Lateral neural borders as precursors of peripheral nervous systems: A comparative view across bilaterians

Zhao, Di; Chen, Siyu; Liu, Xiao

doi:10.1111/dgd.12585

Cited by 12 publications

(19 citation statements)

References 154 publications

(364 reference statements)

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“…Our results align with multiple lines of evidence across Bilateria showing that the function of BMP signaling in neural induction is not conserved across Bilateria (Martín-Durán et al, 2018; Zhao et al, 2019). For example, in vertebrates, formation of the dorsal neural tube relies in part on inhibition of BMP signaling by graded antagonists secreted from the organizer (e.g.…”

Section: Discussionsupporting

confidence: 90%

Role of BMP signaling during early development of the annelidCapitella teleta

Webster

Corbet

Sur

et al. 2020

Preprint

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The mechanisms regulating nervous system development are still unknown for a wide variety of taxa. In insects and vertebrates, bone morphogenetic protein (BMP) signaling is known to play a key role in both neural specification and dorsal-ventral (D-V) axis formation, leading to speculation about the conserved evolution of nervous systems. Studies outside insects and vertebrates show a more diverse picture of what, if any role, BMP signaling plays in neural development across Bilateria. This is especially true in the morphologically diverse Spiralia (~Lophotrochozoa). Despite several studies of D-V axis formation and neural induction in spiralians, there is no consensus for how these two processes are related, or whether BMP signaling may have played an ancestral role in either process. Here we incubated larvae of the sedentary annelid Capitella teleta in BMP4 protein at various cleavage stages to determine the role of BMP signaling during early development. Adding exogenous BMP protein to early-cleaving C. teleta embryos had a striking effect on formation of the brain, eyes, and foregut in a time-dependent manner. However, adding BMP did not block neural specification of the brain or VNC or block formation of the D-V axis. We identified three key time windows of BMP activity, and hypothesize that BMP may cause trans-fate switching of blastomere quadrant identities in at least one time window. 1. Early treatment around 2q caused the loss of the eyes, radialization of the brain, and a reduction of the foregut, which we interpret as a loss of A-, B- and C-quadrant identities with a possible trans-fate switch to a D-quadrant identity. 2. Treatment after 4q induced formation of a third ectopic brain lobe, eye, and foregut lobe, which we interpret as a trans-fate switch of B-quadrant micromeres to a C-quadrant identity. 3. Continuous BMP treatment from early cleavage through mid-larval stages resulted in a modest expansion of Ct-chrdl expression in the dorsal ectoderm and a concomitant loss of the ventral midline (neurotroch ciliary band). Loss of the ventral midline was accompanied by a collapse of the bilaterally-symmetric VNC although the total amount of neural tissue did not appear to be greatly affected. Our results compared to those from other annelids and molluscs suggest that BMP signaling was not ancestrally involved in delimiting neural tissue or establishing the D-V axis in the last common ancestor of annelids. However, the effects of ectopic BMP on quadrant-identity during cleavage stages may represent a very early ‘organizing’ function in the context of spiralian development. Ultimately, studies on a wider range of spiralian taxa are needed to determine if the ability of BMP signaling to block neural induction and help establish the D-V axis was lost within Annelida or if BMP signaling gained these functions multiple times across Bilateria. Ultimately, these comparisons will give us insight into the evolutionary origins of centralized nervous systems and body plans.

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Section: Discussionsupporting

confidence: 90%

Role of BMP signaling during early development of the annelidCapitella teleta

Webster

Corbet

Sur

et al. 2020

Preprint

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“…Take, for example, the neural plate border in vertebrates, the embryonic domain that produces neural crest progenitors. Studies of invertebrates on both the protostome and deuterostome sides of the bilaterian tree have revealed the presence of so-called lateral neural borders that are similar to the neural plate border [120] (figure 3a). These lateral neural borders develop as part of a broad embryonic domain that instructs medial-lateral patterning of the neuroectoderm into the CNS and PNS [120].…”

Section: Ancient Origins Of Neural Crest Regulatory Mechanismsmentioning

confidence: 99%

“…Studies of invertebrates on both the protostome and deuterostome sides of the bilaterian tree have revealed the presence of so-called lateral neural borders that are similar to the neural plate border [120] (figure 3a). These lateral neural borders develop as part of a broad embryonic domain that instructs medial-lateral patterning of the neuroectoderm into the CNS and PNS [120]. Cells derived from lateral neural borders express homologues of Pax, Zic, Msx and Nkx transcription factors and give rise to migratory and non-migratory sensory neurons of the embryonic PNS, just as neural crest cells do in vertebrates [120,121].…”

Section: Ancient Origins Of Neural Crest Regulatory Mechanismsmentioning

confidence: 99%

“…Based on multiple lines of evidence, early chordates probably did not have neural crest or neural crest-like cells. Rather, the first chordates probably inherited a neural plate border (or lateral neural border) involved in medial-lateral patterning of the embryonic neuroectoderm and production of PNS neurons (figure 4), as well as the potential to generate sensory neurons from the ventral epidermis (a feature probably lost in vertebrates [120]). With the evolution of the lineage leading to tunicates and vertebrates (olfactores), we see for the first time cells that have a characteristic neural crest 'signature'.…”

Section: Neural Crest-like Cells In Invertebrate Chordates: Evolutionmentioning

confidence: 99%

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The origin and evolution of vertebrate neural crest cells

York

McCauley

2020

Open Biol.

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The neural crest is a vertebrate-specific migratory stem cell population that generates a remarkably diverse set of cell types and structures. Because many of the morphological, physiological and behavioural novelties of vertebrates are derived from neural crest cells, it is thought that the origin of this cell population was an important milestone in early vertebrate history. An outstanding question in the field of vertebrate evolutionary-developmental biology (evo-devo) is how this cell type evolved in ancestral vertebrates. In this review, we briefly summarize neural crest developmental genetics in vertebrates, focusing in particular on the gene regulatory interactions instructing their early formation within and migration from the dorsal neural tube. We then discuss how studies searching for homologues of neural crest cells in invertebrate chordates led to the discovery of neural crest-like cells in tunicates and the potential implications this has for tracing the pre-vertebrate origins of the neural crest population. Finally, we synthesize this information to propose a model to explain the origin of neural crest cells. We suggest that at least some of the regulatory components of early stages of neural crest development long pre-date vertebrate origins, perhaps dating back to the last common bilaterian ancestor. These components, originally directing neuroectodermal patterning and cell migration, served as a gene regulatory ‘scaffold' upon which neural crest-like cells with limited migration and potency evolved in the last common ancestor of tunicates and vertebrates. Finally, the acquisition of regulatory programmes controlling multipotency and long-range, directed migration led to the transition from neural crest-like cells in invertebrate chordates to multipotent migratory neural crest in the first vertebrates.

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“…The vertebrate Msx/vab-15-specified domain represents the merged expression patterns of Msx1, Msx2, and Msx3 in mouse (Duval et al, 2014;Wang, Chen, Xu, & Lufkin, 1996). BTN, bipolar tail neuron; CNS, central nervous system; DRGN, dorsal root ganglion neurons [Color figure can be viewed at wileyonlinelibrary.com] related bilaterians have revealed that they are similar in overall spatial arrangement and molecular identity mediolaterally (Denes et al, 2007;Li et al, 2017;D. Zhao et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Comparison of differentiation gene batteries for migratory mechanosensory neurons across bilaterians

Zhao

Chen

Horie

et al. 2020

Evolution and Development

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In embryos of distantly related bilaterian phyla, their lateral neural borders give rise to the peripheral nervous system elements, including various mechanosensory cells derived from migratory precursors, such as hair cells and dorsal root ganglion (DRG) neurons in vertebrates, bipolar tail neuron (BTN) in Ciona, chordotonal organ in Drosophila, and AVM/PVM in Caenorhabditis elegans. Developmental genetics studies had revealed a couple of transcription factors (TFs) regulating differentiation of mechanosensory cells shared by vertebrates and arthropods. However, unbiased systematic profiling of regulators is needed to demonstrate conservation of differentiation gene batteries for mechanosensory cells across bilaterians. At first, we observed that in both C. elegans Q neuroblasts and Drosophila lateral neuroectoderm, conserved NPB specifier Msx/vab-15 regulates Atoh1/lin-32, supporting the homology of mechanosensory neuron development in lateral neural border lineage of Ecdysozia. So we used C. elegans as a protostomia model. Single-cell resolution expression profiling of TFs and genetic analysis revealed a differentiation gene battery (Atonh1/lin-32, Drg11/alr-1, Gfi1/pag-3, Lhx5/mec-3, and Pou4/unc-86) for AVM/PVM mechanosensory neurons. The worm-gene battery significantly overlaps with both that of placode-derived Atonh1/lin-32-dependent hair cells and that of NPB-derived Neurogenin-dependent DRG neurons in vertebrates, supporting the homology of molecular mechanisms underlying the differentiation of neural border-derived mechanosensory cells between protostome and deuterostome. At last, Ciona BTN, the homolog of vertebrate DRG, also expresses Atonh1/lin-32, further supporting the homology notion and indicating a common origin of hair cells and DRG in vertebrate lineage.

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Lateral neural borders as precursors of peripheral nervous systems: A comparative view across bilaterians

Cited by 12 publications

References 154 publications

Role of BMP signaling during early development of the annelidCapitella teleta

Role of BMP signaling during early development of the annelidCapitella teleta

The origin and evolution of vertebrate neural crest cells

Comparison of differentiation gene batteries for migratory mechanosensory neurons across bilaterians

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