Hypothalamic agrp and pomc mRNA Responses to Gastrointestinal Fullness and Fasting in Atlantic Salmon (Salmo salar, L.)

Kalananthan, Tharmini; Murashita, Koji; Rønnestad, Ivar; Ishigaki, Mitsumasa; Takahashi, Kota; Silva, Marta S.; Wakabayashi, Yuki; Lai, Floriana; Shimizu, Munetaka; Nilsen, Tom Ole; Martinez, Enrique Pino; Gomes, Ana S.

doi:10.3389/fphys.2020.00061

Cited by 23 publications

(25 citation statements)

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“…A similar effect was described in common carp (Wan et al, 2012). In contrast, in our recent study, hypothalamic agrp1 was upregulated after 3 days of fasting in Atlantic salmon (Kalananthan et al, 2020). However, in the current study, no differences were observed in the hypothalamus or other regions between the fed and fasted groups for either agrp1 or agrp2.…”

Section: Discussionsupporting

confidence: 79%

“…Minimal or no effects of fasting on the mRNA expression of the investigated genes suggest that they play a minor role in the central control of appetite in the short 4 days’ fasting. However, a high individual variability was observed in both fed and fasted experimental groups, which might have led to a possible deviation in the results from our recent study on hypothalamic agrp1 in Atlantic salmon ( Kalananthan et al, 2020 ). Among the factors that contribute to the differences in feed intake, the feeding rate, frequency and time, and social relationships between conspecifics are the result of stimulating competition for a feed resource among individuals ( Attia et al, 2012 ).…”

Section: Discussioncontrasting

confidence: 74%

“…In this study, we have extended the current knowledge on Atlantic salmon pomc and agrp on appetite regulation, which was previously based on the analysis of the whole brain ( Murashita et al, 2009 , 2011 ) or on the hypothalamus ( Kalananthan et al, 2020 ). Murashita et al (2011 , 2009) identified and characterized three pomc gene paralogs ( pomca1 , a2 , and b ) and one splice variant ( pomca2s ) and two agrp paralogs ( agrp1 and 2 ).…”

Section: Discussionmentioning

confidence: 95%

“…GH transgenic common carp ( Zhong et al, 2013 ) and coho salmon ( Kim et al, 2015 ) showed increased hypothalamic agrp1 mRNA and elevated food intake compared to the wild type. Moreover, fasting upregulated the hypothalamic agrp mRNA in goldfish ( Cerdá-Reverter and Peter, 2003 ), coho salmon ( Kim et al, 2015 ), sea bass ( Agulleiro et al, 2014 ), mouth brooding African cichlid ( Astatotilapia burtoni ) ( Porter et al, 2017 ), rainbow trout ( Comesaña et al, 2017 ), seabream ( Sparus aurata ) larvae ( Koch et al, 2019 ), Atlantic salmon ( Kalananthan et al, 2020 ), and Ya-fish embryo ( Schizothorax prenanti ) ( Wei et al, 2013 ). In contrast, an opposite action was described in the brain of common carp ( Wan et al, 2012 ) and Atlantic salmon ( Murashita et al, 2009 ; Valen et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

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The Melanocortin System in Atlantic Salmon (Salmo salar L.) and Its Role in Appetite Control

et al. 2020

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The melanocortin system is a key neuroendocrine network involved in the control of food intake and energy homeostasis in vertebrates. Within the hypothalamus, the system comprises two main distinct neuronal cell populations that express the neuropeptides proopiomelanocortin (POMC; anorexigenic) or agouti-related protein (AGRP; orexigenic). Both bind to the melanocortin-4 receptor (MC4R) in higher order neurons that control both food intake and energy expenditure. This system is relatively well-conserved among vertebrates. However, in Atlantic salmon (Salmo salar L.), the salmonid-specific fourth round whole-genome duplication led to the presence of several paralog genes which might result in divergent functions of the duplicated genes. In the current study, we report the first comprehensive comparative identification and characterization of Mc4r and extend the knowledge of Pomc and Agrp in appetite control in Atlantic salmon. In silico analysis revealed multiple paralogs for mc4r (a1, a2, b1, and b2) in the Atlantic salmon genome and confirmed the paralogs previously described for pomc (a1, a2, and b) and agrp (1 and 2). All Mc4r paralogs are relatively well-conserved with the human homolog, sharing at least 63% amino acid sequence identity. We analyzed the mRNA expression of mc4r, pomc, and agrp genes in eight brain regions of Atlantic salmon post-smolt under two feeding states: normally fed and fasted for 4 days. The mc4ra2 and b1 mRNAs were predominantly and equally abundant in the hypothalamus and telencephalon, the mc4rb2 in the hypothalamus, and a1 in the telencephalon. All pomc genes were highly expressed in the pituitary, followed by the hypothalamus and saccus vasculosus. The agrp genes showed a completely different expression pattern from each other, with prevalent expression of the agrp1 in the hypothalamus and agrp2 in the telencephalon. Fasting did not induce any significant changes in the mRNA level of mc4r, agrp, or pomc paralogs in the hypothalamus or in other highly expressed regions between fed and fasted states. The identification and wide distribution of multiple paralogs of mc4r, pomc, and agrp in Atlantic salmon brain provide new insights and give rise to new questions of the melanocortin system in the appetite regulation in Atlantic salmon.

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Section: Discussionsupporting

confidence: 79%

Section: Discussioncontrasting

confidence: 74%

Section: Discussionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

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The Melanocortin System in Atlantic Salmon (Salmo salar L.) and Its Role in Appetite Control

et al. 2020

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“…In our analysis, no correlation was found between stomach content and ghrl mRNA expression levels (stomach is the compartment where ghrl is mostly expressed) but, rather, between mRNA expression in the PSt and inner content in HG. A previous study indicated a correlation between a complete empty stomach with an increase in only one orexigenic factor (i.e., agrp1 mRNA expression levels) in the hypothalamus of 3 days of induced fasting in Atlantic salmon ( Kalananthan et al, 2020b ), supporting the hypothesis that 4 days of fasting are not sufficient to initiate a significant response. Thus, it is still uncertain how the multiple gastric and intestinal signaling factors responds to fasting with different durations.…”

Section: Discussionmentioning

confidence: 73%

Effects of Short-Term Fasting on mRNA Expression of Ghrelin and the Peptide Transporters PepT1 and 2 in Atlantic Salmon (Salmo salar)

et al. 2021

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Food intake is a vital process that supplies necessary energy and essential nutrients to the body. Information regarding luminal composition in the gastrointestinal tract (GIT) collected through mechanical and nutrient sensing mechanisms are generally conveyed, in both mammals and fish, to the hypothalamic neurocircuits. In this context, ghrelin, the only known hormone with an orexigenic action, and the intestinal peptide transporters 1 and 2, involved in absorption of dietary di- and tripeptides, exert important and also integrated roles for the nutrient uptake. Together, both are potentially involved in signaling pathways that control food intake originating from different segments of the GIT. However, little is known about the role of different paralogs and their response to fasting. Therefore, after 3 weeks of acclimatization, 12 Atlantic salmon (Salmo salar) post-smolt were fasted for 4 days to explore the gastrointestinal response in comparison with fed control (n = 12). The analysis covered morphometric (weight, length, condition factor, and wet content/weight fish %), molecular (gene expression variations), and correlation analyses. Such short-term fasting is a common and recommended practice used prior to any handling in commercial culture of the species. There were no statistical differences in length and weight but a significant lower condition factor in the fasted group. Transcriptional analysis along the gastrointestinal segments revealed a tendency of downregulation for both paralogous genes slc15a1a and slc15a1b and with significant lowered levels in the pyloric ceca for slc15a1a and in the pyloric ceca and midgut for slc15a1b. No differences were found for slc15a2a and slc15a2b (except a higher expression of the fasted group in the anterior midgut), supporting different roles for slc15 paralogs. This represents the first report on the effects of fasting on slc15a2 expressed in GIT in teleosts. Transcriptional analysis of ghrelin splicing variants (ghrl-1 and ghrl-2) showed no difference between treatments. However, correlation analysis showed that the mRNA expression for all genes (restricted to segment with the highest levels) were affected by the residual luminal content. Overall, the results show minimal effects of 4 days of induced fasting in Atlantic salmon, suggesting that more time is needed to initiate a large GIT response.

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Mapping key neuropeptides involved in the melanocortin system in Atlantic salmon (Salmo salar) brain

Norland

Eilertsen

Rønnestad

et al. 2022

J of Comparative Neurology

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The melanocortin system is a key regulator of appetite and food intake in vertebrates. This system includes the neuropeptides neuropeptide y (NPY), agouti‐related peptide (AGRP), cocaine‐ and amphetamine‐regulated transcript (CART), and pro‐opiomelanocortin (POMC). An important center for appetite control in mammals is the hypothalamic arcuate nucleus, with neurons that coexpress either the orexigenic NPY/AGRP or the anorexigenic CART/POMC neuropeptides. In ray‐finned fishes, such a center is less characterized. The Atlantic salmon (Salmo salar) has multiple genes of these neuropeptides due to whole‐genome duplication events. To better understand the potential involvement of the melanocortin system in appetite and food intake control, we have mapped the mRNA expression of npy, agrp, cart, and pomc in the brain of Atlantic salmon parr using in situ hybridization. After identifying hypothalamic mRNA expression, we investigated the possible intracellular coexpression of npy/agrp and cart/pomc in the tuberal hypothalamus by fluorescent in situ hybridization. The results showed that the neuropeptides were widely distributed, especially in sensory and neuroendocrine brain regions. In the hypothalamic lateral tuberal nucleus, the putative homolog to the mammalian arcuate nucleus, npya, agrp1, cart2b, and pomca were predominantly localized in distinct neurons; however, some neurons coexpressed cart2b/pomca. This is the first demonstration of coexpression of cart2b/pomca in the tuberal hypothalamus of a teleost. Collectively, our data suggest that the lateral tuberal nucleus is the center for appetite control in salmon, similar to that of mammals. Extrahypothalamic brain regions might also be involved in regulating food intake, including the olfactory bulb, telencephalon, midbrain, and hindbrain.

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Hypothalamic agrp and pomc mRNA Responses to Gastrointestinal Fullness and Fasting in Atlantic Salmon (Salmo salar, L.)

Cited by 23 publications

References 44 publications

The Melanocortin System in Atlantic Salmon (Salmo salar L.) and Its Role in Appetite Control

The Melanocortin System in Atlantic Salmon (Salmo salar L.) and Its Role in Appetite Control

Effects of Short-Term Fasting on mRNA Expression of Ghrelin and the Peptide Transporters PepT1 and 2 in Atlantic Salmon (Salmo salar)

Mapping key neuropeptides involved in the melanocortin system in Atlantic salmon (Salmo salar) brain

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