Involvement of brain cytokines in zymosan-induced febrile response

Journal of Applied Physiology

Volumn 116, Issue 9, 2014, Pages 1220-1229

  Bastos Pereira, Amanda L ^a   Fraga, Daniel ^a   Ott, Daniela ^b   Simm, Björn ^b   Murgott, Jolanta ^b   Roth, Joachim ^b   Zampronio, Aleksander R ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Cytokine; Fever; MnPO; OVLT; Zymosan

Indexed keywords

CYTOKINE; ZYMOSAN;

ANIMAL; BRAIN; CHEMICALLY INDUCED; DOSE RESPONSE; DRUG EFFECTS; FEVER; MALE; METABOLISM; NEWBORN; RAT; SECRETION (PROCESS); TOXICITY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; FEVER; MALE; RATS; RATS, WISTAR; ZYMOSAN;

EID: 84901218361     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01278.2013     Document Type: Article

References (76)

1. Banks WA, Kastin AJ, Gutierrez EG. Penetration of interleukin-6 across the murine blood-brain barrier. Neurosci Lett 179: 53-56, 1994.
2. Banks WA, Ortiz L, Plotkin SR, Kastin AJ. 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. J Pharmacol Exp Ther 259: 988-996, 1991.
3. Blatteis CM. Role of the OVLT in the febrile response to circulating pyrogens. Prog Brain Res 91: 409-412, 1992.
4. Blatteis CM, Xin L, Quan N. Neuromodulation of fever. A possible role for substance P. Ann NY Acad Sci 741: 162-173, 1994.
5. Blatteis CM, Xin L, Quan N. Neuromodulation of fever: apparent involvement of opioids. Brain Res Bull 26: 219-223, 1991.
6. Bsibsi M, Ravid R, Gveric D, van Noort JM. Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 61: 1013-1021, 2002.
7. Cao C, Matsumura K, Yamagata K, Watanabe Y. Cyclooxygenase-2 is induced in brain blood vessels during fever evoked by peripheral or central administration of tumor necrosis factor. Brain Res Mol Brain Res 56: 45-56, 1998.
8. Cao C, Matsumura K, Yamagata K, Watanabe Y. Endothelial cells of the rat brain vasculature express cyclooxygenase-2 mRNA in response to systemic interleukin-1 beta: a possible site of prostaglandin synthesis responsible for fever. Brain Res 733: 263-272, 1996.
9. Cartmell T, Poole S, Turnbull AV, Rothwell NJ, Luheshi GN. Circulating interleukin-6 mediates the febrile response to localised inflammation in rats. J Physiol 526, Pt 3: 653-661, 2000.
10. Chensue SW, Terebuh PD, Remick DG, Scales WE, Kunkel SL. In vivo biologic and immunohistochemical analysis of interleukin-1 alpha, beta and tumor necrosis factor during experimental endotoxemia. Kinetics, Kupffer cell expression, and glucocorticoid effects. Am J Pathol 138: 395-402, 1991.
11. Coelho MM, Pela IR, Rothwell NJ. Dexamethasone inhibits the pyro-genic activity of prostaglandin F2 alpha, but not prostaglandin E2. Eur J Pharmacol 238: 391-394, 1993.
12. Cooper AL, Brouwer S, Turnbull AV, Luheshi GN, Hopkins SJ, Kunkel SL, Rothwell NJ. Tumor necrosis factor-Alpha and fever after peripheral inflammation in the rat. Am J Physiol Regul Integr Comp Physiol 267: R1431-R1436, 1994.
13. Dantzer R. Cytokine-induced sickness behavior: mechanisms and implications. Ann NY Acad Sci 933: 222-234, 2001.
14. Di Carlo FJ, Fiore JV. On the composition of zymosan. Science 127: 756-757, 1958.
15. Dimopoulos G, Antonopoulou A, Armaganidis A, Vincent JL. How to select an antifungal agent in critically ill patients. J Crit Care 28: 717-727, 2013.
16. Diniz SN, Nomizo R, Cisalpino PS, Teixeira MM, Brown GD, Man-tovani A, Gordon S, Reis LF, Dias AA. PTX3 function as an opsonin for the dectin-1-dependent internalization of zymosan by macrophages. J Leukoc Biol 75: 649-656, 2004.
17. Drgona L, Khachatryan A, Stephens J, Charbonneau C, Kantecki M, Haider S, Barnes R. Clinical and economic burden of invasive fungal diseases in Europe: focus on pre-emptive and empirical treatment of Aspergillus and Candida species. Eur J Clin Microbiol Infect Dis 33: 7-21, 2014.
18. Fabricio AS, Silva CA, Rae GA, D'Orleans-Juste P, Souza GE. Essential role for endothelin ET(B) receptors in fever induced by LPS (E. coli) in rat. Br J Pharmacol 125: 542-548, 1998.
19. Figueiredo MJ, Soares DM, Martins JM, Machado Rde R, Sorgi CA, Faccioli LH, Melo MC, Malvar Ddo C, Souza GE. Febrile response induced by cecal ligation and puncture (CLP) in rats: involvement of prostaglandin E2 and cytokines. Med Microbiol Immunol 201: 219-229, 2012.
20. Fraga D, Machado RR, Fernandes LC, Souza GE, Zampronio AR. Endogenous opioids: role in prostaglandin-dependent and-independent fever. Am J Physiol Regul Integr Comp Physiol 294: R411-R420, 2008.
21. Gatti S, Bartfai T. Induction of tumor necrosis factor-Alpha mRNA in the brain after peripheral endotoxin treatment: comparison with interleukin-1 family and interleukin-6. Brain Res 624: 291-294, 1993.
22. Gegout P, Gillet P, Terlain B, Netter P. Zymosan-induced arthritis in rats. II. Effects of anti-inflammatory drugs. Life Sci 56: PL389-PL394, 1995.
23. Han H, Gong G, Bai X, Lin YC, Sun J, Wang W, Zhao Y, Yang L, Wang X, Zhang Z, Dong H, Hou L, Xiong L. Inhibition of notch signaling protects mouse lung against zymosan-induced injury. Shock 40: 312-319, 2013.
24. Hanada R, Leibbrandt A, Hanada T, Kitaoka S, Furuyashiki T, Fujihara H, Trichereau J, Paolino M, Qadri F, Plehm R, Klaere S, Komnenovic V, Mimata H, Yoshimatsu H, Takahashi N, von Haeseler A, Bader M, Kilic SS, Ueta Y, Pifl C, Narumiya S, Penninger JM. Central control of fever and female body temperature by RANKL/RANK. Nature 462: 505-509, 2009.
25. Harden LM, du Plessis I, Roth J, Loram LC, Poole S, Laburn HP. Differences in the relative involvement of peripherally released interleukin (IL)-6, brain IL-1beta and prostanoids in mediating lipopolysaccharide-induced fever and sickness behavior. Psychoneuroendocrinology 36: 608-622, 2011.
26. Hartog A, Cozijnsen M, de Vrij G, Garssen J. Collagen hydrolysate inhibits zymosan-induced inflammation. Exp Biol Med (Maywood) 238: 798-802, 2013.
27. Hatzelmann T, Harden LM, Roth J, Gerstberger R. Antipyretic effect of central [Pyr1]apelin13 on LPS-induced fever in the rat. Regul Pept 184: 6-13, 2013.
28. Hoffmann O, Braun JS, Becker D, Halle A, Freyer D, Dagand E, Lehnardt S, Weber JR. TLR2 mediates neuroinflammation and neuronal damage. J Immunol 178: 6476-6481, 2007.
29. Hubschle T, Rafalzik S, Gerstberger R, Roth J. Induction of fever and sickness behavior in telemetrically monitored rats during systemic inflammation induced by zymosan. J Anim Vet Adv 6: 569-575, 2007.
30. Jacobs RA, Satta MA, Dahia PL, Chew SL, Grossman AB. Induction of nitric oxide synthase and interleukin-1beta, but not heme oxygenase, messenger RNA in rat brain following peripheral administration of endo-toxin. Brain Res Mol Brain Res 49: 238-246, 1997.
31. Kanashiro A, Pessini AC, Machado RR, Malvar Ddo C, Aguiar FA, Soares DM, do Vale ML, de Souza GE. Characterization and pharmacological evaluation of febrile response on zymosan-induced arthritis in rats. Am J Physiol Regul Integr Comp Physiol 296: R1631-R1640, 2009.
32. Kielian T. Toll-like receptors in central nervous system glial inflammation and homeostasis. J Neurosci Res 83: 711-730, 2006.
33. Kluger MJ. Fever: role of pyrogens and cryogens. Physiol Rev 71: 93-127, 1991.
34. Kobayashi GS, Friedman L. Characterization of the pyrogenicity of Candida albicans, Saccharomyces cerevisiae, and Cryptococcus neoformans. J Bacteriol 88: 660-666, 1964.
35. Lehnardt S, Henneke P, Lien E, Kasper DL, Volpe JJ, Bechmann I, Nitsch R, Weber JR, Golenbock DT, Vartanian T. A mechanism for neurodegeneration induced by group B streptococci through activation of the TLR2/MyD88 pathway in microglia. J Immunol 177: 583-592, 2006.
36. LeMay LG, Vander AJ, Kluger MJ. Role of interleukin 6 in fever in rats. Am J Physiol Regul Integr Comp Physiol 258: R798-R803, 1990.
37. Li S, Llanos QJ, Blatteis C. Thermal response to zymosan: the differential role of complement. Neuroimmunomodulation 10: 122-128, 2002.
38. Li S, Sehic E, Wang Y, Ungar AL, Blatteis CM. Relation between complement and the febrile response of guinea pigs to systemic endotoxin. Am J Physiol Regul Integr Comp Physiol 277: R1635-R1645, 1999.
39. Luheshi GN, Stefferl A, Turnbull AV, Dascombe MJ, Brouwer S, Hopkins SJ, Rothwell NJ. Febrile response to tissue inflammation involves both peripheral and brain IL-1 and TNF-Alpha in the rat. Am J Physiol Regul Integr Comp Physiol 272: R862-R868, 1997.
40. Miller AJ, Hopkins SJ, Luheshi GN. Sites of action of IL-1 in the development of fever and cytokine responses to tissue inflammation in the rat. Br J Pharmacol 120: 1274-1279, 1997.
41. Milton AS. Thermoregulatory actions of eicosanoids in the central nervous system with particular regard to the pathogenesis of fever. Ann NY Acad Sci 559: 392-410, 1989.
42. Minano FJ, Fernandez-Alonso A, Myers RD, Sancibrian M. Hypotha-lamic interaction between macrophage inflammatory protein-1 alpha (MIP-1 alpha) and MIP-1 beta in rats: a new level for fever control? J Physiol 491, Pt 1: 209-217, 1996.
43. Nadeau S, Rivest S. Regulation of the gene encoding tumor necrosis factor alpha (TNF-Alpha) in the rat brain and pituitary in response in different models of systemic immune challenge. J Neuropathol Exp Neurol 58: 61-77, 1999.
44. Nagyoszi P, Wilhelm I, Farkas AE, Fazakas C, Dung NT, Hasko J, Krizbai IA. Expression and regulation of toll-like receptors in cerebral endothelial cells. Neurochem Int 57: 556-564, 2010.
45. Nakamura K. Central circuitries for body temperature regulation and fever. Am J Physiol Regul Integr Comp Physiol 301: R1207-R1228, 2011.
46. Navarro-Xavier RA, Newson J, Silveira VL, Farrow SN, Gilroy DW, Bystrom J. A new strategy for the identification of novel molecules with targeted proresolution of inflammation properties. J Immunol 184: 1516-1525, 2010.
47. Nucci M, Queiroz-Telles F, Tobon AM, Restrepo A, Colombo AL. Epidemiology of opportunistic fungal infections in Latin America. Clin Infect Dis 51: 561-570, 2010.
48. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol 173: 3916-3924, 2004.
49. Ott D, Murgott J, Rafalzik S, Wuchert F, Schmalenbeck B, Roth J, Gerstberger R. Neurons and glial cells of the rat organum vasculosum laminae terminalis directly respond to lipopolysaccharide and pyrogenic cytokines. Brain Res 1363: 93-106, 2010.
50. Ott D, Wuchert F, Murgott J, Rummel C, Gerstberger R, Roth J. The viral mimetic polyinosinic:polycytidylic acid (poly I:C) induces cellular responses in primary cultures from rat brain sites with an incomplete blood-brain barrier. Neurosci Lett 530: 64-68, 2012.
51. Ozinsky A, Underhill DM, Fontenot JD, Hajjar AM, Smith KD, Wilson CB, Schroeder L, Aderem A. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci USA 97: 13766-13771, 2000.
52. Pan W, Banks WA, Kennedy MK, Gutierrez EG, Kastin AJ. Differential permeability of the BBB in acute EAE: enhanced transport of TNT-Alpha. Am J Physiol Endocrinol Metab 271: E636-E642, 1996.
53. Paul R, Koedel U, Winkler F, Kieseier BC, Fontana A, Kopf M, Hartung HP, Pfister HW. Lack of IL-6 augments inflammatory response but decreases vascular permeability in bacterial meningitis. Brain 126: 1873-1882, 2003.
54. Paxinos G, Watson C. The rat brain in extereotaxic coordinates. San Diego: Academic Press, 1998.
55. Poole S, Stephenson JD. Body temperature regulation and thermoneu-trality in rats. Q J Exp Physiol Cogn Med Sci 62: 143-149, 1977.
56. Reis RC, Brito HO, Fraga D, Cabrini DA, Zampronio AR. Central substance P NK receptors are involved in fever induced by LPS but not by IL-1beta and CCL3/MIP-1alpha in rats. Brain Res 1384: 161-169, 2011.
57. Roderfeld M, Geier A, Dietrich CG, Siewert E, Jansen B, Gartung C, Roeb E. Cytokine blockade inhibits hepatic tissue inhibitor of metallo-proteinase-1 expression and up-regulates matrix metalloproteinase-9 in toxic liver injury. Liver Int 26: 579-586, 2006.
58. Roeder A, Kirschning CJ, Rupec RA, Schaller M, Korting HC. Toll-like receptors and innate antifungal responses. Trends Microbiol 12: 44-49, 2004.
59. Romanovsky AA, Ivanov AI, Shimansky YP. Selected contribution: ambient temperature for experiments in rats: a new method for determining the zone of thermal neutrality. J Appl Physiol 92: 2667-2679, 2002.
60. Roth J, De Souza GE. Fever induction pathways: evidence from responses to systemic or local cytokine formation. Braz J Med Biol Res 34: 301-314, 2001.
61. Roth J, Martin D, Storr B, Zeisberger E. Neutralization of pyrogen-induced tumour necrosis factor by its type 1 soluble receptor in guinea-pigs: effects on fever and interleukin-6 release. J Physiol 509, Pt 1: 267-275, 1998.
62. Rothwell NJ. CRF is involved in the pyrogenic and thermogenic effects of interleukin 1 beta in the rat. Am J Physiol Endocrinol Metab 256: E111-E115, 1989.
63. Rothwell NJ, Busbridge NJ, Lefeuvre RA, Hardwick AJ, Gauldie J, Hopkins SJ. Interleukin-6 is a centrally acting endogenous pyrogen in the rat. Can J Physiol Pharmacol 69: 1465-1469, 1991.
64. Rummel C, Sachot C, Poole S, Luheshi GN. Circulating interleukin-6 induces fever through a STAT3-linked activation of COX-2 in the brain. Am J Physiol Regul Integr Comp Physiol 291: R1316-R1326, 2006.
65. Saud B, Nandi J, Ong G, Finocchiaro S, Levine RA. Inhibition of TNF-Alpha improves indomethacin-induced enteropathy in rats by modulating iNOS expression. Dig Dis Sci 50: 1677-1683, 2005.
66. Smith BK, Kluger MJ. Human IL-1 receptor antagonist partially suppresses LPS fever but not plasma levels of IL-6 in Fischer rats. Am J Physiol Regul Integr Comp Physiol 263: R653-R655, 1992.
67. Soares DM, Figueiredo MJ, Martins JM, Machado RR, Sorgi C, Faciolli LH, Alves-Filho JC, Cunha FQ, Souza GE. A crucial role for IL-6 in the CNS of rats during fever induced by the injection of live E. coli. Med Microbiol Immunol 201: 47-60, 2012.
68. Soares DM, Machado RR, Yamashiro LH, Melo MC, Souza GE. Cytokine-induced neutrophil chemoattractant (CINC)-1 induces fever by a prostaglandin-dependent mechanism in rats. Brain Res 1233: 79-88, 2008.
69. Sorenson WG, Shahan TA, Simpson J. Cell wall preparations from environmental yeasts: effect on alveolar macrophage function in vitro. Ann Agric Environ Med 5: 65-71, 1998.
70. Stitt JT, Shimada SG. Enhancement of the febrile responses of rats to endogenous pyrogen occurs within the OVLT region. J Appl Physiol 67: 1740-1746, 1989.
71. Vallieres L, Rivest S. Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflammatory cytokine interleukin-1beta. J Neurochem 69: 1668-1683, 1997.
72. Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, Moreno R, Lipman J, Gomersall C, Sakr Y, Reinhart K. International study of the prevalence and outcomes of infection in intensive care units. JAMA 302: 2323-2329, 2009.
73. Williams H, Dacks PA, Rance NE. An improved method for recording tail skin temperature in the rat reveals changes during the estrous cycle and effects of ovarian steroids. Endocrinology 151: 5389-5394, 2010.
74. Wuchert F, Ott D, Murgott J, Rafalzik S, Hitzel N, Roth J, Gerstberger R. Rat area postrema microglial cells act as sensors for the toll-like receptor-4 agonist lipopolysaccharide. J Neuroimmunol 204: 66-74, 2008.
75. Yoshida K, Li X, Cano G, Lazarus M, Saper CB. Parallel preoptic pathways for thermoregulation. J Neurosci 29: 11954-11964, 2009.
76. Zampronio AR, Souza GE, Silva CA, Cunha FQ, Ferreira SH. Inter-leukin-8 induces fever by a prostaglandin-independent mechanism. Am J Physiol Regul Integr Comp Physiol 266: R1670-R1674, 1994.