Evidence that ABC transporter-mediated autocrine export of an eicosanoid signaling molecule enhances germ cell chemotaxis in the colonial tunicate <i>Botryllus schlosseri</i>

Kassmer, Susannah H.; Rodriguez, Delany; Tomaso, Anthony W. De

doi:10.1242/dev.184663

Cited by 7 publications

(16 citation statements)

References 51 publications

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“…The amount of IA6 cells is not noticeably different between the two species (Additional file 9 : Fig. S4) [ 24 , 36 ]; thus, either the cell populations are different, and B. diegensis retains a mobile pluripotent somatic progenitor, or there is not an appropriate signal or niche for germline precursors to transdifferentiate in B. schlosseri .…”

Section: Discussionmentioning

confidence: 99%

Whole body regeneration and developmental competition in two botryllid ascidians

Nourizadeh

Kassmer

Rodriguez

et al. 2021

EvoDevo

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Background Botryllid ascidians are a group of marine invertebrate chordates that are colonial and grow by repeated rounds of asexual reproduction to form a colony of individual bodies, called zooids, linked by a common vascular network. Two distinct processes are responsible for zooid regeneration. In the first, called blastogenesis, new zooids arise from a region of multipotent epithelium from a pre-existing zooid. In the second, called whole body regeneration (WBR), mobile cells in the vasculature coalesce and are the source of the new zooid. In some botryllid species, blastogenesis and WBR occur concurrently, while in others, blastogenesis is used exclusively for growth, while WBR only occurs following injury or exiting periods of dormancy. In species such as Botrylloides diegensis, injury induced WBR is triggered by the surgical isolation of a small piece of vasculature. However, Botryllus schlosseri has unique requirements that must be met for successful injury induced WBR. Our goal was to understand why there would be different requirements between these two species. Results While WBR in B. diegensis was robust, we found that in B. schlosseri, new zooid growth following injury is unlikely due to circulatory cells, but instead a result of ectopic development of tissues leftover from the blastogenic process. These tissues could be whole, damaged, or partially resorbed developing zooids, and we defined the minimal amount of vascular biomass to support ectopic regeneration. We did find a common theme between the two species: a competitive process exists which results in only a single zooid reaching maturity following injury. We utilized this phenomenon and found that competition is reversible and mediated by circulating factors and/or cells. Conclusions We propose that WBR does not occur in B. schlosseri and that the unique requirements defined in other studies only serve to increase the chances of ectopic development. This is likely a response to injury as we have discovered a vascular-based reversible competitive mechanism which ensures that only a single zooid completes development. This competition has been described in other species, but the unique response of B. schlosseri to injury provides a new model to study resource allocation and competition within an individual.

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Section: Discussionmentioning

confidence: 99%

Whole body regeneration and developmental competition in two botryllid ascidians

Nourizadeh

Kassmer

Rodriguez

et al. 2021

EvoDevo

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“…Two broad and potentially interrelated hypothesises could explain the basis of germline parasitism: first, the winner GSCs could be faster at detecting, migrating to and occupying the developing germline niche; and/or there may be competition for maintaining access to the niche during gametogenesis. Using a combination of in vitro transwell migration assays and in vivo analyses, we had previously found that the migration of GSCs is controlled by a gradient of sphingosine-1-phosphate (S1P) secreted by the newly developing niche [20,21], and also…”

Section: Winner Gscs Have Increased Migration Capabilities Compared T...mentioning

confidence: 99%

“…that S1P chemotaxis may also be dependent on the generation of an autonomous gradient of the bioactive lipid, 12-S-HETE [21]. In order to characterize general migration mechanisms, these studies were done using multiple wild-type genotypes, without regard to the competitive phenotype of the individuals.…”

Section: Plos Onementioning

confidence: 99%

Increased collective migration correlates with germline stem cell competition in a basal chordate

Fentress,

De Tomaso

2023

PLoS ONE

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Cell competition is a process that compares the relative fitness of progenitor cells, resulting in winners, which contribute further to development, and losers, which are excluded, and is likely a universal quality control process that contributes to the fitness of an individual. Cell competition also has pathological consequences, and can create super-competitor cells responsible for tumor progression. We are studying cell competition during germline regeneration in the colonial ascidian, Botryllus schlosseri. Germline regeneration is due to the presence of germline stem cells (GSCs) which have a unique property: a competitive phenotype. When GSCs from one individual are transplanted into another, the donor and recipient cells compete for germline development. Often the donor GSCs win, and completely replace the gametes of the recipient- a process called germ cell parasitism (gcp). gcp is a heritable trait, and winner and loser genotypes can be found in nature and reared in the lab. However, the molecular and cellular mechanisms underlying gcp are unknown. Using an ex vivo migration assay, we show that GSCs isolated from winner genotypes migrate faster and in larger clusters than losers, and that cluster size correlates with expression of the Notch ligand, Jagged. Both cluster size and jagged expression can be manipulated simultaneously in a genotype dependent manner: treatment of loser GSCs with hepatocyte growth factor increases both jagged expression and cluster size, while inhibitors of the MAPK pathway decrease jagged expression and cluster size in winner GSCs. Live imaging in individuals transplanted with labeled winner and loser GSCs reveal that they migrate to the niche, some as small clusters, with the winners having a slight advantage in niche occupancy. Together, this suggests that the basis of GSC competition resides in a combination in homing ability and niche occupancy, and may be controlled by differential utilization of the Notch pathway.

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“…Colonial ascidians belonging to the genus Botrylloides are known for their whole-body regeneration (WBR) phenomenon, in which the entire colony regenerates from only a small portion of the vasculature [153][154][155]. Recently, Kassmer and collaborators [154] identified a population of bloodborne candidate SCs responsible for WBR in the species Botryllus schlosseri. These integrinalpha-6-positive (Ia6+) cells, which constantly divide in healthy colonies, also express genes associated with pluripotency.…”

Section: Tunicatesmentioning

confidence: 99%

Articulating the “stem cell niche” paradigm through the lens of non-model aquatic invertebrates

et al. 2022

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Stem cells (SCs) in vertebrates typically reside in “stem cell niches” (SCNs), morphologically restricted tissue microenvironments that are important for SC survival and proliferation. SCNs are broadly defined by properties including physical location, but in contrast to vertebrates and other “model” organisms, aquatic invertebrate SCs do not have clearly documented niche outlines or properties. Life strategies such as regeneration or asexual reproduction may have conditioned the niche architectural variability in aquatic or marine animal groups. By both establishing the invertebrates SCNs as independent types, yet allowing inclusiveness among them, the comparative analysis will allow the future functional characterization of SCNs.

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Evidence that ABC transporter-mediated autocrine export of an eicosanoid signaling molecule enhances germ cell chemotaxis in the colonial tunicate Botryllus schlosseri

Cited by 7 publications

References 51 publications

Whole body regeneration and developmental competition in two botryllid ascidians

Whole body regeneration and developmental competition in two botryllid ascidians

Increased collective migration correlates with germline stem cell competition in a basal chordate

Articulating the “stem cell niche” paradigm through the lens of non-model aquatic invertebrates

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