Interleukin-1 induces substance P in sympathetic ganglia through the induction of leukemia inhibitory factor (LIF)

Shadiack, Annette M.; Hart, Ronald P.; Carlson, Christopher; Jonakait, G. Miller

doi:10.1523/jneurosci.13-06-02601.1993

Cited by 96 publications

(83 citation statements)

References 54 publications

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“…A recent study has found that IL-1␤ may regulate leukemia inhibitory factor (LIF) release from ganglion nonneuronal cells, that treatment of pure neuronal cultures with LIF induces SP expression, and that cocultures with LIF antibody prevent the SP increase caused by nonneuronal cells (31,45). These studies provide further support for LIF as a signaling molecule regulating SP expression in airway ganglia.…”

Section: Discussionmentioning

confidence: 88%

“…airway inflammation; airway smooth muscle contraction; muscarinic agonists; neurokinin receptor; airway innervation INTERLEUKIN-1 (IL-1), an inflammatory cytokine, has been reported to increase substance P (SP) release and gene expression in neurons of sensory and sympathetic ganglia (27,31,45). The IL-1␤ level in bronchoalveolar lavage fluid is increased in asthmatic patients (6,7), and IL-1␤ induces airway hyperresponsiveness (AHR) in rats (50) and isolated human bronchi (4,23).…”

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confidence: 99%

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Interleukin-1β-induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway

Satterfield

Fedan

et al. 2002

American Journal of Physiology-Lung Cellular and Molecular Phys

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Dey. Interleukin-1␤-induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway. Am J Physiol Lung Cell Mol Physiol 283: L909-L917, 2002. First published April 12, 2002 10.1152/ajplung.00363.2001.-Interleukin (IL)-1␤ causes airway inflammation, enhances airway smooth muscle responsiveness, and alters neurotransmitter expression in sensory, sympathetic, and myenteric neurons. This study examines the role of intrinsic airway neurons in airway hyperresponsiveness (AHR) induced by IL-1␤. Ferrets were instilled intratracheally with IL-1␤ (0.3 g/0.3 ml) or saline (0.3 ml) once daily for 5 days. Tracheal smooth muscle contractility in vitro and substance P (SP) expression in tracheal neurons were assessed. Tracheal smooth muscle reactivity to acetylcholine (ACh) and methacholine (MCh) and smooth muscle contractions to electric field stimulation (EFS) both increased after IL-1␤. The IL-1␤-induced AHR was maintained in tracheal segments cultured for 24 h, a procedure that depletes SP from sensory nerves while maintaining viability of intrinsic airway neurons. Pretreatment with CP-99994, an antagonist of neurokinin 1 receptor, attenuated the IL-1␤-induced hyperreactivity to ACh and MCh and to EFS in cultured tracheal segments. SP-containing neurons in longitudinal trunk, SP innervation of superficial muscular plexus neurons, and SP nerve fiber density in tracheal smooth muscle all increased after treatment with IL-1␤. These results show that IL-1␤-enhanced cholinergic airway smooth muscle contractile responses are mediated by the actions of SP released from intrinsic airway neurons. airway inflammation; airway smooth muscle contraction; muscarinic agonists; neurokinin receptor; airway innervation

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Section: Discussionmentioning

confidence: 88%

mentioning

confidence: 99%

Interleukin-1β-induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway

Satterfield

Fedan

et al. 2002

American Journal of Physiology-Lung Cellular and Molecular Phys

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“…IL-1p regulates substance P levels in sympathic ganglion cells (Hart et al, 1991) through the induction of a neuropoietic cytokine leukaemia inhibitory factor (LIF) (Shadiack et al, 1993). IL-P could alter neuropeptide expression in primary sensory neurones secondary to an increase in NGF levels since NGF has well known actions on the regulation of both substance P and CGRP in adult DRG neurones (Lindsay & Harmar, 1989;Woolf et al, 1994).…”

Section: Discussionmentioning

confidence: 99%

Contribution of interleukin‐1β to the inflammation‐induced increase in nerve growth factor levels and inflammatory hyperalgesia

Safieh‐Garabedian

Poole

Allchorne

et al. 1995

British J Pharmacology

556

324

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Peripheral inflammation is associated with the local production of neuroactive inflammatory cytokines and growth factors. These may contribute to inflammatory pain and hyperalgesia by directly or indirectly altering the function or chemical phenotype of responsive primary sensory neurones. To investigate this, inflammation was produced by the intraplantar injection of complete Freund's adjuvant (CFA) in adult rats. This resulted in a significant elevation in interleukin‐ip (IL‐1β) and nerve growth factor (NGF) levels in the inflamed tissue and of the peptides, substance P and calcitonin gene‐related peptide (CGRP) in the L4 dorsal root ganglion 48 h post CFA injection. The effects of a steroidal (dexamethasone) and a non‐steroidal (indomethacin) anti‐inflammatory drug on the levels of NGF and IL‐1β in inflamed tissue were investigated and compared with alterations in behavioural hyperalgesia and neuropeptide expression in sensory neurones. Systemic dexamethasone (120 μg kg−1 per day starting the day before the CFA injection) had no effect on the inflammatory hyperalgesia. When the dose was administered 3 times daily, a reduction in mechanical and to a lesser extent thermal sensitivity occurred. Indomethacin at 2 mg kg−1 daily (i.p.) had no effect on the hyperalgesia and a dose of 4 mg kg−1 daily was required to reduce significantly mechanical and thermal hypersensitivity. The increase in NGF produced by the CFA inflammation was prevented by both dexamethasone and indomethacin, but only at the higher dose levels. Dexamethasone at the lower and higher dose regimes diminished the upregulation of IL‐1β whereas indomethacin had an effect only at the higher dose. The increase in SP and CGRP levels produced by the CFA inflammation was prevented by dexamethasone and indomethacin at the lower and higher dose regimes. Intraplantar injections of IL‐1β (0.01, 0.1 and 1 ng) produced a brief (6 h) thermal hyperalgesia and an elevation in cutaneous NGF levels which was prevented by pretreatment with human recombinant IL‐1 receptor antagonist (IL‐1 ra) (0.625 μg, i.v.). The thermal hyperalgesia but not the NGF elevation produced by intraplantar IL‐1β (1 ng) was prevented by administration of a polyclonal neutralizing anti‐NGF serum. IL‐1 ra significantly reduced the mechanical hyperalgesia produced by CFA for 6 h after administration as well as the CFA‐induced elevation in NGF levels. Anti‐NGF pretreatment substantially reduced CFA‐induced mechanical and thermal hyperalgesia without reducing the elevation in IL‐1β. Intraplantar NGF (0.O2, 0.2 and 2 μg) injections produced a short lasting thermal and mechanical hyperalgesia but did not change IL‐1β levels in the hindpaw skin. Our results demonstrate that IL‐1β contributes to the upregulation of NGF during inflammation and that NGF has a major role in the production of inflammatory pain hypersensitivity.

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“…It is reported that SP is up-regulated in DRG neurons in CFA-inflamed rats [12], and that the concentration of SP increases in the serum of patients with long-standing rheumatoid arthritis [18]. In contrast, there has been no direct evidence that SP is upregulated in the lumbar SG of inflamed animals and transported and released from sympathetic terminals [19]. Our present observation is, to our knowledge, the first to show an increased expression of SP in SG as a result of inflammation.…”

Section: Discussion (1) Sp Was Involved In the Bf Increase Response Tmentioning

confidence: 99%

“…Our present observation is, to our knowledge, the first to show an increased expression of SP in SG as a result of inflammation. An inflammatory cytokine, IL-1, is reported to stimulate the up-regulation of SP through the induction of a leukemia inhibitory factor in SG [19]. The effect of immunocytokines on SP expression has been studied in relation to nerve injury [20], and it is possible that IL-1 is also increased in SG with peripheral inflammation.…”

Section: Discussion (1) Sp Was Involved In the Bf Increase Response Tmentioning

confidence: 99%

Substance P Is Involved in the Cutaneous Blood Flow Increase Response to Sympathetic Nerve Stimulation in Persistently Inflamed Rats

et al. 2007

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Changed vascular functions have been reported in several pathological conditions, such as chronic regional pain syndrome, obstructive vascular disease, and inflammation. Our previous experiments also showed that electrical stimulation of the lumbar sympathetic trunk (sympathetic stimulation: SS), which normally induces a decrease in blood flow (BF), caused a BF increase in about half of the measured sites in rats persistently inflamed with complete Freund's Adjuvant (AI rats). We also showed that the BF-increase response was only partially suppressed by the α1 antagonist at a higher dosage, suggesting the involvement of nonadrenergic mechanisms. We hypothesize that nonadrenergic mechanisms mediating vasodilatation might involve a vasodilating neuropeptide such as substance P (SP) that is released from sympathetic nerve terminals. In this experiment, we conducted an examination using an NK-1 receptor antagonist to determine whether SP plays any role in changed response to SS in AI rats, and also an immunohistochemical examination of whether SP is expressed in the lumbar sympathetic nerve ganglia (SG) of AI rats. The administration of an NK-1 receptor antagonist, CP-96,345, significantly reduced the BF-increase response to SS in AI rats, but its inactive enantiomer, CP-96,344, had no effect. Immunohistochemistry for SP revealed that SP-ir positive SG neurons (mean 13 neurons/rat) were found in 5 of 8 AI rats, whereas only one neuron was stained in 8 control rats. These results suggest that NK-1 receptor activation is involved in the BF-increase response to SS, and that this activation is in part mediated by SP from lumbar SG that was synthesized de novo in inflamed animals.

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Interleukin-1 induces substance P in sympathetic ganglia through the induction of leukemia inhibitory factor (LIF)

Cited by 96 publications

References 54 publications

Interleukin-1β-induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway

Interleukin-1β-induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway

Contribution of interleukin‐1β to the inflammation‐induced increase in nerve growth factor levels and inflammatory hyperalgesia

Substance P Is Involved in the Cutaneous Blood Flow Increase Response to Sympathetic Nerve Stimulation in Persistently Inflamed Rats

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