Interleukin 37 expression in mice alters sleep responses to inflammatory agents and influenza virus infection

Neurobiology of Sleep and Circadian Rhythms

Volumn 3, Issue , 2017, Pages 1-9

  Davis, Christopher J ^a   Zielinski, Mark R ^a,b,c   Dunbrasky, Danielle ^a   Taishi, Ping ^a   Dinarello, Charles A ^d,e   Krueger, James M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b VA BOSTON HEALTHCARE SYSTEM   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Body weight; IL 1F7; IL 37; Influenza virus H1N1; Interleukin 1 ; Lipopolysaccharide; Sleep deprivation

Indexed keywords

EID: 85016445059     PISSN: 24519944     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbscr.2016.11.005     Document Type: Article

References (83)

1. Alt, J.A., Bohnet, S., Taishi, P., Duricka, D., Obal, F. Jr, Traynor, T., Majde, J.A., Krueger, J.M., Influenza virus-induced glucocorticoid and hypothalamic and lung cytokine mRNA responses in dwarf lit/lit mice. Brain Behav. Immun. 21 (2007), 60–67.
2. Besedovsky, L., Lange, T., Born, J., Sleep and immune function. Pflugers Arch. 463 (2012), 121–137.
3. Bettis, R., Iacuzio, D., Jung, T., Fuchs, R., Aultman, R., Gyldmark, M., Impact of influenza treatment with oseltamivir on health, sleep and daily activities of otherwise healthy adults and adolescents. Clin. Drug Investig. 26 (2006), 329–340.
4. Bufler, P., Azam, T., Gamboni-Robertson, F., Reznifov, L.L., Kumar, S., Dinarello, C.A., Kim, S.H., A complex of the IL-1 homologue IL-1F7b and IL-18-binding protein reduces IL-18 activity. Proc. Natl. Acad. Sci. USA 99 (2002), 13723–13728.
5. Bufler, P., Gamboni-Robertson, F., Azam, T., Kim, S.H., Dinarello, C.A., Interleukin-1 homologues IL-1F7b and IL-18 contain functional mRNA instability elements within the coding region responsive to lipopolysaccharide. Biochem. J. 381 (2004), 503–510.
6. Bulau, A.M., Nold, M.F., Li, S., Nold-Petry, C.A., Fink, M., Mansell, A., Schwerd, T., Hong, J., Rubartelli, A., Dinarello, C.A., Bufler, P., Role of caspase-1 in nuclear translocation of IL-37, release of the cytokine, and IL-37 inhibition of innate immune responses. Proc. Natl. Acad. Sci. USA 111:7 (2014), 2650–2655.
7. Chen, L., Duricka, D., Nelson, S., Mukherjee, S., Bohnet, S.G., Taishi, P., Majde, J.A., Krueger, J.M., Influenza virus-induced sleep responses in mice with targeted disruptions in neuronal or inducible nitric oxide synthases. J. Appl. Physiol. 97 (2004), 17–28.
8. Churchill, L., Rector, D.M., Yasuda, K., Fix, C., Rojas, M.J., Yasuda, T., Krueger, J.M., Tumor necrosis factor alpha: activity dependent expression and promotion of cortical column sleep in rats. Neuroscience 156 (2008), 71–80.
9. Coll-Miro, M., Francos-Quijorna, I., Santos-Nogueira, E., Torres-Espin, A., Bufler, P., Dinarello, C.A., Lopez-Vales, R., Beneficial effects of IL-37 after spinal cord injury in mice. Proc. Natl. Acad. Sci. USA 113:5 (2016), 1411–1416.
10. Davis, C.J., Clinton, J.M., Jewett, K.A., Zielinski, M.R., Krueger, J.M., Delta wave power: an independent sleep phenotype or epiphenomenon?. J. Clin. Sleep. Med. 7 (2011), S16–S18.
11. Davis, C.J., Dunbrasky, D., Oonk, M., Taishi, P., Opp, M.R., Krueger, J.M., The neuron-specific interleukin-1 receptor accessory protein is required for homeostatic sleep and sleep responses to influenza viral challenge in mice. Brain Behav. Immun. 47 (2015), 35–43.
12. Davis, C.J., Krueger, J.M., Sleep and Cytokines. Sleep. Med. Clin.; Biol. Sleep. 7 (2012), 517–527.
13. Dinarello, C.A., IL-1 family nomenclature. Nat. Immunol., 11, 2010, 973.
14. Dinarello, C.A., Nold-Petry, C., Nold, M., Fujita, M., Li, S., Kim, S., Bufler, P., Suppression of innate inflammation and immunity by interleukin-37. Eur. J. Immunol. 46:5 (2016), 1067–1081.
15. Dumaine, J.E., Ashley, N.T., Acute sleep fragmentation induces tissue-specific changes in cytokine gene expression and increases serum corticosterone concentration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 308 (2015), R1062–R1069.
16. Fang, J., Sanborn, C.K., Renegar, K.B., Majde, J.A., Krueger, J.M., Influenza viral infections enhance sleep in mice. Proc. Soc. Exp. Biol. Med 210 (1995), 242–252.
17. Fang, J., Wang, Y., Krueger, J.M., Effects of interleukin-1 beta on sleep are mediated by the type I receptor. Am. J. Physiol. 274 (1998), R655–R660.
18. Faraut, B., Boudjeltia, K.Z., Vanhamme, L., Kerkhofs, M., Immune, inflammatory and cardiovascular consequences of sleep restriction and recovery. Sleep. Med. Rev. 16:2 (2012), 137–149.
19. Franklin, K.B.J., Paxinos, G., The Mouse Brain in Stereotaxic Coordinates, 3rd Edn., 2007, Academic Press, San Diego.
20. Friese, R.S., Bruns, B., Sinton, C.M., Sleep deprivation after septic insult increases mortality independent of age. J. Trauma 66 (2009), 50–54.
21. Fujita, H., Inoue, Y., Seto, K., Komitsu, N., Aihara, M., Interleukin-37 is elevated in subjects with atopic dermatitis. J. Dermatol. Sci. 69 (2013), 173–175.
22. Garlanda, C., Riva, F., Bonavita, E., Mantovani, A., Negative regulatory receptors of the IL-1 family. Semin Immunol. 25 (2013), 408–415.
23. Garlanda, C., Riva, F., Bonavita, E., Gentile, S., Mantovani, A., Decoys and regulatory “receptors” of the IL-1/toll-like receptor superfamily. Front Immunol., 4, 2013, 180.
24. Grimm, D., Staeheli, P., Hufbauer, M., Koerner, I., Martínez-Sobrido, L., Solórzano, A., García-Sastre, A., Haller, O., Kochs, G., Replication fitness determines high virulence of influenza A virus in mice carrying functional Mx1 resistance gene. Proc. Natl. Acad. Sci. USA 104 (2007), 6806–6811.
25. Hallett, H., Churchill, L., Taishi, P., De, A., Krueger, J.M., Whisker stimulation increases expression of nerve growth factor- and interleukin-1beta-immunoreactivity in the rat somatosensory cortex. Brain Res. 1333 (2010), 48–56.
26. Imaeda, H., Takahashi, K., Fujimoto, T., Kasumi, E., Ban, H., Bamba, S., Sonoda, H., Shimizu, T., Fujiyama, Y., Andoh, A., Epithelial expression of interleukin-37b in inflammatory bowel disease. Clin. Exp. Immunol. 172:3 (2013), 410–416.
27. Imeri, L., Opp, M.R., How (and why) the immune system makes us sleep. Nat. Rev. Neurosci. 10 (2009), 199–210.
28. Irwin, M.R., Olmstead, R., Carroll, J.E., Sleep disturbance, sleep duration, and inflammation: a systematic review and meta-analysis of cohort studies and experimental sleep deprivation. Biol. Psychiatry. 80 (2016), 40–52.
29. Jewett, K.A., Krueger, J.M., Humoral sleep regulation; interleukin-1 and tumor necrosis factor. Vitam. Horm. 89 (2012), 241–257.
30. Jewett, K.A., Taishi, P., Sengupta, P., Roy, S., Davis, C.J., Krueger, J.M., Tumor necrosis factor enhances the sleep-like state and electrical stimulation induces a wake-like state in co-cultures of neurons and glia. Eur. J. Neurosci. 42 (2015), 2078–2090.
31. Jhaveri, K.A., Ramkumar, V., Trammell, R.A., Toth, L.A., Spontaneous, homeostatic, and inflammation-induced sleep in NF-kappaB p50 knockout mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 (2006), R1516–R1526.
32. Kapás, L., Bohnet, S.G., Traynor, T.R., Majde, J.A., Szentirmai, E., Magrath, P., Taishi, P., Krueger, J.M., Spontaneous and influenza virus-induced sleep are altered in TNF-alpha double-receptor deficient mice. J. Appl. Physiol. 105 (2008), 1187–1198.
33. Kattler, H., Dijk, D.J., Borbély, A.A., Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J. Sleep. Res 3 (1994), 159–164.
34. Krueger, J.M., Rector, D.M., Roy, S., HPA, Van Dongen, Belenky, G., Panksepp, J., Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci. 9 (2008), 910–919.
35. Krueger, J.M., The role of cytokines in sleep regulation. Curr. Pharm. Des. 14 (2008), 3408–3416.
36. Kubota, T., Fang, J., Kushikata, T., Krueger, J.M., Interleukin-13 and transforming growth factor-beta1 inhibit spontaneous sleep in rabbits. Am. J. Physiol. 279 (2000), R786–R792.
37. Kumar, S., Hanning, C.R., Brigham-Burke, M.R., Rieman, D.J., Lehr, R., Khandekar, S., Kirkpatrick, R.B., Scott, G.F., Lee, J.C., Lynch, F.J., Gao, W., Gambotto, A., Lotze, M.T., Interleukin-1F7B (IL-1H4/IL-1F7) is processed by caspase-1 and mature IL-1F7B binds to the IL-18 receptor but does not induce IFN-gamma production. Cytokine 18 (2002), 61–71.
38. Kuo, T.H., Williams, J.A., Acute sleep deprivation enhances post-infection sleep and promotes survival during bacterial infection in drosophila. Sleep 37 (2014), 859–869.
39. Kushikata, T., Fang, J., Wang, Y., Krueger, J.M., Interleukin-4 inhibits spontaneous sleep in rabbits. Am. J. Physiol., 1998, R1185–R1191.
40. Li, C., Zhao, P., Sun, X., Che, Y., Jiang, Y., Elevated levels of cerebrospinal fluid and plasma interleukin-37 in patients with Guillain-Barré syndrome. Mediat. Inflamm., 2013, 639712.
41. Li, C., Ji, H., Cai, Y., Ayana, D.A., Lv, P., Liu, M., Jiang, Y., Serum interleukin-37 concentrations and HBeAg seroconversion in chronic HBV patients during telbivudine treatment. J. Interferon Cytokine Res 33:10 (2013), 612–618.
42. Li, S., Neff, C.P., Barber, K., Hong, J., Luo, Y., Azam, T., et al. Extracellular forms of IL-37 inhibit innate inflammation in vitro and in vivo but require the IL-1 family decoy receptor IL-1R8. Proc. Natl. Acad. Sci. USA 112:8 (2015), 2497–2502.
43. Luo, Y., Cai, X., Liu, S., Wang, S., Nold-Petry, C.A., et al. Suppression of antigen-specific adaptive immunity by IL-37 via induction of tolerogenic dendritic cells. Proc. Natl. Acad. Sci. USA 111 (2014), 15178–15183.
44. Lunding, L., Webering, S., Vock, C., Schroder, A., Raedler, D., Schaub, B., et al. IL-37 requires IL-18Ralpha and SIGIRR/IL-1R8 to diminish allergic airway inflammation in mice. Allergy 70:4 (2015), 366–373.
45. Lundkvist, G.B., Kristensson, K., Bentivoglio, M., Why trypanosomes cause sleeping sickness. Physiol. (Bethesda) 19 (2004), 198–206.
46. Lupfer, C., Thomas, P.G., Anand, P.K., Vogel, P., Milasta, S., Martinez, J., Huang, G., Green, M., Kundu, M., Chi, H., Xavier, R.J., Green, D.R., Lamkanfi, M., Dinarello, C.A., Doherty, P.C., Kanneganti, T.D., Receptor interacting protein kinase 2-mediated mitophagy regulates inflammasome activation during virus infection. Nat. Immunol. 14 (2013), 480–488.
47. Majde, J.A., Krueger, J.M., Links between the innate immune system and sleep. J. Allergy Clin. Immunol. 116 (2005), 1188–1198.
48. Majde, J.A., Kapás, L., Bohnet, S.G., De, A., Krueger, J.M., Attenuation of the influenza virus sickness behavior in mice deficient in Toll-like receptor 3. Brain Behav. Immun. 24 (2010), 306–315.
49. McNamee, E.N., Masterson, J.C., Jedlicka, P., McManus, M., Grenz, A., Collins, C.B., Nold, M.F., Bufler, P., Dinarello, C.A., Rivera-Nieves, J., Interleukin 37 expression protects mice from colitis. Proc. Natl. Acad. Sci. USA 108 (2011), 16711–16716.
50. Moretti, S., Bozza, S., Oikonomou, V., Renga, G., Casagrande, A., Iannitti, R.G., et al. IL-37 inhibits inflammasome activation and disease severity in murine aspergillosis. PLoS Pathog., 10(11), 2014, e1004462.
51. Mullington, J.M., Simpson, N.S., Meier-Ewert, H.K., Haack, M., Sleep loss and inflammation. Best. Pract. Res Clin. Endocrinol. Metab. 24 (2010), 775–784.
52. Morrow, J.D., Opp, M.R., Diurnal variation of lipopolysaccharide-induced alterations in sleep and body temperature of interleukin-6-deficient mice. Brain Behav. Immun. 19 (2005), 40–51.
53. Newman, T.L., Tuzun, E., Morrison, V.A., Hayden, K.E., Ventura, M., McGrath, S.D., Rocchi, M., Eichler, E.E., A genome-wide survey of structural variation between human and chimpanzee. Genome Res. 15 (2005), 1344–1356.
54. Nold, M.F., Nold-Petry, C.A., Zepp, J.A., Palmer, B.E., Bufler, P., Dinarello, C.A., IL-37 is a fundamental inhibitor of innate immunity. Nat. Immunol. 11 (2010), 1014–1022.
55. Nold-Petry, C.A., Lo, C.Y., Rudloff, I., Elgass, K.D., Li, S., Gantier, M.P., et al. IL-37 requires the receptors IL-18Ralpha and IL-1R8 (SIGIRR) to carry out its multifaceted anti-inflammatory program upon innate signal transduction. Nat. Immunol. 16 (2015), 354–365.
56. Olivadoti, M.D., Opp, M.R., Effects of i.c.v. administration of interleukin-1 on sleep and body temperature of interleukin-6-deficient mice. Neuroscience 153 (2008), 338–348.
57. Opp, M.R., Smith, E.M., Hughes, T.K. Jr, Interleukin-10 (cytokine synthesis inhibitory factor) acts in the central nervous system of rats to reduce sleep. Neuroimmunol 60 (1995), 165–168.
58. Opp, M.R., Obál, F., Krueger, J.M., Interleukin-1 alters rat sleep: temporal and dose-related effects. Am. J. Physiol. 260 (1991), R52–R58.
59. Pan, G., Risser, P., Mao, W., Baldwin, D.T., Zhong, A.W., Filvaroff, E., Yansura, D., Lewis, L., Eigenbrot, C., Henzel, W.J., Vandlen, R., IL-1H, an interleukin 1-related protein that binds IL-18 receptor/IL-1Rrp. Cytokine 13 (2001), 1–7.
60. Pei, B., Xu, S., Liu, T., Pan, F., Xu, J., Ding, C., Associations of the IL-1F7 gene polymorphisms with rheumatoid arthritis in Chinese Han population. Int. J. Immunogenet. 40 (2013), 199–203.
61. Simpson, N., Dinges, D.F., Sleep and inflammation. Nutr. Rev. 65 (2007), S244–S252.
62. Smith, D.E., Renshaw, B.R., Ketchem, R.R., Kubin, M., Garka, K.E., Sims, J.E., Four new members expend the interleukin-1 superfamily. J. Biol. Chem. 275 (2000), 1169–1175.
63. Sharma, S., Kulk, N., Nold, M.F., Gräf, R., Kim, S.H., Reinhardt, D., Dinarello, C.A., Bufler, P., The IL-1 family member 7b translocates to the nucleus and down-regulates proinflammatory cytokines. J. Immunol. 180 (2008), 5477–5482.
64. Slimani, H., Yufeng, Z., Yousif, N., Ao, L., Fullerton, D., Dinarello, C., Meng, X., Critical role IL-37 to ameliorate endotoxemic cardiac depression in aging mice: a critical role of suppression cardiodepressant cytokines. Cardiovasc Res., 103(Suppl. 1), 2014, S92.
65. Taishi, P., Chen, Z., Obál, F. Jr, Hansen, M.K., Zhang, J., Fang, J., Krueger, J.M., Sleep-associated changes in interleukin-1beta mRNA in the brain. J. Interferon Cytokine Res 18 (1998), 793–798.
66. Taishi, P., Davis, C.J., Bayomy, O., Zielinski, M.R., Liao, F., Clinton, J.M., Smith, D.E., Krueger, J.M., Brain-specific interleukin-1 receptor accessory protein in sleep regulation. J. Appl. Physiol. 112 (2012), 1015–1022.
67. Taishi, P., Gardi, J., Chen, Z., Fang, J., Krueger, J.M., Sleep deprivation increases the expression of TNF alpha mRNA and TNF 55kD receptor mRNA in rat brain. Physiologist, 42, 1999, A4.
68. Takahashi, S., Tooley, D.D., Kapás, L., Fang, J., Seyer, J.M., Krueger, J.M., Inhibition of tumor necrosis factor in the brain suppresses rabbit sleep. Pflugers Arch. 431 (1995), 155–160.
69. Takahashi, S., Fang, J., Kapás, L., Wang, Y., Krueger, J.M., Inhibition of brain interleukin-1 attenuates sleep rebound after sleep deprivation in rabbits. Am. J. Physiol. 273 (1997), R677–R682.
70. Tang, Y., Preuss, F., Turek, F.W., Jakate, S., Keshavarzian, A., Sleep deprivation worsens inflammation and delays recovery in a mouse model of colitis. Sleep. Med. 10:6 (2009), 597–603.
71. Taylor, S.L., Renshaw, B.R., Garka, K.E., Smith, D.E., Sims, J.E., Genomic organization of the interleukin-1 locus. Genomics 79 (2002), 726–733.
72. Teng, X., Hu, Z., Wei, X., Wang, Z., Guan, T., Liu, N., Liu, X., Ye, N., Deng, G., Luo, C., Huang, N., Sun, C., Xu, M., Zhou, X., Deng, H., Edwards, C.K. 3rd, Chen, X., Wang, X., Cui, K., Wei, Y., Li, J., IL-37 ameliorates the inflammatory process in psoriasis by suppressing proinflammatory cytokine production. J. Immunol. 192:4 (2014), 1815–1823.
73. Toth, L.A., Tolley, E.A., Krueger, J.M., Sleep as a prognostic indicator during infectious disease in rabbits. Proc. Soc. Exp. Biol. Med. 203 (1993), 179–192.
74. Toth, L.A., Opp, M.R., Cytokine- and microbially induced sleep responses of interleukin-10 deficient mice. Am. J. Physiol., 2001, R1806–R1814.
75. Toth, L.A., Jhaveri, K., Sleep mechanisms in health and disease. Comp. Med. 53 (2003), 473–486.
76. Traynor, T.R., Majde, J.A., Bohnet, S.G., Krueger, J.M., Interferon type I receptor-deficient mice have altered disease symptoms in response to influenza virus. Brain Behav. Immun. 21 (2007), 311–322.
77. Vgontzas, A.N., Zoumakis, E., Bixler, E.O., Lin, H.M., Follett, H., Kales, A., Chrousos, G.P., Adverse effects of modest sleep restriction on sleepiness, performance, and inflammatory cytokines. J. Clin. Endocrinol. Metab. 89 (2004), 2119–2126.
78. Yasuda, T., Yoshida, H., Garcia-Garcia, F., Kay, D., Krueger, J.M., Interleukin-1beta has a role in cerebral cortical state-dependent electroencephalographic slow-wave activity. Sleep 28 (2005), 177–184.
79. Yoshida, H., Peterfi, Z., García-García, F., Kirkpatrick, R., Yasuda, T., Krueger, J.M., State-specific asymmetries in EEG slow wave activity induced by local application of TNFalpha. Brain Res. 1009 (2004), 129–136.
80. Zielinski, M.R., Kim, Y., Karpova, S.A., McCarley, R.W., Strecker, R.E., Gerashchenko, D., Chronic sleep restriction elevates brain interleukin-1 beta and tumor necrosis factor-alpha and attenuates brain-derived neurotrophic factor expression. Neurosci. Lett. 580 (2014), 27–31.
81. Zielinski, M.R., Krueger, J.M., 2011. Sleep and innate immunity. In: Miller, M.A., (Ed.), Encyclopedia of Bioscience, Front. Biosciences. (Schol. Ed.) 3, pp. 632–642.
82. Zielinski, M.R., Souza, G., Taishi, P., Bohnet, S.G., Krueger, J.M., Olfactory bulb and hypothalamic acute-phase responses to influenza virus: effects of immunization. Neuroimmunomodulation. 20 (2013), 323–333.
83. Zielinski, M.R., Taishi, P., Clinton, J.M., Krueger, J.M., 5′-ectonucleotidase knockout mice lack non-REM sleep responses to sleep deprivation. Eur. J. Neurosci. 35 (2012), 1789–1798.