Ultrastructure of cartilage from young adult sea lamprey, <i>Petromyzon marinus</i> L: A new type of vertebrate cartilage

Wright, Glenda M.; Youson, John H.

doi:10.1002/aja.1001670106

Cited by 44 publications

(19 citation statements)

References 21 publications

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“…It was demonstrated that fibrillar collagen is included as a minor component and that the SoxD and SoxE genes are coexpressed in the chondrocytes (Zhang and Cohn, 2006; Zhang et al, 2006a,b; Ohtani et al, 2008; Ota and Kuratani, 2010). However, on the other hand, the agnathan cartilage is mainly composed of elastin‐like fibers, including lamprin and myxnine (Wright and Youson, '83; Wright et al, '84; Robson et al, '93, '97). Thus, the matrix composition of the agnathan cartilage is unique in the vertebrates.…”

Section: Discussionmentioning

confidence: 99%

Regeneration of amphioxus oral cirri and its skeletal rods: implications for the origin of the vertebrate skeleton

Kaneto

Wada

2011

J Exp Zool Pt B

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The oral cirri of amphioxus function as the first filter during feeding by eliminating unwanted large or noxious particulates. In this study, we were able to regenerate cirri following artificial amputation. This is the first firm observation of regeneration in amphioxus. Using this regeneration system, we studied skeletogenesis of the cellular skeleton of amphioxus oral cirri. During regeneration, the skeletal cells showed expression of fibrillar collagen and SoxE genes. These observations suggest that an evolutionarily conserved genetic regulatory system is involved in amphioxus cirrus and vertebrate cartilage skeletogenesis. In addition, Runx and SPARC/osteonectin expression were observed in regenerating cirral skeletal cells, indicating that cirral skeletogenesis is similar to vertebrate osteogenesis. We propose that the common ancestors of chordates possessed a genetic regulatory system that was the prototype of chondrogenesis and osteogenesis in vertebrates. Genome duplications caused divergence of this genetic regulatory system resulting in the emergence of cartilage and mineralized bone. The development of the vertebrate skeleton is an example of the functional segregation and subsequent recruitment of unique genetic materials that may account for the evolutionary diversification of novel cell types.

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Section: Discussionmentioning

confidence: 99%

Regeneration of amphioxus oral cirri and its skeletal rods: implications for the origin of the vertebrate skeleton

Kaneto

Wada

2011

J Exp Zool Pt B

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“…Cartilage based on type II collagen has long been considered a unifying character of gnathostomes that separates them from lampreys and hagfishes (1,19). Recently, we reported that lampreys possess two Col2␣1 orthologs and that adult lamprey cartilage is composed of Col2␣1 protein (2).…”

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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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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“…At least part of the neurocranium, and some of the branchial arches, but apparently not the mucocartilage, show contributions from the neural crest during embryogenesis (Langille and Hall 1988;Martin et al 2009). Instead, the ECM is composed of a network of 15-40 nm diameter, randomly arranged, branched fibrils (Wright and Youson 1983). 4.11).…”

Section: Cranial Skeletonmentioning

confidence: 99%

“…4.11). Verhoeff's stain implies an elastic nature to the lamprey ECM but the amino acid composition varies from elastin protein, leading to the name of lamprin for the major ECM protein of lamprey cartilage (Wright and Youson 1983). Fine structural studies show that the fibrous component of the extracellular matrix (ECM) of annular, piston, cranial, and dorsal plate cartilages is not collagen.…”

Section: Cranial Skeletonmentioning

confidence: 99%

Lampreys: Biology, Conservation and Control

Docker¹

2015

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Ultrastructure of cartilage from young adult sea lamprey, Petromyzon marinus L: A new type of vertebrate cartilage

Cited by 44 publications

References 21 publications

Regeneration of amphioxus oral cirri and its skeletal rods: implications for the origin of the vertebrate skeleton

Regeneration of amphioxus oral cirri and its skeletal rods: implications for the origin of the vertebrate skeleton

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

Lampreys: Biology, Conservation and Control

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