Archives of Pharmacal Research

The Pharmaceutical Society of Korea (대한약학회)
권호 표지

Carbon Monoxide as a Novel Central Pyrogenic Mediator

  • Jang, Choon-Gon (Lab. of Pharmacology, Colleg of Pharmacy, Sungkyunkwan University) ;
  • Lee, Seung-Jin (Lab. of Pharmacology, College of Pharmacy, Sungkyunkwan University) ;
  • Yang, Sang-In (Lab. of Pharmacology, College of Pharmacy, Sungkyunkwan University) ;
  • Kim, Jin-Hak (Lab. of Pharmacology, College of Pharmacy Chung-Ang University) ;
  • Sohn, Uy-Dong (Lab. of Pharmacology, College of Pharmacy Chung-Ang University) ;
  • Lee, Seok-Yong (Lab. of Pharmacology, College of Pharmacy, Sungkyunkwan University)
  • Published : 2002.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Carbon monoxide (CO) are produced by heme oxygenase (HO), and HO was detected in hypothalamus. However, the roles of CO produced in hypothalamus was not fully elucidated. So, we tested the effects of CO on body temperature because preoptic-anterior hypothalamus was known as the presumptive primary fever-producing site. CO-saturated aCSF ($4{\;}{\mu}l$, i.c.v.) and hemin ($10{\;}{\mu}g$, i.c.v.) elicited marked febrile response. Pretreatment with indomethacin completely inhibited CO- and hemin-induced fever. Zinc protoporphyrin-IX ($10{\;}{\mu}g$, i.c.v.) or ODQ ($50{\;}{\mu}g$, i.c.v.) partially reduced hemin-induced febrile response. Dibutyryl-cGMP ($100{\;}{\mu}g$, i.c.v.) produced profound febrile response and this febrile response was attenuated by indomethacin. These results indicate that endogenous CO may have a role as a pyrogenic mediator in CNS and CO-mediated pyresis is dependent on prostaglandin production and partially on activation of soluble guanylate cyclase.

Keywords

References

  1. Burgunder, J. M. and Cheung, P, T, Expression of soluble guanylyl cyclase gene in adult rat brain, Eur. J. Neurosci., 6, 211-217 (1994) https://doi.org/10.1111/j.1460-9568.1994.tb00263.x
  2. Burstyn, J. N., Yu, A. E., Dierks, E. A., Hawkins, B. K. and Dawson, J. H., Studies of the heme coordination and ligand binding properties of soluble guanylyl cyclase (sGC): cha-racterization of Fe(ll)sGC and Fe(ll)sGC(CO) by electronic absorption and magnetic circular dichroism spectroscopies and failure of CO to activate the enzyme. Biochemistry, 34, 5896-5903 (1995) https://doi.org/10.1021/bi00017a019
  3. Canteros, G., Rettori, V, Franchi, A., Cebral, E., Faleti, A, Gimeno, M., McCann, S.M., Ethanol inhibits luteinizing hor-mone-releasing hormone (LHRH) secretion by blocking the response of LHRH neuronal terminals to nitiic oxide. Proc. Natl. Acad. Sci., U.S.A. 92, 3416-3420 (1995) https://doi.org/10.1073/pnas.92.8.3416
  4. Cao C., Matsumura, K., Yamagata, K., and Watanabe, Y, Induction by lipopolysaccharide of cyclooxygenase-2 mRNA in rat brain: its possible role in the febrile response. Brain Res., 697, 187-196 (1995) https://doi.org/10.1016/0006-8993(95)00839-I
  5. Chai Z., Gatti, S., Toniatti, C., Poli, V. and Bartfai, T., Interleukin (IL)-6 gene expression in the central nervous system is necessary for fever response to lipopolysaccharide or IL-1$\beta$: a study on IL-6-deficient mice. J. Exp. Med., 183, 311-316 (1999)
  6. Coceani, F., Prostaglandins and fever: facts and controversies. In Fever: basic mechanisms and management. ed. Mackowiak, P., Raven Press, New York, pp. 39-70 (1990)
  7. Dinarello, C. A., Endoenous pyrogens. The role of cytokines in the pathogenesis of fever. In Fever: basic mechanisms and management. Ed. Mackowiak, P., Raven Press, New York, pp. 23-47 (1990)
  8. Dinarello, C.A., Cytokines as endogenous pyrogens. J. Infect. Dis., 179(suppl 2), S294-S304, (1999) https://doi.org/10.1086/513856
  9. Ewing, J. F., Haber, S. N. and Maines, M. D., Normal and heat-induced patterns of expression of heme oxygenase-1 (HSP32) in rat brain: hyperthermia causes rapid induction of mRNA and protein. J. Neurochem., 58,1140-1149 (1992) https://doi.org/10.1111/j.1471-4159.1992.tb09373.x
  10. Gerstberger, .R, Nitric oxide and body temperature control. N. Physiol. Sci., 14, 30-36 (1999)
  11. Grundemar, L. and Ny, L., Pitfalls using metalloporphyrins in carbon monoxide research. Trends Pharmacol. Sci., 18, 193-195(1997) https://doi.org/10.1016/S0165-6147(97)90622-2
  12. Jansky, L., Vybiral, S., Pospisilowa, D., Roth, J., Dornand, J., Zeisberger, E. and Kaminkowa, J., Production of systemic and hypothalamic cytokines during the early phase of the endotoxin fever. Neuroendocrinology, 62, 55-61 (1995) https://doi.org/10.1159/000126988
  13. Jung, J. K. and Lee, S. Y., Pyrogenic effects of nitric oxide and carbon monoxide. Proceeding of the 51st Annual Meeting of Korean Saciety of Pharmacalagy, 200 (1999)
  14. Jung, J. K., Sohn, U. D. and Lee, S. Y., The hyperthermic effect of nitric oxide in central nervous system. Kor. J. Physiol. Pharmacal., 5, 93-98 (2001)
  15. Kharitonov, V. G., Sharma, V. S., Pilz, R. B., Magde, D. and Koesling, D., Basis of guanylate cyclase activation by carbon monoxide. Proc. Natl. Acad. Sci. U.S.A., 92, 2568-2571(1995) https://doi.org/10.1073/pnas.92.7.2568
  16. Kluger, M. J., Fever: role of pyrogens and cryogens. Physiol. Rev., 71, 93-127 (1991)
  17. LeMay, L. G., Vander, A. J. and Kluger, M. J., Role of interleukin-6 in fever in the rat. Am. J. Physiol., 258, R798-R803(1990)
  18. Lin, J. H. and Lin, M. T., Nitric oxide synthase-cyclo-oxygenase pathways in organum vasculasum laminae terminalis: possible role in pyrogenic fever in rabbits. Br. J. Pharmacol., 118, 179-185 (1996) https://doi.org/10.1111/j.1476-5381.1996.tb15383.x
  19. Maines, M. D., The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol., 37,517-554 (1997) https://doi.org/10.1146/annurev.pharmtox.37.1.517
  20. Mancuso, C., Pistritto, G., Tringali, G., Grossman, A. B., Preziosi, P. and Navarra, P. Evidence that carbon monoxide stimulates prostaglandin endoperoxide synthase activity in rat hypothalamic explants and in primary cultures of rat hypothalamic astrocytes. Brain. Res. Mol. Brain Res., 45, 294-300 (1997) https://doi.org/10.1016/S0169-328X(96)00258-6
  21. Mancuso, C., Tringali, G., Grossman, A, Preziosi, P. and Navarra, P, The generation of nitric oxide and carbon monoxide produces opposite effects on the release of immunoreactive interleukin-1 beta from the rat hypothalamus in vitro: evidence for the involvement of different signaling pathways. Endocrinology, 139, 1031-1037 (1998) https://doi.org/10.1210/en.139.3.1031
  22. Matsuda, T., Hari, T and Nakashima, T., Thermal and PG$E_{2}$ sensitivity of the organum vasculosum laminae terminalis region and preoptic area in rat brain slices. J Physiol.(London), 454,197-212 (1992) https://doi.org/10.1113/jphysiol.1992.sp019260
  23. Matsuoka, I., Giuili, G., Poyard, M., Stengel, D., Parma, J., Guellaen, G. and Hanoune, J., Localization of adenylyl and guanylyl cyclase in rat brain by in situ hybridization: comparison with calmodulin mRNA distribution. J. Neurosci., 12,3350-3360 (1992)
  24. Milton, A. S. and Wendlandt, S., A possible role for prostaglandin E1 as a modulator for temperature regulation in the central nervous system of the cat (abstract). J. Physiol., 207, 76-77P (1970)
  25. Minano, F. J., Armengol, J. A., Sancibrian, M., Pomares, F., Benamar, K. and Myers, R. D., Macrophage inflammatory protein-1 beta and inducible nitric oxide synthase immunoreactivity in rat brain during prostaglandin E2- or lipopolysaccharide -induced fever. Ann. N. Y. Acad. Sci., 813, 272-280 (1997) https://doi.org/10.1111/j.1749-6632.1997.tb51705.x
  26. Paxinos, G. and Watson, C., The Rat Brain in Stereotaxic Coordinates. 3rd ed., Academic Press. Sydney (1997)
  27. Quan, N., Whiteside, M. and Herkenham, M., Cyclooxygenase 2 mRNA expression in rat brain after peripheral injection of lipopolysaccharide. Brain Res., 802,189-197 (1998) https://doi.org/10.1016/S0006-8993(98)00402-8
  28. Redford, J., Bishal, I. and Coceani, F., Pyrogen-prostaglandin coupling in the pathogenesis of fever: evidence against a role for nitric oxide. Can. J. Physiol. Pharmacol., 73, 1466-1474(1995) https://doi.org/10.1139/y95-204
  29. Rizzardini, M., Carelli, M., Cabello Porras, M. R. and Cantoni, L., Mechanisms of endotoxin-induced haem oxygenase mRNA accumulation in mouse liver: synergism by glutathione depletion and protection by N-acetylcysteine. Biochem. J., 304, 477-83 (1994) https://doi.org/10.1042/bj3040477
  30. Rizzardini, M., Terao, M., Falciani, F. and Cantoni, L., Cytokine induction of haem oxygenase mRNA in mouse liver. Interleukin 1 transcriptionally activates the haem oxygenase gene. Biochem. J, 290, 343-7 (1993) https://doi.org/10.1042/bj2900343
  31. Roth, J., Conn, C.A, Kluger, M.J. and Zeisberger, E., Kinetics of systemic and intrahypothalamic IL-6 and tumor necrosis factor during endotoxin fever in the guinea pig. Am. J Physiol., 265, R653-R658 (1993)
  32. Roth, R., Storr, B., Voigt, K. and Zeisberger, E., Inhibition of nitric oxide synthase results in a suppression of interleukin-1-induced fever in rats. Life Sci., 62, PL345-350 (1998) https://doi.org/10.1016/S0024-3205(98)00179-9
  33. Scammell, T. E., Elmquist, J. K. and Saper, C. B., Inhibition of nitric oxide synthase produces hypothermia and depresses lipopolysaccharide fever. Am. J Physiol., 271, R333-338(1996)
  34. Schrammel, A, Behrends, S., Schmidt, K., Koesling, D. and Mayer, B., Characterization of 1H-(1,2,4)oxadiazolo(4,3-a)quinoxalin-1-one as a heme-site inhibitor of nitric oxide-sensitive guanylyl cyclase. Mol. Pharmacol., 50, 1-5 (1996)
  35. Steiner, A. A. and Branco, L. G., Carbon monoxide is the heme oxygenase product with a pyretic action: evidence for a cGMP signaling pathway. Am. J. Physiol. Regul. Integr. Compo Physiol., 280, R448-R457 (2001)
  36. Steiner, A. A. and Branco, L. G., Central CO-heme oxygenase pathway raises body temperature by a prostaglandin-independent way. J. Appl. Physol., 88, 1607-1613 (2000)
  37. Steiner, A .A, Colombari, E. and Branco, L. G., Carbon monoxide as a novel mediator of the febrile response in the central nervous system. Am. J Physiol., 277, R499-R507 (1999)
  38. Sun, Y., Rotenberg, M. O. and Maines, M. D., Developmental expression of heme oxygenase isozymes in rat brain. Two HO-2 mRNAs are detected. J Bioi. Chem., 265, 8212-8217(1990)
  39. Terry, C. M., Clikeman, J. A., Hoidal, J. R. and Callahan, K. S., Effect of tumor necrosis factor-alpha and interleukin-1 alpha on heme oxygenase-1 expression in human endothelial cells. Am. J Physiol., 274, H883-91 (1998)
  40. Van Zee, K. J., DeForge, L. E., Fischer, E., Marano, M. A., Kenney, J. S., Remick, D. G., Lowry, S. F. and Moldawer, L. L., IL-8 in septic shock, endotoxemia, and after IL-1 administration. J. lmmunol., 146, 3478-3482 (1991)
  41. Veale, W. L. and Cooper, K. E., Evidence for the involvement of prostaglandin in fever. In Recent Studies of Hypothalamic Function, ed. Lederis, K. and Veale, W., pp359-370 (1974)
  42. Verma, A, Hirsch, D. J., Glatt, C. E., Ronnett, G. V. and Snyder, S. H., Carbon monoxide: a putative neural messenger. Science, 259, 381-384 (1993) https://doi.org/10.1126/science.7678352
  43. Yermakova, .A and O'Banion, M. K., Cyclooxygenases in the central nervous system: Implications for treatment of neurological disorders. Current Pharmaceutical Design, 6, 1755-1776 (2000) https://doi.org/10.2174/1381612003398672
  44. Yet, S. F., Pellacani, A., Patterson, C., Tan, L., Folta, S. C., Foster, L., Lee, W.S., Hsieh, C.M. and Perrella, M. A, Induction of heme oxygenase-1 expression in vascular smooth muscle cells. A link to endotoxic shock. J Biol. Chem., 272, 4295-301 (1997) https://doi.org/10.1074/jbc.272.7.4295
  45. Zhuo, M., Small, S. A, Kandel, E. R. and Hawkins, R. D., Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science, 260,1946-1950 (1993) https://doi.org/10.1126/science.8100368