Abstract
Interleukin-1β (IL-1β) is a pro-inflammatory cytokine, which plays an important role in the immune response and signal transduction both in the periphery and the central nervous system (CNS). Various diseases of the CNS, including neurodegenerative disorders, vascular lesions, meningo-encephalitis or status epilepticus are accompanied by elevated levels of IL-1β. Different domains within the IL-lβ protein are responsible for distinct functions. The IL-lβ domain in position 208–240 has pyrogenic properties, while the domain in position 193–195 exerts anti-inflammatory effects. Previous studies provide little evidence about the effect of the domain in position 187–207 on the body temperature. Therefore, the aim of the present study was to investigate the action of IL-1β (187–207) and its interaction with IL-1β (193–195) on the body temperature. IL fragments were administered intracerebroventricularly and the body temperature was measured rectally in male Wistar rats. IL-1β (187–207) induced hyperthermia, while IL-1β (193–195) did not influence the core temperature considerably. In co-administration, IL-1β (193–195) completely abolished the IL-1β (187–207)-induced hyperthermia. The non-steroid anti-inflammatory drug metamizole also reversed completely the action of IL-1β (187–207). Our results provide evidence that the IL-lβ domain in position 187–207 has hyperthermic effect. This effect is mediated through prostaglandin E2 stimulation and other mechanisms may also be involved in the action of IL-1β (187–207). It also suggests that IL-lβ domain in position 187–207 and IL-1β (193–195) fragment may serve as novel target for treatment of disorders accompanied with hyperthermia.
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References
Dinarello CA (2002) The IL-1 family and inflammatory diseases. Clin Exp Rheumatol 20(5 Suppl 27):S1–13
Kamo N, Ke B, Ghaffari AA, Shen XD, Busuttil RW, Cheng G, Kupiec-Weglinski JW (2013) ASC/caspase-1/IL-1beta signaling triggers inflammatory responses by promoting HMGB1 induction in liver ischemia/reperfusion injury. Hepatology 58(1):351–362. doi:10.1002/hep.26320
Rasouli J, Lekhraj R, White NM, Flamm ES, Pilla AA, Strauch B, Casper D (2012) Attenuation of interleukin-1beta by pulsed electromagnetic fields after traumatic brain injury. Neurosci Lett 519(1):4–8. doi:10.1016/j.neulet.2012.03.089
Samad TA, Moore KA, Sapirstein A, Billet S, Allchorne A, Poole S, Bonventre JV, Woolf CJ (2001) Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410(6827):471–475. doi:10.1038/35068566
Tonosaki Y, Nishiyama K, Roubos EW, Sugiura Y (2005) Alpha-Melanophore-stimulating hormone (alpha-MSH) antagonizes interleukin-1beta-induced hyperalgesia and Fos expression in the paraventricular and arcuate nucleus of the rat. Neuroendocrinology 81(3):167–173. doi:10.1159/000086888
Chio CC, Tsai SM, Wang JJ, Lin MT (2005) 5-HT2A-mu opioid receptor mechanisms in the hypothalamus mediate interleukin-1beta fever in rats. Neurosci Lett 381(1–2):6–11. doi:10.1016/j.neulet.2005.01.074
Milton AS, Wendlandt S (1971) Effects on body temperature of prostaglandins of the A, E and F series on injection into the third ventricle of unanaesthetized cats and rabbits. J Physiol 218(2):325–336
Sung CS, Wen ZH, Chang WK, Ho ST, Tsai SK, Chang YC, Wong CS (2004) Intrathecal interleukin-1beta administration induces thermal hyperalgesia by activating inducible nitric oxide synthase expression in the rat spinal cord. Brain Res 1015(1–2):145–153. doi:10.1016/j.brainres.2004.04.068
Luger TA, Brzoska T (2007) Alpha-MSH related peptides: a new class of anti-inflammatory and immunomodulating drugs. Ann Rheum Dis 66(Suppl 3):iii52–iii55. doi:10.1136/ard.2007.079780
Brzoska T, Luger TA, Maaser C, Abels C, Bohm M (2008) Alpha-melanocyte-stimulating hormone and related tripeptides: biochemistry, antiinflammatory and protective effects in vitro and in vivo, and future perspectives for the treatment of immune-mediated inflammatory diseases. Endocr Rev 29(5):581–602. doi:10.1210/er.2007-0027
Kusuhara H, Matsuyuki H, Okumoto T (1997) Effects of nonsteroidal anti-inflammatory drugs on interleukin-1 receptor antagonist production in cultured human peripheral blood mononuclear cells. Prostaglandins 54(5):795–804
Obal F Jr, Opp M, Cady AB, Johannsen L, Postlethwaite AE, Poppleton HM, Seyer JM, Krueger JM (1990) Interleukin 1 alpha and an interleukin 1 beta fragment are somnogenic. The American journal of physiology 259(3 Pt 2):R439–R446
Boraschi D, Tagliabue A (1999) Interleukin-1 and interleukin-1 fragments as vaccine adjuvants. Methods 19(1):108–113. doi:10.1006/meth.1999.0835
Pellegrino LJ, Pellegrino AS, Cushman AJ (1979) A stereotaxic atlas of the rat brain, 2nd edn. Plenum Press, New York
Allan SM, Tyrrell PJ, Rothwell NJ (2005) Interleukin-1 and neuronal injury. Nat Rev Immunol 5(8):629–640. doi:10.1038/nri1664
Orio L, O’Shea E, Sanchez V, Pradillo JM, Escobedo I, Camarero J, Moro MA, Green AR, Colado MI (2004) 3,4-Methylenedioxymethamphetamine increases interleukin-1beta levels and activates microglia in rat brain: studies on the relationship with acute hyperthermia and 5-HT depletion. J Neurochem 89(6):1445–1453. doi:10.1111/j.1471-4159.2004.02443.x
Shao HJ, Chen L, Su YB (2005) DNA fragment encoding human IL-1beta 163-171 peptide enhances the immune responses elicited in mice by DNA vaccine against foot-and-mouth disease. Vet Res Commun 29(1):35–46
Davidson J, Milton AS, Rotondo D (1990) A study of the pyrogenic actions of interleukin-1 alpha and interleukin-1 beta: interactions with a steroidal and a non-steroidal anti-inflammatory agent. Br J Pharmacol 100(3):542–546
Wong KY, Rajora N, Boccoli G, Catania A, Lipton JM (1997) A potential mechanism of local anti-inflammatory action of alpha-melanocyte-stimulating hormone within the brain: modulation of tumor necrosis factor-alpha production by human astrocytic cells. NeuroImmunoModulation 4(1):37–41
Galimberti D, Baron P, Meda L, Prat E, Scarpini E, Delgado R, Catania A, Lipton JM, Scarlato G (1999) Alpha-MSH peptides inhibit production of nitric oxide and tumor necrosis factor-alpha by microglial cells activated with beta-amyloid and interferon gamma. Biochem Biophys Res Commun 263(1):251–256. doi:10.1006/bbrc 1999.1276
Poole S, Bristow AF, Lorenzetti BB, Das RE, Smith TW, Ferreira SH (1992) Peripheral analgesic activities of peptides related to alpha-melanocyte stimulating hormone and interleukin-1 beta 193–195. Br J Pharmacol 106(2):489–492
Brzoska T, Kalden DH, Scholzen T, Luger TA (1999) Molecular basis of the alpha-MSH/IL-1 antagonism. Ann N Y Acad Sci 885:230–238
Scholzen TE, Sunderkotter C, Kalden DH, Brzoska T, Fastrich M, Fisbeck T, Armstrong CA, Ansel JC, Luger TA (2003) Alpha-melanocyte stimulating hormone prevents lipopolysaccharide-induced vasculitis by down-regulating endothelial cell adhesion molecule expression. Endocrinology 144(1):360–370
Uehara Y, Shimizu H, Shimomura Y, Negishi M, Fukatsu A, Kashima K, Tanaka Y, Kobayashi I (1991) Central administration of Lys-D-Pro-Thr, an interleukin-1 beta 193-195 analogue, stimulates feeding in rats. Neuropeptides 19(1):9–11
Ramos HJ, Lanteri MC, Blahnik G, Negash A, Suthar MS, Brassil MM, Sodhi K, Treuting PM, Busch MP, Norris PJ, Gale M Jr (2012) IL-1beta signaling promotes CNS-intrinsic immune control of West Nile virus infection. PLoS Pathog 8(11):e1003039. doi:10.1371/journal.ppat.1003039
Caruso C, Sanchez M, Durand D, Perez Mde L, Gonzalez PV, Lasaga M, Scimonelli TN (2010) Alpha-melanocyte-stimulating hormone modulates lipopolysaccharide plus interferon-gamma-induced tumor necrosis factor-alpha expression but not tumor necrosis factor-alpha receptor expression in cultured hypothalamic neurons. J Neuroimmunol 227(1–2):52–59. doi:10.1016/j.jneuroim.2010.06.013
Legos JJ, Whitmore RG, Erhardt JA, Parsons AA, Tuma RF, Barone FC (2000) Quantitative changes in interleukin proteins following focal stroke in the rat. Neurosci Lett 282(3):189–192
Li Z, Li B, Zhu X, Yin P, Liu J, Huang S, Sun R (2013) Neuroprotective effects of anti-high-mobility group box 1 antibody in juvenile rat hippocampus after kainic acid-induced status epilepticus. NeuroReport 24(14):785–790. doi:10.1097/WNR.0b013e328363fed3
Acknowledgments
This work was supported by grants from ETT (01/2006), ETT355-08/2009, TAMOP-4.2.1, TAMOP 4.2.2-A-11/1/KONV-2012-0052 and the Neuroscience Research Group of the Hungarian Academy of Sciences.
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Palotai, M., Kiss, E., Bagosi, Z. et al. Interleukin-1β (187–207)-Induced Hyperthermia is Inhibited by Interleukin-1β (193–195) in Rats. Neurochem Res 39, 254–258 (2014). https://doi.org/10.1007/s11064-013-1215-9
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DOI: https://doi.org/10.1007/s11064-013-1215-9