Intergenerational effects of overfeeding on aversive learning in zebrafish (<i>Danio rerio</i>)

Anwer, Hamza; Mason, Dominic; Zajitschek, Susanne; Hesselson, Daniel; Noble, Daniel W. A.; Morris, Margaret J.; Lagisz, Malgorzata; Nakagawa, Shinichi

doi:10.1002/ece3.9423

Cited by 3 publications

(5 citation statements)

References 111 publications

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“…As an example, RNA-seq analysis of the amygdala of mice derived from fathers exposed to chronic unpredictable stress discovered alterations in several pathways, being the most affected the “notch signaling” one [ 72 ]. Again, for these molecular studies, species such as mice or zebrafish are excellent models [ 73 ]. In the last approach of this work, we perform transcriptomic analyses in the resulting progenies derived from exposed males crossed with unexposed females, to identify molecular mechanisms putatively compromised by paternal exposure to chronic stress.…”

Section: Discussionmentioning

confidence: 99%

Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny

et al. 2023

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Background Chronic stress can produce a severe negative impact on health not only in the exposed individuals but also in their offspring. Indeed, chronic stress may be contributing to the current worldwide scenario of increasing infertility and decreasing gamete quality in human populations. Here, we evaluate the effect of chronic stress on behavior and male reproductive parameters in zebrafish. Our goal is to provide information on the impact that chronic stress has at molecular, histological, and physiological level in a vertebrate model species. Results We evaluated the effects of a 21-day chronic stress protocol covering around three full waves of spermatogenesis in Danio rerio adult males. The induction of chronic stress produced anxiety-like behavior in stressed males as assessed by a novel tank test. At a molecular level, the induction of chronic stress consistently resulted in the overexpression of two genes related to endoplasmic reticulum (ER) stress in the brain. Gene set enrichment analysis (GSEA) of testes suggested a dysregulation of the nonsense-mediated decay (NMD) pathway, which was also confirmed on qPCR analysis. Histological analysis of the testicle did not show significant differences in terms of the relative proportions of each germ-cell type; however, the quality of sperm from stressed males was compromised in terms of motility. RNA-seq analysis in stress-derived larval progenies revealed molecular alterations, including those predicted to affect translation initiation, DNA repair, cell cycle control, and response to stress. Conclusions Induction of chronic stress during a few cycles of spermatogenesis in the vertebrate zebrafish model affects behavior, gonadal gene expression, final gamete quality, and progeny. The NMD surveillance pathway (a key cellular mechanism that regulates the stability of both normal and mutant transcripts) is severely affected in the testes by chronic stress and therefore the control and regulation of RNAs during spermatogenesis may be affected altering the molecular status in the progeny. Graphical Abstract

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Section: Discussionmentioning

confidence: 99%

Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny

et al. 2023

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“…Previous studies involved solely freshly hatched artemia [32] or combined with commercially available fish food [17]. However, in this study, rotifer was used in combination with a dry diet which was specifically formulated for zebrafish husbandry, showing a markedly different nutritional composition to that used in previous studies [17,18,32]. Therefore, standardization of dietary protocols, diet composition, and ulterior studies on the effect of specific nutrients in obesity-induced cognitive and behavioural impairment appears to be critical for future investigations.…”

Section: Discussionmentioning

confidence: 99%

“…The manner in which obesity is induced in zebrafish seems to have effects on behavioural responses and particularly anxiety-like responses. Zebrafish, either larvae or adult specimens, fed obesogenic diets containing high fat levels exhibit anxiety-like behaviours [14,21]; however, obese fish on regular diets at high ratios failed to exhibit such behaviour [17,18]. Due to the wide spectrum of behavioural responses displayed in NTDT by zebrafish [22][23][24], it was decided to enlarge the behavioural variables to corroborate previous results and study the activation of the central monoaminergic circuitry.…”

Section: Discussionmentioning

confidence: 99%

“…The existence of STM and LTM has been demonstrated in zebrafish [31], and the effects of DIO on STM [13] and LTM have previously been studied [21]. DIO induced impairment of both STM and LTM, but OIO protocols had no effect on STM formation [17], although intergenerational effects of obesity have been reported [18]. Unfortunately, OIO effects on LTM response have not been studied.…”

Section: Discussionmentioning

confidence: 99%

“…However, overfeeding-induced obesity (OIO) with commercial food does induce deleterious effects on brain homeostasis and neuronal plasticity, thus promoting anxiety-like responses in zebrafish [16]. Nevertheless, similar experiments following an analogous approach to generating OIO in zebrafish were not able to replicate anxiety-like responses or find differences in aversive learning assays [17,18]. In the face of such controversy, the effects of OIO on anxiety-like behaviour and short-and long-term memory using aversive learning tests in zebrafish were explored.…”

Section: Introductionmentioning

confidence: 99%

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Obesity Impairs Cognitive Function with No Effects on Anxiety-like Behaviour in Zebrafish

Godino-Gimeno,

Thörnqvist,

Chivite

et al. 2023

IJMS

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Over the last decade, the zebrafish has emerged as an important model organism for behavioural studies and neurological disorders, as well as for the study of metabolic diseases. This makes zebrafish an alternative model for studying the effects of energy disruption and nutritional quality on a wide range of behavioural aspects. Here, we used the zebrafish model to study how obesity induced by overfeeding regulates emotional and cognitive processes. Two groups of fish (n = 24 per group) were fed at 2% (CTRL) and 8% (overfeeding-induced obesity, OIO) for 8 weeks and tested for anxiety-like behaviour using the novel tank diving test (NTDT). Fish were first tested using a short-term memory test (STM) and then trained for four days for a long-term memory test (LTM). At the end of the experiment, fish were euthanised for biometric sampling, total lipid content, and triglyceride analysis. In addition, brains (eight per treatment) were dissected for HPLC determination of monoamines. Overfeeding induced faster growth and obesity, as indicated by increased total lipid content. OIO had no effect on anxiety-like behaviour. Animals were then tested for cognitive function (learning and memory) using the aversive learning test in Zantiks AD units. Results show that both OIO and CTRL animals were able to associate the aversive stimulus with the conditioned stimulus (conditioned learning), but OIO impaired STM regardless of fish sex, revealing the effects of obesity on cognitive processes in zebrafish. Obese fish did not show a deficiency in monoaminergic transmission, as revealed by quantification of total brain levels of dopamine and serotonin and their metabolites. This provides a reliable protocol for assessing the effect of metabolic disease on cognitive and behavioural function, supporting zebrafish as a model for behavioural and cognitive neuroscience.

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Understanding the Intense Effects of Caloric Restriction and Overfeeding on Zebrafish (Danio Rerio) Behaviour and Biochemical Processes, Along With Their Implications for Offspring

Tamilarasan,

Devaraja,

Premkumar

et al. 2024

SSRN Journal

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Intergenerational effects of overfeeding on aversive learning in zebrafish (Danio rerio)

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 3 publications

References 111 publications

Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny

Stress decreases spermatozoa quality and induces molecular alterations in zebrafish progeny

Obesity Impairs Cognitive Function with No Effects on Anxiety-like Behaviour in Zebrafish

Understanding the Intense Effects of Caloric Restriction and Overfeeding on Zebrafish (Danio Rerio) Behaviour and Biochemical Processes, Along With Their Implications for Offspring

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