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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.

No MeSH data available.


Choanocyte cell kinetics in early regenerative and steady-state tissue of H. caerulea.Steady-state data were obtained from De Goeij and colleagues (2009). In both tissues, the percentage of BrdU-positive choanocytes (mean ± SE) increased over time until a maximum was reached, representing the growth fraction (GF), i.e., the percentage of choanocytes involved in proliferation. The growth fraction of choanocytes in early regenerative tissue was substantially lower than the growth fraction of choanocytes in steady-state tissue. The duration of the linear increase represents the length of the cell cycle, which was similar in regenerative and steady-state sponges. The lines are the least squares fit obtained using the conditions of the ‘one population model’ described by Nowakowski and colleagues (1989).
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fig-3: Choanocyte cell kinetics in early regenerative and steady-state tissue of H. caerulea.Steady-state data were obtained from De Goeij and colleagues (2009). In both tissues, the percentage of BrdU-positive choanocytes (mean ± SE) increased over time until a maximum was reached, representing the growth fraction (GF), i.e., the percentage of choanocytes involved in proliferation. The growth fraction of choanocytes in early regenerative tissue was substantially lower than the growth fraction of choanocytes in steady-state tissue. The duration of the linear increase represents the length of the cell cycle, which was similar in regenerative and steady-state sponges. The lines are the least squares fit obtained using the conditions of the ‘one population model’ described by Nowakowski and colleagues (1989).

Mentions: The mouse intestine and sponge positive control tissues showed BrdU-positive nuclei. Negative controls (no primary antibody) and tissue samples at t = 0 (not labeled with BrdU) showed no BrdU-positive cells. The cell cycle parameters of the choanocyte population directly adjacent to the wound in early regenerative tissue were compared to choanocyte cell kinetics from H. caerulea in steady-state (data obtained from De Goeij et al., 2009) (Fig. 3 and Table 1). The number of BrdU-positive choanocytes in damaged sponges and steady-state sponges increased linearly until a maximum was reached, after which all proliferative choanocytes had been labeled and had re-entered the S-phase (Fig. 3). This maximum represents the growth fraction, i.e., the percentage of the total population of choanocytes that are proliferative, which was greatly reduced in damaged sponges (7.0 ± 2.5%) compared to steady-state sponges (46.6 ± 2.6%) (Fig. 3 and Table 1). However, the cell cycle (Tc) of choanocytes adjacent to the wound in damaged sponges was similar in length to the cell cycle of choanocytes from steady-state sponges (5.6 ± 3.4 h vs 5.9 ± 0.4 h respectively) (Fig. 3 and Table 1).


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)

Choanocyte cell kinetics in early regenerative and steady-state tissue of H. caerulea.Steady-state data were obtained from De Goeij and colleagues (2009). In both tissues, the percentage of BrdU-positive choanocytes (mean ± SE) increased over time until a maximum was reached, representing the growth fraction (GF), i.e., the percentage of choanocytes involved in proliferation. The growth fraction of choanocytes in early regenerative tissue was substantially lower than the growth fraction of choanocytes in steady-state tissue. The duration of the linear increase represents the length of the cell cycle, which was similar in regenerative and steady-state sponges. The lines are the least squares fit obtained using the conditions of the ‘one population model’ described by Nowakowski and colleagues (1989).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig-3: Choanocyte cell kinetics in early regenerative and steady-state tissue of H. caerulea.Steady-state data were obtained from De Goeij and colleagues (2009). In both tissues, the percentage of BrdU-positive choanocytes (mean ± SE) increased over time until a maximum was reached, representing the growth fraction (GF), i.e., the percentage of choanocytes involved in proliferation. The growth fraction of choanocytes in early regenerative tissue was substantially lower than the growth fraction of choanocytes in steady-state tissue. The duration of the linear increase represents the length of the cell cycle, which was similar in regenerative and steady-state sponges. The lines are the least squares fit obtained using the conditions of the ‘one population model’ described by Nowakowski and colleagues (1989).
Mentions: The mouse intestine and sponge positive control tissues showed BrdU-positive nuclei. Negative controls (no primary antibody) and tissue samples at t = 0 (not labeled with BrdU) showed no BrdU-positive cells. The cell cycle parameters of the choanocyte population directly adjacent to the wound in early regenerative tissue were compared to choanocyte cell kinetics from H. caerulea in steady-state (data obtained from De Goeij et al., 2009) (Fig. 3 and Table 1). The number of BrdU-positive choanocytes in damaged sponges and steady-state sponges increased linearly until a maximum was reached, after which all proliferative choanocytes had been labeled and had re-entered the S-phase (Fig. 3). This maximum represents the growth fraction, i.e., the percentage of the total population of choanocytes that are proliferative, which was greatly reduced in damaged sponges (7.0 ± 2.5%) compared to steady-state sponges (46.6 ± 2.6%) (Fig. 3 and Table 1). However, the cell cycle (Tc) of choanocytes adjacent to the wound in damaged sponges was similar in length to the cell cycle of choanocytes from steady-state sponges (5.6 ± 3.4 h vs 5.9 ± 0.4 h respectively) (Fig. 3 and Table 1).

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.