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Cell kinetics during regeneration in the sponge Halisarca caerulea: how local is the response to tissue damage?

Alexander BE, Achlatis M, Osinga R, van der Geest HG, Cleutjens JP, Schutte B, de Goeij JM - PeerJ (2015)

Bottom Line: We demonstrate that during early regeneration, the growth fraction of the choanocytes (i.e., the percentage of proliferative cells) adjacent to the wound is reduced (7.0 ± 2.5%) compared to steady-state, undamaged tissue (46.6 ± 2.6%), while the length of the cell cycle remained short (5.6 ± 3.4 h).There was no difference in the number of proliferative mesohyl cells in regenerative sponges compared to steady-state sponges.The efficient allocation of limited resources to these life-history traits has enabled the ecological success and diversification of sponges.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Aquatic Ecology and Ecotoxicology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam , Amsterdam , The Netherlands ; Porifarma B.V. , Ede , The Netherlands.

ABSTRACT
Sponges have a remarkable capacity to rapidly regenerate in response to wound infliction. In addition, sponges rapidly renew their filter systems (choanocytes) to maintain a healthy population of cells. This study describes the cell kinetics of choanocytes in the encrusting reef sponge Halisarca caerulea during early regeneration (0-8 h) following experimental wound infliction. Subsequently, we investigated the spatial relationship between regeneration and cell proliferation over a six-day period directly adjacent to the wound, 1 cm, and 3 cm from the wound. Cell proliferation was determined by the incorporation of 5-bromo-2'-deoxyuridine (BrdU). We demonstrate that during early regeneration, the growth fraction of the choanocytes (i.e., the percentage of proliferative cells) adjacent to the wound is reduced (7.0 ± 2.5%) compared to steady-state, undamaged tissue (46.6 ± 2.6%), while the length of the cell cycle remained short (5.6 ± 3.4 h). The percentage of proliferative choanocytes increased over time in all areas and after six days of regeneration choanocyte proliferation rates were comparable to steady-state tissue. Tissue areas farther from the wound had higher rates of choanocyte proliferation than areas closer to the wound, indicating that more resources are demanded from tissue in the immediate vicinity of the wound. There was no difference in the number of proliferative mesohyl cells in regenerative sponges compared to steady-state sponges. Our data suggest that the production of collagen-rich wound tissue is a key process in tissue regeneration for H. caerulea, and helps to rapidly occupy the bare substratum exposed by the wound. Regeneration and choanocyte renewal are competing and negatively correlated life-history traits, both essential to the survival of sponges. The efficient allocation of limited resources to these life-history traits has enabled the ecological success and diversification of sponges.

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Changes in choanocyte proliferation rates over time in H. caerulea during regeneration.There are significantly less proliferative choanocytes closer to the wound compared to 1 cm and 3 cm from the wound (mean ± SE). The percentage of proliferative choanocytes increases over time in each tissue area. The percentages of proliferative choanocytes six days after damage, in tissue located 1 cm, and 3 cm from the wound, are comparable to the percentage of proliferative choanocytes found in steady-state H. caerulea specimens (grey area represents steady-state mean ± SE; data taken from Alexander and colleagues (2014)).
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fig-4: Changes in choanocyte proliferation rates over time in H. caerulea during regeneration.There are significantly less proliferative choanocytes closer to the wound compared to 1 cm and 3 cm from the wound (mean ± SE). The percentage of proliferative choanocytes increases over time in each tissue area. The percentages of proliferative choanocytes six days after damage, in tissue located 1 cm, and 3 cm from the wound, are comparable to the percentage of proliferative choanocytes found in steady-state H. caerulea specimens (grey area represents steady-state mean ± SE; data taken from Alexander and colleagues (2014)).

Mentions: Oscula in H. caerulea were located 1.4 ± 0.1 cm from each other. Therefore, tissue samples taken 1 cm from the wound were likely to be part of the same aquiferous module as the wound, but tissue taken 3 cm from the wound were likely to be from a separate module. Significantly less proliferative choanocytes were found closer to the wound (Fig. 4 and Table 2), i.e., less BrdU-positive choanocytes were found directly adjacent to the wound in comparison to 1 cm from the wound (mixed linear model, p < 0.001), and 1 cm compared to 3 cm from the wound (mixed linear model, p < 0.01). The percentage of proliferative choanocytes increased over time after wound infliction in all tissue areas (Fig. 4): directly adjacent to the wound (linear model, p < 0.01), 1 cm from the wound (linear model, p < 0.001), and 3 cm from the wound (linear model, p < 0.01). After six days of regeneration, there was no significant difference between choanocyte proliferation in steady-state H. caerulea tissue (17.6 ± 1.9%, data from Alexander et al., 2014) and tissue directly adjacent to the wound (12.8 ± 1.0%, linear model, p = 0.19), 1 cm from the wound (18.3 ± 0.4%, linear model, p = 0.99), and 3 cm from the wound (19.1 ± 0.5%, linear model, p = 0.94) (Fig. 4). On average, there are less BrdU-positive choanocytes directly adjacent to the wound after 6 days of regeneration compared to steady-state tissue (Fig. 4), although not statistically significant.


Cell kinetics during regeneration in the sponge Halisarca caerulea: how local is the response to tissue damage?

Alexander BE, Achlatis M, Osinga R, van der Geest HG, Cleutjens JP, Schutte B, de Goeij JM - PeerJ (2015)

Changes in choanocyte proliferation rates over time in H. caerulea during regeneration.There are significantly less proliferative choanocytes closer to the wound compared to 1 cm and 3 cm from the wound (mean ± SE). The percentage of proliferative choanocytes increases over time in each tissue area. The percentages of proliferative choanocytes six days after damage, in tissue located 1 cm, and 3 cm from the wound, are comparable to the percentage of proliferative choanocytes found in steady-state H. caerulea specimens (grey area represents steady-state mean ± SE; data taken from Alexander and colleagues (2014)).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4358696&req=5

fig-4: Changes in choanocyte proliferation rates over time in H. caerulea during regeneration.There are significantly less proliferative choanocytes closer to the wound compared to 1 cm and 3 cm from the wound (mean ± SE). The percentage of proliferative choanocytes increases over time in each tissue area. The percentages of proliferative choanocytes six days after damage, in tissue located 1 cm, and 3 cm from the wound, are comparable to the percentage of proliferative choanocytes found in steady-state H. caerulea specimens (grey area represents steady-state mean ± SE; data taken from Alexander and colleagues (2014)).
Mentions: Oscula in H. caerulea were located 1.4 ± 0.1 cm from each other. Therefore, tissue samples taken 1 cm from the wound were likely to be part of the same aquiferous module as the wound, but tissue taken 3 cm from the wound were likely to be from a separate module. Significantly less proliferative choanocytes were found closer to the wound (Fig. 4 and Table 2), i.e., less BrdU-positive choanocytes were found directly adjacent to the wound in comparison to 1 cm from the wound (mixed linear model, p < 0.001), and 1 cm compared to 3 cm from the wound (mixed linear model, p < 0.01). The percentage of proliferative choanocytes increased over time after wound infliction in all tissue areas (Fig. 4): directly adjacent to the wound (linear model, p < 0.01), 1 cm from the wound (linear model, p < 0.001), and 3 cm from the wound (linear model, p < 0.01). After six days of regeneration, there was no significant difference between choanocyte proliferation in steady-state H. caerulea tissue (17.6 ± 1.9%, data from Alexander et al., 2014) and tissue directly adjacent to the wound (12.8 ± 1.0%, linear model, p = 0.19), 1 cm from the wound (18.3 ± 0.4%, linear model, p = 0.99), and 3 cm from the wound (19.1 ± 0.5%, linear model, p = 0.94) (Fig. 4). On average, there are less BrdU-positive choanocytes directly adjacent to the wound after 6 days of regeneration compared to steady-state tissue (Fig. 4), although not statistically significant.

Bottom Line: We demonstrate that during early regeneration, the growth fraction of the choanocytes (i.e., the percentage of proliferative cells) adjacent to the wound is reduced (7.0 ± 2.5%) compared to steady-state, undamaged tissue (46.6 ± 2.6%), while the length of the cell cycle remained short (5.6 ± 3.4 h).There was no difference in the number of proliferative mesohyl cells in regenerative sponges compared to steady-state sponges.The efficient allocation of limited resources to these life-history traits has enabled the ecological success and diversification of sponges.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Aquatic Ecology and Ecotoxicology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam , Amsterdam , The Netherlands ; Porifarma B.V. , Ede , The Netherlands.

ABSTRACT
Sponges have a remarkable capacity to rapidly regenerate in response to wound infliction. In addition, sponges rapidly renew their filter systems (choanocytes) to maintain a healthy population of cells. This study describes the cell kinetics of choanocytes in the encrusting reef sponge Halisarca caerulea during early regeneration (0-8 h) following experimental wound infliction. Subsequently, we investigated the spatial relationship between regeneration and cell proliferation over a six-day period directly adjacent to the wound, 1 cm, and 3 cm from the wound. Cell proliferation was determined by the incorporation of 5-bromo-2'-deoxyuridine (BrdU). We demonstrate that during early regeneration, the growth fraction of the choanocytes (i.e., the percentage of proliferative cells) adjacent to the wound is reduced (7.0 ± 2.5%) compared to steady-state, undamaged tissue (46.6 ± 2.6%), while the length of the cell cycle remained short (5.6 ± 3.4 h). The percentage of proliferative choanocytes increased over time in all areas and after six days of regeneration choanocyte proliferation rates were comparable to steady-state tissue. Tissue areas farther from the wound had higher rates of choanocyte proliferation than areas closer to the wound, indicating that more resources are demanded from tissue in the immediate vicinity of the wound. There was no difference in the number of proliferative mesohyl cells in regenerative sponges compared to steady-state sponges. Our data suggest that the production of collagen-rich wound tissue is a key process in tissue regeneration for H. caerulea, and helps to rapidly occupy the bare substratum exposed by the wound. Regeneration and choanocyte renewal are competing and negatively correlated life-history traits, both essential to the survival of sponges. The efficient allocation of limited resources to these life-history traits has enabled the ecological success and diversification of sponges.

No MeSH data available.


Related in: MedlinePlus