Simple Telomeres in a Simple Animal: Absence of Subtelomeric Repeat Regions in the Placozoan Trichoplax adhaerens

Infiltration of the endothelial layer of the blood-brain barrier by leukocytes plays a critical role in health and disease. When passing through the endothelial layer during the diapedesis process lymphocytes can either follow a paracellular route or a transcellular one. There is a debate whether these two processes constitute one mechanism, or they form two evolutionary distinct migration pathways. We used artificial intelligence, phylogenetic analysis, HH search, ancestor sequence reconstruction to investigate further this intriguing question. We found that the two systems share several ancient components, such as RhoA protein that plays a critical role in controlling actin movement in both mechanisms. However, some of the key components differ between these two transmigration processes. CAV1 genes emerged during Trichoplax adhaerens, and it was only reported in transcellular process. Paracellular process is dependent on PECAM1. PECAM1 emerged from FASL5 during Zebrafish divergence. Lastly, both systems employ late divergent genes such as ICAM1 and VECAM1. Taken together, our results suggest that these two systems constitute two different mechanical sensing mechanisms of immune cell infiltrations of the brain, yet these two systems are connected. We postulate that the mechanical properties of the cellular polarity is the main driving force determining the migration pathway. Our analysis indicates that both systems coevolved with immune cells, evolving to a higher level of complexity in association with the evolution of the immune system.

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Apicortin, a Constituent of Apicomplexan Conoid/Apical Complex and Its Tentative Role in Pathogen—Host Interaction

Tropical Medicine and Infectious Disease ◽

10.3390/tropicalmed6030118 ◽

2021 ◽

Vol 6 (3) ◽

pp. 118

Author(s):

Ferenc Orosz

Keyword(s):

Plasmodium Falciparum ◽

Toxoplasma Gondii ◽

Therapeutic Target ◽

In Silico ◽

Free Living ◽

Binding Properties ◽

Host Interactions ◽

Trichoplax Adhaerens ◽

Host Interaction ◽

Apical Complex

In 2009, apicortin was identified in silico as a characteristic protein of apicomplexans that also occurs in the placozoa, Trichoplax adhaerens. Since then, it has been found that apicortin also occurs in free-living cousins of apicomplexans (chromerids) and in flagellated fungi. It contains a partial p25-α domain and a doublecortin (DCX) domain, both of which have tubulin/microtubule binding properties. Apicortin has been studied experimentally in two very important apicomplexan pathogens, Toxoplasma gondii and Plasmodium falciparum. It is localized in the apical complex in both parasites. In T. gondii, apicortin plays a key role in shaping the structure of a special tubulin polymer, conoid. In both parasites, its absence or downregulation has been shown to impair pathogen–host interactions. Based on these facts, it has been suggested as a therapeutic target for treatment of malaria and toxoplasmosis.

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Born to sense: biophysical analyses of the oxygen sensing prolyl hydroxylase from the simplest animal Trichoplax adhaerens

Hypoxia ◽

10.2147/hp.s174655 ◽

2018 ◽

Vol Volume 6 ◽

pp. 57-71 ◽

Cited By ~ 3

Author(s):

Kerstin Lippl ◽

Anna Boleininger ◽

Michael McDonough ◽

Martine I. Abboud ◽

Hanna Tarhonskaya ◽

...

Keyword(s):

Oxygen Sensing ◽

Prolyl Hydroxylase ◽

Trichoplax Adhaerens

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Ultrafast epithelial contractions provide insights into contraction speed limits and tissue integrity

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1802934115 ◽

2018 ◽

Vol 115 (44) ◽

pp. E10333-E10341 ◽

Cited By ~ 23

Author(s):

Shahaf Armon ◽

Matthew Storm Bull ◽

Andres Aranda-Diaz ◽

Manu Prakash

Keyword(s):

Apical Cell ◽

Physiological Role ◽

Marine Animal ◽

Trichoplax Adhaerens ◽

Contraction Speed ◽

Order Of Magnitude ◽

Tissue Rupture ◽

Epithelial Layers ◽

Definition Of ◽

External Forces

By definition of multicellularity, all animals need to keep their cells attached and intact, despite internal and external forces. Cohesion between epithelial cells provides this key feature. To better understand fundamental limits of this cohesion, we study the epithelium mechanics of an ultrathin (∼25 μm) primitive marine animal Trichoplax adhaerens, composed essentially of two flat epithelial layers. With no known extracellular matrix and no nerves or muscles, T. adhaerens has been claimed to be the “simplest known living animal,” yet is still capable of coordinated locomotion and behavior. Here we report the discovery of the fastest epithelial cellular contractions known in any metazoan, to be found in T. adhaerens dorsal epithelium (50% shrinkage of apical cell area within one second, at least an order of magnitude faster than other known examples). Live imaging reveals emergent contractile patterns that are mostly sporadic single-cell events, but also include propagating contraction waves across the tissue. We show that cell contraction speed can be explained by current models of nonmuscle actin–myosin bundles without load, while the tissue architecture and unique mechanical properties are softening the tissue, minimizing the load on a contracting cell. We propose a hypothesis, in which the physiological role of the contraction dynamics is to resist external stresses while avoiding tissue rupture (“active cohesion”), a concept that can be further applied to engineering of active materials.

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Peer Review #2 of "Trichoplax adhaerens reveals a network of nuclear receptors sensitive to 9-cis-retinoic acid at the base of metazoan evolution (v0.2)"

10.7287/peerj.3789v0.2/reviews/2 ◽

2017 ◽

Author(s):

M Baker

Keyword(s):

Retinoic Acid ◽

Peer Review ◽

Nuclear Receptors ◽

Metazoan Evolution ◽

Trichoplax Adhaerens

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Para-cellular and transcellular diapedesis are divergent but inter-connected evolutionary events

10.1101/2020.09.21.307066 ◽

2020 ◽

Author(s):

Norwin Kubick ◽

Pavel Klimovich ◽

Patrick Henckel ◽

Michel-Edwar Mickael

Keyword(s):

Immune Cells ◽

Critical Role ◽

Adaptive Immune System ◽

Cellular Process ◽

Endothelial Layer ◽

Trichoplax Adhaerens ◽

Core Proteins ◽

Two Systems ◽

Sequence Reconstruction ◽

Migration Pathways

AbstractInfiltration of the endothelial layer of the blood-brain barrier by leukocytes plays a critical role in health and disease. When passing through the endothelial layer during the diapedesis process lymphocytes can either follow a para-cellular route or a transcellular one. There is a debate whether these two processes constitute one mechanism, or they form two evolutionary distinct migration pathways. We used phylogenetic analysis, HH search, ancestor sequence reconstruction together with functional specificity and positive selection analysis to investigate this intriguing question further. We found that the two systems share several ancient components, such as RhoA protein that plays an important role in controlling actin movement in both mechanisms. However, some of the key components differ between these two transmigration processes. CAV1 genes emerged during Trichoplax adhaerens and it was only reported in trans-cellular process. Para-cellular process core proteins had at least two distinct starting points. First, during drosophila emergence, Tre1 which is homologous to melatonin GPCR receptor diverged. Secondly, PECAM1 emerged from FASL5/3 during elephant shark divergence. Lastly, both systems employ late divergent genes such as ICAM1 and PECAM1. Taken together our results suggest that these two systems constitute different yet interconnected mechanisms of immune cells infiltrations of the brain. Our analysis indicates that this system coevolved with immune cells, evolving to a higher level of complexity in association with the evolution of the adaptive immune system.

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Transcriptome profiling of Trichoplax adhaerens highlights its digestive epithelium and a rich set of genes for fast electrogenic and slow neuromodulatory cellular signaling

10.21203/rs.2.14504/v1 ◽

2019 ◽

Cited By ~ 1

Author(s):

Yuen Yan Wong ◽

Phuong Le ◽

Wassim Elkhatib ◽

Thomas Piekut ◽

Adriano Senatore

Keyword(s):

Nervous System ◽

Intracellular Signaling ◽

Cellular Signaling ◽

Hydrolytic Enzymes ◽

Regulatory Peptides ◽

Transcriptome Profiling ◽

Protein Domain ◽

Trichoplax Adhaerens ◽

Interaction Domains ◽

And Behavior

Abstract Background Trichoplax adhaerens is a fascinating early-diverging animal that lacks a nervous system and synapses, and yet is capable of directed motile feeding behavior culminating in the external digestion of microorganisms by secreted hydrolytic enzymes. The mechanisms by which Trichoplax cells communicate with each other to coordinate their activity and behavior is unclear, though recent studies have suggested that secreted regulatory peptides might be involved.Results Here, we generated a high quality mRNA transcriptome of Trichoplax adhaerens , and predicted secreted proteins to identify gene homologues for digestion, development, immunity, cell adhesion, and peptide signaling. Detailed annotation of the expressed Trichoplax gene set also identified a nearly complete set of electrogenic genes involved in fast neural signalling, plus a set of 665 G-protein coupled receptors that in the nervous system integrate with fast signalling machinery to modulate cellular excitability. Furthermore, Trichoplax expresses an array of genes involved in intracellular signaling, including the key effector enzymes protein kinases A and C that functionally link fast and slow cellular signaling. Also identified were nearly complete sets of pre- and post-synaptic scaffolding genes, most encoding appropriate protein domain architectures. Notably, the Trichoplax proteome was found to bear slightly reduced counts of synaptic protein interaction domains such as PDZ, SH3 and C2 compared to other animals, but abundance of these domains did not appear to predict the presence of synapses in early-diverging groups.Conclusions Despite its apparent cellular and morphological simplicity, Trichoplax expresses a rich set of genes involved in complex animal traits. The transcriptome presented here adds a valuable additional resource for molecular studies on Trichoplax genes, exemplified by our ability to clone cDNAs for nine full-length acid sensing ion channel proteins with almost perfect matches with their corresponding transcriptome sequences.

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Ancient and conserved functional interplay between Bcl-2 family proteins in the mitochondrial pathway of apoptosis

Science Advances ◽

10.1126/sciadv.abc4149 ◽

2020 ◽

Vol 6 (40) ◽

pp. eabc4149 ◽

Cited By ~ 2

Author(s):

Nikolay Popgeorgiev ◽

Jaison D Sa ◽

Lea Jabbour ◽

Suresh Banjara ◽

Trang Thi Minh Nguyen ◽

...

Keyword(s):

Crystal Structure ◽

Ligand Binding ◽

Cancer Cells ◽

Mitochondrial Pathway ◽

Structural Basis ◽

Mitochondrial Outer Membrane ◽

Chemotherapy Treatment ◽

Trichoplax Adhaerens ◽

Binding Groove

In metazoans, Bcl-2 family proteins are major regulators of mitochondrially mediated apoptosis; however, their evolution remains poorly understood. Here, we describe the molecular characterization of the four members of the Bcl-2 family in the most primitive metazoan, Trichoplax adhaerens. All four trBcl-2 homologs are multimotif Bcl-2 group, with trBcl-2L1 and trBcl-2L2 being highly divergent antiapoptotic Bcl-2 members, whereas trBcl-2L3 and trBcl-2L4 are homologs of proapoptotic Bax and Bak, respectively. trBax expression permeabilizes the mitochondrial outer membrane, while trBak operates as a BH3-only sensitizer repressing antiapoptotic activities of trBcl-2L1 and trBcl-2L2. The crystal structure of a trBcl-2L2:trBak BH3 complex reveals that trBcl-2L2 uses the canonical Bcl-2 ligand binding groove to sequester trBak BH3, indicating that the structural basis for apoptosis control is conserved from T. adhaerens to mammals. Finally, we demonstrate that both trBax and trBak BH3 peptides bind selectively to human Bcl-2 homologs to sensitize cancer cells to chemotherapy treatment.

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