Viral Infection Drives the Regulation of Feeding Behavior Related Genes in <i>Salmo salar</i>

The feeding behavior in fish is a complex activity that relies on the ability of the brain to integrate multiple signals to produce appropriate responses in terms of food intake, energy expenditure, and metabolic activity. Upon stress cues including viral infection or mediators such as the proinflam...

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Autores principales: David Muñoz, Ricardo Fuentes, Beatriz Carnicero, Andrea Aguilar, Nataly Sanhueza, Sergio San-Martin, Cristian Agurto, Andrea Donoso, Leonardo E. Valdivia, Jesús M. Miguez, Lluis Tort, Sebastián Boltana
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Publicado: MDPI AG 2021
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Acceso en línea:https://doaj.org/article/1e0076ef803e41068597c48c54be850e
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spelling oai:doaj.org-article:1e0076ef803e41068597c48c54be850e2021-11-11T16:51:57ZViral Infection Drives the Regulation of Feeding Behavior Related Genes in <i>Salmo salar</i>10.3390/ijms2221113911422-00671661-6596https://doaj.org/article/1e0076ef803e41068597c48c54be850e2021-10-01T00:00:00Zhttps://www.mdpi.com/1422-0067/22/21/11391https://doaj.org/toc/1661-6596https://doaj.org/toc/1422-0067The feeding behavior in fish is a complex activity that relies on the ability of the brain to integrate multiple signals to produce appropriate responses in terms of food intake, energy expenditure, and metabolic activity. Upon stress cues including viral infection or mediators such as the proinflammatory cytokines, prostaglandins, and cortisol, both Pomc and Npy/Agrp neurons from the hypothalamus are stimulated, thus triggering a response that controls both energy storage and expenditure. However, how appetite modulators or neuro-immune cues link pathogenesis and energy homeostasis in fish remains poorly understood. Here, we provide the first evidence of a molecular linkage between inflammation and food intake in <i>Salmon salar</i>. We show that in vivo viral challenge with infectious pancreatic necrosis virus (IPNV) impacts food consumption by activating anorexic genes such as <i>mc4r, crf,</i> and <i>pomcb</i> and 5-HT in the brain of <i>S. salar</i>. At the molecular level, viral infection induces an overall reduction in lipid content in the liver, favoring the production of AA and EPA associated with the increment of <i>elovl2</i> gene. In addition, infection upregulates leptin signaling and inhibits insulin signaling. These changes are accompanied by a robust inflammatory response represented by the increment of Il-1b, Il-6, Tnfa, and Pge2 as well as an increased cortisol level in vivo. Thus, we propose a model in which hypothalamic neurons respond to inflammatory cytokines and stress-related molecules and interact with appetite induction/inhibition. These findings provide evidence of crosstalk between pathogenesis-driven inflammation and hypothalamic–pituitary–adrenocortical axes in stress-induced food intake behavior in fish.David MuñozRicardo FuentesBeatriz CarniceroAndrea AguilarNataly SanhuezaSergio San-MartinCristian AgurtoAndrea DonosoLeonardo E. ValdiviaJesús M. MiguezLluis TortSebastián BoltanaMDPI AGarticlefeeding behaviorlipid metabolisminflammationinfectionBiology (General)QH301-705.5ChemistryQD1-999ENInternational Journal of Molecular Sciences, Vol 22, Iss 11391, p 11391 (2021)
institution DOAJ
collection DOAJ
language EN
topic feeding behavior
lipid metabolism
inflammation
infection
Biology (General)
QH301-705.5
Chemistry
QD1-999
spellingShingle feeding behavior
lipid metabolism
inflammation
infection
Biology (General)
QH301-705.5
Chemistry
QD1-999
David Muñoz
Ricardo Fuentes
Beatriz Carnicero
Andrea Aguilar
Nataly Sanhueza
Sergio San-Martin
Cristian Agurto
Andrea Donoso
Leonardo E. Valdivia
Jesús M. Miguez
Lluis Tort
Sebastián Boltana
Viral Infection Drives the Regulation of Feeding Behavior Related Genes in <i>Salmo salar</i>
description The feeding behavior in fish is a complex activity that relies on the ability of the brain to integrate multiple signals to produce appropriate responses in terms of food intake, energy expenditure, and metabolic activity. Upon stress cues including viral infection or mediators such as the proinflammatory cytokines, prostaglandins, and cortisol, both Pomc and Npy/Agrp neurons from the hypothalamus are stimulated, thus triggering a response that controls both energy storage and expenditure. However, how appetite modulators or neuro-immune cues link pathogenesis and energy homeostasis in fish remains poorly understood. Here, we provide the first evidence of a molecular linkage between inflammation and food intake in <i>Salmon salar</i>. We show that in vivo viral challenge with infectious pancreatic necrosis virus (IPNV) impacts food consumption by activating anorexic genes such as <i>mc4r, crf,</i> and <i>pomcb</i> and 5-HT in the brain of <i>S. salar</i>. At the molecular level, viral infection induces an overall reduction in lipid content in the liver, favoring the production of AA and EPA associated with the increment of <i>elovl2</i> gene. In addition, infection upregulates leptin signaling and inhibits insulin signaling. These changes are accompanied by a robust inflammatory response represented by the increment of Il-1b, Il-6, Tnfa, and Pge2 as well as an increased cortisol level in vivo. Thus, we propose a model in which hypothalamic neurons respond to inflammatory cytokines and stress-related molecules and interact with appetite induction/inhibition. These findings provide evidence of crosstalk between pathogenesis-driven inflammation and hypothalamic–pituitary–adrenocortical axes in stress-induced food intake behavior in fish.
format article
author David Muñoz
Ricardo Fuentes
Beatriz Carnicero
Andrea Aguilar
Nataly Sanhueza
Sergio San-Martin
Cristian Agurto
Andrea Donoso
Leonardo E. Valdivia
Jesús M. Miguez
Lluis Tort
Sebastián Boltana
author_facet David Muñoz
Ricardo Fuentes
Beatriz Carnicero
Andrea Aguilar
Nataly Sanhueza
Sergio San-Martin
Cristian Agurto
Andrea Donoso
Leonardo E. Valdivia
Jesús M. Miguez
Lluis Tort
Sebastián Boltana
author_sort David Muñoz
title Viral Infection Drives the Regulation of Feeding Behavior Related Genes in <i>Salmo salar</i>
title_short Viral Infection Drives the Regulation of Feeding Behavior Related Genes in <i>Salmo salar</i>
title_full Viral Infection Drives the Regulation of Feeding Behavior Related Genes in <i>Salmo salar</i>
title_fullStr Viral Infection Drives the Regulation of Feeding Behavior Related Genes in <i>Salmo salar</i>
title_full_unstemmed Viral Infection Drives the Regulation of Feeding Behavior Related Genes in <i>Salmo salar</i>
title_sort viral infection drives the regulation of feeding behavior related genes in <i>salmo salar</i>
publisher MDPI AG
publishDate 2021
url https://doaj.org/article/1e0076ef803e41068597c48c54be850e
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