Table of Contents Author Guidelines Submit a Manuscript
Corrigendum

A corrigendum for this article has been published. To view the corrigendum, please click here.

Mediators of Inflammation
Volume 2013 (2013), Article ID 436263, 7 pages
http://dx.doi.org/10.1155/2013/436263
Research Article

Hypothermia Reduces Toll-Like Receptor 3-Activated Microglial Interferon-β and Nitric Oxide Production

1Department of Laboratory Sciences, Yamaguchi University Graduate School of Medicine, 1-1-1 Minami-kogushi, Ube, Yamaguchi 755-8505, Japan
2ACEL, Inc., SIC1 1201, 5-4-21 Nishihashimoto, Midori-ku, Sagamihara, Kanagawa 252-0131, Japan

Received 8 January 2013; Revised 18 February 2013; Accepted 18 February 2013

Academic Editor: Fulvio D'Acquisto

Copyright © 2013 Tomohiro Matsui et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Akira, S. Uematsu, and O. Takeuchi, “Pathogen recognition and innate immunity,” Cell, vol. 124, no. 4, pp. 783–801, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. M. F. Tsan and B. Gao, “Endogenous ligands of toll-like receptors,” Journal of Leukocyte Biology, vol. 76, no. 3, pp. 514–519, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. G. B. Johnson, G. J. Brunn, and J. L. Platt, “Activation of mammalian toll-like receptors by endogenous agonists,” Critical Reviews in Immunology, vol. 23, no. 1-2, pp. 15–44, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Lehnardt, E. Schott, T. Trimbuch et al., “A vicious cycle involving release of heat shock protein 60 from injured cells and activation of toll-like receptor 4 mediates neurodegeneration in the CNS,” The Journal of Neuroscience, vol. 28, no. 10, pp. 2320–2331, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. T. F. Pais, C. Figueiredo, R. Peixoto, M. H. Braz, and S. Chatterjee, “Necrotic neurons enhance microglial neurotoxicity through induction of glutaminase by a MyD88-dependent pathway,” Journal of Neuroinflammation, vol. 5, article 43, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. L. Minghetti and G. Levi, “Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide,” Progress in Neurobiology, vol. 54, no. 1, pp. 99–125, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. R. B. Rock, G. Gekker, S. Hu et al., “Role of microglia in central nervous system infections,” Clinical Microbiology Reviews, vol. 17, no. 4, pp. 942–964, 2004. View at Publisher · View at Google Scholar
  8. S. Lehnardt, S. Lehmann, D. Kaul et al., “Toll-like receptor 2 mediates CNS injury in focal cerebral ischemia,” Journal of Neuroimmunology, vol. 190, no. 1-2, pp. 28–33, 2007. View at Publisher · View at Google Scholar
  9. G. Ziegler, D. Harhausen, C. Schepers et al., “TLR2 has a detrimental role in mouse transient focal cerebral ischemia,” Biochemical and Biophysical Research Communications, vol. 359, no. 3, pp. 574–579, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. O. Hoffmann, J. S. Braun, D. Becker et al., “TLR2 mediates neuroinflammation and neuronal damage,” The Journal of Immunology, vol. 178, no. 10, pp. 6476–6481, 2007. View at Google Scholar
  11. A. A. Babcock, M. Wirenfeldt, T. Holm et al., “Toll-like receptor 2 signaling in response to brain injury: an innate bridge to neuroinflammation,” The Journal of Neuroscience, vol. 26, no. 49, pp. 12826–12837, 2006. View at Google Scholar
  12. S. M. Allan and N. J. Rothwell, “Cytokines and acute neurodegeneration,” Nature Reviews Neuroscience, vol. 2, no. 10, pp. 734–744, 2001. View at Publisher · View at Google Scholar
  13. S. M. Allan, P. J. Tyrrell, and N. J. Rothwell, “Interleukin-1 and neuronal injury,” Nature Reviews Immunology, vol. 5, no. 8, pp. 629–640, 2005. View at Publisher · View at Google Scholar
  14. D. W. Marion, L. E. Penrod, S. F. Kelsey et al., “Treatment of traumatic brain injury with moderate hypothermia,” The New England Journal of Medicine, vol. 336, no. 8, pp. 540–546, 1997. View at Publisher · View at Google Scholar · View at Scopus
  15. S. A. Bernard, T. W. Gray, M. D. Buist et al., “Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia,” The New England Journal of Medicine, vol. 346, no. 8, pp. 557–563, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. Q. S. Si, Y. Nakamura, and K. Kataoka, “Hypothermic suppression of microglial activation in culture: inhibition of cell proliferation and production of nitric oxide and superoxide,” Neuroscience, vol. 81, no. 1, pp. 223–229, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Maekawa, M. Aibiki, Q. S. Si, Y. Nakamura, Y. Shirakawa, and K. Kataoka, “Differential effects of lowering culture temperature on mediator release from lipopolysaccharide-stimulated neonatal rat microglia,” Critical Care Medicine, vol. 30, no. 12, pp. 2700–2704, 2002. View at Google Scholar · View at Scopus
  18. H. Gibbons, T. A. Sato, and M. Dragunow, “Hypothermia suppresses inducible nitric oxide synthase and stimulates cyclooxygenase-2 in lipopolysaccharide stimulated BV-2 cells,” Molecular Brain Research, vol. 110, no. 1, pp. 63–75, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Matsui and T. Kakeda, “IL-10 production is reduced by hypothermia but augmented by hyperthermia in rat microglia,” Journal of Neurotrauma, vol. 25, no. 6, pp. 709–715, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Matsui, M. Tasaki, T. Yoshioka, Y. Motoki, H. Tsuneoka, and J. Nojima, “Temperature- and time-dependent changes in TLR2-activated microglial NF-κB activity and concentrations of inflammatory and anti-inflammatory factors,” Intensive Care Medicine, vol. 38, no. 8, pp. 1392–1399, 2012. View at Publisher · View at Google Scholar
  21. P. A. Carpentier, D. S. Duncan, and S. D. Miller, “Glial toll-like receptor signaling in central nervous system infection and autoimmunity,” Brain, Behavior, and Immunity, vol. 22, no. 2, pp. 140–147, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Alexopoulou, A. C. Holt, R. Medzhitov, and R. A. Flavell, “Recognition of double-stranded RNA and activation of NF-κB by toll-like receptor 3,” Nature, vol. 413, no. 6857, pp. 732–738, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. A. N. Theofilopoulos, R. Baccala, B. Beutler, and D. H. Kono, “Type I interferons (α/β) in immunity and autoimmunity,” Annual Review of Immunology, vol. 23, pp. 307–336, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Karikó, H. Ni, J. Capodici, M. Lamphier, and D. Weissman, “mRNA is an endogenous ligand for toll-like receptor 3,” The Journal of Biological Chemistry, vol. 279, no. 13, pp. 12542–12550, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Brentano, O. Schorr, R. E. Gay, S. Gay, and D. Kyburz, “RNA released from necrotic synovial fluid cells activates rheumatoid arthritis synovial fibroblasts via toll-like receptor 3,” Arthritis and Rheumatism, vol. 52, no. 9, pp. 2656–2665, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. K. A. Cavassani, M. Ishii, H. Wen et al., “TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events,” The Journal of Experimental Medicine, vol. 205, no. 11, pp. 2609–2621, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. J. K. Olson and S. D. Miller, “Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs,” The Journal of Immunology, vol. 173, no. 6, pp. 3916–3924, 2004. View at Google Scholar · View at Scopus
  28. T. Town, D. Jeng, L. Alexopoulou, J. Tan, and R. A. Flavell, “Microglia recognize double-stranded RNA via TLR3,” The Journal of Immunology, vol. 176, no. 6, pp. 3804–3812, 2006. View at Google Scholar · View at Scopus
  29. L. M. Melton, A. B. Keith, S. Davis, A. E. Oakley, J. A. Edwardson, and C. M. Morris, “Chronic glial activation, neurodegeneration, and APP immunoreactive deposits following acute administration of double-stranded RNA,” Glia, vol. 44, no. 1, pp. 1–12, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. Z. Zhang, K. Trautmann, and H. J. Schluesener, “Microglia activation in rat spinal cord by systemic injection of TLR3 and TLR7/8 agonists,” Journal of Neuroimmunology, vol. 164, no. 1-2, pp. 154–160, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. I. K. Patro, Amit, M. Shrivastava, S. Bhumika, and N. Patro, “Poly I:C induced microglial activation impairs motor activity in adult rats,” Indian Journal of Experimental Biology, vol. 48, no. 2, pp. 104–109, 2010. View at Google Scholar · View at Scopus
  32. M. Matsumoto and T. Seya, “TLR3: interferon induction by double-stranded RNA including poly(I:C),” Advanced Drug Delivery Reviews, vol. 60, no. 7, pp. 805–812, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. T. K. Makar, D. Trisler, C. T. Bever et al., “Stem cell based delivery of IFN-beta reduces relapses in experimental autoimmune encephalomyelitis,” Journal of Neuroimmunology, vol. 196, no. 1-2, pp. 67–81, 2008. View at Publisher · View at Google Scholar
  34. M. Chen, G. Chen, H. Nie et al., “Regulatory effects of IFN-beta on production of osteopontin and IL-17 by CD4+ T cells in MS,” European Journal of Immunology, vol. 39, no. 9, pp. 2525–2536, 2009. View at Publisher · View at Google Scholar
  35. O. Stüve, N. P. Dooley, J. H. Uhm et al., “Interferon beta-1b decreases the migration of T lymphocytes in vitro: effects on matrix metalloproteinase-9,” Annals of Neurology, vol. 40, no. 6, pp. 853–863, 1996. View at Publisher · View at Google Scholar
  36. S. Dedoni, M. C. Olianas, and P. Onali, “Interferon-β induces apoptosis in human SH-SY5Y neuroblastoma cells through activation of JAK-STAT signaling and down-regulation of PI3K/Akt pathway,” Journal of Neurochemistry, vol. 115, no. 6, pp. 1421–1433, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Akwa, D. E. Hassett, M. L. Eloranta et al., “Transgenic expression of IFN-α in the central nervous system of mice protects against lethal neurotropic viral infection but induces inflammation and neurodegeneration,” The Journal of Immunology, vol. 161, no. 9, pp. 5016–5026, 1998. View at Google Scholar · View at Scopus
  38. C. Reyes-Vázquez, B. Prieto-Gómez, and N. Dafny, “Interferon modulates central nervous system function,” Brain Research, vol. 1442, pp. 76–89, 2012. View at Publisher · View at Google Scholar
  39. T. Matsui, Y. Motoki, T. Inomoto et al., “Temperature-related effects of adenosine triphosphate-activated microglia on pro-inflammatory factors,” Neurocritical Care, vol. 17, no. 2, pp. 293–300, 2012. View at Publisher · View at Google Scholar
  40. A. Bal-Price and G. C. Brown, “Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity,” The Journal of Neuroscience, vol. 21, no. 17, pp. 6480–6491, 2001. View at Google Scholar · View at Scopus
  41. L. Zhang, S. Zhao, X. Wang, C. Wu, and J. Yang, “A self-propelling cycle mediated by reactive oxide species and nitric oxide exists in LPS-activated microglia,” Neurochemistry International, vol. 61, no. 7, pp. 1220–1230, 2012. View at Publisher · View at Google Scholar
  42. T. Mosmann, “Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays,” Journal of Immunological Methods, vol. 65, no. 1-2, pp. 55–63, 1983. View at Google Scholar · View at Scopus
  43. U. K. Hanisch, T. V. Johnson, and J. Kipnis, “Toll-like receptors: roles in neuroprotection?” Trends in Neurosciences, vol. 31, no. 4, pp. 176–182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Takeda, T. Kaisho, and S. Akira, “Toll-like receptors,” Annual Review of Immunology, vol. 21, pp. 335–376, 2003. View at Publisher · View at Google Scholar
  45. M. J. Bell, P. M. Kochanek, L. A. Doughty et al., “Interleukin-6 and interleukin-10 in cerebrospinal fluid after severe traumatic brain injury in children,” Journal of Neurotrauma, vol. 14, no. 7, pp. 451–457, 1997. View at Google Scholar · View at Scopus
  46. R. S. B. Clark, P. M. Kochanek, W. D. Obrist et al., “Cerebrospinal fluid and plasma nitrite and nitrate concentrations after head injury in humans,” Critical Care Medicine, vol. 24, no. 7, pp. 1243–1251, 1996. View at Publisher · View at Google Scholar · View at Scopus
  47. M. N. Woodroofe, G. S. Sarna, M. Wadhwa et al., “Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: evidence of a role for microglia in cytokine production,” Journal of Neuroimmunology, vol. 33, no. 3, pp. 227–236, 1991. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Ott, C. J. McClain, M. Gillespie, and B. Young, “Cytokines and metabolic dysfunction after severe head injury,” Journal of Neurotrauma, vol. 11, no. 5, pp. 447–472, 1994. View at Google Scholar · View at Scopus
  49. M. Aibiki, S. Maekawa, S. Ogura, Y. Kinoshita, N. Kawai, and S. Yokono, “Effect of moderate hypothermia on systemic and internal jugular plasma IL-6 levels after traumatic brain injury in humans,” Journal of Neurotrauma, vol. 16, no. 3, pp. 225–232, 1999. View at Google Scholar · View at Scopus
  50. Hypothermia after Cardiac Arrest Study Group, “Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest,” The New England Journal of Medicine, vol. 346, no. 8, pp. 549–556, 2002. View at Publisher · View at Google Scholar
  51. S. Yamaguchi, K. Nakahara, T. Miyagi, T. Tokutomi, and M. Shigemori, “Neurochemical monitoring in the management of severe head-injured patients with hypothermia,” Neurological Research, vol. 22, no. 7, pp. 657–664, 2000. View at Google Scholar · View at Scopus
  52. C. F. Loidl, J. De Vente, M. M. van Ittersum et al., “Hypothermia during or after severe perinatal asphyxia prevents increase in cyclic GMP-related nitric oxide levels in the newborn rat striatum,” Brain Research, vol. 791, no. 1-2, pp. 303–307, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Khorooshi and T. Owens, “Injury-induced type I IFN signaling regulates inflammatory responses in the central nervous system,” The Journal of Immunology, vol. 185, no. 2, pp. 1258–1264, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. M. O. Kim, Q. Si, and J. N. Zhou, “Interferon-beta activates multiple signaling cascades in primary human microglia,” Journal of Neurochemistry, vol. 81, no. 6, pp. 1361–1371, 2002. View at Publisher · View at Google Scholar
  55. L. L. Hua and S. C. Lee, “Distinct patterns of stimulus-inducible chemokine mRNA accumulation in human fetal astrocytes and microglia,” Glia, vol. 30, no. 1, pp. 74–81, 2000. View at Google Scholar
  56. J. Wang and I. L. Campbell, “Innate STAT1-dependent genomic response of neurons to the antiviral cytokine alpha interferon,” Journal of Virology, vol. 79, no. 13, pp. 8295–8302, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Wada, N. Okada, T. Yamamura, and S. Koizumi, “Nerve growth factor induces resistance of PC12 cells to nitric oxide cytotoxicity,” Neurochemistry International, vol. 29, no. 5, pp. 461–467, 1996. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Bsibsi, J. J. Bajramovic, M. H. J. Vogt et al., “The microtubule regulator stathmin is an endogenous protein agonist for TLR3,” The Journal of Immunology, vol. 184, no. 12, pp. 6929–6937, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Liu, C. Stadelmann, M. Moscarello et al., “Expression of stathmin, a developmentally controlled cytoskeleton-regulating molecule, in demyelinating disorders,” The Journal of Neuroscience, vol. 25, no. 3, pp. 737–747, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. C. X. Cao, Q. W. Yang, F. L. Lv, J. Cui, H. B. Fu, and J. Z. Wang, “Reduced cerebral ischemia-reperfusion injury in toll-like receptor 4 deficient mice,” Biochemical and Biophysical Research Communications, vol. 353, no. 2, pp. 509–514, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. F. Hua, J. Ma, T. Ha et al., “Activation of toll-like receptor 4 signaling contributes to hippocampal neuronal death following global cerebral ischemia/reperfusion,” Journal of Neuroimmunology, vol. 190, no. 1-2, pp. 101–111, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Hyakkoku, J. Hamanaka, K. Tsuruma et al., “Toll-like receptor 4 (TLR4), but not TLR3 or TLR9, knock-out mice have neuroprotective effects against focal cerebral ischemia,” Neuroscience, vol. 171, no. 1, pp. 258–267, 2010. View at Publisher · View at Google Scholar · View at Scopus