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Skin healing and scale regeneration in fed and unfed sea bream, Sparus auratus

Vieira FA, Gregório SF, Ferraresso S, Thorne MA, Costa R, Milan M, Bargelloni L, Clark MS, Canario AV, Power DM - BMC Genomics (2011)

Bottom Line: The identification of numerous genes involved in the mitotic checkpoint and cell proliferation indicate that the experimental procedure may be useful for understanding cell proliferation and control in vertebrates within the context of the whole animal physiology.In response to skin damage genes of immune surveillance were up-regulated along with others involved in tissue regeneration required to rapidly re-establish barrier function.Additionally, candidate fish genes were identified that may be involved in cytoskeletal re-modelling, mineralization and stem cells, which are of potential use in aquaculture and fish husbandry, as they may impact on the ability of the fish to produce structural proteins, such as muscle, efficiently.

Affiliation: Comparative and Molecular Endocrinology Group, Centre for Marine Sciences (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal. fvieira@ualg.pt

ABSTRACT

Background: Fish scales are an important reservoir of calcium and phosphorus and together with the skin function as an integrated barrier against environmental changes and external aggressors. Histological studies have revealed that the skin and scales regenerate rapidly in fish when they are lost or damaged. In the present manuscript the histological and molecular changes underlying skin and scale regeneration in fed and fasted sea bream (Sparus auratus) were studied using a microarray 3 and 7 days after scale removal to provide a comprehensive molecular understanding of the early stages of these processes.

Results: Histological analysis of skin/scales revealed 3 days after scale removal re-epithelisation and formation of the scale pocket had occurred and 53 and 109 genes showed significant up or down-regulation, respectively. Genes significantly up-regulated were involved in cell cycle regulation, cell proliferation and adhesion, immune response and antioxidant activities. 7 days after scale removal a thin regenerated scale was visible and only minor changes in gene expression occurred. In animals that were fasted to deplete mineral availability the expression profiles centred on maintaining energy homeostasis. The utilisation of fasting as a treatment emphasised the competing whole animal physiological requirements with regard to barrier repair, infection control and energy homeostasis.

Conclusions: The identification of numerous genes involved in the mitotic checkpoint and cell proliferation indicate that the experimental procedure may be useful for understanding cell proliferation and control in vertebrates within the context of the whole animal physiology. In response to skin damage genes of immune surveillance were up-regulated along with others involved in tissue regeneration required to rapidly re-establish barrier function. Additionally, candidate fish genes were identified that may be involved in cytoskeletal re-modelling, mineralization and stem cells, which are of potential use in aquaculture and fish husbandry, as they may impact on the ability of the fish to produce structural proteins, such as muscle, efficiently.

Longitudinal transverse sections (5 μm) of sea bream skin from each of the experimental groups. A) Removal of scale; B) N (control); C) 3WS (without scales day 3); D) 7WS (without scales day 7); E) amplification of 7WS (without scales day 7); F) 3STWS (fasted without scales day 3); G) 7STWS (fasted without scales day 7); H) 3ST (fasted day 3) and I) 7ST (fasted day 7) stained with Masson's Trichrome. The posterior region of the scale is orientated to the right. Connective tissue is stained green and mineralized and collagen-rich tissues are stained bright red. Sc - scale; scp - scale pocket; ep - epidermis; dm - dermis; hypdm - hypodermis and mc - muscle are indicated. Scale bars: A,B,C,D,F,G,H - 200 μm; E - 50 μm.
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Figure 1: Longitudinal transverse sections (5 μm) of sea bream skin from each of the experimental groups. A) Removal of scale; B) N (control); C) 3WS (without scales day 3); D) 7WS (without scales day 7); E) amplification of 7WS (without scales day 7); F) 3STWS (fasted without scales day 3); G) 7STWS (fasted without scales day 7); H) 3ST (fasted day 3) and I) 7ST (fasted day 7) stained with Masson's Trichrome. The posterior region of the scale is orientated to the right. Connective tissue is stained green and mineralized and collagen-rich tissues are stained bright red. Sc - scale; scp - scale pocket; ep - epidermis; dm - dermis; hypdm - hypodermis and mc - muscle are indicated. Scale bars: A,B,C,D,F,G,H - 200 μm; E - 50 μm.

Mentions: Transverse sections of skin from all the experimental groups at both time points (days 3 and 7) of the experiment were analysed (Figure 1). Sea bream skin had the typical organisation of teleost skin and was composed of three well defined layers: the epidermis, dermis and hypodermis which overlaid a fat layer that varied in thickness. The scales were each enclosed within a scale pocket and were composed of a mineralized external layer and a partially mineralized basal plate. The scale pocket was localized in the superficial dermis and projected into and was covered by a thin layer of epidermis (Figure 1B, H and 1I). Removal of the scales damaged the epidermis, dermis and scale pocket, the latter two tissues became exposed to the ambient water and the epidermis which remained attached to the dermis hung loose (Figure 1A). The ontogeny of the regenerative response was similar in all sea bream. Histology of the day 3 samples revealed a rapid repair process, with the epidermis already re-established and the enclosed scale pocket without a scale was visible in the dermis (Figure 1C and 1F). Hence within 3 days, the animals had re-established their external barrier and protection to the environment and 7 days after scale removal a thin regenerated scale was visible (Figure 1D, E and 1G). From a morphological perspective the regeneration process in sea bream was similar to that described in the cichlid Hemichromis bimaculatus [1,30] and also in zebrafish and goldfish [8,18].

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Skin healing and scale regeneration in fed and unfed sea bream, Sparus auratus

Vieira FA, Gregório SF, Ferraresso S, Thorne MA, Costa R, Milan M, Bargelloni L, Clark MS, Canario AV, Power DM - BMC Genomics (2011)

Longitudinal transverse sections (5 μm) of sea bream skin from each of the experimental groups. A) Removal of scale; B) N (control); C) 3WS (without scales day 3); D) 7WS (without scales day 7); E) amplification of 7WS (without scales day 7); F) 3STWS (fasted without scales day 3); G) 7STWS (fasted without scales day 7); H) 3ST (fasted day 3) and I) 7ST (fasted day 7) stained with Masson's Trichrome. The posterior region of the scale is orientated to the right. Connective tissue is stained green and mineralized and collagen-rich tissues are stained bright red. Sc - scale; scp - scale pocket; ep - epidermis; dm - dermis; hypdm - hypodermis and mc - muscle are indicated. Scale bars: A,B,C,D,F,G,H - 200 μm; E - 50 μm.
© Copyright Policy
Figure 1: Longitudinal transverse sections (5 μm) of sea bream skin from each of the experimental groups. A) Removal of scale; B) N (control); C) 3WS (without scales day 3); D) 7WS (without scales day 7); E) amplification of 7WS (without scales day 7); F) 3STWS (fasted without scales day 3); G) 7STWS (fasted without scales day 7); H) 3ST (fasted day 3) and I) 7ST (fasted day 7) stained with Masson's Trichrome. The posterior region of the scale is orientated to the right. Connective tissue is stained green and mineralized and collagen-rich tissues are stained bright red. Sc - scale; scp - scale pocket; ep - epidermis; dm - dermis; hypdm - hypodermis and mc - muscle are indicated. Scale bars: A,B,C,D,F,G,H - 200 μm; E - 50 μm.
Mentions: Transverse sections of skin from all the experimental groups at both time points (days 3 and 7) of the experiment were analysed (Figure 1). Sea bream skin had the typical organisation of teleost skin and was composed of three well defined layers: the epidermis, dermis and hypodermis which overlaid a fat layer that varied in thickness. The scales were each enclosed within a scale pocket and were composed of a mineralized external layer and a partially mineralized basal plate. The scale pocket was localized in the superficial dermis and projected into and was covered by a thin layer of epidermis (Figure 1B, H and 1I). Removal of the scales damaged the epidermis, dermis and scale pocket, the latter two tissues became exposed to the ambient water and the epidermis which remained attached to the dermis hung loose (Figure 1A). The ontogeny of the regenerative response was similar in all sea bream. Histology of the day 3 samples revealed a rapid repair process, with the epidermis already re-established and the enclosed scale pocket without a scale was visible in the dermis (Figure 1C and 1F). Hence within 3 days, the animals had re-established their external barrier and protection to the environment and 7 days after scale removal a thin regenerated scale was visible (Figure 1D, E and 1G). From a morphological perspective the regeneration process in sea bream was similar to that described in the cichlid Hemichromis bimaculatus [1,30] and also in zebrafish and goldfish [8,18].

Bottom Line: The identification of numerous genes involved in the mitotic checkpoint and cell proliferation indicate that the experimental procedure may be useful for understanding cell proliferation and control in vertebrates within the context of the whole animal physiology.In response to skin damage genes of immune surveillance were up-regulated along with others involved in tissue regeneration required to rapidly re-establish barrier function.Additionally, candidate fish genes were identified that may be involved in cytoskeletal re-modelling, mineralization and stem cells, which are of potential use in aquaculture and fish husbandry, as they may impact on the ability of the fish to produce structural proteins, such as muscle, efficiently.

Affiliation: Comparative and Molecular Endocrinology Group, Centre for Marine Sciences (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal. fvieira@ualg.pt

ABSTRACT

Background:

Background: Fish scales are an important reservoir of calcium and phosphorus and together with the skin function as an integrated barrier against environmental changes and external aggressors. Histological studies have revealed that the skin and scales regenerate rapidly in fish when they are lost or damaged. In the present manuscript the histological and molecular changes underlying skin and scale regeneration in fed and fasted sea bream (Sparus auratus) were studied using a microarray 3 and 7 days after scale removal to provide a comprehensive molecular understanding of the early stages of these processes.

Results: Histological analysis of skin/scales revealed 3 days after scale removal re-epithelisation and formation of the scale pocket had occurred and 53 and 109 genes showed significant up or down-regulation, respectively. Genes significantly up-regulated were involved in cell cycle regulation, cell proliferation and adhesion, immune response and antioxidant activities. 7 days after scale removal a thin regenerated scale was visible and only minor changes in gene expression occurred. In animals that were fasted to deplete mineral availability the expression profiles centred on maintaining energy homeostasis. The utilisation of fasting as a treatment emphasised the competing whole animal physiological requirements with regard to barrier repair, infection control and energy homeostasis.

Conclusions: The identification of numerous genes involved in the mitotic checkpoint and cell proliferation indicate that the experimental procedure may be useful for understanding cell proliferation and control in vertebrates within the context of the whole animal physiology. In response to skin damage genes of immune surveillance were up-regulated along with others involved in tissue regeneration required to rapidly re-establish barrier function. Additionally, candidate fish genes were identified that may be involved in cytoskeletal re-modelling, mineralization and stem cells, which are of potential use in aquaculture and fish husbandry, as they may impact on the ability of the fish to produce structural proteins, such as muscle, efficiently.

View Similar Images In: Results  - Collection
View Article: Pubmed Central - HTML -  PubMed
Show All Figures - Show MeSH
getmorefigures.php?pmc=3199283&rFormat=json&query=null&req=5