Acute Immobilization Stress Triggers Skin Mast Cell Degranulation via Corticotropin Releasing Hormone, Neurotensin, and Substance P: A Link to Neurogenic Skin Disorders

Singh, Leena K.; Pang, Xinzhu; Alexacos, Nicholas; Létourneau, Richard; Theoharides, Theoharis C.

doi:10.1006/brbi.1998.0541

Cited by 322 publications

(246 citation statements)

References 79 publications

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“…CRF is known to stimulate various proinflammatory responses (Leu & Singh, 1992;Singh, Pang, Alexacos, Letourneau, & Theoharides, 1999;Webster et al, 1996). Further, injection of CRF will increase passive responses of isolated guinea pig pups during a brief isolation much as was observed for LPS in Experiment 1 of the present report (Hennessy et al, 1995).…”

Section: Discussionsupporting

confidence: 61%

Anti-inflammatory agents attenuate the passive responses of guinea pig pups: Evidence for stress-induced sickness behavior during maternal separation

Hennessy

Schiml-Webb

Miller

et al. 2007

Psychoneuroendocrinology

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A previous study found that intracerebroventricular (ICV) infusion of 25 μg of α-MSH reduced the passive responses (crouched stance, eye-closing, piloerection) of guinea pig pups during a 3-hr isolation in a novel environment. Because α-MSH has broad anti-inflammatory properties, the results suggested that proinflammatory factors play a role in mediating the behavior of isolated infants. The present study further investigated this possibility. In Experiment 1, injection of lipopolysacchride (LPS) increased the number of 60-s intervals in which pups expressed the same three responses during a 1-hr test, and ICV infusion of α-MSH significantly reduced the effect of LPS on crouching and piloerection. In Experiment 2, the prostaglandin synthesis inhibitor indomethacin (10mg/kg) reduced the number of 60-s intervals in which pups exhibited both crouching and the full suite of passive responses during a 3-hr isolation in a novel environment. Together these results provide further support for the hypothesis that the passive behaviors exhibited during prolonged isolation are "stressinduced sickness behaviors" mediated by proinflammatory factors. Keywords sickness behaviors; acute phase response; inflammation; maternal separation; isolation; guinea pig Stimulation of the innate immune system results in a systemic physiological and behavioral reaction known as the acute phase response or sickness (Baumann & Gauldie, 1994). Components of the acute phase response include: fever, shifts in the synthesis of liver proteins, activation of the hypothalamic-pituitary-adrenal system, sleepiness, assumption of a curled or hunched posture, piloerection, shivering, and reductions in various activities. Though the behavioral components may appear to be simply the result of debilitation, they are adaptive responses that contribute to recuperation by, for instance, supporting the production of fever (e.g., hunched posture, piloerection, shivering), which in turn, can inhibit further proliferation of pathogens (Aubert, 1999;Hart, 1988). The acute phase response is triggered by the release of proinflammatory cytokines (e.g., IL-1, IL-6, TNF-α) in the periphery and CNS (Dantzer, 2004).Address correspondence to: Michael B. Hennessy, PhD, Department of Psychology, 335 Fawcett Hall, Wright State University, 3640 Col Glenn Hwy, Dayton, OH 45435, 937.775.2943 (voice), 937.775.3347 (FAX), michael.hennessy@wright.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. In the last decade, it has become apparent that aspects of the acute phase response, including sickness behaviors, do not occur solely ...

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Section: Discussionsupporting

confidence: 61%

Anti-inflammatory agents attenuate the passive responses of guinea pig pups: Evidence for stress-induced sickness behavior during maternal separation

Hennessy

Schiml-Webb

Miller

et al. 2007

Psychoneuroendocrinology

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“…This evidence is an extension of the idea that mast cells and nerves communicate with each other. Theoharides et al (1995Theoharides et al ( , 1998 demonstrated that intradermal administration of CRF activated mast cells in rat skin, and that acute immobilization stress could trigger mast cell degranulation in rat skin (Singh et al, 1999). They, however, did not confirm whether or not stress induced dermatitis.…”

Section: Discussionmentioning

confidence: 95%

Psychological Stress can Trigger Atopic Dermatitis in NC/Nga Mice: An Inhibitory Effect of Corticotropin-Releasing Factor

Amano

Negishi

Akiyama

et al. 2007

Neuropsychopharmacol

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Atopic dermatitis (AD) is one of the most common inflammatory diseases of the skin and is usually associated with a family history of atopic diathesis. It has been well established that many environmental or psychological factors aggravate AD. However, it is not clear whether psychological stress by itself can trigger AD. We examined the effect of psychological stress on the onset of AD, using an animal model, the NC/Nga mouse. The animals were exposed to the water avoidance stress (WAS) test to induce psychological stress. Additionally, we examined how corticotropin-releasing factor (CRF) affected the development of AD induced by psychological stress. Under specific pathogen-free (SPF) conditions, NC/Nga mice did not develop AD-like skin lesions. In contrast, NC/Nga mice exposed to psychological stress developed AD-like skin lesions along with elevated levels of serum immunoglobulin E even when kept under SPF conditions. The AD-like skin lesions induced by WAS were completely blocked by pretreating the animals with CRF. Our data indicate that a psychological factor is capable of eliciting AD-like skin lesions in NC/Nga mice. It is possible that the inhibitory effect of CRF may be mediated by the functional modification of various cells that have CRF receptors.

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“…The stress-induced increased expression of substance P (SP) in skin nerve fibers and of cutaneous nerve growth factor (NGF) consequently lead to the development of neurogenic skin inflammation, recognized by its classical features of mast cell degranulation, vasodilatation, and plasma extravasation [12,13]. Both SP and NGF are now widely acknowledged as cardinal immunomodulators and prevailing stress markers in different settings [4,[14][15][16]. NGF, an essential trophic factor for axon sprouting of peptidergic and sympathetic neurons, promotes cross-talk between neuronal cells, glia, and immune cells and facilitates monocyte/macrophage migration through vascular endothelium [17].…”

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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Acute Immobilization Stress Triggers Skin Mast Cell Degranulation via Corticotropin Releasing Hormone, Neurotensin, and Substance P: A Link to Neurogenic Skin Disorders

Cited by 322 publications

References 79 publications

Anti-inflammatory agents attenuate the passive responses of guinea pig pups: Evidence for stress-induced sickness behavior during maternal separation

Anti-inflammatory agents attenuate the passive responses of guinea pig pups: Evidence for stress-induced sickness behavior during maternal separation

Psychological Stress can Trigger Atopic Dermatitis in NC/Nga Mice: An Inhibitory Effect of Corticotropin-Releasing Factor

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

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