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Article ; Online: New meaning in the message: noncoding RNAs and their role in retinal development.

Rapicavoli, Nicole A / Blackshaw, Seth

Developmental dynamics : an official publication of the American Association of Anatomists

2009 Volume 238, Issue 9, Page(s) 2103–2114

Abstract: Recent studies have indicated that non-protein-coding RNAs (ncRNAs) may play prominent and diverse roles in the development of the nervous system. These ncRNAs are now known to perform a broad range of cellular functions, and in particular appear to be ... ...

Abstract	Recent studies have indicated that non-protein-coding RNAs (ncRNAs) may play prominent and diverse roles in the development of the nervous system. These ncRNAs are now known to perform a broad range of cellular functions, and in particular appear to be prominent players in the regulation of transcription and translation. In this review, we discuss recent advances in our understanding of the role of ncRNAs in vertebrate retinal development. Noncoding RNAs that are known or suspected to play a functional role in the specification and maturation of retinal cell subtypes include miRNAs, long noncoding opposite-strand transcripts (OSTs), and other long ncRNAs such as Tug1 and RNCR2. Though the mechanism of action of most of these ncRNAs is still largely unclear, it is likely that these molecules represent a major, and thus far largely unappreciated, component of the molecular machinery involved in retinal cell fate specification.
MeSH term(s)	Animals ; Humans ; MicroRNAs/genetics ; MicroRNAs/physiology ; Models, Genetic ; RNA, Untranslated/genetics ; RNA, Untranslated/metabolism ; Retina/cytology ; Retina/embryology
Chemical Substances	MicroRNAs ; RNA, Untranslated
Language	English
Publishing date	2009-09
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.21844
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Article ; Online: The long noncoding RNA RNCR2 directs mouse retinal cell specification.

Rapicavoli, Nicole A / Poth, Erin M / Blackshaw, Seth

BMC developmental biology

2010 Volume 10, Page(s) 49

Abstract: Background: Recent work has identified that many long mRNA-like noncoding RNAs (lncRNAs) are expressed in the developing nervous system. Despite their abundance, the function of these ncRNAs has remained largely unexplored. We have investigated the ... ...

Abstract	Background: Recent work has identified that many long mRNA-like noncoding RNAs (lncRNAs) are expressed in the developing nervous system. Despite their abundance, the function of these ncRNAs has remained largely unexplored. We have investigated the highly abundant lncRNA RNCR2 in regulation of mouse retinal cell differentiation. Results: We find that the RNCR2 is selectively expressed in a subset of both mitotic progenitors and postmitotic retinal precursor cells. ShRNA-mediated knockdown of RNCR2 results in an increase of both amacrine cells and Müller glia, indicating a role for this lncRNA in regulating retinal cell fate specification. We further report that RNCR2 RNA, which is normally nuclear-retained, can be exported from the nucleus when fused to an IRES-GFP sequence. Overexpression of RNCR2-IRES-GFP phenocopies the effects of shRNA-mediated knockdown of RNCR2, implying that forced mislocalization of RNCR2 induces a dominant-negative phenotype. Finally, we use the IRES-GFP fusion approach to identify specific domains of RNCR2 that are required for repressing both amacrine and Müller glial differentiation. Conclusion: These data demonstrate that the lncRNA RNCR2 plays a critical role in regulating mammalian retinal cell fate specification. Furthermore, we present a novel approach for generating dominant-negative constructs of lncRNAs, which may be generally useful in the functional analysis of this class of molecules.
MeSH term(s)	Amacrine Cells/metabolism ; Animals ; In Situ Hybridization, Fluorescence ; Mice ; Neuroglia/metabolism ; RNA, Long Noncoding ; RNA, Untranslated/metabolism ; Retina/cytology ; Retina/embryology ; Retina/metabolism
Chemical Substances	Miat long non-coding RNA ; RNA, Long Noncoding ; RNA, Untranslated
Language	English
Publishing date	2010-05-11
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1471-213X
ISSN (online)	1471-213X
DOI	10.1186/1471-213X-10-49
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Article ; Online: The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity.

Rapicavoli, Nicole A / Poth, Erin M / Zhu, Heng / Blackshaw, Seth

Neural development

2011 Volume 6, Page(s) 32

Abstract: Background: Thousands of different long non-coding RNAs are expressed during embryonic development, but the function of these molecules remains largely unexplored.: Results: Here we characterize the expression and function of Six3OS, a long non- ... ...

Abstract	Background: Thousands of different long non-coding RNAs are expressed during embryonic development, but the function of these molecules remains largely unexplored. Results: Here we characterize the expression and function of Six3OS, a long non-coding RNA that is transcribed from the distal promoter region of the gene encoding the homeodomain transcription factor Six3. Overexpression and knockdown analysis of Six3OS reveals that it plays an essential role in regulating retinal cell specification. We further observe that Six3OS regulates Six3 activity in developing retina, but does not do so by modulating Six3 expression. Finally, we show that Six3OS binds directly to Ezh2 and Eya family members, indicating that Six3OS can act as a molecular scaffold to recruit histone modification enzymes to Six3 target genes. Conclusions: Our findings demonstrate a novel mechanism by which promoter-associated long non-coding RNAs can modulate the activity of their associated protein coding genes, and highlight the importance of this diverse class of molecules in the control of neural development.
MeSH term(s)	Animals ; Eye Proteins/genetics ; Eye Proteins/metabolism ; Female ; Gene Expression Regulation, Developmental/genetics ; HEK293 Cells ; HeLa Cells ; Homeodomain Proteins/genetics ; Homeodomain Proteins/metabolism ; Humans ; Mice ; Mice, Inbred Strains ; NIH 3T3 Cells ; Nerve Tissue Proteins/genetics ; Nerve Tissue Proteins/metabolism ; Neurogenesis/genetics ; Neurons/cytology ; Neurons/metabolism ; Pregnancy ; Promoter Regions, Genetic/genetics ; RNA, Untranslated/genetics ; RNA, Untranslated/metabolism ; Retina/cytology ; Retina/embryology ; Retina/metabolism ; Homeobox Protein SIX3
Chemical Substances	Eye Proteins ; Homeodomain Proteins ; Nerve Tissue Proteins ; RNA, Untranslated
Language	English
Publishing date	2011-09-21
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2254847-6
ISSN	1749-8104 ; 1749-8104
ISSN (online)	1749-8104
ISSN	1749-8104
DOI	10.1186/1749-8104-6-32
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Article ; Online: The long noncoding RNA RNCR2 directs mouse retinal cell specification

Blackshaw Seth / Poth Erin M / Rapicavoli Nicole A

BMC Developmental Biology, Vol 10, Iss 1, p

2010 Volume 49

Abstract: Abstract Background Recent work has identified that many long mRNA-like noncoding RNAs (lncRNAs) are expressed in the developing nervous system. Despite their abundance, the function of these ncRNAs has remained largely unexplored. We have investigated ... ...

Abstract	Abstract Background Recent work has identified that many long mRNA-like noncoding RNAs (lncRNAs) are expressed in the developing nervous system. Despite their abundance, the function of these ncRNAs has remained largely unexplored. We have investigated the highly abundant lncRNA RNCR2 in regulation of mouse retinal cell differentiation. Results We find that the RNCR2 is selectively expressed in a subset of both mitotic progenitors and postmitotic retinal precursor cells. ShRNA-mediated knockdown of RNCR2 results in an increase of both amacrine cells and Müller glia, indicating a role for this lncRNA in regulating retinal cell fate specification. We further report that RNCR2 RNA, which is normally nuclear-retained, can be exported from the nucleus when fused to an IRES-GFP sequence. Overexpression of RNCR2-IRES-GFP phenocopies the effects of shRNA-mediated knockdown of RNCR2, implying that forced mislocalization of RNCR2 induces a dominant-negative phenotype. Finally, we use the IRES-GFP fusion approach to identify specific domains of RNCR2 that are required for repressing both amacrine and Müller glial differentiation. Conclusion These data demonstrate that the lncRNA RNCR2 plays a critical role in regulating mammalian retinal cell fate specification. Furthermore, we present a novel approach for generating dominant-negative constructs of lncRNAs, which may be generally useful in the functional analysis of this class of molecules.
Keywords	Biology (General) ; QH301-705.5
Subject code	571
Language	English
Publishing date	2010-05-01T00:00:00Z
Publisher	BioMed Central
Document type	Article ; Online
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Article: A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics.

Rapicavoli, Nicole A / Qu, Kun / Zhang, Jiajing / Mikhail, Megan / Laberge, Remi-Martin / Chang, Howard Y

eLife

2013 Volume 2, Page(s) e00762

Abstract: Pseudogenes are thought to be inactive gene sequences, but recent evidence of extensive pseudogene transcription raised the question of potential function. Here we discover and characterize the sets of mouse lncRNAs induced by inflammatory signaling via ... ...

Abstract	Pseudogenes are thought to be inactive gene sequences, but recent evidence of extensive pseudogene transcription raised the question of potential function. Here we discover and characterize the sets of mouse lncRNAs induced by inflammatory signaling via TNFα. TNFα regulates hundreds of lncRNAs, including 54 pseudogene lncRNAs, several of which show exquisitely selective expression in response to specific cytokines and microbial components in a NF-κB-dependent manner. Lethe, a pseudogene lncRNA, is selectively induced by proinflammatory cytokines via NF-κB or glucocorticoid receptor agonist, and functions in negative feedback signaling to NF-κB. Lethe interacts with NF-κB subunit RelA to inhibit RelA DNA binding and target gene activation. Lethe level decreases with organismal age, a physiological state associated with increased NF-κB activity. These findings suggest that expression of pseudogenes lncRNAs are actively regulated and constitute functional regulators of inflammatory signaling. DOI:http://dx.doi.org/10.7554/eLife.00762.001.
MeSH term(s)	Animals ; Anti-Inflammatory Agents/therapeutic use ; Inflammation/genetics ; Pseudogenes ; RNA, Long Noncoding/genetics ; Tumor Necrosis Factor-alpha/pharmacology
Chemical Substances	Anti-Inflammatory Agents ; RNA, Long Noncoding ; Tumor Necrosis Factor-alpha
Language	English
Publishing date	2013-07-23
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
ISSN	2050-084X
DOI	10.7554/eLife.00762
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Article ; Online: The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity

Zhu Heng / Poth Erin M / Rapicavoli Nicole A / Blackshaw Seth

Neural Development, Vol 6, Iss 1, p

2011 Volume 32

Abstract: Abstract Background Thousands of different long non-coding RNAs are expressed during embryonic development, but the function of these molecules remains largely unexplored. Results Here we characterize the expression and function of Six3OS , a long non- ... ...

Abstract	Abstract Background Thousands of different long non-coding RNAs are expressed during embryonic development, but the function of these molecules remains largely unexplored. Results Here we characterize the expression and function of Six3OS , a long non-coding RNA that is transcribed from the distal promoter region of the gene encoding the homeodomain transcription factor Six3. Overexpression and knockdown analysis of Six3OS reveals that it plays an essential role in regulating retinal cell specification. We further observe that Six3OS regulates Six3 activity in developing retina, but does not do so by modulating Six3 expression. Finally, we show that Six3OS binds directly to Ezh2 and Eya family members, indicating that Six3OS can act as a molecular scaffold to recruit histone modification enzymes to Six3 target genes. Conclusions Our findings demonstrate a novel mechanism by which promoter-associated long non-coding RNAs can modulate the activity of their associated protein coding genes, and highlight the importance of this diverse class of molecules in the control of neural development.
Keywords	Physiology ; QP1-981 ; Science ; Q ; DOAJ:Physiology ; DOAJ:Biology ; DOAJ:Biology and Life Sciences
Subject code	572
Language	English
Publishing date	2011-09-01T00:00:00Z
Publisher	BioMed Central
Document type	Article ; Online
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Article ; Online: Rejuvenation of gene expression pattern of aged human skin by broadband light treatment: a pilot study.

Chang, Anne Lynn S / Bitter, Patrick H / Qu, Kun / Lin, Meihong / Rapicavoli, Nicole A / Chang, Howard Y

The Journal of investigative dermatology

2012 Volume 133, Issue 2, Page(s) 394–402

Abstract: Studies in model organisms suggest that aged cells can be functionally rejuvenated, but whether this concept applies to human skin is unclear. Here we apply 3'-end sequencing for expression quantification ("3-seq") to discover the gene expression program ...

Abstract	Studies in model organisms suggest that aged cells can be functionally rejuvenated, but whether this concept applies to human skin is unclear. Here we apply 3'-end sequencing for expression quantification ("3-seq") to discover the gene expression program associated with human photoaging and intrinsic skin aging (collectively termed "skin aging"), and the impact of broadband light (BBL) treatment. We find that skin aging was associated with a significantly altered expression level of 2,265 coding and noncoding RNAs, of which 1,293 became "rejuvenated" after BBL treatment; i.e., they became more similar to their expression level in youthful skin. Rejuvenated genes (RGs) included several known key regulators of organismal longevity and their proximal long noncoding RNAs. Skin aging is not associated with systematic changes in 3'-end mRNA processing. Hence, BBL treatment can restore gene expression pattern of photoaged and intrinsically aged human skin to resemble young skin. In addition, our data reveal, to our knowledge, a previously unreported set of targets that may lead to new insights into the human skin aging process.
MeSH term(s)	Adult ; Aged ; Female ; Forearm ; Gene Expression Regulation/physiology ; Gene Expression Regulation/radiation effects ; Humans ; Membrane Proteins/genetics ; Metalloendopeptidases/genetics ; Middle Aged ; Phototherapy/methods ; Pilot Projects ; RNA 3' End Processing/genetics ; RNA, Messenger/genetics ; RNA, Untranslated/genetics ; Rejuvenation/physiology ; Skin Aging/genetics ; Transcriptome
Chemical Substances	Membrane Proteins ; RNA, Messenger ; RNA, Untranslated ; Metalloendopeptidases (EC 3.4.24.-) ; ZMPSTE24 protein, human (EC 3.4.24.84)
Language	English
Publishing date	2012-08-30
Publishing country	United States
Document type	Controlled Clinical Trial ; Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80136-7
ISSN	1523-1747 ; 0022-202X
ISSN (online)	1523-1747
ISSN	0022-202X
DOI	10.1038/jid.2012.287
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Article ; Online: Dynamic chromatin localization of Sirt6 shapes stress- and aging-related transcriptional networks.

Kawahara, Tiara L A / Rapicavoli, Nicole A / Wu, Angela R / Qu, Kun / Quake, Stephen R / Chang, Howard Y

PLoS genetics

2011 Volume 7, Issue 6, Page(s) e1002153

Abstract: The sirtuin Sirt6 is a NAD-dependent histone deacetylase that is implicated in gene regulation and lifespan control. Sirt6 can interact with the stress-responsive transcription factor NF-κB and regulate some NF-κB target genes, but the full scope of ... ...

Abstract	The sirtuin Sirt6 is a NAD-dependent histone deacetylase that is implicated in gene regulation and lifespan control. Sirt6 can interact with the stress-responsive transcription factor NF-κB and regulate some NF-κB target genes, but the full scope of Sirt6 target genes as well as dynamics of Sirt6 occupancy on chromatin are not known. Here we map Sirt6 occupancy on mouse promoters genome-wide and show that Sirt6 occupancy is highly dynamic in response to TNF-α. More than half of Sirt6 target genes are only revealed upon stress-signaling. The majority of genes bound by NF-κB subunit RelA recruit Sirt6, and dynamic Sirt6 relocalization is largely driven in a RelA-dependent manner. Integrative analysis with global gene expression patterns in wild-type, Sirt6-/-, and double Sirt6-/- RelA-/- cells reveals the epistatic relationships between Sirt6 and RelA in shaping diverse temporal patterns of gene expression. Genes under the direct joint control of Sirt6 and RelA include several with prominent roles in cell senescence and organismal aging. These data suggest dynamic chromatin relocalization of Sirt6 as a key output of NF-κB signaling in stress response and aging.
MeSH term(s)	Aging/genetics ; Animals ; Cell Line ; Chromatin/metabolism ; Gene Expression Profiling ; Gene Expression Regulation ; Gene Regulatory Networks/genetics ; Intracellular Space/metabolism ; Mice ; Mice, Knockout ; Models, Genetic ; Protein Transport/genetics ; Reproducibility of Results ; Sirtuins/metabolism ; Stress, Physiological/genetics ; Transcription Factor RelA/metabolism
Chemical Substances	Chromatin ; Transcription Factor RelA ; Sirt6 protein, mouse (EC 2.4.2.31) ; Sirtuins (EC 3.5.1.-)
Language	English
Publishing date	2011-06-30
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.1002153
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Article ; Online: A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics

Nicole A Rapicavoli / Kun Qu / Jiajing Zhang / Megan Mikhail / Remi-Martin Laberge / Howard Y Chang

eLife, Vol

2013 Volume 2

Abstract	Pseudogenes are thought to be inactive gene sequences, but recent evidence of extensive pseudogene transcription raised the question of potential function. Here we discover and characterize the sets of mouse lncRNAs induced by inflammatory signaling via TNFα. TNFα regulates hundreds of lncRNAs, including 54 pseudogene lncRNAs, several of which show exquisitely selective expression in response to specific cytokines and microbial components in a NF-κB-dependent manner. Lethe, a pseudogene lncRNA, is selectively induced by proinflammatory cytokines via NF-κB or glucocorticoid receptor agonist, and functions in negative feedback signaling to NF-κB. Lethe interacts with NF-κB subunit RelA to inhibit RelA DNA binding and target gene activation. Lethe level decreases with organismal age, a physiological state associated with increased NF-κB activity. These findings suggest that expression of pseudogenes lncRNAs are actively regulated and constitute functional regulators of inflammatory signaling.
Keywords	noncoding RNA ; NF-κB ; genomic ; Medicine ; R ; Science ; Q ; Biology (General) ; QH301-705.5
Subject code	572
Language	English
Publishing date	2013-07-01T00:00:00Z
Publisher	eLife Sciences Publications Ltd
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article: Long-read, whole-genome shotgun sequence data for five model organisms.

Kim, Kristi E / Peluso, Paul / Babayan, Primo / Yeadon, P Jane / Yu, Charles / Fisher, William W / Chin, Chen-Shan / Rapicavoli, Nicole A / Rank, David R / Li, Joachim / Catcheside, David E A / Celniker, Susan E / Phillippy, Adam M / Bergman, Casey M / Landolin, Jane M

Scientific data

2014 Volume 1, Page(s) 140045

Abstract: Single molecule, real-time (SMRT) sequencing from Pacific Biosciences is increasingly used in many areas of biological research including de novo genome assembly, structural-variant identification, haplotype phasing, mRNA isoform discovery, and base- ... ...

Abstract	Single molecule, real-time (SMRT) sequencing from Pacific Biosciences is increasingly used in many areas of biological research including de novo genome assembly, structural-variant identification, haplotype phasing, mRNA isoform discovery, and base-modification analyses. High-quality, public datasets of SMRT sequences can spur development of analytic tools that can accommodate unique characteristics of SMRT data (long read lengths, lack of GC or amplification bias, and a random error profile leading to high consensus accuracy). In this paper, we describe eight high-coverage SMRT sequence datasets from five organisms (Escherichia coli, Saccharomyces cerevisiae, Neurospora crassa, Arabidopsis thaliana, and Drosophila melanogaster) that have been publicly released to the general scientific community (NCBI Sequence Read Archive ID SRP040522). Data were generated using two sequencing chemistries (P4C2 and P5C3) on the PacBio RS II instrument. The datasets reported here can be used without restriction by the research community to generate whole-genome assemblies, test new algorithms, investigate genome structure and evolution, and identify base modifications in some of the most widely-studied model systems in biological research.
MeSH term(s)	Animals ; Arabidopsis/genetics ; Drosophila melanogaster/genetics ; Escherichia coli/genetics ; Genome, Bacterial ; Genome, Fungal ; Genome, Insect ; Genome, Plant ; Models, Animal ; Neurospora crassa/genetics ; Saccharomyces cerevisiae/genetics ; Sequence Analysis, DNA
Language	English
Publishing date	2014-11-25
Publishing country	England
Document type	Dataset ; Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2775191-0
ISSN	2052-4463
ISSN	2052-4463
DOI	10.1038/sdata.2014.45
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