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Molecular Mechanism of Thermoregulation in Ectotherms

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Biochemistry".

Deadline for manuscript submissions: closed (30 July 2021) | Viewed by 5924

Special Issue Editor


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Guest Editor
Biotechnology Center, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepcion, Concepcion, Chile
Interests: temperature; fever; thermoregulation; climate change; methylation; inflammatory reflex; cholinergic receptor; thermal perception

Special Issue Information

Dear Colleagues,

Many vertebrates regulate their body temperature in response to thermal variability of the environment. Endotherms maintain relatively stable body temperatures by adjusting metabolic heat production in response to varying environmental heat loads. Although most ectotherms do not display adaptive thermogenesis, they do adapt the cellular machinery and behavioral mechanism to compensate for environmental temperature variation. In general, the maintenance of the core body temperature is a critical brain function accomplished by the central neural network. This orchestrates a complex behavioral and autonomic repertoire in response to environmental temperature challenges or in support of immune responses (e.g., fever). In general, some components of the thermoregulatory systems in endotherms and ectotherms have been evolutionarily conserved. For example, it has been shown that environmental temperature is detected by the primary afferents of the somatosensory neurons in the skin, which express a set of ion channels (TRP receptor family) to detect particular temperatures. Thermal sensory (afferent) information is relayed to the brain (hypothalamus), which initiates a sympathetic efferent response. In recent years, several studies have revealed a number of receptor ion channels that mediate the perception of several temperature ranges. Most of the knowledge about thermoregulation and thermoperception corresponds to mammals and model animals such as rodents, mice and rats; however, the underlying molecular mechanism of the thermoregulation in ectotherms remains unknown. The present Special Issue will allow us to gain an understanding of the anatomical, thermoreceptor and functional relationships within the molecular network that control the thermoregulation in ectotherms. Delineating the molecular circuit mechanism underlying the thermoregulation provides us with a platform for exploring its functional organization, elucidating the molecular underpinnings of its interactions, and discovering novel approaches to modulating body temperature, as well as being able to understand how the ectotherms may cope with climate change.

Prof. Dr. Sebastian Boltana
Guest Editor

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Keywords

  • temperature
  • homeostasis
  • ectotherms
  • thermoregulation
  • thermal perception
  • TRP channels
  • sensory neuron
  • fever

Published Papers (2 papers)

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17 pages, 5359 KiB  
Article
Viral Infection Drives the Regulation of Feeding Behavior Related Genes in Salmo salar
by 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 and Sebastián Boltana
Int. J. Mol. Sci. 2021, 22(21), 11391; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms222111391 - 21 Oct 2021
Cited by 2 | Viewed by 2478
Abstract
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 [...] Read more.
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 Salmon salar. We show that in vivo viral challenge with infectious pancreatic necrosis virus (IPNV) impacts food consumption by activating anorexic genes such as mc4r, crf, and pomcb and 5-HT in the brain of S. salar. 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 elovl2 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. Full article
(This article belongs to the Special Issue Molecular Mechanism of Thermoregulation in Ectotherms)
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24 pages, 5872 KiB  
Article
Behavioural Fever Promotes an Inflammatory Reflex Circuit in Ectotherms
by Nataly Sanhueza, Ricardo Fuentes, Andrea Aguilar, Beatriz Carnicero, Karina Vega, David Muñoz, David Contreras, Nataly Moreno, Eduardo Troncoso, Luis Mercado, Byron Morales-Lange and Sebastian Boltana
Int. J. Mol. Sci. 2021, 22(16), 8860; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22168860 - 17 Aug 2021
Cited by 4 | Viewed by 2446
Abstract
Background: The communication between the brain and the immune system is a cornerstone in animal physiology. This interaction is mediated by immune factors acting in both health and pathogenesis, but it is unclear how these systems molecularly and mechanistically communicate under changing environmental [...] Read more.
Background: The communication between the brain and the immune system is a cornerstone in animal physiology. This interaction is mediated by immune factors acting in both health and pathogenesis, but it is unclear how these systems molecularly and mechanistically communicate under changing environmental conditions. Behavioural fever is a well-conserved immune response that promotes dramatic changes in gene expression patterns during ectotherms’ thermoregulatory adaptation, including those orchestrating inflammation. However, the molecular regulators activating the inflammatory reflex in ectotherms remain unidentified. Methods: We revisited behavioural fever by providing groups of fish a thermal gradient environment during infection. Our novel experimental setup created temperature ranges in which fish freely moved between different thermal gradients: (1) wide thermoregulatory range; T° = 6.4 °C; and (2) restricted thermoregulatory range; T° = 1.4 °C. The fish behaviour was investigated during 5-days post-viral infection. Blood, spleen, and brain samples were collected to determine plasmatic pro- and anti-inflammatory cytokine levels. To characterize genes’ functioning during behavioural fever, we performed a transcriptomic profiling of the fish spleen. We also measured the activity of neurotransmitters such as norepinephrine and acetylcholine in brain and peripheral tissues. Results: We describe the first set of the neural components that control inflammatory modulation during behavioural fever. We identified a neuro-immune crosstalk as a potential mechanism promoting the fine regulation of inflammation. The development of behavioural fever upon viral infection triggers a robust inflammatory response in vivo, establishing an activation threshold after infection in several organs, including the brain. Thus, temperature shifts strongly impact on neural tissue, specifically on the inflammatory reflex network activation. At the molecular level, behavioural fever causes a significant increase in cholinergic neurotransmitters and their receptors’ activity and key anti-inflammatory factors such as cytokine Il10 and Tgfβ in target tissues. Conclusion: These results reveal a cholinergic neuronal-based mechanism underlying anti-inflammatory responses under induced fever. We performed the first molecular characterization of the behavioural fever response and inflammatory reflex activation in mobile ectotherms, identifying the role of key regulators of these processes. These findings provide genetic entry points for functional studies of the neural–immune adaptation to infection and its protective relevance in ectotherm organisms. Full article
(This article belongs to the Special Issue Molecular Mechanism of Thermoregulation in Ectotherms)
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