A Transcriptional Switch Governing Fibroblast Plasticity Underlies Reversibility of Chronic Heart Disease
Preprint posted on 22 July 2020 https://www.biorxiv.org/content/10.1101/2020.07.21.214874v1
Article now published in Nature at http://dx.doi.org/10.1038/s41586-021-03674-1
Fibroblasts: an enigmatic, diverse and plastic cell type that can determine the fate of heart failure
Selected by Osvaldo Contreras, Alexander Ward
Background
Why mammalian cardiac regeneration and repair do not occur in adults remains a mystery.
Heart failure (HF) is a leading cause of mortality and hospitalization thus representing a burden to the life of patients, and the societal costs are astounding. Although progress has been made to reduce mortality and improve the quality of life of patients after HF, the 5-year mortality after an initial diagnosis of HF is about 40%. No effective therapeutics are available for the treatment of HF. Remarkably, HF worsens heart degeneration and organ dysfunction leading to progressive changes in gene expression that dynamically influence HF onset and development. HF is associated with exacerbated deposition of extracellular matrix (ECM) components and proliferation of endogenous cardiac fibroblasts that later differentiate into fibrosis-causing myofibroblasts. Among the several cell types that participate in heart repair, resident fibroblasts play a critical role as progenitor cells and by synthesizing the ECM of the heart. Thus, fibroblasts are essential in modelling and remodelling the structural integrity of tissues and organs in health and disease. Cardiac resident fibroblasts are not produced de novo and they exhibit high heterogeneity, especially after injury. This fuels the need to develop novel pharmacological approaches to combat fibrosis in HF aiming to boost heart function.
Previous preclinical work led by the authors unveiled the participation of Bromodomain and extraterminal domain (BET) protein inhibitors in attenuating heart failure. BET proteins recognise acetyl-lysine on histones and regulate gene transcription and chromatin remodelling. Hence, BETs have been targeted in disease with several ongoing clinical trials seeking to inhibit BETs in diverse pathological settings like cancer and inflammation. The authors have demonstrated that the small molecule BET inhibitor JQ1 prevents the development of cardiac hypertrophy, left ventricle dysfunction and fibrosis when administered at the onset of HF. Furthermore, JQ1 reduces pathology and improves cardiac function in mouse models of HF, even if administered after the disease is established. These promising treatments of HF via BET bromodomain inhibition seem to be mediated by JQ1 blocking inflammatory and profibrotic gene programs like TGF-b signalling. However, the precise cellular and molecular dynamics of the reparative response after HF and BET inhibitor treatment remains an unresolved puzzle.
Researchers have long suspected that endogenous fibroblasts can convert to activated states, such as myofibroblast-like, a contractile and secretory cell phenotype that actively modulates tissue scarring. Hence, both the cellular plasticity and heterogeneity exhibited by fibroblasts are of particular interest given their requirements for wound healing and regeneration. However, the capacity of activated fibroblasts and myofibroblasts to revert to a naïve or basal fibroblast state after an injury is yet unclear. In this preprint, the authors combined single-cell RNA sequencing (scRNA-seq) with single-cell Assay for Transposase-Accessible Chromatin sequencing (scATAC-seq) in a clinically-relevant adult mouse model of HF to interrogate the reversibility of fibroblast-myofibroblast cell states using BET inhibition.
Key findings
Using a classical measure of cardiac function, the Ejection Fraction, the authors first showed that the beneficial effects of BET inhibition, with JQ1 and another small molecule inhibitor, CPI-456, were reversible in the context of two independent cardiac Heart Failure (HF) models, Myocardial Infarction (MI) and Transverse Aortic Constriction (TAC). The implications of a therapeutic reversal of heart failure at later stages are enormous, given that many patients often progress to pre-HF without recognised signs or symptoms. This reversibility effect led them to ponder whether cardiac cell-states were changing with BET inhibition. Typically, during injury-induced remodelling, cell-state changes are common and can be attributed to dynamic regulatory changes of a multitude of chromatin interactors and up- and down-stream effectors. In order to assess cell-states and sub-populations of the heart, the authors separated different cellular compartments through an elegant method of ex vivo Langendorff (rig-based) perfusion, followed by size and mass separation of tissue- and cell-compartments.
Owing to the improved functional outcome, they first evaluated bulk transcriptomic changes in isolated Cardiomyocytes (CMs), the functional units of the beating heart, which surprisingly showed only very minor changes, suggesting that the functional benefit of JQ1 was affecting the non-CM compartment. In this interstitial compartment, fibroblasts and endothelial cells make up the majority of cell-types, with myeloid, endo- and epi-cardial cells making up smaller subpopulations. Using scRNA-seq, the authors profiled these non-CM subpopulations isolated from 4 separate conditions: Sham control (state 1), TAC untreated (2), TAC with constant JQ1 treatment (3) and TAC with JQ1 treatment withdrawn (4), which represented a disease regression-type model. The effect of constant JQ1 was apparent in most non-CM cell-types, with these subpopulations showing distinct clustering from other conditions. However, the pattern of the clustering within fibroblasts revealed a truly dynamic pattern of cell-state shifts, which was specific only to fibroblasts. This dynamic pattern showed that BET inhibition in fibroblasts after injury (state 3) led to the reversion back to a more quiescent and basal state, seen in the control condition (state 1). On the other hand, the withdrawal of treatment resulted in the deterioration of fibroblasts back to a TAC-like stressed state (state 2 and 4), similar to an activated, pathogenic myofibroblast. This bi-directional plasticity of cell-state correlated highly with the reversibility of cardiac function with BET inhibition, which the authors suggest is indicative of a direct influence of fibroblast state on heart failure pathogenesis.
Finally, having identified the sub-population of cardiac cells that were in part responsible for this remarkable therapeutic reversibility, the authors then sought to identify the key switch regulating fibroblast plasticity during BET inhibition. To do this at the individual cell level, authors profiled accessible chromatin and enhancer activation marks through the integration of their scRNA-seq analysis with scATAC-seq, from the same hearts. In doing this, they were able to uncover several key features of BET-dependent cell fate-switching in HF. Firstly, the transcription factor, MEOX1, was critical to the control of fibroblast plasticity during HF-induced remodelling, by directing these cells towards a pathogenic myofibroblast state. Secondly, that specific enhancer accessibility in fibroblasts could be directly correlated with positive or negative functional outcomes. And lastly, when a handful of these key enhancer regions were silenced, fibroblasts were prevented from developing characteristics typical of myofibroblasts upon challenge. All in all, this preprint represents a leap forward in our understanding of both cell-fate plasticity during the remodelling process and identifies a critical mechanism by which BET inhibition may be positively influencing heart function after injury or stress.
“To be, or not to be a myofibroblast, that is the question”.
What we liked of this preprint
This paper deserves praise by its technical flair and elegant, detailed analyses, which makes a simple, but powerful message from a complex set of data. The authors push the limits of what can be achieved from just a handful of hearts and, in doing so, reveal fundamental concepts about regeneration and cell behaviour. At a technological level, this study exemplifies how single-cell approaches can be intricately used to profile disease states and pinpoint therapeutic mechanisms. In providing a specific mechanistic link between transcriptional regulatory proteins and cell-fate-switching in disease, they may have also opened up the possibility for more targeted therapeutic approaches in the future. The implications of reversal of cell fate from a stressed/diseased-state, back to a normal/basal state, are profound, as this has long been considered the “holy grail” for regenerative biologists (or at least a part of the grail!) and this type of study certainly represents a step in the right direction in the quest of achieving true heart regeneration in adult mammals.
Future directions and questions to the authors
- Do you measure other parameters indicative of heart function during JQ1 reversibility treatment rather than ejection fraction of the left ventricle?
- We are curious about the single-cell imaging experiments concerning MEOX1 expression in the fibroblast population. Is there any evidence about the protein expression of MEOX1 in myofibroblasts after heart failure? Do MEOX1+ cells localise around interstitial fibrotic- or perivascular fibrotic-regions, or both?
- Do you expect to have similar single-cell results using the BET inhibitor CPI-456 compared to JQ1, which seems more therapeutically promising due to its high potency and better pharmacokinetic properties than JQ1?
- The work is lacking lineage tracing strategies which are helpful to understand clonality and lineage determination of cells. From what population of endogenous fibroblasts are MEOX1 expressing myofibroblasts descending from?
- Do you expect the reversibility of the dynamic myofibroblast transcriptome under stress after JQ1 treatment to be mirrored by that of the proteome and metabolome within myofibroblasts?
- Does MEOX1 play a role as a chromatin modifier in response to injury-induced signalling (e.g. after TGF-b exposure) and do you have any direct evidence of target gene changes upon challenge?
References
Role of BET protein inhibition in heart failure:
- Anand, P., Brown, J. D., Lin, C. Y., Qi, J., Zhang, R., Artero, P. C., … Haldar, S. M. (2013). BET Bromodomains Mediate Transcriptional Pause Release in Heart Failure. Cell, 154(3), 569–582. https://doi.org/10.1016/j.cell.2013.07.013
- Spiltoir, J. I., Stratton, M. S., Cavasin, M. A., Demos-Davies, K., Reid, B. G., Qi, J., … McKinsey, T. A. (2013). BET acetyl-lysine binding proteins control pathological cardiac hypertrophy. Journal of Molecular and Cellular Cardiology, 63, 175–179. https://doi.org/https://doi.org/10.1016/j.yjmcc.2013.07.017
- Duan, Q., McMahon, S., Anand, P., Shah, H., Thomas, S., Salunga, H. T., … Haldar, S. M. (2017). BET bromodomain inhibition suppresses innate inflammatory and profibrotic transcriptional networks in heart failure. Science Translational Medicine, 9(390), eaah5084. https://doi.org/10.1126/scitranslmed.aah5084
- Stratton, M. S., Bagchi, R. A., Felisbino, M. B., Hirsch, R. A., Smith, H. E., Riching, S. A., … McKinsey, T. A. (2019). Dynamic Chromatin Targeting of BRD4 Stimulates Cardiac Fibroblast Activation. Circulation Research, 125(7), 662–677. https://doi.org/10.1161/CIRCRESAHA.119.315125
- Alexanian, M., Przytycki, P. F., Micheletti, R., Padmanabhan, A., Ye, L., Travers, J. G., … Srivastava, D. (2020). A Transcriptional Switch Governing Fibroblast Plasticity Underlies Reversibility of Chronic Heart Disease. BioRxiv, 2020.07.21.214874. https://doi.org/10.1101/2020.07.21.214874
- Wang, C. Y., & Filippakopoulos, P. (2015). Beating the odds: BETs in disease. Trends in biochemical sciences, 40(8), 468–479. https://doi.org/10.1016/j.tibs.2015.06.002
Cardiac fibroblast heterogeneity and plasticity under stress and disease:
- Farbehi, N., Patrick, R., Dorison, A., Xaymardan, M., Janbandhu, V., Wystub- Lis, K., Ho, J. W. K., Nordon, R. E. and Harvey, R. P. (2019). Single-cell expression profiling reveals dynamic flux of cardiac stromal, vascular and immune cells in health and injury. eLife 8, e43882. doi:10.7554/eLife.43882
- Soliman, H., Paylor, B., Scott, R. W., Lemos, D. R., Chang, C., Arostegui, M., Low, M., Lee, C., Fiore, D., Braghetta, P. et al. (2020). Pathogenic potential of Hic1-expressing cardiac stromal progenitors. Cell Stem Cell 26, 205-220.e8. doi:10.1016/j.stem.2019.12.008
- Fu, X., Khalil, H., Kanisicak, O., Boyer, J. G., Vagnozzi, R. J., Maliken, B. D., Sargent, M. A., Prasad, V., Valiente-Alandi, I., Blaxall, B. C. et al. (2018). Specialized fibroblast differentiated states underlie scar formation in the infarcted mouse heart. Clin. Invest. 128, 2127-2143. doi:10.1172/JCI98215
- Contreras, O., Cruz-Soca, M., Theret, M., Soliman, H., Tung, L. W., Groppa, E., Rossi, F. M. and Brandan, E. (2019). Cross-talk between TGF-β and PDGFRα signaling pathways regulates the fate of stromal fibro–adipogenic progenitors. J. Cell Sci. 132, 232157. doi:10.1242/jcs.232157
- Forte, E., Skelly, D. A., Chen, M., Daigle, S., Morelli, K. A., Hon, O., … Furtado, M. B. (2020). Dynamic Interstitial Cell Response during Myocardial Infarction Predicts Resilience to Rupture in Genetically Diverse Mice. Cell Reports, 30(9), 3149-3163.e6. https://doi.org/https://doi.org/10.1016/j.celrep.2020.02.008
- Kanisicak, O., Khalil, H., Ivey, M. J., Karch, J., Maliken, B. D., Correll, R. N., Brody, M. J., Lin, S.-C., Aronow, B. J., Tallquist, M. D. et al. (2016). Genetic lineage tracing defines myofibroblast origin and function in the injured heart. Nat. Commun. 7, 12260. doi:10.1038/ncomms12260
- McLellan, M. A., Skelly, D. A., Dona, M. S.I., Squiers, G. T., Farrugia, G. E., Gaynor, T. L., Cohen, C. D., Pandey, R., Diep, H., Vinh, A., Rosenthal, N. A., and Pinto, A. R. (2020). High-Resolution Transcriptomic Profiling of the Heart During Chronic Stress Reveals Cellular Drivers of Cardiac Fibrosis and Hypertrophy. Circulation, 0(0). https://doi.org/10.1161/CIRCULATIONAHA.119.045115
Posted on: 11 August 2020 , updated on: 12 August 2020
doi: https://doi.org/10.1242/prelights.23879
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Also in the physiology 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 |
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 |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
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 |
Also in the systems biology category:
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
Single Cell Biology 2020
A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
| List by | Alex Eve |
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. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
| List by | Dey Lab |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
| List by | Alexa Sadier |