Age and sex differences in c-Fos expression and serum corticosterone concentration following LPS treatment

Girard-Joyal, Olivier; Faragher, A; Bradley, Kelly A.; Kane, Leanne; Hrycyk, Lianna; Ismail, Nafissa

doi:10.1016/j.neuroscience.2015.06.035

Cited by 57 publications

(34 citation statements)

References 39 publications

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“…While most previous studies carried out on adults report increased corticosterone levels after systemic inflammatory challenge (Kohman et al 2008; Kasahara et al 2015; Girard-Joyal et al 2015), we found that early-life administration of two different doses of LPS produced a prominent decrease in corticosterone, suggesting compensatory changes in the HPA system. Various challenges that normally increase HPA activity and corticosterone levels in adulthood (Maccari et al 2003; Weinstock 2008) have been shown to have no effect (Koenig et al 2005; Weinstock 2008; Dinel et al 2014) or, like in our study, result in decreases (Cannizzaro et al 2006; Solati et al 2015) when applied during development.…”

Section: Discussioncontrasting

confidence: 64%

“…One of the explanations for the paradoxical decrease of plasma corticosterone in our work can be due to the previously discussed over-expression of hypothalamic hormones regulating adrenal function after early-life LPS injection, which may be followed by a compensatory suppression of glucocorticoid production (Shanks et al 1995; Dinel et al 2014). The direction of corticosterone changes in rodents postnatally treated with LPS was shown to be linked to the development period (Dinel et al 2014; Girard-Joyal et al 2015). For instance, the effects of LPS on blood corticosterone levels in mice were significantly weaker at the peripubertal/adolescent period, particularly in males.…”

Section: Discussionmentioning

confidence: 99%

“…In the present study, we investigate whether or not an early-life (P15–P21) pro-inflammatory LPS challenge that closely mimics clinical conditions alters motor learning in rats. As altered hypothalamic–pituitary–adrenal (HPA) axis functions are one of the long-lasting consequences of early-life inflammatory challenge and are known to negatively affect motor learning (Girard-Joyal et al 2015; Kasahara et al 2015), we also assessed hormonal and behavioural measures of stress response in postnatally challenged adult rats.…”

Section: Introductionmentioning

confidence: 99%

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Postnatal LPS Challenge Impacts Escape Learning and Expression of Plasticity Factors Mmp9 and Timp1 in Rats: Effects of Repeated Training

et al. 2017

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Bacterial intoxication associated with inflammatory conditions during development can impair brain functions, in particular evolutionarily novel forms of memory, such as explicit learning. Little is known about the dangers of early-life inflammation on more basic forms of learning, for example, the acquisition of motor escape abilities, which are generally better preserved under pathological conditions. To address this limitation in knowledge, an inflammatory response was elicited in Wistar pups by lipopolysaccharide (LPS) injections (25 μg/kg) on postnatal days P15, P18 and P21. The acquisition of escape behaviour was tested from P77 by active avoidance footshock model and water maze. Open-field behaviour and blood corticosterone levels were also measured. Rat brain tissue was collected from pups 2 h post-injection and from adult rats which either underwent escape training on P77–P81 or remained untrained. mRNA levels of developmental brain plasticity factors MMP-9 and TIMP-1 were investigated in the medial prefrontal cortex and ventral/dorsal hippocampus. LPS-challenged rats displayed moderately deficient escape responses in both memory tests, increased freezing behaviour and, surprisingly, reduced blood cortisol levels. Mmp9 and Timp1, and their ratio to one another, were differentially altered in pups versus adult untrained rats but remained unchanged overall in rats trained in either learning task. Together, our data indicate that systemic pro-inflammatory response during early postnatal development has long-lasting effects, including on the acquisition of motor escape abilities and plasticity factor expression, into adulthood. Our data suggest that altered stress response could possibly mediate these deviations and repeated training might generate positive effects on plasticity under the employed conditions.Electronic supplementary materialThe online version of this article (doi:10.1007/s12640-017-9720-2) contains supplementary material, which is available to authorized users.

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Section: Discussioncontrasting

confidence: 64%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Postnatal LPS Challenge Impacts Escape Learning and Expression of Plasticity Factors Mmp9 and Timp1 in Rats: Effects of Repeated Training

et al. 2017

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“…For instance, brief exposures to a novel environment (Goldman et al, 1973) or social isolation (Hodges et al, 2014) result in similar corticosterone responses in pre-, mid- and post-adolescent rats. Furthermore, some stressors, such as exposure to lipopolysaccharide (Girard-Joyal et al, 2015; Goble et al, 2011) or placement in the open arm of an elevated plus maze (McCormick et al, 2008) evoke lesser ACTH and/or corticosterone secretion in pre- and mid-adolescent male rats and female mice compared to adults (Figure 3). Therefore, these data highlight the importance of stressor type in instigating age-dependent changes in hormonal stress reactivity.…”

Section: Adolescent Development Of Hpa Stress Reactivitymentioning

confidence: 99%

Adolescence and the ontogeny of the hormonal stress response in male and female rats and mice

Romeo

Patel

Pham

et al. 2016

Neuroscience & Biobehavioral Reviews

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Adolescent development is marked by many changes in neuroendocrine function, resulting in both immediate and long-term influences on an individual’s physiology and behavior. Stress-induced hormonal responses are one such change, with adolescent animals often showing different patterns of hormonal reactivity following a stressor compared with adults. This review will describe the unique ways in which adolescent animals respond to a variety of stressors and how these adolescent-related changes in hormonal responsiveness can be further modified by the sex and previous experience of the individual. Potential central and peripheral mechanisms that contribute to these developmental shifts in stress reactivity are also discussed. Finally, the short- and long-term programming effects of chronic stress exposure during adolescence on later adult hormonal responsiveness are also examined. Though far from a clear understanding of the neurobehavioral consequences of these adolescent-related shifts in stress reactivity, continued study of developmental changes in stress-induced hormonal responses may shed light on the increased vulnerability to physical and psychological dysfunctions that often accompany a stressful adolescence.

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“…Recent findings suggest that differences in the acute stress and immune responses between pubertal and adult male and female mice can provide mechanistic insight into the enduring behavioural alterations following LPS exposure. While LPS treatment increases serum corticosterone concentration in all pubertal and adult male and female mice, adult females show the highest increase two hours after treatment (Girard‐Joyal et al, 2015). Exposure to LPS also results in an increase in c‐Fos expression in many brain regions in adult mice but not in pubertal mice two hours following LPS treatment (Girard‐Joyal et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Sex differences in the peripheral and central immune responses following lipopolysaccharide treatment in pubertal and adult CD‐1 mice

Sharma

Rooke

Kolmogorova

et al. 2018

Intl J of Devlp Neuroscience

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Puberty is a critical developmental period that is characterized by significant brain development. Exposure to stress during this time can alter brain functioning setting the stage for long-lasting behavioural outcomes. The objective of this study was to investigate age and sex differences in the peripheral and central immune responses, along with sickness behaviour, following immune stress. The results showed that LPS treatment increased serum cytokine levels and sickness symptoms in all mice. Pubertal males displayed increased IL-1β concentrations at 2 h and increased IL-6 concentrations at 8 h post-treatment whereas increased concentrations of TNFα, IL-10, IL-12, IL-1β, IFNγ, and IL-6 persisted at 8 and 24 h in adult females. Consistent with peripheral cytokines, pubertal males displayed greater IL-1β, TNFα, and IL-6 mRNA expression in the prefrontal cortex at 2 h, whereas adult males expressed more of the aforementioned cytokines at 8 h compared to saline controls. Adult males also displayed greater IL-1β mRNA expression compared to their female counterparts, and adult females displayed greater TNFα mRNA expression compared to their male counterparts. These results not only provide a better understanding of the age and sex differences in acute immune response, but also show important region- and time-specific differences in the response to an immune challenge, and that the peripheral immune response differs from the central response. This highlights the need to examine immune markers in both the periphery and the central nervous system for an accurate depiction of acute immune response following an immune challenge.

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Age and sex differences in c-Fos expression and serum corticosterone concentration following LPS treatment

Cited by 57 publications

References 39 publications

Postnatal LPS Challenge Impacts Escape Learning and Expression of Plasticity Factors Mmp9 and Timp1 in Rats: Effects of Repeated Training

Postnatal LPS Challenge Impacts Escape Learning and Expression of Plasticity Factors Mmp9 and Timp1 in Rats: Effects of Repeated Training

Adolescence and the ontogeny of the hormonal stress response in male and female rats and mice

Sex differences in the peripheral and central immune responses following lipopolysaccharide treatment in pubertal and adult CD‐1 mice

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