Lamprey lecticans link new vertebrate genes to the origin and elaboration of vertebrate tissues

Root, Zachary D.; Jandzík, Dávid; Allen, Cara; Brewer, Margaux; Romášek, Marek; Square, Tyler A.; Medeiros, Daniel Meulemans

doi:10.1016/j.ydbio.2021.03.020

Cited by 7 publications

(22 citation statements)

References 106 publications

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“…Additionally, we have learned more about the differences in gene expression and histology between the gnathostome-like hyaline cartilage of the larval trabeculae and branchial skeleton and that of mucocartilage, the avascular connective tissue scattered throughout the anterior head skeleton that has several characteristics of articular cartilage ( Johnels, 1948 ; Cerny et al, 2010 ; Cattell et al, 2011 ; Yao et al, 2011 ; Root et al, 2021b ). Recent work has shown that the lamprey larval skeleton expresses multiple Lectican homologs in distinct skeletal populations ( Root et al, 2021a ), an interesting feature which supports previous hypotheses that the lamprey larval skeleton may have as many as six cartilage types ( Cattell et al, 2011 ).…”

Section: Discussionsupporting

confidence: 76%

“…We chose Tahara stages 26 through 28 ( Yutaka, 1988 ), corresponding to mesenchymal condensations in the oropharyngeal skeleton and the differentiation of somitic components. To confirm our observations of expression in the musculoskeletal system, we compared our results to previous reports of the lamprey musculoskeletal system, such as the developing lamprey musculature ( Kusakabe et al, 2004 ; Kusakabe and Kuratani, 2005 ; Kusakabe et al, 2011 ), hyaline cartilage ( Root et al, 2021a ) [ Figure S7 ], and mucocartilage ( Cerny et al, 2010 ; Root et al, 2021a ; Root et al, 2021b ).…”

Section: Resultssupporting

confidence: 58%

“…Although the metazoan muscular system’s origins are thought to be shared and innovated upon an ancestral contractile machinery ( Seipel and Schmid, 2005 ; Steinmetz et al, 2012 ), vertebrates have duplicated actin and myosin heavy chain genes which are differentially expressed across smooth and striated muscle populations ( Vandekerckhove and Weber, 1984 ; Mugue and Ozernyuk, 2006 ; Warkman et al, 2012 ; Witjes et al, 2019 ), forming the vertebrate-unique cardiac muscle and multi-layered skeletal muscles ( Zoghbi et al, 2008 ; Shaffer and Gillis, 2010 ; Luther and Squire, 2014 ). Likewise, cartilage may be a connective tissue shared by bilaterians ( Tarazona et al, 2016 ), but vertebrates have formed unique ECM-rich hyaline cartilages characterized by lectican proteins, all of which are likely vertebrate-specific duplications ( Root et al, 2021a ). Although tendons connect muscle and skeleton in both invertebrates and vertebrates, they are structurally different in both groups and have different developmental origins ( Schweitzer et al, 2010 ), vertebrate tendons are often heterogeneous in morphology, but share their expression of the vertebrate-specific small interstitial leucine-rich repeat proteoglycans (SLRP’s) like fibromodulin, biglycan, decorin, and lumican ( Yoon and Halper, 2005 ).…”

Section: Introductionmentioning

confidence: 99%

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A Comprehensive Analysis of Fibrillar Collagens in Lamprey Suggests a Conserved Role in Vertebrate Musculoskeletal Evolution

Root

Allen

Gould

et al. 2022

Front. Cell Dev. Biol.

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Vertebrates have distinct tissues which are not present in invertebrate chordates nor other metazoans. The rise of these tissues also coincided with at least one round of whole-genome duplication as well as a suite of lineage-specific segmental duplications. Understanding whether novel genes lead to the origin and diversification of novel cell types, therefore, is of great importance in vertebrate evolution. Here we were particularly interested in the evolution of the vertebrate musculoskeletal system, the muscles and connective tissues that support a diversity of body plans. A major component of the musculoskeletal extracellular matrix (ECM) is fibrillar collagens, a gene family which has been greatly expanded upon in vertebrates. We thus asked whether the repertoire of fibrillar collagens in vertebrates reflects differences in the musculoskeletal system. To test this, we explored the diversity of fibrillar collagens in lamprey, a jawless vertebrate which diverged from jawed vertebrates (gnathostomes) more than five hundred million years ago and has undergone its own gene duplications. Some of the principal components of vertebrate hyaline cartilage are the fibrillar collagens type II and XI, but their presence in cartilage development across all vertebrate taxa has been disputed. We particularly emphasized the characterization of genes in the lamprey hyaline cartilage, testing if its collagen repertoire was similar to that in gnathostomes. Overall, we discovered thirteen fibrillar collagens from all known gene subfamilies in lamprey and were able to identify several lineage-specific duplications. We found that, while the collagen loci have undergone rearrangement, the Clade A genes have remained linked with the hox clusters, a phenomenon also seen in gnathostomes. While the lamprey muscular tissue was largely similar to that seen in gnathostomes, we saw considerable differences in the larval lamprey skeletal tissue, with distinct collagen combinations pertaining to different cartilage types. Our gene expression analyses were unable to identify type II collagen in the sea lamprey hyaline cartilage nor any other fibrillar collagen during chondrogenesis at the stages observed, meaning that sea lamprey likely no longer require these genes during early cartilage development. Our findings suggest that fibrillar collagens were multifunctional across the musculoskeletal system in the last common ancestor of vertebrates and have been largely conserved, but these genes alone cannot explain the origin of novel cell types.

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Section: Discussionsupporting

confidence: 76%

Section: Resultssupporting

confidence: 58%

Section: Introductionmentioning

confidence: 99%

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A Comprehensive Analysis of Fibrillar Collagens in Lamprey Suggests a Conserved Role in Vertebrate Musculoskeletal Evolution

Root

Allen

Gould

et al. 2022

Front. Cell Dev. Biol.

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“…However, the major archetypal domain structures of lectican proteins are present because the missed sequences are in the middle of the gene, which does not contain any conserved domains. As reported (Root et al, 2021), no lamprey lectican possessed the extra link domain seen in human and other mammalian ACANs, even using the full-length lectican genes predicted by NIH. However, the complement control protein (CCP) domain, which is reported missing in lectican A by Root et al (2021), appeared in its corresponding longer sequences of lamprey VCAN variants.…”

Section: Lamprey Genome Has Homologs Of Vertebrate Lecticansmentioning

confidence: 63%

“…No BCAN were annotated. However, the sequences of four lamprey lecticans were assembled recently from transcriptomic reads of t.26.5 embryos (Tahara, 1988) and late larval oral disc tissue (Root et al, 2021). Based on studies of phylogeny and genomic arrangement, it was concluded that lamprey lecticans lack clear one-to-one orthologies to gnathostome lecticans, and therefore, the lamprey lecticans were designated simply as''A'', ''B'', ''C'', and ''D''.…”

Section: Lamprey Lectican Family and Phylogenetic Analysismentioning

confidence: 99%

The Composition and Cellular Sources of CSPGs in the Glial Scar After Spinal Cord Injury in the Lamprey

Zhang

Jin

Rodemer

et al. 2022

Front. Mol. Neurosci.

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Axon regrowth after spinal cord injury (SCI) is inhibited by several types of inhibitory extracellular molecules in the central nervous system (CNS), including chondroitin sulfate proteoglycans (CSPGs), which also are components of perineuronal nets (PNNs). The axons of lampreys regenerate following SCI, even though their spinal cords contain CSPGs, and their neurons are enwrapped by PNNs. Previously, we showed that by 2 weeks after spinal cord transection in the lamprey, expression of CSPGs increased in the lesion site, and thereafter, decreased to pre-injury levels by 10 weeks. Enzymatic digestion of CSPGs in the lesion site with chondroitinase ABC (ChABC) enhanced axonal regeneration after SCI and reduced retrograde neuronal death. Lecticans (aggrecan, versican, neurocan, and brevican) are the major CSPG family in the CNS. Previously, we cloned a cDNA fragment that lies in the most conserved link-domain of the lamprey lecticans and found that lectican mRNAs are expressed widely in lamprey glia and neurons. Because of the lack of strict one-to-one orthology with the jawed vertebrate lecticans, the four lamprey lecticans were named simply A, B, C, and D. Using probes that distinguish these four lecticans, we now show that they all are expressed in glia and neurons but at different levels. Expression levels are relatively high in embryonic and early larval stages, gradually decrease, and are upregulated again in adults. Reductions of lecticans B and D are greater than those of A and C. Levels of mRNAs for lecticans B and D increased dramatically after SCI. Lectican D remained upregulated for at least 10 weeks. Multiple cells, including glia, neurons, ependymal cells and microglia/macrophages, expressed lectican mRNAs in the peripheral zone and lesion center after SCI. Thus, as in mammals, lamprey lecticans may be involved in axon guidance and neuroplasticity early in development. Moreover, neurons, glia, ependymal cells, and microglia/macrophages, are responsible for the increase in CSPGs during the formation of the glial scar after SCI.

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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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Lamprey lecticans link new vertebrate genes to the origin and elaboration of vertebrate tissues

Cited by 7 publications

References 106 publications

A Comprehensive Analysis of Fibrillar Collagens in Lamprey Suggests a Conserved Role in Vertebrate Musculoskeletal Evolution

A Comprehensive Analysis of Fibrillar Collagens in Lamprey Suggests a Conserved Role in Vertebrate Musculoskeletal Evolution

The Composition and Cellular Sources of CSPGs in the Glial Scar After Spinal Cord Injury in the Lamprey

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

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