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Article ; Online: Selective degradation of ribosomes during oncogene-induced senescence: molecular insights and biological perspectives.

López, Aida Rodríguez / Frankel, Lisa B

2024 , Page(s) 1–3

Abstract: Ribosomes are conserved macromolecular machines that are responsible for protein synthesis in all cells. While our knowledge of ribosome biogenesis and function has increased significantly in recent years, little is known about how ribosomes are degraded ...

Abstract	Ribosomes are conserved macromolecular machines that are responsible for protein synthesis in all cells. While our knowledge of ribosome biogenesis and function has increased significantly in recent years, little is known about how ribosomes are degraded under specific cellular conditions. We recently uncovered that ribosomes are efficiently turned over by selective macroautophagy/autophagy during oncogene-induced senescence (OIS). By profiling the ribosome interactome in human fibroblasts undergoing OIS, we discovered a key role for the de-ubiquitinating enzyme USP10 in guiding this process. Release of USP10 from ribosomes during senescence leads to their enhanced ubiquitination and selective sequestering by autophagy through the SQSTM1/p62 receptor protein. This process is important for sustaining senescence-associated metabolome and secretome alterations.
Language	English
Publishing date	2024-02-21
Publishing country	United States
Document type	Journal Article
ZDB-ID	2454135-7
ISSN	1554-8635 ; 1554-8627
ISSN (online)	1554-8635
ISSN	1554-8627
DOI	10.1080/15548627.2024.2319022
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Article ; Online: Post-transcriptional dynamics and RNA homeostasis in autophagy and cancer.

Kolapalli, Srinivasa Prasad / Nielsen, Thorbjørn M / Frankel, Lisa B

Cell death and differentiation

2023

Abstract: Autophagy is an essential recycling and quality control pathway which preserves cellular and organismal homeostasis. As a catabolic process, autophagy degrades damaged and aged intracellular components in response to conditions of stress, including ... ...

Abstract	Autophagy is an essential recycling and quality control pathway which preserves cellular and organismal homeostasis. As a catabolic process, autophagy degrades damaged and aged intracellular components in response to conditions of stress, including nutrient deprivation, oxidative and genotoxic stress. Autophagy is a highly adaptive and dynamic process which requires an intricately coordinated molecular control. Here we provide an overview of how autophagy is regulated post-transcriptionally, through RNA processing events, epitranscriptomic modifications and non-coding RNAs. We further discuss newly revealed RNA-binding properties of core autophagy machinery proteins and review recent indications of autophagy's ability to impact cellular RNA homeostasis. From a physiological perspective, we examine the biological implications of these emerging regulatory layers of autophagy, particularly in the context of nutrient deprivation and tumorigenesis.
Language	English
Publishing date	2023-08-09
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	1225672-9
ISSN	1476-5403 ; 1350-9047
ISSN (online)	1476-5403
ISSN	1350-9047
DOI	10.1038/s41418-023-01201-5
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Article ; Online: EIF5A mediates autophagy via translation of ATG3.

Frankel, Lisa B

Autophagy

2018 Volume 14, Issue 7, Page(s) 1288–1289

Abstract: The core macroautophagy/autophagy machinery consists of a large group of autophagy-related (ATG) proteins, that mediate highly controlled, step-wise execution of this conserved intracellular degradation process. Whereas ATG proteins have been intensely ... ...

Abstract	The core macroautophagy/autophagy machinery consists of a large group of autophagy-related (ATG) proteins, that mediate highly controlled, step-wise execution of this conserved intracellular degradation process. Whereas ATG proteins have been intensely studied in terms of protein interactions, post-translational modifications and transcriptional regulation, the mechanisms ensuring efficient translation of ATG proteins are not well understood. In a recent study, we describe an evolutionarily conserved role for EIF5A (eukaryotic translation initiation factor 5A) in autophagy. We demonstrate that EIF5A mediates Atg8-family protein lipidation and autophagosome formation via translation of the E2-like ATG3 protein. Moreover, we identify a particular motif in ATG3 causing EIF5A-dependency for its efficient translation.
MeSH term(s)	Animals ; Autophagy ; Autophagy-Related Protein 5/metabolism ; Cell Line ; Humans ; Models, Biological ; Peptide Initiation Factors/metabolism ; Protein Biosynthesis ; RNA-Binding Proteins/metabolism ; Eukaryotic Translation Initiation Factor 5A
Chemical Substances	Autophagy-Related Protein 5 ; Peptide Initiation Factors ; RNA-Binding Proteins
Language	English
Publishing date	2018-07-20
Publishing country	United States
Document type	Journal Article
ZDB-ID	2454135-7
ISSN	1554-8635 ; 1554-8627
ISSN (online)	1554-8635
ISSN	1554-8627
DOI	10.1080/15548627.2018.1491213
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Article ; Online: EIF4A3: a gatekeeper of autophagy.

Sakellariou, Despoina / Frankel, Lisa B

Autophagy

2021 Volume 17, Issue 12, Page(s) 4504–4505

Abstract: EIF4A3 (eukaryotic translation initiation factor 4A3) is an RNA helicase and core component of the exon junction complex. While this RNA-binding protein (RBP) is well-characterized for its crucial roles in splicing, RNA trafficking and nonsense-mediated ... ...

Abstract	EIF4A3 (eukaryotic translation initiation factor 4A3) is an RNA helicase and core component of the exon junction complex. While this RNA-binding protein (RBP) is well-characterized for its crucial roles in splicing, RNA trafficking and nonsense-mediated decay, its role in the regulation of metabolic signaling pathways remains elusive. In a recent study, we describe a new role for EIF4A3 as a negative regulator of macroautophagy/autophagy. Mechanistically, we report that EIF4A3, through its ability to safeguard splicing, can maintain low basal levels of autophagy through the cytosolic retention of the key autophagy transcription factor TFEB. Upon EIF4A3 depletion, the shuttling of TFEB to the nucleus results in an integrated transcriptional response, which induces both early and late steps of the autophagy pathway and enhances autophagic flux. We further report the upregulation of EIF4A3 across multiple cancer types and highlight the relevance of this newly identified EIF4A3-TFEB signaling axis in human tumors.
MeSH term(s)	Autophagy/genetics ; Basic Helix-Loop-Helix Leucine Zipper Transcription Factors/metabolism ; DEAD-box RNA Helicases/genetics ; DEAD-box RNA Helicases/metabolism ; Eukaryotic Initiation Factor-4A/genetics ; Eukaryotic Initiation Factor-4A/metabolism ; Humans ; RNA Splicing/genetics ; RNA-Binding Proteins/genetics ; RNA-Binding Proteins/metabolism
Chemical Substances	Basic Helix-Loop-Helix Leucine Zipper Transcription Factors ; RNA-Binding Proteins ; Eukaryotic Initiation Factor-4A (EC 2.7.7.-) ; EIF4A3 protein, human (EC 3.6.1.-) ; DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2021-10-13
Publishing country	United States
Document type	Journal Article
ZDB-ID	2454135-7
ISSN	1554-8635 ; 1554-8627
ISSN (online)	1554-8635
ISSN	1554-8627
DOI	10.1080/15548627.2021.1985881
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Article: Selective Autophagy of the Protein Homeostasis Machinery: Ribophagy, Proteaphagy and ER-Phagy.

Beese, Carsten J / Brynjólfsdóttir, Sólveig H / Frankel, Lisa B

Frontiers in cell and developmental biology

2020 Volume 7, Page(s) 373

Abstract: The eukaryotic cell has developed intricate machineries that monitor and maintain proteome homeostasis in order to ensure cellular functionality. This involves the carefully coordinated balance between protein synthesis and degradation pathways, which ... ...

Abstract	The eukaryotic cell has developed intricate machineries that monitor and maintain proteome homeostasis in order to ensure cellular functionality. This involves the carefully coordinated balance between protein synthesis and degradation pathways, which are dynamically regulated in order to meet the constantly changing demands of the cell. Ribosomes, together with the endoplasmic reticulum (ER), are the key drivers of protein synthesis, folding, maturation and sorting, while the proteasome plays a pivotal role in terminating the existence of thousands of proteins that are misfolded, damaged or otherwise obsolete. The synthesis, structure and function of these dedicated machines has been studied for decades, however, much less is understood about the mechanisms that control and execute their own turnover. Autophagy, an evolutionarily conserved catabolic pathway, mediates degradation of a large variety of cytosolic substrates, ranging from single proteins to entire organelles or multi-subunit macromolecular complexes. In this review, we focus on selective autophagy of three key components of the protein homeostasis machinery: ribosomes, ER and proteasomes, through the selective autophagy pathways of ribophagy, ER-phagy, and proteaphagy. We discuss newly discovered mechanisms for the selective clearance of these substrates, which are often stress-dependent and involve specialized signals for cargo recognition by a growing number of receptors. We further discuss the interplay between these pathways and their biological impact on key aspects of proteome homeostasis and cellular function in health and disease.
Language	English
Publishing date	2020-01-21
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2737824-X
ISSN	2296-634X
ISSN	2296-634X
DOI	10.3389/fcell.2019.00373
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Article: The Autophagy-RNA Interplay: Degradation and Beyond.

Abildgaard, Marie H / Brynjólfsdóttir, Sólveig H / Frankel, Lisa B

Trends in biochemical sciences

2020 Volume 45, Issue 10, Page(s) 845–857

Abstract: Autophagy is a highly conserved degradation pathway that ensures nutrient recycling and removal of unwanted substrates. This process has a fundamental role in stress adaptation and maintenance of cellular homeostasis. Here, we discuss emerging aspects of ...

Abstract	Autophagy is a highly conserved degradation pathway that ensures nutrient recycling and removal of unwanted substrates. This process has a fundamental role in stress adaptation and maintenance of cellular homeostasis. Here, we discuss emerging aspects of the autophagy-RNA interplay, including autophagy-mediated degradation of RNA, RNA-binding proteins (RBPs), and ribonucleoprotein (RNP) complexes. Beyond degradation, we review new roles for autophagy players in the secretion and intracellular transport of RNA and related complexes. We discuss the physiological importance of these events for RNA homeostasis and gene expression programs, as well as their implications for disease, including cancer and neurodegeneration. Lastly, we examine how post-transcriptional regulation of autophagy, through specialized processing and selective translation of key transcripts, challenges and updates our current view of autophagy complexity.
MeSH term(s)	Autophagy ; Biological Transport ; Homeostasis ; Hydrolysis ; Lysosomes/metabolism ; RNA/metabolism ; Ribonucleoproteins/metabolism
Chemical Substances	Ribonucleoproteins ; RNA (63231-63-0)
Language	English
Publishing date	2020-08-19
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	194216-5
ISSN	1362-4326 ; 0968-0004 ; 0376-5067
ISSN (online)	1362-4326
ISSN	0968-0004 ; 0376-5067
DOI	10.1016/j.tibs.2020.07.007
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Article: The Autophagy–RNA Interplay: Degradation and Beyond

Abildgaard, Marie H / Brynjólfsdóttir, Sólveig H / Frankel, Lisa B

Trends in biochemical sciences. 2020 Oct., v. 45, no. 10

2020

Abstract	Autophagy is a highly conserved degradation pathway that ensures nutrient recycling and removal of unwanted substrates. This process has a fundamental role in stress adaptation and maintenance of cellular homeostasis. Here, we discuss emerging aspects of the autophagy–RNA interplay, including autophagy-mediated degradation of RNA, RNA-binding proteins (RBPs), and ribonucleoprotein (RNP) complexes. Beyond degradation, we review new roles for autophagy players in the secretion and intracellular transport of RNA and related complexes. We discuss the physiological importance of these events for RNA homeostasis and gene expression programs, as well as their implications for disease, including cancer and neurodegeneration. Lastly, we examine how post-transcriptional regulation of autophagy, through specialized processing and selective translation of key transcripts, challenges and updates our current view of autophagy complexity.
Keywords	RNA transport ; autophagy ; gene expression ; homeostasis ; neurodegenerative diseases ; ribonucleoproteins ; secretion
Language	English
Dates of publication	2020-10
Size	p. 845-857.
Publishing place	Elsevier Ltd
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	194220-7
ISSN	0968-0004 ; 0376-5067
ISSN	0968-0004 ; 0376-5067
DOI	10.1016/j.tibs.2020.07.007
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Article ; Online: Emerging connections between RNA and autophagy.

Frankel, Lisa B / Lubas, Michal / Lund, Anders H

Autophagy

2017 Volume 13, Issue 1, Page(s) 3–23

Abstract: Macroautophagy/autophagy is a key catabolic process, essential for maintaining cellular homeostasis and survival through the removal and recycling of unwanted cellular material. Emerging evidence has revealed intricate connections between the RNA and ... ...

Abstract	Macroautophagy/autophagy is a key catabolic process, essential for maintaining cellular homeostasis and survival through the removal and recycling of unwanted cellular material. Emerging evidence has revealed intricate connections between the RNA and autophagy research fields. While a majority of studies have focused on protein, lipid and carbohydrate catabolism via autophagy, accumulating data supports the view that several types of RNA and associated ribonucleoprotein complexes are specifically recruited to phagophores (precursors to autophagosomes) and subsequently degraded in the lysosome/vacuole. Moreover, recent studies have revealed a substantial number of novel autophagy regulators with RNA-related functions, indicating roles for RNA and associated proteins not only as cargo, but also as regulators of this process. In this review, we discuss widespread evidence of RNA catabolism via autophagy in yeast, plants and animals, reviewing the molecular mechanisms and biological importance in normal physiology, stress and disease. In addition, we explore emerging evidence of core autophagy regulation mediated by RNA-binding proteins and noncoding RNAs, and point to gaps in our current knowledge of the connection between RNA and autophagy. Finally, we discuss the pathological implications of RNA-protein aggregation, primarily in the context of neurodegenerative disease.
Keywords	covid19
Language	English
Publishing date	2017-01-02
Publishing country	United States
Document type	Journal Article
ZDB-ID	2454135-7
ISSN	1554-8635 ; 1554-8627
ISSN (online)	1554-8635
ISSN	1554-8627
DOI	10.1080/15548627.2016.1222992
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Article ; Online: Measuring Autophagic Cargo Flux with Keima-Based Probes.

Engedal, Nikolai / Sønstevold, Tonje / Beese, Carsten J / Selladurai, Sarvini / Melcher, Thea / Simensen, Julia E / Frankel, Lisa B / Urbanucci, Alfonso / Torgersen, Maria L

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

2021 Volume 2445, Page(s) 99–115

Abstract: Autophagy and autophagy-associated genes are implicated in a growing list of cellular, physiological, and pathophysiological processes and conditions. Therefore, it is ever more important to be able to reliably monitor and quantify autophagic activity. ... ...

Abstract	Autophagy and autophagy-associated genes are implicated in a growing list of cellular, physiological, and pathophysiological processes and conditions. Therefore, it is ever more important to be able to reliably monitor and quantify autophagic activity. Whereas autophagic markers, such as LC3 can provide general indications about autophagy, specific and accurate detection of autophagic activity requires assessment of autophagic cargo flux. Here, we provide protocols on how to monitor bulk and selective autophagy by the use of inducible expression of exogenous probes based on the fluorescent coral protein Keima. To exemplify and demonstrate the power of this system, we provide data obtained by analyses of cytosolic and mitochondrially targeted Keima probes in human retinal epithelial cells treated with the mTOR-inhibitor Torin1 or with the iron chelator deferiprone (DFP). Our data indicate that Torin1 induces autophagic flux of cytosol and mitochondria to a similar degree, that is, compatible with induction of bulk autophagy, whereas DFP induces a highly selective form of mitophagy that efficiently excludes cytosol.
MeSH term(s)	Autophagy/physiology ; Microtubule-Associated Proteins/metabolism ; Mitochondria/metabolism ; Mitophagy
Chemical Substances	Microtubule-Associated Proteins
Language	English
Publishing date	2021-12-22
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-2071-7_7
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Article ; Online: Restructuring of the plasma membrane upon damage by LC3-associated macropinocytosis.

Sønder, Stine Lauritzen / Häger, Swantje Christin / Heitmann, Anne Sofie Busk / Frankel, Lisa B / Dias, Catarina / Simonsen, Adam Cohen / Nylandsted, Jesper

Science advances

2021 Volume 7, Issue 27

Abstract: The plasma membrane shapes and protects the eukaryotic cell from its surroundings and is crucial for cell life. Although initial repair mechanisms to reseal injured membranes are well established, less is known about how cells restructure damaged ... ...

Abstract	The plasma membrane shapes and protects the eukaryotic cell from its surroundings and is crucial for cell life. Although initial repair mechanisms to reseal injured membranes are well established, less is known about how cells restructure damaged membranes in the aftermath to restore homeostasis. Here, we show that cells respond to plasma membrane injury by activating proteins associated with macropinocytosis specifically at the damaged membrane. Subsequent to membrane resealing, cells form large macropinosomes originating from the repair site, which eventually become positive for autophagy-related LC3B protein. This process occurs independent of ULK1, ATG13, and WIPI2 but dependent on ATG7, p62, and Rubicon. Internalized macropinosomes shrink in the cytoplasm, likely by osmotic draining, and eventually fuse with lysosomes. We propose that a form of macropinocytosis coupled to noncanonical autophagy, which we term LC3-associated macropinocytosis (LAM) functions to remove damaged material from the plasma membrane and restore membrane integrity upon injury.
Language	English
Publishing date	2021-07-02
Publishing country	United States
Document type	Journal Article
ZDB-ID	2810933-8
ISSN	2375-2548 ; 2375-2548
ISSN (online)	2375-2548
ISSN	2375-2548
DOI	10.1126/sciadv.abg1969
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