scholarly journals High cell diversity and complex peptidergic signalling underlie placozoan behaviour

2018 ◽  
Author(s):  
Frédérique Varoqueaux ◽  
Elizabeth A Williams ◽  
Susie Grandemange ◽  
Luca Truscello ◽  
Kai Kamm ◽  
...  

SUMMARYPlacozoans, together with sponges, are the only animals devoid of a nervous system and muscles, yet both respond to sensory stimulation in a coordinated manner. How behavioural control in these free-living animals is achieved in the absence of neurons and, more fundamentally, how the first neurons evolved from more primitive communication cells during the rise of animals is not yet understood [1–5]. The placozoan Trichoplax adhaerens is a millimeter-wide, flat, free-living marine animal composed of six morphologically identified cell types distributed across a simple bodyplan [6–9]: a flat upper epithelium and a cylindrical lower epithelium interspersed with a loose layer of fiber cells. Its genome encodes several proneuropeptide genes and genes involved in neurosecretion in animals with a nervous system [10–12]. Here we investigate neuropeptide signalling in Trichoplax adhaerens. We found specific expression of several neuropeptides in non-overlapping cell populations distributed over the three cell layers, revealing an unsuspected cell-type diversity of Trichoplax adhaerens. Using live imaging, we uncovered that treatments with 11 different neuropeptides elicited striking and consistent effects on the animals’ shape, patterns of movement and velocity that we categorized under three main types: (i) crinkling, (ii) turning, and (iii) flattening and churning. Together, the data demonstrate a crucial role for peptidergic signalling in nerveless placozoans and suggest that peptidergic volume signalling may have predated synaptic signalling in the evolution of nervous systems.

2020 ◽  
Author(s):  
Daria Y. Romanova ◽  
Frederique Varoqueaux ◽  
Jean Daraspe ◽  
Mikhail A. Nikitin ◽  
Michael Eitel ◽  
...  

AbstractFrom a morphological point of view, placozoans are among the most simple free-living animals. This enigmatic phylum is critical for our understanding of the evolution of animals and their cell types. Their millimeter-sized, disc-like bodies consist of only three cell layers that are shaped by roughly six major cell types. Placozoans lack muscle cells and neurons but are able to move using their ciliated lower surface and take up food in a highly coordinated manner. Intriguingly, the genome of Trichoplax adhaerens, the founding member of the enigmatic phylum, has disclosed a surprising level of genetic complexity. Moreover, recent molecular and functional investigations have uncovered a much larger, so-far hidden cell-type diversity. Here, we have extended the microanatomical characterization of a recently described placozoan species – Hoilungia hongkongensis. In H. hongkongensis, we recognized the established canonical three-layered placozoan body plan but also came across several morphologically distinct and potentially novel cell types, among them novel gland cells and “shiny spheres”-bearing cells at the upper epithelium. Thus, the diversity of cell types in placozoans is indeed higher than anticipated.


2019 ◽  
Vol 116 (18) ◽  
pp. 8901-8908 ◽  
Author(s):  
Carolyn L. Smith ◽  
Thomas S. Reese ◽  
Tzipe Govezensky ◽  
Rafael A. Barrio

Trichoplax adhaerens is a small, ciliated marine animal that glides on surfaces grazing upon algae, which it digests externally. It has no muscles or nervous system and only six cell types, all but two of which are embedded in its epithelium. The epithelial cells are joined by apical adherens junctions; neither tight junctions nor gap junctions are present. Monociliated epithelial cells on the lower surface propel gliding. The cilia beat regularly, but asynchronously, and transiently contact the substrate with each stroke. The animal moves in random directions in the absence of food. We show here that it exhibits chemotaxis, moving preferentially toward algae embedded in a disk of agar. We present a mathematical model to explain how coherent, directional movements could arise from the collective actions of a set of ciliated epithelial cells, each independently sensing and responding to a chemoattractant gradient. The model incorporates realistic values for viscoelastic properties of cells and produces coordinated movements and changes in body shape that resemble the actual movements of the animal. The model demonstrates that an animal can move coherently in search of food without any need for chemical signaling between cells and introduces a different approach to modeling behavior in primitive multicellular organisms.


2010 ◽  
Vol 21 (16) ◽  
pp. 2860-2868 ◽  
Author(s):  
G. Harper Mazock ◽  
Amlan Das ◽  
Christine Base ◽  
Ronald R. Dubreuil

The protein spectrin is ubiquitous in animal cells and is believed to play important roles in cell shape and membrane stability, cell polarity, and endomembrane traffic. Experiments here were undertaken to identify sites of essential β spectrin function in Drosophila and to determine whether spectrin and ankyrin function are strictly linked to one another. The Gal4-UAS system was used to drive tissue-specific overexpression of a β spectrin transgene or to knock down β spectrin expression with dsRNA. The results show that 1) overexpression of β spectrin in most of the cell types studied was lethal; 2) knockdown of β spectrin in most tissues had no detectable effect on growth or viability of the organism; and 3) nervous system-specific expression of a UAS-β spectrin transgene was sufficient to overcome the lethality of a loss-of-function β spectrin mutation. Thus β spectrin expression in other cells was not required for development of fertile adult males, although females lacking nonneuronal spectrin were sterile. Previous data indicated that binding of the DAnk1 isoform of ankyrin to spectrin was partially dispensable for viability. Domain swap experiments here uncovered a different requirement for neuronal DAnk2 binding to spectrin and establish that DAnk2-binding is critical for β spectrin function in vivo.


2019 ◽  
Author(s):  
Hadi Najafi ◽  
Kyle Wong ◽  
Woo Jae Kim

ABSTRACTDrosophila melanogaster is a proper model organism for studying the development and function of the nervous system. The Drosophila nervous system consists of distinct cell types with significant homologies to various cell types of more advanced organisms, including human. Among all cell types of the nervous system, astrocyte-like glia (ALG) have conserved functions to mammals and are essential for normal physiology and behaviours of the fly.In this study, we exploited the gene expression profile of single cells in Drosophila optic lobe to identify the genes with specific expression pattern in each cell type. Through a bioinformatical analysis of the data, a novel ALG-specific gene (here assigned as deathstar) was identified. Immunostaining of deathstar in the central nervous system (CNS) showed its presence in specific regions of Drosophila ventral nerve cord, which previously has been characterized as ALG cells. Consistent with the bioinformatical analysis, deathstar-related signals were overlapped with the signals of the previously-reported ALG marker, Eaat1, supporting its specific expression in ALG cells.At the physiological level, RNAi-mediated suppression of deathstar gene impeded the normal development of male flies without any effects on females. Cell type-specific expression of deathstar RNAi showed that deathstar gene affects locomotion behaviour and lifespan of D. melanogaster, in an ALG-specific manner.Taken together, we showed that bioinformatical analysis of a previously reported expression data of Drosophila optic lobe successfully predicted the ALG-specific expression pattern of deathstar gene. Moreover, it was consistent with the ALG-specific effects of this gene on locomotion and lifespan of D. melanogaster, in vivo.


2021 ◽  
Vol 9 (11) ◽  
pp. 1229
Author(s):  
Tatiana D. Mayorova

Trichoplax adhaerens are simple animals with no nervous system, muscles or body axis. Nevertheless, Trichoplax demonstrate complex behaviors, including responses to the direction of the gravity vector. They have only six somatic cell types, and one of them, crystal cells, has been implicated in gravity reception. Multiple crystal cells are scattered near the rim of the pancake-shaped animal; each contains a cup-shaped nucleus and an intracellular crystal, which aligns its position according to the gravity force. Little is known about the development of any cell type in Trichoplax, which, in the laboratory, propagate exclusively by binary fission. Electron and light microscopy were used to investigate the stages by which crystal cells develop their mature phenotypes and distributions. Nascent crystal cells, identified by their possession of a small crystal, were located farther from the rim than mature crystal cells, indicating that crystal cells undergo displacement during maturation. They were elongated in shape and their nucleus was rounded. The crystal develops inside a vacuole flanked by multiple mitochondria, which, perhaps, supply molecules needed for the biomineralization process underlying crystal formation. This research sheds light on the development of unique cells with internal biomineralization and poses questions for further research.


2020 ◽  
Author(s):  
Hadi Najafi ◽  
Kyle Wong ◽  
Woo Jae Kim

Abstract Background Drosophila melanogaster is a proper model organism for studying the development and function of the nervous system. The Drosophila nervous system consists of distinct cell types with significant homologies to various cell types of more advanced organisms, including human. Among all cell types of the nervous system, astrocyte-like glia (ALG) have conserved functions to mammals and are essential for normal physiology and behaviours of the fly. Results In this study, we exploited the gene expression profile of single cells in Drosophila optic lobe to identify the genes with specific expression pattern in each cell type. Through a bioinformatical analysis of the data, a novel ALG-specific gene (here assigned as deathstar ) was identified. Immunostaining of deathstar in the central nervous system (CNS) showed its presence in specific regions of Drosophila ventral nerve cord, which previously has been characterized as ALG cells. Consistent with the bioinformatical analysis, deathstar -related signals were overlapped with the signals of the previously-reported ALG marker, Eaat1 , supporting its specific expression in ALG cells. At the physiological level, RNAi-mediated suppression of deathstar gene impeded the normal development of male flies without any effects on females. Cell type-specific expression of deathstar RNAi showed that deathstar gene affects locomotion behaviour and lifespan of D. melanogaster , in an ALG-specific manner. Conclusions Taken together, we showed that bioinformatical analysis of a previously reported expression data of Drosophila optic lobe successfully predicted the ALG-specific expression pattern of deathstar gene. Moreover, it was consistent with the ALG-specific effects of this gene on locomotion and lifespan of D. melanogaster, in vivo .


2019 ◽  
Author(s):  
Hadi Najafi ◽  
Kyle Wong ◽  
Woo Jae Kim

Abstract Background: Drosophila melanogaster is a proper model organism for studying the development and function of the nervous system. The Drosophila nervous system consists of distinct cell types with significant homologies to various cell types of more advanced organisms, including human. Among all cell types of the nervous system, astrocyte-like glia (ALG) have conserved functions to mammals and are essential for normal physiology and behaviours of the fly.Results: In this study, we exploited the gene expression profile of single cells in Drosophila optic lobe to identify the genes with specific expression pattern in each cell type. Through a bioinformatical analysis of the data, a novel ALG-specific gene (here assigned as deathstar) was identified. Immunostaining of deathstar in the central nervous system (CNS) showed its presence in specific regions of Drosophila ventral nerve cord, which previously has been characterized as ALG cells. Consistent with the bioinformatical analysis, deathstar-related signals were overlapped with the signals of the previously-reported ALG marker, Eaat1, supporting its specific expression in ALG cells. At the physiological level, RNAi-mediated suppression of deathstar gene impeded the normal development of male flies without any effects on females. Cell type-specific expression of deathstar RNAi showed that deathstar gene affects locomotion behaviour and lifespan of D. melanogaster, in an ALG-specific manner.Conclusions: Taken together, we showed that bioinformatical analysis of a previously reported expression data of Drosophila optic lobe successfully predicted the ALG-specific expression pattern of deathstar gene. Moreover, it was consistent with the ALG-specific effects of this gene on locomotion and lifespan of D. melanogaster, in vivo.


Viruses ◽  
2021 ◽  
Vol 13 (1) ◽  
pp. 91
Author(s):  
Verena Schultz ◽  
Stephanie L. Cumberworth ◽  
Quan Gu ◽  
Natasha Johnson ◽  
Claire L. Donald ◽  
...  

Understanding how Zika virus (Flaviviridae; ZIKV) affects neural cells is paramount in comprehending pathologies associated with infection. Whilst the effects of ZIKV in neural development are well documented, impact on the adult nervous system remains obscure. Here, we investigated the effects of ZIKV infection in established mature myelinated central nervous system (CNS) cultures. Infection incurred damage to myelinated fibers, with ZIKV-positive cells appearing when myelin damage was first detected as well as axonal pathology, suggesting the latter was a consequence of oligodendroglia infection. Transcriptome analysis revealed host factors that were upregulated during ZIKV infection. One such factor, CCL5, was validated in vitro as inhibiting myelination. Transferred UV-inactivated media from infected cultures did not damage myelin and axons, suggesting that viral replication is necessary to induce the observed effects. These data show that ZIKV infection affects CNS cells even after myelination—which is critical for saltatory conduction and neuronal function—has taken place. Understanding the targets of this virus across developmental stages including the mature CNS, and the subsequent effects of infection of cell types, is necessary to understand effective time frames for therapeutic intervention.


2021 ◽  
Vol 22 (6) ◽  
pp. 3233
Author(s):  
Christopher Kapitza ◽  
Rittika Chunder ◽  
Anja Scheller ◽  
Katherine S. Given ◽  
Wendy B. Macklin ◽  
...  

Multiple sclerosis (MS) has been considered to specifically affect the central nervous system (CNS) for a long time. As autonomic dysfunction including dysphagia can occur as accompanying phenomena in patients, the enteric nervous system has been attracting increasing attention over the past years. The aim of this study was to identify glial and myelin markers as potential target structures for autoimmune processes in the esophagus. RT-PCR analysis revealed glial fibrillary acidic protein (GFAP), proteolipid protein (PLP), and myelin basic protein (MBP) expression, but an absence of myelin oligodendrocyte glycoprotein (MOG) in the murine esophagus. Selected immunohistochemistry for GFAP, PLP, and MBP including transgenic mice with cell-type specific expression of PLP and GFAP supported these results by detection of (1) GFAP, PLP, and MBP in Schwann cells in skeletal muscle and esophagus; (2) GFAP, PLP, but no MBP in perisynaptic Schwann cells of skeletal and esophageal motor endplates; (3) GFAP and PLP, but no MBP in glial cells surrounding esophageal myenteric neurons; and (4) PLP, but no GFAP and MBP in enteric glial cells forming a network in the esophagus. Our results pave the way for further investigations regarding the involvement of esophageal glial cells in the pathogenesis of dysphagia in MS.


2021 ◽  
Vol 22 (11) ◽  
pp. 5793
Author(s):  
Brianna M. Quinville ◽  
Natalie M. Deschenes ◽  
Alex E. Ryckman ◽  
Jagdeep S. Walia

Sphingolipids are a specialized group of lipids essential to the composition of the plasma membrane of many cell types; however, they are primarily localized within the nervous system. The amphipathic properties of sphingolipids enable their participation in a variety of intricate metabolic pathways. Sphingoid bases are the building blocks for all sphingolipid derivatives, comprising a complex class of lipids. The biosynthesis and catabolism of these lipids play an integral role in small- and large-scale body functions, including participation in membrane domains and signalling; cell proliferation, death, migration, and invasiveness; inflammation; and central nervous system development. Recently, sphingolipids have become the focus of several fields of research in the medical and biological sciences, as these bioactive lipids have been identified as potent signalling and messenger molecules. Sphingolipids are now being exploited as therapeutic targets for several pathologies. Here we present a comprehensive review of the structure and metabolism of sphingolipids and their many functional roles within the cell. In addition, we highlight the role of sphingolipids in several pathologies, including inflammatory disease, cystic fibrosis, cancer, Alzheimer’s and Parkinson’s disease, and lysosomal storage disorders.


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