Prenatal Stress Enhances Susceptibility of Murine Adult Offspring toward Airway Inflammation

Pincus-Knackstedt, Maike K.; Joachim, Ricarda; Blois, Sandra M.; Douglas, Alison J.; Orsal, Arif S.; Klapp, Burghard F.; Wahn, Ulrich; Hamelmann, Eckard; Arck, Petra C.

doi:10.4049/jimmunol.177.12.8484

Cited by 126 publications

(102 citation statements)

References 38 publications

(33 reference statements)

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“…Evidence in rhesus monkeys links prenatal stress to antigen-induced responses at birth (22). Dysregulated immune response to antigen challenge has also been demonstrated in prenatally stressed adult mice, reflected by an enhanced Th2 adaptive response (23).…”

Section: What This Study Adds To the Fieldmentioning

confidence: 99%

Prenatal Maternal Stress and Cord Blood Innate and Adaptive Cytokine Responses in an Inner-City Cohort

Wright¹,

Visness²,

Calatroni³

et al. 2010

Am J Respir Crit Care Med

204

157

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Rationale: Stress-elicited disruption of immunity begins in utero. Objectives: Associations among prenatal maternal stress and cord blood mononuclear cell (CBMC) cytokine responses were prospectively examined in the Urban Environment and Childhood Asthma Study (n 5 557 families). Methods: Prenatal maternal stress included financial hardship, difficult life circumstances, community violence, and neighborhood/block and housing conditions. Factor analysis produced latent variables representing three contexts: individual stressors and ecological-level strains (housing problems and neighborhood problems), which were combined to create a composite cumulative stress indicator. CBMCs were incubated with innate (lipopolysaccharide, polyinosinic-polycytidylic acid, cytosine-phosphate-guanine dinucleotides, peptidoglycan) and adaptive (tetanus, dust mite, cockroach) stimuli, respiratory syncytial virus, phytohemagglutinin, or medium alone. Cytokines were measured using multiplex ELISAs. Using linear regression, associations among increasing cumulative stress and cytokine responses were examined, adjusting for sociodemographic factors, parity, season of birth, maternal asthma and steroid use, and potential pathway variables (prenatal smoking, birth weight for gestational age). Measurements and Main Results: Mothers were primarily minorities (Black [71%], Latino [19%]) with an income less than $15,000 (69%). Mothers with the highest cumulative stress were older and more likely to have asthma and deliver lower birth weight infants. Higher prenatal stress was related to increased IL-8 production after microbial (CpG, PIC, peptidoglycan) stimuli and increased tumor necrosis factor-a to microbial stimuli (CpG, PIC). In the adaptive panel, higher stress was associated with increased IL-13 after dust mite stimulation and reduced phytohemagglutinin-induced IFN-g. Conclusions: Prenatal stress was associated with altered innate and adaptive immune responses in CBMCs. Stress-induced perinatal immunomodulation may impact the expression of allergic disease in these children.

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Section: What This Study Adds To the Fieldmentioning

confidence: 99%

Prenatal Maternal Stress and Cord Blood Innate and Adaptive Cytokine Responses in an Inner-City Cohort

Wright¹,

Visness²,

Calatroni³

et al. 2010

Am J Respir Crit Care Med

204

157

View full text Add to dashboard Cite

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“…Sound stress, which is widely used in neuro-endocrine-immunological research [3,5,20,21], has been demonstrated to induce neurogenic skin inflammation in mice [4,22] and the premature termination of murine hair growth [2,4]. Blockade of the neurokinin-1 receptor [2], for which SP has the highest affinity, as well as neutralization of NGF abrogate stress-induced neurogenic inflammation [4].…”

Section: Introductionmentioning

confidence: 99%

Neuronal plasticity of the “brain–skin connection”: stress-triggered up-regulation of neuropeptides in dorsal root ganglia and skin via nerve growth factor-dependent pathways

et al. 2007

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Emerging research indicates that central-nervous stress perception is translated to peripheral tissues such as the skin not only via classical stress hormones but also via neurotrophins and neuropeptides. This can result in neurogenic inflammation, which is likely to contribute to the triggering and/aggravation of immunodermatoses. Although the existence of such a "brain-skin connection" is supported by steadily increasing experimental evidence, it remains unclear to which extent perceived stress affects the sensory "hardwiring" between skin and its afferent neurons in the corresponding dorsal root ganglia (DRG). In this paper, we provide experimental evidence in a murine model of stress (exposure of C57BL/6 mice to sound stress) that stress exposure, or intracutaneous injection of recombinant nerve growth factor (NGF) to mimic the skin's response to stress, up-regulate the percentage of substance P (SP) + or calcitonin gene-related peptide (CGRP) + sensory neurons in skin-innervating DRG. Further, we show that the number of SP + or CGRP + sensory nerve fibers in the dermis of stressed C57BL/6 mice is significantly increased. Finally, we document that neutralization of NGF activity abrogates

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“…Animal studies suggest effects begin prenatally. Prenatal stress increases allergen-induced airway inflammation (10,11) and airway hyperesponsiveness (12) in mice offspring and impacts the newborn's antigen response in primates (13). Although no prospective human study has measured prenatal maternal stress directly in association with wheeze or other early asthma phenotypes in children, three have considered maternal psychologic functioning as a correlate of stress exposure.…”

mentioning

confidence: 99%

Prenatal and Postnatal Maternal Stress and Wheeze in Urban Children

Chiu¹,

Coull

Cohen

et al. 2012

Am J Respir Crit Care Med

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Rationale: Critical periods for programming early wheeze risk may include pregnancy and infancy. Effects of timing remain poorly understood. Objectives: Associations among prenatal and postnatal maternal stress and children's wheeze were prospectively examined in 653 families. Effect modification by maternal sensitization was also examined. Methods: Stress was indexed by a maternal negative life events (NLEs) score (range, 0-9) ascertained during pregnancy and between 1 and 2 years postpartum. Mothers reported child wheeze every 3 months up to age 2 years. Relationships of prenatal and postnatal maternal NLEs with repeated wheeze (>2 episodes) were examined using logistic regression adjusting for covariates. Penalized splines were implemented to explore possible nonlinear associations. We also examined the interaction between prenatal stress and maternal sensitization indexed by allergen-specific IgE from maternal prenatal serum. Measurements and Main Results: Adjusted models considering prenatal or postnatal NLEs alone both showed an exposure-response relationship between higher stress and child wheeze. When considering prenatal and postnatal stress concurrently, only children of mothers with high stress in both periods were significantly more likely to wheeze (adjusted odds ratio, 3.04; 95% confidence interval, 1.67-5.53) than children of mothers reporting low stress in both periods. Associations between high prenatal stress and wheeze were significant in children born to nonsensitized mothers (any IgE ,0.35 kU/L) but not in the sensitized group (P for interaction ¼ 0.03). Conclusions: Although children have heightened sensitivity to maternal stress in utero and in early childhood, those with higher stress in both periods were particularly at risk for wheeze. The prenatal maternal immune milieu modified effects.Keywords: negative life events; stress; pregnancy; maternal sensitization; childhood wheeze Childhood wheezing illnesses account for significant morbidity and health care use (1). Recurrent wheeze may be a precedent of asthma and reduced lung function (2). An important step in identifying children at risk for costly respiratory disorders is characterizing risk factors and mechanisms that lead to and maintain early predisposition.Although the spectrum of wheeze phenotypes is complex and mechanisms of early environmental influences are incompletely understood (3, 4), aberrant proinflammatory states are central determinants (5, 6). Glucocorticoid action and sympathovagal balance are important in regulating immune function and airway response in early development (7,8). Thus, environmental factors, such as psychosocial stressors, that influence the programming of regulatory systems involved in these processes (i.e., hypothalamic-pituitary-adrenal [HPA] axis, autonomic nervous system, immune function) may be particularly relevant.Evidence links psychosocial stress to wheeze, asthma, and airway hyperesponsiveness (9). Animal studies suggest effects begin prenatally. Prenatal stress increases allergen-induced ...

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Prenatal Stress Enhances Susceptibility of Murine Adult Offspring toward Airway Inflammation

Cited by 126 publications

References 38 publications

Prenatal Maternal Stress and Cord Blood Innate and Adaptive Cytokine Responses in an Inner-City Cohort

Prenatal Maternal Stress and Cord Blood Innate and Adaptive Cytokine Responses in an Inner-City Cohort

Neuronal plasticity of the “brain–skin connection”: stress-triggered up-regulation of neuropeptides in dorsal root ganglia and skin via nerve growth factor-dependent pathways

Prenatal and Postnatal Maternal Stress and Wheeze in Urban Children

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