The threshold of gp130-dependent STAT3 signaling is critical for normal regulation of hematopoiesis

Blood

Volumn 105, Issue 9, 2005, Pages 3512-3520

  Jenkins, Brendan J ^a   Roberts, Andrew W ^b   Najdovska, Meri ^b   Grail, Dianne ^b   Ernst, Matthias ^b  

^a ROYAL MELBOURNE HOSPITAL   (Australia)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GLYCOPROTEIN GP 130; INTERLEUKIN 6; STAT1 PROTEIN; STAT3 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMPOSITION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; HEMATOPOIESIS; HEMATOPOIETIC CELL; HETEROZYGOSITY; HOMEOSTASIS; LYMPH NODE; LYMPHADENOPATHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPLENOMEGALY; THROMBOCYTOSIS; THYMUS;

EID: 18244383058     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-09-3751     Document Type: Article

References (43)

1. Peters M, Muller AM, Rose-John S. Interleukin-6 and soluble interleukin-6 receptor: direct stimulation of gp130 and hematopoiesis. Blood. 1998;92:3495-3504.
2. Kishimoto T, Akira S, Narazaki M, Taga T. Interleukin-6 family of cytokines and gp130. Blood. 1995;86:1243-1254.
3. Yoshida K, Taga T, Saito M, et al. 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 U S A. 1996;93:407-411.
4. Escary JL, Perreau J, Dumenil D, Ezine S, Brulet P. Leukaemia inhibitory factor is necessary for maintenance of haematopoietic stem cells and thymocyte stimulation. Nature. 1993;363:361-364.
5. Bernad A, Kopf M, Kulbacki R, Weich N, Koehler G, Gutierrez-Ramos JC. Interleukin-6 is required in vivo for the regulation of stem cells and committed progenitors of the hematopoietic system. Immunity. 1994;1:725-731.
6. Ware CB, Horowitz MC, Renshaw BR, et al. Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development. 1995;121:1283-1299.
7. Shen MM, Skoda RC, Cardiff RD, Campos-Torres J, Leder P, Ornitz DM. Expression of LIF in transgenic mice results in altered thymic epithelium and apparent interconversion of thymic and lymph node morphologies. EMBO J. 1994;13:1375-1385.
8. Peters M, Schirmacher P, Goldschmitt J, et al. Extramedullary expansion of hematopoietic progenitor cells in interleukin (IL)-6-sIL-6R double transgenic mice. J Exp Med. 1997;185:755-766.
9. Hilton DJ, Hilton AA, Raicevic A, et al. Cloning of a murine IL-11 receptor alpha-chain; requirement for gp130 for high affinity binding and signal transduction. EMBO J. 1994;13:4765-4775.
10. Murakami M, Hibi M, Nakagawa N, et al. IL-6-induced homodimerization of gp130 and associated activation of a tyrosine kinase. Science. 1993;260:1808-1810.
11. Gearing DP, Thut CJ, VandeBos T, et al. Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130. EMBO J. 1991;10:2839-2848.
12. Mosley B, De Imus C, Friend D, et al. Dual oncostatin M (OSM) receptors. Cloning and characterization of an alternative signaling subunit conferring OSM-specific receptor activation. J Biol Chem. 1996;271:32635-32643.
13. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L. Interleukin-6-type cytokine signaling through the gp130/Jak/STAT pathway. Biochem J. 1998;334:297-314.
14. Gerhartz C, Heesel B, Sasse J, et al. Differential activation of acute phase response factor/STAT3 and STAT1 via the cytoplasmic domain of the interleukin 6 signal transducer gp130, I: definition of a novel phosphotyrosine motif mediating STAT1 activation. J Biol Chem. 1996;271:12991-12998.
15. Nicholson SE, De Souza D, Fabri LJ, et al. Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc Natl Acad Sci U S A. 2000;97:6493-6498.
16. Takahashi-Tezuka M, Yoshida Y, Fukada T, et al. Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Mol Cell Biol. 1998;18:4109-4117.
17. Tebbutt NC, Giraud A, Inglese M, et al. Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat Med. 2002;8:1089-1097.
18. Stahl N, Farruggella TJ, Boulton TG, Zhong Z, Darnell Jr JE, Yancopoulos GD. Choice of STATs and other substrates specified by modular tyrosine-based motifs in cytokine receptors. Science. 1995;267:1349-1353.
19. Lehmann U, Schmitz J, Weissenbach M, et al. SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J Biol Chem. 2003;278:661-671.
20. Krebs DL, Hilton DJ. SOCS proteins: negative regulators of cytokine signaling. Stem Cells. 2001;19:378-387.
21. Auernhammer CJ, Bousquet C, Melmed S. Autoregulation of pituitary corticotroph SOCS-3 expression: characterization of the murine SOCS-3 promoter. Proc Natl Acad Sci U S A. 1999;96:6964-6959.
22. Lee CK, Raz R, Gimeno R, et al. STAT3 is a negative regulator of granulopoiesis but is not required for G-CSF-dependent differentiation. Immunity. 2002;17:63-72.
23. Ohtani T, Ishihara K, Atsumi T, et al. Dissection of signaling cascades through gp130 in vivo: reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity. 2000;12:95-105.
24. Ernst M, Jenkins BJ. Acquiring signaling specificity from the cytokine receptor gp130. Trends Genet. 2004;20:23-32.
25. Takeda K, Kaisho T, Yoshida N, Takeda J, Kishimoto T, Akira S. Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell-specific Stat3-deficient mice. J Immunol. 1998;161:4652-4660.
26. Welte T, Zhang S, Wang T, et al. STAT3 deletion during hematopoiesis causes Crohn's disease-like pathogenesis and lethality: a critical role of STAT3 in innate immunity. Proc Natl Acad Sci U S A. 2003;100:1879-1884.
27. Benekli M, Baer MR, Baumann H, Wetzler M. Signal transducer and activator of transcription proteins in leukemias. Blood. 2003;101:2940-2954.
28. Jenkins BJ, Quilici C, Roberts AW, Grail D, Dunn AR, Ernst M. Hematopoietic abnormalities in mice deficient in gp130-mediated STAT signaling. Exp Hematol. 2002;30:1248-1256.
29. Takeda K, Noguchi K, Shi W, et al. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci U S A. 1997;94:3801-3804.
30. Jenkins BJ, Grail D, Inglese M, et al. Imbalanced gp130-dependent signaling in macrophages alters macrophage colony-stimulating factor responsiveness via regulation of c-fms expression. Mol Cell Biol. 2004;24:1453-1463.
31. Wen Z, Zhong Z, Darnell Jr JE. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell. 1995;82:241-250.
32. Maritano D, Sugrue ML, Tininini S, et al. The STAT3 isoforms alpha and beta have unique and specific functions. Nat Immunol. 2004;5:401-409.
33. Levy DE, Lee CK. What does Stat3 do? J Clin Invest. 2002;109:1143-1148.
34. Croker BA, Metcalf D, Robb L, et al. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity. 2004;20:153-165.
35. Croker BA, Krebs DL, Zhang JG, et al. SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol. 2003;4:540-545.
36. Ishibashi T, Shikama Y, Kimura H, et al. Thrombopoietic effects of interleukin-6 in long-term administration in mice. Exp Hematol. 1993;21:640-646.
37. Leonard JP, Quinto CM, Kozitza MK, Neben TY, Goldman SJ. Recombinant human interleukin-11 stimulates multilineage hematopoietic recovery in mice after a myelosuppressive regimen of sublethal irradiation and carboplatin. Blood. 1994;83:1499-1506.
38. Neben TY, Loebelenz J, Hayes L, et al. Recombinant human interleukin-11 stimulates megakaryocytopoiesis and increases peripheral platelets in normal and splenectomized mice. Blood. 1993;81:901-908.
39. Miller CL, Eaves CJ. Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability. Proc Natl Acad Sci U S A. 1997;94:13648-13653.
40. Tajima S, Tsuji K, Ebihara Y, et al. Analysis of interleukin 6 receptor and gp130 expressions and proliferative capability of human CD34+ cells. J Exp Med. 1996;184:1357-1364.
41. Audet J, Miller CL, Rose-John S, Piret JM, Eaves CJ. Distinct role of gp130 activation in promoting self-renewal divisions by mitogenically stimulated murine hematopoietic stem cells. Proc Natl Acad Sci U S A. 2001;98:1757-1762.
42. Oh IH, Eaves CJ. Overexpression of a dominant negative form of STAT3 selectively impairs hematopoietic stem cell activity. Oncogene. 2002;21:4778-4787.
43. Matsuda T, Nakamura T, Nakao K, et al. STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells. EMBO J. 1999;18:4261-4269.