Insights into the early evolution of <i>SOX</i> genes from expression analyses in a ctenophore

Jager, Muriel; Quéinnec, Éric; Chiori, Roxane; Guyader, Hervé Le; Manuel, Michaël

doi:10.1002/jez.b.21244

Cited by 45 publications

(73 citation statements)

References 50 publications

(93 reference statements)

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“…Yes, these genes are present in ctenophore genomes but they cannot be considered as pan-neuronal markers in ctenophores because they are expressed in many other cell types. Plus their neuronal colocalization at the cellular level has not been shown (Jager et al, 2006;Derelle and Manuel, 2007;Jager et al, 2008;Ryan et al, 2010;Simmons et al, 2012;Schnitzler et al, 2014). The fact that some of these genes are associated with the aboral organ or polar fields does not mean that in these structures these genes are expressed in neurons (e.g.…”

Section: Reviewmentioning

confidence: 99%

“…These species are perfectly amenable to various experimental manipulations, including reliable fixation (most other ctenophores simply disintegrate in the majority of common fixatives), development, neurobiological and behavioral tests (Tamm, 1982;Tamm, 1984;Tamm and Moss, 1985), as well as molecular manipulations (Alié et al, 2010;Jager et al, 2008;Moroz et al, 2014). Many ctenophores possess a characteristic cydippid larva that is similar to adult Pleurobrachia (Fig.…”

Section: Rise Of Ctenophore Genomics -Pleurobrachia Bachei As An Emermentioning

confidence: 99%

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Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

116

139

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Neurons are defined as polarized secretory cells specializing in directional propagation of electrical signals leading to the release of extracellular messengers -features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. Multiple origins of neurons and synapses from different classes of ancestral secretory cells might have occurred more than once during ~600 million years of animal evolution with independent events of nervous system centralization from a common bilaterian/cnidarian ancestor without the bona fide central nervous system. Ctenophores, or comb jellies, represent an example of extensive parallel evolution in neural systems. First, recent genome analyses place ctenophores as a sister group to other animals. Second, ctenophores have a smaller complement of pan-animal genes controlling canonical neurogenic, synaptic, muscle and immune systems, and developmental pathways than most other metazoans. However, comb jellies are carnivorous marine animals with a complex neuromuscular organization and sophisticated patterns of behavior. To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organization of integrative and locomotory systems. Third, many bilaterian/cnidarian neuron-specific genes and 'classical' neurotransmitter pathways are either absent or, if present, not expressed in ctenophore neurons (e.g. the bilaterian/cnidarian neurotransmitter, γ-amino butyric acid or GABA, is localized in muscles and presumed bilaterian neuronspecific RNA-binding protein Elav is found in non-neuronal cells). Finally, metabolomic and pharmacological data failed to detect either the presence or any physiological action of serotonin, dopamine, noradrenaline, adrenaline, octopamine, acetylcholine or histamineconsistent with the hypothesis that ctenophore neural systems evolved independently from those in other animals. Glutamate and a diverse range of secretory peptides are first candidates for ctenophore neurotransmitters. Nevertheless, it is expected that other classes of signal and neurogenic molecules would be discovered in ctenophores as the next step to decipher one of the most distinct types of neural organization in the animal kingdom.

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Section: Reviewmentioning

confidence: 99%

Section: Rise Of Ctenophore Genomics -Pleurobrachia Bachei As An Emermentioning

confidence: 99%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

116

139

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“…SoxB and SoxE protein-coding genes are found among others in the ctenophore Pleurobrachia pileus in which they are detected in adult neurosensory structures (Jager et al 2008). Genes coding for SoxB (MleSox1), SoxC (MleSox2) and SoxE (MleSox3, MleSox4) proteins are characterized in the ctenophore Mnemiopsis leidyi (Schnitzler et al 2014).…”

Section: Sponges and Ctenophores: Two Special Casesmentioning

confidence: 99%

Can the ‘neuron theory’ be complemented by a universal mechanism for generic neuronal differentiation

Ernsberger

2014

Cell Tissue Res

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With the establishment of the 'neuron theory' at the turn of the twentieth century, this remarkably powerful term was introduced to name a breathtaking diversity of cells unified by a characteristic structural compartmentalization and unique information processing and propagating features. At the beginning of the twenty-first century, developmental, stem cell and reprogramming studies converged to suggest a common mechanism involved in the generation of possibly all vertebrate, and at least a significant number of invertebrate, neurons. Sox and, in particular, SoxB and SoxC proteins as well as basic helix-loop-helix proteins play major roles, even though their precise contributions to progenitor programming, proliferation and differentiation are not fully resolved. In addition to neuronal development, these transcription factors also regulate sensory receptor and endocrine cell development, thus specifying a range of cells with regulatory and communicative functions. To what extent microRNAs contribute to the diversification of these cell types is an upcoming question. Understanding the transcriptional and post-transcriptional regulation of genes coding for cell type-specific cytoskeletal and motor proteins as well as synaptic and ion channel proteins, which mark differences but also similarities between the three communicator cell types, will provide a key to the comprehension of their diversification and the signature of 'generic neuronal' differentiation. Apart from the general scientific significance of a putative universal core instruction for neuronal development, the impact of this line of research for cell replacement therapy and brain tumor treatment will be of considerable interest.

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“…Expression of vasa , nanos , and sox genes in the stem cell precursors of adult (Jager et al 2008 ;Alié et al 2011 ) and embryonic (Reitzel et al 2015 . ) ctenophores is consistent with maintenance of the pluripotent state, although these ideas have not been functionally tested.…”

Section: Mnemiopsis Leidyi As a Ctenophore Model For Evodevo Researchmentioning

confidence: 97%

“…Although there are a limited number of genes whose expression has been examined in adult ctenophores (Jager et al 2008 ;Alié et al 2011 ), gene expression patterns in developing ctenophores have only been described for a single species, Mnemiopsis leidyi . In situ hybridization experiments for over 50 genes (Table 8.1 ) have been published for Mnemiopsis including a number of important gene families and pathways such as homeodomain genes Martindale 2008b , 2009 ;Ryan et al 2010 ;Simmons et al 2012 ), forkhead genes (Yamada and Martindale 2002 ), T-box genes (Yamada et al 2007 ), nuclear receptors (Reitzel et al 2011 ), and sox genes (Schnitzler et al 2014 ).…”

Section: Gene Expressionmentioning

confidence: 99%