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A Transcriptional Switch Governing Fibroblast Plasticity Underlies Reversibility of Chronic Heart Disease

Michael Alexanian, Pawel F. Przytycki, Rudi Micheletti, Arun Padmanabhan, Lin Ye, Joshua G. Travers, Barbara Gonzalez Teran, Qiming Duan, Sanjeev S. Ranade, Franco Felix, Ricardo Linares-Saldana, Yu Huang, Gaia Andreoletti, Jin Yang, Kathryn N. Ivey, Rajan Jain, Timothy A. McKinsey, Michael G. Rosenfeld, Casey Gifford, Katherine S. Pollard, Saptarsi M. Haldar, Deepak Srivastava

Posted on: 11 August 2020 , updated on: 12 August 2020

Preprint posted on 22 July 2020

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”.

Graphical abstract. A fibroblast-myofibroblast epigenetic cell-state switch regulates heart failure. Credits: Osvaldo Contreras and Alex Ward.

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

  1. Do you measure other parameters indicative of heart function during JQ1 reversibility treatment rather than ejection fraction of the left ventricle?
  2. 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?
  3. 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?
  4. 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?
  5. 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?
  6. 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:

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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:

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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

Tags: bet proteins, cardiovascular disease, epigenetics, fibroblasts, heart, myofibroblasts, regeneration, transcriptomics

doi: https://doi.org/10.1242/prelights.23879

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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

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

Lung Disease and Regeneration

This preprint list compiles highlights from the field of lung biology.

 



List by Rob Hynds

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

BSCB/BSDB Annual Meeting 2019

Preprints presented at the BSCB/BSDB Annual Meeting 2019

 



List by Dey Lab

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

Biophysical Society Annual Meeting 2019

Few of the preprints that were discussed in the recent BPS annual meeting at Baltimore, USA

 



List by Joseph Jose Thottacherry

ASCB/EMBO Annual Meeting 2018

This list relates to preprints that were discussed at the recent ASCB conference.

 



List by Dey Lab, Amanda Haage

Also in the developmental biology category:

BSDB/GenSoc Spring Meeting 2024

A list of preprints highlighted at the British Society for Developmental Biology and Genetics Society joint Spring meeting 2024 at Warwick, UK.

 



List by Joyce Yu, Katherine Brown

GfE/ DSDB meeting 2024

This preList highlights the preprints discussed at the 2024 joint German and Dutch developmental biology societies meeting that took place in March 2024 in Osnabrück, Germany.

 



List by Joyce Yu

‘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

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

The Society for Developmental Biology 82nd Annual Meeting

This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.

 



List by Joyce Yu, 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

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

Alumni picks – preLights 5th Birthday

This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.

 



List by Sergio Menchero et al.

CellBio 2022 – An ASCB/EMBO Meeting

This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.

 



List by Nadja Hümpfer et al.

2nd Conference of the Visegrád Group Society for Developmental Biology

Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)

 



List by Nándor Lipták

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

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

EMBL Conference: From functional genomics to systems biology

Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020

 



List by Jesus Victorino

Single Cell Biology 2020

A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.

 



List by Alex Eve

Society for Developmental Biology 79th Annual Meeting

Preprints at SDB 2020

 



List by Irepan Salvador-Martinez, Martin Estermann

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

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

Cell Polarity

Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.

 



List by Yamini Ravichandran

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

3D Gastruloids

A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.

 



List by Paul Gerald L. Sanchez and Stefano Vianello

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.

EDBC Alicante 2019

Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.

 



List by Sergio Menchero 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

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

Lung Disease and Regeneration

This preprint list compiles highlights from the field of lung biology.

 



List by Rob Hynds

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

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

BSCB/BSDB Annual Meeting 2019

Preprints presented at the BSCB/BSDB Annual Meeting 2019

 



List by Dey Lab

Zebrafish immunology

A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.

 



List by Shikha Nayar

Also in the genomics category:

BSCB-Biochemical Society 2024 Cell Migration meeting

This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.

 



List by Reinier Prosee

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

Semmelweis Symposium 2022: 40th anniversary of international medical education at Semmelweis University

This preList contains preprints discussed during the 'Semmelweis Symposium 2022' (7-9 November), organised around the 40th anniversary of international medical education at Semmelweis University covering a wide range of topics.

 



List by Nándor Lipták

20th “Genetics Workshops in Hungary”, Szeged (25th, September)

In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf

 



List by Nándor Lipták

EMBL Conference: From functional genomics to systems biology

Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020

 



List by Jesus Victorino

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

Also in the immunology category:

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

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

Single Cell Biology 2020

A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 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

Antimicrobials: Discovery, clinical use, and development of resistance

Preprints that describe the discovery of new antimicrobials and any improvements made regarding their clinical use. Includes preprints that detail the factors affecting antimicrobial selection and the development of antimicrobial resistance.

 



List by Zhang-He Goh

Zebrafish immunology

A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.

 



List by Shikha Nayar
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