An amphioxus Msx gene expressed predominantly in the dorsal neural tube

An important question in biology is why some animals are able to regenerate, whereas others are not. The basal chordate amphioxus is uniquely positioned to address the evolution of regeneration. We report here the high regeneration potential of the European amphioxus Branchiostoma lanceolatum. Adults regenerate both anterior and posterior structures, including neural tube, notochord, fin, and muscle. Development of a classifier based on tail regeneration profiles predicts the assignment of young and old adults to their own class with >94% accuracy. The process involves loss of differentiated characteristics, formation of an msx-expressing blastema, and neurogenesis. Moreover, regeneration is linked to the activation of satellite-like Pax3/7 progenitor cells, the extent of which declines with size and age. Our results provide a framework for understanding the evolution and diversity of regeneration mechanisms in vertebrates.invertebrate chordate-vertebrate transition | stem cells | cephalochordate R egeneration, as an evolutionary trait, is distributed widely and nonuniformly across the Metazoa; it is also highly variable in quality and structural specificity. Recently, there has been a resurgence of interest in the evolutionary distribution and basis of regeneration (1). A question of general interest is why certain lineages have lost or reduced regenerative capacity relative to their regeneration-competent sister taxa. In particular, the properties of CNS regeneration in more basal vertebrates may shed light on the reasons for reduced capacity in mammals and birds (2). Despite the plethora of hypotheses that attempt to explain the evolutionary significance of regenerative ability, the unresolved central issue is whether the ability to regenerate is adaptive or simply a byproduct of selection on other metabolic or developmental processes.Studies across phyla indicate that there is broad conservation of the developmental signaling pathways involved in regeneration (3), but the signals that initiate regeneration on injury and the downstream targets that they induce have proven more elusive. Moreover, the historical distinction between invertebrate-and vertebrate-type regeneration can make comparisons difficult. In planaria and Hydra, for example, the contribution of pluripotent stem cells has been the predominant focus of regeneration research. In contrast, among vertebrate models, studies have highlighted dedifferentiation of existing structures or the role of muscle satellite cells (3). Bridging the gap, ambulacrarian deuterostomes and urochordates show considerable regenerative capacity (1, 4-6) (Fig. 1A). However, their anatomy is not readily comparable with the vertebrate body plan, making it difficult to draw conclusions from such derived phyla. The origins and evolution of chordate regeneration mechanisms are, therefore, still unresolved.The cephalochordate amphioxus, the most basal living chordate (7), possesses many ancestral anatomical characters, whereas many derived vertebrate features, such as bona fi...

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“…4A). This finding differs from what is seen during embryogenesis in B. floridae, in which msx is not expressed in the tailbud (24).…”

Section: Amphioxus Adults Regenerate Anterior As Well As Posterior Stcontrasting

confidence: 99%

Vertebrate-like regeneration in the invertebrate chordate amphioxus

Somorjai

Garcia‐Fernàndez

et al. 2011

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

114

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“…In amphioxus, BMP, Notch, and Wnt signaling pathways are expressed in a similar pattern to those observed in vertebrates, consistent with them playing a conserved patterning role in the early ectoderm (Yu et al, 2007). In addition, homologues of neural plate border specifiers Msx, Zic, and Pax3/7 are found at the neural plate border of amphioxus in the late gastrula/early neurula (Gostling and Shimeld, 2003;Holland et al, 1999;Holland et al, 1996;Sharman et al, 1999). These findings suggest that initial formation of the neural plate border may occur via a mechanisms conserved between cephalochordates and vertebrates.…”

Section: Nonvertebrate Chordatesmentioning

confidence: 61%

Evolution of the neural crest viewed from a gene regulatory perspective

Sauka‐Spengler

Bronner‐Fraser

2008

Genesis

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Summary: Neural crest cells are a vertebrate innovation and form a wide variety of embryonic cell types as diverse as peripheral neurons and facial skeleton. They undergo complex migration and differentiation processes from their site of origin in the developing central nervous system to their final destinations in the periphery. In this review, we summarize recent data on the current formulation of a gene regulatory network underlying neural crest formation and its roots at the base of the vertebrate lineage. Analyzing neural crest formation from a gene regulatory viewpoint provides insights into both the developmental mechanisms and evolutionary origins of this vertebrate-specific cell type. genesis 46:673-682,

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“…This may therefore reflect an ancestral function for these genes in central nervous system (CNS) patterning. Indeed, the single Msx gene of Amphioxus is expressed exclusively at this site (Sharman et al, 1999). In Drosophila, Msh, the Msx ortholog, is required for the specification of lateral neuroblasts, which can be considered as the homologs of the dorsal neurons in vertebrates (Cornell and von Ohlen, 2000).…”

Section: Introductionmentioning

confidence: 99%

Msx1is required for dorsal diencephalon patterning

et al. 2003

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The dorsal midline of the neural tube has recently emerged as a major signaling center for dorsoventral patterning. Msx genes are expressed at the dorsal midline, although their function at this site remains unknown. Using Msx1nlacZ mutant mice, we show that the normal expression domain of Msx1 is interrupted in the pretectum of mutant embryos. Morphological and gene expression data further indicate that a functional midline is not maintained along the whole prosomere 1 in Msx1 mutant mice. This results in the downregulation of genes expressed laterally to the midline in prosomere 1, confirming the importance of the midline as a signaling center. Wnt1 is essential for dorsoventral patterning of the neural tube. In the Msx1 mutant, Wnt1 is downregulated before the midline disappears, suggesting that its expression depends on Msx1. Furthermore, electroporation in the chick embryo demonstrates that Msx1 can induce Wnt1 expression in the diencephalon neuroepithelium and in the lateral ectoderm. In double Msx1/Msx2 mutants, Wnt1 expression is completely abolished at the dorsal midline of the diencephalon and rostral mesencephalon. This indicates that Msx genes may regulate Wnt1 expression at the dorsal midline of the neural tube. Based on these results, we propose a model in which Msx genes are intermediary between Bmp and Wnt at this site.

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An amphioxus Msx gene expressed predominantly in the dorsal neural tube

Cited by 92 publications

References 19 publications

Vertebrate-like regeneration in the invertebrate chordate amphioxus

Vertebrate-like regeneration in the invertebrate chordate amphioxus

Evolution of the neural crest viewed from a gene regulatory perspective

Msx1is required for dorsal diencephalon patterning

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