Unification of multi-species vertebrate anatomy ontologies for comparative biology in Uberon

Journal of Biomedical Semantics

Christopher J Mungall⁵  Paul C Sereno⁹  Marc Robinson-Rechavi^1,10  Anne Niknejad^1,10  Paula M Mabee⁷  Suzanna E Lewis⁵  Nizar Ibrahim⁹  Terry F Hayamizu²  Robert E Druzinsky¹  Thomas A Dececchi⁷  Wasila M Dahdul⁷  Aurelie Comte^1,10  Yvonne Bradford³  Judith A Blake²  David C Blackburn⁴  Frederic B Bastian^1,10  James P Balhoff⁸  Melissa A Haendel⁶ 

[1] Department of Oral Biology, University of Illinois-Chicago, Chicago, IL 60612, USA;The Jackson Laboratory, Bar Harbor, ME 04609, USA;The Zebrafish Model Organism Database, University of Oregon, Eugene, OR 97403, USA;Department of Vertebrate Zoology and Anthropology, California Academy of Sciences, San Francisco, CA 94118, USA;Lawrence Berkeley National Laboratory, 1 Cyclotron Rd, Berkeley, CA 94720, USA;Department of Medical Informatics & Epidemiology, Oregon Health & Science University, Portland, OR, USA;Department of Biology, University of South Dakota, Vermillion, SD 57069, USA;National Evolutionary Synthesis Center, Durham, NC, USA;Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA;Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

关键词: Bio-ontology;    Semantic integration;    Phenotype;    Morphological variation;    Evolutionary biology;   

Others  :  815377
DOI  :  10.1186/2041-1480-5-21

 received in 2013-07-10, accepted in 2014-03-25,  发布年份 2014

【 摘 要 】

Background

Elucidating disease and developmental dysfunction requires understanding variation in phenotype. Single-species model organism anatomy ontologies (ssAOs) have been established to represent this variation. Multi-species anatomy ontologies (msAOs; vertebrate skeletal, vertebrate homologous, teleost, amphibian AOs) have been developed to represent ‘natural’ phenotypic variation across species. Our aim has been to integrate ssAOs and msAOs for various purposes, including establishing links between phenotypic variation and candidate genes.

Results

Previously, msAOs contained a mixture of unique and overlapping content. This hampered integration and coordination due to the need to maintain cross-references or inter-ontology equivalence axioms to the ssAOs, or to perform large-scale obsolescence and modular import. Here we present the unification of anatomy ontologies into Uberon, a single ontology resource that enables interoperability among disparate data and research groups. As a consequence, independent development of TAO, VSAO, AAO, and vHOG has been discontinued.

Conclusions

The newly broadened Uberon ontology is a unified cross-taxon resource for metazoans (animals) that has been substantially expanded to include a broad diversity of vertebrate anatomical structures, permitting reasoning across anatomical variation in extinct and extant taxa. Uberon is a core resource that supports single- and cross-species queries for candidate genes using annotations for phenotypes from the systematics, biodiversity, medical, and model organism communities, while also providing entities for logical definitions in the Cell and Gene Ontologies.

The ontology release files associated with the ontology merge described in this manuscript are available at: http://purl.obolibrary.org/obo/uberon/releases/2013-02-21/

Current ontology release files are available always available at: http://purl.obolibrary.org/obo/uberon/releases/

【 授权许可】

   
2014 Haendel et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Bard JL, Kaufman MH, Dubreuil C, Brune RM, Burger A, Baldock RA, Davidson DR: An internet-accessible database of mouse developmental anatomy based on a systematic nomenclature. Mech Dev 1998, 74:111-120.
• [2]Hayamizu T, Mangan M, Corradi J, Kadin J, Ringwald M: The adult mouse anatomical dictionary: a tool for annotating and integrating data. Genome Biol 2005, 6:R29. BioMed Central Full Text
• [3]Rosse C, Mejino JL V: A Reference Ontology for Bioinformatics: The Foundational Model of Anatomy. J Biomed Informat 2003, 36:478-500.
• [4]Bard J: A new ontology (structured hierarchy) of human developmental anatomy for the first 7 weeks (Carnegie stages 1–20). J Anat 2012, 221:406-416.
• [5]Van Slyke CE, Bradford YM, Westerfield M, Haendel MA: The zebrafish anatomy and stage ontologies: representing the anatomy and development of Danio rerio. J Biomed Semant 2014, 5:12. BioMed Central Full Text
• [6]Costa M, Reeve S, Grumbling G, Osumi-Sutherland D: The Drosophila anatomy ontology. J Biomed Semant 2013, 4:32. BioMed Central Full Text
• [7]Segerdell E, Bowes JB, Pollet N, Vize PD: An ontology for Xenopus anatomy and development. BMC Dev Biol 2008, 8:92. BioMed Central Full Text
• [8]Segerdell E, Ponferrada VG, James-Zorn C, Burns KA, Fortriede JD, Dahdul WM, Vize PD, Zorn AM: Enhanced XAO: the ontology of Xenopus anatomy and development underpins more accurate annotation of gene expression and queries on Xenbase. J Biomed Semant 2013, 4:31. BioMed Central Full Text
• [9]Haendel MA, Neuhaus F, Osumi-Sutherland D, Mabee PM, Mejino JLV, Mungall CJ, Smith B: CARO - The Common Anatomy Reference Ontology. In Anatomy Ontologies for Bioinformatics: Principles and Practice. Edited by Burger A, Davidson D, Bladock R. Volume Albert Bur: Springer; 2007.
• [10]Washington NL, Haendel MA, Mungall CJ, Ashburner M, Westerfield M, Lewis SE: Linking human diseases to animal models using ontology-based phenotype annotation. PLoS Biol 2009, 7:e1000247.
• [11]Mungall CJ, Torniai C, Gkoutos GV, Lewis SE, Haendel MA: Uberon, an integrative multi-species anatomy ontology. Genome Biol 2012, 13:R5. BioMed Central Full Text
• [12]Dahdul WM, Lundberg JG, Midford PE, Balhoff JP, Lapp H, Vision TJ, Haendel MA, Westerfield M, Mabee PM: The teleost anatomy ontology: anatomical representation for the genomics age. Syst Biol 2010, 59:369-383.
• [13]Mabee PM, Arratia G, Coburn M, Haendel M, Hilton EJ, Lundberg JG, Mayden RL, Rios N, Westerfield M: Connecting evolutionary morphology to genomics using ontologies: a case study from Cypriniformes including zebrafish. J Exp Zool B Mol Dev Evol 2007, 308:655-668.
• [14]Dahdul WM, Balhoff JP, Engeman J, Grande T, Hilton EJ, Kothari C, Lapp H, Lundberg JG, Midford PE, Vision TJ, Westerfield M, Mabee PM: Evolutionary characters, phenotypes and ontologies: curating data from the systematic biology literature. PLoS One 2010, 5:e10708.
• [15]Maglia AM, Leopold JL, Pugener LAÌ, Gauch S: An anatomical ontology for amphibians. Pac Symp Biocomput 2007, 12:367-378.
• [16]Dahdul WM, Balhoff JP, Blackburn DC, Diehl AD, Haendel MA, Hall BK, Lapp H, Lundberg JG, Mungall CJ, Ringwald M, Segerdell E, Van Slyke CE, Vickaryous MK, Westerfield M, Mabee PM: A unified anatomy ontology of the vertebrate skeletal system. PLoS One 2012, 7:e51070.
• [17]Niknejad A, Comte A, Parmentier G, Roux J, Bastian F, Robinson-Rechavi M: vHOG , a multi-species vertebrate ontology of homologous organs groups. Bioinformatics 2012, 28:1017-1020.
• [18]Mabee PM, Balhoff JP, Dahdul WM, Lapp H, Midford PE, Vision TJ, Westerfield M: 500,000 fish phenotypes: The new informatics landscape for evolutionary and developmental biology of the vertebrate skeleton. J Appl Ichthyol 2012, 28:300-305.
• [19]Bastian F, Parmentier G, Roux J, Moretti S, Laudet V, Robinson-Rechavi M: Bgee: Integrating and Comparing Heterogeneous Transcriptome Data Among Species. Data Integr Life Sci 2008, 124-131.
• [20]Bgee: A database for gene expression evolution http://bgee.unil.ch
• [21]Parmentier G, Bastian FB, Robinson-Rechavi M: Homolonto: generating homology relationships by pairwise alignment of ontologies and application to vertebrate anatomy. Bioinformatics 2010, 26:1766-1771.
• [22]Phenotype Research Coordination Network http://www.phenotypercn.org/
• [23]Neural Crest Workshop Sponsored by Phenotype RCN http://wiki.phenotypercn.org/wiki/Neural_Crest_Workshop
• [24]Wall CE, Vinyard CJ, Williams SH, Gapeyev V, Liu X, Lapp H, German RZ: Overview of FEED, the feeding experiments end-user database. Integr Comp Biol 2011, 51:215-223.
• [25]Shubin NH, Daeschler EB, Coates MI: The early evolution of the tetrapod humerus. Science 2004, 304:90-93.
• [26]Hall BK: Fins into Limbs: Evolution, Development, and Transformation. Chicago: University of Chicago Press; 2007.
• [27]Haeckel E: Systematische Phylogenie. Entwurf eines Natürlichen Systems der Organismen auf Grund ihrer Stammesgeschichte. Dritter Theil: Systematische Phylogenie der Wirbelthiere (Vertebrata); 1895.
• [28]Chiu C, Hamrick M: Evolution and development of the primate limb skeleton. Evol Anthro 2002, 11:94-107.
• [29]Tamura K, Yonei-Tamura S, Yano T, Yokoyama H, Ide H: The autopod: its formation during limb development. Dev Growth Differ 2008, 50(Suppl 1):S177-S187.
• [30]Shou S, Scott V, Reed C, Hitzemann R, Stadler HS: Transcriptome analysis of the murine forelimb and hindlimb autopod. Dev Dyn 2005, 234:74-89.
• [31]Vukičević TT, Alić I, Slavica A, Poletto M, Kužir S: Preliminary osteometrical analysis of metapodium and acropodium bones of fallow deer (Dama dama l.) from the Brijuni islands, Croatia. Veterinarski arhiv 2012, 82:75-88.
• [32]Wagner GP, Chiu CH: The tetrapod limb: a hypothesis on its origin. J Exp Zool 2001, 291:226-240.
• [33]Johanson Z, Joss J, Boisvert CA, Ericsson R, Sutija M, Ahlberg PE: Fish fingers: digit homologues in sarcopterygian fish fins. J Exp Zool B Mol Dev Evol 2007, 308:757-768.
• [34]The Uberon User Manual http://purl.obolibrary.org/obo/uberon/docs/manual
• [35]Pree W: Design Patterns for Object-Oriented Software Development. Reading, Mass: Addison-Wesley; 1994.
• [36]Aranguren ME, Antezana E, Kuiper M, Stevens R: Ontology Design Patterns for bio-ontologies: a case study on the Cell Cycle Ontology. BMC Bioinforma 2008, 9(Suppl 5):S1. BioMed Central Full Text
• [37]The Uberon Documentation System http://purl.obolibrary.org/obo/uberon/docs/About-documentation
• [38]Uberon Design Document - Modeling Articulations https://github.com/obophenotype/uberon/wiki/Modeling-articulations-Design-Pattern
• [39]Zheng W, Wang Z, Collins JE, Andrews RM, Stemple D, Gong Z: Comparative transcriptome analyses indicate molecular homology of zebrafish swimbladder and mammalian lung. PLoS One 2011, 6:e24019.
• [40]Bgee Anatomical similarity annotations https://sourceforge.net/p/bgee/wiki/Similarity%20annotation/
• [41]Uberon tracker http://purl.obolibrary.org/obo/uberon/tracker
• [42]Anderson JT, Willis JH, Mitchell-Olds T: Evolutionary genetics of plant adaptation. Trends Genet 2011, 27:258-266.
• [43]Vickaryous MK, Sire J-Y: The integumentary skeleton of tetrapods: origin, evolution, and development. J Anat 2009, 214:441-464.
• [44]Zug GR, Vitt LJ, Caldwell JP: Herpetology: An Introductory Biology of Amphibians and Reptiles. London: Academic Press; 2001.
• [45]Zylberberg L, Wake MH: Structure of the scales of Dermophis and Microcaecilia (Amphibia: Gymnophiona), and a comparison to dermal ossifications of other vertebrates. J Morphol 1990, 206:25-43.
• [46]Malone J, Holloway E, Adamusiak T, Kapushesky M, Zheng J, Kolesnikov N, Zhukova A, Brazma A, Parkinson H: Modeling sample variables with an experimental factor ontology. Bioinformatics 2010, 26:1112-1118.
• [47]Cephalopod ontology project https://github.com/obophenotype/cephalopod-ontology
• [48]Chen C-K, Mungall CJ, Gkoutos GV, Doelken SC, Köhler S, Ruef BJ, Smith C, Westerfield M, Robinson PN, Lewis SE, Schofield PN, Smedley D: MouseFinder: candidate disease genes from mouse phenotype data. Hum Mutat 2012, 33:858-866.
• [49]Doelken SC, Köhler S, Mungall CJ, Gkoutos GV, Ruef BJ, Smith C, Smedley D, Bauer S, Klopocki E, Schofield PN, Westerfield M, Robinson PN, Lewis SE: Phenotypic overlap in the contribution of individual genes to CNV pathogenicity revealed by cross-species computational analysis of single-gene mutations in humans, mice and zebrafish. Dis Model Mech 2013, 6:358-372.
• [50]Robinson P, Köhler S, Oellrich A, Wang K, Mungall C, Lewis SE, Washington N, Bauer S, Seelow DS, Krawitz P, Gilissen C, Haendel M, Smedley D: Improved exome prioritization of disease genes through cross species phenotype comparison. Genome Res 2013. http://www.genome.org/cgi/doi/10.1101/gr.160325.113
• [51]Smedley D, Oellrich A, Köhler S, Ruef B, Westerfield M, Robinson P, Lewis S, Mungall C: PhenoDigm: analyzing curated annotations to associate animal models with human diseases. Database (Oxford) 2013, 2013:bat025.
• [52]Day-Richter J, Harris MA, Haendel M, Lewis S, Group GOO-EW: OBO-Edit--an ontology editor for biologists. Bioinformatics 2007, 23:2198-2200.
• [53]Mungall C, Dietze H, Carbon S, Ireland A, Bauer S, Lewis S: Continuous Integration of Open Biological Ontology Libraries. Bio-Ontologies 2012. http://bio-ontologies.knowledgeblog.org/405
• [54]Cui H: CharaParser for fine-grained semantic annotation of organism morphological descriptions. J Am Soc Inf Sci Technol 2012, 63:738-754.
• [55]Image depiction Protégé plugin https://github.com/balhoff/image-depictions-view