Effect of starvation on transcriptomes of brain and liver in adult female zebrafish (Danio rerio)

Abstract

Only agouti-related protein 1 (agrp1) significantly responded, with increased expression in brains of starved fish. In contrast, a 21-day period of starvation significantly downregulated 466 and upregulated 108 transcripts in the liver, indicating an overall decrease in metabolic activity, reduced lipid metabolism, protein biosynthesis, proteolysis, and cellular respiration, and increased gluconeogenesis. Starvation also regulated expression of many components of the unfolded protein response, the first such report in a species other than yeast (Saccharomyces cerevisiae) and mice (Mus musculus). The response of the zebrafish hepatic transcriptome to starvation was strikingly similar to that of rainbow trout (Oncorhynchus mykiss) and less similar to mouse, while the response of common carp (Cyprinus carpio) differed considerably from the other three species. microarray analysis; metabolic signaling; quantitative real-time polymerase chain reaction; neuropeptide THE ADAPTIVE PHYSIOLOGICAL response to starvation conserves the health and function of key organs and redistributes resources toward essential biological functions. In mammals and birds, this reallocation of resources is part of a predictable and sequential transition of metabolic changes (reviewed in Ref. 72). These metabolic changes appear to be similar in fish and other ectotherms, although the transitions occur over a much longer time frame, largely the result of lower metabolic rates (72). Variation in metabolic rate in fish is in turn influenced by body size and body temperature (10, 29). As the most diverse group of vertebrates, fish species vary considerably in body size, thermal habitat, and metabolic rate, and many species differ in susceptibility or have unique adaptations to prolonged periods of fasting in their natural environment (37, 72). The considerable variation among fish species in the response to starvation provides a useful context for identifying mechanisms that are conserved among vertebrate species. Understanding these conserved mechanisms requires multiple investigations of a diverse array of species that identify the metabolic pathways that respond to starvation and genetic mechanisms that regulate them.Here we used microarrays and quantitative real-time PCR (qRT-PCR) to examine the transcriptomic response to starvation in both brain and liver tissues of adult female zebrafish (Danio rerio). The zebrafish is an important model organism for the study of development and is now emerging as a model organism in other fields, including behavioral, physiological, and nutritional genomics (42,49,76). Despite its importance as a developmental and genomic model organism, our understanding of the nutritional physiology of the zebrafish remains very limited. Our goal was to identify the metabolic pathways impacted by starvation in zebrafish, contrasting two organs that 1) serve biosynthetic and energy-mobilizing functions (liver) and 2) consume energy and direct behavioral responses (brain). In addition, we offer an interpretation of these d...

Can the behaviour of threespine stickleback parasitized with Schistocephalus solidus be replicated by manipulating host physiology?

“…Secondly, we could not identify significant differences between treatments with the food intake test, even in the STRV group. One possibility is that the 72 h food withholding period might have been insufficient to elicit behavioural changes; previous studies investigating the effects of food withholding have starved fish for longer [zebrafish: 21 days (Drew et al, 2008), walleye pollock: 30-54 days (Sogard and Olla, 1997)], to see differences in transcriptomes and behaviour, respectively. Alternatively, as this was the final test, fish might have been stressed.…”

Postprandial Regulation of Growth- and Metabolism-Related Factors in Zebrafish

“…The chemical composition of the diets was analyzed using the following procedures: dry matter was determined after drying at 105°C for 24 h, protein content (N · 6.25) was determined by the Kjeldahl method after acid digestion, 4 fat by petroleum ether extraction (Soxtherm), and gross energy in an adiabatic bomb calorimeter (IKA).…”

“…2 However, to our knowledge, studies on the field remain scarce and deal mainly with the effect of fasting and/or refeeding. 3,4 Here, we investigated in this species not only the effect of a single meal on the postprandial expression of several hepatic and muscle metabolism-related genes and proteins but also that of manipulating proteins and carbohydrates content of the diet. Our data show that following the genes or functions considered, the responses obtained with this species are similar to those observed in carnivorous species such as rainbow trout (e.g., lack of refeeding effect on the expression of PK), similar to those usually attributed to rodent species (e.g., effect of refeeding on cPEPCK gene expression) or specific to this model (e.g., no significant modification of SREBP1 mRNA expression between fasted and refed fish).…”

“…2 However, this potential has not yet been realized, and to our knowledge, studies on the field remain scarce and concern mainly the effect of long-term food deprivation and/or refeeding on hepatic, brain, and skeletal muscle transcriptomes. 3,4 Recently, Robison et al examined for the first time the effect of manipulating dietary macronutrient composition on hepatic gene expression in zebrafish. 5 They demonstrated that long-term (12 weeks) manipulation of dietary carbohydrate levels had a significant effect on the pattern of expression of several hepatic genes during the postabsorptive period (24 h after the last meal).…”

Functional Genomic Analysis of the Nutritional and Hormonal Regulation of Fish Glucose and Lipid Metabolism

“…FBPase gene expression has been demonstrated in the livers of rainbow trout (Panserat et al, 2001b), common carp, and gilthead sea bream (Panserat et al, 2002b). In rainbow trout, expression of FBPase seems to be poorly regulated by feeding or refeeding (Panserat et al, 2001b;Kirchner et al, 2008;Lansard et al, 2009), whereas starvation significantly increased expression of FBPase in zebrafish (Drew et al, 2008).…”