Interleukin-10 (cytokine synthesis inhibitory factor) acts in the central nervous system of rats to reduce sleep
Abstract
Interleukin-10 (IL-10), originally designated a cytokine synthesis inhibitory factor, inhibits the synthesis of the pro-inflammatory cytokines IL-1 and tumor necrosis factor by stimulated human and mouse monocytes/macrophages; these cytokines are involved in the regulation of sleep. To determine if IL-10 reduces spontaneous sleep, we injected murine recombinant IL-10 intracerebroventricularly into rats prior to light onset. Non-rapid eye movements sleep was reduced. The behavioral responses to IL-10 were abolished by heat-inactivation of this cytokine. We believe these to be the first observations of central nervous system actions for this cytokine. These results further support the hypothesis that cytokines are involved in the regulation of sleep, and suggest an additional mechanism whereby sleep may be altered in response to an activated immune system.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
IL-10 inhibits synthesis of TNF-α.
“IL‐10 inhibits synthesis of TNF‐α (212).”
From Muscle–Organ Crosstalk: The Emerging Roles of Myokines (2020) · cites this paper as [212]
Cites
IL-10 inhibits cytokine production by activated macrophages
Fiorentino, D. F., Zlotnik, A., Mosmann, T. R., Howard, M., & O’Garra, A. (1991) · The Journal of Immunology · doi:10.4049/jimmunol.147.11.3815 · Cited by 2,888 · see citing works
Fiorentino, D. F., Bond, M. W., & Mosmann, T. R. (1989) · The Journal of Experimental Medicine · doi:10.1084/jem.170.6.2081 · Cited by 2,733 · see citing works
Interleukin-1 and interleukin-1 antagonism
Dinarello, C. A. (1991) · Blood · doi:10.1182/blood.v77.8.1627.1627 · Cited by 2,303 · see citing works
Moore, K. W., O’Garra, A., Malefyt, R. D. W., Vieira, P., & Mosmann, T. R. (1993) · Annual Review of Immunology · doi:10.1146/annurev.iy.11.040193.001121 · Cited by 1,883 · see citing works
Recombinant tumor necrosis factor and interleukin 1 enhance slow-wave sleep
Shoham, S., Davenne, D., Cady, A. B., Dinarello, C. A., & Krueger, J. M. (1987) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1987.253.1.r142 · Cited by 290 · see citing works
Sleep Disorders in Patients with Chronic Fatigue
Buchwald, D., Pascualy, R. A., Bombardier, C. H., & Kith, P. (1994) · Clinical Infectious Diseases · doi:10.1093/clinids/18.supplement_1.s68 · Cited by 116 · see citing works
Sleep, sleep deprivation and infectious disease: Studies in animals
Toth, L. A. (1995) · Advances in Neuroimmunology · doi:10.1016/0960-5428(94)00045-p · Cited by 93 · see citing works
Interferon alpha-2 enhances slow-wave sleep in rabbits
Krueger, J. M., Dinarello, C. A., Shoham, S., Davenne, D., Walter, J., & Kubillus, S. L. (1987) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(87)90107-x · Cited by 93 · see citing works
Cytokine Involvement in the Regulation of Sleep
Opp, M. R., Kapás, L., & Toth, L. A. (1992) · Experimental Biology and Medicine · doi:10.3181/00379727-201-43474 · Cited by 92 · see citing works
Self-citationTumor necrosis factor-beta induces sleep, fever, and anorexia
Kapás, L., & Krueger, J. M. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.263.3.r703 · Cited by 70 · see citing works
Krueger, J. M., Toth, L. A., Floyd, R., Fang, J., Kapás, L., Bredow, S., & Obál, Jr. (2010) · Neuroimmunomodulation · doi:10.1159/000097142 · Cited by 54 · cited 1× · see citing works
“(IL-l; Krueger et al., 1983; Ob61 et al., 19901, tumor necrosis factor (Y and /3 (TNF, Shoham et al., 1987; Kapas and Krueger, 1992), and interferon LY (Krueger et al., 1987) (for reviews see Opp et al., 1992; Krueger et al., 1994).”
BackgroundEvidence for the production and action of interleukin-10 in pituitary cells
Hughes, T. K., Cadet, P., Rady, P. L., Tyring, S. K., Chin, R., & Smith, E. M. (1994) · Cellular and Molecular Neurobiology · doi:10.1007/bf02088589 · Cited by 33 · see citing works
Self-citation
Flagged first, then by citations
1 of the 13 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Muscle–Organ Crosstalk: The Emerging Roles of Myokines
Severinsen, M. C. K., & Pedersen, B. K. (2020) · Endocrine Reviews · doi:10.1210/endrev/bnaa016 · Cited by 1,226 · see citing works
“Moreover, it was shown that IL‐6‐deficient knockout mice have elevated levels of TNF‐α (214).”
InfluentialAnti-inflammatory effects of exercise: role in diabetes and cardiovascular disease
Pedersen, B. K. (2017) · European Journal of Clinical Investigation · doi:10.1111/eci.12781 · Cited by 617 · see citing works
Sick and tired: does sleep have a vital role in the immune system?
Bryant, P. A., Trinder, J., & Curtis, N. (2004) · Nature Reviews Immunology · doi:10.1038/nri1369 · Cited by 551 · see citing works
Shearer, W. T., Reuben, J. M., Mullington, J. M., Price, N. J., Lee, B.-N., Smith, E. O., Szuba, M. P., Van Dongen, H. P. A., & Dinges, D. F. (2001) · Journal of Allergy and Clinical Immunology · doi:10.1067/mai.2001.112270 · Cited by 455 · see citing works
Self-citationOpp, M. R. (2005) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2005.01.002 · Cited by 393 · see citing works
Self-citationEffects of sleep and sleep loss on immunity and cytokines
Irwin, M. R. (2002) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00003-x · Cited by 366 · see citing works
Functions and Mechanisms of Sleep
Zielinski, M. R., McKenna, J. T., & McCarley, R. W. (2016) · AIMS neuroscience · doi:10.3934/neuroscience.2016.1.67 · Cited by 347 · see citing works
Biochemical regulation of non-rapid-eye-movement sleep
Krueger, J. M. (2003) · Frontiers in Bioscience · doi:10.2741/1033 · Cited by 329 · see citing works
Inflammatory cytokine-associated depression
Lotrich, F. E. (2015) · Brain Research · doi:10.1016/j.brainres.2014.06.032 · Cited by 183 · see citing works
Sleep disorders in patients with multiple sclerosis
Brass, S. D., Duquette, P., Proulx-Therrien, J., & Auerbach, S. H. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2009.07.005 · Cited by 184 · see citing works
Central injection of IL-10 antagonizes the behavioural effects of lipopolysaccharide in rats
Bluthé, R.-M., Castanon, N., Pousset, F., Bristow, A., Ball, C., Lestage, J., Michaud, B., KELLEY, K. W., & Dantzer, R. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00077-8 · Cited by 179 · see citing works
Zielinski, M. R., Kim, Y., Karpova, S. A., McCarley, R. W., Strecker, R. E., & Gerashchenko, D. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.07.043 · Cited by 153 · see citing works
Effects of interleukin-1β on sleep are mediated by the type I receptor
Fang, J., Wang, Y., & Krueger, J. M. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.274.3.r655 · Cited by 152 · see citing works
Lorton, D., Lubahn, C. L., Estus, C., Millar, B. A., Carter, J. L., Wood, C. A., & Bellinger, D. L. (2006) · NeuroImmunoModulation · doi:10.1159/000104864 · Cited by 147 · see citing works
Molecular Mechanisms of Cancer-Induced Sleep Disruption
Walker, W. H., II, & Borniger, J. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20112780 · Cited by 146 · see citing works
Kelly, A. M., Lynch, A. M., Vereker, E., Nolan, Y. M., Queenan, P., Whittaker, E., O'Neill, L. A. J., & Lynch, M. A. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m108757200 · Cited by 140 · see citing works
Sickness behavior, its mechanisms and significance
Tizard, I. R. (2008) · Animal Health Research Reviews · doi:10.1017/s1466252308001448 · Cited by 129 · see citing works
IL-10 as a mediator in the HPA axis and brain
Smith, E. M., Cadet, P., Stefano, G. B., Opp, M. R., & Hughes, T. K. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00206-4 · Cited by 116 · see citing works
Self-citationAn antipyretic role for interleukin-10 in LPS fever in mice
Leon, L. R., Kozak, W., Rudolph, K., & Kluger, M. J. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.1.r81 · Cited by 117 · see citing works
Anti-Inflammatory Cytokines: Expression and Action in the Brain
Vitković, L., Maeda, S., & STERNBERG, E. M. (2001) · NeuroImmunoModulation · doi:10.1159/000059387 · Cited by 117 · see citing works
Humoral regulation of physiological sleep: cytokines and GHRH
Krueger, Obál, Jr., & Fang (1999) · Journal of Sleep Research · doi:10.1046/j.1365-2869.1999.00009.x · Cited by 112 · see citing works
Hadji, H., & Bouchemal, K. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.114101 · Cited by 112 · see citing works
Disordered Sleep, Nocturnal Cytokines, and Immunity in Alcoholics
Redwine, L., Dang, J., Hall, M., & Irwin, M. (2003) · Psychosomatic Medicine · doi:10.1097/01.psy.0000038943.33335.d2 · Cited by 109 · see citing works
Muscle-Organ Crosstalk: Focus on Immunometabolism
Bay, M. L., & Pedersen, B. K. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.567881 · Cited by 110 · see citing works
Evidence that vitamin D3 reverses age-related inflammatory changes in the rat hippocampus
Moore, M. E., Piazza, A., McCartney, Y., & Lynch, M. A. (2005) · Biochemical Society Transactions · doi:10.1042/bst0330573 · Cited by 102 · see citing works
Buske-Kirschbaum, A., Ebrecht, M., & Hellhammer, D. H. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.06.013 · Cited by 96 · see citing works
Opp, M. R. (1995) · Advances in Neuroimmunology · doi:10.1016/0960-5428(95)00004-l · Cited by 96 · see citing works
Self-citationChronic rhinosinusitis and sleep: a contemporary review
Alt, J. A., & Smith, T. L. (2013) · International Forum of Allergy & Rhinology · doi:10.1002/alr.21217 · Cited by 90 · see citing works
Interleukin-10: A Key Cytokine in Depression?
Roque, S., Correia-Neves, M., Mesquita, A. R., Palha, J. A., & Sousa, N. (2009) · Cardiovascular Psychiatry and Neurology · doi:10.1155/2009/187894 · Cited by 89 · see citing works
Somnogenic relationships between tumor necrosis factor and interleukin-1
Takahashi, S., Kapás, L., Fang, J., & Krueger, J. M. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.4.r1132 · Cited by 87 · see citing works
Rodent models of insomnia: A review of experimental procedures that induce sleep disturbances
Revel, F. G., Gottowik, J., Gatti, S., Wettstein, J. G., & Moreau, J. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.03.002 · Cited by 82 · see citing works
Cytokines, epilepsy and epileptic drugs--is there a mutual influence?
Młodzikowska-Albrecht, J., Steinborn, B., & Żarowski, M. (2007) · PubMed · Cited by 80 · see citing works
Cytokine- and microbially induced sleep responses of interleukin-10 deficient mice
Toth, L. A., & Opp, M. R. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.6.r1806 · Cited by 75 · see citing works
Self-citationBrambilla, D., Franciosi, S., Opp, M. R., & Imeri, L. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05796.x · Cited by 72 · see citing works
Self-citationLin, H., Barnett, M. P. G., Roy, N. C., Joyce, N. I., Zhu, S., Armstrong, K., Helsby, N. A., Ferguson, L. R., & Rowan, D. D. (2010) · Journal of Proteome Research · doi:10.1021/pr901130s · Cited by 70 · see citing works
Interleukin-18 promotes sleep in rabbits and rats
Kubota, T., Fang, J., Brown, R. A., & Krueger, J. M. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.3.r828 · Cited by 69 · see citing works
Inflammatory, cardio-metabolic and diabetic profiling of chronic schizophrenia
Balõtšev, R., Koido, K., Vasar, V., Janno, S., Kriisa, K., Mahlapuu, R., Ljubajev, Ü., Parksepp, M., Veiksaar, P., Volke, V., et al. (2016) · European Psychiatry · doi:10.1016/j.eurpsy.2016.05.010 · Cited by 65 · see citing works
Interactions of Gut Microbiota, Endotoxemia, Immune Function, and Diet in Exertional Heatstroke
Armstrong, L. E., Lee, E. C., & Armstrong, E. M. (2018) · Journal of Sports Medicine · doi:10.1155/2018/5724575 · Cited by 63 · see citing works
Choi, S., Jung, S., & Ko, K. S. (2018) · Nutrients · doi:10.3390/nu10030363 · Cited by 61 · see citing works
Interleukin-4 inhibits spontaneous sleep in rabbits
Kushikata, T., Fang, J., Wang, Y., & Krueger, J. M. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.4.r1185 · Cited by 60 · see citing works
Nava, F. A., Calapai, G., Facciolá, G., Cuzzocrea, S., Marciano, M., Sarro, A. D., & Caputi, A. P. (1997) · International Journal of Immunopharmacology · doi:10.1016/s0192-0561(97)00006-4 · Cited by 56 · see citing works
Singh, L., Kaur, A., Bhatti, M. S., & Bhatti, R. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02805-5 · Cited by 55 · see citing works
Role of IL‐10 in Inflammation: Studies Using Cytokine Knockout Micea
Leon, L. R., Kozak, W., & Kluger, M. J. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb08314.x · Cited by 55 · see citing works
Interleukin-13 and transforming growth factor-β1 inhibit spontaneous sleep in rabbits
Kubota, T., Fang, J., Kushikata, T., & Krueger, J. M. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.3.r786 · Cited by 48 · see citing works
Neuron-Derived Extracellular Vesicles Modulate Microglia Activation and Function
Peng, H., Harvey, B. T., Richards, C. I., & Nixon, K. (2021) · Biology · doi:10.3390/biology10100948 · Cited by 49 · see citing works
Growth factor-functionalized silk membranes support wound healing in vitro
Bienert, M., Hoss, M., Bartneck, M., Weinandy, S., Böbel, M., Jockenhoevel, S., Knüchel, R., Pottbacker, K., Wöltje, M., Jahnen‐Dechent, W., et al. (2017) · Biomedical Materials · doi:10.1088/1748-605x/aa7695 · Cited by 46 · see citing works
Anti-inflammatory influences on behavioral, but not cortisol, responses during maternal separation
Perkeybile, A. M., Schiml‐Webb, P. A., O’Brien, E., Terrence Deak, B., & Hennessy, M. B. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.02.014 · Cited by 43 · see citing works
Taraz, M., Khatami, M., Gharekhani, A., Abdollahi, A., Khalili, H., & Dashti‐Khavidaki, S. (2012) · European Cytokine Network · doi:10.1684/ecn.2013.0326 · Cited by 40 · see citing works
Antisomnogenic cytokines, quality of life, and chronic rhinosinusitis: A pilot study
Alt, J. A., Sautter, N. B., Mace, J. C., Detwiller, K. Y., & Smith, T. L. (2013) · The Laryngoscope · doi:10.1002/lary.24412 · Cited by 40 · see citing works
Enterococcus faecalis EF-2001 protects DNBS-induced inflammatory bowel disease in mice model
Choi, E., Lee, H. J., Kim, W.-J., Han, K.-I., Iwasa, M., Kobayashi, K., Debnath, T., Tang, Y., Kwak, Y., Yoon, J.-H., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0210854 · Cited by 36 · see citing works
Hong, Y. H., Yi, Y., Han, S. Y., Aziz, N., Kim, H. G., Park, S. H., Hossain, M. A., Baik, K. S., Choi, S. Y., Lee, J., et al. (2019) · Phytotherapy Research · doi:10.1002/ptr.6256 · Cited by 34 · see citing works
Xie, J., Guo, L., Pang, G., Wu, X., & Zhang, M. (2011) · Natural Product Research · doi:10.1080/14786419.2010.534474 · Cited by 33 · see citing works
Role of interleukin-10 (IL-10) in regulation of GABAergic transmission and acute response to ethanol
Suryanarayanan, A., Carter, J. M., Landin, J. D., Morrow, A. L., Werner, D. F., & Spigelman, I. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.03.027 · Cited by 33 · see citing works
REM sleep deprivation of rats induces acute phase response in liver
Pandey, A., & Kar, S. K. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.05.123 · Cited by 33 · see citing works
BIOLOGICAL ACTIVITY OF INTERLEUKIN-10 IN THE CENTRAL NERVOUS SYSTEM
ZOCCHIA, C., SPIGA, G., Rabin, S. J., Grekova, M. C., Richert, J. R., Chernyshev, O. N., Colton, C. A., & Mocchetti, I. (1997) · Neurochemistry International · doi:10.1016/s0197-0186(96)00079-4 · Cited by 30 · see citing works
Zhang, Y., Liang, H., Wang, Y., Cheng, R., Pu, F., Yang, Y., Li, J., Wu, S., Shen, X. P., & He, F. (2022) · BMC Neuroscience · doi:10.1186/s12868-022-00724-w · Cited by 29 · see citing works
Opp, M. R., Jan Born, A., & Irwin, M. R. (2007) · Elsevier eBooks · doi:10.1016/b978-012088576-3/50034-4 · Cited by 29 · see citing works
Self-citationEvidence for endogenous interleukin-10 during nociception
Tu, H., Juelich, T. L., Smith, E. M., Tyring, S. K., Rady, P. L., & Hughes, T. K. (2003) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(03)00126-7 · Cited by 27 · see citing works
Self-citationStefano, G. B., Prévot, V., Beauvillain, J., & Hughes, T. K. (1998) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00703-4 · Cited by 27 · see citing works
Self-citationZhao, F., Liu, W., Yu, Y., Liu, X., Yin, H., Liu, L., & Yi, G. (2019) · RSC Advances · doi:10.1039/c8ra09036j · Cited by 26 · see citing works
Taraz, M., Khatami, M., Hajiseyedjavadi, M., Farrokhian, A., Amini, M., Khalili, H., Abdollahi, A., & Dashti‐Khavidaki, S. (2013) · Hemodialysis International · doi:10.1111/hdi.12035 · Cited by 25 · see citing works
Harvey, D. R., Smith, R., English, K., Mahon, B. P., & Commins, S. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.002 · Cited by 25 · see citing works
Characterization of Early Peripheral Immune Responses in Patients with Sepsis and Septic Shock
Beltrán-García, J., Osca-Verdegal, R., Jávega, B., Herrera, G., O’Connor, J., García-López, E., Casabó-Vallés, G., Rodríguez, M. D. P., Ferreres, J., Carbonell, N., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10030525 · Cited by 24 · see citing works
Stefano, G. B., & Smith, E. M. (1996) · Medical Hypotheses · doi:10.1016/s0306-9877(96)90028-6 · Cited by 24 · see citing works
Self-citationLegaard, G. E., & Pedersen, B. K. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814593-7.00013-x · Cited by 24 · see citing works
Hormonal Activities of Cytokines
Smith, E. M. (1997) · KARGER eBooks · doi:10.1159/000058658 · Cited by 23 · see citing works
Self-citationRole of Protein Arginine Methyltransferases and Inflammation in Muscle Pathophysiology
So, H.-K., Kim, S., Kang, J., & Lee, S.-J. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.712389 · Cited by 22 · see citing works
Blood levels of cytokines in children with idiopathic partial and generalized epilepsy
Sönmez, F. M., Serin, H. M., Alver, A., Aliyazıcıoğlu, R., Cansu, A., Çan, G., & Zaman, D. (2013) · Seizure · doi:10.1016/j.seizure.2013.03.014 · Cited by 22 · see citing works
Neuroimmunology of Disordered Sleep in Depression and Alcoholism
Irwin, M. R. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00338-4 · Cited by 22 · see citing works
Stanfield, B. A., Purves, J. T., Palmer, S. M., Sullenger, B. A., Welty‐Wolf, K. E., Haines, K., Agarwal, S., & Kasotakis, G. (2021) · PLoS ONE · doi:10.1371/journal.pone.0245169 · Cited by 21 · see citing works
Cytokines and Sleep Regulation
Krueger, J. M., & Churchill, L. (2003) · Neurobiological foundation of aberrant behaviors · doi:10.1007/978-1-4615-0323-1_8 · Cited by 21 · see citing works
Park, D. R., Ko, R., Kwon, S. H., Min, B., Yun, S. H., Kim, M. H., Minatelli, J., Hill, S., & Lee, S. Y. (2016) · Journal of Medicinal Food · doi:10.1089/jmf.2016.3787 · Cited by 20 · see citing works
Davis, C. J., Zielinski, M. R., Dunbrasky, D., Taishi, P., Dinarello, C. A., & Krueger, J. M. (2016) · Neurobiology of Sleep and Circadian Rhythms · doi:10.1016/j.nbscr.2016.11.005 · Cited by 19 · see citing works
Islamoglu, H., Cao, R., Teskey, G., Gyurjian, K., Lucar, S., Fraix, M. P., Sathananthan, A., Chan, J., & Venketaraman, V. (2018) · Journal of Clinical Medicine · doi:10.3390/jcm7030040 · Cited by 19 · see citing works
Zhang, Z., Li, Y., Xie, Q. M., Li, P., Nan, X., Kong, L., Zeng, D., Ding, Z., & Wang, S. (2018) · Journal of Eukaryotic Microbiology · doi:10.1111/jeu.12639 · Cited by 19 · see citing works
Mulholland, C. V., Somogyi, A. A., Barratt, D. T., Coller, J. K., Hutchinson, M. R., Jacobson, G. M., Cursons, R. T. M., & Sleigh, J. W. (2013) · Journal of Molecular Neuroscience · doi:10.1007/s12031-013-0201-7 · Cited by 18 · see citing works
Connard, S. S., Linardi, R. L., Even, K. M., Berglund, A. K., Schnabel, L. V., & Ortved, K. F. (2021) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2021.110203 · Cited by 17 · see citing works
Tucker, J. A., Osann, K., Hsieh, S., Wahi, A., Monk, B. J., Wenzel, L. B., & Nelson, E. L. (2021) · International Journal of Behavioral Medicine · doi:10.1007/s12529-020-09950-0 · Cited by 18 · see citing works
Cytokines, neurophysiology, neuropsychology, and psychiatric symptoms.
Schwarz, M. (2003) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2003.5.2/mschwarz · Cited by 17 · see citing works
Interleukin-10 Regulated Gene Expression in Cells of Hypothalamic-Pituitary-Adrenal Axis Origin
Tu, H., Rady, P. L., Juelich, T. L., Tyring, S. K., Koldzic‐Zivanovic, N., Smith, E. M., & Hughes, T. K. (2007) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-006-9137-6 · Cited by 17 · see citing works
Self-citationChen, L., Liu, G., Wu, J., Zhou, X., Zhao, Y., Chen, Z., Lin, Z., & Xiao, Y. (2019) · Applied Materials Today · doi:10.1016/j.apmt.2019.100485 · Cited by 16 · see citing works
Tumor Derived Extracellular Vesicles Modulate Gene Expression in T cells
Pando, A., Schorl, C., Fast, L. D., & Reagan, J. L. (2022) · Gene · doi:10.1016/j.gene.2022.146920 · Cited by 15 · see citing works
Role of Distinct Fat Depots in Metabolic Regulation and Pathological Implications
Sahu, B., Tikoo, O., Pati, B., Senapati, U., & Bal, N. C. (2022) · Reviews of physiology, biochemistry and pharmacology · doi:10.1007/112_2022_73 · Cited by 15 · see citing works
Mei, S., Flemington, E. K., & Zhang, K. (2018) · BMC Genomics · doi:10.1186/s12864-018-4873-9 · Cited by 15 · see citing works
Rhind, S. G., & Shek, P. N. (1999) · Springer eBooks · doi:10.1007/978-2-8178-0857-4_7 · Cited by 15 · see citing works
Regulation of breathing pattern by IL-10
Giannakopoulou, C. E., Sotiriou, A., Dettoraki, M., Yang, M., Perlikos, F., Toumpanakis, D., Prezerakos, G. K., Koutsourelakis, I., Kastis, G. A., Vassilakopoulou, V., et al. (2019) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00065.2019 · Cited by 14 · see citing works
Potential for the effects of anabolic steroid abuse in the immune and neuroendocrine axis
Hughes, T. K., Rady, P. L., & Smith, E. M. (1998) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00233-6 · Cited by 14 · see citing works
Self-citationPEG-rIL-10 treatment decreases FoxP3+Tregs despite upregulation of intratumoral IDO
Chan, I. H., Wu, V. H., Bilardello, M., Jorgenson, B., Bal, H., McCauley, S., Vlasselaer, P. V., & Mumm, J. B. (2016) · OncoImmunology · doi:10.1080/2162402x.2016.1197458 · Cited by 14 · see citing works
Irwin, M. R., & Rinetti, G. (2004) · Alcohol · doi:10.1016/j.alcohol.2003.10.002 · Cited by 13 · see citing works
Yang, T., Wang, H., Mou, Y., Liu, W.-C., Wang, Y., Song, X.-Y., Ren, C., & Song, X. (2024) · Nature and Science of Sleep · doi:10.2147/nss.s482258 · Cited by 13 · see citing works
Aviña, A. E., Paz, D. D., Huang, S.-C., Chen, K., Chang, Y., Lee, C.-M., Lin, C.-H., Wei, F., & Wang, A. Y. L. (2023) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2023.02.016 · Cited by 12 · see citing works
Zhong, C., Zeng, X., Yi, X., Yang, Y., Hu, J., Yin, R., & Chen, X. (2025) · Current Issues in Molecular Biology · doi:10.3390/cimb47030158 · Cited by 11 · see citing works
Kurczewska, E., Ferensztajn‐Rochowiak, E., Rybakowski, F., Michalak, M., & RYBAKOWSKI, J. K. (2020) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2020.1755449 · Cited by 11 · see citing works
Hormones, Cytokines, and Sleep
Obál, F., & Krueger, J. M. (2001) · Comprehensive physiology · doi:10.1002/cphy.cp070416 · Cited by 11 · see citing works
Aryaeian, N., Hadidi, M., Mahmoudi, M., Asgari, M., Hezaveh, Z. S., & Sedehi, S. K. (2020) · Phytotherapy Research · doi:10.1002/ptr.6874 · Cited by 10 · see citing works
Lund, K. P., von Stemann, J. H., Eriksson, F., Hansen, M. B., Pedersen, B. K., Sørensen, S. S., & Brüünsgaard, H. (2019) · Transplant International · doi:10.1111/tri.13425 · Cited by 10 · see citing works
González‐Garza, M. T., Cruz‐Vega, D. E., & Maldonado‐Bernal, C. (2020) · IntechOpen eBooks · doi:10.5772/intechopen.90806 · Cited by 10 · see citing works
Müller, A. F., Strauss, L., Greter, M., Gast, H., Recher, M., Becher, B., & Fontana, A. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.02.027 · Cited by 9 · see citing works
Immune system benefits of pulmonary rehabilitation in chronic obstructive pulmonary disease
Abbasi, A., Wang, D., Stringer, W. W., Casaburi, R. H., & Rossiter, H. B. (2024) · Experimental Physiology · doi:10.1113/ep091678 · Cited by 7 · see citing works
Translational Research in Cancer
Sundaresan, S., & Gu, Y. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.73772 · Cited by 7 · see citing works
- Authors
- Opp, M. R., Smith, E. M., & Hughes, T. K.
- Affiliations
- The University of Texas Medical Branch at Galveston (US)
- Corresponding author
- Opp, M.R.
- ORCID
- Venue
- Journal of Neuroimmunology
- Publisher
- Elsevier BV
- Published
- 1995-07
- Volume
- 60
- Issue
- 1-2
- Pages
- 165-168
- ISSN
- 0165-5728 (ISSN-L)
- OpenAlex
- W2092703130
- Cited by
- 145
- References
- 13
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 2 · 2023: 2 · 2022: 9 · 2021: 11 · 2020: 9 · 2019: 11 · 2018: 8 · 2017: 3 · 2016: 7 · 2015: 1 · 2014: 2 · 2013: 5 · 2012: 3
- FWCI
- 3.63
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroimmunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01dk041034-06, 5r01da008354-03)
- National Institute on Drug Abuse (DA-08354)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK41034)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- IL-10, sleep regulation, NREM sleep, cytokines, central nervous system, intracerebroventricular administration, inflammatory cytokines, TNF-α, interleukin-1
- MeSH terms
- Animals, Brain, Injections, Intraventricular, Male, Recombinant Proteins, Sleep, Sleep Stages, Interleukin-10, Rats, Sprague-Dawley, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
