Reciprocal interaction between the suprachiasmatic nucleus and the immune system tunes down the inflammatory response to lipopolysaccharide

Guerrero‐Vargas, Natalí N.; Salgado‐Delgado, Roberto; Basualdo, María del Carmen; García, Joselyn; Guzmán-Ruiz, Mara; Carrero, Julio César; Escobar, Carolina; Buijs, Ruud M.

doi:10.1016/j.jneuroim.2014.05.012

Cited by 55 publications

(60 citation statements)

References 84 publications

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“…A day-night rhythm in the susceptibility to lethal doses of LPS has already been demonstrated, and inflammation may directly affect the SCN, as suggested by the LPS-induced phase delays during the subjective night [21]. These time-dependent effects are reflected in several phenomena since LPS administration at the beginning of the active period induces severer responses in temperature and proinflammatory cytokines than LPS given in the rest period [22]. As a matter of fact, the evolution of the acute inflammatory environment occurs rapidly, when LPS induces substantially higher levels of cytokines with peak levels between 1.5 and 4 h, which begins to decline 8 h after administration [18].…”

Section: Discussionmentioning

confidence: 99%

Suprachiasmatic Nucleus and Subordinate Brain Oscillators: Clock Gene Desynchronization by Neuroinflammation

Campos

Buchaim

Silva

et al. 2017

Neuroimmunomodulation

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Objective: The clock genes Period (per) 1 and 2 are essential components in the generation and adjustment of biological circadian rhythms by the suprachiasmatic nucleus (SCN). Both genes are also rhythmically present in extrahypothalamic areas such as the hippocampus and cerebellum, considered subordinate oscillators. Several pathological conditions alter rhythmic biological phenomena, but the mechanisms behind these changes involving the clock genes are not well defined. The current study investigated changes in PER1 and PER2 immunoreactivity in the SCN, hippocampus, and cerebellum in a neuroinflammation model. Methods: Wistar rats received lipopolysaccharide (LPS) or vehicle intracerebroventricularly. The melatonin plasmatic content was quantified by ELISA to confirm the alterations in biological rhythms, and PER1 and PER2 immunoreactivities were analyzed in brain sections by immunohistochemistry. Results: In the SCN, intracerebroventricular LPS changed PER1 expression, increasing the number of PER1-immunoreactive (IR) cells at zeitgeber time (ZT) 15, decreasing it at ZT5 and ZT20 and not changing it at ZT10. LPS also induced a decrease in PER2-IR cells at ZT5, ZT10, and ZT15 but not at ZT20 in the SCN. In the hippocampus, LPS induced a decrease in PER1-IR and PER2-IR cells at both ZTs (ZT10 and ZT15). In the cerebellum, LPS increased the number of PER1-IR cells at ZT10 and decreased it at ZT15, while the number of PER2-IR cells was reduced at both ZTs. Conclusions: These results indicate that a neuroinflammatory condition leads to desynchronization of primary and subordinate brain oscillators, supporting the existence of the integration between the immune and the circadian system.

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Section: Discussionmentioning

confidence: 99%

Suprachiasmatic Nucleus and Subordinate Brain Oscillators: Clock Gene Desynchronization by Neuroinflammation

Campos

Buchaim

Silva

et al. 2017

Neuroimmunomodulation

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“…LPS has been reported to attenuate (Wachulec et al, 1997) or exacerbate (Guerrero-Vargas et al, 2014) T b responses to LPS in SCNx rats. The dose of LPS and route of administration may account for these divergent results.…”

Section: Discussionmentioning

confidence: 99%

“…The dose of LPS and route of administration may account for these divergent results. Species and sex differences (Wachulec et al, 1997; Guerrero-Vargas et al, 2014) and the procedures employed to induce circadian arrhythmia also may affect responses to LPS. For example, the effects of circadian arrhythmia on memory processing differ categorically depending on whether arrhythmia is induced via SCNx or DPS (Fernandez et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Circadian Disruption Alters the Effects of Lipopolysaccharide Treatment on Circadian and Ultradian Locomotor Activity and Body Temperature Rhythms of Female Siberian Hamsters

et al. 2015

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The effect of circadian rhythm (CR) disruption on immune function depends on the method by which CRs are disrupted. Behavioral and thermoregulatory responses induced by lipopolysaccharide (LPS) treatment were assessed in female Siberian hamsters in which circadian locomotor activity (LMA) rhythms were eliminated by exposure to a disruptive phase-shifting protocol (DPS) that sustains arrhythmicity even when hamsters are housed in a light-dark cycle. This noninvasive treatment avoids genome manipulations and neurological damage associated with other models of CR disruption. Circadian rhythmic (RHYTH) and arrhythmic (ARR) hamsters housed in a 16L:8D photocycle were injected with bacterial LPS near the onset of the light (zeitgeber time 1; ZT1) or dark (ZT16) phase. LPS injections at ZT16 and ZT1 elicited febrile responses in both RHYTH and ARR hamsters, but the effect was attenuated in the arrhythmic females. In ZT16, LPS inhibited LMA in the dark phase immediately after injection but not on subsequent nights in both chronotypes; in contrast, LPS at ZT1 elicited more enduring (~4 day) locomotor hypoactivity in ARR than in RHYTH hamsters. Power and period of dark-phase ultradian rhythms (URs) in LMA and Tb were markedly altered by LPS treatment, as was the power in the circadian waveform. Disrupted circadian rhythms in this model system attenuated responses to LPS in a trait- and ZT-specific manner; changes in UR period and power are novel components of the acute-phase response to infection that may affect energy conservation.

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“…Cytokine and sickness responses are also altered following disruption of the circadian timing system (lesions: Wachulec et al, 1997; Guerrero-Vargas et al, 2014; disruptive light treatments: Prendergast et al, 2015; simulated shift work: Guerrero-Vargas et al, 2015). CRs in immunity are not limited to innate immune responses: T cell-dependent inflammation (a measure of the adaptive immune response) is greater when antigen exposure occurs during the rest as compared to the active phase ( Pownall et al, 1979).…”

Section: Introductionmentioning

confidence: 99%

Circadian rhythms accelerate wound healing in female Siberian hamsters

Cable

Onishi

Prendergast

2017

Physiology & Behavior

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Circadian rhythms (CRs) provide temporal regulation and coordination of numerous physiological traits, including immune function. CRs in multiple aspects of immune function are absent in rodents that have been rendered circadian-arrhythmic through various methods. In Siberian hamsters, circadian arrhythmia can be induced by disruptive light treatments (DPS). Here we examined CRs in wound healing, and the effects of circadian disruption on wound healing in DPS-arrhythmic hamsters. Circadian entrained/rhythmic (RHYTH) and behaviorally-arrhythmic (ARR) female hamsters were administered a cutaneous wound either 3 h after light onset (ZT03) or 2 h after dark onset (ZT18); wound size was quantified daily using image analyses. Among RHYTH hamsters, ZT03 wounds healed faster than ZT18 wounds, whereas in ARR hamsters, circadian phase did not affect wound healing. In addition, wounds healed slower in ARR hamsters. The results document a clear CR in wound healing, and indicate that the mere presence of organismal circadian organization enhances this aspect of immune function. Faster wound healing in CR-competent hamsters may be mediated by CR-driven coordination of the temporal order of mechanisms (inflammation, leukocyte trafficking, tissue remodeling) underlying cutaneous wound healing.

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Reciprocal interaction between the suprachiasmatic nucleus and the immune system tunes down the inflammatory response to lipopolysaccharide

Cited by 55 publications

References 84 publications

Suprachiasmatic Nucleus and Subordinate Brain Oscillators: Clock Gene Desynchronization by Neuroinflammation

Suprachiasmatic Nucleus and Subordinate Brain Oscillators: Clock Gene Desynchronization by Neuroinflammation

Circadian Disruption Alters the Effects of Lipopolysaccharide Treatment on Circadian and Ultradian Locomotor Activity and Body Temperature Rhythms of Female Siberian Hamsters

Circadian rhythms accelerate wound healing in female Siberian hamsters

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