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Human interleukin (IL) 1 alpha, murine IL-1 alpha and murine IL-1 beta are transported from blood to brain in the mouse by a shared saturable mechanism.
Abstract
Interleukins (ILs) 1 alpha and 1 beta are important components of the neuroimmune axis. Recent work has shown that human 125I-IL-1 alpha can enter the brain from the blood by a saturable system, suggesting a mechanism that may directly link the immune and nervous systems. Here, it is shown that radioiodinated murine IL-1 beta and especially murine IL-1 alpha are even more rapidly transported into the brain of the mouse than is radioiodinated human IL-1 alpha after i.v. injection. All three cytokines exhibited self-inhibition, thus demonstrating saturable transport. Also, they all cross-inhibited the transport of each other. This shows that there are not three separate transport systems, but that they either share transport systems with overlapping affinities or share a single system. It was calculated that 0.06% to 0.08% of the dose of human 125I-IL-1 alpha injected i.v. was present in the brain during the first 60 min. By contrast, no saturable component could be detected in the brain to blood passage of the three ILs. No disruption of the blood-brain barrier to radioactively labeled albumin was found with i.v. doses of up to 50 micrograms/kg of human IL-1 alpha. Additional studies on the blood to brain transport of human 125I-IL-1 alpha showed no modification by dexamethasone, morphine, indomethacin or alpha-melanocyte stimulating hormone. Studies with antibodies directed toward the binding or nonbinding sites of IL or its receptor on the murine T lymphocyte suggest similar, but not identical, structural requirements for transport and for receptor binding.(ABSTRACT TRUNCATED AT 250 WORDS)
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“the active transport of cytokines (Banks et al, 1991;Gutierrez et al, 1993;Plotkin et al, 1996), notably IL1, IL6, and TNF, is likely an important contributor to changes in sleep that occur during prolonged disease or infection.”
From Sleep health: Reciprocal regulation of sleep and innate immunity (2017) · cites this paper as Banks et al, 1991
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Banks, W. A., Kastin, A. J., & Ehrensing, C. A. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020293 · Cited by 63
Self-citationJakhmola, S., & Jha, H. C. (2021) · Virology · doi:10.1016/j.virol.2021.04.005 · Cited by 61
Hormones, Lymphohemopoietic Cytokines and the Neuroimmune Axis
Johnson, R. W., Arkins, S., Dantzer, R., & Kelley, K. W. (1997) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/s0300-9629(96)00277-0 · Cited by 61
The interleukins-1α, -1β, and -2 do not acutely disrupt the murine blood - brain barrier
Banks, W. A., & Kastin, A. J. (1992) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(92)90124-4 · Cited by 61
Self-citationCampbell, S. J., Deacon, R. M. J., Jiang, Y., Ferrari, C. C., Pitossi, F. J., & Anthony, D. C. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.04.013 · Cited by 60
“Following a single bolus injection of IL-1β, others have shown that some escapes from the CSF into the peripheral circulation (Banks et al., 1991; De Simoni et al., 1993), but the production of IL-1β by the virus is likely be at a level that can be cleared by endogenous mechanisms.”
Central mediators involved in the febrile response: effects of antipyretic drugs
Zampronio, A. R., Soares, D. D. M., & de Souza, G. E. P. (2015) · Temperature · doi:10.1080/23328940.2015.1102802 · Cited by 60
Campisi, J., Hansen, M. K., O’Connor, K., Biedenkapp, J. C., Watkins, L. R., Maier, S. F., & Fleshner, M. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00371.2003 · Cited by 59
Subdiaphragmatic vagotomy does not block intraperitoneal lipopolysaccharide-induced fever
Hansen, M. K., Daniels, S., Goehler, L. E., Gaykema, R. P. A., Maier, S. F., & Watkins, L. R. (2000) · Autonomic Neuroscience · doi:10.1016/s1566-0702(00)00224-1 · Cited by 61
Interleukin‐1β Depolarizes Paraventricular Nucleus Parvocellular Neurones
Ferri, C. C., & Ferguson, A. V. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.00870.x · Cited by 60
Cognitive impairment after long COVID-19: current evidence and perspectives
Li, Z., Zhang, Z., Zhang, Z., Wang, Z., & Li, H. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1239182 · Cited by 70
Essential role of interleukin-15 receptor in normal anxiety behavior
Wu, X., He, Y., Hsuchou, H., Kastin, A. J., Rood, J. C., & Pan, W. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.06.012 · Cited by 58
“Preliminary results also showed that IL1β did not show a significant change, although bloodborne IL1β crosses the blood-brain barrier by a saturable transport system (Banks et al., 1991).”
BackgroundSelf-citationCytokines: How important are they in mediating sickness?
Poon, D. C.-H., Ho, J. Y. S., Chiu, K., & Chang, R. C. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.11.001 · Cited by 59
“Furthermore, increasing lines of evidence indicate that ertain cytokines such as IL-1 (Banks et al., 2001, 1991), IL-1Ra Gutierrez et al., 1994), TNF (Osburg et al., 2002), and IL-6 (Banks t al., 1994) can be selectively transported across the BBB in a bloodo-brain direction, mostly via saturable…”
Threlkeld, S. W., Lynch, J. L., Lynch, K. M., Sadowska, G. B., Banks, W. A., & Stonestreet, B. S. (2010) · NeuroImmunoModulation · doi:10.1159/000288265 · Cited by 56
Self-citationAuernhammer, C. J., Chesnokova, V., & Melmed, S. K. (1998) · Endocrinology · doi:10.1210/endo.139.5.6017 · Cited by 57
“administered IL-1b to be transported to the hypothalamus by a saturable transport mechanism (52).”
BackgroundReyes, T. M., & Coe, C. L. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00687-2 · Cited by 53
Leptin regulates interleukin-1β expression in the brain via the STAT3-independent mechanisms
Hosoi, T., Okuma, Y., & Nomura, Y. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02974-8 · Cited by 56
Chen, G., Castro, W. L., Chow, H.-H., & Reichlin, S. (1997) · Endocrinology · doi:10.1210/endo.138.11.5533 · Cited by 55
Metadata
- Authors
- Banks, W. A., Ortiz, L., Plotkin, S. R., & Kastin, A. J.
- Affiliations
- Veterans Health Administration (US)
- Venue
- The Journal of Pharmacology and Experimental Therapeutics
- Publisher
- Elsevier BV
- Published
- 1991-12
- Volume
- 259
- Issue
- 3
- Pages
- 988-996
- ISSN
- 0022-3565 (ISSN-L)
- OpenAlex
- W1892932767
- Cited by
- 474
- References
- 0
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 8 · 2023: 12 · 2022: 6 · 2021: 10 · 2020: 13 · 2019: 5 · 2018: 12 · 2017: 8 · 2016: 11 · 2015: 17 · 2014: 15 · 2013: 10 · 2012: 11
- FWCI
- 9.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Pharmacology and Experimental Therapeutics (publishedVersion)
- PubMed (publishedVersion)
- PubMed
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- interleukin-1 alpha, IL-1β, blood-brain barrier, cytokine transport, saturable transport, neuroimmune axis, blood-brain barrier integrity, interleukin-1 receptor, T cells
- MeSH terms
- Animals, Antibodies, Biological Transport, Blood-Brain Barrier, Brain, Humans, Injections, Intravenous, Injections, Intraventricular, Interleukin-1, Iodine Radioisotopes, Recombinant Proteins, Mice
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