Production of mice deficient in genes for interleukin (IL)-1α, IL-1β, IL-1α/β, and IL-1 receptor antagonist shows that IL-1β is crucial in turpentine-induced fever development and glucocorticoid secretion

Journal of Experimental Medicine

Volumn 187, Issue 9, 1998, Pages 1463-1475

  Horai, Reiko ^a   Asano, Masahide ^a   Sudo, Katsuko ^a   Kanuka, Hirotaka ^a   Suzuki, Masatoshi ^a   Nishihara, Masugi ^a   Takahashi, Michio ^a   Iwakura, Yoichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; CYCLOOXYGENASE 2; GLUCOCORTICOID; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; TURPENTINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE RELEASE; CYTOKINE PRODUCTION; DIENCEPHALON; FEMALE; FEVER; GROWTH RETARDATION; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL;

ANIMALS; BODY WEIGHT; BRAIN; CORTICOSTERONE; FEVER; GLUCOCORTICOIDS; INFLAMMATION; INTERLEUKIN-1; LIPOPOLYSACCHARIDES; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-1; RNA, MESSENGER; TURPENTINE;

EID: 0032482168     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.9.1463     Document Type: Article

References (62)

1. Dinarello, C.A. 1996. Biologic basis for interleukin-1 in disease. Blood. 87:2095-2147.
2. Durum, S.K., and J.J. Oppenheim. 1993. Proinflammatory cytokines and immunity. In Fundamental Immunology, 3rd ed. W.E. Paul, editor. Raven Press, Ltd., New York. 801-835.
3. Toed, M.J., and J.A. Schmidt. 1997. Interleukin-1: structure and function. In Cytokines in Health and Disease, 2nd ed. D.C. Remick and J.S. Friedland, editors. Marcel Dekker, Inc., New York. 1-27.
4. Dinarello, C.A. 1991. Interleukin-1 and interleukin-1 antagonism. Blood. 77:1627-1652.
5. Silver, A.K.J., W.K. Masson, A.M. George, J. Adam, and R. Cox. 1990. The IL-1α and β genes are closely linked (<70 kb) on mouse chromosome 2. Somatic Cell Mol. Genet. 16: 549-556.
6. D'Eustachio, P., S. Jadidi, R.C. Fuhlbrigge, P.W. Gray, and D.D. Chaplin. 1987. Interleukin-1α and β genes: linkage on chromosome 2 in the mouse. Immunogenetics. 26:339-343.
7. Sims, J.E., M.A. Gayle, J.L. Slack, M.R. Alderson, T.A. Bird, J.G. Giri, F. Colotta, F. Re, A. Mantovani, K. Shanebeck, et al. 1993. Interleukin 1 signaling occurs exclusively via the type I receptor. Proc. Natl. Acad. Sci. USA. 90:6155-6159.
8. Colotta, F., F. Re, M. Muzio, R. Bertini, N. Polentarutti, M. Sironi, J.G. Giri, S.K. Dower, J.E. Sims, and A. Mantovani. 1993. Interleukin-1 type II receptor: a decoy target for IL-1 that is regulated by IL-4. Science. 261:472-475.
9. Carter, D.B., M.R. Deibel, Jr., C.J. Dunn, C.-S.C. Tomich, A.L. Laborde, J.L. Slightom, A.E. Berger, M.J. Bienkowski, F.F. Sun, R.N. McEwan, et al. 1990. Purification, cloning, expression and biological characterization of an interleukin-1 receptor antagonist protein. Nature. 344:633-638.
10. Hannum, C.H., C.J. Wilcox, W.P. Arend, F.G. Joslin, D.J. Dripps, P.L. Heimdal, L.G. Armes, A. Sommer, S.P. Eisenberg, and R.C. Thompson. 1990. Interleukin-1 receptor antagonist activity of a human interleukin-1 inhibitor. Nature. 343:336-340.
11. Haskill, S., G. Martin, L. Van Le, J. Morris, A. Peace, C.F. Bigler, G.J. Jaffe, C. Hammerberg, S.A. Sporn, S. Fong, W.P. Arend, and P. Ralph. 1991. cDNA cloning of an intracellular form of the human interleukin 1 receptor antagonist associated with epithelium. Proc. Natl. Acad. Sci. USA. 88: 3681-3685.
12. Muzio, M., N. Polentarutti, M. Sironi, G. Poli, L. De Gioia, M. Introna, A. Mantovani, and F. Colotta. 1995. Cloning and characterization of a new isoform of the interleukin 1 receptor antagonist. J. Exp. Med. 182:623-628.
13. Kluger, M.J. 1991. Fever: role of pyrogens and cryogens. Physiol. Rev. 71:93-127.
14. Long, N.C., I. Otterness, S.L. Kunkel, A.J. Vander, and M.J. Kluger. 1990. Roles of interleukin 1β and tumor necrosis factor in lipopolysaccharide fever in rats. Am. J. Physiol. 259: R724-R728.
15. Kozak, W., H. Zheng, C.A. Conn, D. Soszynski, L.H.T. Van der Ploeg, and M.J. Kluger. 1995. Thermal and behavioral effects of lipopolysaccharide and influenza in interleukin-1β-deficient mice. Am. J. Physiol. 269:R969-R977.
16. Alheim, K., Z. Chai, G. Fantuzzi, H. Hasanvan, D. Malinowsky, E. Di Santo, P. Ghezzi, C.A, Dinarello, and T. Bartfai. 1997. Hyperresponsive febrile reactions to interleukin (IL)-1α and IL-1β, and altered brain cytokine mRNA and serum cytokine levels, in IL-1β-deficient mice. Proc. Natl. Acad. Sci. USA. 94:2681-2686.
17. Zheng, H., D. Fletcher, W. Kozak, M. Jiang, K.J. Hofmann, C.A. Conn, D. Soszynski, C. Grabiec, M.E. Trumbauer, A. Shaw, et al. 1995. Resistance to fever induction and impaired acute-phase response in interleukin-1β-deficient mice. Immunity. 3:9-19.
18. Leon, L.R., C.A. Conn, M. Glaccum, and M.J. Kluger. 1996. IL-1 type I receptor mediates acute phase response to turpentine, but not lipopolysaccharide, in mice. Am. J. Physiol. 271:R1668-R1675.
19. Chrousos, G.P. 1995. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N. Engl. J. Med. 332:1351-1362.
20. Dunn, A.J. 1992. The role of interleukin-1 and tumor necrosis factor a in the neurochemical and neuroendocrine re-sponses to endotoxin. Brain Res. Bull. 29:807-812.
21. Perlstein, R.S., M.H. Whitnall, J.S. Abrams, E.H. Mougey, and R. Neta. 1993. Synergistic roles of interleukin-6, interleukin-1, and tumor necrosis factor in the adrenocorticotropin response to bacterial lipopolysaccharide in vivo. Endocrinology. 132:946-952.
22. Rivier, C., R. Chizzonite, and W. Vale. 1989. In the mouse, the activation of the hypothalamic-pituitary-adrenal axis by a lipopolysaccharide (endotoxin) is mediated through interleukin-1. Endocrinology. 125:2800-2805.
23. Turnbull, A.V., and C. Rivier. 1996. Corticotropin-releasing factor, vasopressin, and prostaglandins mediate, and nitric oxide restrains, the hypothalamic-pituitary-adrenal response to acute local inflammation in the rat. Endocrinology. 137:455-463.
24. Ebisui, O., J. Fukata, N. Murakami, H. Kobayashi, H. Segawa, S. Muro, I. Hanaoka, Y. Naito, Y. Masui, Y. Ohmoto, et al. 1994. Effect of IL-1 receptor antagonist and antiserum to TNF-α on LPS-induced plasma ACTH and corticosterone rise in rats. Am. J. Physiol. 266:E986-E992.
25. Fantuzzi, G., and C.A. Dinarello. 1996. The inflammatory response in interleukin-1β-deficient mice: comparison with other cytokine-related knock-out mice. J. Leukocyte Biol. 59: 489-493.
26. Soriano, P., C. Montgomery, R. Geske, and A. Bradley. 1991. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell. 64:693-702.
27. Sawai, S., A. Shimono, K. Hanaoka, and H. Kondoh. 1991. Embryonic lethality resulting from disruption of both N-myc alleles in mouse zygotes. New Biol. 3:861-869.
28. Yagi, T., S. Nada, N. Watanabe, H. Tamemoto, N. Kohmura, Y. Ikawa, and S. Aizawa. 1993. A novel negative selection for homologous recombinants using diphtheria toxin A fragment gene. Anal. Biochem. 214:77-86.
29. Asano, M., K. Furukawa, M. Kido, S. Matsumoto, Y. Umesaki, N. Kochibe, and Y. Iwakura. 1997. Growth retardation and early death of β-1,4-galactosyltransferase knockout mice with augmented proliferation and abnormal differentiation of epithelial cells. EMBO (Eur. Mol. Biol. Organ.) J. 16:1850-1857.
30. Nagy, A., J. Rossant, R. Nagy, W. Abramow-Newerly, and J.C. Roder. 1993. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA. 90:8424-8428.
31. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal. Biochem. 162:156-159.
32. Lomedico, P.T., U. Gubler, C.P. Hellmann, M. Dukovich, J.G. Giri, Y.-C.E. Pan, K. Collier, R. Semionow, A.O. Chua, and S.B. Mizel. 1984. Cloning and expression of murine interleukin-1 cDNA in Escherichia coli. Nature. 312:458-462.
33. Gray, P.W., D. Glaister, E. Chen, D.V. Goeddel, and D. Pennica. 1986. Two interleukin 1 genes in the mouse: cloning and expression of the cDNA for murine interleukin 1β. J. Immunol. 137:3644-3648.
34. Takahashi, Y., Y. Taketani, T. Endo, S. Yamamoto, and M. Kumegawa. 1994. Studies on the induction of cyclooxygenase isozymes by various prostaglandins in mouse osteoblastic cell line with reference to signal transduction pathways. Biochim. Biophys. Acta. 1212:217-224.
35. Chiu, C.-P., C. Moulds, R.L. Coffman, D. Rennick, and F. Lee. 1988. Multiple biological activities are expressed by a mouse interleukin 6 cDNA clone isolated from bone marrow stromal cells. Proc. Natl. Acad. Sci. USA. 85:7099-7103.
36. Pennica, D., J.S. Hayflick, T.S. Bringman, M.A. Palladino, and D.V. Goeddel. 1985. Cloning and expression in Escherichia cell of the cDNA for murine tumor necrosis factor. Proc. Natl. Acad. Sci. USA. 82:6060-6064.
37. Minty, A.J., S. Alonso, M. Caravatti, and M.E. Buckingham, 1982. A fetal skeletal muscle actin mRNA in the mouse and its identity with cardiac actin mRNA. Cell. 30:185-192.
38. Zahedi, K., M.F. Seldin, M. Rits, R.A.B. Ezekowitz, and A.S. Whitehead. 1991. Mouse IL-1 receptor antagonist protein. Molecular characterization, gene mapping, and expression of mRNA in vitro and in vivo. J. Immunol. 146:4228-4233.
39. Zahedi, K.A., C.M. Uhlar, M. Rits, A.E. Prada, and A.S. Whitehead. 1994. The mouse interleukin 1 receptor antagonist protein: gene structure and regulation in vitro. Cytokine. 6:1-9.
40. Narita, K., M. Nishihara, and M. Takahashi. 1994. Concomitant regulation of running activity and metabolic change by the ventromedial nucleus of the hypothalamus. Brain Res. 642:290-296.
41. Furutani, Y., M. Notake, T. Fukui, M. Ohue, H. Nomura, M. Yamada, and S. Nakamura. 1986. Complete nucleotide sequence of the gene for human interleukin 1 alpha. Nucleic Acids Res. 14:3167-3179.
42. Telford, J.L., G. Macchia, A. Massone, V. Carinci, E. Palla, and M. Melli. 1986. The murine interleukin 1β gene: structure and evolution. Nucleic Acids Res. 14:9955-9963.
43. 2 production and sphingomyelin metabolism. Evidence for the regulation of cyclooxygenase gene expression by sphingosine and ceramide. J. Biol. Chem. 267:20044-20050.
44. Shornick, L.P., P.D. Togni, S. Mariathasan, J. Goellner, J. Strauss-Schoenberger, R.W. Karr, T.A. Ferguson, and D.D. Chaplin. 1996. Mice deficient in IL-1β manifest impaired contact hypersensitivity to trinitrochlorobenzene. J. Exp. Med. 183:1427-1436.
45. Hirsch, E., V.M. Irikura, S.M. Paul, and D. Hirsh. 1996. Functions of interleukin 1 receptor antagonist in gene knockout and overproducing mice. Proc. Natl. Acad. Sci. USA. 93: 11008-11013.
46. Labow, M., D. Shuster, M. Zetterstrom, P. Nunes, R. Terry, E.B. Cullinan, T. Bartfai, C. Solorzano, L.L. Moldawer, R. Chizzonite, and K.W. McIntyre. 1997. Absence of IL-1 signaling and reduced inflammatory response in IL-1 type I receptor-deficient mice. J. Immunol. 159:2452-2461.
47. Hurwitz, A., D.W. Payne, J.N. Packman, C.L. Andreani, C.E. Resnick, E.R. Hernandez, and E.Y. Adashi. 1991. Cytokine-mediated regulation of ovarian function: interleukin-1 inhibits gonadotropin-induced androgen biosynthesis. Endocrinology. 129:1250-1256.
48. De, M., T.H. Sanford, and G.W. Wood. 1992. Detection of interleukin-1, interleukin-6, and tumor necrosis factor-α in the uterus during the second half of pregnancy in the mouse. Endocrinology. 131:14-20.
49. Plata-Salamán, C.R., and J.M. Ffrench-Mullen. 1992. Intracerebroventricular administration of a specific IL-1 receptor antagonist blocks food and water intake suppression induced by interleukin-1β. Physiol. Behav. 51:1277-1279.
50. Sonti, G., S.E. Ilyin, and C.R. Plata-Salamán. 1996. Anorexia induced by cytokine interactions at pathophysiological concentrations. Am. J. Physiol. 270:R1394-R1402.
51. Fantuzzi, G., H. Zheng, R. Faggioni, F. Benigni, P. Ghezzi, J.D. Sipe, A.R. Shaw, and C.A. Dinarello. 1996. Effect of endotoxin in IL-1β-deficient mice. J. Immunol. 157:291-296.
52. Li, P., H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, et al. Mice deficient in IL-1β-converting enzyme are defective in production of mature IL-1β and resistant to endotoxic shock. Cell. 80:401-411.
53. Dinarello, C.A., T. Ikejima, S.J.C. Warner, S.F. Orencole, G. Lonnemann, J.G. Cannon, and P. Libby. 1987. Interleukin 1 induces interleukin 1. I. Induction of circulating interleukin 1 in rabbits in vivo and in human mononuclear cells in vitro. J. Immunol. 139:1902-1910.
54. Asano, M., M. Hayashi, E. Yoshida, Y. Kawade, and Y. Iwakura. 1990. Induction of interferon-α by interferon-β, but not of interferon-β by interferon-α, in the mouse. Virology. 176:30-38.
55. Ilyin, S.E., and C.R. Plata-Salamán. 1996. In vivo regulation of the IL-1β system (ligand, receptors I and II, receptor accessory protein, and receptor antagonist) and TNF-α mRNAs in specific brain regions. Biochem. Biophys. Res. Commun. 227:861-867.
56. Bargetzi, M.J., M. Lantz, C.G. Smith, P.M. Torti, I. Olsson, S.P. Eisenberg, and H.F. Starnes, Jr. 1993. Interleukin-1β induces interleukin-1 receptor antagonist and tumor necrosis factor binding protein in humans. Cancer Res. 53:4010-4013.
57. Olson, E.N., H.-H. Arnold, P.W.J. Rigby. and B.J. Wold. 1996. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell. 85:1-4.
58. Hillhouse, E.W., and K. Mosley. 1993. Peripheral endotoxin induces hypothalamic immunoreactive interleukin-1β in the rat. Br. J. Pharmacol. 109:289-290.
59. Chai, Z., S. Gatti, G. Toniatti, V. Poli, and T. Bartfai. 1996. Interleukin (IL)-6 gene expression in the central nervous system is necessary for fever response to lipopolysaccharide or IL-1β: a study on IL-6-deficient mice. J. Exp. Med. 183: 311-316.
60. Cao, C., K. Matsumura, K. Yamagata, and Y. Watanabe. 1996. Endothelial cells of the rat brain vasculature express cyclooxygenase-2 mRNA in response to systemic interleukin-1β: a possible site of prostaglandin synthesis responsible for fever. Brain Res. 733:263-272.
61. Sapolsky, R., C. Rivier, G. Yamamoto, P. Plotsky, and W. Vale. 1987. Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor. Science. 238:522-524.
62. Kakucska, I., Y. Qi, B.D. Clark, and R.M. Lechan. 1993. Endotoxin-induced corticotropin-releasing hormone gene expression in the hypothalamic paraventricular nucleus is mediated centrally by interleukin-1. Endocrinology. 133:815-821.