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Educational Resources for 26 Yuk Jing Loke and Jeffrey M. Craig

Abstract Easy-to-read articles and Epigenetics can appear as an impenetrable sub- web sites aimed at a broad ject; not just to those encountering it for the first audience time, but to those within the field too. However, epigenetics, like any subject can be made easier ‘Epigenetics’ by Brona McVittie to understand using a combination of clear lan- (McVittie, 2006; http://www. guage, creative illustrations and even animations scienceinschool.org/2006/issue2/ and film clips. This chapter aims to point readers epigenetics) of all experiences towards helpful and easy-to- This is an excellent two-page article about epige- read resources that educate about epigenetics. netics by a member of the Network It is split into two main sections, the first aimed Of Excellence (see below). It is aimed at an audi- at a lay audience including teachers and high ence from school student to lay person and begins school students and the second, at graduate and by likening the DNA code as a musical score postgraduate students and beyond. Each section being played by an orchestra of cells conducted contains summaries of published articles and web and played by epigenetic factors. It introduces sites. The chapter ends with a short section on and DNA in simple epigenetic societies and research networks and a terms and focuses on how the environment can summary table of resources. It is intended to pro- influence epigenetics as exemplified by studies vide a sample of some of the best short to medium in plants and animals, and by recent findings that length reviews on general topics within the field genetically identical can have different epi- of epigenetics and while we cover a wide variety genetic marks, especially as they age. The article of themes, we apologise for any areas not covered. also introduces the idea of epigenetic We cite the URLs of freely available articles wher- causing a ‘hazardous cacophony’ in and ever possible, but many articles will require library the possibility of epigenetic . access. We also urge readers to contact authors or publishers if they wish to distribute any of the ‘, Epigenetics, and Maternal articles for teaching purposes. ’ by Asim K. Duttaroy (Dut- taroy, 2006; http://www.mukto-mona. com/Special_Event_/Darwin_day/ evolution_asim120206.htm) This is a simple yet comprehensive review of evolution, epigenetics and the influence of nutri- tion on epigenetics. The review starts with an

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introduction of Darwin’s theory of evolution, fol- Molecular – Epigenetics lowed by a link to the influence of epigenetics in by Mark Hill (http://embryology.med. evolution. The author provides a good explanation unsw.edu.au/MolDev/epigenetic.htm) of epigenetics, covering the most widely studied This excellent web site is maintained by Dr Mark mechanism, DNA methylation. Duttaroy then Hill from the University of New South Wales, Aus- concentrates on how epigenetics influences tralia, containing many resources centred round expression and to illustrate this brings in the topic epigenetics and mammalian development. It gives of imprinted , which are expressed depend- a broad coverage of quite a number of aspects of ing whether they are inherited from the mother epigenetics, ranging from a brief introduction or father. The author provides many interesting to its mechanisms, to more specific aspects of examples of epigenetic phenomena, alongside epigenetics such as twins’ epigenetics and the rela- clear illustrations. Find out how there is a ‘battle tionship between epigenetics and expression of of the sexes’ within the genes under the control of imprinted genes. Aside from epigenetics, the web epigenetics. The author also gives a good account site also gives a good coverage of developmental on the link between maternal nutrition and epige- insights by providing basic introductions to differ- netics, and how maternal nutrition can influence ent developmental stages of humans. The web site the epigenetics of their offspring. References are also has a section on how environmental factors included and it is a good read for those who want can cause abnormalities in offspring. An introduc- to know more than just the basics of epigenetics. tion to statistics can also be found in this web site, which is very user friendly as it has links that ‘Epigenetics: , meet your envi- easily lead the reader to the required information. ronment’ by Leslie Pray (Pray, 2004; It also contains fun illustrations for easy , http://www.the-scientist.com/article/ and most importantly, the author structures the home/14798/) web site in a way where there is a compilation of This is an excellent summary of how the envi- updated resources and references for each section. ronment can affect epigenetics. It provides a good historical background on how the study NOVA scienceNOW: Epigenetics epigenetic s came about and even compares cur- (http://www.pbs.org/wgbh/nova/ rent epigenetic theories to that of Jean-Baptise teachers/activities/3411_02_nsn. Lamarck 200 years ago. Pray presents a compre- html) hensive comparison of current theories from This is a classroom activity and teachers’ guide renowned epigeneticists some of which may to epigenetics based on the Nova Epigenetics support Lamarck’s theory of the inheritance of documentary originally aired in 2007. It expands acquired traits. The article covers a wide range the readers’ knowledge from to epige- of early experimental evidence to introduce how netics, by offering epigenetics-related resources, environment can be a major factor contribut- including some useful definitions of key terms, a ing to the establishment of epigenetic patterns streamed version of the show, an audio slide show in an organism and its offspring. It gives a brief about how the epigenome produces epigenetic introduction and explanation of the mechanisms differences in identical mice, and an ‘Ask the of epigenetics, focusing on DNA methylation, Expert’ area where site visitors can ask researcher modification, and imprinting. The author Randy Jirtle questions about epigenetics. The also discusses how epigenetics is an important part practical illustrations and activities suggested in of studies and concludes with an emphasis this web site promote active and fun learning for that epigenetics works hand in hand with genetics. students to understand the concept of epigenet- This article is a broad overview on the subject of ics. The questions in the activity challenge them environment and epigenetics and provides a good to think about how epigenetics works, and how platform for anyone who wishes to read further it differs from genetics. Printable worksheets and into this area. activities are also available for student handouts.

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Epigenetics? (http://epigenome.eu/) What is it? A simplified descrip- This is a multilingual public science web site tion of DNA methylation (http:// set up by the European Epigenome Network of es.landesbioscience.com/pub/faq/) Excellence (see below). Features short, easy-to- This is an excellent review about DNA meth- read articles on epigenetics aimed at laypeople ylation from the Epigenetics Society (see below). and school/university students. The titles and The unnamed author starts by giving a brief intro- the contents of the articles are structured in a duction of genetics and epigenetics with the use narrative form, which allow readers to better of simple terms. They describe how the regulation understand the different aspects and influences of DNA methylation completes the picture of the of epigenetics in daily living. With just a click on development and of an organism. The the user-friendly hyperlinks, the site expands the author also succeeds in inserting an example in reader’s on epigenetics and covers a wide almost every paragraph, providing a good plat- range of relevant and recent epigenetic topics, form for the reader to understand the hows, whys ranging from stem cells to epigenetics in the and whats of DNA methylation. In addition, the human immunodeficiency virus (HIV). Find out article introduces the enzymes that are involved how epigenetics can also be a way to overcome in the establishment and maintenance of DNA drug too! The reader gets to find out methylation discusses how the malfunction of about different aspects on epigenetics with the these enzymes can be detrimental to the organism. help of simple illustrations. The web site also con- It is stated that as one ages, the chance of having tains fun animations for school students, allowing abnormality in DNA methylation increases too. them to appreciate the essence of Darwin’s theory The article ends with the discussion of the conse- of evolution. This online-magazine-look-alike web quences of abnormal DNA methylation, but also site is highly recommended to read for people of concludes nicely by highlighting how the scientific all ages and disciplines. is focused on research into this area.

Epigenetics and Imprinted Genes Learn.Genetics’epigenetics page (http://www.hopkinsmedicine.org/ (http://learn.genetics.utah.edu/ press/2002/November/epigenetics. content/epigenetics/) htm) An excellent interactive web site from the Uni- This is a short and understandable article that versity of Utah, that contains lots of visual aids to concentrates on , originat- assist readers new to epigenetics in grasping the ing from the Johns Hopkins Medical Institute, basic concepts. The site covers topics including Baltimore, MD, USA. Readers are able to quickly the effect of nutrition on the epigenome, differ- grasp the simple concepts linking epigenetics and ences between the of identical twins, imprinted genes. The unnamed author presents and epigenetic mechanisms. All information is the article in a ‘Frequently Asked Question’ format illustrated in a simple manner, accompanied by which contains basic questions with compre- video clips and interactive games to allow a better hensive answers. The author covers the topic by understanding of the topic. The site also cites defining epigenetics, linking how imprinted genes numerous examples of animal and human studies come into the picture of epigenetic modification, as a good source of evidence for each concept. and the consequences of these modifications. The Find out interesting facts like why queen bees explanations are fairly simple and it is suitable for are different from other female bees, or how our readers who have very little background in this grandparents’ diet could affect our own health. area. This it is a good site for educators to obtain ideas and resources for their teaching of epigenetics as it contains lesson plans and suggestions to creatively teach this topic.

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Epigenetics news – iscoveries and Institute, a small, independent not-for- advances (http://www.epigenetics- profit research and education organization, covers news.com/tag/epigenetics/) everything from to . A blog maintained by Trevor Covert, a Research Associate in the laboratory of Dr Michael Skin- ner at Washington State University in Pullman, Scholarly review articles aimed WA, USA. The blog focuses solely on reviewing at a broad scientific audience epigenetics-related articles from various sources of scientific and popular press. It contains com- ‘Controlling the double helix’ by Gary pilations of different opinions and views on the Felsenfeld and Mark Groudine (Felsen- latest advances of epigenetics from researchers all feld and Groudine, 2003) over the world, ranging from discussions of how This article fromNature is from before era of epigenetics is linked to cancer, to the influences of and non-coding but is never- environment on epigenetics. Apart from human theless an excellent comprehensive and relatively studies, the author also covers discussions on plant brief overview of epigenetics. Felsenfeld and and stem epigenetics studies. All opinions and Groudine focus on the constituents of chromatin information are cited together with a link to the including chromatin remodellers and histone original article. There are also tags and links to variants. The authors also discuss specialized other blogs that allow readers to obtain opinions chromatin structures such as , telom- and information from other relevant epigenetics eres and the inactive mammalian X , researchers. and the mechanisms of propagation of epigenetic marks along chromatin and across . Epigenie (http://epigenie.com/index. The article also contains excellent, simple figures html) summarizing chromosome structure and histone EpiGenie is not only an excellent on modifications. everything epigenetics but will also keep you in touch with updated epigenetics news and ‘Reading signals on the with events if you subscribe to their newsletter. Also a new nomenclature for modified his- available on this web site are sections separated tones’ by Brian Turner (Turner, 2005) into ‘product and method reviews’, ‘interviews Short review from Nature Structural on with leading researchers in the field’, ‘upcoming histone modifications from a leading figure in the conferences’, and ‘epigenetics background’. In the field. In this article, Turner proposes a nomen- ‘epigenetics background’ section, brief summaries clature for histone modifications that is now and reviews of epigenetics can be obtained to universally used in the field. In this nomenclature, assist readers who are new to the field, and each the histone comes first, then the modified amino summary is linked to another page with more acid residue, then the epigenetic mark, noting that comprehensive information if the readers wish to some amino acids can have more than one copy know more about the topic. Databases and online of that mark. For example, describes tools relevant to epigenetics work are available modified at 4 with 3 methyl in this section too. The links created in this site groups. The article also includes references to the makes it very user-friendly as they categorize each original hypothesis which posited section to ‘DNA methylation’, ‘chromatin’, and that combinations of histone modifications dic- ‘non-coding RNA’, allowing the reader to access tate chromosomal activity. relevant updated information promptly. ‘Perceptions of epigenetics’ by Adrian A (mostly) nontechnical glossary of epi- Bird (Bird, 2007) genetics (http://www.natureinstitute. , who has been a leading figure in the org/txt/st/mqual/glossary.htm) field of epigenetics for over 20 years, discusses how This excellent, simply written glossary from the the definitions of epigenetics have been stretched

UNCORRECTED FIRST PROOFS Educational Resources for epigenetics | 441 to encompass phenomena such as short-lived Association for Cancer Research changes to chromatin structure. In this ‘Insight’ Task Force and the article in Nature, he suggests a widening of defini- European Union Network of Excellence tion of epigenetics to ‘the structural of Scientific Advisory Board (Jones PA, chromosomal regions so as to register, signal or 2008) perpetuate altered activity states’. This definition These two short feature articles from the journal is meant to unite disparate views of epigenetic Nature from 2006 and 2008 focus on the Human phenomena (e.g. Ptashne, 2007) and reconcile Epigenome Project (HEP) and the more formal- the contrasting findings that histone modification ized Alliance for the Human Epigenome and can have a rapid turnover whereas DNA meth- Disease (AHEAD). The Qiu article provides ylation can be stable over many cell cycles. This the better introduction to the subject of epige- definition also views epigenetic changes as being netics and cites striking examples of epigenetic responsive and not proactive; they are responsible effects such as epigenetically different ‘identical’ for registering a change imposed by other events. twins and the role of epigenetics in program- Bird reviews some of the more controversial find- ming future health. The AHEAD article goes ings in the field and concludes that more work is into more detail about the aims and scope of the needed to resolve some disparate findings. For HEP, which will provide reference epigenomes example, while one study concluded that twins from healthy cells with which to compare with drift apart epigenetically over time (Fraga et al., those from cells from cancer and other diseases. 2005), another non-twins study, found strong There is tremendous potential to use the data evidence for stability of epigenetic marks over generated to develop diagnostic and prognostic time (Eckhardt et al., 2006). Bird also summarizes tests for specific diseases in addition to pointing epigenetics as ‘encompass[ing] some of the most towards targeted epigenetic therapies. The HEP exciting contemporary biology and is portrayed will involve a scale of magnitude larger than the by the popular press as a revolutionary new genome project because of two major factors. science – an antidote to the idea that we are hard- Firstly, as different cell types have different sets wired by our genes.’ of epigenetic marks, there will be multiple epi- to decode. Secondly, as diseases such ‘Epigenetics: The Science Of Change’ as cancer can develop from poorly differentiated by Bob Weinhold (Weinhold, 2006; cells, epigenomes will need to be studied longitu- http://www.ehponline.org/mem- dinally in cell lineages as they develop from stem bers/2006/114–3/ehp0114-a00160. cells. The HEP aims to characterize epigenetic pdf) marks such as DNA methylation and multiple Excellent open-access article on epigenetics by covalent histone modifications in each of these Bob Weinhold that briefly covers topics such as dimensions. The AHEAD article presents an epigenetic mechanisms, involvement in disease, overview of US, European, Asian and Australian epigenetic therapies, environmental effects, strategies to advance the HEP and stresses the the human epigenome project and epigenetic need for an interdisciplinary approach, including organizations. It is accompanied in the same the importance of bioinformatic data processing. issue by an open access guest editorial entitled This article also summarizes some of the methods ‘Epigenetics: environmental instructions for the used to define epigenomes and adds another genome’ by Paul Wade and Trevor Archer (Wade dimension to the picture with the sequencing of and Archer, 2006; http://www.ehponline.org/ the epigenomes of ‘model’ organisms such Dros- docs/2006/114–3/EHP114pa140PDF.PDF). ophila and Arabidopsis. The AHEAD article also summarizes the recommended histone markers ‘Epigenetics: unfinished symphony’ to study for transcriptional activity, silencing elon- by Jane Qiu (Qiu, 2006) and ‘Moving gation, chromosomal organization and stress/ AHEAD with an international human damage response. Finally, both articles include epigenome project’ by the American the same simple figure summarizing epigenetic

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modifications, with the addition of non-coding of environmental exposure in one generation RNAs in the later article. leading to epigenetic changes inherited by the next. Relton and colleagues present short but ‘Epigenetics: a landscape takes shape’ informative summaries of the major classes of by Aaron Goldberg, David Allis and environmental factors shown to affect epigenetic Emily Bernstein (Goldberg et al., 2007) marks for example nutrition, stress, smoking and An excellent article from Cell that reviews the in addition to summarizing the influ- mechanisms of epigenetics and how they interact. ence of age and genetic factors on the epigenome. The authors introduce Conrad Waddington’s ‘epi- They discuss controversial findings of epigenetic genetic landscape’ in which a ball (representative consequences of in vitro fertilization and the of a cell) is shown to navigate a landscape hills involvement of epigenetic in cancer and diseases and valleys representing preferred developmen- such as spectrum disorders. The authors tal channels overlaid with potential changes in make the important distinction between cause developmental trajectory. The authors also adapt and consequence of disease, which can be solved and update this ‘landscape’ to a pinball machine in only by conducting longitudinal studies. Impor- which a pinball (cell) is buffeted around an epige- tantly, they conclude that as DNA methylation netic landscape by changes to different classes of can be seen as a phenotype, then smaller sample epigenetic modifications. sizes are required in genome-wide searches for disease-associated epigenetic change, compared ‘Epigenetics in human disease and with genome-wide association studies (GWAS). prospects for epigenetic ’ by Finally, this article contains a useful flow chart for Gerda Egger and colleagues (Egger et such studies and a summary of methods used to al., 2004) study the epigenetic mark of DNA methylation. This excellent ‘Insight’ review article from Nature from Jones and colleagues summarizes what is Henderson and Steven Jacobsen (Hen- known about the role of epigenetics in human derson and Jacobsen, 2007) disease and details the different ways in which In this ‘Insight’ article from Nature, Henderson and drugs that can reverse disease-associated epige- Jacobsen present a compact and comprehensive netic marks could reverse those marks and restore review of epigenetic phenomena in plants, focus- health. The authors discuss the different classes of ing on the model organisms Arabidopsis thaliana epigenetic drugs including nucleoside analogue and . The authors also focus on non-coding inhibitors of DNA methylation and histone dea- RNAs and their role in phenomena such as RNA- cetylase inhibitors (HDACi) and describe how directed DNA methylation, in which genomic they could be used in combination. Jones and sequences sharing homology with viral RNAs are colleagues also discuss the potential pitfalls of methylated. They also discuss how the RNA inter- epigenetic therapies, such as off-target affects. ference (RNAi) machinery can guide plant DNA (DNMTs) to specific regions Epigenetics and child health: basic of the genome, shedding light on an important principles by Alix Groom and colleagues part of the epigenetic puzzle. Plants share most of (Groom et al., 2010) their epigenetic mechanisms with animals, exam- This is an excellent medium-length article focus- ples being silencing-associated gene ing on studies of the roles of epigenetic events in methylation and genomic imprinting, which in early mammalian development and how epige- plants is needed for proper seed development. netic marks can be altered by the environment However, this article also discusses some of the and in turn ‘programme’ future health. It touches differences. The first example given in paramuta- on the ideas that mammalian genomes may be tion (see also the chapters in this book by Arteaga more susceptible to environment-induced change and McGinnis), first described in maize, in which in early and the ‘neo-Lamarckian’ concept allelic interactions cause a meiotically heritable

UNCORRECTED FIRST PROOFS Educational Resources for epigenetics | 443 change in the expression of one of the . allergies, which may go some way to explaining Henderson and Jacobsen also discuss Polycomb the ‘hygiene hypothesis’ of increased incidence of group (Pc-G) , which, while present in such diseases. plants and animals, exhibit a greater variation in subunits in plants. Pc-G proteins also play a role in ‘The seductive allure of behavioural epi- the plant-specific phenomenon of vernalization, genetics’ by Greg Miller (Miller, 2010) in which exposure to long periods of low tempera- This ‘News Focus’ article from Science focuses first ture in winter facilitates flowering in the spring. on the work of Canadians Michael Meaney and The authors finish by stressing that studying epi- Moshe Szyf, who have shown that the way that genetic mechanisms in plants has led to the wider rat mothers interact with their new-born offspring understanding of epigenetic phenomena in other can programme their future behaviour though organisms, particularly through high-throughput epigenetic modifications of genes within pathways sequencing approaches to epigenomics. such as those involved in stress response (also reviewed in Szyf et al., 2008). Studies from other ‘Tools and landscapes of epigenetics’ by groups have implicated epigenetic mechanisms in Alexander Tarakhovsky (Tarakhovsky, response to stress in adult mice and in influenc- 2010) ing expression levels of a neural growth factor In this ‘Commentary’ article from Nature Immu- gene in the offspring of stressed mouse moth- nology, Tarakhovsky starts by tipping his hat to ers. The author then raises the question of how Aristotle and Conrad Waddington. The former relevant such studies are for human behavioural invented the term ‘’ to describe the research. Certainly, early life experiences such idea that development proceeded from the as and being raised in a family with simple zygote through successive stages of dif- low socioeconomic status can influence future ferentiation towards the complex organism. The mental and physical health. However, studies have latter first defined epigenetics as ‘the interactions found evidence both for and against involvement of genes with their environment, which bring the of epigenetic mechanisms in these phenomena phenotype into being’. The authors discuss the in humans (also covered in an excellent recent important point that although changes to marks ‘News’ feature in Nature; Buchen, 2010). Never- such as DNA methylation require cell division theless, this area of research remains a very active for propagation, epigenetic marks such as his- one for many reasons including the potential, tone modifications can still be in a state of flux revealed in animal studies, for epigenetic drugs to within terminally differentiated cell types such counteract the effects of adverse social conditions as . Importantly, Tarakhovsky succinctly in early life and to even reverse ageing-associated summarizes the roles of epigenetic ‘writers’, such phenomena such as a reduced capacity for learn- as histone acetyltransferases, which add epige- ing and formation. netic marks, ‘erasers’ such as histone deacetylases that can remove epigenetic marks and ‘readers’ ‘Epigenomics reveals a functional that recognize a particular epigenetic mark and genome and a new approach nucleate macromolecular complexes around it, to common disease’ by Andrew Feinberg which either promote or repress . (Feinberg, 2010) Emphasis is also put on the role of non-coding In this short article from Nature , RNAs in establishing epigenetic marks and the Andrew Feinberg discusses how genome-scale possibility that histone-modifying enzymes can studies of epigenetics have transformed our under- affect targets other than . The author then standing of the genome. Technologies such as discusses evidence that microbes can directly microarrays and next generation sequencing have interfere with epigenetic readers and suggests that enabled researchers to map the positions of DNA that some influence epigenetic methylation, chromatin proteins and non-coding marks to the extent that they actually prevent RNAs in cell types from stem cells to cancer cells. the onset of some disease such as and Such research has led to some unexpected findings.

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For example, in cancer, methylation changes can epigenetics. The introduction by Jason Goia occur in blocks of large genomic regions span- provides an excellent summary of epigenetic ning many genes, and in the ‘shores’ or flanking mechanisms and phenomena in diverse organisms regions of promoter-associated CpG islands from Drosophila to the fungus . (Irizarry et al., 2009). Another unexpected find- This is followed by a review by Alexander Meiss- ing from genome-scale studies was the discovery ner focusing on epigenetics and development. of widespread interaction between distant genes This article discusses epigenetic properties of stem on the same chromosome and between genes on cells and has summary paragraphs on imprinting, different (van Steensel and Dekker, X inactivation and the role of non-coding RNAs 2010). Feinberg also discusses his own the find- in epigenetic regulation. Jaroslav Jelinek and Jean- ings that some genes may be prepared to respond Pierre Issa then provide an excellent summary of to environmental influence by tolerating a larger epigenetics and cancer, which includes sections range of epigenetic states and that although this on the interaction between genetics and epigenet- could provide an evolutionary advantage in the ics and the relationship between stem cells and long term, these regions may be more susceptible cancer. Finally, Xi Yu Jia provides a great review of to short-term changes in environment such as epigenetic regulation of gene expression in insects the post-war Western diet. The author finishes by and plants. The author focuses on research involv- stressing the need for the marriage of epigenetics ing Drosophila and Honeybees for insects and on and , at the centre of which is the Arabidopsis thaliana for plants. The newsletter also collection and storage of biological samples. contains an epigenetics glossary.

‘What is epigenetics?’ by Guy Riddi- ‘Histone Modifications: A Sampler’ by hough and Laura Zahn (Riddihough Steve Talbott (http://natureinstitute. and Zahn, 2010) org/txt/st/mqual/histone_mods.htm) This one-page summary that introduces a special Talbott presents a brief but informative point- section on epigenetics in a recent issue of the form summary of histone modifications and their journal Science. Riddihough and Zahn discuss functional and structural consequences. Data definitions of epigenetics, the diversity of which reviewed are mainly from studies of , is illustrated by an accompanying video in although other organisms such as are cov- which leaders in the field each provide their own ered briefly. The author presents recent findings in definition (http://videolab.sciencemag.org/ a simple manner while acknowledging that we still Featured/650920373001/1). Interestingly, one have a long way to go to be able to put together of the accompanying articles defines an epigenetic a complete picture of histone modifications, their system as ‘heritable, self-perpetuating and revers- interactions with one another and with other ible’ (Bonasio et al., 2010), a definition that may chromatin proteins. surprisingly exclude histone modifications and include (Halfmann and Lindquist, 2010). Other articles in this special issue focus on devel- Epigenetics societies and opmental (Feng et al., 2010), research networks small RNAs (Bourc’his and Voinnet, 2010), in plants (Chandler, 2010) and epi- The Epigenetics Society (http:// genetic cancer therapies (Kaiser, 2010). es.landesbioscience.com/index.php). The Epigenetics Society, associated with Landes Special epigenetics edition of Peanuts, Bioscience, is an international scientific society the newsletter from Zymo Research open to all those interested in any aspects of DNA (http://www.zymoresearch.com/zrc/ methylation. The ‘members-only’ section con- pdf/peanuts6.pdf) tains contact information of other members of the Compiled in 2009, this freely available resource society as well as updated information on recently contains four 3–4-page review articles on published papers and topical reviews from some

UNCORRECTED FIRST PROOFS Educational Resources for epigenetics | 445 of the foremost scientists interested in this area. (e.g. 5–11, 11+, 18+). Other useful, easy-to-read The ‘public’ page contains a simple description of pages include ‘A short introduction to epigenet- DNA methylation and a summary of the activities ics’, ‘Frequently asked questions’ and a glossary of held for members of the society. The site also has epigenetics. some useful links to epigenetic resources such as a catalogue of imprinted genes, a CpG island search The Australian Epigenome Alliance algorithm and to MethDB, a database of gene- (www.epialliance.org.au) specific DNA methylation. The Australian Epigenome Alliance (AEpiA) aims to provide an avenue for Australasian research The Epigenome Network Of Excellence groups to share expertise and insights in the area (http://epigenome-noe.net/) of epigenetics. The homepage of the site contains The Epigenome Network Of Excellence (NOE) information about the latest conferences and describes itself as the focal point for the European workshops, together with highlights of previous epigenetics research community. The site con- events. This site also contains links to other useful tains links to epigenetics groups, protocols, tools, epigenetic resources such as blogs and highlights resources, news and events. It also contains some of epigenetic articles in journals and magazines, excellent educational pages including the multi- along with a brief explanation of the basics of lingual public science site ‘Epigenetics?’ (http:// epigenetics. In addition, it compiles a list of ref- www.epigenome.eu/), which contains news and erences published by AEpiA members. A list of articles aimed at a broad public audience. It also AEpiA members and their research interests is has an ‘Educational Tools and Resources’ page also provided, nicely grouped according to states which contains videos, webcasts and articles about and countries, with links to laboratory web pages. epigenetics and related fields, with articles tagged with the recommended age range of readership

Table 26.1 Summary of educational resources Reference/title/URL Content Easy-to read articles and web sites aimed at a broad audience McVittie (2006) (http://www.scienceinschool.org/2006/ Introduction to epigenetics for students and those with issue2/epigenetics) limited knowledge of the area Duttaroy (2006) (http://www.mukto-mona.com/ Good article linking the relevance of evolution, nutrition, Special_Event_/Darwin_day/evolution_asim120206. and imprinted genes to epigenetics htm) Pray (2004) (http://www.the-scientist.com/article/ Comprehensive article featuring evidence of how home/14798/) the environment has an active role in shaping the epigenome ‘Molecular Development – Epigenetics’ (http:// Gives a broad coverage of and illustrations relating to .med.unsw.edu.au/MolDev/epigenetic. epigenetics, ranging from its mechanisms to its role in htm) human development NOVA scienceNOW: Epigenetics (http://www.pbs.org/ Interactive web site with great teaching resources to wgbh/nova/teachers/activities/3411_02_nsn.html) assist in a classroom setting Epigenetics? (http://epigenome.eu/) Multilingual site suited for students and lay people to learn how epigenetics plays an active role in our ‘Epigenetics and Imprinted Genes’ (http://www. Short article centred on explaining the link between hopkinsmedicine.org/press/2002/November/ epigenetic modifications and imprinted genes epigenetics.htm) ‘What is it? A simplified description of DNA Review with good examples explaining the concept of methylation’ (http://es.landesbioscience.com/pub/ DNA methylation faq/) Learn.Genetics, epigenetics page (http://learn. Web site that creatively presents the basic concepts genetics.utah.edu/content/epigenetics/) of epigenetics by including video clips and interactive games

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Table 26.1 continued

Reference/title/URL Content Epigenetics news – discoveries and advances (http:// Compilation of opinions and information about www.epigeneticsnews.com/tag/epigenetics/) epigenetics from researchers from all over the world Epigenie (http://epigenie.com/index.html) User-friendly site containing reviews on epigenetics and information about relevant upcoming conferences ‘A (mostly) nontechnical glossary of genetics, Glossary of terms used in epigenetics research. epigenetics and ’ http://www. natureinstitute.org/txt/st/mqual/glossary.htm

Scholarly review articles aimed at a broad scientific audience Felsenfeld and Groudine (2003) Comprehensive overview of epigenetics with a focus on chromatin remodellers and histone variants Turner (2005) Review of how histone modifications are involved in epigenetic change Bird (2007) Successful attempt by the author to reconcile disparate epigenetics views by widening its definition Weinhold (2006) Open access article that summarises the implications of epigenetic regulation in living organisms Qiu (2006) Introduction to epigenetics and the implications for future health Rine and Wu (2008) Article presenting the aims and advances of the Human Epigenome Project (HEP) Goldberg, Allis, Bernstein (2007) Review of how epigenetics shapes the of living organisms Egger, Liang, Aparicio, Jones (2004) Review of how drugs could restore health by reversing disease-associated epigenetic marks Groom, Elliott, Embleton, Relton (2010) Article focusing on the susceptibility to epigenetic change in early mammalian development via environmental exposures. Henderson, Jacobsen (2007) Compact and comprehensive review of epigenetic phenomena in plants, focusing on non-coding RNA Tarakhovsky (2010) Discusses epigenetic ‘writers’, ‘readers’ and ‘erasers’, non-coding RNAs and how microorganisms can affect the host epigenome Miller (2010) Review of animal studies in which maternal interactions can ‘reprogramme’ epigenetics in offspring and discussion of relevance to humans Feinberg (2010) Review of genome-scale epigenetic studies and the unexpected results they have revealed Riddihough, Zahn (2010) One-page summary from a special edition of Science, accompanied by reviews on developmental reprogramming, small RNAs, paramutation in plants, and cancer http://www.zymoresearch.com/zrc/pdf/peanuts6.pdf Contains short review articles on epigenetic mechanisms, development, cancer, insects and plants http://natureinstitute.org/txt/st/mqual/histone_mods. Summary of histone modifications htm Epigenetics societies and research networks http://es.landesbioscience.com/index.php International DNA methylation society with members’ and public pages, including resources http://epigenome-noe.net/ Links to European epigenetics researchers, protocols, news and educational pages http://es.landesbioscience.com/index.php Links to Australian epigenetics researchers, meeting reports, epigenetics resource

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