Role of TRPM8 in switching between fever and hypothermia in adult mice during endotoxin-induced inflammation

Shiraki, Chinatsu; Horikawa, Ririka; Oe, Yuzuki; Fujimoto, Momoka; Okamoto, Kazuhiro; Kurganov, Erkin; Miyata, Seiji

doi:10.1016/j.bbih.2021.100291

Cited by 4 publications

(3 citation statements)

References 79 publications

(115 reference statements)

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“…Although mice are physiologically different from humans, it is still a widely used model. In mice, hypothermia can be displayed, but also temperature rise upon infections, particularly after LPS administrated in low doses and endotoxin [ 53 , 54 ]. Eskilsson et al (2021) have recently reported that, in mice, the humoral response is implicated in eliciting fever responses during localized inflammation [ 55 ].…”

Section: Discussionmentioning

confidence: 99%

Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo

Solar Venero,

Galeano,

Luqman

et al. 2024

BMC Biol

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Background Staphylococcus aureus (SA) and Pseudomonas aeruginosa (PA) cause a wide variety of bacterial infections and coinfections, showing a complex interaction that involves the production of different metabolites and metabolic changes. Temperature is a key factor for bacterial survival and virulence and within the host, bacteria could be exposed to an increment in temperature during fever development. We analyzed the previously unexplored effect of fever-like temperatures (39 °C) on S. aureus USA300 and P. aeruginosa PAO1 microaerobic mono- and co-cultures compared with 37 °C, by using RNAseq and physiological assays including in vivo experiments. Results In general terms both temperature and co-culturing had a strong impact on both PA and SA with the exception of the temperature response of monocultured PA. We studied metabolic and virulence changes in both species. Altered metabolic features at 39 °C included arginine biosynthesis and the periplasmic glucose oxidation in S. aureus and P. aeruginosa monocultures respectively. When PA co-cultures were exposed at 39 °C, they upregulated ethanol oxidation-related genes along with an increment in organic acid accumulation. Regarding virulence factors, monocultured SA showed an increase in the mRNA expression of the agr operon and hld, pmsα, and pmsβ genes at 39 °C. Supported by mRNA data, we performed physiological experiments and detected and increment in hemolysis, staphyloxantin production, and a decrease in biofilm formation at 39 °C. On the side of PA monocultures, we observed an increase in extracellular lipase and protease and biofilm formation at 39 °C along with a decrease in the motility in correlation with changes observed at mRNA abundance. Additionally, we assessed host–pathogen interaction both in vitro and in vivo. S. aureus monocultured at 39οC showed a decrease in cellular invasion and an increase in IL-8—but not in IL-6—production by A549 cell line. PA also decreased its cellular invasion when monocultured at 39 °C and did not induce any change in IL-8 or IL-6 production. PA strongly increased cellular invasion when co-cultured at 37 and 39 °C. Finally, we observed increased lethality in mice intranasally inoculated with S. aureus monocultures pre-incubated at 39 °C and even higher levels when inoculated with co-cultures. The bacterial burden for P. aeruginosa was higher in liver when the mice were infected with co-cultures previously incubated at 39 °C comparing with 37 °C. Conclusions Our results highlight a relevant change in the virulence of bacterial opportunistic pathogens exposed to fever-like temperatures in presence of competitors, opening new questions related to bacteria-bacteria and host–pathogen interactions and coevolution.

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Section: Discussionmentioning

confidence: 99%

Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo

Solar Venero,

Galeano,

Luqman

et al. 2024

BMC Biol

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“…Pharmacological methods have also been reported to either increase (adrenergic and cholinergic agonists, TRPV1 agonists, prostaglandins, catecholamines, cannabinoid, and thyroid hormone) or decrease BT (adrenergic or cholinergic antagonists, TRPA1 agonists, non-steroidal anti-inflammatory drugs, barbiturates, benzodiazepines, and opioids). Pyrogenic endotoxins such as LPS can cause hypothermia or fever, depending on their dose of administration and on ambient temperature 10,11 .…”

Section: Introductionmentioning

confidence: 99%

Prolonged body temperature tuning in mice using radio frequency generating electromagnetic resonant circuit-system

Franck

Borgne

Cazier

et al. 2023

Preprint

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Rational: In endothermic animals, body temperature (BT) is an evolutionary conserved and well characterized physical parameter that guarantees physiological functioning state. It results from the sum of bioenergetic processes of the body weighted by behavioral strategies, heat loss, and thermolytic processes. However, the intrinsic impact of temperature and temperature changes on the biology is far less understood. To date, the modification of the environmental temperature has constituted the main lever to evaluate the impact of thermic changes in small animal. However, studying intrinsic effect of temperature remains impossible using conventional laboratory equipment, mainly because hypothalamus instructed with information grabbed from the environmental temperature finely regulates and maintain body temperature around 37°C. Numerous pharmacological treatments have been used to block these thermoregulatory mechanisms, but confer high toxicity while dysregulating the central nervous responses and can potentially have confounding direct effects on studied peripheral tissues. Alternatively, physical methods using energy irradiation were reported, but they remain expensive and usually involve animal immobilization. We aimed at designing a simple and affordable device to adjust and maintain body temperature on the long course in conscious and free-moving animals. Method: We developed an electromagnetic LC resonant circuit (ELM circuit) producing a radio frequency signal (64 kHz) inside a copper coil refrigerated with a water circuit. This setting is powered by a simple a 0-48V AC generator, allowing the use of a domestic electrical network. This setting can accommodate metal-free 3D-printed circular cages, where adult mice, previously implanted with thermometric ID transponders, are monitored remotely for intraperitoneal temperature over time. Results: The BT of mice placed in the ELM circuit could be regulated in a reproducible fashion. Healthy mice increased their BT from 37 to 39.8±1°C, upon power supply ranging from 0 to 48V, respectively. In septic mice developing hypothermia (33±1 °C), BT could be either normalized to normothermia (37°C, 24V), or increased to fever-range hyperthermia (40°C, 48V) as a function of radiofrequency energy. BT tuning was accurate and stable for at least 12h. Blood count after 6 or 12 hours showed no modifications between groups, cardiomyocyte displayed heat shock response within the first hour in mice exposed to the maximal dose (BT = 41°C). MALDI TOF imaging on brain microsections revealed modifications of the brain proteome, as suggested by differential PKC-theta, and prolactin 7B1 load in heated mice, as compared to controls. Conclusion: Precise body temperature tuning is achievable in small animals, and could be of high interest to understand the impact of temperature in (patho)physiology.

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“…There is no apparent difference in the activation of NF-κB and STAT3 between astrocytes and tanycytes after peripheral administration of LPS ( Nakano et al, 2015 ; Muneoka et al, 2019 ). In TRM8 KO mice, ( Shiraki et al, 2021 ; Kasuga et al, 2022 ) i.c.v. injection of an LPS antagonist LPS-RS attenuates NF-κB signaling in the astrocytes and tanycytes of the CVOs after peripheral administration of LPS ( Muneoka et al, 2019 ).…”

Section: General Introductionmentioning

confidence: 99%

Glial functions in the blood-brain communication at the circumventricular organs

Miyata

2022

Front. Neurosci.

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The circumventricular organs (CVOs) are located around the brain ventricles, lack a blood-brain barrier (BBB) and sense blood-derived molecules. This review discusses recent advances in the importance of CVO functions, especially glial cells transferring periphery inflammation signals to the brain. The CVOs show size-limited vascular permeability, allowing the passage of molecules with molecular weight <10,000. This indicates that the lack of an endothelial cell barrier does not mean the free movement of blood-derived molecules into the CVO parenchyma. Astrocytes and tanycytes constitute a dense barrier at the distal CVO subdivision, preventing the free diffusion of blood-derived molecules into neighboring brain regions. Tanycytes in the CVOs mediate communication between cerebrospinal fluid and brain parenchyma via transcytosis. Microglia and macrophages of the CVOs are essential for transmitting peripheral information to other brain regions via toll-like receptor 2 (TLR2). Inhibition of TLR2 signaling or depletion of microglia and macrophages in the brain eliminates TLR2-dependent inflammatory responses. In contrast to TLR2, astrocytes and tanycytes in the CVOs of the brain are crucial for initiating lipopolysaccharide (LPS)-induced inflammatory responses via TLR4. Depletion of microglia and macrophages augments LPS-induced fever and chronic sickness responses. Microglia and macrophages in the CVOs are continuously activated, even under normal physiological conditions, as they exhibit activated morphology and express the M1/M2 marker proteins. Moreover, the microglial proliferation occurs in various regions, such as the hypothalamus, medulla oblongata, and telencephalon, with a marked increase in the CVOs, due to low-dose LPS administration, and after high-dose LPS administration, proliferation is seen in most brain regions, except for the cerebral cortex and hippocampus. A transient increase in the microglial population is beneficial during LPS-induced inflammation for attenuating sickness response. Transient receptor potential receptor vanilloid 1 expressed in astrocytes and tanycytes of the CVOs is responsible for thermoregulation upon exposure to a warm environment less than 37°C. Alternatively, Nax expressed in astrocytes and tanycytes of the CVOs is crucial for maintaining body fluid homeostasis. Thus, recent findings indicate that glial cells in the brain CVOs are essential for initiating neuroinflammatory responses and maintaining body fluid and thermal homeostasis.

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Role of TRPM8 in switching between fever and hypothermia in adult mice during endotoxin-induced inflammation

Cited by 4 publications

References 79 publications

Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo

Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo

Prolonged body temperature tuning in mice using radio frequency generating electromagnetic resonant circuit-system

Glial functions in the blood-brain communication at the circumventricular organs

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