Sex Differences in Nucleus Accumbens Transcriptome Profiles Associated with Susceptibility versus Resilience to Subchronic Variable Stress

Hodes, Georgia E.; Pfau, Madeline L.; Purushothaman, Immanuel; Ahn, Hongryul; Golden, Sam A.; Christoffel, Daniel J.; Magida, Jane; Brancato, Anna; Takahashi, Akiyoshi; Flanigan, Meghan E.; Ménard, Caroline; Aleyasin, Hossein; Koo, Ja Wook; Lorsch, Zachary S.; Feng, Jian; Heshmati, Mitra; Wang, Minghui; Turecki, Gustavo; Neve, Rachel L.; Zhang, Bin; Shen, Li; Nestler, Eric J.; Russo, Scott J.

doi:10.1523/jneurosci.1392-15.2015

Cited by 332 publications

(385 citation statements)

References 82 publications

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“…Herpes simplex virus (HSV) plasmids were packaged into high-titer viral particles as described previously (Maze et al, 2010). Viral titers were between 3 and 4 ϫ 10 8 particles/ml.…”

Section: Methodsmentioning

confidence: 99%

“…Place conditioning was performed as described previously (Maze et al, 2010) with slight modifications. Several visual and nonvisual (tactile) cues enabled the animals to distinguish two side chambers of a three-chamber apparatus.…”

Section: Methodsmentioning

confidence: 99%

“…We next examined the regulation of Baz1b in NAc by CSDS, an ethologically validated mouse model of depression (Berton et al, 2006;Hollis et al, 2011). Over 10 consecutive days, C57BL/6J male mice were subjected to daily 10 min aggressive encounters with CD1 mice, followed by sensory but not physical contact for the remainder of the day.…”

Section: Baz1b and Smarca5 In Csdsmentioning

confidence: 99%

“…Chronic cocaine administration and chronic social defeat stress (CSDS) each alter gene expression in the nucleus accumbens (NAc), an important brain reward region, and chromatin regulation-in particular, histone writers and erasers as well as proteins that control DNA methylation-has been shown to be important for mediating these events (Renthal et al, 2007;Hunter et al, 2009;Jiang et al, 2010;Maze et al, 2010;Covington et al, 2011;Hollis et al, 2011;Deng et al, 2014;Feng et al, 2015;Hodes et al, 2015). ATP-dependent chromatin remodeling complexes also play a key role in regulating nucleosome positioning to control gene expression and have recently been implicated in complex behavior such as learning and memory (Whitehouse et al, 2007;Clapier and Cairns, 2009;Yen et al, 2012;Narlikar et al, 2013;Vogel-Ciernia et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…The BAZ family of proteins contain a BAZ type of bromodomain (Jones et al, 2000) and BAZ1B in particular is implicated in several chromatin remodeling/transcriptional complexes (including associating with the ISWI subunit, SMARCA5) with diverse roles in regulating DNA replication, DNA repair, and transcription (Bozhenok et al, 2002;Poot et al, 2004;Cavellán et al, 2006;Percipalle et al, 2006;Xiao et al, 2009;Vintermist et al, 2011;Culver-Cochran and Chadwick, 2013;Lundqvist et al, 2013;Sarshad et al, 2013;Takada, 2015).…”

Section: Introductionmentioning

confidence: 99%

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BAZ1B in Nucleus Accumbens Regulates Reward-Related Behaviors in Response to Distinct Emotional Stimuli

et al. 2016

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ATP-dependent chromatin remodeling proteins are being implicated increasingly in the regulation of complex behaviors, including models of several psychiatric disorders. Here, we demonstrate that Baz1b, an accessory subunit of the ISWI family of chromatin remodeling complexes, is upregulated in the nucleus accumbens (NAc), a key brain reward region, in both chronic cocaine-treated mice and mice that are resilient to chronic social defeat stress. In contrast, no regulation is seen in mice that are susceptible to this chronic stress. Viral-mediated overexpression of Baz1b, along with its associated subunit Smarca5, in mouse NAc is sufficient to potentiate both rewarding responses to cocaine, including cocaine self-administration, and resilience to chronic social defeat stress. However, despite these similar, proreward behavioral effects, genome-wide mapping of BAZ1B in NAc revealed mostly distinct subsets of genes regulated by these chromatin remodeling proteins after chronic exposure to either cocaine or social stress. Together, these findings suggest important roles for BAZ1B and its associated chromatin remodeling complexes in NAc in the regulation of reward behaviors to distinct emotional stimuli and highlight the stimulus-specific nature of the actions of these regulatory proteins.

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“…Herpes simplex virus (HSV) plasmids were packaged into high-titer viral particles as described previously (Maze et al, 2010). Viral titers were between 3 and 4 ϫ 10 8 particles/ml.…”

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Baz1b and Smarca5 In Csdsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

BAZ1B in Nucleus Accumbens Regulates Reward-Related Behaviors in Response to Distinct Emotional Stimuli

et al. 2016

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Widespread transcriptional alternations in oligodendrocytes in the adult mouse brain following chronic stress

Liu

Dietz

Hodes

et al. 2017

Developmental Neurobiology

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Emerging evidence shows that oligodendrogenesis and myelination are highly responsive to behavioral experience, including physical activity and social experience. This form of myelin plasticity is being increasingly appreciated and examined in the prefrontal cortex (PFC), a critical brain region involved in complex emotional and cognitive behavior. However, it remains unclear whether myelination in other brain regions is affected by behavioral experience. Here we report that exposure to 4 weeks of chronic variable stress induced anxiety- and depressive-like behavior in male adult mice. In concert with these behavioral responses, transcriptional analysis of PFC, and nucleus accumbens (NAc)-a brain region critical for reward response-revealed downregulation of transcripts encoding for myelin genes and oligodendrocyte-specific genes. In contrast, upregulation of myelin-related transcripts was observed in the corpus callosum (CC), whereas the amygdala (AMG) did not show significant changes. Shorter exposure to the same stressors induced behavioral changes to a less extent and was followed by a stress habituation period. However, reduced myelin and oligodendrocyte-specific gene transcripts were detected as early as one week following stress exposure in the PFC and NAc. These data indicate that oligodendrocyte and their progenitors in multiple brain regions are responsive to stressful experiences and show distinctive and region-specific patterns of gene expression. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 78: 152-162, 2018.

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Sex‐specific mechanisms for responding to stress

Bangasser

Wicks

2016

J of Neuroscience Research

159

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Posttraumatic stress disorder and major depression share stress as an etiological contributor and are more common in women than in men. Traditionally, preclinical studies investigating the neurobiological underpinnings of stress vulnerability have used only male rodents, however, recent studies that include females are finding sex-specific mechanisms for responding to stress. Here we review some of this recent literature using a framework developed by McCarthy and colleagues (2012) that highlights different types of sex differences. First, we detail how learned fear responses in rats are sexually dimorphic. Then we contrast this finding to fear extinction, which is similar in males and females at the behavioral level, but at the circuitry level is associated with sex-specific cellular changes and thus exemplifies a sex convergence. Next, sex differences in stress hormones are detailed. Finally, the effects of stress on learning, attention, and arousal are used to highlight the concept of a sex divergence, in which the behavior of males and females is similar at baseline but diverges following stressor exposure. We argue that appreciating and investigating the diversity of sex differences in stress response systems will improve our understanding of vulnerability and resilience to stress-related psychiatric disorders, and likely lead to the development of novel therapeutics to better treat these disorders in both men and women.

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Sex Differences in Nucleus Accumbens Transcriptome Profiles Associated with Susceptibility versus Resilience to Subchronic Variable Stress

Cited by 332 publications

References 82 publications

BAZ1B in Nucleus Accumbens Regulates Reward-Related Behaviors in Response to Distinct Emotional Stimuli

BAZ1B in Nucleus Accumbens Regulates Reward-Related Behaviors in Response to Distinct Emotional Stimuli

Widespread transcriptional alternations in oligodendrocytes in the adult mouse brain following chronic stress

Sex‐specific mechanisms for responding to stress

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