Sex differences in depression-like behavior after nerve injury are associated with differential changes in brain-derived neurotrophic factor levels in mice subjected to early life stress

Nishinaka, Takashi; Kinoshita, Megumi; Nakamoto, Kazuo; Tokuyama, Shogo

doi:10.1016/j.neulet.2015.02.053

Cited by 30 publications

(18 citation statements)

References 46 publications

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“…In addition, though sex differences have not been widely studied in human studies or seen in many results, the interaction of prenatal opiate exposure, poor environmental conditions or stress, and the sex of the individual are likely important to consider when examining the immediate and long-term consequences of prenatal opiate exposure on cognitive outcomes. This is particularly important given that there is substantial evidence that males may be more vulnerable to the impact of early-life stressors such as maternal separation [50][51][52][53]. In addition, the observations of Slamberova et al [43] and Nasiraei-Moghadam et al [44] in rodents suggest that sex hormones during puberty may play a role in the sexdependent risk of cognitive and behavioural deficits caused by prenatal opiate exposure.…”

Section: (A) Prenatal Exposure To Opiatesmentioning

confidence: 99%

An examination of sex differences in the effects of early-life opiate and alcohol exposure

Terasaki¹,

Gomez²,

Schwarz³

2016

Phil. Trans. R. Soc. B

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One contribution of 16 to a theme issue 'Multifaceted origins of sex differences in the brain'. Early-life exposure to drugs and alcohol is one of the most preventable causes of developmental, behavioural and learning disorders in children. Thus a significant amount of basic, animal and human research has focused on understanding the behavioural consequences and the associated neural effects of exposure to drugs and alcohol during early brain development. Despite this, much of the previous research that has been done on this topic has used predominantly male subjects or rodents. While many of the findings from these male-specific studies may ultimately apply to females, the purpose of this review is to highlight the research that has also examined sex as a factor and found striking differences between the sexes in their response to early-life opiate and alcohol exposure. Finally, we will also provide a framework for scientists interested in examining sex as a factor in future experiments that specifically examine the consequences of early-life drug and alcohol exposure.

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Section: (A) Prenatal Exposure To Opiatesmentioning

confidence: 99%

An examination of sex differences in the effects of early-life opiate and alcohol exposure

Terasaki¹,

Gomez²,

Schwarz³

2016

Phil. Trans. R. Soc. B

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“…As mentioned above, some studies using different strains found distinct responses to maternal separation according to the sex of the studied animals (Kundakovic et al, 2013;Meagher et al, 2010;Nishinaka et al, 2015;Romeo et al, 2003). Comparisons of maternal separation mice and control mice without sex 20 distinction could represent an important bias for data interpretation because they do not take into account the sex-specific biological profile of the animals (Toufexis et al, 2014).…”

Section: Inconsistencies In Ms Studies and Possible Effects On Findingsmentioning

confidence: 99%

An overview of maternal separation effects on behavioural outcomes in mice: Evidence from a four-stage methodological systematic review

Tractenberg

Levandowski

Azeredo

et al. 2016

Neuroscience & Biobehavioral Reviews

218

203

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“…However, the GFAP expression in the LC of MSSI mice with PSL was different between males and females. We previously showed that MSSI sex-dependently induced emotional dysfunction after nerve injury, which was associated with sex differences in the stress-induced regulation of BDNF expression (Nishinaka et al, 2015a). It is thought that neuronal function in the brain of male mice is protected from early life stresses, such as MSSI, by altered expression of several stress-responsive factors, including BDNF upregulation, such that MSSI male mice might acquire resistance to stress.…”

Section: Discussionmentioning

confidence: 99%

“…On the other hand, there is no increased GFAP expression following MSSI in male mice although MSSI-mediated neuropathic pain exacerbation observed in male mice (Nishinaka et al, 2015a). This discrepancy between male and female indicates that other factors which inhibit astrocyte activation may be produced in MSSI stressed male mice, but not female stressed mice.…”

Section: Discussionmentioning

confidence: 99%

Astrocyte Activation in Locus Coeruleus Is Involved in Neuropathic Pain Exacerbation Mediated by Maternal Separation and Social Isolation Stress

et al. 2017

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Our previous studies demonstrated that emotional dysfunction associated with early life stress exacerbated nerve injury-induced mechanical allodynia. Sex differences were observed in several anxiety tests, but not in mechanical allodynia. To elucidate the mechanism underlying these findings, we have now investigated the involvement of astrocytes in emotional dysfunction and enhancement of nerve injury-induced mechanical allodynia in mice subjected to maternal separation combined with social isolation (MSSI) as an early life stress. We measured expression of glial fibrillary acidic protein (GFAP), an astrocyte maker, in each brain area by immunohistochemistry. GFAP expression in the locus coeruleus (LC) of female, but not of male mice, significantly increased after MSSI, corresponding to the behavioral changes at 7 and 12 weeks of age. Lipopolysaccharide (LPS)-treated astrocyte-derived supernatant was administered to local brain regions, including LC. Intra-LC injection of conditioned medium from cultured astrocytes treated with LPS increased GFAP expression, anxiety-like behavior and mechanical allodynia in both male and female mice. Furthermore, increases in anxiety-like behavior correlated with increased mechanical allodynia. These findings demonstrate that emotional dysfunction and enhanced nerve injury-induced mechanical allodynia after exposure to MSSI are mediated, at least in part, by astrocyte activation in the LC. Male but not female mice may show resistance to MSSI stress during growth.

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Sex differences in depression-like behavior after nerve injury are associated with differential changes in brain-derived neurotrophic factor levels in mice subjected to early life stress

Cited by 30 publications

References 46 publications

An examination of sex differences in the effects of early-life opiate and alcohol exposure

An examination of sex differences in the effects of early-life opiate and alcohol exposure

An overview of maternal separation effects on behavioural outcomes in mice: Evidence from a four-stage methodological systematic review

Astrocyte Activation in Locus Coeruleus Is Involved in Neuropathic Pain Exacerbation Mediated by Maternal Separation and Social Isolation Stress

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