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Article ; Online: Enhanced Yeast One-Hybrid Assays to Study Protein-DNA Interactions.

Berenson, Anna / Fuxman Bass, Juan Ignacio

Methods in molecular biology (Clifton, N.J.)

2022 Volume 2599, Page(s) 11–20

Abstract: The specificity in gene regulation is controlled by interactions between transcription factors (TFs) and genomic DNA regions such as promoters and enhancers. Enhanced yeast one-hybrid (eY1H) assays are among the methods used for high-throughput detection ...

Abstract	The specificity in gene regulation is controlled by interactions between transcription factors (TFs) and genomic DNA regions such as promoters and enhancers. Enhanced yeast one-hybrid (eY1H) assays are among the methods used for high-throughput detection of transcription factor-DNA interactions. Here, we describe the procedure for screening interactions between DNA regions of interest ("DNA-baits") and an array of transcription factors ("TF-preys"), after DNA-bait and TF-prey yeast strains have been generated. Using a high-density array robotic platform, this method can be used to screen interactions between multiple DNA regions and >1000 TFs within a single experiment.
MeSH term(s)	Saccharomyces cerevisiae/genetics ; Saccharomyces cerevisiae/metabolism ; Two-Hybrid System Techniques ; DNA/genetics ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Gene Expression Regulation
Chemical Substances	DNA (9007-49-2) ; Transcription Factors
Language	English
Publishing date	2022-11-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-2847-8_2
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Article ; Online: Identification of conserved skeletal enhancers associated with craniosynostosis risk genes.

He 何璇, Xuan Anita / Berenson, Anna / Bernard, Michelle / Weber, Chris / Cook, Laura E / Visel, Axel / Fuxman Bass, Juan I / Fisher, Shannon

Human molecular genetics

2023 Volume 33, Issue 10, Page(s) 837–849

Abstract: Craniosynostosis, defined by premature fusion of one or multiple cranial sutures, is a common congenital defect affecting more than 1/2000 infants and results in restricted brain expansion. Single gene mutations account for 15%-20% of cases, largely as ... ...

Abstract	Craniosynostosis, defined by premature fusion of one or multiple cranial sutures, is a common congenital defect affecting more than 1/2000 infants and results in restricted brain expansion. Single gene mutations account for 15%-20% of cases, largely as part of a syndrome, but the majority are nonsyndromic with complex underlying genetics. We hypothesized that the two noncoding genomic regions identified by a GWAS for craniosynostosis contain distal regulatory elements for the risk genes BMPER and BMP2. To identify such regulatory elements, we surveyed conserved noncoding sequences from both risk loci for enhancer activity in transgenic Danio rerio. We identified enhancers from both regions that direct expression to skeletal tissues, consistent with the endogenous expression of bmper and bmp2. For each locus, we also found a skeletal enhancer that also contains a sequence variant associated with craniosynostosis risk. We examined the activity of each enhancer during craniofacial development and found that the BMPER-associated enhancer is active in the restricted region of cartilage closely associated with frontal bone initiation. The same enhancer is active in mouse skeletal tissues, demonstrating evolutionarily conserved activity. Using enhanced yeast one-hybrid assays, we identified transcription factors that bind each enhancer and observed differential binding between alleles, implicating multiple signaling pathways. Our findings help unveil the genetic mechanism of the two craniosynostosis risk loci. More broadly, our combined in vivo approach is applicable to many complex genetic diseases to build a link between association studies and specific genetic mechanisms.
MeSH term(s)	Craniosynostoses/genetics ; Animals ; Zebrafish/genetics ; Enhancer Elements, Genetic ; Humans ; Mice ; Genome-Wide Association Study ; Bone Morphogenetic Protein 2/genetics ; Bone Morphogenetic Protein 2/metabolism ; Genetic Predisposition to Disease ; Conserved Sequence/genetics ; Zebrafish Proteins/genetics ; Zebrafish Proteins/metabolism ; Animals, Genetically Modified ; Mutation
Chemical Substances	Bone Morphogenetic Protein 2 ; Zebrafish Proteins
Language	English
Publishing date	2023-10-26
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1108742-0
ISSN	1460-2083 ; 0964-6906
ISSN (online)	1460-2083
ISSN	0964-6906
DOI	10.1093/hmg/ddad182
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Article: A large-scale cancer-specific protein-DNA interaction network.

Lu, Yunwei / Berenson, Anna / Lane, Ryan / Guelin, Isabelle / Li, Zhaorong / Chen, Yilin / Shah, Sakshi / Yin, Meimei / Soto-Ugaldi, Luis Fernando / Fiszbein, Ana / Fuxman Bass, Juan Ignacio

bioRxiv : the preprint server for biology

2024

Abstract: Cancer development and progression are generally associated with dysregulation of gene expression, often resulting from changes in transcription factor (TF) sequence or expression. Identifying key TFs involved in cancer gene regulation provides a ... ...

Abstract	Cancer development and progression are generally associated with dysregulation of gene expression, often resulting from changes in transcription factor (TF) sequence or expression. Identifying key TFs involved in cancer gene regulation provides a framework for potential new therapeutics. This study presents a large-scale cancer gene TF-DNA interaction network as well as an extensive promoter clone resource for future studies. Most highly connected TFs do not show a preference for binding to promoters of genes associated with either good or poor cancer prognosis, suggesting that emerging strategies aimed at shifting gene expression balance between these two prognostic groups may be inherently complex. However, we identified potential for oncogene targeted therapeutics, with half of the tested oncogenes being potentially repressed by influencing specific activator or bifunctional TFs. Finally, we investigate the role of intrinsically disordered regions within the key cancer-related TF estrogen receptor ɑ (ESR1) on DNA binding and transcriptional activity, and found that these regions can have complex trade-offs in TF function. Altogether, our study not only broadens our knowledge of TFs involved in the cancer gene regulatory network but also provides a valuable resource for future studies, laying a foundation for potential therapeutic strategies targeting TFs in cancer.
Language	English
Publishing date	2024-01-29
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.01.24.577099
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Article: Compendium of human transcription factor effector domains

Soto, Luis F. / Li, Zhaorong / Santoso, Clarissa S. / Berenson, Anna / Ho, Isabella / Shen, Vivian X. / Yuan, Samson / Fuxman Bass, Juan I.

Molecular cell. 2022 Feb. 03, v. 82, no. 3

2022

Abstract: Transcription factors (TFs) regulate gene expression by binding to DNA sequences and modulating transcriptional activity through their effector domains. Despite the central role of effector domains in TF function, there is a current lack of a ... ...

Abstract	Transcription factors (TFs) regulate gene expression by binding to DNA sequences and modulating transcriptional activity through their effector domains. Despite the central role of effector domains in TF function, there is a current lack of a comprehensive resource and characterization of effector domains. Here, we provide a catalog of 924 effector domains across 594 human TFs. Using this catalog, we characterized the amino acid composition of effector domains, their conservation across species and across the human population, and their roles in human diseases. Furthermore, we provide a classification system for effector domains that constitutes a valuable resource and a blueprint for future experimental studies of TF effector domain function.
Keywords	DNA ; amino acid composition ; gene expression ; human population ; humans ; transcription (genetics) ; transcription factors
Language	English
Dates of publication	2022-0203
Size	p. 514-526.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2021.11.007
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Article ; Online: Role of Basal Forebrain Neurons in Adrenomyeloneuropathy in Mice and Humans.

Gong, Yi / Laheji, Fiza / Berenson, Anna / Li, Yedda / Moser, Ann / Qian, April / Frosch, Matthew / Sadjadi, Reza / Hahn, Ryan / Maguire, Casey A / Eichler, Florian

Annals of neurology

2023 Volume 95, Issue 3, Page(s) 442–458

Abstract: Objective: X-linked adrenoleukodystrophy is caused by mutations in the peroxisomal half-transporter ABCD1. The most common manifestation is adrenomyeloneuropathy, a hereditary spastic paraplegia of adulthood. The present study set out to understand the ... ...

Abstract	Objective: X-linked adrenoleukodystrophy is caused by mutations in the peroxisomal half-transporter ABCD1. The most common manifestation is adrenomyeloneuropathy, a hereditary spastic paraplegia of adulthood. The present study set out to understand the role of neuronal ABCD1 in mice and humans with adrenomyeloneuropathy. Methods: Neuronal expression of ABCD1 during development was assessed in mice and humans. ABCD1-deficient mice and human brain tissues were examined for corresponding pathology. Next, we silenced ABCD1 in cholinergic Sh-sy5y neurons to investigate its impact on neuronal function. Finally, we tested adeno-associated virus vector-mediated ABCD1 delivery to the brain in mice with adrenomyeloneuropathy. Results: ABCD1 is highly expressed in neurons located in the periaqueductal gray matter, basal forebrain and hypothalamus. In ABCD1-deficient mice (Abcd1-/y), these structures showed mild accumulations of α-synuclein. Similarly, healthy human controls had high expression of ABCD1 in deep gray nuclei, whereas X-ALD patients showed increased levels of phosphorylated tau, gliosis, and complement activation in those same regions, albeit not to the degree seen in neurodegenerative tauopathies. Silencing ABCD1 in Sh-sy5y neurons impaired expression of functional proteins and decreased acetylcholine levels, similar to observations in plasma of Abcd1-/y mice. Notably, hind limb clasping in Abcd1-/y mice was corrected through transduction of ABCD1 in basal forebrain neurons following intracerebroventricular gene delivery. Interpretation: Our study suggests that the basal forebrain-cortical cholinergic pathway may contribute to dysfunction in adrenomyeloneuropathy. Rescuing peroxisomal transport activity in basal forebrain neurons and supporting glial cells might represent a viable therapeutic strategy. ANN NEUROL 2024;95:442-458.
MeSH term(s)	Humans ; Animals ; Mice ; Adult ; Adrenoleukodystrophy/genetics ; Adrenoleukodystrophy/metabolism ; ATP-Binding Cassette Transporters/genetics ; Basal Forebrain/metabolism ; Neuroblastoma ; Neurons/metabolism ; Cholinergic Agents ; ATP Binding Cassette Transporter, Subfamily D, Member 1/genetics
Chemical Substances	ATP-Binding Cassette Transporters ; Cholinergic Agents ; Abcd1 protein, mouse ; ATP Binding Cassette Transporter, Subfamily D, Member 1
Language	English
Publishing date	2023-12-26
Publishing country	United States
Document type	Journal Article
ZDB-ID	80362-5
ISSN	1531-8249 ; 0364-5134
ISSN (online)	1531-8249
ISSN	0364-5134
DOI	10.1002/ana.26849
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Zs.MO 478: Show issues

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Article ; Online: Compendium of human transcription factor effector domains.

Soto, Luis F / Li, Zhaorong / Santoso, Clarissa S / Berenson, Anna / Ho, Isabella / Shen, Vivian X / Yuan, Samson / Fuxman Bass, Juan I

Molecular cell

2021 Volume 82, Issue 3, Page(s) 514–526

Abstract	Transcription factors (TFs) regulate gene expression by binding to DNA sequences and modulating transcriptional activity through their effector domains. Despite the central role of effector domains in TF function, there is a current lack of a comprehensive resource and characterization of effector domains. Here, we provide a catalog of 924 effector domains across 594 human TFs. Using this catalog, we characterized the amino acid composition of effector domains, their conservation across species and across the human population, and their roles in human diseases. Furthermore, we provide a classification system for effector domains that constitutes a valuable resource and a blueprint for future experimental studies of TF effector domain function.
MeSH term(s)	Amino Acid Sequence ; Binding Sites ; DNA/genetics ; DNA/metabolism ; Evolution, Molecular ; Gene Expression Regulation ; Humans ; Mutation ; Protein Binding ; Protein Domains ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Transcription, Genetic
Chemical Substances	Transcription Factors ; DNA (9007-49-2)
Language	English
Publishing date	2021-12-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2021.11.007
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Article ; Online: Paired yeast one-hybrid assays to detect DNA-binding cooperativity and antagonism across transcription factors.

Berenson, Anna / Lane, Ryan / Soto-Ugaldi, Luis F / Patel, Mahir / Ciausu, Cosmin / Li, Zhaorong / Chen, Yilin / Shah, Sakshi / Santoso, Clarissa / Liu, Xing / Spirohn, Kerstin / Hao, Tong / Hill, David E / Vidal, Marc / Fuxman Bass, Juan I

Nature communications

2023 Volume 14, Issue 1, Page(s) 6570

Abstract: Cooperativity and antagonism between transcription factors (TFs) can drastically modify their binding to regulatory DNA elements. While mapping these relationships between TFs is important for understanding their context-specific functions, existing ... ...

Abstract	Cooperativity and antagonism between transcription factors (TFs) can drastically modify their binding to regulatory DNA elements. While mapping these relationships between TFs is important for understanding their context-specific functions, existing approaches either rely on DNA binding motif predictions, interrogate one TF at a time, or study individual TFs in parallel. Here, we introduce paired yeast one-hybrid (pY1H) assays to detect cooperativity and antagonism across hundreds of TF-pairs at DNA regions of interest. We provide evidence that a wide variety of TFs are subject to modulation by other TFs in a DNA region-specific manner. We also demonstrate that TF-TF relationships are often affected by alternative isoform usage and identify cooperativity and antagonism between human TFs and viral proteins from human papillomaviruses, Epstein-Barr virus, and other viruses. Altogether, pY1H assays provide a broadly applicable framework to study how different functional relationships affect protein occupancy at regulatory DNA regions.
MeSH term(s)	Humans ; Transcription Factors/genetics ; Transcription Factors/metabolism ; Saccharomyces cerevisiae/genetics ; Saccharomyces cerevisiae/metabolism ; Epstein-Barr Virus Infections ; Protein Binding ; Herpesvirus 4, Human/genetics ; Herpesvirus 4, Human/metabolism ; DNA/metabolism ; Binding Sites
Chemical Substances	Transcription Factors ; DNA (9007-49-2)
Language	English
Publishing date	2023-10-18
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/s41467-023-42445-6
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Article ; Online: Peroxisome Metabolism Contributes to PIEZO2-Mediated Mechanical Allodynia.

Gong, Yi / Laheji, Fiza / Berenson, Anna / Qian, April / Park, Sang-O / Kok, Rene / Selig, Martin / Hahn, Ryan / Sadjadi, Reza / Kemp, Stephan / Eichler, Florian

Cells

2022 Volume 11, Issue 11

Abstract: Mutations in the peroxisomal half-transporter ABCD1 cause X-linked adrenoleukodystrophy, resulting in elevated very long-chain fatty acids (VLCFA), progressive neurodegeneration and an associated pain syndrome that is poorly understood. In the nervous ... ...

Abstract	Mutations in the peroxisomal half-transporter ABCD1 cause X-linked adrenoleukodystrophy, resulting in elevated very long-chain fatty acids (VLCFA), progressive neurodegeneration and an associated pain syndrome that is poorly understood. In the nervous system of mice, we found ABCD1 expression to be highest in dorsal root ganglia (DRG), with satellite glial cells (SGCs) displaying higher expression than neurons. We subsequently examined sensory behavior and DRG pathophysiology in mice deficient in ABCD1 compared to wild-type mice. Beginning at 8 months of age,
MeSH term(s)	ATP Binding Cassette Transporter, Subfamily D, Member 1/metabolism ; ATP-Binding Cassette Transporters/metabolism ; Adrenoleukodystrophy/genetics ; Adrenoleukodystrophy/metabolism ; Animals ; Fatty Acids/metabolism ; Hyperalgesia/genetics ; Hyperalgesia/metabolism ; Ion Channels/genetics ; Ion Channels/metabolism ; Mice ; Pain/metabolism ; Peroxisomes/metabolism
Chemical Substances	ATP Binding Cassette Transporter, Subfamily D, Member 1 ; ATP-Binding Cassette Transporters ; Abcd1 protein, mouse ; Fatty Acids ; Ion Channels ; Piezo2 protein, mouse
Language	English
Publishing date	2022-06-04
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells11111842
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Article ; Online: Intragenic proviral elements support transcription of defective HIV-1 proviruses.

Kuniholm, Jeffrey / Armstrong, Elise / Bernabe, Brandy / Coote, Carolyn / Berenson, Anna / Patalano, Samantha D / Olson, Alex / He, Xianbao / Lin, Nina H / Fuxman Bass, Juan I / Henderson, Andrew J

PLoS pathogens

2021 Volume 17, Issue 12, Page(s) e1009982

Abstract: HIV-1 establishes a persistent proviral reservoir by integrating into the genome of infected host cells. Current antiretroviral treatments do not target this persistent population of proviruses which include latently infected cells that upon treatment ... ...

Abstract	HIV-1 establishes a persistent proviral reservoir by integrating into the genome of infected host cells. Current antiretroviral treatments do not target this persistent population of proviruses which include latently infected cells that upon treatment interruption can be reactivated to contribute to HIV-1 rebound. Deep sequencing of persistent HIV proviruses has revealed that greater than 90% of integrated HIV genomes are defective and unable to produce infectious virions. We hypothesized that intragenic elements in the HIV genome support transcription of aberrant HIV-1 RNAs from defective proviruses that lack long terminal repeats (LTRs). Using an intact provirus detection assay, we observed that resting CD4+ T cells and monocyte-derived macrophages (MDMs) are biased towards generating defective HIV-1 proviruses. Multiplex reverse transcription droplet digital PCR identified env and nef transcripts which lacked 5' untranslated regions (UTR) in acutely infected CD4+ T cells and MDMs indicating transcripts are generated that do not utilize the promoter within the LTR. 5'UTR-deficient env transcripts were also identified in a cohort of people living with HIV (PLWH) on ART, suggesting that these aberrant RNAs are produced in vivo. Using 5' rapid amplification of cDNA ends (RACE), we mapped the start site of these transcripts within the Env gene. This region bound several cellular transcription factors and functioned as a transcriptional regulatory element that could support transcription and translation of downstream HIV-1 RNAs. These studies provide mechanistic insights into how defective HIV-1 proviruses are persistently expressed to potentially drive inflammation in PLWH.
MeSH term(s)	Genome, Viral/genetics ; HIV Infections/virology ; HIV-1/genetics ; Humans ; Macrophages/virology ; Polymerase Chain Reaction ; Proviruses/genetics ; RNA, Viral/genetics ; Transcription, Genetic ; env Gene Products, Human Immunodeficiency Virus/genetics ; nef Gene Products, Human Immunodeficiency Virus/genetics
Chemical Substances	RNA, Viral ; env Gene Products, Human Immunodeficiency Virus ; nef Gene Products, Human Immunodeficiency Virus ; nef protein, Human immunodeficiency virus 1
Language	English
Publishing date	2021-12-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1009982
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Article: Widespread variation in molecular interactions and regulatory properties among transcription factor isoforms.

Lambourne, Luke / Mattioli, Kaia / Santoso, Clarissa / Sheynkman, Gloria / Inukai, Sachi / Kaundal, Babita / Berenson, Anna / Spirohn-Fitzgerald, Kerstin / Bhattacharjee, Anukana / Rothman, Elisabeth / Shrestha, Shaleen / Laval, Florent / Yang, Zhipeng / Bisht, Deepa / Sewell, Jared A / Li, Guangyuan / Prasad, Anisa / Phanor, Sabrina / Lane, Ryan /

Campbell, Devlin M / Hunt, Toby / Balcha, Dawit / Gebbia, Marinella / Twizere, Jean-Claude / Hao, Tong / Frankish, Adam / Riback, Josh A / Salomonis, Nathan / Calderwood, Michael A / Hill, David E / Sahni, Nidhi / Vidal, Marc / Bulyk, Martha L / Fuxman Bass, Juan I

bioRxiv : the preprint server for biology

2024

Abstract: Most human Transcription factors (TFs) genes encode multiple protein isoforms differing in DNA binding domains, effector domains, or other protein regions. The global extent to which this results in functional differences between isoforms remains unknown. ...

Abstract	Most human Transcription factors (TFs) genes encode multiple protein isoforms differing in DNA binding domains, effector domains, or other protein regions. The global extent to which this results in functional differences between isoforms remains unknown. Here, we systematically compared 693 isoforms of 246 TF genes, assessing DNA binding, protein binding, transcriptional activation, subcellular localization, and condensate formation. Relative to reference isoforms, two-thirds of alternative TF isoforms exhibit differences in one or more molecular activities, which often could not be predicted from sequence. We observed two primary categories of alternative TF isoforms: "rewirers" and "negative regulators", both of which were associated with differentiation and cancer. Our results support a model wherein the relative expression levels of, and interactions involving, TF isoforms add an understudied layer of complexity to gene regulatory networks, demonstrating the importance of isoform-aware characterization of TF functions and providing a rich resource for further studies.
Language	English
Publishing date	2024-04-10
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.12.584681
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