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

Paksa A, Bandemer J, Hoeckendorf B, Razin N, Tarbashevich K, Minina S, Meyen D, Biundo A, Leidel SA, Peyrieras N, Gov NS, Keller PJ, Raz E - Nat Commun (2016)

Bottom Line: Using primordial germ cells that participate in gonad formation, we present the developmental mechanisms maintaining a motile progenitor cell population at the site where the organ develops.Employing high-resolution live-cell microscopy, we find that repulsive cues coupled with physical barriers confine the cells to the correct bilateral positions.This analysis revealed that cell polarity changes on interaction with the physical barrier and that the establishment of compact clusters involves increased cell-cell interaction time.

View Article: PubMed Central - PubMed

Affiliation: Institute for Cell Biology, ZMBE, Von-Esmarch-Street 56, 48149 Muenster, Germany.

ABSTRACT
The precise positioning of organ progenitor cells constitutes an essential, yet poorly understood step during organogenesis. Using primordial germ cells that participate in gonad formation, we present the developmental mechanisms maintaining a motile progenitor cell population at the site where the organ develops. Employing high-resolution live-cell microscopy, we find that repulsive cues coupled with physical barriers confine the cells to the correct bilateral positions. This analysis revealed that cell polarity changes on interaction with the physical barrier and that the establishment of compact clusters involves increased cell-cell interaction time. Using particle-based simulations, we demonstrate the role of reflecting barriers, from which cells turn away on contact, and the importance of proper cell-cell adhesion level for maintaining the tight cell clusters and their correct positioning at the target region. The combination of these developmental and cellular mechanisms prevents organ fusion, controls organ positioning and is thus critical for its proper function.

No MeSH data available.


Related in: MedlinePlus

PGCs are motile at the gonad region.(a) PGCs migrate from four different positions in the embryo (green clusters in 6 hpf image) towards the developing gonads to form two separate cell clusters by end of the first day of embryonic development (lateral and dorsal views). Insets display higher magnification of the gonad region (white boxes). Scale bars represent 50 μm. (b) A schematic cross-section of a 1-day-old zebrafish embryo showing the somites (magenta), the two separate PGC clusters (green cells) located on either side of the developing gut (red structure), as well as the expression of cxcl12a at this stage (yellow). (c) Snapshots from a time-lapse movie (Supplementary Movie 2) showing a lateral view of a PGC cluster starting at 24 hpf In the first three time points posterior migration of a PGC is highlighted (green track) and lateral–medial migration of the same PGC is presented in the following panels (yellow track). Scale bar, 25 μm.
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f1: PGCs are motile at the gonad region.(a) PGCs migrate from four different positions in the embryo (green clusters in 6 hpf image) towards the developing gonads to form two separate cell clusters by end of the first day of embryonic development (lateral and dorsal views). Insets display higher magnification of the gonad region (white boxes). Scale bars represent 50 μm. (b) A schematic cross-section of a 1-day-old zebrafish embryo showing the somites (magenta), the two separate PGC clusters (green cells) located on either side of the developing gut (red structure), as well as the expression of cxcl12a at this stage (yellow). (c) Snapshots from a time-lapse movie (Supplementary Movie 2) showing a lateral view of a PGC cluster starting at 24 hpf In the first three time points posterior migration of a PGC is highlighted (green track) and lateral–medial migration of the same PGC is presented in the following panels (yellow track). Scale bar, 25 μm.

Mentions: Following their specification at four locations (Fig. 1a, left panel), zebrafish PGCs migrate toward the regions where the gonads develop, forming two clusters separated by the developing gut and ventral to the somites by the end of the first day of embryonic development (Fig. 1a, right panels and Fig. 1b; reviewed in ref. 25). Importantly, similar to other organogenesis processes, the progenitor cells that reached their migration target maintain their position and participate in the establishment of functional organs, gonad in this case1.


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

Paksa A, Bandemer J, Hoeckendorf B, Razin N, Tarbashevich K, Minina S, Meyen D, Biundo A, Leidel SA, Peyrieras N, Gov NS, Keller PJ, Raz E - Nat Commun (2016)

PGCs are motile at the gonad region.(a) PGCs migrate from four different positions in the embryo (green clusters in 6 hpf image) towards the developing gonads to form two separate cell clusters by end of the first day of embryonic development (lateral and dorsal views). Insets display higher magnification of the gonad region (white boxes). Scale bars represent 50 μm. (b) A schematic cross-section of a 1-day-old zebrafish embryo showing the somites (magenta), the two separate PGC clusters (green cells) located on either side of the developing gut (red structure), as well as the expression of cxcl12a at this stage (yellow). (c) Snapshots from a time-lapse movie (Supplementary Movie 2) showing a lateral view of a PGC cluster starting at 24 hpf In the first three time points posterior migration of a PGC is highlighted (green track) and lateral–medial migration of the same PGC is presented in the following panels (yellow track). Scale bar, 25 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4837475&req=5

f1: PGCs are motile at the gonad region.(a) PGCs migrate from four different positions in the embryo (green clusters in 6 hpf image) towards the developing gonads to form two separate cell clusters by end of the first day of embryonic development (lateral and dorsal views). Insets display higher magnification of the gonad region (white boxes). Scale bars represent 50 μm. (b) A schematic cross-section of a 1-day-old zebrafish embryo showing the somites (magenta), the two separate PGC clusters (green cells) located on either side of the developing gut (red structure), as well as the expression of cxcl12a at this stage (yellow). (c) Snapshots from a time-lapse movie (Supplementary Movie 2) showing a lateral view of a PGC cluster starting at 24 hpf In the first three time points posterior migration of a PGC is highlighted (green track) and lateral–medial migration of the same PGC is presented in the following panels (yellow track). Scale bar, 25 μm.
Mentions: Following their specification at four locations (Fig. 1a, left panel), zebrafish PGCs migrate toward the regions where the gonads develop, forming two clusters separated by the developing gut and ventral to the somites by the end of the first day of embryonic development (Fig. 1a, right panels and Fig. 1b; reviewed in ref. 25). Importantly, similar to other organogenesis processes, the progenitor cells that reached their migration target maintain their position and participate in the establishment of functional organs, gonad in this case1.

Bottom Line: Using primordial germ cells that participate in gonad formation, we present the developmental mechanisms maintaining a motile progenitor cell population at the site where the organ develops.Employing high-resolution live-cell microscopy, we find that repulsive cues coupled with physical barriers confine the cells to the correct bilateral positions.This analysis revealed that cell polarity changes on interaction with the physical barrier and that the establishment of compact clusters involves increased cell-cell interaction time.

View Article: PubMed Central - PubMed

Affiliation: Institute for Cell Biology, ZMBE, Von-Esmarch-Street 56, 48149 Muenster, Germany.

ABSTRACT
The precise positioning of organ progenitor cells constitutes an essential, yet poorly understood step during organogenesis. Using primordial germ cells that participate in gonad formation, we present the developmental mechanisms maintaining a motile progenitor cell population at the site where the organ develops. Employing high-resolution live-cell microscopy, we find that repulsive cues coupled with physical barriers confine the cells to the correct bilateral positions. This analysis revealed that cell polarity changes on interaction with the physical barrier and that the establishment of compact clusters involves increased cell-cell interaction time. Using particle-based simulations, we demonstrate the role of reflecting barriers, from which cells turn away on contact, and the importance of proper cell-cell adhesion level for maintaining the tight cell clusters and their correct positioning at the target region. The combination of these developmental and cellular mechanisms prevents organ fusion, controls organ positioning and is thus critical for its proper function.

No MeSH data available.


Related in: MedlinePlus