Beyond an inflammatory mediator: Interleukin-1 in neurophysiology.
central nervous system
cytokine
inflammation
interleukin-1β
neurophysiology
Journal
Experimental physiology
ISSN: 1469-445X
Titre abrégé: Exp Physiol
Pays: England
ID NLM: 9002940
Informations de publication
Date de publication:
Jul 2023
Jul 2023
Historique:
received:
18
01
2023
accepted:
20
03
2023
medline:
3
7
2023
pubmed:
10
4
2023
entrez:
9
4
2023
Statut:
ppublish
Résumé
What is the topic of this review? This review focuses on the physiological role of the cytokine interleukin-1β in the CNS. What advances does it highlight? Traditionally, interleukin-1β is known as a key mediator of inflammation and immunity. This review highlights the more recent findings describing how interleukin-1β signalling is required to maintain homeostasis in the CNS. Since its discovery in the early 1940s, the interleukin-1 (IL-1) cytokine family has been associated primarily with acute and chronic inflammation. The family member IL-1β is produced by different leucocytes, endothelial cells and epithelial cells. This cytokine has been characterized as a key modulator of inflammation and innate immunity because it induces the transcription of several downstream inflammatory genes. More recently, several groups have demonstrated that IL-1β production is also required to maintain homeostasis in several organ systems. This review focuses on providing an overview of the more recently characterized role of IL-1β in the physiology of the CNS. So far, IL-1β signalling has been implicated in neuronal survival, neurite growth, synaptic pruning, synaptic transmission, neuroplasticity and neuroendocrine functions.
Substances chimiques
Cytokines
0
Inflammation Mediators
0
Interleukin-1beta
0
IL1B protein, human
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
917-924Informations de copyright
© 2023 The Authors. Experimental Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Akama, K. T., & Van Eldik, L. J. (2000). β-amyloid stimulation of inducible nitric-oxide synthase in astrocytes is interleukin-1β- and tumor necrosis factor-α (TNFα)-dependent, and involves a TNFα receptor-associated factor- and NFκB-inducing kinase-dependent signaling mechanism. Journal of Biological Chemistry, 275(11), 7918-7924.
Atkins, E. (1984). Fever: The old and the new. The Journal of Infectious Diseases, 149(3), 339-348.
Auron, P. E., Webb, A. C., Rosenwasser, L. J., Mucci, S. F., Rich, A., Wolff, S. M., & Dinarello, C. A. (1984). Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proceedings of the National Academy of Sciences, 81(24), 7907-7911.
Bal-Price, A., & Brown, G. C. (2001). Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. The Journal of Neuroscience, 21(17), 6480-6491.
Barbanel, G., Ixart, G., Szafarczyk, A., Malaval, F., & Assenmacher, I. (1990). Intrahypothalamic infusion of interleukin-1 beta increases the release of corticotropin-releasing hormone (CRH 41) and adrenocorticotropic hormone (ACTH) in free-moving rats bearing a push-pull cannula in the median eminence. Brain Research, 516(1), 31-36.
Bernton, E. W., Beach, J. E., Holaday, J. W., Smallridge, R. C., & Fein, H. G. (1987). Release of multiple hormones by a direct action of interleukin-1 on pituitary cells. Science, 238(4826), 519-521.
Boato, F., Hechler, D., Rosenberger, K., Lüdecke, D., Peters, E. M., Nitsch, R., & Hendrix, S. (2011). Interleukin-1 beta and neurotrophin-3 synergistically promote neurite growth in vitro. Journal of Neuroinflammation, 8(1), 183.
Carlson, N. G., Wieggel, W. A., Chen, J., Bacchi, A., Rogers, S. W., & Gahring, L. C. (1999). Inflammatory cytokines IL-1 alpha, IL-1 beta, IL-6, and TNF-alpha impart neuroprotection to an excitotoxin through distinct pathways. Journal of Immunology, 163(7), 3963-3968.
Colotta, F., Dower, S. K., & Mantovani, A. (1994). The type II ‘decoy’ receptor: a novel regulatory pathway for interleukin 1. Immunol Today, 15(12), 562-566.
Correale, J., & Villa, A. S. (2004). The neuroprotective role of inflammation in nervous system Injuries. Journal of Neurology, 251(11), 1304-1316.
Cvetkovic, R. S., & Keating, G. (2002). Anakinra. Biodrugs, 16(4), 303-311. discussion 313-304.
Davies, C. A., Loddick, S. A., Toulmond, S., Stroemer, R. P., Hunt, J., & Rothwell, N. J. (1999). The progression and topographic distribution of interleukin-1beta expression after permanent middle cerebral artery occlusion in the rat. Journal of Cerebral Blood Flow and Metabolism, 19(1), 87-98.
del Rey, A., Balschun, D., Wetzel, W., Randolf, A., & Besedovsky, H. O. (2013). A cytokine network involving brain-borne IL-1β, IL-1ra, IL-18, IL-6, and TNFα operates during long-term potentiation and learning. Brain, Behavior, and Immunity, 33, 15-23.
Del Rey, A., Verdenhalven, M., Lörwald, A. C., Meyer, C., Hernangómez, M., Randolf, A., Roggero, E., König, A. M., Heverhagen, J. T., Guaza, C., & Besedovsky, H. O. (2016). Brain-borne IL-1 adjusts glucoregulation and provides fuel support to astrocytes and neurons in an autocrine/paracrine manner. Molecular Psychiatry, 21(9), 1309-1320.
Dinarello, C. A., Renfer, L., & Wolff, S. M. (1977). Human leukocytic pyrogen: Purification and development of a radioimmunoassay. Proceedings of the National Academy of Sciences, 74(10), 4624-4627.
Dinarello, C. A., Simon, A., & van der Meer, J. W. (2012). Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nature Reviews Drug Discovery, 11(8), 633-652.
Dostert, C., PéTrilli, V., Van Bruggen, R., Steele, C., Mossman, B. T., & Tschopp, J. R. (2008). Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science, 320(5876), 674-677.
Elsaafien, K., Korim, W. S., Setiadi, A., May, C. N., & Yao, S. T. (2019). Chemoattraction and recruitment of activated immune cells, central autonomic control, and blood pressure regulation. Frontiers in Physiology, 10, 984.
Ferreira, R., Xapelli, S., Santos, T., Silva, A. P., Cristóvão, A., Cortes, L., & Malva, J. O. (2010). Neuropeptide Y modulation of interleukin-1β (IL-1β)-induced nitric oxide production in microglia. Journal of Biological Chemistry, 285(53), 41921-41934.
Gabay, C., Lamacchia, C., & Palmer, G. (2010). IL-1 pathways in inflammation and human diseases. Nature Reviews Rheumatology, 6(4), 232-241.
Gądek-Michalska, A., & Bugajski, J. (2010). Interleukin-1 (IL-1) in stress-induced activation of limbic-hypothalamic-pituitary adrenal axis. Pharmacol Rep, 62(6), 969-982.
Gentile, A., Fresegna, D., Musella, A., Sepman, H., Bullitta, S., De Vito, F., Fantozzi, R., Usiello, A., Maccarrone, M., Mercuri, N. B., Lutz, B., Mandolesi, G., & Centonze, D. (2016). Interaction between interleukin-1β and type-1 cannabinoid receptor is involved in anxiety-like behavior in experimental autoimmune encephalomyelitis. Journal of Neuroinflammation, 13(1), 231.
Giulian, D., Baker, T. J., Shih, L. C., & Lachman, L. B. (1986). Interleukin 1 of the central nervous system is produced by ameboid microglia. Journal of Experimental Medicine, 164(2), 594-604.
Goshen, I., Kreisel, T., Ben-Menachem-Zidon, O., Licht, T., Weidenfeld, J., Ben-Hur, T., & Yirmiya, R. (2008). Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Molecular Psychiatry, 13(7), 717-728.
Goshen, I., Kreisel, T., Ounallah-Saad, H., Renbaum, P., Zalzstein, Y., Ben-Hur, T., Levy-Lahad, E., & Yirmiya, R. (2007). A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology, 32(8-10), 1106-1115.
Halle, A., Hornung, V., Petzold, G. C., Stewart, C. R., Monks, B. G., Reinheckel, T., Fitzgerald, K. A., Latz, E., Moore, K. J., & Golenbock, D. T. (2008). The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nature Immunology, 9(8), 857-865.
Hoffman, H. M., Mueller, J. L., Broide, D. H., Wanderer, A. A., & Kolodner, R. D. (2001). Mutation of a new gene encoding a putative pyrin-like protein causes familial cold autoinflammatory syndrome and Muckle-Wells syndrome. Nature Genetics, 29(3), 301-305.
Huang, F.-P., Wang, Z.-Q., Wu, D.-C., Schielke, G. P., Sun, Y., & Yang, G.-Y. (2003). Early NFkappaB activation is inhibited during focal cerebral ischemia in interleukin-1?-converting enzyme deficient mice. Journal of Neuroscience Research, 73(5), 698-707.
Imeri, L., & Opp, M. R. (2009). How (and why) the immune system makes us sleep. Nature Reviews Neuroscience, 10(3), 199-210.
Kary, S., & Burmester, G. R. (2003). Anakinra: The first interleukin-1 inhibitor in the treatment of rheumatoid arthritis. International Journal of Clinical Practice, 57(3), 231-234.
Khani, E., Shahrabi, M., Rezaei, H., Pourkarim, F., Afsharirad, H., & Solduzian, M. (2022). Current evidence on the use of Anakinra in COVID-19. International Immunopharmacology, 111, 109075.
Kitazawa, M., Cheng, D., Tsukamoto, M. R., Koike, M. A., Wes, P. D., Vasilevko, V., Cribbs, D. H., & LaFerla, F. M. (2011). Blocking IL-1 signaling rescues cognition, attenuates tau pathology, and restores neuronal β-catenin pathway function in an Alzheimer's disease model. Journal of Immunology, 187(12), 6539-6549.
Krueger, J. M. (2008). The role of cytokines in sleep regulation. Current Pharmaceutical Design, 14(32), 3408-3416.
Krueger, J. M., Fang, J., Taishi, P., Chen, Z., Kushikata, T., & Gardi, J. (1998). Sleep. A physiologic role for IL-1 beta and TNF-alpha. Annals of the New York Academy of Sciences, 856(1), 148-159.
Liu, X., Nemeth, D. P., McKim, D. B., Zhu, L., Disabato, D. J., Berdysz, O., Gorantla, G., Oliver, B., Witcher, K. G., Wang, Y., Negray, C. E., Vegesna, R. S., Sheridan, J. F., Godbout, J. P., Robson, M. J., Blakely, R. D., Popovich, P. G., Bilbo, S. D., & Quan, N. (2019). Cell-type-specific interleukin 1 receptor 1 signaling in the brain regulates distinct neuroimmune activities. Immunity, 50(2), 317-333.e6. e316.
Liu, X., & Quan, N. (2018). Microglia and CNS Interleukin-1: Beyond Immunological Concepts. Frontiers in Neurology, 9, 8.
Lu, K. T., Wu, C. Y., Yen, H. H., Peng, J. H., Wang, C. L., & Yang, Y. L. (2007). Bumetanide administration attenuated traumatic brain injury through IL-1 overexpression. Neurological Research, 29(4), 404-409.
Maes, M., Song, C., & Yirmiya, R. (2012). Targeting IL-1 in depression. Expert Opinion on Therapeutic Targets, 16(11), 1097-1112.
Martinon, F., Mayor, A., & Tschopp, J. (2009). The inflammasomes: guardians of the body. Annual Review of Immunology, 27(1), 229-265.
McCann, S. K., Cramond, F., Macleod, M. R., & Sena, E. S. (2016). Systematic review and meta-analysis of the efficacy of interleukin-1 receptor antagonist in animal models of stroke: An update. Translational Stroke Research, 7(5), 395-406.
Meylan, E., Tschopp, J., & Karin, M. (2006). Intracellular pattern recognition receptors in the host response. Nature, 442(7098), 39-44.
Noe, F. M., Polascheck, N., Frigerio, F., Bankstahl, M., Ravizza, T., Marchini, S., Beltrame, L., Banderó, C. R., Löscher, W., & Vezzani, A. (2013). Pharmacological blockade of IL-1β/IL-1 receptor type 1 axis during epileptogenesis provides neuroprotection in two rat models of temporal lobe epilepsy. Neurobiology of Disease, 59, 183-193.
Ogilvie, A. C., Hack, C. E., Wagstaff, J., van Mierlo, G. J., Erenberg, A. J., Thomsen, L. L., Hoekman, K., & Rankin, E M. (1996). IL-1 beta does not cause neutrophil degranulation but does lead to IL-6, IL-8, and nitrite/nitrate release when used in patients with cancer. The Journal of Immunology, 156(1), 389-394.
Paré, A., Mailhot, B., Lévesque, S. A., & Lacroix, S. (2017). Involvement of the IL-1 system in experimental autoimmune encephalomyelitis and multiple sclerosis: Breaking the vicious cycle between IL-1β and GM-CSF. Brain, Behavior, and Immunity, 62, 1-8.
Park, S.-Y., Kang, M.-J., & Han, J.-S. (2018). Interleukin-1 beta promotes neuronal differentiation through the Wnt5a/RhoA/JNK pathway in cortical neural precursor cells. Molecular Brain, 11(1), 39.
Pyrillou, K., Burzynski, L. C., & Clarke, M. C. H. (2020). Alternative pathways of IL-1 activation, and its role in health and disease. Frontiers in Immunology, 11, 613170.
Qu, Y., Franchi, L., Nunez, G., & Dubyak, G. R. (2007). Nonclassical IL-1 beta secretion stimulated by P2×7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. Journal of Immunology, 179(3), 1913-1925.
Rossi, S., Sacchetti, L., Napolitano, F., De Chiara, V., Motta, C., Studer, V., Musella, A., Barbieri, F., Bari, M., Bernardi, G., Maccarrone, M., Usiello, A., & Centonze, D. (2012). Interleukin-1 causes anxiety by interacting with the endocannabinoid system. Journal of Neuroscience, 32(40), 13896-13905.
Schroder, K., & Tschopp, J. (2010). The inflammasomes. Cell, 140(6), 821-832.
Schwartz, G. J., Plata-Salamán, C. R., & Langhans, W. (1997). Subdiaphragmatic vagal deafferentation fails to block feeding-suppressive effects of LPS and IL-1 beta in rats. American Journal of Physiology, 273(3 Pt 2), R1193-1198.
Shi, J., Gao, W., & Shao, F. (2017). Pyroptosis: Gasdermin-mediated programmed necrotic cell death. Trends in Biochemical Sciences, 42(4), 245-254.
Sims, J. E., & Smith, D. E. (2010). The IL-1 family: Regulators of immunity. Nature Reviews Immunology, 10(2), 89-102.
Song, C., Zhang, Y., & Dong, Y. (2013). Acute and subacute IL-1β administrations differentially modulate neuroimmune and neurotrophic systems: Possible implications for neuroprotection and neurodegeneration. Journal of Neuroinflammation, 10(1), 59.
Stemkowski, P. L., Noh, M.-C., Chen, Y., & Smith, P. A. (2015). Increased excitability of medium-sized dorsal root ganglion neurons by prolonged interleukin-1β exposure is K+channel dependent and reversible. The Journal of Physiology, 593(16), 3739-3755.
Szczepanska-Sadowska, E. (2008). Role of neuropeptides in central control of cardiovascular responses to stress. Journal of Physiology and Pharmacology, 59(suppl 8), 61-89.
Szczepańska-Sadowska, E. (2006). Neuropeptides in neurogenic disorders of the cardiovascular control. Journal of Physiology and Pharmacology, 57(suppl 11), 31-53.
Sznejder-Pachołek, A., Joniec-Maciejak, I., Wawer, A., Ciesielska, A., & Mirowska-Guzel, D. (2017). The effect of α-synuclein on gliosis and IL-1α, TNFα, IFNγ, TGFβ expression in murine brain. Pharmacological Reports, 69(2), 242-251.
Taishi, P., Chen, Z., Obál, F. Jr, Hansen, M. K., Zhang, J., Fang, J., & Krueger, J. M. (1998). Sleep-associated changes in interleukin-1beta mRNA in the brain. Journal of Interferon & Cytokine Research, 18(9), 793-798.
Temporin, K., Tanaka, H., Kuroda, Y., Okada, K., Yachi, K., Moritomo, H., Murase, T., & Yoshikawa, H. (2008). IL-1β promotes neurite outgrowth by deactivating RhoA via p38 MAPK pathway. Biochemical and Biophysical Research Communications, 365(2), 375-380.
Thornberry, N. A., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., Miller, D. K., Molineaux, S. M., Weidner, J. R., Aunins, J., Elliston, K. O., Ayala, J. M., Casano, F. J., Chin, J., Ding, G. J. F., Egger, L. A., Gaffney, E. P., Limjuco, G., Palyha, O. C., … Tocci, M. J. (1992). A novel heterodimeric cysteine protease is required for interleukin-1βprocessing in monocytes. Nature, 356(6372), 768-774.
Uehara, A., Gottschall, P. E., Dahl, R. R., & Arimura, A. (1987). Stimulation of ACTH release by human interleukin-1β, but not by interleukin-1α, in conscious, freely-moving rats. Biochemical and Biophysical Research Communications, 146(3), 1286-1290.
Ufnal, M., Dudek, M., Zera, T., & Szczepańska-Sadowska, E. (2006). Centrally administered interleukin-1 beta sensitizes to the central pressor action of angiotensin II. Brain Research, 1100(1), 64-72.
Weber, A., Wasiliew, P., & Kracht, M. (2010). Interleukin-1beta (IL-1beta) processing pathway. Science Signaling, 3(105), cm2.
Wu, H., Wang, X., Gao, J., Liang, S., Hao, Y., Sun, C., Xia, W., Cao, Y., & Wu, L. (2017). Fingolimod (FTY720) attenuates social deficits, learning and memory impairments, neuronal loss and neuroinflammation in the rat model of autism. Life Sciences, 173, 43-54.
Yadlapati, S., & Efthimiou, P. (2016). Impact of IL-1 inhibition on fatigue associated with autoinflammatory syndromes. Modern Rheumatology, 26(1), 3-8.