Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer

EMBO Journal

Volumn 18, Issue 8, 1999, Pages 2127-2136

  Kamiya, Akihide ^a   Kinoshita, Taisei ^a   Ito, Yoshiaki ^a   Matsui, Takaaki ^a   Morikawa, Yoshihiro ^a,b   Senba, Emiko ^a,b   Nakashima, Kinichi ^a,c   Taga, Tetsuya ^a,c   Yoshida, Kanji ^a,d   Kishimoto, Tadamitsu ^a,e   Miyajima, Atsushi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

gp130; Hepatocyte; Liver development; Oncostatin M

Indexed keywords

CD45 ANTIGEN; GLUCOCORTICOID; GLYCOGEN; GLYCOPROTEIN GP 130; INTERLEUKIN 6; ONCOSTATIN M; RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL MATURATION; CELL STRUCTURE; EMBRYO; FETUS; GLYCOGEN SYNTHESIS; HEMATOPOIETIC STEM CELL; LIVER CELL; LIVER DEVELOPMENT; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 0033560748     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.8.2127     Document Type: Article

References (67)

1. Abelev, G.I. (1971) Alpha-fetoprotein in ontogenesis and its association with malignant tumors. Adv. Cancer Res., 14, 295-358.
2. Baumann, H., Ziegler, S.F., Mosley, B., Morella, K.K., Pajovic, S. and Gearing, D.P. (1993) Reconstitution of the response to leukemia inhibitory factor, oncostatin M, and ciliary neurotrophic factor in hepatoma cells. J. Biol. Chem., 268, 8414-8417.
3. Bazan, J.F. (1991) Neuropoietic cytokines in the hematopoietic fold. Neuron, 7, 197-208.
4. Belanger, L., Frain, M., Baril, P., Gingras, M.C., Bartkowiak, J. and Saa-Trepat, J.M. (1981) Glucocorticosteroid suppression of alphal-fetoprotein synthesis in developing rat liver. Evidence for selective gene repression at the transcriptional level. Biochemistry, 20, 6665-6672.
5. Bruce, A.G., Hoggatt, I.H. and Rose, T.M. (1992) Oncostatin M is a differentiation factor for myeloid leukemia cells. J. Immunol, 149, 1271-1275.
6. Burgess-Beusse, B.L. and Darlington, G.J. (1998) C/EBPalpha is critical for the neonatal acute-phase response to inflammation. Mol. Cell. Biol., 18, 7269-7277.
7. Cake, M.H. (1986) Induction of tyrosine aminotransferase in utero by anti-insulin agents. Biochem. J., 238, 927-929.
8. Chomczynski, P. and Sacchi, . (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
9. Cole, T.J. et al. (1995) Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev., 9, 1608-1621.
10. Cressman, D.E., Greenbaum, L.E., DeAngelis, R.A., Ciliberto, G., Furth, E.E., Poli, V. and Taub, R. (1996) Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science, 274, 1379-1383.
11. de Juan, C., Benilo, M., Alvarez, A. and Fabregat, I. (1992) Differential proliferative response of cultured fetal and regenerating hepatocytes to growth factors and hormones. Exp. Cell Res., 202, 495-500.
12. Derman, E., Krauter, K., Walling, L., Weinberger, C., Ray, M. and Darnell, J.E.,Jr (1981) Transcriptional control in the production of liver-specific mRNAs. Cell, 23, 731-739.
13. Douarin, N.M. (1975) An experimental analysis of liver development. Med. Biol., 53, 427-455.
14. Foster, D.O., Ray, P.D. and Lardy, H.A. (1966) Studies on the mechanisms underlying adaptive changes in rat liver phosphoenolpyruvate carboxykinase. Biochemistry, 5, 555-562.
15. Gearing, D.P., Thut, C.J., VandeBos, T., Gimpel, S.D., Delaney, P.B., King, J., Price, V., Cosman, D. and Beckmann, M.P. (1991) Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130. EMBO J., 10, 2839-2848.
16. Gearing, D.P. et al (1992) The IL-6 signal transducer, gp130: an oncostatin M receptor and affinity converter for the LIF receptor Science, 255, 1434-1437.
17. Greengard, O. (1970) The developmental formation of enzymes in rat liver. In Litwack, G. (ed.), Biochemical Actions of Hormones. Academic Press Inc., New York, pp. 53-87.
18. Grove, R.I., Eberhardt, C., Abid, S., Mazzucco, C., Liu, J., Kiener, P., Todaro, G. and Shoyab, M. (1993) Oncostatin M is a mitogen for rabbit vascular smooth muscle cells. Proc. Natl Acad. Sci. USA, 90, 823-827.
19. Haber, B.A., Chin, S., Chuang, E., Buikhuisen, W., Naji, A. and Taub, R. (1995) High levels of glucose-6-phosphatase gene and protein expression reflect an adaptive response in proliferating liver and diabetes. J. Clin. Invest., 95, 832-841.
20. Hilberg, F., Aguzzi, A., Howells, N. and Wagner, E.F. (1993) c-jun is essential for normal mouse development and hepatogenesis. Nature, 365, 179-181.
21. Ho, K.K.W., Cake, M.H., Yeoh, G.C.T and Oliver, I.T. (1981) Insulin antagonism of glucocorticoid induction of tyrosine aminotransferase in cultured fetal hepatocytes. Eur. J. Biochem., 118, 137-142.
22. Houssaint, E. (1980) Differentiation of the mouse hepatic primordium. I. An analysis of tissue interactions in hepatocyte differentiation. Cell Differ., 9, 269-279.
23. Hu, Z., Evarts, R.P., Fujio, K., Marsden, E.R. and Thorgeirsson, S.S. (1993) Expression of hepatocyte growth factor and c-met genes during hepatic differentiation and liver development in the rat. Am. J. Pathol., 142, 1823-1830.
24. Ichihara, M., Hara, T., Kim, H., Murate, T. and Miyajima, A. (1997) Oncostatin M and leukemia inhibitory factor do not use the same functional receptor in mice (published erratum appears in Blood, 90, 2120). Blood, 90, 165-173.
25. Johnson, G.R. and Moore, M.A. (1975) Role of stem cell migration in initiation of mouse fetal liver haemopoiesis. Nature, 258, 726-728.
26. Kagoshima, M., Kinoshita, T., Matsumoto, K. and Nakamura, T. (1992) Developmental changes in hepatocyte growth factor mRNA and its receptor in rat liver, kidney and lung. Eur. J. Biochem., 210, 375-380.
27. Kawasaki, K. et al. (1997) Osteoclasts are present in gp130-deficient mice. Endocrinology, 138, 4959-4965.
28. Kinoshita, T., Tashiro, K. and Nakamura, T. (1989) Marked increase of HGF mRNA in non-parenchymal liver cells of rats treated with hepatotoxins. Biochem. Biophys. Res. Commun., 165, 1229-1234.
29. Lindberg, R.A., Juan, T.S., Welcher, A.A., Sun, Y., Cupples, R., Guthrie, B. and Fletcher, F.A. (1998) Cloning and characterization of a specific receptor for mouse oncostatin M. Mol. Cell. Biol., 18, 3357-3367.
30. Liu, J., Modrell, B., Aruffo, A., Marken, J.S., Taga, T., Yasukawa, K., Murakami, M., Kishimoto, T. and Shoyab, M. (1992) Interleukin-6 signal transducer gp130 mediates oncostatin M signaling. J. Biol. Chem., 267, 16763-16766.
31. Malik, N. et al. (1989) Molecular cloning, sequence analysis, and functional expression of a novel growth regulator, oncostatin M. Mol. Cell. Biol., 9, 2847-2853.
32. Matsumoto, K. and Nakamura, T. ( 1997) Hepatocyte growth factor (HGF) as a tissue organizer for organogenesis and regeneration. Biochem. Biophys. Res. Commun., 239, 639-644.
33. Michalopoulos, G.K. and DeFrances, M.C. (1997) Liver regeneration. Science, 276, 60-66.
34. Mosley, B., De Imus, C., Friend, D., Boiani, N., Thoma, B., Park, L.S. and Cosman, D. (1996) Dual oncostatin M (OSM) receptors. Cloning and characterization of an alternative signaling subunit conferring osm-specific receptor activation. J. Biol. Chem., 271, 32635-32643.
35. Mukouyama, Y., Hara, T., Xu, M., Tamura, K., Donovan, P.J., Kim, H., Kogo, H., Tsuji, K., Nakahata, T. and Miyajima, A. (1998) In vitro expansion of murine multipotential hematopoietic progenitors from the embryonic aorta-gonad-mesonephros region. Immunity, 8, 105-114.
36. Nagao, M., Nakamura, T. and Ichihara, A. (1986) Developmental control of gene expression of tryptophan 2,3-dioxygenase in neonatal rat liver. Biochim. Biophys. Acta, 867, 179-186.
37. Nakamura, T., Tomita, Y., Hirai, R., Yamaoka, K., Kaji, K. and Ichihara, A. (1985) Inhibitory effect of transforming growth factor-beta on DNA synthesis of adult rat hepatocytes in primary culture. Biochem. Biophys. Res. Commun., 133, 1042-1050.
38. Nawa, K., Nakamura, T., Kumatori, A., Noda, C. and Ichihara, A. (1986) Glucocorticoid-dependent expression of the albumin gene in adult rat hepatocytes. J. Biol. Chem., 261, 16883-16888.
39. Nemeth, A.M., Insull, W.,Jr and Flexner, L.B. (1953) Glycogenesis in the liver of the fetal guinea pig. J. Biol. Chem., 208, 765-776.
40. Nettleton, G.S. and Carpenter, A.M. (1977) Studies of the mechanism of the periodic acid-Schiff histochemical reaction for glycogen using infrared spectroscopy and model chemical compounds. Stain Technol., 52, 63-77.
41. Nishina, H. et al. (1999) Defective liver formation and liver cell apoptosis in mice lacking the stress signaling kinase SEK1/MEKK4. Development, 126, 505-516.
42. Noda, C., Ohguri, M. and Ichihara, A. (1990) Developmental and growth-related regulation of expression of serine dehydratase mRNA in rat liver. Biochem. Biophys. Res. Commun., 168, 335-342.
43. Noda, C., Fukushima, C., Fujiwara, T., Matsuda, K., Kobune, Y. and Ichihara, A. (1994) Developmental regulation of rat serine dehydratase gene expression: evidence for the presence of a represser in fetal hepatocytes. Biochim. Biophys. Acta, 1217, 163-173.
44. Noji, S., Tashiro, K., Koyama, E., Nohno, T., Ohyama, K., Taniguchi, S. and Nakamura, T. (1990) Expression of hepatocyte growth factor gene in endothelial and Kupffer cells of damaged rat livers, as revealed by in situ hybridization. Biochem. Biophys. Res. Commun., 173, 42-47.
45. Panduro, A., Shalaby, F. and Shafritz, D.A. (1987) Changing patterns of transcriptional and post-transcriptional control of liver-specific gene expression during rat development. Genes Dev., 1, 1172-1182.
46. Pennica, D. et al. (1995) Cardiotrophin-1. Biological activities and binding to the leukemia inhibitory factor receptor/gp130 signaling complex. J. Biol. Chem., 270, 10915-10922.
47. Philippidis, H. and Ballard, F.J. (1969) The development of glycogenesis in rat liver: experiments in vivo. Biochem. J., 113, 651-657.
48. Ramadori, G., Neubauer, K., Odenthal, M., Nakamura, T., Knittel, T., Schwogler, S. and Meyer zum Buschenfelde, K.H. (1992) The gene of hepatocyte growth factor is expressed in fat-storing cells of rat liver and is downregulated during cell growth and by transforming growth factor-beta. Biochem. Biophys. Res. Commun., 183, 739-742.
49. Richards, C.D., Brown, T.J., Shoyab, M., Baumann, H. and Gauldie, J. (1992) Recombinant oncostatin M stimulates the production of acute phase proteins in HepG2 cells and rat primary hepatocytes in vitro. J. Immunol., 148, 1731-1736.
50. Richards, C.D., Kerr, C., Tanaka, M., Hara, T., Miyajima, A., Pennica, D., Botelho, F. and Langdon, C.M. (1997) Regulation of tissue inhibitor of metalloproleinase-1 in fibroblasts and acute phase proteins in hepatocytes in vitro by mouse oncostatin M, cardiotrophin-1, and IL-6. J. Immunol., 159, 2431-2437.
51. Rose, T.M. and Bruce, A.G. (1991) Oncostatin M is a member of a cytokine family that includes leukemia-inhibitory factor, granulocyte colony-stimulating factor, and interleukin 6. Proc. Natl Acad. Sci. USA, 88, 8641-8645.
52. Sanchez, A., Alvarez, A.M., Benito, M. and Fabregat, J. (1995) Transforming growth factor beta modulates growth and differentiation of fetal hepatocytes in primary culture. J. Cell. Physiol., 165, 398-405.
53. Sassi, H., Pictet, R. and Grange, T. (1998) Glucocorticoids are insufficient for neonatal gene induction in the liver. Proc. Natl Acad. Sci. USA, 95, 5621-5625.
54. Shelly, L.L., Tynan, W., Schmid, W., Schutz, G. and Yeoh, G.C. (1989) Hepatocyte differentiation in vitro: initiation of tyrosine amino-transferase expression in cultured fetal rat hepatocytes. J. Cell Biol., 109, 3403-3410.
55. Shiojiri, N., Lemire, J.M. and Fausto, N. (1991) Cell lineages and oval cell progenitors in rat liver development. Cancer Res., 51, 2611-2620.
56. Taga, T. and Kishimoto, T. (1997) Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol., 15, 797-819.
57. Tanaka, M., Hara,T., Copeland, N.G., Gilbert, D.J., Jenkins, N.A. and Miyajima, A. (1999) Reconstitution of the functional mouse oncostatin M (OSM) receptor: molecular cloning of the mouse OSM receptor beta subunit. Blood, 93, 804-815.
58. Thoma, B., Bird, T.A., Friend, D.J., Gearing, D.P. and Dower, S.K. (1994) Oncostatin M and leukemia inhibitory factor trigger overlapping and different signals through partially shared receptor complexes. J. Biol. Chem., 269, 6215-6222.
59. Tilghman, S.M. and Belayew, A. (1982) Transcriptional control of the murine albumin/alpha-fetoprotein locus during development. Proc. Natl Acad. Sci. USA, 79, 5254-5257.
60. Wang, N.D., Finegold, M.J., Bradley, A., Ou, C.N., Abdelsayed, S.V., Wilde, M.D., Taylor, L.R., Wilson, D.R. and Darlington, G.J. (1995) Impaired energy homeostasis in C/EBP alpha knockout mice. Science, 269, 1108-1112.
61. Wijelath, E.S., Carlsen, B., Cole, T., Chen, J., Kothari, S. and Hammond, W.P. (1997) Oncostatin M induces basic fibroblast growth factor expression in endothelial cells and promotes endothelial cell proliferation, migration and spindle morphology. J. Cell Sci., 110, 871-879.
62. Yamane, A., Seetharam, L., Yamaguchi, S., Gotoh, N., Takahashi, J., Neufeld, G. and Shibuya, M. (1994) A new communication system between hepatocytes and sinusoidal endothelial cells in liver through vascular endothelial growth factor and F1t tyrosine kinase receptor family (F1t-1 and KDR/F1k-1). Oncogens, 9, 2683-2690.
63. Yasukawa, K., Futatsugi, K., Saito, T., Yawata, H., Narazaki, M., Suzuki, H., Taga, T. and Kishimoto, T. (1992) Association of recombinant soluble IL-6-signal transducer, gp130, with a complex of IL-6 and soluble IL-6 receptor, and establishment of an ELISA for soluble gp130. Immunol. Lett., 31, 123-130.
64. Yawata, H., Yasukawa, K., Natsuka, S., Murakami, M., Yamasaki, K., Hibi, M., Taga, T. and Kishimoto, T. (1993) Structure-function analysis of human IL-6 receptor: dissociation of amino acid residues required for IL-6-binding and for IL-6 signal transduction through gp130. EMBO J., 12, 1705-1712.
65. Yeung, D. and Oliver, I.T. (1967) Glycogenesis from amino acids in neonatal rat liver. Biochem. J., 103, 744-748.
66. Yoshida, K. et al. (1996) Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc. Natl Acad. Sci. USA, 93, 407-411.
67. Yoshimura, A., Ichihara, M., Kinjyo, I., Moriyama, M., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Hara, T. and Miyajima, A. (1996) Mouse oncostatin M: an immediate early gene induced by multiple cytokines through the JAK-STAT5 pathway. EMBO J., 15, 1055-1063.