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Corals Use Similar Immune Cells and Wound-Healing Processes as Those of Higher Organisms

Palmer CV, Traylor-Knowles NG, Willis BL, Bythell JC - PLoS ONE (2011)

Bottom Line: The four phases included (i) plug formation via the degranulation of melanin-containing granular cells; (ii) immune cell infiltration (inflammation); (iii) granular tissue formation (proliferation); and (iv) maturation.This study provides detailed documentation of the processes involved in scleractinian wound healing for the first time and further elucidates the roles of previously-described immune cells, such as fibroblasts.These results demonstrate the conservation of wound healing processes from anthozoans to humans.

Affiliation: ARC Centre of Excellence for Coral Reef Studies and School of Marine and Tropical Biology, James Cook University, Townsville, Queensland, Australia. caroline.palmer@jcu.edu.au

ABSTRACT

Sessile animals, like corals, frequently suffer physical injury from a variety of sources, thus wound-healing mechanisms that restore tissue integrity and prevent infection are vitally important for defence. Despite the ecological importance of reef-building corals, little is known about the cells and processes involved in wound healing in this group or in phylogenetically basal metazoans in general. A histological investigation into wound healing of the scleractinian coral Porites cylindrica at 0 h, 6 h, 24 h and 48 h after injury revealed differences in cellular components between injured and healthy tissues. Cell counts of the obligate endosymbiont, Symbiodinium, and melanin volume fraction analysis revealed rapid declines in both Symbiodinium abundance and tissue cross-sectional area occupied by melanin-containing granular cells after injury. Four phases of wound healing were identified, which are similar to phases described for both vertebrates and invertebrates. The four phases included (i) plug formation via the degranulation of melanin-containing granular cells; (ii) immune cell infiltration (inflammation); (iii) granular tissue formation (proliferation); and (iv) maturation. This study provides detailed documentation of the processes involved in scleractinian wound healing for the first time and further elucidates the roles of previously-described immune cells, such as fibroblasts. These results demonstrate the conservation of wound healing processes from anthozoans to humans.

A series of schematic diagrams representing the wound healing process between 0 and 48 h in P. cylindrica.1) Healthy coral tissue is composed of a surface body wall layer including the epidermis, a thin mesogloea and a gastrodermal layer. The epithelial layers are then mirrored on the other side of the gastrovascular cavity, to form the basal body wall, with a squamous epithelium forming the calicodermis. 2) Upon injury of the surface body wall epithelial layer, cell lysis and degranulation of melanin-containing granular cells starts to form a rudimentary clot, or plug. 3) Infiltration of granular amoebocytes, some potentially via the mesogloea, occurs at 6 h to form a cell barrier behind which melanin-containing granular cells aggregate, along with agranular amoebocytes and some fibroblasts. 4) At 24 h, infiltrated cells have begun to proliferate and the granular amoebocytes are reorientated and elongated to form an undifferentiated epidermis. 5) By 48 h, differentiation begins to occur and the epithelial layers begin to form from the lesion edge. The high abundance of amoebocytes and fibroblasts, potentially due to proliferation, is reduced by apoptosis.
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pone-0023992-g012: A series of schematic diagrams representing the wound healing process between 0 and 48 h in P. cylindrica.1) Healthy coral tissue is composed of a surface body wall layer including the epidermis, a thin mesogloea and a gastrodermal layer. The epithelial layers are then mirrored on the other side of the gastrovascular cavity, to form the basal body wall, with a squamous epithelium forming the calicodermis. 2) Upon injury of the surface body wall epithelial layer, cell lysis and degranulation of melanin-containing granular cells starts to form a rudimentary clot, or plug. 3) Infiltration of granular amoebocytes, some potentially via the mesogloea, occurs at 6 h to form a cell barrier behind which melanin-containing granular cells aggregate, along with agranular amoebocytes and some fibroblasts. 4) At 24 h, infiltrated cells have begun to proliferate and the granular amoebocytes are reorientated and elongated to form an undifferentiated epidermis. 5) By 48 h, differentiation begins to occur and the epithelial layers begin to form from the lesion edge. The high abundance of amoebocytes and fibroblasts, potentially due to proliferation, is reduced by apoptosis.

Mentions: A series of schematic diagrams (Figure 12), based on histological observations of wound healing in Porites cylindrica, depict the various stages that were observed. There were four discernable stages that relate to the established phases of wound healing identified in other animals (Figure 12, 2 to 5), from plug formation within the first hour post-injury, to wound maturation at 48 h post-injury.

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Corals Use Similar Immune Cells and Wound-Healing Processes as Those of Higher Organisms

Palmer CV, Traylor-Knowles NG, Willis BL, Bythell JC - PLoS ONE (2011)

A series of schematic diagrams representing the wound healing process between 0 and 48 h in P. cylindrica.1) Healthy coral tissue is composed of a surface body wall layer including the epidermis, a thin mesogloea and a gastrodermal layer. The epithelial layers are then mirrored on the other side of the gastrovascular cavity, to form the basal body wall, with a squamous epithelium forming the calicodermis. 2) Upon injury of the surface body wall epithelial layer, cell lysis and degranulation of melanin-containing granular cells starts to form a rudimentary clot, or plug. 3) Infiltration of granular amoebocytes, some potentially via the mesogloea, occurs at 6 h to form a cell barrier behind which melanin-containing granular cells aggregate, along with agranular amoebocytes and some fibroblasts. 4) At 24 h, infiltrated cells have begun to proliferate and the granular amoebocytes are reorientated and elongated to form an undifferentiated epidermis. 5) By 48 h, differentiation begins to occur and the epithelial layers begin to form from the lesion edge. The high abundance of amoebocytes and fibroblasts, potentially due to proliferation, is reduced by apoptosis.
© Copyright Policy
pone-0023992-g012: A series of schematic diagrams representing the wound healing process between 0 and 48 h in P. cylindrica.1) Healthy coral tissue is composed of a surface body wall layer including the epidermis, a thin mesogloea and a gastrodermal layer. The epithelial layers are then mirrored on the other side of the gastrovascular cavity, to form the basal body wall, with a squamous epithelium forming the calicodermis. 2) Upon injury of the surface body wall epithelial layer, cell lysis and degranulation of melanin-containing granular cells starts to form a rudimentary clot, or plug. 3) Infiltration of granular amoebocytes, some potentially via the mesogloea, occurs at 6 h to form a cell barrier behind which melanin-containing granular cells aggregate, along with agranular amoebocytes and some fibroblasts. 4) At 24 h, infiltrated cells have begun to proliferate and the granular amoebocytes are reorientated and elongated to form an undifferentiated epidermis. 5) By 48 h, differentiation begins to occur and the epithelial layers begin to form from the lesion edge. The high abundance of amoebocytes and fibroblasts, potentially due to proliferation, is reduced by apoptosis.
Mentions: A series of schematic diagrams (Figure 12), based on histological observations of wound healing in Porites cylindrica, depict the various stages that were observed. There were four discernable stages that relate to the established phases of wound healing identified in other animals (Figure 12, 2 to 5), from plug formation within the first hour post-injury, to wound maturation at 48 h post-injury.

Bottom Line: The four phases included (i) plug formation via the degranulation of melanin-containing granular cells; (ii) immune cell infiltration (inflammation); (iii) granular tissue formation (proliferation); and (iv) maturation.This study provides detailed documentation of the processes involved in scleractinian wound healing for the first time and further elucidates the roles of previously-described immune cells, such as fibroblasts.These results demonstrate the conservation of wound healing processes from anthozoans to humans.

Affiliation: ARC Centre of Excellence for Coral Reef Studies and School of Marine and Tropical Biology, James Cook University, Townsville, Queensland, Australia. caroline.palmer@jcu.edu.au

ABSTRACT

Sessile animals, like corals, frequently suffer physical injury from a variety of sources, thus wound-healing mechanisms that restore tissue integrity and prevent infection are vitally important for defence. Despite the ecological importance of reef-building corals, little is known about the cells and processes involved in wound healing in this group or in phylogenetically basal metazoans in general. A histological investigation into wound healing of the scleractinian coral Porites cylindrica at 0 h, 6 h, 24 h and 48 h after injury revealed differences in cellular components between injured and healthy tissues. Cell counts of the obligate endosymbiont, Symbiodinium, and melanin volume fraction analysis revealed rapid declines in both Symbiodinium abundance and tissue cross-sectional area occupied by melanin-containing granular cells after injury. Four phases of wound healing were identified, which are similar to phases described for both vertebrates and invertebrates. The four phases included (i) plug formation via the degranulation of melanin-containing granular cells; (ii) immune cell infiltration (inflammation); (iii) granular tissue formation (proliferation); and (iv) maturation. This study provides detailed documentation of the processes involved in scleractinian wound healing for the first time and further elucidates the roles of previously-described immune cells, such as fibroblasts. These results demonstrate the conservation of wound healing processes from anthozoans to humans.

View Similar Images In: Results  - Collection
View Article: MedlinePlus - PubMed Central -  PubMed
Show All Figures - Show MeSH
getmorefigures.php?pmc=3161096&rFormat=json&query=the&fields=all&favor=none&it=none&sp=none&sub=none&req=5