Selective Advantages of Synapses in Evolution

Moroz, Leonid L.; Romanova, Daria Y.

doi:10.3389/fcell.2021.726563

Cited by 19 publications

(10 citation statements)

References 99 publications

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“…In the NPC, the genes originating in the third phylostratum (Opisthokonta) show a lower expression in the MP compared with the ESC, and the UC–MC transition is thus delayed to the fourth phylostratum (Metazoa, recent sponges). This difference can arise because the nervous system is of a later evolutionary origin [ 22 ]. After the 9th phylostratum (Euteleostomi), there is also some limited variation.…”

Section: Resultsmentioning

confidence: 99%

Cellular Biogenetic Law and Its Distortion by Protein Interactions: A Possible Unified Framework for Cancer Biology and Regenerative Medicine

Vinogradov

Anatskaya

2022

IJMS

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The biogenetic law (recapitulation law) states that ontogenesis recapitulates phylogenesis. However, this law can be distorted by the modification of development. We showed the recapitulation of phylogenesis during the differentiation of various cell types, using a meta-analysis of human single-cell transcriptomes, with the control for cell cycle activity and the improved phylostratigraphy (gene dating). The multipotent progenitors, differentiated from pluripotent embryonic stem cells (ESC), showed the downregulation of unicellular (UC) genes and the upregulation of multicellular (MC) genes, but only in the case of those originating up to the Euteleostomi (bony vertebrates). This picture strikingly resembles the evolutionary profile of regulatory gene expansion due to gene duplication in the human genome. The recapitulation of phylogenesis in the induced pluripotent stem cells (iPSC) during their differentiation resembles the ESC pattern. The unipotent erythroblasts differentiating into erythrocytes showed the downregulation of UC genes and the upregulation of MC genes originating after the Euteleostomi. The MC interactome neighborhood of a protein encoded by a UC gene reverses the gene expression pattern. The functional analysis showed that the evolved environment of the UC proteins is typical for protein modifiers and signaling-related proteins. Besides a fundamental aspect, this approach can provide a unified framework for cancer biology and regenerative/rejuvenation medicine because oncogenesis can be defined as an atavistic reversal to a UC state, while regeneration and rejuvenation require an ontogenetic reversal.

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Section: Resultsmentioning

confidence: 99%

Cellular Biogenetic Law and Its Distortion by Protein Interactions: A Possible Unified Framework for Cancer Biology and Regenerative Medicine

Vinogradov

Anatskaya

2022

IJMS

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“…The Aplysia genome encodes 41 MADF genes, and a many of them expressed in developmental stages as well as in specific neuronal populations, suggesting their involvement in the control of cell-specific phenotypes (data not shown) as well as contributing to the very origin of neuronal organizations and diversification events ( Erwin, 2009 ; Mustafin and Khusnutdinova, 2020 ; Moroz and Romanova, 2021 ). Homologs of these Aplysia MADF genes are missing in the sequenced Biomphalaria genome a related gastropod species ( Adema et al, 2017 ; Kocot et al, 2011 ), which encodes only three of these MADF genes.…”

Section: Discussionmentioning

confidence: 99%

Transposon-derived transcription factors across metazoans

Mukherjee

Moroz

2023

Front. Cell Dev. Biol.

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Transposable elements (TE) could serve as sources of new transcription factors (TFs) in plants and some other model species, but such evidence is lacking for most animal lineages. Here, we discovered multiple independent co-options of TEs to generate 788 TFs across Metazoa, including all early-branching animal lineages. Six of ten superfamilies of DNA transposon-derived conserved TF families (ZBED, CENPB, FHY3, HTH-Psq, THAP, and FLYWCH) were identified across nine phyla encompassing the entire metazoan phylogeny. The most extensive convergent domestication of potentially TE-derived TFs occurred in the hydroid polyps, polychaete worms, cephalopods, oysters, and sea slugs. Phylogenetic reconstructions showed species-specific clustering and lineage-specific expansion; none of the identified TE-derived TFs revealed homologs in their closest neighbors. Together, our study established a framework for categorizing TE-derived TFs and informing the origins of novel genes across phyla.

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“…Indeed, in contrast to nutrients, the receiver (=postsynaptic cell) does not 'know' what the signal value would be from the information standpoint (Miguel-Tome and Llinas, 2021). However, the selection of neurotransmitters includes chemical and past evolutionary history and bioenergetic constraints for preserving, eliminating, or expanding selected messengers in particular neural circuits and species (Moroz et al, 2021b;Moroz and Romanova, 2021).…”

Section: Figurementioning

confidence: 99%

“…Finally, the evolutionary making of the chemical synapse involved a dramatic reorganization of the endoplasmic reticulum, lipid diversifications, and compartmentalization within intracellular membranes, further promoting the rise of a neuronal organization (Moroz and Romanova, 2021). Molecular and functional classification of synapses, as performed in mammals (Emes et al, 2008;Grant, 2009;Masch et al, 2018;Roy et al, 2018;Zhu et al, 2018;Cizeron et al, 2020;Grant and Fransen, 2020;Bulovaite et al, 2022), is the most perspective direction to uncover the principles of neural 'designs' in basal metazoans.…”

Section: Figurementioning

confidence: 99%

Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)

Moroz

Romanova

2022

Front. Cell Dev. Biol.

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How to make a neuron, a synapse, and a neural circuit? Is there only one ‘design’ for a neural architecture with a universally shared genomic blueprint across species? The brief answer is “No.” Four early divergent lineages from the nerveless common ancestor of all animals independently evolved distinct neuroid-type integrative systems. One of these is a subset of neural nets in comb jellies with unique synapses; the second lineage is the well-known Cnidaria + Bilateria; the two others are non-synaptic neuroid systems in sponges and placozoans. By integrating scRNA-seq and microscopy data, we revise the definition of neurons as synaptically-coupled polarized and highly heterogenous secretory cells at the top of behavioral hierarchies with learning capabilities. This physiological (not phylogenetic) definition separates ‘true’ neurons from non-synaptically and gap junction-coupled integrative systems executing more stereotyped behaviors. Growing evidence supports the hypothesis of multiple origins of neurons and synapses. Thus, many non-bilaterian and bilaterian neuronal classes, circuits or systems are considered functional rather than genetic categories, composed of non-homologous cell types. In summary, little-explored examples of convergent neuronal evolution in representatives of early branching metazoans provide conceptually novel microanatomical and physiological architectures of behavioral controls in animals with prospects of neuro-engineering and synthetic biology.

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Selective Advantages of Synapses in Evolution

Cited by 19 publications

References 99 publications

Cellular Biogenetic Law and Its Distortion by Protein Interactions: A Possible Unified Framework for Cancer Biology and Regenerative Medicine

Cellular Biogenetic Law and Its Distortion by Protein Interactions: A Possible Unified Framework for Cancer Biology and Regenerative Medicine

Transposon-derived transcription factors across metazoans

Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)

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