Leukemia inhibitory factor, a potent cardiac hypertrophic cytokine, activates the JAK/STAT pathway in rat cardiomyocytes

Circulation Research

Volumn 81, Issue 5, 1997, Pages 656-663

  Kodama, Hiroaki ^a   Fukuda, Keiichi ^a   Pan, Jing ^a   Makino, Shinji ^a   Baba, Akiyasu ^a   Hori, Shingo ^a   Ogawa, Satoshi ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

Cardiac hypertrophy; JAK kinase; Leukemia inhibitory factor; Signal transducer(s) and activator(s) of transcription; Signal transduction

Indexed keywords

CYTOKINE; GLYCOPROTEIN GP 130; LEUKEMIA INHIBITORY FACTOR; PHOSPHOTRANSFERASE; PROTEIN KINASE; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

EID: 0030696081     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.81.5.656     Document Type: Article

References (59)

1. Kishimoto T, Taga T, Akira S, Cytokine signal transduction. Cell. 1994;76:253-262.
2. Simon MI, Strathman MP, Gautam N. Diversity of G protein in signal transduction. Science. 1991;252:802-808.
3. Marshal CJ. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell. 1995;8:179-185.
4. 1adrenergic receptor interaction. Circ Res. 1985;56:884-894.
5. Schneider M, Parker TG. Cardiac myocyles for the action of peptide growth factors. Circulation. 1989;80:219-233.
6. Parker TG, Schneider MD. Peptide growth factor can provoke 'fetal' contractile protein gene expression in rat cardiac myocytes. J Clin Invest. 1990;85:507-514.
7. Kardami E, Fancdrich RR. Basic fibroblast growth factor in atria and ventricles of the vertebrate heart. J Cell Biol. 1989;109: 1865-1875.
8. Fukada K. Purification and partial characterization of a cholinergic neuronal differentiation factor. Pror Natl Acad Sci U S A. 1985;82: 8795-8799.
9. Yamamori T, Fukada K, Aebersold R, Korsching S, Fann M, Patterson PH. The cholinergic neuronal differentiation factor from heart cell is identical to leukemia inhibitory factor. Science, 1989; 246:1412-1416.
10. Pennica D, Shaw KJ, Swanson TA, Moore MW, Shelton DL, Zioncheck KA, Rosenthal A, Taga T, Paoni NF, Wood WI. Cardiotrophin-1. J Biol Chem. 1995;270:10915-10922.
11. Pennica D, King KL, Shaw KJ, Luis E, Rullamas E, Luoh SM, Decabonne WC, Knutzon DS, Yen R, Chien KR, Baker JB, Wood WI. Expression cloning of cardiotrophin-1, a cytokine that induces cardiac hypertrophy. Proc Natl Acad Sci U S A. 1995;92:1142-1146.
12. Metcalf D. The leukemia inhibitory factor. Int J Cell Cloning. 1991; 9:95-108.
13. Ip NY, Nye SH, Boulton TG, Davis S, Taga T, Li Y, Birren SJ, Yasuhara K, Kishimoto T, Andersen DJ. CNTF and LIF act neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component of gp130. Cell. 1992;69: 1121-1132.
14. Wijdenes J, Heinrich PC, Muller-Newen G, Roche C, Gu ZG, Clement C, Klein B. Interleukin-6 signal transducer gp130 has specific binding sites for different cytokines as determined by antagonistic and agonistic anti-gp130 monoclonal antibodies. Eur J Immunol. 1995;25:3474-3481.
15. Gearing DP, Thut CJ, Vanderbos T, Gimpel SD, Pamela BPB, King J, Price V, Cosrnan D, Beckman MP. Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp 130. EMBO J. 1991;10:2839-2848.
16. Guschin D, Rogers N, Briseoe J, Witthuhn B, Watling D, Horn F, Pellegrini S, Yasukawa K, Heinrich P, Stark GR, Ihle JN, Kerr IM. A major role for the protein kinase JAK1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO J. 1995; 14:1421-1429.
17. Ihle JN. Cytokine receptor signalling. Nature. 1995;377:591-594.
18. Narazaki M, Wittthuhn RA, Yoshida K, Silvernnoinen O, Yasukawa K, Ihle JN, Kishimoto T, Taga T, Activation of JAK2 kinase mediated by the interleukin 6 signal transducer gp130. Proc Natl Acad Sci U S A. 1994;91:2285-2289.
19. Boulton TG, Zhong Z, Wen Z, Darnell JE, Stahl N, Yanocopolos GD. STAT3 activation by cytokine utilizing gp130 and related transducers involves a secondary modification requiring an H7sensitive kinase. Proc Natl Acad Sci U S A. 1995;92:6915-6919.
20. Johnston JA, Bacon CM, Finbloom DS, Rees RC, Kaplan D, Shibuya K, Ortaldo JR, Gupla S, Chen YQ, Giri JD, O'Shea JJ. Tyrosine phosphorylation and activation of STAT5, STAT3, and Janus kinase by interleukin 2 and 15. Proc Natl Acad Sci U S A. 1995;92:8705-8709.
21. Shuai K, Shindler C, Prezioso YR, Darnel JE Jr. Activation of transcription by IFN-γ: tyrosine phosphorylation of a 91 kD DNA binding protein. Science.1992;258:1808-1812.
22. Shuai K, Stark GR, Kerr IM, Darnel JE Jr. A single phosphotyrosine residue of Stat91 required for gene activation by Interferon-γ. Science. 1993;261:1744-1746.
23. Boulton TG, Stahl N, Yancopoulous GD. Ciliary neurotrophic factor/leukemia inhibitory factor/interleukin 6/oncostatin M family of cytokines induces tyrosine phosphorylation of a common set of proteins overlapping those induced by other cytokines and growth factors. J Biol Chem. 1994;269:11648-11655.
24. Wang YAF. Interleukin-6 and ciliary neurotrophic factor trigger Janus kinase activation and early gene response in rat hepatocytes. Gene. 1995;162:285-289.
25. Baumann H, Ziegler SF, Mosley B, Morella KK, Pajovic S, Gearing DP. Reconstitution of the response to leukemia inhibitory factor, oncostalin M, and ciliary neurotrophic factor in hepatoma cells. J Biol Chem. 1993;268:8414-8417.
26. Thoma B, Bird TA, Friend DJ, Gearing DP, Dower SK. Oncostatin M and leukemia inhibitory factor trigger overlapping and different signals through partially shared receptor. J Biol Chem. 1994;269: 6215-6222.
27. Ip NY, Nye S, Boulton TG, Davis S, Taga T, Li Y, Birren SJ, Yasukawa K, Kishimoto T, Anderson DJ, Stahl N, Yancopoulous GD. CNTF and LIF act on neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component gp130. Cell. 1992;69:1121-1132.
28. Stahl N, Boulton TG, Farruggella T, Ip NY, Davis S, Witthuhn B, Quelle FW, Silvenoinen O, Barbieri G, Pellegrini S, Ihle JN, Yancopoulous GD. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-lL-6 beta receptor components. Science. 1994; 263:92-95.
29. Stahl N. Farruggella T, Boulton TG, Zhong Z, Darnell JE, Yancopoulous GD. Choice of STATs and other substrates specified by modular tyrosine-based motif in cytokine receptors. Science. 1995; 267:1349-1353.
30. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 19983;11:1475-1489.
31. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
32. Hayes TE, Kitchen AM, Cochran BH. Inducible binding of a factor to the c-fos regulatory region. Proc Natl Acad Sci U S A. 1987;84: 1272-1276.
33. Gearing DP, Comeau MR, Friend DJ, Gimpel SD, Thut CJ, McGourty J, Brasher KK, King JA, Giliis S, Mosley B, Ziegler SF, Cosman D. The IL-6 signal transducer, gp130: an oncostatin M receptor and affinity converter for the LIF receptor. Science. 1992; 255:1434-1437.
34. Wijdennes J, Heinrich PC, Muller-Newen G, Roche C, Gu ZJ, Celement C, Klein B. Interleukin-6 signal transducer gp130 has specific binding sites for different cytokines as determined by antagonistic and agonistic anti-gp130 monoclonal antibodies. Eur J Immunol. 1995;25:3474-3481.
35. Luttincken C, Wegenka UM, Yuan J, Buschmann J, Schidler C, Ziemiecki A, Harpur AG, Wilks AF, Yasukawa K, Taga T, Kishimoto T, Barbieri G, Pellegrini S, Sendtner M, Heinrich PC, Horn F. Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science. 1994;263:89-94.
36. Sadowski HB, Shuai K, Darnell JE, Gilman MZ. A common nuclear signal transduction pathway activated by growth factor cytokine receptors. Science. 1993;26l:1739-1744.
37. Campbell GS, Meyer DJ, Raz R, Levy DE, Schwartz J, Carter-Su C. Activation of acute response factor (APRF)/Stat3 transcription factor by growth hormone. J Biol Chem. 1995;270:3974-3979.
38. Douglas W, Leaman SP, Flickinger TW, Commane MA, Schlessinger J, Kerr IM, Levy DE, Stark GR. Roles of JAKs in activation of STATs and stimulation of c-fos gene expression by epidermal growth factor. Mol Cell Biol. 1996;16:369-375.
39. Quelle FW, Thierfelder W, Witthuhn BA, Tang B, Cohen S, Ihle JM. Phosphorylation and activation of the DNA binding activity of purified STAT1 by the janus protein-tyrosine kinase and the epidermal growth factor receptor. J Biol Cham. 1995;270:20775-20780.
40. Sakatsume M, Igarashi K, Winestock KD, Garotta G, Larner AC, Finbloom DS. The JAK kinases differentially associate with the α and β chains of the interferon-γ receptor to form a functional receptor unit capable of activating STAT transcription factors. J Biol Chem. 1995;270:17523-17534.
41. Decker T, Lew DJ, Mirkovitch J, Darnell JE. Cytoplasmic activation of GAF, an IFN-γ regulated DNA-binding factor. EMBO J. 1991;10:927-932.
42. Hilton DJ, Nicola NA, Metcalf D. Specific binding of murine leukemia inhibitory factor to normal and lecukemic monocytic cells. Proc Natl Acad Sci U S A. 1988;85:5971-5975.
43. Tanigawa T, Nicola N, McArthur GA, Strasser A, Begley CG. Differential regulation of macrophage differentiation in response to leukemia inhibitory factor/oncostatin-M/interleukin-6: the effect of enforced expression of the SCL transcription factor. Blood. 1995; 85:379-390.
44. Burnstein SA, Mei RL, Henthorn J, Turner K. Leukemia inhibitory actor and interleukin-11 promote maturation of murine and human megakaryocyte production in vitro. J Cell Physiol. 1992;153:305-312.
45. Beadling C, Guschin D, Witthuhn BA, Ziemiecki A, Ihle JN, Kerr IM, Cantrell DA. Activation of JAK kinase and interferon α, but not the T cell antigen receptor, in human T lymphocytes. EMBO J. 1994;13:5605-5615.
46. Baumann H, Symes AJ, Comeau MR, Morella KK, Wang Y, Friend D, Ziegler F, Finks JS, Gearing DP. Multiple regions within the cytoplasmic domains of the leukemia inhibitory factor and gp130 cooperate in signal transduction in hepatic and neuronal cells. Mol Cell Biol. 1994;14:138-146.
47. Li M, Sendtner M., Smith A, Essential function of LIF receptor in motor neurons. Nature. 1995;378:724-727.
48. Metcalf D, Gough NM, Stahl J, Hilton DJ, Nicola NA. Leukemia inhibitory factor. In: Aggarwal BB, Gutterman JU, eds. Human Cytokines: Handbook for Basic and Clinical Researchers. Cambridge, Mass: Blackwell Scientific; 1991.
49. Marchall MK, Doerrler W, Feingold KR, Grunfeld C. Leukemia inhibitory factor induces changes in lipid metabolism in cultured adipocyte. Endocrinology. 1994;135:141-147.
50. Akita S, Webster J, Ren SG, Takino H, Said J, Melmed S. Human and murine pituitary expression of leukemia inhibitory factor: novel intrapituitary regulation of adrenocorticotropin hormone synthesis and secretion. J Clin Invest. 1995;95:1288-1298.
51. Williams RL, Hilton DJ, Pease S, Willison TA, Stewart CL, Gearing DP, Wagner EF, Metcalf D, Nicola NA, Gough AM. Myeloid leukemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature. 1988;336:684-687.
52. Moreau JF, Donaldson DD, Bennett F, Witck-Giannotti F, Clark SC, Wong GG. Leukemia inhibitory factor is identical to the myeloid growth factor human interleukin for DA cells. Nature. 1988;336:690-696.
53. Escary JL, Perreeau J, Dumenil D, Ezine S, Brulet P. Leukemia inhibitory factor is necessary for maintenance of haematopoietic stem cells and thymocyte stimulation. Nature. 1993;363:361-364.
54. Metcalf D, Hilton D, Nicola NA. Leukemia inhibitory actor can potentiate murine megakaryocyte production in vitro. Blood. 1991; 77:2150-2153.
55. Tomida M, Yamamoto-Yamaguchi Y, Hozumi M. Purification of a factor differentiation of mouse myeloid leukemic M1 cells from conditioned medium of mouse fibroblast L929 cells. J Biol Chem. 1984;259:10928-10982.
56. Yoshida K, Taga M, Suematsu S, Kumanogoh A, Tanaka T, Fujiwara H, Hirata M, Yamagami T, Nakahata T, Hirabayashi T, Yoneda Y, Tanaka K, Wang WZ, Mori C, Shiota K, Yoshida N, Kishimoto T. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytekines, leads to myocardial and hematological disorders. Proc Natl Acad Sci U S A. 1996;93:407-411.
57. Hirota H, Yoshida K, Kishimoto T, Taga T. Continuous activation of gp130, a signal-transducing component for interleukin 6-related cytokines, causes myocardial hypertrophy in mice. Proc Natl Acad Sci U S A. 1995;92:4862-4866.
58. Peters M, Roeb E, Pennica D, Meyer KH, Rose-John S. A new hepatocyte stimulating factor: cardiotrophin-1. FEBS Lett. 1995; 372:177-180.
59. Kunisada K, Hirota H, Fujio Y, Matsui H, Tani Y, Takihara KY, Kishimoto T. Activation of JAK-STAT and MAP kinases by leukemia inhibitory factor through gp130 in cardiac myocytes. Circulation. 1996;94:2626-2632.