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A Concept Paper for the Establishment of a Dictyostelium Bioinformatics Center

 

Summary:

 

   Dictyostelium discoideum has been an important experimental organism for the analysis of fundamental biological processes, including cell migration (Parent and Devreotes, 1999), cell – cell signaling and signal transduction (Parent and Devreotes, 1996; van Es and Devreotes, 1999), phagocytosis (Titus, 2000), signaling during morphogenesis and cell fate choice (Meili et al., 2000) and recently for the growth and study of intracellular microbial pathogens such as Legionella (Solomon et al., 2000).    Because of the unique experimental opportunities it provides, the NIH has included Dictyostelium in its list of important model organisms.  One goal for the NIH support of model organisms is to provide infrastructure that facilitates the use of the experimental system.  A critical component of this infrastructure is a well-organized and up-to-date on-line bioinformatics resource that organizes and presents information about the experimental system.  As the genome sequence is completed, experimental results from functional genomics studies, proteomics, genetic screens and from single gene functional studies represent an important resource for the community using Dictyostelium in their studies.  In addition, making this information, as well as specific protocols for working with Dictyostelium readily available on the internet will facilitate the use of the system by investigators wishing to apply its unique experimental advantages to their studies.  Our goal is to expand the current, volunteer effort to provide a one-stop resource for Dictyostelium bioinformatics by obtaining support for personnel and hardware.  This site would also serve as a front end for the stock center whose establishment is described in a companion document.  Together these services support the entire community of investigators interested in the use of Dictyostelium as a model system.

 

Introduction:

 

   D. discoideum was has many experimental advantages for studying fundamental cellular processes with powerful combination of molecular genetic, biochemical and cell biological tools.  These processes include cytokinesis, motility, phagocytosis, chemotaxis, signal transduction, and aspects of development such as cell sorting, pattern formation, and cell-type determination.  The combination of biochemical, molecular genetic, and cell biological tools that can be applied to Dictyostelium are unique among model organisms.  Each experimental system has both strengths and weaknesses.  The strengths of Dictyostelium include its easy growth and synchronous development.  This makes possible the economical culture of large quantities of both wildtype and mutant strains that facilitate biochemical analysis.  The range of available cell biological assays has made Dictyostelium the experimental system of choice for a variety of fundamental studies on motility, signaling, cytokinesis and phagocytosis – and especially important, these cell biological studies can be readily correlated with biochemical analysis.  For example, Dictyostelium has been one of the most important systems for analyzing the function of actin-associated proteins in cell locomotion, regulation of cell shape and cell behavior.  Similarly the function of myosin outside of the context of muscle has been more extensively studied in Dictyostelium than any other organism (Chen et al., 1994; Chen et al., 1995; De Lozanne and Spudich, 1987; Knecht and Loomis, 1987; Moores et al., 1996; Ruppel and Spudich, 1996; Zang et al., 1997).  The development of live cell imaging coupled to the ready manipulation of gene expression has produced important new understanding about cytokinesis (Weber et al., 1999), phagoctyosis (Weber et al., 1999), and chemotaxis (Parent et al., 1998).  The transient recruitment of cellular components to the membrane during chemotaxis was first demonstrated using Dictyostelium (Parent et al., 1998).  Molecular genetic manipulation is now allowing careful dissection of the pathways leading from binding of chemoattractant to its cell surface receptor to reorganization of the cytoskeleton to produce directed cell migration (van Es and Devreotes, 1999). 

 

   The value of Dictyostelium as a model organism is being greatly enhanced by the development of an expressed sequence tag database, progress toward the completion of the genome sequence by an international consortium, development of proteomics and DNA array technology, and development of large screens to identify novel components of the signaling and motility systems.  These developments, coupled with the unique experimental opportunities available through the use of Dictyostelium as an experimental organism are drawing investigators from other fields.  For example, the growth of intracellular parasites, such as Legionella (Solomon et al., 2000), in Dictyostelium has attracted investigators interested in understanding the cellular requirements for intracellular parasite growth.  Dictyostelium can provide them with a genetic system for identifying key host cell genes required for this growth and may eventually lead the way to novel means of interfering with this process.  Similarly, Alexander and his colleagues have identified Dictyostelium mutants resistant to the cancer chemotheraputic agent cisplatin.  By identifying the mutant pathways in these strains, Dictyostelium may contribute to an understanding of the mechanisms of drug resistance that develop during chemotherapy.    The use of Dictyostelium for similar studies by investigators not familiar with the system, as well as increased progress in areas where Dictyostelium has already proven its value would be greatly facilitated by a comprehensive, well organized on-line informatics resource. 

 

   For the last seven years we have been developing an on-line bioinformatics resource for Dictyostelium – the Dictyostelium Virtual Library (http://dicty.cmb.northwestern.edu/dicty/).  This effort began with a listserv type mailing list that allowed rapid communication between investigators using Dictyostelium.  An electronic newsletter that provides abstracts of papers once they are accepted for publication has facilitated sharing of information between investigators.  The newsletter is also searchable using a search engine on the front page of the web site.  A compilation of the Dictyostelium literature, produced and maintained by Dr. Jakob Franke (Columbia University) can be downloaded through the Dictyostelium web site.  The current web site also has an on-line, user-modifiable database of investigators using Dictyostelium.  A database of Dictyostelium genes using a modified version of AceDB, called DictyDB has been developed by Dr. Doug Smith (UCSD) and is available through the central Dictyostelium web site.  In addition, there are links to web sites for Dictyostelium laboratories with web sites.  The Dictyostelium Virtual Library also includes links to all of the Dictyostelium genome sequencing centers, a limited number of protocols and methods for using Dictyostelium, a listing of Dictyostelium genes that have been disrupted by gene targeting and their phenotypes.  However useful these volunteer efforts have been, their scope has surpassed our ability to provide continuous updates and links for protocols, vectors, maps, gene function, etc.  Investigators using Dictyostelium now require a central, dedicated bioinformatics resource.

 

Goal of Dictyostelium on-line informatics resource. 

 

   The goal of establishing a comprehensive Dictyostelium bioinformatics resource is to provide a single portal through which all Dictyostelium bioinformatics can be accessed.  A central goal is to establish, maintain and annotate relational databases that allow investigators to utilize DNA sequence, global expression data, mutant phenotypes, and physiological and biochemical results in a concerted fashion.  In addition we will make available protocols for working with Dictyostelium.  These goals are currently being pursued for other model organisms for which the genome sequences have been completed, including yeast (http://genome-www.stanford.edu) , Drosophila (http://www.flybase.bio.Indiana.edu and  http://fruitfly.bdgp.berkeley.edu/) , C. elegans (http://elegans.swmed.edu/) and mouse (http://www.informatics.jax.org).  Our goal for this resource is not to reinvent the overall schemes being developed by these and similar efforts, but rather to apply the best features of them to the data being obtained for Dictyostelium.  This allows us to focus our efforts on annotation rather than database development.  For example, the Gene Ontology consortium represents an on-going effort to establish common vocabularies by which gene function can be described (Ashburner et al., 2000).  We anticipate affiliating the Dictyostelium informatics resource with this effort.  In a similar fashion, in a collaborative effort with other organism-based bioinformatics resources, whenever possible, the Dictyostelium resource would use existing relational database structures so as to facilitate direct comparisons between organisms. 

 

    The resource will also serve as the portal for the stock center that is being proposed by Drs. Richard Kessin and Jakob Franke.  The databases developed by the informatics resource will contain data about strain availability.  We propose to develop a system that links strain availability directly to DNA sequences, gene expression, disruption, mutant phenotypes and the literature.  A single click on a button would generate a request to the stock center for the strain.

 

     We envision this effort starting out modestly with two or three curators familiar with both the informatics side of the effort and with Dictyostelium as an organism and a database engineer to handle the data structures and web presentation.  See the section below on implementation.

 

What unique features does Dictyostelium offer that justify this effort?

 

   One of the most important questions that will arise is: why support Dictyostelium informatics?  Perhaps one of the best arguments comes from its unique place in the biological kingdom.  Dictyostelium sits at the transition between free-living single cells and multicellular organisms.  During its lifecycle Dictyostelium exists both as single cells (during vegetative growth) and as a multicellular tissue capable of morphogenesis (during development).  Because of this position, understanding the complement of Dictyostelium genes may give insight into the biological functions important for multicellularity.  As a free-ranging amoeba, Dictyostelium is a consummate phagocyte.  Comparisons with cells such as yeast and macrophages may give significant insight into this critical biological process.  Similarly, as an amoeba, Dictyostelium exhibits extensive motility and chemotaxis.  As such it will likely provide a valuable insight into the collection of functions required for ameboid movement – a function that is significant for important health related issues such as wound healing, mounting of an immune response and susceptibility to parasitic diseases. 

 

   When these unique biological features are coupled with the ease and efficiency of molecular genetic manipulation, the ability to validate biochemical pathways experimentally because of the ease of growing adequate quantities of cells for biochemical analysis, and the strong cell biology available in Dictyostelium, we believe Dictyostelium provides a unique model system of particular advantage for studies on cell motility, signal transduction, phagocytosis and the mechanisms important for multicellularity. 

    Since there is a strong on-going international genome sequencing effort, a large and growing expressed sequence tag database, the genomic data is being generated and accumulating rapidly.  For example the Japanese effort has already identified over 3000 gene families in Dictyostelium.  The resource will provide an ongoing mechanism to correlate this data with the variety of other data available for Dictyostelium.  Delaying the implementation of this resource will decrease the immediacy and impact of much of this data.

 

Implementation of the Resource.

 

The Dictyostelium Bioinformatics Resource will share a great deal of similarity in scope and concept with a number of other successful model organism sites such as the Drosophila Flybase sites at http://flybase.harvard.edu:7081/ and http://flybase.bio.indiana.edu/, the yeast Saccharomyces Genome Database at http://genome-www.stanford.edu/Saccharomyces/ and the C. elegans resource http://elegans.swmed.edu/.  These resources all share a number of common elements – they have a shallow navigational structure to allow researchers to easily move between sections of the resource, they attempt to put a consistent interface and terminology on a number of formally independent data sources. For example, with Flybase, an investigator can easily flip between different ‘data views’ of available information for Drosophila, including genetic maps, genes, clones, alleles, gene products, and stocks. We would like to take these very good ideas and implement them in a way that makes sense for Dictyostelium and the community of investigators who use or who might wish to take advantage of the experimental opportunities this organism provides.  We would also like to build in ‘web portal’ concepts, allowing researchers to build a profile of sequences, genes, phenotypes and/or strains they are interested in and receive automated notification whenever new entries are added to the system.

 

We propose using Oracle, an industry standard relational database, as the underlying data engine for the Dictyostelium Bioinformatics Resource.  We believe that this will allow development of a more versatile site and will allow us to take better advantage of much of the research and optimization that has gone on in the past few years and will continue to go on in commercial sector database design.  At Northwestern we have assembled a team with experience taking standard ‘E-commerce’ technologies and they have applied these technologies to bioinformatics problems in both the basic and clinical sciences.  We propose to take advantage of the expertise and the experience of this team to build a modern and extensible Dictyostelium web site. 

 

Architecture and technologies.  In addition to using Oracle as the data engine for storage and retrieval of sequence, strain and other relevant data, we will couple Oracle to the web using standard SQL queries run through Allaire ColdFusion. We have extensive experience using ColdFusion, currently the best rapid prototyping and application development platform availabe for database to web development.  We have been using ColdFusion in production applications since 1997. The current version works natively with EJB (Enterprise Java beans) and can translate data from a number of different sources into XML without additional coding.  By relying on mainstream commercial packages we will be able concentrate on bioinformatics rather than technology development.

 

Implementation.  The data repository for the Dictyostelium Bioinformatics Resource will be held in an Oracle 8i database running on Sun servers. This system is in use in many high-throughput, high transaction volume applications in industry and academia. This will give us a solid, high-throughput technology platform on which to build our analysis tools. The Oracle database will house genetic, sequence, strain, gene profile, bibliographic and phenotypic data.  These data will be collated from multiple sources including the current genome projects, published single gene functional studies, and the published Dictyostelium literature.  All queries, reports, and results will be dynamically generated from the database and be accessible to members of the Dictyostelium community via the internet using middleware built with Allaire ColdFusion.  The existing Dictyostelium site uses this technology to present data from the investigator database (http://www.basic.nwu.edu/dicty/search.cfm).

 

Because the database and the middleware are ‘connected’ using standard SQL, once a particular report has been written the report can be easily stored and run at any future time. All our reports will be written using a combination of Allaire ColdFusion and standard SQL (Structured Query Language, a standard programming language for ‘querying’ databases), making all the results instantly web accessible anywhere in the world.  Further, we have used these technologies to generate automatic messaging and email-based notification systems for both event-driven and date-driven notifications.

 

We are also anxious to participate in collaborative interactions with other organism based informatics resources to facilitate comparisons of data housed for different organisms.  We would propose the establishment of a consortium of organism based informatics resources that could standardize technologies and share applications.

 

The facility will be directed by Rex Chisholm, Professor of Cell and Molecular Biology at Northwestern University Medical School.  Dr. Chisholm has worked with Dictyostelium for over twenty years.  He has been responsible for establishing and maintaining the existing Dictyostelium internet resources at http://dicty.cmb.northwestern.edu/dicty/.  In addition, the technical aspects of the resource will be overseen by Dr. Warren Kibbe, an experienced bioinformaticist who has substantial experience with interfacing relational database with biologically based internet sites.  An experienced Oracle database engineer, Ms. Lorraine Padour is already part of the Northwestern University Medical Informatics resource and a portion of her effort will be available to this project.  We will also hire two curators familiar with Dictyostelium to actively populate, maintain and annotate the databases.  A budget our estimated first year costs is attached. 

 

Questions to be addressed in a concept paper:

 

·        By what process did the community obtain input and reach a consensus about the priority for the proposed project?  At the most recent International Dictyostelium Conference, Dictyostelium 1999 held in Bar Harbor, Maine, a community board was established.  The composition of the community board is international in nature (see http://dicty.cmb.northwestern.edu/dicty/pnd/organizing_committee.htm).  The first priority of the organizing committee was to develop the interactive web site at http://dicty.cmb.northwestern.edu/dicty/pnd/ for the trans-NIH Coordinating Committee for Non-Mammalian Models (see http://www.nih.gov/science/models).  The community board has selected establishment of the Dictyostelium bioinformatics resource and the stock center as its highest priorities together with the completion of the genome sequence.  In addition, over 400 investigators who are listed in the investigator database use the current configuration of the Dictyostelium Virtual Library.  The community already recognizes the current site as the central Dictyostelium portal.  It averages over 1500 visits each month indicating significant use for a resource that is significantly less comprehensive than the proposed effort.

 

·        Other Sources of Support: The sequencing of the Dictyostelium genome is currently supported by the NIH through a grant to Baylor College of Medicine from the National Institute for Child Health and Development.  In addition the European Community and the German National Science Foundation have also supported Dictyostelium genome sequencing.  Each of these projects has an informatics component.  However, the focus of these informatics components is the analysis of genome sequence and cDNA sequences.  The focus of this request is to consolidate current and past gene by gene based research, genomic expression studies, mutant phenotypes, and other similar data together with that being generated by the genome sequencing and EST efforts into an easy to use on-line system.

 

·        Advantages and Limitations:  The primary advantage of establishing this resource is that it will provide a single source for bioinformatics of Dictyostelium.  This facility will maximize the investment made in Dictyostelium genome sequencing and the large number of single gene, cell biological and biochemical studies by making them all accessible online through a single web portal.  This will benefit both investigators experienced with Dictyostelium and those without experience using the experimental system, but interested in taking advantage of some of its unique experimental opportunities.

 

·        Do we need the genomic resources now?  Two main factors argue for implementing this resource as soon as possible.  First, there is already a large amount of data to be cataloged.  This includes both genomic and cDNA sequences generated by the international genome sequencing consortium and the Japanese cDNA project.  In addition a large number of gene disruption strains has already been produced, several large genetic screens have been undertaken and extensive gene regulation studies have been completed.  We currently estimate that approximately 95% of the Dictyostelium genes have representative sequences available, that approximately 50% of the genes are fully sequenced and that approximately 80% of the entire genome has been sequenced.  In addition, around 30% of the developmentally regulated genes have already been characterized by mutational analysis.  Delay in implementing the resource results in lost opportunities for investigators both inside and outside the field.  A second factor is that costs for establishing and maintaining the resource will unlikely decrease in the future.  Because of its unique position in the biological kingdom having an active Dictyostelium bioinformatics resource is also likely to enhance the value of similar resources for other organisms by facilitating organism to organism comparisons of core proteome size as well as specialized functions.  By working closely with the other organism based informatics resources a Dictyostelium resource would be able to enhance development of database structures so as to encompass a wide variety of organisms with different niches in the biological kingdom.  Thus there

 

·        Are there plans to develop the resources outside the US? No. The Dictyostelium Virtual library is already serving as the central portal for Dictyostelium information and the Dictyostelium resource would work with genomics and proteomics efforts elsewhere to ensure that it meets their needs.  Participants from each major genomics activity would serve an the advisory board for the Dictyostelium informatics resource.

 

·        What are the unique advantages of this organism: The advantages of Dictyostelium are discussed above in the introduction and the section entitled “What unique features does Dictyostelium offer that justify this effort?”  In addition, the community has created a on-line tutorial (http://dicty.cmb.northwestern.edu/dicty/pnd/) that highlights many of the unique features of Dictyostelium. 

 

·        What scientific advances will be made possible? As noted above, the unique position of Dictyostelium in the biological kingdom makes it a particularly useful organism that will help define the genes important for multicellularity.  In addition, research in areas of fundamental biological inquiry where Dictyostelium excels, such as cell motility, signal transduction and phagocytosis are likely to benefit from the availability of this resource.  For example, the ability to begin to correlate mutations in signal transduction pathways with cytoskeletal mutants are likely to have a great impact on understanding of chemotaxis.  Similarly the recent interest by the infectious disease community in using Dictyostelium as a host for intracellular microorganisms will certainly benefit since this effort is being spearheaded by investigators who are unfamiliar with Dictyostelium.  For them the internet presence we propose to develop will serve as a valuable resource for those new to the organism.

 

·        What is the cost? Initially we request funds to purchase a dedicated server and hire two full time curators/informaticians to define database structure (primarily by collaborating with similar efforts in other organisms) and to begin to populate and annotate the data and technical support to guide construction of the datastructures and development of the web interfaces.  We expect the initial start up costs to be about $40,000 plus the salary and fringe benefits and operating budget of about $200,000 annually.   A detailed budget is appended.

 

·        What is the duration? A primary reason for requesting support through this mechanism is the need for on-going support for this activity.  We initially request five years of support initially.  At the end of the five year period the success of the resource and its value to the Dictyotelium community and the biomedical research community at large should be evaluated. 

 

·        How will the repository be supported after the completion of the project?  It is anticipated that the resource would require NIH or other extramural support as long as it serves the needs of the community.  As bioinformatics develops, it may be that the organism based information resources could be housed in a centralized operation similar to Genebank, housed perhaps by the National Center for Biotechnology Information.  However, certainly during the early stages it will be necessary that the curators have experience with Dictyostelium as an experimental model to efficiently annotate and organize the experimental data.

 

·        How will the resources be made available to the research community? This will be an on-line resource available to everyone on the internet.

 

·        What resources currently exist? The current on-line resource, the Dictyostelium Virtual Library, is operated on a strictly volunteer basis.  The rate at which data about this organism has outstripped our ability to keep the information up-to-date.  Our goal is to obtain resources that provides the resources necessary to have a focused and dedicated effort to grow the existing resource into a first rate bioinformatics effort for Dictyostelium.

 

·        What is the size of the research community? The size of the community is roughly five hundred active scientists in 80 laboratories.  Because of the cell biological and genetic possibilities of the organism, the community is growing. It is also widely used as a teaching tool. The community is organized and has a board of directors that is international in scope and seeks to make research on the organism as efficient and as cooperative as possible. The record of cooperation in this field, like that in the C. elegans community, is excellent.

 

·        Who will benefit? We imagine that anyone actively using Dictyostelium as an experimental organism would benefit from this resource.  In addition, the resource will also be of great value to anyone who might be interested in using the organism.  Finally we believe the entire field of functional genomics will benefit because Dictyostelium has a unique position at the intersection between single celled and multicellular organisms.  Efforts to define core proteomes and specialized proteomes important for fundamental biological functions such as multicellularity, chemotaxis, and phagocytosis will benefit certainly benefit from a concerted effort to make Dictyostelium bioinformatics readily available to the biological research community. 

 

·        What will be the benefits? The primary benefit will be an improvement in the accessibility, organization and usability of bioinformatics as it relates to Dictyostelium.  The existing data represents a valuable resource much of which has been funded by the NIH and NSF.  The NIH is already a substantial contributor to the genome sequencing effort.  A concerted effort to produce and maintain a Dictyostelium bioinformatics resource will ensure that the investments already made by NIH in studies using Dictyostelium as well as the Dictyostelium genome are maximized.  This resource will ensure that the valuable data produced from studies using  Dictyostelium as a model organism will be available to the entire research community in a format that facilitates organism by organism comparisons and stimulates cross-talk between researchers using different model organisms.

 

Conclusion

 

We believe that developing an integrated informatics infrastructure that is tightly coupled to the Dictyostelium research community will be an important factor in allowing Dictyostelium to fulfill its unique role as a model organism.  The goal of the Bioinformatics Resource is to rapidly build modular, scalable, and cost effective tools for the biomedical research community. By careful consideration of scaling issues in the initial design we hope to concentrate on the biological information collection, analysis and distribution methods as we move forward rather than needing to “reinvent” the underlying technology infrastructure as new techniques or technologies emerge.  We believe that funding of this resource will produce more efficient use of NIH resources currently committed to studies using Dictyostelium.  In addition we believe that wide availability of this information will facilitate biomedical research in general by stimulating the use of Dictyostelium for studies that take advantage of its unique features, such as has recently occurred in the infectious disease community with the use of Dictyostelium as a host for intracellular bacterial parasites.  Together with its position in the evolutionary “tree of life” at the junction between single celled and multicelled organisms, ready availability of informatics resources will facilitate understanding of both the core proteomes and the specific collections of genes important for multicellularity as well as the fundamental cell biological processes to which Dictyostelium has already become a proven and important contributor. 

 

 

 
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Peter v. Sengbusch - b-online@botanik.uni-hamburg.de