Repulsive cues combined with physical barriers and cell–cell adhesion determine progenitor cell positioning during organogenesis

Paksa, Azadeh; Bandemer, Jan; Hoeckendorf, Burkhard; Razin, Nitzan; Tarbashevich, Katsiaryna; Minina, Sofia; Meyen, Dana; Biundo, Antonio; Leidel, Sebastian A.; Peyriéras, Nadine; Gov, Nir S.; Keller, Philipp J.; Raz, Erez

doi:10.1038/ncomms11288

Cited by 45 publications

(48 citation statements)

References 72 publications

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“…Our work is motivated by observations that adhesive or repulsive cell-boundary interactions are significant during development. For instance, repulsive membranes are required for correct organ placement in zebrafish [25]. In this work, we formulate different biological boundary conditions for model (1.1), describing adhesive, repulsive, or neutral boundary interactions.…”

mentioning

confidence: 99%

Nonlocal Adhesion Models for Microorganisms on Bounded Domains

Hillen¹,

Buttenschön²

2020

SIAM J. Appl. Math.

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In 2006 Armstrong, Painter and Sherratt formulated a non-local differential equation model for cell-cell adhesion. For the one dimensional case we derive various types of adhesive, repulsive, and no-flux boundary conditions. We prove local and global existence and uniqueness for the resulting integro-differential equations. In numerical simulations we consider adhesive, repulsive and neutral boundary conditions and we show that the solutions mimic known behavior of fluid adhesion to boundaries. In addition, we observe interior pattern formation due to cell-cell adhesion.

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confidence: 99%

Nonlocal Adhesion Models for Microorganisms on Bounded Domains

Hillen¹,

Buttenschön²

2020

SIAM J. Appl. Math.

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“…What is less clear is whether the signals downstream of wunens and hmgcr exist in vertebrates, perhaps playing a more subtle role. Tantalising evidence of from zebrafish suggests this might be the case, with simultaneous knockdown of all the Wunen homologues causing some germ cells to mis-migrate (Paksa et al, 2016). Therefore, the cues that regulate Drosophila germ cell migration might actually be more conserved than we first thought.…”

Section: Discussionmentioning

confidence: 84%

Hmgcr promotes a long-range signal to attract germ cells which is aided by Wunens but independent ofhh

Kenwrick

Mukherjee

Renault

2018

Preprint

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StatementMigrating Drosophila germ cells are attracted by a long range Hmgcr mediated signal which is aided and acts simultaneously with Wunens suggesting that these pathways converge on a single chemoattractant. AbstractIn a developing embryo, many cell types migrate from their point of specification to their final position. This usually involves highly stereotyped routes which are determined through deployment of cell surface or secreted guidance molecules. Whilst genetic techniques have been successful in identifying these molecules, the distances over which such signals operate in their native context can be difficult to determine. Here we have quantified the range of an attractive signal for the migration of Drosophila germ cells. Their migration is guided by an attractive signal generated by the expression of genes in the 3-hydroxy-3-methyl-glutarylcoenzyme A reductase (Hmgcr) pathway, and by a repulsive signal generated by the expression of Wunens. We demonstrate that the attractive signal downstream of Hmgcr operates over a long range and is sufficient to reach germ cells for the entirety of their migration. Furthermore, Hmgcr-mediated attraction and Wunen-mediated repulsion can operate simultaneously ruling out a model in which these pathways operate consecutively.Indeed, we show that Hmgcr-mediated attraction is boosted by Wunens suggesting the action of these two pathways is linked. Lastly, several papers have pointed to the secreted molecule Hedgehog (Hh) as being the germ cell attractant, whose secretion is increased by hmgcr. In this paper, we provide evidence that Hh is not downstream of hmgcr in germ cell migration.

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“…While the ligand for Tre1 still unknown, the closest mammalian homolog, GPR84, binds to medium chain fatty acids. In Drosophila and zebrafish, lipid phosphate phosphatases are required for directed migration of germ cells 5,6 . To our knowledge, no other studies have addressed the role of lipids in germ cell migration in other species.…”

Section: Discussionmentioning

confidence: 99%

“…However, this mechanism appears to be conserved, as LPPs also repel germ cells away from nearby somites in the zebrafish 6 . Recently, our group discovered that migration of germ cells is directed by the lysophospholipid Sphingosine-1-phosphate (S1P) in the colonial ascidian Botryllus schlosseri 7 .…”

Section: Introductionmentioning

confidence: 99%

ABC-transporter activity and autocrine eicosanoid-signaling are required for germ cell migration a basal chordate

Kassmer¹,

Rodriguez²,

DeTomaso³

2018

Preprint

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In the colonial ascidian Botryllus schlosseri, long-lived germline stem cells (GSCs) migrate to new germline niches as they develop during repetitive cycles of asexual reproduction. ABC-transporters are involved in the export of lipid-signaling molecules, but their roles in germ cell migration are poorly understood. Here, we show that in Botryllus, abcc1 and abcb1 are highly expressed in germ cells, and inhibition of ABCtransporter activity leads to failure of germ cell migration. Phospholipase A2 (PLA2) produces arachidonic acid, which is further metabolized to eicosanoid signaling molecules. In humans, 12-lipoxygenase (LOX) metabolizes arachidonic acid to12-Hydroxyeicosatetraenoic acid (12-S-HETE), which stimulates migration of mammalian cancer cells and smooth muscle cells. We show that PLA2 and LOX activity are required for germ cell migration. A potential homolog to the human receptor for 12-S-HETE, BSgpr31, is expressed in germ cells. 12-S-HETE rescues migration towards S1P in the presence of inhibitors of ABCC1, ABCB1, PLA2 or LOX, and a gradient of 12-S-HETE enhances chemotaxis towards S1P and stimulates motility. We conclude that 12-S-HETE is a secondary chemoattractant exported by ACB-transporters that is required for migration of germ cells towards S1P. We also find that in the presence of S1P, detection of an 12-S-HETE gradient initiates an autologous positive feedback loop that may sustain migration. This is the first report of an eicosanoid-signaling molecule regulating germ cell migration.

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Repulsive cues combined with physical barriers and cell–cell adhesion determine progenitor cell positioning during organogenesis

Cited by 45 publications

References 72 publications

Nonlocal Adhesion Models for Microorganisms on Bounded Domains

Nonlocal Adhesion Models for Microorganisms on Bounded Domains

Hmgcr promotes a long-range signal to attract germ cells which is aided by Wunens but independent ofhh

ABC-transporter activity and autocrine eicosanoid-signaling are required for germ cell migration a basal chordate

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