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- Coordinated regulation of chromatophore differentiation and melanogenesis during the ontogeny of skin pigmentation of Solea senegalensis (Kaup, 1858)Publication . Darias, Maria J.; Andree, Karl B.; Boglino, Anais; Fernandez, Ignacio; Estevez, Alicia; Gisbert, EnricAbnormal pigmentation of Senegalese sole has been described as one problem facing the full exploitation of its commercial production. To improve our understanding of flatfish pigmentation of this commercially important species we have evaluated eleven genes related to two different processes of pigmentation: melanophore differentiation, and melanin production. The temporal distribution of gene expression peaks corresponds well with changes in pigmentation patterns and the intensity of skin melanization. Several gene ratios were also examined to put in perspective possible genetic markers for the different stages of normal pigmentation development. Further, the phenotypic changes that occur during morphogenesis correspond well with the main transitions in gene expression that occur. Given the dramatic phenotypic alterations which flatfish undergo, including the asymmetric coloration that occurs between the ocular and the blind side, and the synchrony of the two processes of morphogenesis and pigmentation ontogenesis, these species constitute an interesting model for the study of pigmentation. In this study we present a first approximation towards explaining the genetic mechanisms for regulating pigmentation ontogeny in Senegalese sole, Solea senegalensis.
- Skeletal anomalies in reared European fish larvae and juveniles. Part 1: normal and anomalous skeletogenic processesPublication . Boglione, Clara; Gavaia, Paulo; Koumoundouros, Giorgos; Gisbert, Enric; Moren, Mari; Fontagne, Stephanie; Witten, Paul EckhardThis critical review summarizes the knowledge about fish skeletal tissues and inherent normal and anomalous development. Particular emphasis is given to existing literature on reared European fishes. The aim was to identify the main gaps of knowledge that require to be filled, in order to precociously identify anomalous developmental patterns that lead to skeletal anomalies in reared finfish larvae and juveniles. The review also aims to extend our knowledge about the factors that are possibly involved in the onset of skeletal anomalies. The final goal is the optimization of the morphological quality of farmed juvenile fish.
- Skeletal anomalies in reared European fish larvae and juveniles. Part 1: normal and anomalous skeletogenic processesPublication . Boglione, C.; Gavaia, Paulo J.; Koumoundouros, Giorgos; Gisbert, Enric; Moren, M.; Fontagné, Stéphanie; Witten, PaulThis critical review summarises the knowledge about fish skeletal tissues and inherent normal and anomalous development. Particular emphasis is given to existing literature on reared European fishes. The aim was to identify the main gaps of knowledge that require to be fulfilled, in order to precociously identify anomalous developmental patterns that lead to skeletal anomalies in reared finfish larvae and juveniles. The review also aims at to extending our knowledge about the factors that are possibly be involved in the onset of skeletal anomalies. The long period goal is the optimization of the morphological quality of farmed juvenile fish.
- Retinoic acid differentially affects in vitro proliferation, differentiation and mineralization of two fish bone-derived cell lines: Different gene expression of nuclear receptors and ECM proteinsPublication . Fernández, Ignacio; Tiago, Daniel; Laizé, Vincent; Cancela, Leonor; Gisbert, EnricRetinoic acid (RA), the main active metabolite of vitamin A, regulates vertebrate morphogenesis through signaling pathways not yet fully understood. Such process involves the specific activation of retinoic acid and retinoid X receptors (RARs and RXRs), which are nuclear receptors of the steroid/thyroid hormone receptor superfamily. Teleost fish are suitable models to study vertebrate development, such as skeletogenesis. Cell systems capable of in vitro mineralization have been developed for several fish species and may provide new insights into the specific cellular and molecular events related to vitamin A activity in bone, complementary to in vivo studies. This work aims at investigating the in vitro effects of RA (0.5 and 12.5 μM) on proliferation, differentiation and extracellular matrix (ECM) mineralization of two gilthead seabream bone-derived cell lines (VSa13 and VSa16), and at identifying molecular targets of its action through gene expression analysis. RA induced phenotypic changes and cellular proliferation was inhibited in both cell lines in a cell type-dependent manner (36–59% in VSa13 and 17–46% in VSa16 cells). While RA stimulated mineral deposition in VSa13 cell cultures (50–62% stimulation), it inhibited the mineralization of extracellular matrix in VSa16 cells (11–57% inhibition). Expression of hormone receptor genes (rars and rxrs), and extracellular matrix-related genes such as matrix and bone Gla proteins (mgp and bglap), osteopontin (spp1) and type I collagen (col1a1) were differentially regulated upon exposure to RA in proliferating, differentiating and mineralizing cultures of VSa13 and VSa16 cells. Altogether, our results show: (i) RA affects proliferative and mineralogenic activities in two fish skeletal cell types and (ii) that during phenotype transitions, specific RA nuclear receptors and bone-related genes are differentially expressed in a cell type-dependent manner.
- Invasion genetics of the mummichog (Fundulus heteroclitus): recent anthropogenic introduction in IberiaPublication . Morim, Teófilo; Bigg, Grant R.; Madeira, Pedro M.; Palma, Jorge; Duvernell, David D.; Gisbert, Enric; Lopes Da Cunha, Regina; Castilho, RitaHuman activities such as trade and transport have increased considerably in the last decades, greatly facilitating the introduction and spread of non-native species at a global level. In the Iberian Peninsula, Fundulus heteroclitus, a small euryhaline coastal fish with short dispersal, was found for the first time in the mid-1970s. Since then, F. heteroclitus has undergone range expansions, colonizing the southern region of Portugal, southwestern coast of Spain and the Ebro Delta in the Mediterranean Sea. Cytochrome b sequences were used to elucidate the species invasion pathway in Iberia. Three Iberian locations (Faro, Cádiz and Ebro Delta) and 13 other locations along the native range of F. heteroclitus in North America were sampled. Results revealed a single haplotype, common to all invasive populations, which can be traced to the northern region of the species' native range. We posit that the origin of the founder individuals is between New York and Nova Scotia. Additionally, the lack of genetic structure within Iberia is consistent with a recent invasion scenario and a strong founder effect. We suggest the most probable introduction vector is associated with the aquarium trade. We further discuss the hypothesis of a second human-mediated introduction responsible for the establishment of individuals in the Ebro Delta supported by the absence of adequate muddy habitats linking Cádiz and the Ebro Delta. Although the species has a high tolerance to salinity and temperature, ecological niche modelling indicates that benthic habitat constraints prevent along-shore colonisation suggesting that such expansions would need to be aided by human release.
- Vitamin A affects flatfish development in a thyroid hormone signaling and metamorphic stage dependent mannerPublication . Fernandez, Ignacio; Ortiz-Delgado, Juan B.; Darias, Maria J.; Hontoria, Francisco; Andree, Karl B.; Manchado, Manuel; Sarasquete, Carmen; Gisbert, EnricVitamin A (VA) and retinoid derivatives are known morphogens controlling vertebrate development. Despite the research effort conducted during the last decade, the precise mechanism of how VA induces post-natal bone changes, and particularly those operating through crosstalk with the thyroid hormones (THs) remain to be fully understood. Since effects and mechanisms seem to be dose and time-dependent, flatfish are an interesting study model as they undergo a characteristic process of metamorphosis driven by THs that can be followed by external appearance. Here, we studied the effects of VA imbalance that might determine Senegalese sole (Solea senegalensis) skeletogenetic phenotype through development of thyroid follicles, THs homeostasis and signaling when a dietary VA excess was specifically provided during pre-, pro-or post-metamorphic stages using enriched rotifers and Artemia as carriers. The increased VA content in enriched live prey was associated to a higher VA content in fish at all developmental stages. Dietary VA content clearly affected thyroid follicle development, T3 and T4 immunoreactive staining, skeletogenesis and mineralization in a dose and time-dependent fashion. Gene expression analysis showed that VA levels modified the mRNA abundance of VA- and TH-specific nuclear receptors at specific developmental stages. Present results provide new and key knowledge to better understand how VA and TH pathways interact at tissue, cellular and nuclear level at different developmental periods in Senegalese sole, unveiling how dietary modulation might determine juvenile phenotype and physiology.
- Temperature responsiveness of gilthead sea bream bone; an in vitro and in vivo approachPublication . Riera-Heredia, Natalia; Martins, Rute; Patricia Mateus, Ana; Costa, Rita; Gisbert, Enric; Navarro, Isabel; Gutierrez, Joaquim; Power, Deborah M.; Capilla, EncarnacionThis study aimed to characterize the molecules involved in osteogenesis in seabream and establish using in vitro/in vivo approaches the responsiveness of selected key genes to temperature. The impact of a temperature drop from 23 to 13 degrees C was evaluated in juvenile fish thermally imprinted during embryogenesis. Both, in vitro/in vivo, Fib1a, appeared important in the first stages of bone formation, and Col1A1, ON and OP, in regulating matrix production and mineralization. OCN mRNA levels were up-regulated in the final larval stages when mineralization was more intense. Moreover, temperature-dependent differential gene expression was observed, with lower transcript levels in the larvae at 18 degrees C relative to those at 22 degrees C, suggesting bone formation was enhanced in the latter group. Results revealed that thermal imprinting affected the long-term regulation of osteogenesis. Specifically, juveniles under the low and low-to-high-temperature regimes had reduced levels of OCN when challenged, indicative of impaired bone development. In contrast, gene expression in fish from the high and high-to-low-temperature treatments was unchanged, suggesting imprinting may have a protective effect. Overall, the present study revealed that thermal imprinting modulates bone development in seabream larvae, and demonstrated the utility of the in vitro MSC culture as a reliable tool to investigate fish osteogenesis.
- Skeletal anomalies in reared European fish larvae and juveniles. Part 2: main typologies, occurrences and causative factorsPublication . Boglione, Clara; Gisbert, Enric; Gavaia, Paulo; Witten, Paul E.; Moren, Mori; Fontagne, Stephanie; Koumoundouros, GiorgosThe presence of skeletal anomalies in farmed teleost fish is currently a major problem in aquaculture, entailing economical, biological and ethical issues. The common occurrence of skeletal abnormalities in farmed fish and the absence of effective solutions for avoiding their onset or definitely culling out the affected individuals as early as possible from the productive cycle, highlight the need to improve our knowledge on the basic processes regulating fish skeletogenesis and skeletal tissues differentiation, modelling and remodelling. Severe skeletal anomalies may actually occur throughout the entire life cycle of fish, but their development often begins with slight aberrations of the internal elements. Comprehensive investigation efforts conducted on reared larvae and juveniles could provide a great contribution in filling the gap in knowledge, as skeletogenesis and skeletal tissue differentiation occur during these early life stages. The aim of this review is to provide a synthetic but comprehensive picture of the actual knowledge on the ontogeny, typologies and occurrence of skeletal anomalies, and on the proposed causative factors for their onset in larvae and juveniles of European farmed fish. The state-of-art of knowledge of these issues is analysed critically intending to individualize the main gaps of knowledge that require to be filled, in order to optimize the morphological quality of farmed juveniles.
- Comparative analysis of a teleost skeleton transcriptome provides insight into its regulationPublication . Vieira, Florbela A.; Thorne, Michael A. S.; Stueber, K.; Darias, M.; Reinhardt, Richard; Clark, M. S.; Gisbert, Enric; Power, DeborahAn articulated endoskeleton that is calcified is a unifying innovation of the vertebrates, however the molecular basis of the structural divergence between terrestrial and aquatic vertebrates, such as teleost fish, has not been determined. In the present study long-read next generation sequencing (NGS, Roche 454 platform) was used to characterize acellular perichondral bone (vertebrae) and chondroid bone (gill arch) in the gilthead sea bream (Sparus auratus). A total of 15.97 and 14.53 Mb were produced, respectively from vertebrae and gill arch cDNA libraries and yielded 32,374 and 28,371 contigs (consensus sequences) respectively. 10,455 contigs from vertebrae and 10,625 contigs from gill arches were annotated with gene ontology terms. Comparative analysis of the global transcriptome revealed 4249 unique transcripts in vertebrae, 4201 unique transcripts in the gill arches and 3700 common transcripts. Several core gene networks were conserved between the gilthead sea bream and mammalian skeleton. Transcripts for putative endocrine factors were identified in acellular gilthead sea bream bone suggesting that in common with mammalian bone it can act as an endocrine tissue. The acellular bone of the vertebra, in contrast to current opinion based on histological analysis, was responsive to a short fast and significant (p < 0.05) down-regulation of several transcripts identified by NGS, osteonectin, osteocalcin, cathepsin K and IGFI occurred. In gill arches fasting caused a significant (p < 0.05) down-regulation of osteocalcin and up-regulation of MMP9.
- Normal and histopathological organization of the opercular bone and vertebrae in gilthead sea bream Sparus aurataPublication . Ortiz-Delgado, Juan B.; Fernández Monzón, Ignacio Valentín; Sarasquete, Carmen; Gisbert, EnricThis study provides a comprehensive description of the tissue organization of non-deformed and deformed opercula and vertebrae from gilthead sea bream Sparus aurata juveniles by means of histological, histochemical and immunohistochemical approaches. Two types of opercular anomalies are described: the folding of the opercle and subopercle into the gill chamber, starting at the upper corner of the branchial cleft and extending down to its lower third; and the partial lack of the operculum (opercle, subopercle, interopercle and preopercle underdeveloped) with a regression of the loose edge extending down to its lower third. Histological observations revealed a rare type of bone remodelling process in the opercular structure, which consisted of the coalescence of contacting bone tissues (presumably from the preopercle and opercle), resulting in skeletal tissue with a trabecular aspect filled by a single-cell epithelium of cubic osteoblastic-like cells. Differences in collagen fiber thickness and its 3-dimensional arrangement between normal and deformed opercula were also found. Lordotic vertebrae were characterized by the formation of fibrous cartilage in the haemal and/or neural sides, indicating that a metaplastic shift occurred during the process of lordosis. Another major histomorphological change found in lordotic vertebrae was the complete loss of notochordal sheath integrity. Histological alterations were coupled with an imbalance of cell death and cell proliferation processes in lordotic vertebrae as well as that of bone formation/resorption, and extracellular matrix deposition activity differences which might have resulted from the remodelling process occurring in lordotic vertebrae. Altogether, these results provide an increase in our basic knowledge of bone disorders that contribute to our understanding of the mechanisms by which these skeletal anomalies appear in this fish species and which hamper its production efficiency.