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Thermal imprinting modifies bone homeostasis in cold-challenged sea bream (Sparus aurata)

Publication . Mateus, Ana; Costa, Rita; Gisbert, Enric; PI Pinto, PPinto; Andree, Karl B.; Estevez, Alicia; Power, Deborah

Fish are ectotherms and temperature plays a determinant role in their physiology, biology and ecology, and is a driver of seasonal responses. The present study assessed how thermal imprinting during embryonic and larval stages modified the response of adult fish to low water temperature. We targeted the gilthead sea bream, which develops a condition known as winter syndrome when it is exposed to low water temperatures. Eggs and larvae of sea bream were exposed to four different thermal regimes and then the response of the resulting adults to a low temperature challenge was assessed. Sea bream exposed to a high-low thermal regime as eggs and larvae (HLT; 22 degrees C until hatch and then 18 degrees C until larvae-juvenile transition) had increased plasma cortisol and lower sodium and potassium in response to a cold challenge compared with the other thermal history groups. Plasma glucose and osmolality were increased in cold-challenged HLT fish relative to the unchallenged HLT fish. Cold challenge modified bone homeostasis/responsiveness in the low-high thermal regime group (LHT) relative to other groups, and ocn, ogn1/2, igf1, gr and tr alpha/beta transcripts were all downregulated. In the low temperature group (LT) and HLT group challenged with a low temperature, alkaline phosphatase (ALP) and tartrate-resistant acid phosphatase (TRAP) activities were decreased relative to unchallenged groups, and bone calcium content also decreased in the LT group. Overall, the results indicate that thermal imprinting during early development of sea bream causes a change in the physiological response of adults to a cold challenge.

2017-10Journal article

Open access

Persistence of the ABCC6 genes and the emergence of the bony skeleton in vertebrates

Publication . Parreira, Bruna; Cardoso, João; Costa, Rita; Couto, Ana Rita; Bruges-Armas, Jacome; Power, Deborah M.

The ATP-binding cassette transporter 6 (ABCC6) gene encodes a cellular transmembrane protein transporter (MRP6) that is involved in the regulation of tissue calcification in mammals. Mutations in ABCC6 are associated with human ectopic calcification disorders. To gain insight into its evolution and involvement in tissue calcification we conducted a comparative analysis of the ABCC6 gene and the related gene ABCC1 from invertebrates to vertebrates where a bony endoskeleton first evolved. Taking into consideration the role of ABCC6 in ectopic calcification of human skin we analysed the involvement of both genes in the regeneration of scales, mineralized structures that develop in fish skin. The ABCC6 gene was only found in bony vertebrate genomes and was absent from Elasmobranchs, Agnatha and from invertebrates. In teleost fish the abcc6 gene duplicated but the two genes persisted only in some teleost genomes. Six disease causing amino acid mutations in human MRP6 are a normal feature of abcc6 in fish, suggesting they do not have a deleterious effect on the protein. After scale removal the abcc6 (5 and 10 days) and abcc1 (10 days) gene expression was up-regulated relative to the intact control skin and this coincided with a time of intense scale mineralization.

2018-04Journal article

Open access

Thermal imprinting modifies adult stress and innate immune responsiveness in the teleost sea bream

Publication . Mateus, Ana; A Costa, Rita; Cardoso, João CR; Andree, Karl B.; Estevez, Alicia; Gisbert, Enric; Power, Deborah

The impact of thermal imprinting on the plasticity of the hypothalamic-pituitary-interrenal (HPI) axis and stress response in an adult ectotherm, the gilthead sea bream (Sparus aurata, L.), during its development was assessed. Fish were reared under 4 thermal regimes, and the resulting adults exposed to acute confinement stress and plasma cortisol levels and genes of the HPI axis were monitored. Changes in immune function, a common result of stress, were also evaluated using histomorphometric measurements of melanomacrophages centers (MMCs) in the head kidney and by monitoring macrophage-related transcripts. Thermal history significantly modified the HPI responsiveness in adult sea bream when eggs and larvae were reared at a higher than optimal temperature (HT, 22 degrees C), and they had a reduced amplitude in their cortisol response and significantly upregulated pituitary pomc and head kidney star transcripts. Additionally, after an acute stress challenge, immune function was modified and the head kidney of adult fish reared during development at high temperatures (HT and LHT, 18-22 degrees C) had a decreased number of MMCs and a significant downregulation of dopachrome tautomerase. Thermal imprinting during development influenced adult sea bream physiology and increased plasma levels of glucose and sodium even in the absence of an acute stress in fish reared under a high-low thermal regime (HLT, 22-18 degrees C). Overall, the results demonstrate that temperature during early development influences the adult HPI axis and immune function in a teleost fish.

2017-06Journal article

Open access

Temperature responsiveness of gilthead sea bream bone; an in vitro and in vivo approach

Publication . Riera-Heredia, Natalia; Martins, Rute; Patricia Mateus, Ana; Costa, Rita; Gisbert, Enric; Navarro, Isabel; Gutierrez, Joaquim; Power, Deborah M.; Capilla, Encarnacion

This 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.

2018Journal article

Open access

Vertebrate SLRP family evolution and the subfunctionalization of osteoglycin gene duplicates in teleost fish

Publication . Costa, Rita; Brazona, Rute Sofia Tavares Martins; Capilla, E.; Anjos, Liliana; Power, Deborah

Background Osteoglycin (OGN, a.k.a. mimecan) belongs to cluster III of the small leucine-rich proteoglycans (SLRP) of the extracellular matrix (ECM). In vertebrates OGN is a characteristic ECM protein of bone. In the present study we explore the evolution of SLRP III and OGN in teleosts that have a skeleton adapted to an aquatic environment. Results The SLRP gene family has been conserved since the separation of chondrichthyes and osteichthyes. Few gene duplicates of the SLRP III family exist even in the teleosts that experienced a specific whole genome duplication. One exception is ogn for which duplicate copies were identified in fish genomes. The ogn promoter sequence and in vitro mesenchymal stem cell (MSC) cultures suggest the duplicate ogn genes acquired divergent functions. In gilthead sea bream (Sparus aurata) ogn1 was up-regulated during osteoblast and myocyte differentiation in vitro, while ogn2 was severely down-regulated during bone-derived MSCs differentiation into adipocytes in vitro. Conclusions Overall, the phylogenetic analysis indicates that the SLRP III family in vertebrates has been under conservative evolutionary pressure. The retention of the ogn gene duplicates in teleosts was linked with the acquisition of different functions. The acquisition by OGN of functions other than that of a bone ECM protein occurred early in the vertebrate lineage.

2018-12-13Journal article

Open access