Skeletal System Research Papers

1. Analysis of Existing Anatomy Ontologies

To build a common representation of skeletal anatomy, we surveyed existing representations in the vertebrate subgroup ontologies (Table 1) to determine the various ways that each had classified skeletal elements and to leverage existing work. Some of the most common issues, including varied representations, found in our examination of the anatomy ontologies were as follows: 1) The representation of bone as an organ, i.e., a skeletal element, and bone as a tissue were conflated as was cartilage as an organ and cartilage as a tissue. In the amphibian (AAO), teleost fish (TAO), the frog Xenopus (XAO), and zebrafish (ZFA) anatomy ontologies, for example, the single class ‘bone’ was a type of tissue and was used to classify skeletal elements rather than tissue types. 2) The upper-level skeletal classifications did not relate the multiple organizational levels of the skeletal system to each other. For example, ‘osteocyte,’ a cell type that produces mineralized bone matrix within bone tissue, was not related to ‘bone tissue’ in any of the vertebrate anatomy ontologies. 3) Developmental processes of the skeleton were poorly represented. Many skeletal terms can be defined biologically by the developmental processes producing them, but this was not reflected in the existing anatomy ontologies. For example, endochondral bones were not formally related to the process whereby bone tissue replaces cartilage tissue other than by the fact that they are called endochondral, which presumes the process of endochondral ossification. 4) The multiple relationships to composition and developmental differentia were not well or consistently represented across the ontologies. For example, ‘cartilage element’ has_part ‘cartilage tissue’ and ‘cartilage element’ develops_from ‘chondrogenic condensation’ were not asserted in any of the vertebrate ontologies.

Following the analysis of existing anatomy ontologies and skeletal classification schemes, we began development of the VSAO by focusing on the properties of skeletal anatomical entities. We used CARO as the upper ontology from which to subclass the VSAO terms. CARO provides a high level classification of anatomical entities, such as cells, tissues, and organs, to link together the different levels of anatomical granularity. Because it is also used by many of the existing anatomy ontologies, it was a natural choice as an upper ontology for the VSAO. We evaluated the Cell Ontology (CL) as a source of cell types from which to link the VSAO. We added new skeletal cell types to it and redefined existing types as appropriate (see section 2.1). To represent the processes involved in skeletal system development, we used terms from the GO Biological Process ontology. For example, VSAO terms are related to GO terms for skeletal development processes (e.g., VSAO: ‘endochondral element’ participates_in GO: ‘endochondral ossification’). We proposed six new GO terms that were subsequently added to the GO (‘direct ossification’, ‘intratendinous ossification’, ‘ligamentous ossification’, ‘metaplastic ossification’, ‘perichondral ossification’, and ‘replacement ossification’), and we provided improvements to definitions for others (‘endochondral ossification’, ‘intramembranous ossification’, ‘ossification involved in bone remodeling’, and ‘osteoblast differentiation’). Several existing multispecies anatomy ontologies also contain skeletal types. These include Uberon [29], which has a broader focus in representing structures in all anatomical systems for metazoans, and the Vertebrate Homologous Organ Groups ontology (vHOG) [37], which contains terms based on homologous organ groupings. Future incorporation of the VSAO and vHOG into Uberon will provide an integrated representation of skeletal anatomy for vertebrates across ontologies.

2. Classifying Skeletal Anatomy According to Multiple Criteria

In developing the VSAO, we focused on enumerating the essential characteristics (e.g., composition, structure, development) of the components of the skeletal system (e.g., cells, tissues, structures). To avoid errors and omissions (see below and Methods), we automated the task of classification (computing inferred subclass relationships) for bone and cartilage terms by using the OBO-Edit reasoner. We first partitioned skeletal anatomy into four categories based on level of anatomical granularity, from cell types up to organism parts, and made these child concepts of CARO classes (Figure 1). These categories were ‘cell’, ‘skeletal tissue’, ‘skeletal element’, and ‘skeletal subdivision’. We then classified terms based on several axes of classification, reflecting the different ways that biologists describe anatomy, including cell and/or tissue composition, structure, position, biological process, function, and development.

Figure 1. Four high-level classes of skeletal anatomy (‘cell’, ‘skeletal tissue’, ‘skeletal element’, ‘skeletal subdivision’) and their children based on anatomical granularity.

Cell terms (CL) are shown in yellow fill, tissue terms in grey fill, skeletal element terms in blue fill, and skeletal subdivision terms in green fill. Parent classes from CARO in red font. Alligator mississippiensis sectioned maxilla (∼day 27 in ovo; Ferguson stage 19) stained with Mallory's trichrome (A); midsagittally sectioned embryonic head (day 45 in ovo; Ferguson stage 23) in lateral (B) and saggital (C) view, double stained whole-mount (alizarin red and alcian blue).

https://doi.org/10.1371/journal.pone.0051070.g001

2.1 Cells of the skeletal system.

Accurate representation of cell types is important to define skeletal tissue types, especially where intermediate tissue types are concerned. To enable cross-species inquiry regarding cell type contributions to skeletal development, differences in gene expression, and phenotypic diversity, we related terms in the VSAO to cell terms from the CL. However, for applicability across vertebrates and to relate cells to tissue types, we broadened existing cell term definitions. We also added both new cell types and new developmental relations between new and existing cell types to represent the full diversity of cell types across vertebrates and developmental stages. In the CL, we proposed new definitions for 13 existing skeletogenic cell types, proposed 18 new cell types along with definitions (e.g., ‘skeletogenic cell’, ‘chordoblast’, and ‘preameloblast’), and made eight relationships to specific tissue types. For example, the definition of ‘chondroblast’ in CL was formerly “An immature cartilage-producing cell found in growing cartilage.” Based on our agreed-upon logical differentiae for this cell type, we refined the definition to read “Skeletogenic cell that is typically non-terminally differentiated, secretes an avascular, GAG rich matrix; is not buried in cartilage tissue matrix, retains the ability to divide, located adjacent to cartilage tissue (including within the perichondrium), and develops from prechondroblast (and thus prechondrogenic) cell.” We added relationships from cells to other cells, cellular condensations, and skeletal tissues based on their composition, location, development, and histology (Figure 2), for example:

‘chondroblast’ is_a ‘connective tissue cell’.

‘chondroblast’ develops_from some ‘prechondroblast’.

‘chondroblast’ produces some ‘cartilage tissue’.

‘chondroblast’ produces some ‘avascular GAG-rich matrix’.

Logically, these relationships extend to every individual cell of a cell type; for example, every chondroblast produces some cartilage tissue. It is important to note that these logically specified relations allow computation across different levels of granularity and via different axes of classification. This was our central motivation for developing an ontology.

2.2 Skeletal tissue.

‘skeletal tissue’: A specialized form of connective tissue in which the extracellular matrix is firm, providing the tissue with resilience, and/or mineralized and that functions in mechanical and structural support.

Although all of the vertebrate anatomy ontologies recognized some skeletal tissues as tissues, such as ‘bone tissue’ and ‘cartilage tissue’, other tissues were categorized incorrectly. Specifically, enamel and dentine were types of ‘portion of organism substance’ in ZFA and TAO, ‘portion of body substance’ in the human Foundational Model of Anatomy ontology (FMA) [38], and ‘body fluid or substance’ in the MA. Enamel and dentine, and related intermediate tissues such as enameloid and osteodentine, however, are skeletal tissues [39] and we added these to the VSAO as subtypes of ‘odontoid tissue’ (Figure 3). The component vertebrate anatomy ontologies (AAO, TAO, XAO, ZFA) also classified ‘cartilage’ and ‘bone’ as subtypes of ‘connective tissue’ (Figure 4a). To correct this, ‘cartilage element’ and ‘cartilage tissue’ are now separate terms in the VSAO, and subtypes of ‘cartilage tissue’ now include tissue types such as ‘hyaline cartilage tissue’, ‘fibrocartilage’, and ‘secondary cartilage tissue’ (Figure 3). Other newly added types of skeletal tissue in the VSAO include ‘mineralized tissue’, ‘odontoid tissue’, and intermediate tissues such as ‘chondroid tissue’ (Figure 3). The characteristics that distinguish these tissue types has been outlined [40], and this is represented in the VSAO’s tissue hierarchy (see section 2.3 and Figure 3). As described above, although tissues are often defined by their constituent cell types they can also be defined in terms of the extracellular materials they secrete, the developmental processes in which they participate, and the skeletal elements that they comprise.

Figure 3. Some skeletal tissues in the VSAO and selected relationships to other tissues, cells, and skeletal elements.

CL terms are shown in yellow fill, tissue terms in grey fill, skeletal element terms in blue fill, and skeletal subdivision terms in green fill.

https://doi.org/10.1371/journal.pone.0051070.g003

Skeletal tissue types not universal to vertebrates can be connected to the VSAO through taxon-specific anatomy ontologies. For example, the human anatomy ontology (FMA) includes ‘acellular cementum’ which is present only in mammals and crocodiles [40]. As a type of odontoid tissue, it could be linked to the VSAO in the future within a broader scope ontology such as the Uberon.

2.3 Skeletal elements.

‘skeletal element’: Organ entity that is typically involved in mechanical support and may have different skeletal tissue compositions at different stages.

‘Bone’ is the most common concept associated with the skeletal system. However, in common usage, this term may refer to either a vertebrate tissue type (bone tissue) or an individuated skeletal element such as the frontal bone. Likewise, in anatomy ontologies, skeletal elements have been represented as types of organs or, incorrectly, as types of tissues. For example, the AAO, TAO, XAO, and ZFA classified ‘bone’ as a type of ‘tissue’ (Figure 4a). The FMA and MA, however, distinguished between ‘bone tissue’ and ‘bone organ’. Similar to conflation of different concepts of bone, most vertebrate ontologies failed to distinguish cartilage tissue from cartilage elements.

Figure 4. Representation of the skeleton in vertebrate anatomy ontologies.

The vertebrate skeleton can be partitioned according to many different criteria – and it had been by the different groups (Table 1) that developed anatomy ontologies. For example (A), ‘bone’ had been treated as a type of tissue by all except the MA, who also related it to the concept of ‘bone organ’. In the VSAO (B), the concepts of bone tissue and bone element were disentangled, named and defined. Individual bone elements were related to their tissue and cell components as well as developmental processes. From these links one can reason that, e.g., the ‘femur’ is part_of ‘endoskeleton’, develops_from ‘cartilage element’, and participates_in the process of ‘endochondral ossification’, whereas the ‘frontal bone’ is part_of ‘dermal skeleton’ and participates_in the process of ‘direct ossification’. Image on left shows chondrocytes embedded in a bone matrix developed from periosteum of fractured chick dermal bone. Image on right shows a late gestational stage mouse embryo stained with alcian blue and alizarin red. CL term is shown in yellow fill, tissue terms in grey fill, skeletal element terms in blue fill, and skeletal subdivision terms in green fill. Parent classes from CARO are in red font, GO terms in green font, TAO terms in blue font, and VSAO terms in black font.

https://doi.org/10.1371/journal.pone.0051070.g004

VSAO contains the term ‘skeletal element’, which is used in the comparative literature to refer to individual bone or cartilage elements. Individual bones and cartilages are classified in VSAO as ‘skeletal elements’, which are types of ‘organ’ in CARO. We further created the class ‘cartilage element’ for skeletal elements that are composed of ‘cartilage tissue’ and ‘bone element’ for skeletal elements composed of ‘bone tissue’. The crucial part of the CARO definition for ‘organ’ (CARO: ‘compound organ’) is that they are distinct structural units demarcated by bona fide boundaries. By distinguishing bone elements from bone tissues there is flexibility to represent the variety of tissue compositions of different elements in the VSAO. VSAO includes terms for a few skeletal elements that are common to all vertebrates, for example, ‘vertebral element’ [41]. Other individual skeletal element terms (e.g., ‘anocleithrum’) can be linked to VSAO terms based on research requirements.

Skeletal elements have part_of relationships to skeletal subdivisions (see 2.4 below) that are based on position. Parthood relationships are used in logical definitions to infer classification based on skeletal subdivisions. For example, ‘cartilage element’ is logically defined based on its part_of relationship to the ‘endoskeleton’.

Bone elements are classified according to developmental mode. ‘Membrane bone’ and its subtype ‘dermal bone’ both participates_in ‘intramembranous ossification’. ‘Endochondral bone’ has the inferred relationship participates_in ‘endochondral ossification’, a relationship inherited from its parent ‘endochondral element’. Teleost ‘frontal bone’ is a subtype of ‘dermal bone’, and from the ontology we can reason that it participates_in ‘intramembranous ossification’ (Figure 4b). By articulating these aspects of skeletal elements in relationships between terms, rather than only in a definition of a term, we gain the power to reason across both anatomy and processes for inquiries related to skeletal phenotypes.

2.4 Skeletal subdivisions.

‘skeletal subdivision’: Anatomical cluster consisting of the skeletal elements that are part of the skeleton.

Skeletal subdivisions in the VSAO include the organizational regions ‘appendicular skeleton’, ‘axial skeleton’, ‘cranial skeleton’, ‘integumentary skeleton’, and ‘postcranial axial skeleton’ (Figure 5). The VSAO also contains skeletal subdivision terms based on developmental origin, such as ‘dermal skeleton’, which is defined based on its component entities developing through direct ossification, or the ‘endoskeleton’, which is defined as: “Skeletal subdivision that undergoes indirect development and includes elements that develop as a replacement or substitution of other elements or tissues”.

Just as definitions of skeletal elements may not apply to all vertebrates, the set of skeletal elements that comprise a skeletal subdivision may differ among vertebrate taxa because of evolutionary changes in the development of the skeleton or because of differences in definition across different domains of biological knowledge. The endoskeleton, for example, includes cranial bones such as the intercalar; in teleost fishes, however, the intercalar does not develop from a cartilage precursor [42] but instead develops directly within a connective tissue membrane. Representing the intercalar in the VSAO as part_of the endoskeleton would not be appropriate because the part_of relationship must hold universally across all taxa. Although this taxonomically variable relationship could be directly specified in individual multispecies or single species anatomy ontologies, there are unlikely to be separate anatomy ontologies for all the taxa of concern. Because VSAO does not describe the taxonomic distribution of anatomy, one way that this variation could be represented is by creating post-compositions of an anatomy term with terms from a taxonomy ontology [12].

3. Logical definitions and automating term classification

Most of the skeletal branches of the various vertebrate anatomy ontologies (Table 1) contained some level of asserted multiple inheritance. Asserted multiple inheritance, in which a term has more than one is_a parent (superclass) asserted, can be difficult to maintain in an ontology and can lead both to errors in reasoning [8] and to errors whereby not all children adhere to their parental definitions. Often, however, multiple is_a parents reflect a need for biologists to classify entities along multiple conceptual axes. For example, a bone may exhibit two different modes of development within the same organism, as in the tripus, a bone of the axial skeleton in otophysan fishes that develops by both endochondral and intramembranous ossification. ‘Tripus’ would therefore be classified as both a type of ‘endochondral bone’ and ‘membrane bone’ (Figure 6). Similarly, a structure can be classified according to both its developmental and structural attributes. For example, ‘tripus’ is also a type of ‘Weberian ossicle’ because it is a skeletal element that is associated with the Weberian apparatus. Because of these relationships, one could search for the tripus by querying for the structures that participates_in ‘endochondral ossification’ or ‘intramembranous ossification’.

Figure 6. Representation of a skeletal element with multiple classification criteria.

The ‘tripus’ is directly asserted (solid lines) to be a type of ‘endochondral bone’, part_of the ‘Weberian ossicle set’, part_of ‘vertebra 3′ and to form through the process of (‘participates_in’) ‘intramembranous ossification’. The reasoner infers (dotted lines) the tripus to be a type of ‘membrane bone’ and a ‘Weberian ossicle’, and infers it to participate in ‘endochondral ossification’. Skeletal element terms are shown in blue fill, skeletal subdivision term in green fill, TAO terms in blue font, VSAO terms in black font, and GO process terms in green font.

https://doi.org/10.1371/journal.pone.0051070.g006

A logically preferable way to accommodate multiple inheritances is to infer the polyhierarchy by using logical definitions in which terms are defined by relationships to other terms such that their classification can be automated by a reasoner. A reasoner is a software tool that computationally infers relationships implied by those asserted, including class subsumption relationships. The logical definition of a class constitutes the necessary and sufficient conditions for class membership. In the VSAO, these are of the form ‘An X is a G that D’, where X is the defined class, G is its asserted superclass and D is the set of discriminating characteristic(s) that distinguishes instances of X from instances of other subclasses of G [8], [9]. In the tripus example (Figure 6), rather than subclassify ‘tripus’ with three asserted is_a relationships to ‘endochondral bone’, ‘membrane bone’, and ‘Weberian ossicle’, we created logical definitions based on relationships to other terms (part_of ‘Weberian ossicle set’, part_of ‘vertebra 3′, participates_in ‘intramembranous ossification’; Figure 6). Based on these differentiae the reasoner added two implied is_a links (is_a ‘membrane bone’ and is_a ‘Weberian ossicle’). In VSAO, we created logical definitions for types of skeletal elements, which enables multiple classification schemes to be represented in VSAO via reasoning.

Alternatives to creating logical definitions include explicitly naming parts of elements according to development, such as ‘endochondral part of tripus’. This has the disadvantage of introducing terms in the ontology that are unfamiliar to users. A similar but yet more complex scheme could have been adopted for bones composed of multiple developmental types. For example, a class of bone could be introduced such as ‘mixed endochondral/intramembranous bone’ or ‘compound bone’ that would be the single parent for tripus. We decided not to use this scheme because we anticipate that users will search primarily on single developmental types rather than on a combined term.

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