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Proteomic Approach to Skin Regeneration in a Marine Teleost: Modulation by Oestradiol-17β

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Abstract

Skin and scale formation and regeneration in teleosts have mainly been described from a morphological perspective, and few studies of the underlying molecular events exist. The present study evaluates (1) the change in the skin proteome during its regeneration in a marine teleost fish (gilthead sea bream, Sparus aurata) and (2) the impact of oestradiol-17β (Ε2) on regeneration and the involvement of oestrogen receptor (ER) isoforms. Thirty-five candidate proteins were differentially expressed (p < 0.05) between intact and regenerated skin proteome 5 days after scale removal, and 27 proteins were differentially expressed after E2 treatment. Agglomerative hierarchical clustering of the skin proteome revealed that the skin treated with E2 clustered most closely to intact skin, while regenerating untreated skin formed an independent cluster. Gene Ontology classification associated the differentially expressed proteins in E2-treated skin with developmental processes and cellular morphogenesis. The proteins modified during skin regeneration suggest a balance exists between immune response and anatomical repair. Overall, the results indicate that, even after 5 days regeneration, the composition of mature skin is not attained, and endocrine factors, in particular E2, can accelerate wound repair acting possibly via ERβs expressed in the skin-scales. Several candidate proteins probably involved in scale development, osteoglycin, lipocalin2 and lamin A and the transcription factors PHD and grainyhead were identified. Future studies of fish skin regeneration will be required to provide further insight into this multistage process, and the present study indicates it will be useful to explore immune adaptations of epithelia permanently exposed to an aqueous environment.

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Abbreviations

2-DE:

Two-dimensional electrophoresis

ACN:

Acetonitrile

Ca:

Calcium

DTT:

Dithiothreitol

E2 :

Oestradiol-17β

ER:

Oestrogen receptor

LC:

Liquid chromatography

MALDI-TOF:

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometer

MS:

Mass spectrometry

P:

Phosphorus

PBS:

Phosphate-buffered saline

PMF:

Peptide mass fingerprinting

qPCR:

Quantitative polymerase chain reaction

RT:

Reverse trancriptase

SDS-PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

Vgt:

Vitellogenin

ACTA1:

Actin

ACTB:

Skeletal alpha-actin type 2b

ACTB:

Actin beta

ACTC1:

Actin, alpha cardiac muscle 1

ALDH1A1:

Aldehyde dehydrogenase

ANXA3:

Annexin max 3

C1QL4:

Complement c1q-like protein 4

CFL2:

Cofilin 2

CKM:

Muscle-type creatine kinase

COL1A1:

Collagen type I alpha 1

COL6A1:

Collagen type VI alpha 1

COL6A3:

Collagen type VI alpha 3

CP:

Ceruloplasmin

DPYS:

Dihydropyrimidinase

GAPDH:

Glyceraldehide 3P dehydrogenase

GRLH1:

Grainyhead-like protein

IGKV:

Immunoglobulin light chain

IMPA1:

Myo-inositol monophosphatase

KRT:

Keratin

LCN2:

Tributyltin binding protein type 2

LMNA:

Lamin A

MYH:

Myosin heavy chain

MYL:

Myosin light chain

NDK:

Nucleoside diphosphate kinase B

OGN:

Osteoglycin

PHF3:

PHD finger protein 3

TF:

Transferrin

WAP65:

WT acclimation-related protein

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Acknowledgements

We thank Antonia Òdena and Eliandre de Oliveira from the ‘Centre Científic i Tecnològic’ (CCIT-UB) for valuable help during proteomic analyses. This research was funded by an AQUAGENOME (SSP8, no. 044481) resource exchange grant and pluriannual funding to CCMAR from the Portuguese Science and Technology Foundation (FCT) and XRAq projects (Generalitat de Catalunya, Spain). AI was recipient of a research grant from the Spanish Government (Programa de Ayudas de Mobilidad José Castillejo). PP was recipient of a fellowship SFRH/BPD/25247/2005 (PP) from the Portuguese Foundation for Science and Technology (FCT).

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Authors and Affiliations

  1. Dept Fisiologia i Immunologia (Biologia), University of Barcelone, Xarxa de Referència de Recerca i Desenvolupament en Aqüicultura de la Generalitat de Catalunya, Diagonal 643, 08028, Barcelona, Spain

    Antoni Ibarz

  2. CMEG, Centro de Ciências do Mar, CIMAR-Laboratório Associado, University of Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    Patricia I. S. Pinto & Deborah M. Power

  3. Fish Endocrinology Laboratory, Department of Biological and Environmental Sciences, University of Gothenburg, Box 463, 40530, Gothenburg, Sweden

    Deborah M. Power

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  1. Antoni Ibarz
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  2. Patricia I. S. Pinto
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Correspondence to Antoni Ibarz.

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Additional Fig. 1

Multi-scatter plot of normalised volume (vol.%) spots from 2D-gels of skin proteome within each experimental condition: IC intact skin, Reg regenerated skin, E2 intact skin E2 treated, RegE2 regenerated skin E2 treated. Correlation coefficients (r) are indicated in each plot (DOC 99 kb) (DOC 99 kb)

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Ibarz, A., Pinto, P.I.S. & Power, D.M. Proteomic Approach to Skin Regeneration in a Marine Teleost: Modulation by Oestradiol-17β. Mar Biotechnol 15, 629–646 (2013). https://doi.org/10.1007/s10126-013-9513-4

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