Differential effects of acute versus chronic stress on ethanol sensitivity: Evidence for interactions on both behavioral and neuroimmune outcomes

Doremus-Fitzwater, Tamara L.; Paniccia, Jacqueline E.; Gano, Anny; Vore, Andrew S.; Deak, Terrence

doi:10.1016/j.bbi.2018.02.009

Cited by 20 publications

(16 citation statements)

References 121 publications

(158 reference statements)

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“…Nevertheless, the finding that hippocampal c-Fos was more strongly induced by footshock CED group raises many questions about how the HPC is modulated by the CED procedure, and highlights this region as highly plastic in responding to predictable stressors. Indeed, other work from our laboratory has recently demonstrated that acute footshock exposure led to enhanced IL-6 responses evoked by acute ethanol intoxication, whereas CED exposure led to a blunted increase in hippocampal IL-6 as well as altered behavioral sensitivity to ethanol-induced loss of righting reflex ( Doremus-Fitzwater et al, 2018 ). Furthermore, the transition of the brain toward a more inflamed state during later stages of natural aging might be accelerated by life history of stressful events, as stress early in life is a known threat to natural aging ( Bale and Epperson, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

“…It is therefore critical to develop highly tractable models of chronic stress in which the underlying physiological mechanisms of adaptation and ultimately, adverse health consequences of stress can be studied effectively. Toward this end, a wide variety of acute stress models are commonly utilized to study the underlying neural and hormonal consequences of stress, and may have important implications for understanding sensitivity to alcohol ( Doremus-Fitzwater et al, 2018 ) and natural aging processes ( Bale and Epperson, 2015 ). To model chronic stress experienced by humans, investigators often assemble daily stress challenges to specifically manipulate psychological features of the stressful experience, including the controllability ( Maier et al, 1986 ), predictability ( Weiss, 1970 ), duration ( Martí et al, 1994 ), and general intensity ( Natelson et al, 1988 ) of the stressful circumstances.…”

Section: Introductionmentioning

confidence: 99%

“…1 A). This 11-day procedure contains 3 distinct phases that capitalize on several well-established models/findings in the literature and has previously been shown to alter behavioral and neuroimmune sensitivity to a later alcohol challenge, effects that were categorically distinct from what was observed after exposure to footshock alone ( Doremus-Fitzwater et al, 2018 ). Experiment 1 assessed body weight and CORT dynamics at several points during the CED procedure in peripheral blood as a first step toward understanding the impact of CED on general physiological manifestations of stress.…”

Section: Introductionmentioning

confidence: 99%

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Neuroendocrine and neuroimmune adaptation to Chronic Escalating Distress (CED): A novel model of chronic stress

Lovelock

Deak

2018

Neurobiology of Stress

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Acute and chronic stress challenges have a profound influence on the development and expression of subsequent affective disorders, alcohol use disorders, and natural aging processes. These experiments examined adaptation in neuroimmune and neuroendocrine responses that occurred as a result of exposure to a novel model of chronic stress, termed chronic escalating distress (CED). This model involves exposure to highly predictable daily stress challenges involving a systematic escalation in both the intensity and length of daily stress challenges, and has recently been shown to profoundly alter alcohol sensitivity. Male Sprague-Dawley rats were exposed to an 11 day procedure where days 1–5 consisted of 60  min of restraint, days 6–10 consisted of 60  min of restraint immediately followed by 30  min of forced swim, and on day 11 subjects were exposed to a 2 h session of intermittent footshock. Experiment 1 examined adaptation in the corticosterone (CORT) response at key points in the 11 day procedure, and found that the escalation in stressors disrupted habituation to restraint, whereas the CORT response to daily forced swim exposure increased across days. Experiment 2 investigated the impact of this stress paradigm on the expression of several cytokine (IL-1β, IL-6, TNF-α) and cellular activation marker (c-Fos, CD14, CD200R) genes in key brain regions (PVN, HPC, & PFC) known to be influenced by stress. Interestingly, a history of CED had no effect on footshock-induced neuroimmune changes (increased IL-1 in the PVN; increased IL-6 in the HPC and PFC). In addition, acute footshock and CED produced similar c-fos induction within the PVN whereas CED led to enhanced c-fos induction in both the HPC and PFC. These findings support recent work indicating that neuroimmune responses to acute stress challenges persisted in rats with a recent history of repeated stress exposure, and that these effects occurred contemporaneously with ongoing changes in HPA axis reactivity. Overall, this CED model may serve as a highly tractable model for studying adaptation to chronic stress, and may have implications for understanding stress-induced alterations in alcohol sensitivity and natural aging processes.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Neuroendocrine and neuroimmune adaptation to Chronic Escalating Distress (CED): A novel model of chronic stress

Lovelock

Deak

2018

Neurobiology of Stress

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“…Preclinical studies have demonstrated that in some cases, following alcohol exposure, immune proteins act as important signaling molecules in the brain in addition to their role in the periphery (Crews et al, ; Szabo and Lippai, ). For example, repeated cycles of exposure and/or larger doses of alcohol (Crews, ; Marshall et al, ; Peng et al, ; Zahr et al, ; Zhao et al, ) are known to produce a long‐lasting induction of neuroimmune genes as well as increases in levels of serum cytokines (Crews and Vetreno, ; Doremus‐Fitzwater et al, ; Doremus‐Fitzwater et al, ; Zou and Crews, ). Several preclinical studies have additionally demonstrated that adolescent alcohol exposure can also induce neuroinflammatory changes (Crews and Vetreno, ; Crews et al, ; Guerri and Pascual, ; Montesinos et al, ; Pascual et al, ).…”

mentioning

confidence: 99%

Time Course of Blood and Brain Cytokine/Chemokine Levels Following Adolescent Alcohol Exposure and Withdrawal in Rats

Sanchez‐Alavez

Nguyen

Mori

et al. 2019

Alcoholism Clin & Exp Res

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Background: Adolescence is a critical period for neural development, and alcohol exposure during adolescence can lead to an elevated risk for health consequences as well as alcohol use disorders. Clinical and experimental data suggest that chronic alcohol exposure may produce immunomodulatory effects that can lead to the activation of pro-inflammatory cytokine pathways as well as microglial markers. The present study evaluated, in brain and blood, the effects of adolescent alcohol exposure and withdrawal on microglia and on the most representative pro-and anti-inflammatory cytokines and major chemokines that can contribute to the establishing of a neuroinflammatory environment.Methods: Wistar rats (males, n = 96) were exposed to ethanol (EtOH) vapors, or air control, for 5 weeks over adolescence (PD22-PD58). Brains and blood samples were collected at 3 time points: (i) after 35 days of vapor/air exposure (PD58); (ii) after 1 day of withdrawal (PD59), and (iii) 28 days after withdrawal (PD86). The ionized calcium-binding adapter molecule 1 (Iba-1) was used to index microglial activation, and cytokine/chemokine responses were analyzed using magnetic bead panels.Results: After 35 days of adolescent vapor exposure, a significant increase in Iba-1 immunoreactivity was seen in amygdala, frontal cortex, hippocampus, and substantia nigra. However, Iba-1 density returned to control levels at both 1 day and 28 days of withdrawal except in the hippocampus where Iba-1 density was significantly lower than controls. In serum, adolescent EtOH exposure induced a reduction in IL-13 and an increase in fractalkine at day 35. After 1 day of withdrawal, IL-18 was reduced, and IP-10 was elevated, whereas both IP-10 and IL-10 were elevated at 28 days following withdrawal. In the frontal cortex, adolescent EtOH exposure induced an increase in IL-1b at day 35, and 28 days of withdrawal, and IL-10 was increased after 28 days of withdrawal.Conclusion: These data demonstrate that EtOH exposure during adolescence produces significant microglial activation; however, inflammatory markers seen in the blood appear to differ from those observed in the brain.

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“…Yet, an acute binge‐like EtOH challenge resulted in increased IL‐6 gene expression during EtOH intoxication and suppression of IL‐1β and TNF‐α, whereas clearance (withdrawal) of EtOH saw these effects reversed within 12 to 18 hours of EtOH administration (Doremus‐Fitzwater et al., , 2015; Gano et al., ). Additionally, the expression of IL‐6, but not other cytokines, was strongly influenced by prior EtOH exposure (Doremus‐Fitzwater et al., ), the schedule of EtOH exposure (Gano et al., ), and recent stress history (Doremus‐Fitzwater et al., ). Thus, the time‐dependent effects of EtOH on a multitude of cytokines suggest there would be great value in the ability to assess continuous cytokine protein changes following EtOH exposure in awake, behaving rats.…”

mentioning

confidence: 99%

Assessment of Extracellular Cytokines in the Hippocampus of the Awake Behaving Rat Using Large‐Molecule Microdialysis Combined with Multiplex Arrays After Acute and Chronic Ethanol Exposure

Gano

Vore

Sammakia

et al. 2019

Alcoholism Clin & Exp Res

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Background: Studies have demonstrated persistent changes in central nervous system (CNS) cytokine gene expression following ethanol (EtOH) exposure. However, the low endogenous expression and short half-lives of cytokines in the CNS have made cytokine protein detection challenging. The goal of these studies was to establish parameters for use of large-molecule microdialysis and sensitive multiplexing technology for the simultaneous detection of brain cytokines, corticosterone (CORT), and EtOH concentrations in the awake behaving rat.Methods: Adult (P75+) male Sprague Dawley rats that were either na€ ıve to EtOH (Experiment 1) or had a history of adolescent chronic intermittent EtOH (CIE; Experiment 2) were given an acute EtOH challenge during microdialysis. Experiment 1 examined brain EtOH concentrations, CORT and a panel of neuroimmune analytes, including cytokines associated with innate and adaptive immunity. The natural time course of changes in these cytokines was compared to the effects of an acute 1.5 or 3.0 g/kg intraperitoneal (i.p.) EtOH challenge. In Experiment 2, rats with a history of adolescent CIE or controls exposed to vehicle were challenged with 3.0 g/kg i.p. EtOH during microdialysis in adulthood, and a panel of cytokines was examined in parallel with brain EtOH concentrations and CORT.Results: The microdialysis procedure itself induced a cytokine-specific response that replicated across studies, specifically a sequential elevation of interleukin-6 (IL-6), tumor necrosis factor alpha (TNF-a), and IL-10. Surprisingly, acute EtOH did not significantly alter this course of cytokine fluctuations in the hippocampus. However, a history of adolescent CIE showed drastic effects on multiple neuroimmune analytes when rechallenged with EtOH as adults. Rats with a history of adolescent EtOH displayed a severely blunted neuroimmune response in adulthood, evinced by suppressed IL-1b, IL-10, and TNF-a.Conclusions: Together, these findings provide a methodological framework for assessment of cytokine release patterns, their modulation by EtOH, and the long-lasting changes to neuroimmune reactivity evoked by a history of adolescent CIE.

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Differential effects of acute versus chronic stress on ethanol sensitivity: Evidence for interactions on both behavioral and neuroimmune outcomes

Cited by 20 publications

References 121 publications

Neuroendocrine and neuroimmune adaptation to Chronic Escalating Distress (CED): A novel model of chronic stress

Neuroendocrine and neuroimmune adaptation to Chronic Escalating Distress (CED): A novel model of chronic stress

Time Course of Blood and Brain Cytokine/Chemokine Levels Following Adolescent Alcohol Exposure and Withdrawal in Rats

Assessment of Extracellular Cytokines in the Hippocampus of the Awake Behaving Rat Using Large‐Molecule Microdialysis Combined with Multiplex Arrays After Acute and Chronic Ethanol Exposure

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