OptoGranules reveal the evolution of stress granules to ALS-FTD pathology
Posted on: 7 July 2018
Preprint posted on 18 June 2018
Optogenetic tool to identify and study how chronic stress causes the formation of pathogenic inclusions in neurodegenerative diseases.
Selected by Srivats Venkataramanan
Categories: biochemistry, cell biology, molecular biology, neuroscience, pathology
Context:
Amyotrophic Lateral Sclerosis (ALS – also known as Lou Gehrig’s Disease), is a progressive, fatal neurodegenerative disease. Both ALS and a clinically overlapping condition, Fronto-Temporal Dementia (FTD) are characterized by insoluble cytoplasmic aggregates within affected neurons. The appearance of these inclusions precedes neuronal destruction, and they are typically highly enriched in a hyper-phosphorylated and ubiquitinated form of a 43KDa DNA-binding protein, TDP-43. In addition, these pathological inclusions also host a variety of RNA-binding proteins, as well as mRNA [1].
All of the proteins within these inclusions are also components of stress granules (SGs), cytoplasmic mRNP granules that form when cells experience a wide variety of stresses that also repress mRNA translation. In fact, translation repression has long been considered a pre-requisite for endogenous SG formation. The similarities between the composition of these transient, dynamic SGs, and the persistent, pathological cytoplasmic inclusions seen in ALS affected neurons have led many to hypothesize that the formation of these inclusions might relate to altered/perturbed stress granule dynamics [2]. As support for this hypothesis, mutations in a number of SG-related proteins are strongly correlated with the occurrence of ALS [3].
However, the hypothesis that SGs are required for the formation of pathological inclusions has never been robustly tested, and neither have any potential mechanistic connections between the two addressed. The challenges have largely been technical. Since most SG-associated proteins are RNA-binding proteins and all of them have other cellular functions, abrogating SG formation via genetic methods causes too many pleiotropic effects to provide a clean assay [4]. On the other hand, methods to artificially induce SGs rely on subjecting cells to external stressors, all of which introduce the confounding variable of translation repression (most often via the inhibitory phosphorylation of initiation faction eIF2⍺) [5]. In this preprint, Zhang et al. develop a novel optogenetic tool to induce SG formation rapidly and robustly without the confounding variable of translation repression, allowing them to define the role of SGs in the formation of pathogenic ALS-type cytoplasmic inclusions.
Tools and Key Findings:
Zhang et al. replace the dimerization domain of G3BP1 (a core protein of SGs) with the dimerization domain from cryptochrome 2 (CRY2 – a blue light-absorbing photosensor from Arabidopsis thaliana), thereby allowing rapid assembly of SGs in response to blue light. Importantly, these light-induced granules (named OptoGranules) contain polyadenylated mRNA as well as every canonical SG protein tested, indicating that they are, in fact, bona fide stress granules.
Zhang et al. Supplementary Video 2: Opto-G3BP1 forms granules
upon activation by blue light.
Critically, the formation of OptoGranules DOES NOT involve general translational repression via eIF2⍺ phosphorylation, thereby eliminating the major confounding variable involved in the study of the biological consequences of SG formation. In addition, OptoGranules form within seconds of induction by blue light, and disassemble within ~5 minutes once the light stimulus is withdrawn. The OptoGranules also provide evidence for a definite hierarchy within the SG proteome. While G3BP acts as a nucleator of granules, other canonical SG proteins, such as TIA1, FUS and even TDP-43, are unable to serve as initiators of SG assembly, and are likely client proteins.
With this tool in hand, the authors examine the consequences of chronic, intermittent SG formation. They use a blue-light treatment regime forcing cycles of OptoGranule assembly-disasembly, mimicking chronic stress cells might face within the context of an organism. The OptoGranules formed at the beginning of this regimen contain TDP-43, but not in the hyper-phosphorylated form seen in the pathological ALS inclusions, indicating that they are canonical SGs. However, when cells are subjected to this pattern of OptoGranule assembly and disassembly for extended periods of time, the TDP-43 incorporated within them becomes increasingly phosphorylated and ubiquitinated, and cell viability decreases, a characteristic of ALS inclusions. While the authors’ initial results are performed in the context of a transformed cell line, they recapitulate their experiments in neurons derived from iPSCs expressing OptoGranule-compatible G3BP1, demonstrating in a neuronal context the evolution of SGs into pathogenic ALS-like inclusions.
Taken together, the authors demonstrate that the chronic assembly of SGs is detrimental to the cell, independently of the distal stressor. Further, they demonstrate convincingly that chronically and intermittently stressing cells (and more specifically, neurons) results in the SGs within them to morph into ALS-like pathological inclusions.
Why I chose this preprint:
The cellular response to any individual stress almost invariably involves the activation and/or repression of a multitude of pathways and mechanisms. Inferring a causal chain by deconvoluting the various pathways the cell uses to adapt and survive remains a challenge. In the case of ALS-FTD, a link between SGs and the pathological inclusions had long been suspected, but never proven, due to the confounding variables described above. I found the approach taken by the authors to develop a tool to remove the confounding variable and allow the study of SGs in isolation to be an extraordinarily elegant experimental system. The power of this system was demonstrated in the establishment of a concrete link between SG dynamics and ALS pathology, viz. the evolution of SGs into phosphorylated/ubiquitinated TDP-43 containing pathological cytoplasmic inclusions under chronic stress.
Open questions and future directions:
The authors speculate that physiological amyloid-like states in SGs could serve as ‘seeds’ for the formation of TDP-43 pathological amyloids under chronic stress. One open question that remains is the context and mechanism of TDP-43 phosophorylation. Is TDP-43 phosphorylated during, or as a consequence of, SG incorporation and subsequent amyloid formation? Or does the phosphorylation occur extra-granularly, and promote amyloid formation?
Additionally, given that global translation is presumably not downregulated upon OptoGranule formation (as evidenced by the lack of eIF2⍺ phosphorylation, I would be curious to know whether the Optogranules recapitulate the translationally null state of endogenous SGs.
Broadly, the OptoGranule system offers a marvelous opportunity to further study modulators of SG assembly, dynamics and the biological roles played by this phase-separated cytoplasmic organelle. More specifically, the tool provides an assay to test the roles of various ALS-associated mutations on the formation of the pathological cytoplasmic inclusions. Understanding these mechanisms is critical to inform future efforts to slow or even reverse disease progression.
References:
- Ling, S.C., M. Polymenidou, and D.W. Cleveland, Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron, 2013. 79(3): p. 416-38.
- Aulas, A. and C. Vande Velde, Alterations in stress granule dynamics driven by TDP-43 and FUS: a link to pathological inclusions in ALS? Front Cell Neurosci, 2015. 9: p. 423.
- Figley, M.D., et al., Profilin 1 associates with stress granules and ALS-linked mutations alter stress granule dynamics. J Neurosci, 2014. 34(24): p. 8083-97.
- Youn, J.Y., et al., High-Density Proximity Mapping Reveals the Subcellular Organization of mRNA-Associated Granules and Bodies. Mol Cell, 2018. 69(3): p. 517-532 e11.
- Buchan, J.R. and R. Parker, Eukaryotic stress granules: the ins and outs of translation. Mol Cell, 2009. 36(6): p. 932-41.
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| List by | Rob Hynds |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |
Also in the neuroscience category:
May in preprints – the CellBio edition
A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: 1) Biochemistry/metabolism 2) Cancer cell Biology 3) Cell adhesion, migration and cytoskeleton 4) Cell organelles and organisation 5) Cell signalling and 6) Genetics
| List by | Barbora Knotkova et al. |
April in preprints – the CellBio edition
A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: 1) biochemistry/metabolism 2) cell cycle and division 3) cell organelles and organisation 4) cell signalling and mechanosensing 5) (epi)genetics
| List by | Vibha SINGH et al. |
Biologists @ 100 conference preList
This preList aims to capture all preprints being discussed at the Biologists @100 conference in Liverpool, UK, either as part of the poster sessions or the (flash/short/full-length) talks.
| List by | Reinier Prosee, Jonathan Townson |
2024 Hypothalamus GRC
This 2024 Hypothalamus GRC (Gordon Research Conference) preList offers an overview of cutting-edge research focused on the hypothalamus, a critical brain region involved in regulating homeostasis, behavior, and neuroendocrine functions. The studies included cover a range of topics, including neural circuits, molecular mechanisms, and the role of the hypothalamus in health and disease. This collection highlights some of the latest advances in understanding hypothalamic function, with potential implications for treating disorders such as obesity, stress, and metabolic diseases.
| List by | Nathalie Krauth |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
Journal of Cell Science meeting ‘Imaging Cell Dynamics’
This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.
| List by | Helen Zenner |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Young Embryologist Network Conference 2019
Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London
| List by | Alex Eve |
Also in the pathology category:
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
COVID-19 / SARS-CoV-2 preprints
List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic
| List by | Dey Lab, Zhang-He Goh |
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Cellular metabolism
A curated list of preprints related to cellular metabolism at Biorxiv by Pablo Ranea Robles from the Prelights community. Special interest on lipid metabolism, peroxisomes and mitochondria.
| List by | Pablo Ranea Robles |