STAT3 and COX-2 activation in the guinea-pig brain during fever induced by the Toll-like receptor-3 agonist polyinosinic:polycytidylic acid

Cell and Tissue Research

Volumn 328, Issue 3, 2007, Pages 549-561

  Voss, Thilo ^a   Barth, Stephan W ^b   Rummel, Christoph ^a   Gerstberger, Rüdiger ^a   Hübschle, Thomas ^a   Roth, Joachim ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

Author keywords

Cyclooxygenase; Cytokines; Fever; Guinea pig (male); Systemic inflammation; Toll like receptors; Transcription factors

Indexed keywords

CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; DICLOFENAC; DRUG DERIVATIVE; INTERLEUKIN 1BETA; MESSENGER RNA; NIMESULIDE; POLYINOSINIC POLYCYTIDYLIC ACID; STAT3 PROTEIN; TOLL LIKE RECEPTOR 3 AGONIST; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN CELL; BRAIN REGION; CELL ACTIVATION; CELL POPULATION; CONTROLLED STUDY; DRUG INDUCED DISEASE; ENDOTHELIUM; FEVER; FLUORESCENCE IN SITU HYBRIDIZATION; GENE TRANSLOCATION; GUINEA PIG; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RHOMBENCEPHALON; SENSE ORGAN; UPREGULATION;

ANIMALS; ASTROCYTES; BRAIN; CELL NUCLEUS; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FEVER; GUINEA PIGS; INTERLEUKIN-1BETA; MALE; POLY I-C; PROTEIN TRANSPORT; STAT3 TRANSCRIPTION FACTOR; TISSUE DISTRIBUTION; TOLL-LIKE RECEPTOR 3;

CAVIA;

EID: 34247647069     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-007-0386-6     Document Type: Article

References (57)

1. Absher M, Stinebring WR (1969) Toxic properties of a synthetic double-stranded RNA: pyrogenicity of Poly I:Poly C in rabbits. Nature 223:715-717
2. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA (2001) Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413:732-738
3. Barth SW, Riediger T, Lutz TA, Rechkemmer G (2004) Peripheral amylin activates circumventricular organs expressing calcitonin receptor a/b subtypes and receptor activity modifying proteins in the rat. Brain Res 997:97-102
4. Blatteis CM (2006) Endotoxic fever: new concepts of its regulation suggest new approaches to its management. Pharmacol Ther 111:194-223
5. Botting R (2004) Antipyretic therapies. Front Biosci 9:956-966
6. Botting RM (2006) Cyclooxygenase: past, present and future. A tribute to John R. Vane (1927-2004). J Therm Biol 31:208-219
7. Breder CD, Saper CB (1996) Expression of inducible cyclooxygenase mRNA in the mouse brain after systemic administration of bacterial lipopolysaccharide. Brain Res 713:64-69
8. Cao C, Matsumura K, Yamagata K, Watanabe Y (1995) Induction by lipopolysaccharide of cyclooxygenase-2 mRNA in rat brain: its possible role in febrile response. Brain Res 613:331-336
9. Cao C, Matsumura K, Yamagata K, Watanabe Y (1997) Involvement of cyclooxygenase-2 in LPS-induced fever and regulation of its mRNA by LPS in the rat brain. Am J Physiol Regul Integr Comp Physiol 287:R1712-R1725
10. Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F (1998) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 274:10689-10692
11. Chuang J, Lin MT, Chan SA, Won SJ (1990) Febrile effects of polyriboinosinic: polyribocytidylic acid and interferon: relationship to somatostatin in rat hypothalamus. Pflügers Arch Eur J Physiol 415:606-610
12. Cooper KE, Blähser S, Malkinson TJ, Merker G, Roth J, Zeisberger E (1988) Changes in body temperature and vasopressin content of brain neurons, in pregnant and non-pregnant guinea pigs, during fevers produced by Poly I:Poly C. Pflügers Arch Eur J Physiol 412:292-296
13. Ellis S, Mouihate A, Pittman QJ (2006) Neonatal programming of the rat neuroimmune response: stimulus specific changes elicited by bacterial and viral mimetics. J Physiol (Lond) 571:695-701
14. Fabricio ASC, Veiga FH, Cristofoletti R, Navarra P, Souza GEP (2004) The effects of selective and nonselective cyclooxygenase inhibitors on endothelin-1-induced fever in rats. Am J Physiol Regul Integr Comp Physiol 288:R671-R677
15. Fortier ME, Kent S, Ashdown H, Poole S, Boksa P, Luheshi GN (2004) The viral mimic, polyinosinic:polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanisms. Am J Physiol Regul Integr Comp Physiol 287:R759-R766
16. Gautron L, Lafon P, Chaigniau M, Tramu G, Layé S (2002) Spatiotemporal analysis of signal transducer and activator of transcription 3 activation in rat brain astrocytes and pituitary following peripheral immune stimulation. Neuroscience 112:717-729
17. Harré EM, Roth J, Gerstberger R, Hübschle T (2003) Interleukin-6 mediates lipopolysaccharide-induced nuclear STAT3 translocation in astrocytes of rat sensory circumventricular organs. Brain Res 980:151-155
18. Harré EM, Roth J, Pehl U, Kueth M, Gerstberger R, Hübschle T (2002) Selected contribution: role of IL-6 in LPS-induced nuclear STAT3 translocation in sensory circumventricular organs during fever in rats. J Appl Physiol 92:2657-2666
19. Heinrich P, Behrmann C, Müller-Newen J, Schaper GF, Graeve L (1998) Interleukin-6-type cytokine signalling through the gp130/ Jak/STAT pathway. Biochem J 334:297-314
20. Hosoi T, Okuma Y, Kawagishi T, Qi X, Matsuda T, Nomura Y (2004) Bacterial endotoxin induces STAT3 activation in the mouse brain. Brain Res 1023:48-53
21. Hübschle T, Thom E, Watson A, Roth J, Klaus S, Meyerhof W (2001) Leptin-induced nuclear translocation of STAT3 immunoreactivity in hypothalamic nuclei involved in body weight regulation. J Neurosci 21:2413-2424
22. Hübschle T, Mütze J, Mühlradt PF, Korte S, Gerstberger R, Roth J (2006) Pyrexia, anorexia, adipsia, and depressed motor activity in rats during systemic inflammation induced by the Toll-like receptors-2 and -6 agonists MALP-2 and FSL-1. Am J Physiol Regul Integr Comp Physiol 290:R180-R187
23. Ivanov AI, Romanovsky AA (2004) Prostaglandin E2 as a mediator of fever: synthesis and catabolism. Front Biosci 9:1977-1993
24. Jacobs BL, Langland JQ (1996) When two strands are better than one: the mediators and modulators of the cellular responses to double stranded RNA. Virology 219:339-349
25. Kano A, Wolfgang MJ, Gao Q, Jacobi J, Chai GX, Hansen W, Iwamoto Y, Pober JS, Flavell RA, Fu XY (2003) Endothelial cells require STAT3 for protection against endotoxin-induced inflammation. J Exp Med 198:1517-1525
26. Kimura M, Toth LA, Agostini H, Cady AB, Majde JA, Krueger JM (1994) Comparison of acute phase responses induced in rabbits by lipopolysaccharide and double stranded RNA. Am J Physiol Regul Integr Comp Physiol 267:R1596-R1605
27. Kluger MJ (1991) Fever: role of pyrogens and cryogens. Physiol Rev 71:93-127
28. Konsman JP, Vigues S, Mackerlova L, Bristow A, Blomqvist A (2004) Rat brain vasculature distribution of interleukin-1 type-1 receptor immunoreactivity: relationship to patterns of inducible cyclooxygenase expression by peripheral inflammatory stimuli. J Comp Neurol 472:113-129
29. Kozak W, Wrotek S, Kozak A (2006) Pyrogenicity of CpG-DNA in mice: role of interleukin-6, cyclooxygenases, and nuclear factor-κB. Am J Physiol Regul Integr Comp Physiol 290:R871-R880
30. Krishan KL, Sohi KK, Pathak CM, Kaushik G (2006) Nimesulide inhibits lipopolysaccharide-induced production of superoxide anions and nitric oxide and iNOS expression in alveolar macrophages. Life Sci 78:1662-1669
31. Lebel E, Vallières L, Rivest S (2000) Selective involvement of interleukin-6 in the transcriptional activation of the suppressor of cytokine signalling-3 in the brain during systemic immune challenges. Endocrinology 141:3749-3763
32. Li S, Wang Y, Matsumura K, Ballou LR, Morham SG, Blatteis CM (1999) The febrile response to lipopolysaccharide is blocked in cyclooxygenase-2?/?, but not cyclooxygenase-1?/? mice. Brain Res 825:86-94
33. Li S, Sehic E, Ungar AL, Blatteis CM (2000) Complement does not mediate the febrile responses of guinea pigs to muramyl dipeptide and polyriboinosinic-polyribocycytidylic acid. J Therm Biol 25:51-58
34. Luheshi GN, Rothwell NJ (1996) Cytokines and fever. Int Arch Allergy Immunol 109:301-307
35. Mütze J, Roth J, Gerstberger R, Matsumura K, Hübschle T (2006) Immunohistochemical evidence of functional leptin receptor expression in neuronal and endothelial cells of the rat brain. Neurosci Lett 394:105-110
36. Nadjar A, Combe C, Layé S, Tridon V, Dantzer R, Amedee T, Parnet P (2003) Nuclear factor κB nuclear translocation as a crucial marker of brain response to interleukin-1. A study in rat and interleukin-1 type I deficient mouse. J Neurochem 87:1024-1036
37. Polotrak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B (1998) Defective LPS signalling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085-2088
38. Riedel W, Lang U, Oetjen U, Schlapp U, Shibata M (2003) Inhibition of oxygen radical formation by methylene blue, aspirin, or alipoic acid prevents bacterial-lipopolysaccharide-induced fever. Mol Cell Biochem 247:83-94
39. Roth J, Aslan T, Störr B, Zeisberger E (1997) Lack of cross tolerance between LPS and muramyl dipeptide in induction of circulating TNF-α and IL-6 in guinea pigs. Am J Physiol Regul Integr Comp Physiol 273:R1529-R1533
40. Roth J, Hübschle T, Pehl U, Ross G, Gerstberger R (2002) Influence of systemic treatment with cyclooxygenase inhibitors on lipopolysaccharide- induced fever and circulating levels of cytokines and cortisol in guinea pigs. Pflügers Arch Eur J Physiol 412:292-296
41. Roth J, Harré EM, Rummel C, Gerstberger R, Hübschle T (2004) Signaling the brain in systemic inflammation: role of sensory circumventricular organs. Front Biosci 9:290-300
42. Roth J, Rummel C, Barth SW, Gerstberger R, Hübschle T (2006) Molecular aspects of fever and hyperthermia. Neurol Clin 24:421-439
43. Rotondo D, Abul HT, Milton AS, Davidson J (1988) Pyrogenic immunomodulators increase the level of prostaglandin E2 in the blood simultaneously with the onset of fever. Eur J Pharmacol 154:145-152
44. Rummel C, Hübschle T, Gerstberger R, Roth J (2004) Nuclear translocation of the transcription factor STAT3 in the guinea pig brain during systemic or localized inflammation. J Physiol (Lond) 557:671-687
45. Rummel C, Barth SW, Voss T, Korte S, Gerstberger R, Hübschle T, Roth J (2005a) Localized vs. systemic inflammation in guinea pigs: a role for prostaglandins at distinct points of the fever induction pathways? Am J Physiol Regul Integr Comp Physiol 289:340-347
46. Rummel C, Voss T, Matsumura K, Korte S, Gerstberger R, Roth J, Hübschle T (2005b) Nuclear STAT3 translocation in guinea pig and rat brain endothelium during systemic challenge with lipopolysaccharide and interleukin-6. J Comp Neurol 491:1-14
47. Sako K, Okuma Y, Hosoi T, Nomura Y (2005) STAT3 activation and c-FOS expression in the brain following peripheral administration of bacterial DNA. J Neuroimmunol 158:40-49
48. Soszynski D, Kozak W, Szewczenko M (1991) Course of fever response to repeated administration of sublethal doses of lipopolysaccharides, polyinosinic:polycytidylic acid and muramyl dipeptide to rabbits. Experientia 47:43-47
49. Steiner AA, Li S, Llanos-Q J, Blatteis CM (2001) Differential inhibition by nimesulide of the early and late phases of intravenous- and intracerebroventricular-LPS-induced fever in guinea pigs. Neuroimmunomodulation 9:263-275
50. Steiner AA, Rudaya AY, Robbins JR, Dragic AS, Langenbach R, Romanovsky AA (2005) Expanding the role of cyclooxygenase-2 to the previously overlooked responses. Am J Physiol Regul Integr Comp Physiol 289:R1253-R1257
51. Steiner AA, Chakravarty S, Rudaya AY, Herkenham M, Romanovsky AA (2006) Bacterial lipopolysaccharide fever is initiated via Tolllike receptor 4 on hematopoietic cells. Blood 107:4000-4002
52. Strömberg H, Svensson SP, Hermanson O (2000) Distribution of the transcription factor signal transducer and activator of transcription 3 in the rat central nervous system and dorsal root ganglia. Brain Res 853:105-114
53. Takeda K, Akira S (2000) STAT family of of transcription factors in cytokine-mediated biological responses. Cytokine Growth Factors Rev 11:199-211
54. Traynor TN, Majde JA, Bohnet SG, Krueger JM (2004) Intratracheal double-stranded RNA plus interferon-γ: a model for analysis of the acute phase response to respiratory viral infections. Life Sci 74:2563-2576
55. Voss T, Rummel C, Gerstberger R, Hübschle T, Roth J (2006) Fever and circulating cytokines induced by double stranded RNA in guinea pigs: dependence on the route of administration and effects of repeated injections. Acta Physiol 187:379-389
56. Won SJ, Lin MT (1988) Pyrogenicity of interferon and its inducer in rabbits. Am J Physiol Regul Integr Comp Physiol 254:340-347
57. Zhang YH, Lu J, Elmquist JK, Saper CB (2003) Specific roles of cyclooxygenase-1 and cyclooxygenase-2 in lipopolysaccharide-induced fever and Fos expression in rat brain. J Comp Neurol 463:3-12