Controlling stem cell divisions in time and space

Lead Research Organisation: University of Oxford
Department Name: Biochemistry

Abstract

Animals and plants are multicellular (metazoan), and are made up of cells descended from a single original cell, the fertilized egg. Complex organisms such as humans are composed of trillions of cells, whereas simple organisms may consist of just a few hundred cells. During development from egg to adult, cells of all metazoan organisms therefore need to divide, or proliferate, in order to increase in number. However, it is equally as important that cells stop proliferating at the appropriate time and differentiate (take on specialised roles appropriate to their individual circumstances of position, ancestory and timing). Proliferation and differentiation therefore need to be in perfect balance to ensure that tissues and organs develop with the correct size and functionality. Stem cells have particularly important properties. They have the ability to self-renew (make more of themselves) as well as give rise to daughters that differentiate. They do this by dividing asymmetrically: one daughter cell retains the stem cell fate of further proliferation, whereas the other daughter stops dividing in order to differentiate. Stem cells can also sometimes divide symmetrically, with both daughters retaining the ability to proliferate further, helping to expand the number of progenitor cells for particular purposes. Stem cells sometimes retain the ability to proliferate throughout the lifetime of the organism in order to generate (and sometimes re-generate) particular tissues and organs. For example, hematopoietic stem cells generate blood cells throughout the lifetime of many organisms, and epidermal stem cells constantly generate new skin cells. Stem cell divisions must therefore be very tightly controlled, so that the conflicting demands of proliferation vs. differentiation are correctly balanced. Understanding how stem cell divisions are controlled is crucial to 21st century biological research because it may be possible to harness these cells in order to produce any required cell type on demand, for example new spinal cord neurons for patients with spinal injury. It is also thought that stem cells are at the heart of carcinogenesis. However, we have much to understand about the basic biology of stem cells before potential therapies can become routine. All properties of cells are ultimately under genetic control, which dictates that the appropriate RNA and protein molecules are produced at the correct time and place. Human development is an incredibly complicated process, involving trillions of cells and many thousands of genes, therefore before we can begin to understand human development and human stem cells, we need to investigate a simpler system. This is where the tiny worm Caenorhabditis elegans comes in. Many of the genes that are important for C. elegans development are remarkably similar to human genes, therefore studying C. elegans development will ultimately shed light on the biology of higher animals including humans. C. elegans have cells called seam cells. These are stem cells, in that they divide throughout development to give rise to more stem cells, as well as daughters that differentiate by becoming skin cells and neurons. Our aim is to understand which genes are important for controlling the correct pattern of seam cell divisions. Previously, we have isolated two genes, rnt-1 and bro-1, as being important for this process. Strikingly, the human counterparts of both these genes, Runx and CBFb, are also involved in stem cell development, including haematopoietic and epidermal stem cells. This means we are studying a conserved process, and lessons gained from studying the problem in C. elegans are very likely to be applicable to higher organisms including humans. In this proposal, we are seeking to understand more about how rnt-1 and bro-1 control seam cell divisions, and also to isolate new genes involved in this process.

Technical Summary

This application proposes to use C. elegans as model system for studying the control of stem cell division patterns. During development, cells must stop proliferating and differentiate at the appropriate time. This decision is particularly pertinent in stem cells, which both self-renew and give rise to differentiated cells that can generate particular cell types over the lifetime of an organism. In C. elegans, the seam cells offer a paradigm for the stem cell mode of division. They are multipotent neuroectodermal cells that divide symmetrically to expand the pool of progenitor cells, and asymmetrically to contribute various differentiated cell types (as well as more stem cells). Our previous work has sought to analyse mutants with defects in seam cell proliferation and differentiation. We have identified rnt-1, a homologue of the Runx family of transcription factors, and bro-1, a CBFb (Runx DNA binding partner) homologue, as being key players in the decision between proliferation and differentiation. Loss of function of bro-1 or rnt-1 results in a failure of seam cell proliferation whereas over-expression results in too much proliferation, at the expense of differentiation. The experiments described in this proposal build on a substantial body of pilot data aimed at identifying the molecular mechanisms responsible for the correct dynamic regulation of rnt-1 and bro-1 during development. Methods proposed include mutant/RNAi analysis of gene function, lineage analysis, use of transgenic gene expression reporter strains/ immunofluorescence, and site directed mutagenesis of regulatory regions. We also aim to use targeted RNAi screens to identify novel pathways operating in parallel to rnt-1/bro-1 to regulate stem cell division patterns. Given that Runx/CBFb genes are also heavily involved in regulating stem cell lineages in mammalian systems, for example in haematopoietic stem cells, we expect knowledge gained from C. elegans to be generally applicable.
 
Description 1) miRNA control of the timing of rnt-1 expression and interaction with other heterochronic genes

Using a series of transgenic sensor strains, we have found direct evidence of mir-48/84/241 mediated down-regulation of rnt-1 at particular developmental stages. This control prevents premature cell cycle re-entry, and acts in parallel to the alternative let-7 miRNA family target hbl-1, with rnt-1 working in the seam cells and hbl-1 working in the surrounding hypodermis.

2) Investigation of rnt-1/bro-1 cis-regulatory architecture

Using a 1-hybrid screen we identified the GATA factor ELT-1 as being a direct upstream regulator of bro-1.  Further analysis revealed that bro-1 has dual roles in regulating seam cell divisions, both promoting proliferation by directly activating bro-1, and preventing inappropriate differentiation by regulating the fusogen eff-1. 

3) ) RNAi screen for rnt-1/bro-1 synthetic lethals

Several interesting synthetic lethal genes were isolated in our screen, including the Meis homologue unc-62 and the caudal/cdx homologue pal-1.
Exploitation Route peer-reviewed academic publication, further funding, dissemination to the wider scientific (and non-scientific) sector
Sectors Healthcare,Pharmaceuticals and Medical Biotechnology

 
Description BBSRC DTP studentship
Amount £75,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 10/2012 
End 09/2015
 
Description EPA Cephalosporin Fund
Amount £64,000 (GBP)
Organisation University of Oxford 
Department E P A Cephalosporin Fund
Sector Charity/Non Profit
Country United Kingdom
Start 05/2013 
End 04/2014
 
Description WT studentship
Amount £100,000 (GBP)
Organisation Wellcome Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 10/2012 
End 09/2015
 
Description WT studentship
Amount £100,000 (GBP)
Organisation Wellcome Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 10/2015 
End 09/2018
 
Description Collaboration with Research group at Imperial College 
Organisation Imperial College London
Country United Kingdom 
Sector Academic/University 
PI Contribution contribution of expertise and preliminary data to successful grant application by partner (new investigator grant)
Collaborator Contribution future data discussion and sharing
Impact successful funding application for collaborator Manuscript in submission
Start Year 2012
 
Description Collaboration with research group at UCL 
Organisation University College London
Department Biosciences
Country United Kingdom 
Sector Academic/University 
PI Contribution expertise and collaboration
Collaborator Contribution access to automated lineage determining facility
Impact manuscript in preparation
Start Year 2015
 
Description "Genetics as revolution" talk to student society in Dublin 
Form Of Engagement Activity A talk or presentation
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Geographic Reach Local
Primary Audience Postgraduate students
Results and Impact "Genetics as revolution" talk for student Genetics Society at Trinity College, Dublin
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URL http://www.bbc.co.uk/nature/25430552
 
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URL http://www.express.co.uk/life-style/health/450310/Could-Jellyfish-be-the-key-to-a-longer-life
 
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URL http://www.theguardian.com/commentisfree/2013/aug/05/in-praise-of-alison-woollard
 
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unknown
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high levels of interest
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URL http://rigb.org/blog/2014/april/lobster
 
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A couple of students have applied to do internships in my lab
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Description Life Scientific Radio 4 interview 
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Very positive feedback and increased interest in genetics
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Description Participation in Science comedy event for Ada Lovelace day 
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I've been asked to do other similar activities
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URL http://www.scienceoxford.com/live/whats-on-events/ada-lovelace-night
 
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Description Podcast for Ashmolean Museum 
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Some school children in the audience contacted me for further information about studying genetics
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positive feedback and further interest
Year(s) Of Engagement Activity 2014
 
Description Radio Show Singapore 
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Results and Impact show sparked media interest

unknown
Year(s) Of Engagement Activity 2014
URL https://www.youtube.com/watch?v=DH_7VMawXAc
 
Description Radio show 
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URL http://www.bbc.co.uk/programmes/b03kpnjn
 
Description Reddit AMA 
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Geographic Reach International
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Results and Impact Many questions

unknown
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URL http://www.reddit.com/r/science/comments/204qe3/science_ama_series_prof_alison_woollard/
 
Description Reflections on Life Fantastic blog 
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URL http://thenode.biologists.com/of-worms-and-women-reflections-on-the-life-fantastic-christmas-lecture...
 
Description Research Seminar Cambridge 
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Description Royal Institution Christmas Lectures 2013 
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Results and Impact These lectures were broadcast to a global TV audience, viewing figures in the UK around 4 million

This activity is likely to lead to (and has already led to) many more engagement activities. Many positive feedback letters (more than 50)
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URL http://www.rigb.org/christmas-lectures
 
Description Royal Institution advent calendar film series 
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URL http://www.rigb.org/advent/01
 
Description STAR Lecture, Singapore 
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Geographic Reach National
Primary Audience Schools
Results and Impact Talk sparked questions, discussion and media interest

unkown
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URL https://www.facebook.com/video.php?v=10152708550318482
 
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Results and Impact well attended talk which sparked questions and debate
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Description School visit (Kingston upon Thames) 
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Results and Impact Talk at school, included section on careers in life sciences
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Description School visit (Oxford) 
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Results and Impact visit to local primary school to engage
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Description School visit (Winchester) 
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Primary Audience Schools
Results and Impact Talk sparked questions and discussion

Increased interest in studying biology A Level
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Description Science comedy SciBar 
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Results and Impact Oxford SciBar science comedy evening. Talk made into podcast for greater reach. Sparked questions and enthusiasm
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Description Science show at FameLab 
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Results and Impact Comedy show (interval entertainment) about research at Oxfordshire regional FameLab finals
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Description Seminar Oxford 
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Geographic Reach Local
Primary Audience Postgraduate students
Results and Impact Research seminar University of Oxford
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Description Seminar Warwick 
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Geographic Reach Local
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Results and Impact Research seminar University of Warwick
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Description Sheffield University Graduate Students Symposium 
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Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Talk sparked discussion about careers in science and science communication

Further interest from audience in science communication
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Description Sun article on natural superheroes 
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URL http://beta.thesun.co.uk/sol/homepage/features/5351216/Real-life-superpowers.html
 
Description Talk about Public Engagement activities (Oxford) 
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Results and Impact Talk sparked questions and discussion afterwards

After my talk several members of the audience are planning public engagement activities of their own
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Description Talk at Applied Biology meeting 
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Results and Impact Talk describing uses of C. elegans in food security research and toxicity testing
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Description Talk at Cheltenham Science Festival 
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Description Talk at Crick Institute, part of Graduate Student symposium 
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Description Talk at Genetics Society Summer studentship symposium 
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Description Talk at Green Man Festival 
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Description Talk at Matthew Arnold school 
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Results and Impact Talk on Developmental and ageing biology, and also on being a scientist, Matthew Arnold school
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Description Talk at UCL student retreat 
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Results and Impact Talk on research and careers at Cumberland Lodge UCL Biology undergraduate retreat
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Description Talk on public engagement at Genetics Society science communication course 
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Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Talk on effective public engagement at the Genetics Society "Communicating your science" workshop
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Description Telegraph article on de-extinction 
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Year(s) Of Engagement Activity 2013
URL http://www.telegraph.co.uk/science/dinosaurs/10533240/A-real-life-Jurassic-Park-Birds-could-be-theor...
 
Description Telegraph interview on ageing research 
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Results and Impact article sparked comments and questions

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Description Women in Science symposium UCL 
Form Of Engagement Activity A talk or presentation
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Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Talk sparked questions and discussion

Unknown
Year(s) Of Engagement Activity 2014
 
Description participation in British Society for Gene and Cell Therapy public outreach day 
Form Of Engagement Activity A talk or presentation
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Geographic Reach Regional
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Impacts unknown
Year(s) Of Engagement Activity 2014
 
Description radio show Australia 
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Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Show sparked interest in my research

unknown
Year(s) Of Engagement Activity 2013
URL http://www.abc.net.au/radionational/programs/scienceshow/christmas-lectures-13007jpg/5120890
 
Description research seminar CRUK London 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach Local
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Talk sparked questions and discussion

possible future collaboration
Year(s) Of Engagement Activity 2014
 
Description research seminar Nijmegen 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact Research seminar Nijmegen, Netherlands. Talk sparked interest and enthusiasm
Year(s) Of Engagement Activity 2016