Cartilage is a metazoan tissue; integrating data from nonvertebrate sources

Cole, Alison G.; Hall, Brian K.

doi:10.1111/j.0001-7272.2004.00159.x

Cited by 46 publications

(38 citation statements)

References 64 publications

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“…It has been suggested that the notochord may represent a primitive form of cartilage, based on their many shared structural, cellular, and molecular properties, and that vertebrate chondrocytes may have evolved from notochordal cells (21,22). In gnathostomes, the notochord and͞or notochordal sheath expresses most of the vertebrate clade A fibrillar collagen genes (15,(23)(24)(25).…”

Section: Discussionmentioning

confidence: 99%

“…We suggest that duplication and divergence of the clade A collagen genes in stem-group vertebrates may have facilitated the evolutionary diversification of chondrocytes and notochordal cells. This hypothesis deals specifically with the origin of vertebrate chondrocytes, and it is important to note that cartilage is also found in several invertebrates, including cephalopods, snails, and horseshoe crabs (1,21). Future work on the molecular basis of invertebrate chondrogenesis should reveal whether fibrillar collagens also were used in these independent evolutionary events.…”

Section: Discussionmentioning

confidence: 99%

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Hagfish and lancelet fibrillar collagens reveal that type II collagen-based cartilage evolved in stem vertebrates

Zhang

Cohn

2006

Proc. Natl. Acad. Sci. U.S.A.

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The origin of vertebrates was defined by evolution of a skeleton; however, little is known about the developmental mechanisms responsible for this landmark evolutionary innovation. In jawed vertebrates, cartilage matrix consists predominantly of type II collagen (Col2␣1), whereas that of jawless fishes has long been thought to be noncollagenous. We recently showed that Col2␣1 is present in lamprey cartilage, indicating that type II collagen-based cartilage evolved earlier than previously recognized. Here, we investigate the origin of vertebrate cartilage, and we report that hagfishes, the sister group to lampreys, also have Col2␣1-based cartilage, suggesting its presence in the common ancestor of crown-group vertebrates. We go on to show that lancelets, a sister group to vertebrates, possess an ancestral clade A fibrillar collagen (ColA) gene that is expressed in the notochord. Together, these results suggest that duplication and diversification of ColA genes at the chordate-vertebrate transition may underlie the evolutionary origin of vertebrate skeletal tissues.development ͉ gene duplication ͉ skeleton evolution ͉ chordate ͉ notochord T he phylogenetic relationships of the vertebrates were established largely based on anatomical characters, particularly those of the skeleton. The skeletons of jawed vertebrates (gnathostomes) are composed of cartilage and bone, which contain high levels of type II and type I collagen (Col2␣1 and Col1␣1͞2 protein, respectively). By contrast, the cartilaginous skeletons of lampreys and hagfishes, the only extant jawless fishes (agnathans), have been reported to be noncollagenous and to contain instead the elastin-like proteins lamprin and myxinin (1). This difference in the extracellular matrices of vertebrate skeletons led to the idea that type II collagen became the major structural component of gnathostome cartilage after the divergence of these two lineages (1). However, this view was challenged by our recent report that lampreys have two Col2␣1 orthologs and that both genes are expressed during chondrogenesis. Adult lamprey cartilage was also shown to be rich in Col2␣1 protein (2). Furthermore, we identified a lamprey ortholog of Sox9, a direct transcriptional regulator of Col2␣1 in gnathostomes, and we showed that it is coexpressed with Col2␣1 (2). This discovery revealed that the genetic pathway for vertebrate chondrogenesis predated the divergence of lampreys and gnathostomes, although precisely how early this character arose is unknown. Here, we investigate the evolutionary origin of Col2␣1-based cartilage by expanding our analysis to the most inclusive clade of vertebrates, which includes the hagfishes, and to a sister group to the vertebrates, the lancelets (3, 4). We report that hagfishes also have Col2␣1-based cartilage, suggesting that this type of cartilage was present in common ancestor of all crown vertebrates. Our analysis of lancelets revealed the presence of an ancestral clade A fibrillar collagen (ColA) gene that is expressed in the notochord. Thus, during th...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Hagfish and lancelet fibrillar collagens reveal that type II collagen-based cartilage evolved in stem vertebrates

Zhang

Cohn

2006

Proc. Natl. Acad. Sci. U.S.A.

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“…In fact within the invertebrates that have been investigated, a spectrum of histological tissues that parallels the diversity found within modern fishes is found (Cole and Hall, 2004b). Cartilages found within Cephalopod mollusks are remarkably similar to vertebrate hyaline cartilage at a histological level (Cole and Hall, 2004a). On close inspection, one can find one significant difference between vertebrate hyaline cartilage and that found within the cephalopod -the extra-cellular matrix of the cephalopod, in addition to the chondrocytes, is riddled with small canals -through which pass thin extensions of chondrocyte processes which retain connections between one another (Bairati et al, 1998;Leone et al, 2004;Cole and Hall, 2009).…”

Section: Ag Colementioning

confidence: 89%

“…The affinity of the notochord to cartilage remains debatable; Cole and Hall (2004a) argue for its inclusion as a vesicular cartilage, whereas Witten et al (2010) consider the notochord as "cartilage-related" (See Hall, 2005, for further discussion). Chondrocytes, or "chondrocyte-like" cells are predominant Fig.…”

Section: Ag Colementioning

confidence: 99%

“…Cartilage can be defined generally as an internal cellular support tissue high in fibrous protein and mucopolysaccharide content (see Cole and Hall, 2004a, for discussion). In mammals 3 classic types of cartilage have been histologically identified based upon the relative contribution and distribution of fibers within the extracellular matrix: hyaline cartilage is the typical cartilage that is generally referred to when one thinks of cartilage.…”

Section: Introductionmentioning

confidence: 99%

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A review of diversity in the evolution and development of cartilage: the search for the origin of the chondrocyte

2011

eCM

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Mammalian cartilage is a complex and developmentally important tissue type. Outside the mammalian lineage, cartilage may persist as an adult tissue, which shows a much wider diversity of histological structure. Tissues similar to vertebrate cartilage are also found within multiple invertebrate lineages, including mollusks, arthropods, and polychaetes, however the relationship of these tissues to vertebrate cartilage is unknown. Detailed molecular analysis of these invertebrate tissues is necessary to assess the degree of homology, if any, of cartilage throughout the metazoans. The purpose of the following review is to introduce readers to this diversity of cartilage and to synthesize the known genetic interactions that give rise to vertebrate cartilage into the format of a gene regulatory network (GRN). This chondrogenesis GRN highlights a large number of transcription factors known to be expressed during chondrogenesis, whose role in this process has yet to be elucidated. Verification and expansion of this initial GRN will assist in the identification of the core set of the genetic interactions necessary for the specification of the vertebrate chondrocyte. This is the necessary first step in allowing detailed comparison of the molecular signature of vertebrate chondrocytes with that of invertebrates with the ultimate goal of understanding the evolutionary origin of this important skeletal cell type.

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Development of the vertebra and fin skeleton in the lamprey and its implications for the homology of vertebrate vertebrae

Kariyayama,

Gogoleva,

Harada

et al. 2023

Developmental Dynamics

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BackgroundAlthough vertebrae are the defining character of vertebrates, they are found only in rudimentary form in extant agnathans. In addition, the vertebrae of agnathans possess several unique features, such as elastin‐like molecules as the main matrix component and late (post‐metamorphosis) differentiation of lamprey vertebrae. In this study, by tracing the developmental process of vertebrae in lamprey, we examined the homology of vertebrae between lampreys and gnathostomes.ResultsWe found that the lamprey somite is first subdivided mediolaterally, with myotome cells differentiating medially and non‐myotome cells emerging laterally. Subsequently, collagen‐positive non‐myotome cells surround the myotome. This pattern of somitogenesis is rather similar to that in amphioxi and sheds doubt on the presence of a sclerotome, in terms of mesenchyme cells induced by a signal from the notochord, in lamprey. Further tracing of non‐myotome cell development revealed that fin cartilage develops in ammocoete larvae approximately 35 mm in body length. The development of the fin cartilage occurs much earlier than that of the vertebra whose development proceeds during metamorphosis.ConclusionWe propose that the homology of vertebrae between agnathans and gnathostomes should be discussed carefully, because the developmental process of the lamprey vertebra is different from that of gnathostomes.

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Cartilage is a metazoan tissue; integrating data from nonvertebrate sources

Cited by 46 publications

References 64 publications

Hagfish and lancelet fibrillar collagens reveal that type II collagen-based cartilage evolved in stem vertebrates

Hagfish and lancelet fibrillar collagens reveal that type II collagen-based cartilage evolved in stem vertebrates

A review of diversity in the evolution and development of cartilage: the search for the origin of the chondrocyte

Development of the vertebra and fin skeleton in the lamprey and its implications for the homology of vertebrate vertebrae

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