Paracellular and Transcellular Leukocytes Diapedesis Are Divergent but Interconnected Evolutionary Events

Mickael, Michel‐Edwar; Kubick, Norwin; Klimovich, Pavel; Flournoy, Patrick Henckell; Bieńkowska, Irmina; Sacharczuk, Mariusz

doi:10.3390/genes12020254

Cited by 20 publications

(21 citation statements)

References 91 publications

(110 reference statements)

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“…Phylogenetic investigation was done in two steps [2,27,28]. First, IL family amino acid sequences were aligned using MAFFT using the iterative refinement method (FFT-NS-i).…”

Section: Alignment and Phylogenetic Analysismentioning

confidence: 99%

“…We applied the maximum likelihood method to infer the ancestral sequence of each of the proteins investigated. For each protein, we used the ASR algorithm implemented in MEGA6 to build ancestral sequences [2,29]. This was followed by BlastP against the nearest earlier diverging organism.…”

Section: Ancestral Sequence Reconstruction (Asr)mentioning

confidence: 99%

“…The HHsearch method was used to examine the evolutionary history of the ILs. Only proteins that have already diverged before the most ancient members of the family were considered as candidate parents [2,27].…”

Section: Hhsearchmentioning

confidence: 99%

“…Lower invertebrates are capable of defending themselves against pathogens using three main mechanisms: (i) pattern recognition receptors that allow nonspecific recognition of microbes, (ii) a phagocyte response that helps them eliminate foreign microbes, and (iii) cellular and biochemical factors such as the production of antimicrobial peptides that lyse cells, and ROS that target DNA [1]. The adaptive immune system first appeared in lampreys and hagfish [2]. Vertebrates' adaptive immune system recognizes antigens with high specificity and applies appropriate responses against them.…”

Section: Introductionmentioning

confidence: 99%

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Interleukins and Interleukin Receptors Evolutionary History and Origin in Relation to CD4+ T Cell Evolution

Kubick

Klimovich²,

Flournoy³

et al. 2021

Genes

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Understanding the evolution of interleukins and interleukin receptors is essential to control the function of CD4+ T cells in various pathologies. Numerous aspects of CD4+ T cells’ presence are controlled by interleukins including differentiation, proliferation, and plasticity. CD4+ T cells have emerged during the divergence of jawed vertebrates. However, little is known about the evolution of interleukins and their origin. We traced the evolution of interleukins and their receptors from Placozoa to primates. We performed phylogenetic analysis, ancestral reconstruction, HH search, and positive selection analysis. Our results indicated that various interleukins' emergence predated CD4+ T cells divergence. IL14 was the most ancient interleukin with homologs in fungi. Invertebrates also expressed various interleukins such as IL41 and IL16. Several interleukin receptors also appeared before CD4+ T cells divergence. Interestingly IL17RA and IL17RD, which are known to play a fundamental role in Th17 CD4+ T cells first appeared in mollusks. Furthermore, our investigations showed that there is not any single gene family that could be the parent group of interleukins. We postulate that several groups have diverged from older existing cytokines such as IL4 from TGFβ, IL10 from IFN, and IL28 from BCAM. Interleukin receptors were less divergent than interleukins. We found that IL1R, IL7R might have diverged from a common invertebrate protein that contained TIR domains, conversely, IL2R, IL4R and IL6R might have emerged from a common invertebrate ancestor that possessed a fibronectin domain. IL8R seems to be a GPCR that belongs to the rhodopsin-like family and it has diverged from the Somatostatin group. Interestingly, several interleukins that are known to perform a critical function for CD4+ T cells such as IL6, IL17, and IL1B have gained new functions and evolved under positive selection. Overall evolution of interleukin receptors was not under significant positive selection. Interestingly, eight interleukin families appeared in lampreys, however, only two of them (IL17B, IL17E) evolved under positive selection. This observation indicates that although lampreys have a unique adaptive immune system that lacks CD4+ T cells, they could be utilizing interleukins in homologous mode to that of the vertebrates' immune system. Overall our study highlights the evolutionary heterogeneity within the interleukins and their receptor superfamilies and thus does not support the theory that interleukins evolved solely in jawed vertebrates to support T cell function. Conversely, some of the members are likely to play conserved functions in the innate immune system.

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“…Phylogenetic investigation was done in two steps [2,27,28]. First, IL family amino acid sequences were aligned using MAFFT using the iterative refinement method (FFT-NS-i).…”

Section: Alignment and Phylogenetic Analysismentioning

confidence: 99%

Section: Ancestral Sequence Reconstruction (Asr)mentioning

confidence: 99%

Section: Hhsearchmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Interleukins and Interleukin Receptors Evolutionary History and Origin in Relation to CD4+ T Cell Evolution

Kubick

Klimovich²,

Flournoy³

et al. 2021

Genes

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“…However a glial BBB like structure was detected, together with CAV1. We as well as other have shown that CAV1 and PECAM1 play an indispensable role in BBB diapedesis 21 . Interestingly, drosophila melanogaster does not express either CAV1 or PECAM1 which are vital for transcellular and paracellular diapedesis.…”

Section: Role Of Tre1 and Moody In Bbbmentioning

confidence: 53%

Evolutionary history and origin of Tre1 superfamily shed light on its role in regulating blood brain barrier

Kubick

Klimovich²,

Bieńkowska

et al. 2021

Preprint

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Understanding how the evolutionary relationship between immune cells and the blood-brain is important to devise therapeutic strategies that can regulate their critical function. In vertebrates, immune cells follow either a paracellular or transcellular pathway to infiltrate the BBB. In drosophila glial cells form the BBB that regulates the access of immune-like cells to the drosophila brain. However, it is still not known which route immune-like cells follow to infiltrate the drosophila brain. In vertebrates, paracellular migration is dependent on PECAM1, while transcellular migration is dependent on the expression of CAV1. Interestingly drosophila genome lacks both genes. Tre1 superfamily (Tre1, Moody, and Dmel_CG4313) play a diverse role in regulating transepithelial migration in drosophila. However, its evolutionary history and origin are not yet known. We performed phylogenetic analysis, together with HH search, positive selection, and ancestral reconstruction to investigate the Tre1 family Interestingly we found that Tre1 exists in mollusks, insects, ambulacria, and sclaidphora. Moody is shown to be a more ancient protein and it existed since cnidaria emergence and has a homolog (GPCR84) in mammals. The third family member (Dmel_CG4313) only exists in insects. The origin of the family seems to be related to the rhodopsin-like family and in particular family α. We found that opsin is the nearest receptor to have a common ancestor with the Tre1 superfamily that seems to have diverged in sponges. We investigated the positive selection of the Tre1 family using PAML. Tre1 seems to have evolved under negative selection, whereas Moody has evolved during positive selection. The sites that we found under positive selection are Likely to play a role in the speciation of function in the case of Moody. We have identified an SH3, in Tre1 and, moody and Dmel_CG4313. Sh3 is known to play a fundamental role in regulating actin movement in a Rho-dependent manner. We suggest that Tre1 could be playing an important role in paracellular diapedesis in drosophila.

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Distribution changes of non‐self‐test cells and self‐tunic cells surrounding the outer body during Ciona metamorphosis

Totsuka,

Kuwana,

Sawai

et al. 2023

Developmental Dynamics

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Background: Ascidians significantly change their body structure through metamorphosis, but the spatio‐temporal cell dynamics in the early metamorphosis stage has not been clarified. A natural Ciona embryo is surrounded by maternally derived non‐self‐test cells before metamorphosis. However, after metamorphosis, the juvenile is surrounded by self‐tunic cells derived from mesenchymal cell lineages. Both test cells and tunic cells are thought to be changed their distributions during metamorphosis, but the precise timing is unknown.Results: Using a metamorphosis induction by mechanical stimulation, we investigated the dynamics of mesenchymal cells during metamorphosis in a precise time course. After the stimulation, two‐round Ca2+ transients were observed. Migrating mesenchymal cells came out through the epidermis within 10 min after the second phase. We named this event “cell extravasation.” The cell extravasation occurred at the same time as the backward movement of posterior trunk epidermal cells. Timelapse imaging of transgenic‐line larva revealed that non‐self‐test cells and self‐tunic cells temporarily coexist outside the body until the test cells are eliminated. At the juvenile stage, only extravasated self‐tunic cells remained outside the body.Conclusions: We found that mesenchymal cells extravasated following two‐round Ca2+ transients, and distributions of test cells and tunic cells changed in the outer body after tail regression.

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Paracellular and Transcellular Leukocytes Diapedesis Are Divergent but Interconnected Evolutionary Events

Cited by 20 publications

References 91 publications

Interleukins and Interleukin Receptors Evolutionary History and Origin in Relation to CD4+ T Cell Evolution

Interleukins and Interleukin Receptors Evolutionary History and Origin in Relation to CD4+ T Cell Evolution

Evolutionary history and origin of Tre1 superfamily shed light on its role in regulating blood brain barrier

Distribution changes of non‐self‐test cells and self‐tunic cells surrounding the outer body during Ciona metamorphosis

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