Interleukin-1 induces analgesia in mice by a central action

Nakamura, Hideo; Nakanishi, Kiyomi; Kita, Atsuko; Kadokawa, Toshiaki

doi:10.1016/0014-2999(88)90040-4

Cited by 95 publications

(19 citation statements)

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“…Rostra1 raphe stimulation has also been found to influence the secretion of hypothalamic growth hormone (Koibuchi et al, 1988) and pituitary luteinizing hormone (Morello and Taleisnik, 1985). Fifth, stimulation of the raphe, which sends dense serotonergic projections to the trigeminal nuclei and to the spinal cord (see Tork, 1985) elicits profound behavioral analgesia (Fields and Basbaum, 1978;Zieglgansberger, 1986) of the type reported to follow central IL-l administration (Nakamura et al, 1988). And sixth, the raphe densely innervates the dorsal vagal complex (see Tork, 1985) thus providing an indirect route for IL-l-mediated inhibition of gastric acid and pepsin secretion.…”

Section: Discussionmentioning

confidence: 99%

“…In addition, centrally administered IL-l has been found to elevate circulating levels of growth hormone and prolactin, while inhibiting the release of thyroid-stimulating hormone (Rettori et al, 1987;Dubuis et al, 1988). More recently, intracerebroventricular IL-l has also been observed to inhibit both gastric acid (Ishikawa et al, 1990;Saperas et al, 1990;Uehara et al, 1990;Okumura et al, 199 1;Shibasaki et al, 199 1) and pepsin (Okumura et al, , 1991 secretion, and to have profound analgesic properties (Nakamura et al, 1988).…”

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confidence: 99%

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In situ histochemical localization of type I interleukin-1 receptor messenger RNA in the central nervous system, pituitary, and adrenal gland of the mouse

et al. 1992

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The cytokine interleukin-1 (IL-l) has a number of biologic activities, including pronounced effects on the nervous and neuroendocrine systems. In this study, in situ histochemical techniques were used to investigate the distribution of cells expressing type I IL-1 receptor mRNA in the CNS, pituitary, and adrenal gland of the mouse. Hybridization of %-labeled antisense cRNA probes derived from a murine T-cell IL-1 receptor cDNA revealed a distinct regional distribution of the type I IL-1 receptor, both in brain and in the pituitary gland. In the brain, an intense signal was observed over the granule cell layer of the dentate gyrus, over the entire midline raphe system, over the choroid plexus, and over endothelial cells of postcapillary venules throughout the neuraxis. A weak to moderate signal was observed over the pyramidal ceil layer of the hilus and CA3 region of the hippocampus, over the anterodorsal thalamic nucleus, over Purkinje cells of the cerebellar cortex, and in scattered clusters over the externalmost layer of the median eminence.In the pituitary gland, a dense and homogeneously distributed signal was observed over the entire anterior lobe. No autoradiographic signal above background was observed over the posterior and intermediate lobes of the pituitary, or over the adrenal gland. This study therefore provides evidence for discrete receptor substrates subserving the central effects of IL-l, thus supporting the notion that IL-1 acts as a neurotransmitter/neuromodulator in brain. It also supports studies suggesting that IL-1 -mediated activation of the hypothalamic-pituitary-adrenal axis occurs primarily at the level of the brain and/or pituitary gland.Interleukin-1 (IL-l) is one of a growing number of cytokines that mediate important regulatory interactions between lymphocytes and many other cell types (see Dinarello, 1989). IL-l has also been identified as a key mediator in the acute-phase

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

In situ histochemical localization of type I interleukin-1 receptor messenger RNA in the central nervous system, pituitary, and adrenal gland of the mouse

et al. 1992

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“…IL-1 p administration has a variety of biological effects such as fever [1], production of acute-phase proteins [2], decreased food intake [3] and analgesia [4], IL-lp also triggers the hypothalamo-pituitary-adrenal (HPA) axis and acutely stimulates plasma ACTH and corticosterone (CORT) levels [5,6], In vivo, rise in ACTH concentra tions follows an acute IL-ip treatment and parallels an early and sustained increase (<30 min) in the rate of POMC gene transcription and a delayed (4 h) increase in levels of POMC mRNA in the cytoplasm [7,8]. The brain is probably the primary site of action for the acute ACTH response induced by IL-ip, because both pituitary and adrenal stimulation require a prolonged in vitro exposure to IL-ip (4-12 h) [9,10].…”

Section: Introductionmentioning

confidence: 99%

Effects of Continuous Infusion of Interleukin 1β on Corticotropin-Releasing Hormone (CRH), CRH Receptors, Proopiomelanocortin Gene Expression and Secretion of Corticotropin, β-Endorphin and Corticosterone

et al. 1997

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A number of recent studies suggest that interleukin 1β (IL-1β) is a major mediator of hypothalamo-pituitary-adrenal (HPA) responses following infectious aggression. We investigated whether IL-1β mediates long-term changes in HP A activity and studied the cellular regulation of the anterior pituitary. To mimic chronically elevated IL-1β production thought to occur during infectious diseases, osmotic pumps (Alzet type) were implanted in the peritoneal cavity of male rats and hIL-1β was infused continuously at rates of 1 or 3 µg/day. Effects of hIL-1β action on plasma ACTH, β-endorphin (β-EP) and corticosterone (CORT) secretion and on anterior pituitary (AP), ACTH and β-EP content were followed. In addition, hypothalamic (HT) CRH mRNA and in AP, CRH receptor (CRH-Rc) mRNA, POMC nuclear primary transcript RNA, POMC nuclear intermediate processing RNA and POMC nuclear and cytoplasmic mRNA were quantified using a highly sensitive solution hybridization nuclease protection assay. Continuous infusion of hIL-1 β stimulated the HPA axis at varying degrees. Increased HT CRH gene expression, AP POMC gene transcription, ACTH and β-EP release occurred only during the first 3 days of the treatment. A long-lasting enhancement of ACTH and β-EP synthesis and of POMC gene expression resulted from activated POMC gene transcription followed by an increased POMC mRNA stability and decreased POMC mRNA turnover. In the AP, stimulation of ACTH and β-EP secretion and POMC gene transcription disappeared after continuous IL-1β treatment, possibly in part due to a refractory process mediated by decreased CRH-Rc gene expression in corticotropes.

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“…Since peripherally administered IL-1 can produce analgesia (Nakamura, Nakanishi, Kita & Kadokawa, 1988), at least part of this analgesia could be mediated directly at the spinal cord rather than only at the brain. The delivery of cytokines to the CNS for therapeutic reasons may need to include consideration of the spinal cord (Butter, Baker, O'Neill & Turk, 1991), especially for immune diseases that affect the spinal cord first or affect it to a greater extent than the brain.…”

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Blood‐borne interleukin‐1 alpha is transported across the endothelial blood‐spinal cord barrier of mice.

Banks

Kastin

Ehrensing

1994

The Journal of Physiology

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1. Previous work has shown that one mechanism by which blood-borne interleukin-lcz (IL-1) may be able to affect the central nervous system (CNS) is by direct transport into the brain across the blood-brain barrier (BBB). The BBB of the brain consists of endothelial (between blood and interstitial fluid) and ependymal (between blood and cerebrospinal fluid) barriers. Which of these barriers IL-1 can cross has not previously been investigated. At the spinal cord, which could be the site of action for some of the effects of IL-1 such as analgesia, the BBB consists only of the endothelial barrier. 2. We show here that IL-1 labelled with 125I (I-IL) is transported across the BBB of the spinal cord by a saturable system similar to the one previously described for the brain. High performance liquid chromatography (HPLC) showed that most of the material entering the spinal cord represented intact I-IL. The BBB of the spinal cord was no more leaky to radioactively labelled albumin than the BBB of the brain and was not disrupted by 50 ug kg1 of IL-1. 3. Capillary depletion showed that most of the I-IL entered the parenchymal-interstitial fluid space of the spinal cord with only a modest amount being sequestered by the endothelial cells of its BBB. 4. I-IL entered the cervical, thoracic and lumbar regions of the spinal cord equally well.I-IL entering at the brain and diffusing caudally was estimated only to account for about 1% of the total radioactivity found in the spinal cord after i.v. injection. These results show that I-IL is able to cross the endothelial part of the BBB and that bloodborne IL-1 has direct access to the spinal cord.Interleukin-loc (IL-1) and other cytokines play major roles in the co-ordination of the neuroimmune axis (PlataSalaman, 1991). Several possible mechanisms (Breder,

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Interleukin-1 induces analgesia in mice by a central action

Cited by 95 publications

References 16 publications

In situ histochemical localization of type I interleukin-1 receptor messenger RNA in the central nervous system, pituitary, and adrenal gland of the mouse

In situ histochemical localization of type I interleukin-1 receptor messenger RNA in the central nervous system, pituitary, and adrenal gland of the mouse

Effects of Continuous Infusion of Interleukin 1β on Corticotropin-Releasing Hormone (CRH), CRH Receptors, Proopiomelanocortin Gene Expression and Secretion of Corticotropin, β-Endorphin and Corticosterone

Blood‐borne interleukin‐1 alpha is transported across the endothelial blood‐spinal cord barrier of mice.

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