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Article: The ChAHP Complex Counteracts Chromatin Looping at CTCF Sites that Emerged from SINE Expansions in Mouse

Kaaij, Lucas J.T / Bühler, Marc / de Wit, Elzo / Mohn, Fabio / van der Weide, Robin H

Cell. 2019 Sept. 05, v. 178, no. 6

2019

Abstract: CCCTC-binding factor (CTCF) and cohesin are key players in three-dimensional chromatin organization. The topologically associating domains (TADs) demarcated by CTCF are remarkably well conserved between species, although genome-wide CTCF binding has ... ...

Abstract	CCCTC-binding factor (CTCF) and cohesin are key players in three-dimensional chromatin organization. The topologically associating domains (TADs) demarcated by CTCF are remarkably well conserved between species, although genome-wide CTCF binding has diverged substantially following transposon-mediated motif expansions. Therefore, the CTCF consensus motif poorly predicts TADs, and additional factors must modulate CTCF binding and subsequent TAD formation. Here, we demonstrate that the ChAHP complex (CHD4, ADNP, HP1) competes with CTCF for a common set of binding motifs. In Adnp knockout cells, novel insulated regions are formed at sites normally bound by ChAHP, whereas proximal canonical boundaries are weakened. These data reveal that CTCF-mediated loop formation is modulated by a distinct zinc-finger protein complex. Strikingly, ChAHP-bound loci are mainly situated within less diverged SINE B2 transposable elements. This implicates ChAHP in maintenance of evolutionarily conserved spatial chromatin organization by buffering novel CTCF binding sites that emerged through SINE expansions.
Keywords	binding sites ; chromatin ; consensus sequence ; loci ; mice ; transposons ; zinc finger motif
Language	English
Dates of publication	2019-0905
Size	p. 1437-1451.e14.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2019.08.007
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Article ; Online: Systemic Loss and Gain of Chromatin Architecture throughout Zebrafish Development.

Kaaij, Lucas J T / van der Weide, Robin H / Ketting, René F / de Wit, Elzo

Cell reports

2018 Volume 24, Issue 1, Page(s) 1–10.e4

Abstract: The spatial organization of chromosomes is critical in establishing gene expression programs. We generated in situ Hi-C maps throughout zebrafish development to gain insight into higher-order chromatin organization and dynamics. Zebrafish chromosomes ... ...

Abstract	The spatial organization of chromosomes is critical in establishing gene expression programs. We generated in situ Hi-C maps throughout zebrafish development to gain insight into higher-order chromatin organization and dynamics. Zebrafish chromosomes segregate in active and inactive chromatin (A/B compartments), which are further organized into topologically associating domains (TADs). Zebrafish A/B compartments and TADs have genomic features similar to those of their mammalian counterparts, including evolutionary conservation and enrichment of CTCF binding sites at TAD borders. At the earliest time point, when there is no zygotic transcription, the genome is highly structured. After zygotic genome activation (ZGA), the genome loses structural features, which are re-established throughout early development. Despite the absence of structural features, we see clustering of super-enhancers in the 3D genome. Our results provide insight into vertebrate genome organization and demonstrate that the developing zebrafish embryo is a powerful model system to study the dynamics of nuclear organization.
MeSH term(s)	Animals ; Chromatin/metabolism ; Embryonic Development/genetics ; Enhancer Elements, Genetic/genetics ; Epigenomics ; Genome ; Histone Code ; Zebrafish/embryology ; Zebrafish/genetics
Chemical Substances	Chromatin
Language	English
Publishing date	2018-08-09
Publishing country	United States
Document type	Journal Article ; 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.2018.06.003
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Article ; Online: Systemic Loss and Gain of Chromatin Architecture throughout Zebrafish Development

Lucas J.T. Kaaij / Robin H. van der Weide / René F. Ketting / Elzo de Wit

Cell Reports, Vol 24, Iss 1, Pp 1-10.e

2018 Volume 4

Abstract: ... organize their genome? Kaaij et al. show that, early in development, when there is no transcription ...

Abstract	Summary: The spatial organization of chromosomes is critical in establishing gene expression programs. We generated in situ Hi-C maps throughout zebrafish development to gain insight into higher-order chromatin organization and dynamics. Zebrafish chromosomes segregate in active and inactive chromatin (A/B compartments), which are further organized into topologically associating domains (TADs). Zebrafish A/B compartments and TADs have genomic features similar to those of their mammalian counterparts, including evolutionary conservation and enrichment of CTCF binding sites at TAD borders. At the earliest time point, when there is no zygotic transcription, the genome is highly structured. After zygotic genome activation (ZGA), the genome loses structural features, which are re-established throughout early development. Despite the absence of structural features, we see clustering of super-enhancers in the 3D genome. Our results provide insight into vertebrate genome organization and demonstrate that the developing zebrafish embryo is a powerful model system to study the dynamics of nuclear organization. : How do developing zebrafish embryos organize their genome? Kaaij et al. show that, early in development, when there is no transcription, the genome is highly structured; however, when the zygotic genome is activated, this organization is lost. Later in development, the genome again adopts a structured organization.
Keywords	Biology (General) ; QH301-705.5
Language	English
Publishing date	2018-07-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
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Article ; Online: The ChAHP Complex Counteracts Chromatin Looping at CTCF Sites that Emerged from SINE Expansions in Mouse.

Kaaij, Lucas J T / Mohn, Fabio / van der Weide, Robin H / de Wit, Elzo / Bühler, Marc

Cell

2019 Volume 178, Issue 6, Page(s) 1437–1451.e14

Abstract	CCCTC-binding factor (CTCF) and cohesin are key players in three-dimensional chromatin organization. The topologically associating domains (TADs) demarcated by CTCF are remarkably well conserved between species, although genome-wide CTCF binding has diverged substantially following transposon-mediated motif expansions. Therefore, the CTCF consensus motif poorly predicts TADs, and additional factors must modulate CTCF binding and subsequent TAD formation. Here, we demonstrate that the ChAHP complex (CHD4, ADNP, HP1) competes with CTCF for a common set of binding motifs. In Adnp knockout cells, novel insulated regions are formed at sites normally bound by ChAHP, whereas proximal canonical boundaries are weakened. These data reveal that CTCF-mediated loop formation is modulated by a distinct zinc-finger protein complex. Strikingly, ChAHP-bound loci are mainly situated within less diverged SINE B2 transposable elements. This implicates ChAHP in maintenance of evolutionarily conserved spatial chromatin organization by buffering novel CTCF binding sites that emerged through SINE expansions.
MeSH term(s)	Animals ; Binding Sites ; CCCTC-Binding Factor/metabolism ; Cell Line ; Chromatin/metabolism ; Chromosomal Proteins, Non-Histone/metabolism ; DNA Helicases/metabolism ; Embryonic Stem Cells/cytology ; Embryonic Stem Cells/metabolism ; Homeodomain Proteins/metabolism ; Mice ; Nerve Tissue Proteins/metabolism ; Protein Binding ; Protein Domains ; Retroelements
Chemical Substances	Adnp protein, mouse ; CCCTC-Binding Factor ; Chromatin ; Chromosomal Proteins, Non-Histone ; Ctcf protein, mouse ; Homeodomain Proteins ; Nerve Tissue Proteins ; Retroelements ; heterochromatin-specific nonhistone chromosomal protein HP-1 (107283-02-3) ; Mi-2beta protein, mouse (EC 3.6.1.3) ; DNA Helicases (EC 3.6.4.-)
Language	English
Publishing date	2019-09-06
Publishing country	United States
Document type	Journal Article
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2019.08.007
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Article ; Online: piRNA dynamics in divergent zebrafish strains reveal long-lasting maternal influence on zygotic piRNA profiles.

Kaaij, Lucas J T / Hoogstrate, Suzanne W / Berezikov, Eugene / Ketting, René F

RNA (New York, N.Y.)

2013 Volume 19, Issue 3, Page(s) 345–356

Abstract: Transposable elements (TEs) are mobile genetic elements that can have many deleterious effects on the fitness of their host. The germline-specific PIWI pathway guards the genome against TEs, deriving its specificity from sequence complementarity between ... ...

Abstract	Transposable elements (TEs) are mobile genetic elements that can have many deleterious effects on the fitness of their host. The germline-specific PIWI pathway guards the genome against TEs, deriving its specificity from sequence complementarity between PIWI-bound small RNAs (piRNAs) and the TEs. The piRNAs are derived from so-called piRNA clusters. Recent studies have demonstrated that the piRNA repertoire can be adjusted to accommodate recent TE invasions by capturing invading TEs in piRNA loci. Thus far, no information concerning piRNA divergence is available from vertebrates. We present piRNA analyses of two relatively divergent zebrafish strains. We find that significant differences in the piRNA populations have accumulated, most notably among active class I TEs. This divergence can be split into differences in piRNA abundance per element and differences in sense/antisense polarity ratios. In crosses between animals of the different strains, many of these differences are resolved in the progeny. However, some differences remain, often leaning to the maternally contributed piRNA population. These differences can be detected at least two generations later. Our data illustrate, for the first time, the fluidity of piRNA populations in vertebrates and how the established diversity is transmitted to future generations.
MeSH term(s)	Animals ; Crosses, Genetic ; DNA Transposable Elements ; Epigenesis, Genetic ; Female ; Male ; RNA, Small Interfering/chemistry ; RNA, Small Interfering/metabolism ; Zebrafish/genetics ; Zebrafish/metabolism ; Zygote/metabolism
Chemical Substances	DNA Transposable Elements ; RNA, Small Interfering
Language	English
Publishing date	2013-01-18
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1241540-6
ISSN	1469-9001 ; 1355-8382
ISSN (online)	1469-9001
ISSN	1355-8382
DOI	10.1261/rna.036400.112
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Article ; Online: Dcr1 tracked down.

Kaaij, Lucas J T / Ketting, René F

Developmental cell

2010 Volume 18, Issue 1, Page(s) 6–7

Abstract: RNAi is essential for pericentromeric heterochromatic formation in S. pombe, and although Dcr1, the initiator protein of this process, has been biochemically well described, its subcellular localization has remained elusive. In this issue of ... ...

Abstract	RNAi is essential for pericentromeric heterochromatic formation in S. pombe, and although Dcr1, the initiator protein of this process, has been biochemically well described, its subcellular localization has remained elusive. In this issue of Developmental Cell, Emmerth et al. now show that Dcr1 is dynamically shuttling between nucleus and cytoplasm, adding new insight into the subcellular mechanics of RNAi.
MeSH term(s)	Active Transport, Cell Nucleus/genetics ; Animals ; Cell Nucleus/genetics ; Cell Nucleus/metabolism ; Cytoplasm/genetics ; Cytoplasm/metabolism ; Heterochromatin/genetics ; Humans ; Intracellular Signaling Peptides and Proteins/genetics ; Nuclear Pore/genetics ; Nuclear Pore/metabolism ; Protein Transport ; RNA Interference/physiology ; Ribonuclease III/genetics ; Ribonuclease III/metabolism ; Schizosaccharomyces/genetics ; Schizosaccharomyces/metabolism
Chemical Substances	Gid8 protein, S cerevisiae ; Heterochromatin ; Intracellular Signaling Peptides and Proteins ; Ribonuclease III (EC 3.1.26.3)
Language	English
Publishing date	2010-01-19
Publishing country	United States
Document type	Comment ; Journal Article
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2010.01.001
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Article ; Online: Tdrd6a Regulates the Aggregation of Buc into Functional Subcellular Compartments that Drive Germ Cell Specification.

Roovers, Elke F / Kaaij, Lucas J T / Redl, Stefan / Bronkhorst, Alfred W / Wiebrands, Kay / de Jesus Domingues, António M / Huang, Hsin-Yi / Han, Chung-Ting / Riemer, Stephan / Dosch, Roland / Salvenmoser, Willi / Grün, Dominic / Butter, Falk / van Oudenaarden, Alexander / Ketting, René F

Developmental cell

2018 Volume 46, Issue 3, Page(s) 285–301.e9

Abstract: Phase separation represents an important form of subcellular compartmentalization. However, relatively little is known about how the formation or disassembly of such compartments is regulated. In zebrafish, the Balbiani body (Bb) and the germ plasm (Gp) ... ...

Abstract	Phase separation represents an important form of subcellular compartmentalization. However, relatively little is known about how the formation or disassembly of such compartments is regulated. In zebrafish, the Balbiani body (Bb) and the germ plasm (Gp) are intimately linked phase-separated structures essential for germ cell specification and home to many germ cell-specific mRNAs and proteins. Throughout development, these structures occur as a single large aggregate (Bb), which disperses throughout oogenesis and upon fertilization accumulates again into relatively large assemblies (Gp). Formation of the Bb requires Bucky ball (Buc), a protein with prion-like properties. We found that the multi-tudor domain-containing protein Tdrd6a interacts with Buc, affecting its mobility and aggregation properties. Importantly, lack of this regulatory interaction leads to significant defects in germ cell development. Our work presents insights into how prion-like protein aggregations can be regulated and highlights the biological relevance of such regulatory events.
MeSH term(s)	Animals ; Cytoplasm/metabolism ; Germ Cells/metabolism ; Oocytes/metabolism ; Oogenesis/physiology ; Organelles/metabolism ; RNA, Messenger/metabolism ; Zebrafish ; Zebrafish Proteins/metabolism
Chemical Substances	RNA, Messenger ; Zebrafish Proteins ; buc protein, zebrafish
Language	English
Publishing date	2018-08-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2018.07.009
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Article ; Online: Enhancers reside in a unique epigenetic environment during early zebrafish development.

Kaaij, Lucas J T / Mokry, Michal / Zhou, Meng / Musheev, Michael / Geeven, Geert / Melquiond, Adrien S J / de Jesus Domingues, António M / de Laat, Wouter / Niehrs, Christof / Smith, Andrew D / Ketting, René F

Genome biology

2016 Volume 17, Issue 1, Page(s) 146

Abstract: Background: Enhancers, not promoters, are the most dynamic in their DNA methylation status throughout development and differentiation. Generally speaking, enhancers that are primed to or actually drive gene expression are characterized by relatively low ...

Abstract	Background: Enhancers, not promoters, are the most dynamic in their DNA methylation status throughout development and differentiation. Generally speaking, enhancers that are primed to or actually drive gene expression are characterized by relatively low levels of DNA methylation (hypo-methylation), while inactive enhancers display hyper-methylation of the underlying DNA. The direct functional significance of the DNA methylation state of enhancers is, however, unclear for most loci. Results: In contrast to conventional epigenetic interactions at enhancers, we find that DNA methylation status and enhancer activity during early zebrafish development display very unusual correlation characteristics: hypo-methylation is a unique feature of primed enhancers whereas active enhancers are generally hyper-methylated. The hypo-methylated enhancers that we identify (hypo-enhancers) are enriched close to important transcription factors that act later in development. Interestingly, hypo-enhancers are de-methylated shortly before the midblastula transition and reside in a unique epigenetic environment. Finally, we demonstrate that hypo-enhancers do become active at later developmental stages and that they are physically associated with the transcriptional start site of target genes, irrespective of target gene activity. Conclusions: We demonstrate that early development in zebrafish embodies a time window characterized by non-canonical DNA methylation-enhancer relationships, including global DNA hypo-methylation of inactive enhancers and DNA hyper-methylation of active enhancers.
MeSH term(s)	Animals ; Cell Differentiation/genetics ; DNA Methylation/genetics ; Embryonic Development/genetics ; Enhancer Elements, Genetic ; Epigenesis, Genetic ; Gene Expression Regulation, Developmental ; Transcription Initiation Site ; Zebrafish/genetics ; Zebrafish/growth & development
Language	English
Publishing date	2016-07-05
Publishing country	England
Document type	Journal Article
ZDB-ID	2040529-7
ISSN	1474-760X ; 1465-6914 ; 1465-6906
ISSN (online)	1474-760X ; 1465-6914
ISSN	1465-6906
DOI	10.1186/s13059-016-1013-1
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Article: Enhancers reside in a unique epigenetic environment during early zebrafish development

Kaaij, Lucas J. T / Mokry, Michal / Zhou, Meng / Musheev, Michael / Geeven, Geert / Melquiond, Adrien S. J / de Jesus Domingues, António M / de Laat, Wouter / Niehrs, Christof / Smith, Andrew D / Ketting, René F

Genome biology. 2016 Dec., v. 17, no. 1

2016

Abstract: BACKGROUND: Enhancers, not promoters, are the most dynamic in their DNA methylation status throughout development and differentiation. Generally speaking, enhancers that are primed to or actually drive gene expression are characterized by relatively low ... ...

Abstract	BACKGROUND: Enhancers, not promoters, are the most dynamic in their DNA methylation status throughout development and differentiation. Generally speaking, enhancers that are primed to or actually drive gene expression are characterized by relatively low levels of DNA methylation (hypo-methylation), while inactive enhancers display hyper-methylation of the underlying DNA. The direct functional significance of the DNA methylation state of enhancers is, however, unclear for most loci. RESULTS: In contrast to conventional epigenetic interactions at enhancers, we find that DNA methylation status and enhancer activity during early zebrafish development display very unusual correlation characteristics: hypo-methylation is a unique feature of primed enhancers whereas active enhancers are generally hyper-methylated. The hypo-methylated enhancers that we identify (hypo-enhancers) are enriched close to important transcription factors that act later in development. Interestingly, hypo-enhancers are de-methylated shortly before the midblastula transition and reside in a unique epigenetic environment. Finally, we demonstrate that hypo-enhancers do become active at later developmental stages and that they are physically associated with the transcriptional start site of target genes, irrespective of target gene activity. CONCLUSIONS: We demonstrate that early development in zebrafish embodies a time window characterized by non-canonical DNA methylation–enhancer relationships, including global DNA hypo-methylation of inactive enhancers and DNA hyper-methylation of active enhancers.
Keywords	DNA ; DNA methylation ; Danio rerio ; developmental stages ; early development ; epigenetics ; gene expression ; loci ; transcription (genetics) ; transcription factors
Language	English
Dates of publication	2016-12
Size	p. 146.
Publishing place	BioMed Central
Document type	Article
ZDB-ID	2040529-7
ISSN	1474-760X ; 1465-6906
ISSN (online)	1474-760X
ISSN	1465-6906
DOI	10.1186/s13059-016-1013-1
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Article ; Online: Extremely stable Piwi-induced gene silencing in Caenorhabditis elegans.

Luteijn, Maartje J / van Bergeijk, Petra / Kaaij, Lucas J T / Almeida, Miguel Vasconcelos / Roovers, Elke F / Berezikov, Eugene / Ketting, René F

The EMBO journal

2012 Volume 31, Issue 16, Page(s) 3422–3430

Abstract: In recent years, the Piwi pathway has been shown to regulate the silencing of mobile genetic elements. However, we know little about how Piwi pathways impose silencing and even less about trans-generational stability of Piwi-induced silencing. We ... ...

Abstract	In recent years, the Piwi pathway has been shown to regulate the silencing of mobile genetic elements. However, we know little about how Piwi pathways impose silencing and even less about trans-generational stability of Piwi-induced silencing. We demonstrate that the Caenorhabditis elegans Piwi protein PRG-1 can initiate an extremely stable form of gene silencing on a transgenic, single-copy target. This type of silencing is faithfully maintained over tens of generations in the absence of a functional Piwi pathway. Interestingly, RNAi can also trigger permanent gene silencing of a single-copy transgene and the phenomenon will be collectively referred to as RNA-induced epigenetic silencing (RNAe). RNAe can act in trans and is dependent on endogenous RNAi factors. The involvement of factors known to act in nuclear RNAi and the fact that RNAe is accompanied by repressive chromatin marks indicate that RNAe includes a transcriptional silencing component. Our results demonstrate that, at least in C. elegans, the Piwi pathway can impose a state of gene silencing that borders on 'permanently silent'. Such a property may be more widely conserved among Piwi pathways in different animals.
MeSH term(s)	Animals ; Animals, Genetically Modified ; Argonaute Proteins/metabolism ; Caenorhabditis elegans/enzymology ; Caenorhabditis elegans/physiology ; Caenorhabditis elegans Proteins/metabolism ; Gene Expression Profiling ; Gene Silencing ; Models, Biological
Chemical Substances	Argonaute Proteins ; Caenorhabditis elegans Proteins ; PRG-1 protein, C elegans
Language	English
Publishing date	2012-07-31
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	586044-1
ISSN	1460-2075 ; 0261-4189
ISSN (online)	1460-2075
ISSN	0261-4189
DOI	10.1038/emboj.2012.213
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