FGF signalling controls formation of the apical sensory organ in the cnidarian<i>Nematostella vectensis</i>

Rentzsch, Fabian; Fritzenwanker, Jens H.; Scholz, Corinna; Technau, Ulrich

doi:10.1242/dev.020784

Cited by 163 publications

(243 citation statements)

References 65 publications

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“…In agreement with the theoretical expectation for an inhibitor, Lefty2 diffuses much faster than Nodal [17,18]. Most remarkable is that, in this and in other systems [19], the inhibitor interrupts the self-enhancement by blocking the receptor that is required for activation. Thus, the inhibitory action occurs outside the cell.…”

Section: Pattern Formation Requires Local Self-enhancement and Long-rsupporting

confidence: 87%

Turing's theory of morphogenesis of 1952 and the subsequent discovery of the crucial role of local self-enhancement and long-range inhibition

2012

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In his pioneering work, Alan Turing showed that de novo pattern formation is possible if two substances interact that differ in their diffusion range. Since then, we have shown that pattern formation is possible if, and only if, a self-enhancing reaction is coupled with an antagonistic process of longer range. Knowing this crucial condition has enabled us to include nonlinear interactions, which are required to design molecularly realistic interactions. Different reaction schemes and their relation to Turing's proposal are discussed and compared with more recent observations on the molecular-genetic level. The antagonistic reaction may be accomplished by an inhibitor that is produced in the activated region or by a depletion of a component that is used up during the self-enhancing reaction. The autocatalysis may be realized by an inhibition of an inhibition. Activating molecules can be processed into molecules that have an inhibiting function; patterning of the Wnt pathway is proposed to depend on such a mechanism. Three-component systems, as discussed in Turing's paper, are shown to play a major role in the generation of highly dynamic patterns that never reach a stable state.

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Section: Pattern Formation Requires Local Self-enhancement and Long-rsupporting

confidence: 87%

Turing's theory of morphogenesis of 1952 and the subsequent discovery of the crucial role of local self-enhancement and long-range inhibition

2012

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“…In diverse ciliated marine larvae (15), the apical organ, an anterior cluster of larval sensory neurons (16) with a strong neurosecretory character (17)(18)(19)(20), has been implicated in the detection of cues for the initiation of larval settlement (21). Although molecular markers of the apical organ have been described (22)(23)(24), our knowledge of the neuroendocrine mechanisms with which apical organ cells transmit signals to initiate larval settlement behavior is incomplete.…”

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confidence: 99%

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

Conzelmann

Williams

Tunaru

et al. 2013

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

134

216

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Life-cycle transitions connecting larval and juvenile stages in metazoans are orchestrated by neuroendocrine signals including neuropeptides and hormones. In marine invertebrate life cycles, which often consist of planktonic larval and benthic adult stages, settlement of the free-swimming larva to the sea floor in response to environmental cues is a key life cycle transition. Settlement is regulated by a specialized sensory-neurosecretory system, the larval apical organ. The neuroendocrine mechanisms through which the apical organ transduces environmental cues into behavioral responses during settlement are not yet understood. Here we show that myoinhibitory peptide (MIP)/allatostatin-B, a pleiotropic neuropeptide widespread among protostomes, regulates larval settlement in the marine annelid Platynereis dumerilii. MIP is expressed in chemosensory-neurosecretory cells in the annelid larval apical organ and signals to its receptor, an orthologue of the Drosophila sex peptide receptor, expressed in neighboring apical organ cells. We demonstrate by morpholino-mediated knockdown that MIP signals via this receptor to trigger settlement. These results reveal a role for a conserved MIP receptor-ligand pair in regulating marine annelid settlement.M etazoan life cycles show great diversity in larval, juvenile, and adult forms, as well as in the timing and ecological context of the transitions between these forms. In many animal species, neuroendocrine signals involving hormones and neuropeptides regulate life cycle transitions (1-3). Environmental cues are often important instructors of the timing of life cycle transitions (4), and can affect behavioral, physiological, or morphological change via neuroendocrine signaling (5).Marine invertebrate larval settlement is a prime example of the strong link between environmental cues and the timing of life-cycle transitions. Marine invertebrate life cycles often consist of a free-swimming (i.e., pelagic) larval stage that settles to the ocean floor and metamorphoses into a bottom-dwelling (i.e., benthic) juvenile (6-8). In many invertebrate larvae, a pelagicbenthic transition is induced by chemical cues from the environment (9, 10). Larval settlement commonly includes the cessation of swimming and the appearance of substrate exploratory behavior, including crawling on or attachment to the substrate (11-14). In diverse ciliated marine larvae (15), the apical organ, an anterior cluster of larval sensory neurons (16) with a strong neurosecretory character (17-20), has been implicated in the detection of cues for the initiation of larval settlement (21). Although molecular markers of the apical organ have been described (22-24), our knowledge of the neuroendocrine mechanisms with which apical organ cells transmit signals to initiate larval settlement behavior is incomplete.Here, we identify a conserved myoinhibitory peptide (MIP)/ allatostatin-B receptor-ligand pair as a regulator of larval settlement behavior in the marine polychaete annelid Platynereis dumerilii. MIPs are pleiotro...

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“…Prebilaterian groups like sponges and cnidarians lack a DV axis. The antagonistic BMP-Chordin network seems absent in sponges, whereas in cnidarians it is initially expressed along the primary body axis (Rentzsch et al 2008).…”

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confidence: 99%

The Evolution of the Wnt Pathway

Holstein

2012

Cold Spring Harbor Perspectives in Biology

194

176

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Wnt genes are important regulators of embryogenesis and cell differentiation in vertebrates and insects. New data revealed by comparative genomics have now shown that members of the Wnt signaling pathway can be found in all clades of metazoans, but not in fungi, plants, or unicellular eukaryotes. This article focuses on new data from recent genomic analyses of several basal metazoan organisms, providing evidence that the Wnt pathway was a primordial signaling pathway during evolution. The formation of a Wnt signaling center at the site of gastrulation was instrumental for the formation of a primary, anterior-posterior body axis, which can be traced throughout animal evolution.

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FGF signalling controls formation of the apical sensory organ in the cnidarianNematostella vectensis

Cited by 163 publications

References 65 publications

Turing's theory of morphogenesis of 1952 and the subsequent discovery of the crucial role of local self-enhancement and long-range inhibition

Turing's theory of morphogenesis of 1952 and the subsequent discovery of the crucial role of local self-enhancement and long-range inhibition

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

The Evolution of the Wnt Pathway

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