated the mechanisms of cross-sarbecovirus protective immunity using a panel of alphavirus-vectored vaccines covering bat to human strains. While vaccination did not prevent virus replication, it protected against lethal heterologous disease outcomes in both SARS-CoV-2 and clade 2 bat sarbecovirus HKU3-SRBD challenge models. The spike vaccines tested primarily elicited a highly S1-specific homologous neutralizing antibody response with no detectable cross-virus neutralization. We found non-neutralizing antibody functions that mediated cross protection in wild-type mice were mechanistically linked to FcgR4 and spike S2-binding antibodies. Protection was lost in FcR knockout mice, further supporting a model for non-neutralizing, protective antibodies. These data highlight the importance of FcR-mediated cross-protective immune responses in universal pan-sarbecovirus vaccine designs.
Language	English
Publishing date	2022-11-28
Publishing country	United States
Document type	Preprint
DOI	10.1101/2022.11.28.518175
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Article ; Online: Host-pathogen genetic interactions underlie tuberculosis susceptibility in genetically diverse mice.

Smith, Clare M / Baker, Richard E / Proulx, Megan K / Mishra, Bibhuti B / Long, Jarukit E / Park, Sae Woong / Lee, Ha-Na / Kiritsy, Michael C / Bellerose, Michelle M / Olive, Andrew J / Murphy, Kenan C / Papavinasasundaram, Kadamba / Boehm, Frederick J / Reames, Charlotte J / Meade, Rachel K / Hampton, Brea K / Linnertz, Colton L / Shaw, Ginger D / Hock, Pablo /

Bell, Timothy A / Ehrt, Sabine / Schnappinger, Dirk / Pardo-Manuel de Villena, Fernando / Ferris, Martin T / Ioerger, Thomas R / Sassetti, Christopher M

eLife

2022 Volume 11

Abstract: The outcome of an encounter ... ...

Abstract	The outcome of an encounter with
MeSH term(s)	Animals ; Collaborative Cross Mice/genetics ; Disease Models, Animal ; Genetic Predisposition to Disease ; Genetic Variation ; Genotype ; Host-Pathogen Interactions/genetics ; Male ; Mice ; Mycobacterium tuberculosis/genetics ; Mycobacterium tuberculosis/pathogenicity ; Phenotype ; Tuberculosis/microbiology
Language	English
Publishing date	2022-02-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.74419
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Article ; Online: Fc mediated pan-sarbecovirus protection after alphavirus vector vaccination

Adams, Lily E. / Leist, Sarah R / Dinnon, Kenneth H / West, Ande / Gully, Kendra L / Anderson, Elizabeth / Loome, Jennifer F / Madden, Emily / Powers, John / Schaefer, Alexandra / Sarkar, Sanjay / Castillo, Izabella / Maron, Jenny / McNamara, Ryan P / Bertera, Harry L / Zweigart, Mark R / Higgins, Jaclyn S / Hampton, Brea K / Lakshmanane, Prem /

Alter, Galit / Montgomery, Stephanie / Baxter, Victoria / Heise, Mark T. / Baric, Ralph S.

bioRxiv

Abstract: Two group 2B beta-coronaviruses (sarbecoviruses) have caused regional and global epidemics in modern history. The mechanisms of cross protection driven by the sarbecovirus spike, a dominant immunogen, are less clear yet critically important for pan- ... ...

Abstract	Two group 2B beta-coronaviruses (sarbecoviruses) have caused regional and global epidemics in modern history. The mechanisms of cross protection driven by the sarbecovirus spike, a dominant immunogen, are less clear yet critically important for pan-sarbecovirus vaccine development. We evaluated the mechanisms of cross-sarbecovirus protective immunity using a panel of alphavirus-vectored vaccines covering bat to human strains. While vaccination did not prevent virus replication, it protected against lethal heterologous disease outcomes in both SARS-CoV-2 and clade 2 bat sarbecovirus HKU3-SRBD challenge models. The spike vaccines tested primarily elicited a highly S1-specific homologous neutralizing antibody response with no detectable cross-virus neutralization. We found non-neutralizing antibody functions that mediated cross protection in wild-type mice were mechanistically linked to FcgR4 and spike S2-binding antibodies. Protection was lost in FcR knockout mice, further supporting a model for non-neutralizing, protective antibodies. These data highlight the importance of FcR-mediated cross-protective immune responses in universal pan-sarbecovirus vaccine designs.
Keywords	covid19
Language	English
Publishing date	2022-11-28
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2022.11.28.518175
Database	COVID19

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Article: Common Mechanism of SARS-CoV and SARS-CoV-2 Pathogenesis across Species.

Schäfer, Alexandra / Gralinski, Lisa E / Leist, Sarah R / Winkler, Emma S / Hampton, Brea K / Mooney, Michael A / Jensen, Kara L / Graham, Rachel L / Agnihothram, Sudhakar / Jeng, Sophia / Chamberlin, Steven / Bell, Timothy A / Scobey, D Trevor / VanBlargan, Laura A / Thackray, Larissa B / Hock, Pablo / Miller, Darla R / Shaw, Ginger D / de Villena, Fernando Pardo Manuel /

McWeeney, Shannon K / Montgomery, Stephanie A / Diamond, Michael S / Heise, Mark T / Menachery, Vineet D / Ferris, Martin T / Baric, Ralph S

bioRxiv : the preprint server for biology

2021

Abstract: Sarbecovirus (CoV) infections, including Severe Acute Respiratory CoV (SARS-CoV) and SARS-CoV-2, are considerable human threats. Human GWAS studies have recently identified loci associated with variation in SARS-CoV-2 susceptibility. However, genetically ...

Abstract	Sarbecovirus (CoV) infections, including Severe Acute Respiratory CoV (SARS-CoV) and SARS-CoV-2, are considerable human threats. Human GWAS studies have recently identified loci associated with variation in SARS-CoV-2 susceptibility. However, genetically tractable models that reproduce human CoV disease outcomes are needed to mechanistically evaluate genetic determinants of CoV susceptibility. We used the Collaborative Cross (CC) and human GWAS datasets to elucidate host susceptibility loci that regulate CoV infections and to identify host quantitative trait loci that modulate severe CoV and pan-CoV disease outcomes including a major disease regulating loci including
Language	English
Publishing date	2021-05-14
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.05.14.444205
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