The impact of prenatal stress on insulin-like growth factor-1 and pro-inflammatory cytokine expression in the brains of adult male rats: The possible role of suppressors of cytokine signaling proteins

Szczęsny, Ewa; Basta‐Kaim, Agnieszka; Ślusarczyk, Joanna; Trojan, Ewa; Głombik, Katarzyna; Regulska, Magdalena; Leśkiewicz, Monika; Budziszewska, Bogusława; Kubera, Marta; Lasoń, W.

doi:10.1016/j.jneuroim.2014.08.001

Cited by 42 publications

(38 citation statements)

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“…In this study, the prenatal stress procedure led to a significant increase in IL-1b mRNA expression both in the FCx and Hp. Moreover, the upregulation of TNF-a gene expression in the FCx of the adult rats has been noted, which is consistent with our previous results (Szczesny et al, 2014). Importantly, Alda-1 administration significantly reduced FCx and Hp TNF-a mRNA up-regulation and tended to decrease the FCx IL-1b mRNA expression in the prenatally stressed rats.…”

Section: Discussionsupporting

confidence: 92%

The impact of mitochondrial aldehyde dehydrogenase (ALDH2) activation by Alda-1 on the behavioral and biochemical disturbances in animal model of depression

Stachowicz

Głombik

Olszanecki

et al. 2016

Brain, Behavior, and Immunity

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Section: Discussionsupporting

confidence: 92%

The impact of mitochondrial aldehyde dehydrogenase (ALDH2) activation by Alda-1 on the behavioral and biochemical disturbances in animal model of depression

Stachowicz

Głombik

Olszanecki

et al. 2016

Brain, Behavior, and Immunity

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“…The expression of IL-1β, IL-18, TNF-α and IL-6 mRNA and protein were increased in comparison to cultures obtained from control offspring. This observation is interesting in the context of our previous studies showing that enhanced pro-inflammatory activity is characterized by the up-regulation of IL-1β, TNF-α and by disturbances in SOCS proteins in the hippocampus and frontal cortex of adult prenatally stressed rats (Szczesny et al, 2014). It has been found that the regulation of inflammation involves changes in gene expression mediated by post-translational modification of histones including acetylation, methylation, phosphorylation, ubiquitination and circullination (Garden, 2013) In fact, it has been found that increased maternal care led to changes in the methylation pattern of IL-10 gene, leading to enhanced IL-10 expression in brain areas and a reduction of morphine evoked addiction behavior (Schwarz et al, 2011).…”

Section: Discussionmentioning

confidence: 57%

“…Some data showed that IGF-1 regulates the immune cell function by influencing the ratio of pro-inflammatory cytokines (Downer et al, 2009; Park et al, 2011) and that its insufficient concentration may enhance the inflammatory response. Consistent with this, prenatally stressed animals have an elevated pro-inflammatory status, which is characterized by the up-regulation of IL-1β, TNF-α and IFN-γ and an exacerbated response to an inflammatory challenge in the hippocampus and frontal cortex of male adult rats (Branchi et al, 2004; Szczesny et al, 2014). Interestingly, changes in some cytokine levels were detected in brain areas of young offspring, suggesting pro-inflammatory orientation in the young immune system (Vanbesien-Mailliot et al, 2007).…”

Section: Introductionmentioning

confidence: 79%

“…We observed in previous studies that adult prenatally stressed rats had lower levels of IGF-1 protein expression in the hippocampus and frontal cortex (Basta-Kaim et al, 2014a,b). Moreover, bidirectional communication between IGF-1 and pro-inflammatory cytokines is impaired in specific brain areas of adult offspring from prenatally stressed dams (Szczesny et al, 2014). It may be postulated that this communication is also disturbed in microglia cultures.…”

Section: Discussionmentioning

confidence: 99%

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Prenatal stress is a vulnerability factor for altered morphology and biological activity of microglia cells

Ślusarczyk

Trojan

Głombik

et al. 2015

Front. Cell. Neurosci.

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Several lines of evidence suggest that the dysregulation of the immune system is an important factor in the development of depression. Microglia are the resident macrophages of the central nervous system and a key player in innate immunity of the brain. We hypothesized that prenatal stress (an animal model of depression) as a priming factor could affect microglial cells and might lead to depressive-like disturbances in adult male rat offspring. We investigated the behavioral changes (sucrose preference test, Porsolt test), the expression of C1q and CD40 mRNA and the level of microglia (Iba1 positive) in 3-month-old control and prenatally stressed male offspring rats. In addition, we characterized the morphological and biochemical parameters of potentially harmful (NO, iNOS, IL-1β, IL-18, IL-6, TNF-α, CCL2, CXCL12, CCR2, CXCR4) and beneficial (insulin-like growth factor-1 (IGF-1), brain derived neurotrophic factor (BDNF)) phenotypes in cultures of microglia obtained from the cortices of 1–2 days old control and prenatally stressed pups. The adult prenatally stressed rats showed behavioral (anhedonic- and depression-like) disturbances, enhanced expression of microglial activation markers and an increased number of Iba1-immunopositive cells in the hippocampus and frontal cortex. The morphology of glia was altered in cultures from prenatally stressed rats, as demonstrated by immunofluorescence microscopy. Moreover, in these cultures, we observed enhanced expression of CD40 and MHC II and release of pro-inflammatory cytokines, including IL-1β, IL-18, TNF-α and IL-6. Prenatal stress significantly up-regulated levels of the chemokines CCL2, CXCL12 and altered expression of their receptors, CCR2 and CXCR4 while IGF-1 production was suppressed in cultures of microglia from prenatally stressed rats. Our results suggest that prenatal stress may lead to excessive microglia activation and contribute to the behavioral changes observed in depression in adulthood.

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“…Brain inflammatory processes are causally related to the enhanced neurodegeneration changes and reduced neurogenesis observed in the course of depression. Moreover, numerous studies have found that depression is associated with elevated levels of proinflammatory cytokines (Kubera et al 2000;Maes et al 2009;Dowlati et al 2010;Szczesny et al 2014) and with an increased rate of single nucleotide polymorphisms within proinflammatory genes (Galecki et al 2010). Microglia are considered the main source of cytokines in the brain (Hanisch 2002).…”

mentioning

confidence: 99%

Retracted: Anti‐inflammatory properties of tianeptine on lipopolysaccharide‐induced changes in microglial cells involve toll‐like receptor‐related pathways

Ślusarczyk

Trojan

Głombik

et al. 2016

Journal of Neurochemistry

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Accumulating evidence suggests that activation of microglia plays a key role in the pathogenesis of depression. Activated microglia produce a wide range of factors whose prolonged or excessive release may lead to brain disorders. Thus, the inhibition of microglial cells may be beneficial in the treatment of depressive diseases. Tianeptine is an atypical antidepressant drug with proven clinical efficacy, but its mechanism of action remains still not fully understood. In the present study, using microglial cultures we investigated whether tianeptine modifies microglial activation after lipopolysaccharide (LPS) stimulation and which intracellular pathways are involved in the activity of this antidepressant. Our study shows that tianeptine attenuated the LPS-evoked inflammatory activation of microglia by decreasing the expression of proinflammatory cytokines such as IL-1b, IL-18, IL-6 and tumor necrosis factor a (TNF-a), the release of nitric oxide (NO) and reactive oxygen species (ROS) as well as the expression of inducible nitric oxide synthase. Analyses of signaling pathways demonstrate that tianeptine led to the suppression of LPS-induced TLR4 expression and ERK1/2 phosphorylation. Furthermore, our study reveals the inhibitory impact of tianeptine on caspase-3-induced PKCd degradation and consequently on the activation of NF-jB factor in microglial cells. Taken together, present results show anti-inflammatory properties of tianeptine in microglial cultures stimulated by LPS. This study provides evidence that the inhibition of microglial activation may underlie the therapeutic activity of tianeptine. Keywords: antidepressant drugs, cytokines, inflammation, intracellular pathways, microglia, tianeptine. J. Neurochem. (2016) 136, 958-970. Increasing evidence indicates that microglia, the resident immune cells in the central nervous system (CNS), may be considered the main mediators of inflammation-associated disorders. These cells manage the innate and adaptive immune responses in various pathological processes including brain trauma, ischemia, stroke and infections, as well as during CNS repair (Graeber and Streit 2010;Yang et al. 2011). It has been observed that active microglia can clear Received September 29, 2015; revised manuscript received November 16, 2015; accepted November 17, 2015. Address correspondence and reprint requests to Agnieszka BastaKaim, Department of Experimental Neuroendocrinology, Polish Academy of Sciences, 12 Sme z tna St., 31-343 Krak ow, Poland. E-mail: basta@if-pan.krakow.plAbbreviations used: AP-1, activator protein-1; CD40, cluster of differentiation 40; DCFH, 2 0 ,7 0 -dichlorodihydrofluorescin; DCFH-DA, 2 0 ,7 0 -dichlorofluorescin diacetate; DMEM, Dulbecco's modified Eagle medium; FAM, fluorescein amidite; FBS, fetal bovine serum; HBSS, Hank's Balanced Salt Solution; HPA, hypothalamus-pituitary-adrenal; IL-18, interleukin 18; IL-1b, interleukin 1b; IL-6, interleukin 6; JNK, cJun N-terminal kinase; LDH, lactate dehydrogenase; MCP-1, monocyte chemoattractant protein-1;...

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The impact of prenatal stress on insulin-like growth factor-1 and pro-inflammatory cytokine expression in the brains of adult male rats: The possible role of suppressors of cytokine signaling proteins

Cited by 42 publications

References 59 publications

The impact of mitochondrial aldehyde dehydrogenase (ALDH2) activation by Alda-1 on the behavioral and biochemical disturbances in animal model of depression

The impact of mitochondrial aldehyde dehydrogenase (ALDH2) activation by Alda-1 on the behavioral and biochemical disturbances in animal model of depression

Prenatal stress is a vulnerability factor for altered morphology and biological activity of microglia cells

Retracted: Anti‐inflammatory properties of tianeptine on lipopolysaccharide‐induced changes in microglial cells involve toll‐like receptor‐related pathways

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