The single AmphiTrk receptor highlights increased complexity of neurotrophin signalling in vertebrates and suggests an early role in developing sensory neuroepidermal cells

Benito‐Gutiérrez, Èlia; Näke, Christian; Llovera, Marta; Comella, Joan X.; Garcia‐Fernàndez, Jordi

doi:10.1242/dev.01803

Cited by 70 publications

(82 citation statements)

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“…1J-M) (Benito-Gutierrez et al, 2005a;Satoh et al, 2001); subsequently, at the mid-to lateneurula stage, many of these differentiating ESNs appear to delaminate from the ectoderm and invaginate into the subepidermal space to migrate towards the dorsal side of the neurula (Fig. 1N-Q) (Benito-Gutierrez et al, 2005b;Kaltenbach et al, 2009). At the late neurula to early larval stage, the ESNs re-insert into the epidermal ectoderm and send out axons to innervate the CNS (Kaltenbach et al, 2009), and many of these ESNs are immunoreactive to antibodies against the neurotransmitter -aminobutyric acid (GABA) (Fig.…”

Section: Introductionmentioning

confidence: 99%

“…1R-W) (Anadon et al, 1998). Using embryonic ontogeny and expression data for several homologs of placode marker genes, it has been speculated that these amphioxus ESNs are homologs of vertebrate placodederived neurons (Benito-Gutierrez et al, 2005a;Benito-Gutierrez et al, 2005b;Holland, 2005;Holland and Yu, 2002;Kaltenbach et al, 2009;Kozmik et al, 2007;Mazet et al, 2004;Meulemans and Bronner-Fraser, 2007;Rasmussen et al, 2007). However, the molecular mechanism controlling the specification of amphioxus ESNs remains unclear, and this situation has impeded our understanding of the relationship of these ESNs to the peripheral sensory neurons in other animals.…”

Section: Introductionmentioning

confidence: 99%

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BMP and Delta/Notch signaling control the development of amphioxus epidermal sensory neurons: insights into the evolution of the peripheral sensory system

Luo

2012

Development

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SUMMARYThe evolution of the nervous system has been a topic of great interest. To gain more insight into the evolution of the peripheral sensory system, we used the cephalochordate amphioxus. Amphioxus is a basal chordate that has a dorsal central nervous system (CNS) and a peripheral nervous system (PNS) comprising several types of epidermal sensory neurons (ESNs). Here, we show that a proneural basic helix-loop-helix gene (Ash) is co-expressed with the Delta ligand in ESN progenitor cells. Using pharmacological treatments, we demonstrate that Delta/Notch signaling is likely to be involved in the specification of amphioxus ESNs from their neighboring epidermal cells. We also show that BMP signaling functions upstream of Delta/Notch signaling to induce a ventral neurogenic domain. This patterning mechanism is highly similar to that of the peripheral sensory neurons in the protostome and vertebrate model animals, suggesting that they might share the same ancestry. Interestingly, when BMP signaling is globally elevated in amphioxus embryos, the distribution of ESNs expands to the entire epidermal ectoderm. These results suggest that by manipulating BMP signaling levels, a conserved neurogenesis circuit can be initiated at various locations in the epidermal ectoderm to generate peripheral sensory neurons in amphioxus embryos. We hypothesize that during chordate evolution, PNS progenitors might have been polarized to different positions in various chordate lineages owing to differential regulation of BMP signaling in the ectoderm.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

BMP and Delta/Notch signaling control the development of amphioxus epidermal sensory neurons: insights into the evolution of the peripheral sensory system

Luo

2012

Development

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“…Although most components of the gene networks involved in neural crest specification are expressed in the border of the amphioxus neural tube, in a similar pattern to vertebrates, no cell migration has been reported in amphioxus at these embryonic stages and locations (Barrallo-Gimeno and Nieto, 2006;Meulemans and Bronner-Fraser, 2004). Intriguingly, a population of cells in the amphioxus neurula shows migratory capabilities and may have the ability to perform epithelial/mesenchymal transition (Benito-Gutiérrez et al, 2005) That amphioxus is the best representative of the first chordate has insightful implications, which help to clarify the evolutionary pathways within chordates and to vertebrates. Two examples are the origin of the Spemann-Mangold organizer, and the origin of the neural crest.…”

Section: The Changing (And Definitive?) Phylogenetic Position Of Amphmentioning

confidence: 99%

Section: The Barcelona Lab: Genome and Embryos A La Cartementioning

confidence: 99%

“…We initially mainly embryos was a limiting factor for experimental research. As such, little literature includes gene or embryo manipulation (Beaster-Jones et al, 2007;Benito-Gutiérrez et al, 2005;Schubert et al, 2005).Hatschek, Conklin or Kowalevsky, among other classic embryologists, studied the European species, B. lanceolatum, (Conklin, 1932;Hatschek, 1881;Kowalevsky, 1867) focused on amphioxus homeobox genes (Brooke et al, 1998;Ferrier et al, 2000; and the data obtained in our laboratory served to suggest global hypothesis on the evolution of homeobox clusters in metazoans (Garcia-Fernàndez, 2005a;Garcia-Fernàndez, 2005b;). Later we expanded as well the research to more global studies: the evolution of nervous system and mesodermal derivatives, genome evolution, alternative splicing and phylogenies are among interests in the recent years (e.g.…”

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confidence: 91%

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From the American to the European amphioxus: towards experimental Evo-Devo at the origin of chordates

et al. 2009

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Pallid anchovy fillet, friendly filtering, peacefully laying and little lancelet are some of the nicknames and adjectives the cephalochordate amphioxus has received throughout the last two centuries. Traditionally regarded as the living representative of the last ancestor of vertebrates, amphioxus has recently been promoted to the privileged position of being the most ancient chordate. The preliminary analysis of its prototypical genome is nearly completed, and its hidden secrets towards the understanding of the primitive chordate and deuterostome genomes will soon see the light. Amphioxus embryonic development and body plan have remained in evolutionary stasis since the cephalochordate lineage split from the chordate ancestor about 500 million years ago. In contrast, amphioxus research is far from being at a standstill; in Europe, thanks to the international cooperation and the Banyuls Oceanographic Station, amphioxus embryos are obtained on demand during the spawning season. We summarise here our progress towards the dream of the experimental manipulation of the amphioxus embryo, to enter the era of Experimental Evo-Devo. KEY WORDS: amphioxus, Evo-Devo, chordate, gene duplication, vertebrateCommonality of embryonic structure reveals community of descent. As simple as it sounds today, the striking sentence of Charles Darwin (1859) highlighting the importance of embryonic development to indicate evolutionary relationships was not seriously taken into account by geneticists and evolutionary biologists until late 20th century, when molecular genetics showed that most gene networks responsible for embryonic development and functioning of metazoans were conserved; evolution may have well worked by tinkering and bricolage of a basic genetic toolkit to shape animal body plans and adaptations.In Comparative Zoology, Evolution and modern Evolutionary Developmental Biology (Evo-Devo), the origin of vertebrates has always received much attention, most probably due to a vertebroand anthropo-centrist view of scientists (Duboule, 2007), but also due to the fact that the origin of vertebrates involved the appearance of several intriguing innovations. Among those, vertebrae, regionalised anterior brain, neural crest cells and paired limbs evolved in the ancestor of vertebrates and generated, among other Int. J. Dev. Biol. 53: 1359-1366 (2009) Lancelets, or amphioxus, are small marine animals with a fishlike shape that spend most of their life partially burrowed in the sand, filtering sea water trough their jawless mouth, in search of their main food, unicellular algae. Currently, the subphylum Cephalochordata comprises 29 species of amphioxus (Poss and Boschung, 1996). The brilliant embryologist Alexander Kowalevsky (1867) already noted that amphioxus shared key anatomical features with vertebrates, such as a hollow dorsal nerve tube, an endostyle, a segmented body derived from somites and a postanal tail (Fig. 1). However, amphioxus lacks some vertebrate key characteristics, including migratory neural crest cells...

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Amphioxus as a Model for Mechanisms in Vertebrate Development

Benito‐Gutiérrez¹

2011

Encyclopedia of Life Sciences

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For the last two centuries, the cephalochordates, commonly known as lancelets or amphioxus, have been central to investigate the evolutionary genesis of vertebrates. At first, by classical morphologists fascinated by their odd but at the same time familiar anatomical traits and later by molecular biologists giving the first insights into their slow evolving nature. The present data available not only holds amphioxus as an organism of preternatural importance within the tree of life but also boosts its potential to untangle the molecular basis underlying the vertebrate complexity. This is a walk through the past and present of the amphioxus field merging morphological and molecular data in linkage with the fossil record and the modern vertebrates. The resulting picture is drawn together with comparative maps of genome organisation, gastrulation and the origin of the vertebrate organiser, neurulation and the origin of the neural crest, and shared signalling mechanisms between vertebrates and amphioxus during development. Special attention is also given to some of the most critical vertebrate novelties and how the pre‐duplicative amphioxus genetic toolkit might have contributed to set the basis for evolving complexity in the course of vertebrate evolution. Key Concepts: Cephalochordates occupy at present the key phylogenetic position to get insights into the invertebrate–vertebrate transition and the evolutionary genesis of vertebrates. Whole‐genome duplications in the lineage leading to modern vertebrates might have established the basis for molecular and morphological innovation. The amphioxus genome appears to be the best surrogate available for the ancestral chordate genome regarding the gene content, gene structure and chromosomal organisation. The amphioxus prototypical body plan with respect to vertebrates facilitates the comparative analysis and linkage between invertebrates and vertebrates. The pre‐duplicative genome of amphioxus offers the possibility of analysing vertebrate‐like gene regulatory networks in a simpler biological context with a reduced number of molecular players.

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The single AmphiTrk receptor highlights increased complexity of neurotrophin signalling in vertebrates and suggests an early role in developing sensory neuroepidermal cells

Cited by 70 publications

References 45 publications

BMP and Delta/Notch signaling control the development of amphioxus epidermal sensory neurons: insights into the evolution of the peripheral sensory system

BMP and Delta/Notch signaling control the development of amphioxus epidermal sensory neurons: insights into the evolution of the peripheral sensory system

From the American to the European amphioxus: towards experimental Evo-Devo at the origin of chordates

Amphioxus as a Model for Mechanisms in Vertebrate Development

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