Sponge Genes Provide New Insight into the Evolutionary Origin of the Neurogenic Circuit

Richards, Gemma S.; Simionato, Elena; Perron, Muriel; Adamska, Maja; Vervoort, Michel; Degnan, Bernard M.

doi:10.1016/j.cub.2008.06.074

Cited by 145 publications

(169 citation statements)

References 31 publications

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“…1). Simply put, ancestral proneurons can be viewed as one of many populations of polarized secretory cells (Richards et al, 2008). Not surprisingly, the recruitment of different secretory cell lineages for more localized neural-like signaling might have occurred multiple times in evolution.…”

Section: Quest For Neurogenic Genes and Signal Molecules In Ctenophoresmentioning

confidence: 99%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

120

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: Quest For Neurogenic Genes and Signal Molecules In Ctenophoresmentioning

confidence: 99%

Convergent evolution of neural systems in ctenophores

Moroz

2015

Journal of Experimental Biology

120

139

View full text Add to dashboard Cite

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“…A number of PSD genes (Homer, CRIPT, DLG etc.) are expressed in globular cells of the epithelium of the larva of Amphimedon queenslandica, which are interpreted to be potential sensory cells receiving signal cues that guide settlement behaviour (Sakaraya et al, 2007;Richards et al, 2008). Normally PSDs are in the cell receiving the signal, not the sensory cell, so their location in the globular cell of Amphimedon is confusing.…”

Section: Conducting Pathways and Effectorsmentioning

confidence: 99%

Elements of a ‘nervous system’ in sponges

Leys

2015

Journal of Experimental Biology

128

123

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Genomic and transcriptomic analyses show that sponges possess a large repertoire of genes associated with neuronal processes in other animals, but what is the evidence these are used in a coordination or sensory context in sponges? The very different phylogenetic hypotheses under discussion today suggest very different scenarios for the evolution of tissues and coordination systems in early animals. The sponge genomic 'toolkit' either reflects a simple, pre-neural system used to protect the sponge filter or represents the remnants of a more complex signalling system and sponges have lost cell types, tissues and regionalization to suit their current suspensionfeeding habit. Comparative transcriptome data can be informative but need to be assessed in the context of knowledge of sponge tissue structure and physiology. Here, I examine the elements of the sponge neural toolkit including sensory cells, conduction pathways, signalling molecules and the ionic basis of signalling. The elements described do not fit the scheme of a loss of sophistication, but seem rather to reflect an early specialization for suspension feeding, which fits with the presumed ecological framework in which the first animals evolved.

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“…For these purposes it has to employ a particular tool to be able to obtain information about its surroundings, which has to be processed and translated into an adequate response. This tool is the nervous system; the first hints of its appearance were present in the sponge, which has no neurons but has a set of post-synaptic scaffolding genes pre-announcing them 28 . After the divergence of sponge and eumetazoan, this last lineage developed transmembrane receptor genes, such as the glutamate receptors family found at the post-synapse of the most developed species, where recognizable nervous structures can be found 29 .…”

Section: A Thought About Thinkingmentioning

confidence: 99%

Are astrocytes executive cells within the central nervous system?

Sica

Caccuri

Quarracino

et al. 2016

Arq. Neuro-Psiquiatr.

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Experimental evidence suggests that astrocytes play a crucial role in the physiology of the central nervous system (CNS) by modulating synaptic activity and plasticity. Based on what is currently known we postulate that astrocytes are fundamental, along with neurons, for the information processing that takes place within the CNS. On the other hand, experimental findings and human observations signal that some of the primary degenerative diseases of the CNS, like frontotemporal dementia, Parkinson’s disease, Alzheimer’s dementia, Huntington’s dementia, primary cerebellar ataxias and amyotrophic lateral sclerosis, all of which affect the human species exclusively, may be due to astroglial dysfunction. This hypothesis is supported by observations that demonstrated that the killing of neurons by non-neural cells plays a major role in the pathogenesis of those diseases, at both their onset and their progression. Furthermore, recent findings suggest that astrocytes might be involved in the pathogenesis of some psychiatric disorders as well.

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Sponge Genes Provide New Insight into the Evolutionary Origin of the Neurogenic Circuit

Cited by 145 publications

References 31 publications

Convergent evolution of neural systems in ctenophores

Convergent evolution of neural systems in ctenophores

Elements of a ‘nervous system’ in sponges

Are astrocytes executive cells within the central nervous system?

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