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An understanding of heart development is critical in any systems biology approach to cardiovascular disease. The interpretation of data generated from high-throughput technologies (such as microarray and proteomics) is also essential to this approach. However, characterizing the role of genes in the processes underlying heart development and cardiovascular disease involves the non-trivial task of data analysis and integration of previous knowledge. The Gene Ontology (GO) Consortium provides structured controlled biological vocabularies that are used to summarize previous functional knowledge for gene products across all species. One aspect of GO describes biological processes, such as development and signaling.
In order to support high-throughput cardiovascular research, we have initiated an effort to fully describe heart development in GO; expanding the number of GO terms describing heart development from 12 to over 280. This new ontology describes heart morphogenesis, the differentiation of specific cardiac cell types, and the involvement of signaling pathways in heart development and aligns GO with the current views of the heart development research community and its representation in the literature. This extension of GO allows gene product annotators to comprehensively capture the genetic program leading to the developmental progression of the heart. This will enable users to integrate heart development data across species, resulting in the comprehensive retrieval of information about this subject.
The revised GO structure, combined with gene product annotations, should improve the interpretation of data from high-throughput methods in a variety of cardiovascular research areas, including heart development, congenital cardiac disease, and cardiac stem cell research. Additionally, we invite the heart development community to contribute to the expansion of this important dataset for the benefit of future research in this area.
Forming as the result of an elegant coordination of integrated processes, the heart is one of the first organs to develop in a vertebrate embryo. Understanding this developmental process is critical to the understanding of cardiovascular disease (CVD), a leading cause of mortality worldwide (Batsis and Lopez-Jimenez, 2010). One aspect of CVD is damaged heart tissue, and the possibility of using stem cells to repair a heart, is an active area of research (Bollini et al., 2011). However, to fully understand how to repair a heart we must first understand the processes by which a heart is formed. Heart development is a complex process controlled by a multitude of coordinated cellular processes resulting in proper patterns of cell differentiation and tissue morphogenesis (Abu-Issa and Kirby, 2007; Dyer and Kirby, 2009). The events in the process are still being identified, thus, the study of genes and proteins involved in cardiovascular development is an important research area. As with any multi-genic process, there is an important role for high-throughput methods to characterize the genes and proteins involved in both developmental and disease processes. However, interpretation of high-throughput data with regard to previously established work is a non-trivial task, associated with a need for categorization of gene functions to enable data analysis. To assist with the interpretation of these data, the Gene Ontology Consortium (GOC) provides a robust hierarchical controlled vocabulary, the Gene Ontology (GO) (Ashburner et al., 2000). Individually each GO term can be applied to gene products across all species to summarize individual experiments. However, the power of GO lies in the fact that it is a categorization of gene products characteristics, rather than a categorization of gene products themselves. Thus, large numbers of gene products can be grouped on the basis of their characteristics, as defined by GO terms. Many high-throughput analysis tools have been developed for this purpose (Hendrickson et al., 2008; Malik et al., 2010; Werner, 2008). GO currently contains over 33,000 terms and is routinely used for the analysis of large datasets (Colak et al., 2009; Herbert et al., 2009; Mace et al., 2009).
The GOC comprises of GO editors who develop the ontology, and GO annotators who read the primary literature and create annotations using the ontology (Gene Ontology Consortium, 2009). The two groups of curators work closely together. As a result GO terms are continuously examined, evaluated and tested during the annotation process based on the experimental literature. The GOC has set up several mechanisms for handling ontology issues. We utilize a SourceForge tracker for ontology questions, have a 'help' resource available from the GO web site and provide contact information for curator interest groups who coordinate biological areas of ontology development (see box). There are more than a dozen model organism databases (MOD) represented in the GOC, which use GO to annotate the gene products of their specific organism. Additionally there are other annotation groups focusing on specific areas of biology. The BHF-UCL (British Heart Foundation-University College London) GO team focuses on cardiovascular biology and has the specific remit of annotating human proteins involved in cardiovascular processes and disease (Lovering et al., 2008). An advantage to having a specialized annotation group like the BHF-UCL group is that it allows for development of a whole branch of the ontology alongside the creation of gene annotations using the new ontology terms. GO annotators read the primary literature and create GO annotations using a variety of evidence codes that describe the nature of the experiments that support the annotation. In practice annotations to developmental processes are mostly derived from direct assays, mutational studies or gene interaction studies. Annotators are cautious about using expression data for GO annotations since expression may correlate with a process, but not necessarily be actively involved in the process.
In general, there are two ways in which ontology development can be coordinated with annotation: 1) terms can be requested individually as annotators find need for them; 2) large-scale development of the ontology can be undertaken in anticipation of the terms needed for annotation. In practice, we have found that the latter method is very efficient for developing focused areas of the ontology (Diehl et al., 2007; Feltrin et al., 2009; Maccagnan et al., 2010). Specifically, we find that collaboration between expert annotators, ontology developers and experimental biologists working in the relevant field is a productive way to create an accurate and complete representation of an area of biology in the shortest amount of time.
In order to establish the groundwork for an expansion of the representation of GO biological processes involved in heart development, an initial meeting was held between gene annotators (from the BHF-UCL GO team and several model-organism databases), GOC ontology developers and cardiac development experts (all authors of this paper). At the start of the work, there were 12 terms in GO that represented all of heart development. Work during the meeting, as well as subsequent revisions and discussions have resulted in the addition of 281 new terms to date (see Supplemental Table for full list of new terms). These new terms have been added to GO and are fully integrated with relationships to other developmental processes in the existing biological processes ontology, and all additional parent terms. The new terms are publically available as part of the current version of GO. GO now includes terms describing an anatomical representation of heart development (such as the valves and the heart chambers), as well as terms that describe specific types of processes that contribute to heart development (such as cell differentiation and signaling pathways). In this article we introduce the new heart development Gene Ontology, demonstrate how it is used for annotations and invite the heart development community to contribute to this important resource.
Gene Ontology (GO) is a controlled vocabulary that is used to classify the biological characteristics of gene products. GO terms describe three characteristics, Biological Process (BP), Molecular Function (MF) and Cellular Component (CC). BP terms describe the general process a gene product is involved in, MF terms describe the specific molecular function of a gene product and CC terms describe the subcellular compartment in which a gene product is found. This work focused on the expansion of the BP part of GO, which encompasses all developmental processes.
Gene annotators use experimentally supported data from published literature to associate specific GO terms with the genes that have been shown to bear the attributes described by the GO term. Taken as a whole, the set of annotations to a given gene product aims to describe the totality of what is currently known about that gene product's role in biology, while an individual annotation describes the results of a single experiment. Annotators use their biological knowledge alongside information presented in the paper to judge the most specific term possible for each annotation. For example, individual experiments have shown that the homeobox NKX2-5 gene product takes part in the process of cardiac muscle cell differentiation (GO:0055007; BP) (Tanaka et al., 1999), has transcription factor activity (GO:0003700; MF) (Kasahara and Izumo, 1999) and is found in the nucleus (GO:0005634; CC) (Zhu et al., 2000). Thus the NKX2-5 gene product has been annotated to each of those terms. Additionally gene products may have multiple functions, often take part in more than one process and can be found in multiple subcellular compartments. GO allows a single gene product to be annotated to any number of terms from each of the three ontologies.
GO terms are structured in a directed acyclic graphs (DAG), where each term can have multiple relationships to broader 'parent' and more specific 'child' terms. The parent and child terms have specific relationships with each other. In GO, there are seven types of relationships (Gene Ontology Consortium, 2009; Smith et al., 2005), of which five are relevant to the heart development ontology. The 'is_a' relationship means that a child term is always a type of its parent term; for example heart development (GO:0007507) is a type of organ development (GO:0048513). The 'part_of' relationship means that the child term is always a part of the parent term; for example cell migration involved in vasculogenesis (GO:0035441) is part of vasculogenesis (GO:0001570). The 'regulates', 'positively_regulates', and 'negatively_regulates' relationships signify that the children have a regulatory effect on the parent; for example the term negative regulation of cardiac muscle tissue development (GO:0055026) has a 'negatively_regulates' relationship to the term cardiac muscle tissue development (GO:0048738). To illustrate how terms and relationships are used in GO, Figure 1 shows that the term vasculogenesis (GO:0001570) has two direct ancestors, cell differentiation (GO:0030154) and blood vessel morphogenesis (GO:0048514). Vasculogenesis 'is a' type of cell differentiation and is also 'part of' the process of blood vessel morphogenesis.
An important benefit of building a DAG, rather than a flat-list of controlled vocabulary terms, is that relationships can be used to make inferences from one term to another. For example, vasculogenesis (GO:0001570) is part of blood vessel morphogenesis (GO:0048514) and blood vessel morphogenesis (GO:0048514) is part of blood vessel development (GO:0001568). Therefore, because the 'part_of' relationship is transitive, vasculogenesis (GO:0001570) can also be considered to be a part of blood vessel development (GO:0001568), and does not require a direct link between the two terms. This transitive nature is very useful when using GO to find gene products annotated as being involved in a particular process; for example a search for gene products annotated to blood vessel morphogenesis (GO:0048514) will include those annotated directly to the more specific processes of vasculogenesis (GO:0001570) and angiogenesis (GO:0001525), both of which are a part of blood vessel morphogenesis (GO:0048514).
Each GO term has several different components (Figure 2). The GO ID is unique to each term. The definition is a textual description of what the term means and in many cases disambiguates the use of identical terms that are used to mean different things. Additionally the placement of the term within the ontology also provides a necessary definition through the terms relationships with its parents. For example the term lateral ventricle development (GO:0021670) may at first glance be ambiguous, but upon viewing the ontology it is clear that this term is a descendant of central nervous system development (GO:0007417), and thus 'ventricle' in this context refers to a brain ventricle and not a heart ventricle.
GO allows for the description of processes that occur at multiple levels of biology: i) the organ level, ii) the multicellular (tissue) level and iii) the level of the single cell. It also allows for the description of generic processes that are used in multiple ways to accomplish a given objective. The developmental process section of the biological process ontology allows for the description of developmental events either from an anatomical perspective or from a process perspective. Standard developmental terms such as cell differentiation (GO:0030154) are defined generically and are then used consistently to describe the process in the context of all of the different processes in which it is involved (Hill et al., 2010). The following sections illustrate how the newly created ontology can be used to describe the heart developmental processes that occur at each of these three levels; heart morphogenesis at the organ level, cell differentiation in the heart at the cellular level, and signaling pathways to describe interactions between cells that make up tissues.
The terms and relationships in the ontology are carefully chosen so that regardless of the species the ontology is always correct. Species-neutrality enables experimentally supported annotations in model organisms, to be transferred to human gene products, if appropriate. For example, based on the observation that expression of mouse Mesp1 in embryonic stem cells (ESCs) results in transcriptional regulation of key genes controlling early mesoderm and endoderm cell fates and promotes the progression of cells toward a cardiac fate (Bondue et al., 2008), one of the terms that was used to annotate the mouse Mesp1 gene product is cardiac cell fate determination (GO:0060913). At the time of writing there are 26 experimentally supported annotations associated with the mouse Mesp1 gene product, whereas there are 10 such annotations associated to the human MESP1 gene product. The unique mouse annotations have been transferred to the orthologous human protein, thus enhancing our knowledge about how the orthologous gene products might be involved in human biology or disease.
In GO, morphogenesis is used to describe the initial formation of an anatomical structure and its subsequent shaping in an anatomical context. Because the ontology does not contain temporal relationships, GO does not describe lineage relationships between anatomical structures. Although often embedded in the definition of a term, lineage relationships themselves are not specified in the ontology. An important aspect in the creation of the development domain of GO is identifying when a structure begins to exist and what processes lead to its formation. In addition, GO developers need to reflect the prevailing thought of the scientific community of a given field. This approach allows GO to be used in a practical manner as it is aligned with current scientific thought. The heart is formed from a distinct group of cells (distinguishable from the surrounding cell population only by the proteins expressed) that make up the heart fields. These cells proliferate and migrate to form distinct subpopulations of cells, which then form the discrete substructures of the heart, for example the valves and the chambers. GO reflects that the specification of the heart field is one of the initial processes of heart development and contains terms for primary heart field specification (GO:0003138) and secondary heart field specification (GO:0003139). Both of these terms are types of a more generic heart field specification (GO:0003128). The induction process whereby the mesoderm, endoderm, and ectoderm interact are not part of the formation of the heart per se, but rather positively regulate its formation. The rationale behind this decision is that when this inductive process is occurring, the heart has not formed and the delineation of the field is the first step in the formation of the actual structure. This decision is consistent with all inductive interactions in the development domain of the ontology (Hill et al., 2010). Other terms that are part of the morphogenesis of the heart reflect both the morphogenesis of anatomical parts of the heart such as cardiogenic plate morphogenesis (GO:0003142) and endocardial cushion morphogenesis (GO:0003203), or conserved processes that contribute to the shaping of the structure itself such as apoptosis involved in heart morphogenesis (GO:0003278) and growth involved in heart morphogenesis (GO:0003241). The latter category of terms allows users of GO to search for gene products that might be conserved in apoptosis or growth involved morphogenesis of other anatomical structures.
Much of development at the cellular level can be considered to be successive cell differentiation events that eventually lead to terminally differentiated cells that contribute to the functioning of a mature anatomical structure. GO describes cell differentiation in two parts. First an undifferentiated cell somehow decides what it will become and then in the second step the cell undergoes the actual process of becoming differentiated. In GO, the term cell differentiation (GO:0030154) is the parent of the terms cell fate commitment (GO:0045165) that describes how a cell decides what to become, and cell development (GO:0048468) that describes how a cell undergoes the actual differentiation process. The relationship between these terms and further descendants of these terms are shown in Figure 3. The way that GO defines cell differentiation, and in particular the phrases used in the definitions of these terms, is discussed in greater depth in a review of Gene Ontology and developmental biology (Hill et al.).
This structure allows GO to describe the differentiation of any cell type in the heart. As a result, we have included 26 cell type terms specific to the heart in the revised ontology (Table 1). These range from very general cell type terms like cardiac fibroblast cell differentiation (GO:0060935) to very specific cell type terms like atrioventricular bundle cell differentiation (GO:0003167).
The structure that is now in place will permit gene product annotations to be integrated into knowledge about not only the generic types of cells that cardiac cells represent but also integrated into the way they play specific roles in the development of the heart. For example, atrioventricular bundle cell differentiation is related to generalized cardiac muscle cell differentiation as well as to the development of the cardiac conduction system (Figure 4).
The arrangement of the cell differentiation terms allows for the placement of new terms easily into the ontology. It also allows for the detailed annotation of gene products at a level of detail that is supported by the experimental data. For example, in the context of ESC differentiation, when ESCs are transfected with POU5F1 cDNA and stimulated with BMP2, pluripotency is lost, the cells express SOX17 and adopt a cardiovascular fate (Stefanovic et al., 2009). However, without the BMP2 signal, transfection with POU5F1 cDNA maintains the pluripotency of the ESC. Thus, POU5F1 specifies a cardiac cell fate only if the cell is subject to a specific environment, and so POU5F1 was annotated with cardiac cell fate specification (GO:0060912). (The mouse Pou5f1 and human POU5F1 gene products respectively have 68 and 18 additional experimentally supported annotations). On the other hand, once the human ESC expresses SOX17, it is committed to a cardiac cell fate regardless of the environment (Stefanovic et al., 2009); thus SOX17 was annotated with cardiac cell fate determination (GO:0060913). (The mouse Sox17 and human SOX17 gene products respectively have 15 and 11 other experimentally supported annotations).
The revised heart development ontology allows for the annotation of gene products that describe signaling processes between different types of heart cells. Terms like endodermal-mesodermal cell signaling involved in heart induction (GO:0003134) describe signaling processes where it is known that the cells of the endoderm signal to cells of the mesoderm, but the molecular nature of the signaling is unknown. Where the molecular nature of the signaling is known, we are able to create terms for the specific pathways. So far we have created terms for the BMP, hedgehog, FGF, Notch, TGF-beta and WNT signaling pathways as children of cell surface receptor linked signaling pathway involved in heart development (GO:0061311). By creating these high-level generic terms, we have built the framework for the addition of more specific terms, involving these and other signaling pathways, as needed to annotate new data. For example, it has shown that heart induction is a result of several signaling pathways, the BMP signaling pathway (Dyer and Kirby, 2009), the Notch pathway (MacGrogan et al., 2010) and the FGF receptor signaling pathway (Samuel and Latinkic, 2009); whilst the canonical Wnt receptor signaling pathway plays a negative role (Palpant et al., 2007; van de Schans et al., 2008). As an example of the types of signaling pathway terms GO can support, we have created terms such as BMP signaling pathway involved in heart induction (GO:0003130), fibroblast growth factor receptor signaling pathway involved in heart induction (GO:0003135) and Notch signaling pathway involved in heart induction (GO:0003137), all as 'part of' heart induction (GO:0003129) (Bondue et al., 2008; Lough et al., 1996; Schlange et al., 2000).
We have also created the term negative regulation of heart induction by canonical Wnt receptor signaling pathway (GO:0003136) to describe the role of that pathway in the process. Annotations are made to gene products involved in each of the pathways, and these can then be used during analysis of high-throughput data to identify members of signaling pathways that play roles in heart induction. For example, BMP2 induces a cardiac fate (Stefanovic et al., 2009) and has therefore been annotated to BMP signaling pathway involved in heart induction (GO:003130) while the Mesp1 gene product promotes cardiovascular differentiation by inhibiting the canonical Wnt signaling pathway (David et al., 2008), hence Mesp1 was annotated to the term positive regulation of heart induction by negative regulation of canonical Wnt receptor signaling pathway (GO:0090082). This term positively regulates heart induction and therefore describes the role of the Mesp1 gene product. As an example of how we plan to handle the complexity of signaling pathways in heart development, we have expanded the Wnt-receptor signaling portion of the ontology in detail.
As shown in Figure 5, Wnt receptor signaling pathway involved in heart development (GO:0003306) has two child terms, canonical Wnt receptor signaling pathway involved in heart development (GO:0061316) and non-canonical Wnt receptor signaling pathway involved in heart development (GO:0061341). Based on the literature, the canonical Wnt receptor signaling pathway involved in heart development (GO:0061316) term has been given six child terms to describe the role of canonical Wnt signaling in cardiac muscle cell fate commitment (GO:0061317), cardiac neural crest cell differentiation (GO:0061310), cardiac muscle cell proliferation (GO:0061315), cardiac outflow tract cell proliferation (GO:0061324), secondary heart field cardioblast proliferation (GO:0003267), and heart induction (Brade et al., 2006; Kwon et al., 2007; Song et al., 2010).
We have begun using these terms for the annotation of gene products. As detailed annotations accumulate, it will become increasingly easy to identify all proteins that act in signaling pathways resulting in specific developmental events in the heart. As more experimental evidence becomes available to support the role of a particular signaling pathway in a particular developmental event, we will continue to expand the ontology and the associated annotations.
GO is designed so that it can be used for the annotation of all gene products across all species. This allows GO to be used to examine orthologous gene products from a variety of species and to make conclusions about conserved or diverse biological processes based on annotations to similar or dissimilar GO terms. It also allows us to transfer annotations from one species to another when genes appear to have conserved functions across species (Mi et al., 2009). For example, orthologs of TBX5 have been shown to be key players in the patterning of the ventricle. These gene products have differential expression patterns in the 3-chambered amphibian heart compared to the 4-chambered mammalian and avian hearts. In the red-eared slider turtle (Trachemys scripta elegans), the expression of Tbx5 was homogenous throughout its single ventricle, whereas in the chick it was restricted to the left ventricle (Koshiba-Takeuchi et al., 2009). Furthermore, the loss of Tbx5 in the mouse ventricle resulted in the development of a single ventricle, similar to that of the turtle (Koshiba-Takeuchi et al., 2009). In this relatively simple scenario, the mouse and chick Tbx5 gene products are annotated to ventricular septum development (GO:0003281) and cardiac left ventricle formation (GO:0003218). The turtle Tbx5 gene product would be annotated to the parent of the latter term, cardiac ventricle formation (GO:0003211). Thus the structure of the ontology allows for the differential annotation of orthologous gene products that take part in related but distinct processes in different species.
However, there are also cases where different species have specific structures. In the zebrafish (Danio rerio), the bulbus arteriosus is an elastic heart chamber that receives blood from the heart, and maintains its flow to the gill arches. There is no orthologous structure in mammals, so we created the term bulbus arteriosus development (GO:0003232) to capture this fish-specific process.
There are also some processes that appear to be species specific. In the zebrafish, the establishment of left/right asymmetry of the heart tube has been observed to occur through a two step process of heart tube displacement and rotation called 'heart jogging' and 'heart looping' (Chen et al., 1997). The resulting left/right asymmetry of the heart tube is reversed or otherwise disrupted in a number of zebrafish mutants affecting genes including the chd, acvr1l, smad5, bmp7a, ndr2, foxh1, pkd2, lrrc6, spaw, and cha genes (Chen et al., 1997; Hashimoto et al., 2004; Long et al., 2003). Experimentally supported data from such mutants has been curated to a number of GO BP terms relating to heart development, including heart jogging (GO:0003146), heart looping (GO:00011947), cell migration involved in heart jogging (GO:0003305), and determination of left/right symmetry (GO:0007368). The process of heart jogging has not been observed in mammals, in addition there does not appear to be an orthologous process. Therefore, restrictions in the ontology have been created to ensure that any annotations made to zebrafish gene products to heart jogging (GO:0003146) and its child terms cannot be transferred to mammalian orthologs. The GOC has mechanisms in place to ensure that inappropriate annotations are not made (Deegan et al., 2010).
With the new ontology structure for heart development in place, the challenge now is to utilize the new terms in annotations and to continue to refine and add to the ontology. This is a daunting task for MOD curators since the existing experimental literature is voluminous. Manual GO annotation is a painstaking process, with a large volume of literature to sort through and relatively few curators at each MOD dedicated to GO annotation. One way to increase the amount of information about how gene products play a role in heart development is to take advantage of the orthology strategies described above. However, the annotation effort can also be greatly helped by input from research scientists working in collaboration with professional curators. This exercise in ontology development is proof that input from experts in the field can have dramatic effects on a bioinformatics resource such as GO. Since experimental biologists are necessarily much more familiar with their field of research, they know the details and location of the experimental evidence to support a GO annotation or a new ontology term better than a GO curator, who does not necessarily specialize in the field.
Research scientists can help to improve the GO annotation dataset for heart development in a number of ways. 1) Review the information we have captured about a gene in which they specialize, informing us of inaccurate or missing annotations. 2) Help identify key papers in a field or research, resulting in the manual curation representing the most comprehensive and accurate information. 3) Review the ontology to be sure that it is complete and aligns with the current thought in the field. 4) Provide feedback about how they have used GO in their analyses, reporting about what they liked, didn't like or features they would like to see available. 5) Researchers could also provide GO annotations from their own papers, this has been working well with the Arabidopsis community (Ort and Grennan, 2008). Input can be provided to the GOC in multiple ways (see box). Once suggestions are made ontology curators will address issues that are raised, with help from domain experts in the field. We suggest that a good time for researchers to provide GO annotations would be when proofreading accepted papers. This would ensure the latest data would be included in the GO annotation dataset. Annotated papers may be cited more often, since GO is widely used in bioinformatics analyses.
Although the GOC consists of curators working at several different MODs in multiple different locations around the world, GO curators communicate regularly and utilize each other's expertise. For example, a curator working on human gene products may contact a curator working for another MOD as needed, to annotate a paper on an organism which is unfamiliar to them. Therefore the GO curators are able to call upon a wide range of species-specific expertise as needed. Additionally, GO curators are proactive about involving expert researchers as needed to work on a particular area of the ontology, as evidenced by the work described here and by previous ontology development projects (Feltrin et al., 2009; Maccagnan et al., 2010).
In this article we have described the work that we have done to refine and expand the representation of heart development in GO. We have expanded the heart development section of the ontology from 12 to over 250 terms. In the process, we have integrated the representation of heart development with other cellular and developmental processes in GO. Biological Process GO terms can now be used to interpret all aspects of heart development processes, from an anatomical perspective, to a cell differentiation perspective, through to a cellular perspective such as signaling. Heart development is a complex process underpinned by multiple gene regulatory networks and signaling pathways, and the use of GO terms can help to simplify the categorization of gene products which are important to this process. Additionally, the fact that GO terms and their associated annotations are freely available means that this dataset is a vitally important resource for the heart research community, from those wishing to analyze high-throughput data (Marques et al., 2010; Tranter et al., 2010) to those wishing to use the heart as a model for understanding how organogenesis initiates and unfolds (Abdulla et al., 2010).
The structure we have established not only places heart development in alignment with other developmental processes in GO, but also allows for the interpretation of gene product annotations using the variety of ontology structures and the detail of terms. This new structure should prove useful for researchers in the field who are performing genomic studies or searching for genes that could be involved in a given process. As the terms are used for annotation and as researchers generate new biological knowledge, we anticipate additional terms will need to be created. The existing mechanisms established by the GOC for revising the ontology will continue to be used. However, the ontology foundations presented here will permit easy additions of new terms in the future as children of existing heart development terms. For example the differentiation of a new cell type can be added as a differentiation of an existing generic cell type and a part of the development of the structure to which it contributes.
With the structure of the heart development ontology now in place, the rate-limiting step for using GO to its full potential is the annotation of gene products to the new terms in the ontology. Curators from the relevant model organism databases are working alongside the BHF-UCL GO team to screen the literature and identify papers containing gene products that are involved in heart development. It is at this step, and in the continued development of the ontology where experts in the field could help us to streamline the process. By helping us to identify key genes, literature and areas of the ontology on which to focus, researchers could make certain that the limited curatorial resources available are utilized in the most efficient manner. In the end this will add to the value of our resource for the benefit of the entire cardiovascular research community.
The BHF-UCL team is funded by the British Heart Foundation (SP/07/007/23671), as part of the Cardiovascular GO Annotation Initiative. The Gene Ontology Consortium is funded by NHGRI grant HG002273 to J. Blake, J. M. Cherry, S. Lewis and M. Ashburner. Dr. Constance Smith and Dr. Cynthia Smith for their critical reading of the manuscript.
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Something I was proud ofJun. 16th, 2014 05:36 pm
I did a fanfic based on Future GPX Cyber Formula, particularly on its OVA series "Zero". Only a few people, or at least I know about two (Car dummy Miki Shinichiro did one as well?), has done Cyber Formula fics. That is especially in English.
And since I was impressed with the series, the TV show being smart and about a boy and a machine, and the OVA being dramatic with interesting visuals (my fun slowly being thrown away like shoveled sand due to bad subs, repeated footage, and Asurada oversteering its tail nearly into a circle and passing through a curve successfully to pass
( Spoilerish about ZERO series, but if you don't mind )
RC Type!
Game footage. A nice rivalry against Knight Shumacher. There's also Kaga, Shinjyo, Hayato, and I think Hiyama Nobuyuki's character, Andrea. It's hard to tell because he has a scar on his forehead. Sounds like him. BGM is Identity Crisis.

subset: commoncrawl


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Thursday, March 4, 2010
WWAUW - March Blog Prompt #3
To My Family and Friends,
I'm writing this letter in hopes of encouraging you to start keeping a journal. As you know, I have been working on genealogy for quite a few years. What does this have to do with keeping a journal? I'll try to explain.
Most of the information I find is not personal information. It doesn't tell a story like a journal would. Yes. It helps me in my journey of putting the family in this town, county, state or country. However, there is nothing personal. The information I find doesn't tell me what the weather was like on a given day. It doesn't go into detail of a family wedding or any traditions that come from the family. Most of my information is family tradition and is passed down from one family member to another. Sometimes important details get lost from one family member to another.
Keeping a journal will show those that love you what you have done during the course of keeping your journal. Whether it be months or years. It could mention the birth's of children, marriages, hardships and places they have lived or lands they have traveled to. It may cover jobs and the friends that they had during their lives.
Although the gentleman wasn't my direct ancestor but a cousin, I got to read his Civil War journal. Another was letters he had written. It showed me the importance of keeping a journal.
I know that after writing this letter to you, I am going to take the time to start a daily journal of my own. I want my family or friends that might read it to know the things I enjoyed, my pet peeves and that one of the things I enjoy most is the sound of the wind when it gently blows through a ripened wheat field or that I think it looks like a field of gold.
Love and Hugs,
©Karen A J Rinehart
5 comments:
Karen, I keep a journal and I fully agree with your thoughts on this. I don't always remember to write in it every day but I do keep it up to date with important happenings or events that will matter to my children some day. Thanks for another wonderful blog post.ReplyDelete
I remember journaling from my English Comp class. We had to keep one during the class. I, too, found it hard to write in it every day. I am sure that my journal won't be quite as interesting as yours, but I do think it important. Thank you for reading my writing. It means so much to me.ReplyDelete
Karen, I've started & stopped personal journaling many times over my lifetime. You're letter is tempting me to start anew, tho' I'm not sure anyone will be around to want it when I'm gone..:-)ReplyDelete
I can so understand how your geneology would have you wanting to know the everday personal items of interest to somehow validate the people of your ancestry. And again, I applaud you being interested enough to gather all the ancestral belongings into one place for safekeeping.
Ruthi, you may not have family that would be interested in your life, but you have friends. Friends that care deeply about you and would have an interest in your journals.ReplyDelete
Genealogy, as you know, has been a passion of mine for many years. I still am in awe of the things I am finding.
OK, if I do begin another journal, I'll put your name and phone number in it, it'll be all yours!ReplyDelete
Loveya Karen!


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Please note—contact Gayle at X228 when making reservations for all events! Thank you!!
This year's Arline Phillips Achievement Award Recipient is Atty. Stephanie Fernandes!!
Congratulations Stephanie!!!!
If you are interested in attending our Annual Awards Dinner on October 19, 2017 please
contact Amy for more info at 570-693-3555 x223 or at firstname.lastname@example.com. To learn more please click here.
Contact Gayle at 877-693-3555 X228 to make a reservation for the Support Groups and to arrange for transportation.
WAYNE COUNTY-Honesdale Senior Center (323 10th St, Honesdale, PA 18431)
- Tuesday, July 11th from 11:00am-12:00pm
- Tuesday, August 8th from 11:00am-12:00pm
- Tuesday, September 12th from 11:00am-12:00pm
PIKE COUNTY-Area Agency on Aging Senior Center (506 Avenue Q, Matamoras, PA 18336) **
- Wed., July19th from 10:30am-11:30am
- Wed., August 16th from 10:30am-11:30am- Speaker will be from Pike County Voter Registration Office.
- Wed., September 28th from 10:30am-11:30am
**Please take note of NEW MEETING LOCATION
Coffee and dessert will be served at all events.
VIP Support Group
Thurs. July 27 from 11:00am-12:00pm
Topic: "Gift of Life Program"
Light refreshments will be served. RSVP by July 21.
Lunch and Learn Session
Wed. August 30 from 11:00am-12:30pm
Topic: "Medicare Fraud" presented by the
Center for Advocacy for the Rights & Interests of the Elderly
Italian Hoagies and Chips will be served.
RSVP by August 25.
VIP Support Group
Thurs. Sept. 28 from 11:00am-12:00pm
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Light refreshments will be served. RSVP by Sept. 22.
All above events will be held at the Susquehanna Apartments (25 Avery Street, Tunkhannock)
Please contact Gayle for Trans. 1-877-693-3555 x228
- Wed. 5th: Book Club 2-3:30. "The Racketeer" by John Grisham
- Thurs. 6th: Client Picnic at the Plains Pavilion 5:00-7:30PM, Plenty of food, refreshments, family friendly entertainment, fun and games for all to enjoy!! RSVP by 7/3.
- Mon 17th: Sight Loss Support Group,5-7PM, 300G Laird St., Wilkes-Barre.
- Wed. 26th: Lunch & Learn, 11:30-1:30PM, RSVP by 7/21. TOPIC: "How to be Happy" with Rabbi Kaplan MENU: Ham & Cheese
- Wed. 2nd: Book Club 2-3:30PM "A Prisoner of Birth" by Jeffery Archer
- Thurs. 17th: Chicken & Biscuits & Bingo, 5:30-7:30PM, RSVP by 8/11.
- Mon 21st: Sight Loss Support Group,5-7PM, 300G Laird St., Wilkes-Barre.
- Wed. 23rd: Lunch & Learn 11:30-1:30PM, RSVP by 8/18. TOPIC: "LCTA Changes andQ &A" with Kathleen Bednarek MENU: Turkey & Cheese Hoagies
- Wed. 6th: Book Club 2-3:30PM "Lone Wolf" by Jodi Picoult
- Mon 18th: Sight Loss Support Group,5-7PM, 300G Laird St., Wilkes-Barre.
- Mon. 25th: Bloomsburg Fair Trip-Bus will leave our office at 9AM and return to our office at 5PM. RSVP by 9/18. Each visually impaired person MUST bring a guide capable of escorting them through the fair. Each visually impaired person and one guide will attend free of charge.Additional guests are welcome but must pay their own admission into the fair. You must arrange your own transportation to and from our office. Cars may park in our lot for the day.
- Wed. 27th: Lunch & Learn 11:30-1:30PM, RSVP by 9/22. TOPIC: "Exercising Your Right to Vote" MENU: Roast Beef Hoagies
Unless otherwise stated, the following applies to our activities and events. Each visually impaired person and a guide may attend FREE. Additional guests for Lunch & Learn- $5; additional guests for Bingo Dinners- $10. If needed, we will arrange FREE transportation for visually impaired individuals to most of our activities and events.


text: How Do You Handle Defeat? Defeat may test you; it need not stop you. If at first you don't succeed, try another way. For every obstacle there is a solution. Nothing in the world can take the place of persistence. The greatest mistake is giving up. author unknown Share this:TwitterFacebookEmail


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Melissa contacted me last winter about shooting her wedding in McCall, Idaho. She lives in Florida, but grew up in Idaho. We would not get the chance to meet until her wedding day. Fast forward to the big day. After a beautiful drive to McCall, we followed a winding dirt road to find a rustic cabin with breathtaking views of the mountains where the couple and their family was staying. That was the first of many lovely surprises that day. Meeting Melissa and Carter was another delight. Friendly, generous and kind; they treated us like part of the family.
Melissa and Carter held their quiet ceremony in the backyard of the cabin, which overlooks the river. The quiet setting of only their closest family and friends lent a warmth and intimacy that was truly special. The mood of their reception was a mixture of tears and joy as everyone gathered for a delicious meal, toasts, cake and dancing while the dusky sky faded to black, and a blanket of stars glowed overhead. Afterward, the party moved to inside the cabin, where they enjoyed a shot or two, a lot of laughter, and each other's company.
Thank you, Melissa and Carter. You are so beautiful together, and it's plain to see that you value and appreciate the most important things in life…close family and friends. It was an honor to be a part of such a wonderful day.
Thanks, also to my friend and assistant photographer, Frank Espinoza. Several of the photos below are his, and the day wouldn't have been the same without him.
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Think about what career is best suited for you, and where you want to study. Request more information now.
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PLEASE DON'T CUT ME … I WANT YOUR CHILDREN TO SEE ME TOO!! Campaign to reserve our *Turned Tulips* in skirts of Zagros chain mountain بیایید تا همگی برای حفظ لاله های واژگون تلاش کنیم
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Looking for the skinny on practice tracks around So Cal. Me and some of the buds from Vegas want to trek down (probably on a weekend) to get some So Cal riding in. I see a lot of guys posting about Elsinore, what's up with that track?
Obviously, Glen Helen is closest to us here in Vegas, some guys do a day trip to there. I'm thinkin a trip for us to Elsinore would require an overnight, in that case none of us have enclosed trailers so I'd worry about our scoots getting ripped off at some hotel.
Thanks for the info in advance.
p.s. where all Vet riders (early 30s) so supercross tracks are not really the most fun for us to ride when trying out new tracks far away from home


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Maybe they can but what effect would it have?
He not an American citizen and he's not subject to any of congress's authority....or do I have it wrong?
They can only charge him with anything if he lied. Galloway is not stupid - he wouldn't be there if he would incriminate himself.
Lets be honest here, the Senate has no power over him even if he did lie.
Not a US lawyer but by my reckoning once he stepped foot in the United States he subjected himself to US juristiction. Once he took the oath in the senate understanding that he was subject to perjury, well, he's subject to perjury! We tend to extradite folk whenever you ask.... that is why I actually think this is one massive PR blunder. I don't think he would've gone if there was truth in the specific allegations. THe daft thing about this is whilst he accuses the committee of being a 'smokescreen' for the 'failure in Iraq' - he is actually using it as a smokescreen to bring up the old arguments about WMD rather than concentrating on the fact that Iraq has an Iraqi government free from the grip of an evil dictator and a future in the peoples gift. This really is a PR disaster. I'm stunned the US let him in.
Perjury isn't a legistlative thing, he would be at odds with the Judiciary.


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Maria Sharapova blasts Open organisers over extreme heat policy
R\ussian is among several contenders who are confused by seemingly random decision to suspend play
Maria Sharapova on Thursday demanded more clarity from organisers on their heat policy after surviving a brutal three-hour marathon in scorching conditions at the Australian Open.
The third seed battled through a third set lasting nearly two hours to overcome Karin Knapp 6-3, 4-6, 10-8 in temperatures above 40 degrees Celsius.
The conditions were so tough that organisers suspended play midway through the third set. However, under tournament rules, Sharapova and Knapp had to first finish the set.
"There is no way getting around the fact that the conditions were extremely difficult, and have been for the last few days," she said.
"I mean, I think the question I have is no one really knows what the limit is. Not the players; the trainers themselves, when you ask them when will the roof be closed.
"No one actually knows what that number is in comparison to humidity or the actual heat.
"Sometimes you wish you know, because it just depends on I'm not sure who, a referee or the meteorologist, and there are just a lot of questions in the air that maybe should be solved."
The policy was put into force at 1.50pm local time as the mercury headed towards a peak of 43.4 degrees Celsius and no play was possible until 6pm.
In a bizarre turn of events, less than two hours after the resumption, the players were forced off again by lightning and rain.
France's Alize Cornet said conditions were similar a day earlier when temperatures peaked at 42.2 degrees.
"On Tuesday, I wonder why they didn't stop play. It was like an oven," she said. "The wind was scorching, and some people fainted. They shouldn't go to such an extreme.
"Why today and not on Tuesday? The conditions are similar, it's maybe one degree more. It looks like their decision is made a bit on the fly, and that's a pity."
The extreme heat policy, introduced in 1998, relies on the "wet bulb global temperature" - a complex calculation factoring air temperature, humidity, wind and sunlight. The last time it was used was in 2009, the hottest Australian Open on record.
While Sharapova came through her match unscathed, she still has vivid memories of 2007 when she played in searing heat at Melbourne against France's Camille Pin after which she said she was "so delusional I couldn't think".
Ivan Dodig became the 10th player to retire in the first three days on Wednesday and said he feared for his life.
Twelve doubles matches were cancelled on Thursday. The heat was forecast to continue on Friday before a dramatic drop in temperatures at the weekend.
Additional reporting by Reuters
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All colors and artwork dyed into the fabric Artwork for names, logos, etc. must be provided in vector to our Graphic Arts Department Lighter colors can be more transparent Poly/Lycra fabric with moisture management Matman Sublimated Colors Pink, Royal, Red, Copper, Columbia Blue, Vegas Gold, Silver Grey, Old Gold, Orange, Kelly Green, Purple, Maroon, Navy, Lime Green, Dark Green, Cardinal, Athletic Gold, Brown, Teal, Charcoal Grey
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For over forty years, Matman Wrestling has been manufacturing and distributing top-quality wrestling singlets, uniforms, warm ups, shoes, knee pads, ear guards, mat tape, and other wrestling accessories. The company uses the finest materials to provide stock and customized apparel for your wrestling team. The stock, sublimated, and sewn uniforms easily accommodate special custom designs and logos as well as special sizes for women and youth.
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March 21, 2012
Protandim contains an ingredient whose roots' smell is best
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system, calm mental processes, foster healthy sleep patterns,
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‹‹ newer posts
© LifeVantage Corporation 2013. All rights reserved. ® Protandim is a registered trademark of LifeVantage Corporation. (LFVN)


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Kaskaskia College exercise science
Think about what career is best suited for you, and where you want to study. Request more information now.
Think about what career is best suited for you, and where you want to study. Request more information now.
Think about what career is best suited for you, and where you want to study. Request more information now.
Info concerning Kaskaskia College exercise science, and registering for discussion sections and departmental electives. Not all recruiting is done like NCAA Division I teams. College coaches want to see you play. A lot of the time college coaches may have only one chance to see potential recruits play, so be ready to shine if you are visiting the campus in person. Finally, check with your major department for assistance with prerequisites, tuition payment deadlines, and Kaskaskia College Weightlifting information. Please use the form above to request admissions info for Kaskaskia College.
In the weight room, don't be fooled by players who are always pumping iron. It takes a lot more than big muscles to succeed in college sports. Players are becoming more agile, and developing superior game skills every year. You need to develop muscle strength as well, it's true, but your primary focus in weight training should be to use the equipment to help you develop strength along a natural range of motion.
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text:
In the code below, the AngularJS
$http method calls the URL, and submits the xsrf object as a "Request Payload" (as described in the Chrome debugger network tab). The jQuery
$.ajax method does the same call, but submits xsrf as "Form Data".
How can I make AngularJS submit xsrf as form data instead of a request payload?
var url = "http://somewhere.com/";
var xsrf = {fkey: "xsrf key"};
method: "POST",
url: url,
data: xsrf
}).success(function () {});
type: "POST",
url: url,
data: xsrf,
dataType: "json",
success: function() {}
The following line needs to be added to the $http object that is passed:
headers: {'Content-Type': 'application/x-www-form-urlencoded'}
And the data passed should be converted to a URL-encoded string:
> $.param({fkey: "key"})
So you have something like:
method: 'POST',
url: url,
data: $.param({fkey: "key"}),
headers: {'Content-Type': 'application/x-www-form-urlencoded'}


text:
[Plugin: Twitter Tools] Too many custom fields!
I've got twitter tools posting a tweet when a new blog post is saved. It creates a custom field 'aktt_notify_twitter' initially set to 'no'. So I write my post, and set it to 'yes'. Save the post, tweet gets sent, new field called 'aktt_tweeted' appears, with value 'yes'. All good.
But next time I save the post, another custom field gets created, also called 'aktt_notify_twitter', and also set to 'yes'. So I end up with two custom fields, both called the same name, and both holding the same value. That can't be right, can it?
Viewing 1 replies (of 1 total)
Viewing 1 replies (of 1 total)
- The topic '[Plugin: Twitter Tools] Too many custom fields!' is closed to new replies.


text:
Anyone who owns a Carter knife knows they are the best in the world. We offer life-time sharpening complimentary on all Carter Cutlery knives we sell.
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5 star hotels in Marbella
Filter Results
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22 properties found
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Puente Romano
Crta. De Cadiz, Km 177 , Marbella, Spain (Show map)
Built in 1979 and renovated in 2004, this beach hotel is located on a main road and comprises a 2-floored main building and a 3-floored annexe building.
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Marriott'S Marbella Beach Resort
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The luxury Marriott'S Marbella Beach Resort is placed on the beachfront.
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1986 Ford F-250 Regular Cab 4WD
2 days ago
Belgrade, MT 59714, USA
Belgrade, MT
Make offer
1986 Ford F-250 2dr XLT 4WD Extended Cab LB HD
1 week ago
Clovis, CA 93612, USA
Clovis, CA
1986 Ford F-250 2dr XL Standard Cab LB
2 weeks ago
Shoreline, WA 98133, USA
96,511 Miles
Shoreline, WA
Shoreline, WA
... to treat our customers like our friends...because they are. http://www.shorelinefamilyautocareandsales.com (206)362-7007 Call if you have any questions ● Power Steering ● Power Brakes ● Radio - Am ● Tire Type ● Wheel Diameter - 16 Inch ● Front...
- Mileage: 96,511 Miles
- Location: Shoreline, WA 98133
- Exterior: Tan
- Transmission: Automatic 4-Speed
- Seller: Shoreline Family Auto Care And Sales
1986 Ford F-250 2dr 4WD Extended Cab LB HD
3 weeks ago
Anchorage, AK 99501, USA
Anchorage, AK
1986 Ford F-250 2dr Extended Cab LB HD
30+ days ago
Seattle, WA 98107, USA
64,000 Miles
Seattle, WA
Seattle, WA
... Ford truck.Almost impossible to find this vintage Ford truck in any better condition.64,000 original miles. This was my everyday driver for 18 months. Starts rightup and runs very well. I still drive it fairly often. Several 200+ mile tripsover the past 18 months. Recent fixes/u...
- Mileage: 64,000 Miles
- Location: Seattle, WA 98107
- Exterior: Red
- Transmission: Automatic 4-Speed
- Seller: Auto Connections Seattle
1986 Ford F-250 2dr XLT 4WD Standard Cab LB HD
30+ days ago
Mandan, ND 58554, USA
138,251 Miles
Mandan, ND
Mandan, ND
1986 Ford F-250
30+ days ago
Joelton, TN 37080, USA
55,000 Miles
Joelton, TN
Joelton, TN
1986 Ford F-250 Diesel Flatbed
30+ days ago
Belgrade, MT 59714, USA
Belgrade, MT
1986 Ford F-250 Supercab
30+ days ago
Portland, ND 58274, USA
55,876 Miles
Portland, ND
Portland, ND
1986 Ford F-250
30+ days ago
Kent, WA 98042, USA
Kent, WA
86 Ford F-250 flat bed diesel
30+ days ago
Buellton, CA 93427, USA
Buellton, CA
86 Ford F-250
30+ days ago
Coeurdalene, MT 59904, USA
112,678 Miles
Coeurdalene, MT
Coeurdalene, MT
1986 Ford F-250 w plow
30+ days ago
Coventry, CT 6238, USA
95,000 Miles
Coventry, CT
Coventry, CT
1986 Ford F-250
30+ days ago
Staunton, VA 24401, USA
141,650 Miles
Staunton, VA
Staunton, VA
1986 Ford F-250 parts truck
30+ days ago
Arnold, CA 95223, USA
61,957 Miles
Arnold, CA
Arnold, CA
1986 Ford F-250 Lariat
30+ days ago
Oak Grove, VA 22403, USA
Oak Grove, VA
86 Ford F-250 Diesel 4x4
30+ days ago
Eugene, OR 97403, USA
Eugene, OR
86 Ford F-250 extended cab
30+ days ago
Ninilchik, AK 99639, USA
Ninilchik, AK
... and dinged up, but not totally cancer ridden. Now, this is not a \"Saturday night girl hunting wagon,\" as a couple of potential buyers seemed to expect. This is not auu Bentley. This truck is a \"beater with a heater.\" Please don\'t call unless you\'re serious. It\'s kept in hap...
- Location: Ninilchik, AK 99639
- Transmission: automatic
1986 Ford F-250 diesel
30+ days ago
Anniston, AL 36206, USA
Anniston, AL
1986 Ford F-250
30+ days ago
Vermilion, OH 44089, USA
75,000 Miles
Vermilion, OH
Vermilion, OH


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Goodreads helps you keep track of books you want to read.
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Tarzan in Color: 1949-1950 (Tarzan (1949-1950))
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Hardcover, 64 pages
Published February 1st 1997 by Nbm Pub Co
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Burne Hogarth started young. Born in 1911, he was enrolled in the Chicago Art Institute at the age of 12 and an assistant cartoonist at Associated Editors' Syndicate at 15. At the age of 26, he was chosen from a pool of a dozen applicants as Hal Foster's successor on the United Features Syndicate strip, "Tarzan". His first strip, very much in Foster's style, appeared May 9, 1937. It wasn't long be ...moreMore about Burne Hogarth...
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