Experimental Hematology
Volume 36, Issue 7 , Pages 786-798 , July 2008

Socs3 maintains the specificity of biological responses to cytokine signals during granulocyte and macrophage differentiation

  • Ben A. Croker

      Affiliations

    • Cancer and Haematology Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • Drs. Croker, Mielke, and Wormald contributed equally to this work.
    • ,
  • Lisa A. Mielke

      Affiliations

    • Cancer and Haematology Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • Divisions of Molecular Medicine, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • Drs. Croker, Mielke, and Wormald contributed equally to this work.
    • ,
  • Sam Wormald

      Affiliations

    • Cancer and Haematology Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • Bioinformatics, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • Drs. Croker, Mielke, and Wormald contributed equally to this work.
    • ,
  • Donald Metcalf

      Affiliations

    • Cancer and Haematology Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • ,
  • Hiu Kiu

      Affiliations

    • Cancer and Haematology Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • ,
  • Warren S. Alexander

      Affiliations

    • Cancer and Haematology Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • ,
  • Douglas J. Hilton

      Affiliations

    • Cancer and Haematology Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • Divisions of Molecular Medicine, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • ,
  • Andrew W. Roberts

      Affiliations

    • Cancer and Haematology Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria, Australia
    • Corresponding Author InformationOffprint requests to: Andrew W. Roberts, M.D., Ph.D., The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria, 3050, Australia

Received 29 November 2007 ,Revised 11 February 2008 ,Accepted 11 February 2008.

References 

  1. Iwasaki H, Mizuno S, Arinobu Y, et al. The order of expression of transcription factors directs hierarchical specification of hematopoietic lineages. Genes Dev. 2006;20:3010–3021
  2. Rosenbauer F, Tenen DG. Transcription factors in myeloid development: balancing differentiation with transformation. Nat Rev Immunol. 2007;7:105–117
  3. Starr R, Willson TA, Viney EM, et al. A family of cytokine-inducible inhibitors of signaling. Nature. 1997;387:917–921
  4. Croker BA, Krebs DL, Zhang JG, et al. SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol. 2003;4:540–545
  5. 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
  6. Yasukawa H, Ohishi M, Mori H, et al. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol. 2003;4:551–556
  7. Lang R, Pauleau AL, Parganas E, et al. SOCS3 regulates the plasticity of gp130 signaling. Nat Immunol. 2003;4:546–550
  8. Robb L, Boyle K, Rakar S, et al. Genetic reduction of embryonic leukemia-inhibitory factor production rescues placentation in SOCS3-null embryos but does not prevent inflammatory disease. Proc Natl Acad Sci U S A. 2005;102:16333–16338
  9. Ridley AJ. Membrane ruffling and signal transduction. Bioessays. 1994;16:321–327
  10. Mori H, Hanada R, Hanada T, et al. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat Med. 2004;10:739–743
  11. Hilton DJ, Richardson RT, Alexander WS, et al. Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc Natl Acad Sci U S A. 1998;95:114–119
  12. Yoshimura A, Ohkubo T, Kiguchi T, et al. A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J. 1995;14:2816–2826
  13. Zhang JG, Farley A, Nicholson SE, et al. The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc Natl Acad Sci U S A. 1999;96:2071–2076
  14. Boyle K, Egan P, Rakar S, et al. The SOCS box of suppressor of cytokine signaling-3 contributes to the control of G-CSF responsiveness in vivo. Blood. 2007;110:1466–1474
  15. Kamura T, Sato S, Haque D, et al. The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev. 1998;12:3872–3881
  16. Babon JJ, McManus EJ, Yao S, et al. The structure of SOCS3 reveals the basis of the extended SH2 domain function and identifies an unstructured insertion that regulates stability. Mol Cell. 2006;22:205–216
  17. 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
  18. Hortner M, Nielsch U, Mayr LM, Johnston JA, Heinrich PC, Haan S. Suppressor of cytokine signaling-3 is recruited to the activated granulocyte-colony stimulating factor receptor and modulates its signal transduction. J Immunol. 2002;169:1219–1227
  19. Nicholson SE, Willson TA, Farley A, et al. Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibition of LIF and IL-6 signal transduction. EMBO J. 1999;18:375–385
  20. Schmitz J, Weissenbach M, Haan S, Heinrich PC, Schaper F. SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J Biol Chem. 2000;275:12848–12856
  21. Akbarzadeh S, Ward AC, McPhee DO, Alexander WS, Lieschke GJ, Layton JE. Tyrosine residues of the granulocyte colony-stimulating factor receptor transmit proliferation and differentiation signals in murine bone marrow cells. Blood. 2002;99:879–887
  22. Ward AC, Smith L, de Koning JP, van Aesch Y, Touw IP. Multiple signals mediate proliferation, differentiation, and survival from the granulocyte colony-stimulating factor receptor in myeloid 32D cells. J Biol Chem. 1999;274:14956–14962
  23. Metcalf D. Clonal culture of hemopoietic cells : techniques and applications. Amsterdam: Elsevier; 1984;
  24. Roberts AW, Metcalf D. Granulocyte colony-stimulating factor induces selective elevations of progenitor cells in the peripheral blood of mice. Exp Hematol. 1994;22:1156–1163
  25. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19:185–193
  26. Metcalf D, Nicola NA. Direct proliferative actions of stem cell factor on murine bone marrow cells in vitro: effects of combination with colony-stimulating factors. Proc Natl Acad Sci U S A. 1991;88:6239–6243
  27. Fattori E, Cappelletti M, Costa P, et al. Defective inflammatory response in interleukin 6-deficient mice. J Exp Med. 1994;180:1243–1250
  28. Hilbert DM, Kopf M, Mock BA, Kohler G, Rudikoff S. Interleukin 6 is essential for in vivo development of B lineage neoplasms. J Exp Med. 1995;182:243–248
  29. Schirmacher P, Peters M, Ciliberto G, et al. Hepatocellular hyperplasia, plasmacytoma formation, and extramedullary hematopoiesis in interleukin (IL)-6/soluble IL-6 receptor double- transgenic mice. Am J Pathol. 1998;153:639–648
  30. 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
  31. Lord BI, Bronchud MH, Owens S, et al. The kinetics of human granulopoiesis following treatment with granulocyte colony-stimulating factor in vivo. Proc Natl Acad Sci U S A. 1989;86:9499–9503
  32. Lord BI, Molineux G, Pojda Z, Souza LM, Mermod JJ, Dexter TM. Myeloid cell kinetics in mice treated with recombinant interleukin-3, granulocyte colony-stimulating factor (CSF), or granulocyte-macrophage CSF in vivo. Blood. 1991;77:2154–2159
  33. Cartwright P, McLean C, Sheppard A, Rivett D, Jones K, Dalton S. LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development. 2005;132:885–896
  34. Wilson A, Murphy MJ, Oskarsson T, et al. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 2004;18:2747–2763
  35. Tian SS, Lamb P, Seidel HM, Stein RB, Rosen J. Rapid activation of the STAT3 transcription factor by granulocyte colony-stimulating factor. Blood. 1994;84:1760–1764
  36. Zhong Z, Wen Z, Darnell JE. STAT3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science. 1994;264:95–98
  37. Numata A, Shimoda K, Kamezaki K, et al. Signal transducers and activators of transcription 3 augments the transcriptional activity of CCAAT/enhancer-binding protein alpha in granulocyte colony-stimulating factor signaling pathway. J Biol Chem. 2005;280:12621–12629
  38. Dahl R, Walsh JC, Lancki D, et al. Regulation of macrophage and neutrophil cell fates by the PU.1:C/EBPalpha ratio and granulocyte colony-stimulating factor. Nat Immunol. 2003;4:1029–1036
  39. Wang D, D'Costa J, Civin CI, Friedman AD. C/EBPalpha directs monocytic commitment of primary myeloid progenitors. Blood. 2006;108:1223–1229
  40. Zhang DE, Hetherington CJ, Meyers S, et al. CCAAT enhancer-binding protein (C/EBP) and AML1 (CBF alpha2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol Cell Biol. 1996;16:1231–1240
  41. Smith LT, Hohaus S, Gonzalez DA, Dziennis SE, Tenen DG. PU.1 (Spi-1) and C/EBP alpha regulate the granulocyte colony-stimulating factor receptor promoter in myeloid cells. Blood. 1996;88:1234–1247
  42. Heath V, Suh HC, Holman M, et al. C/EBPalpha deficiency results in hyperproliferation of hematopoietic progenitor cells and disrupts macrophage development in vitro and in vivo. Blood. 2004;104:1639–1647
  43. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ, Tenen DG. Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc Natl Acad Sci U S A. 1997;94:569–574
  44. Jones LC, Lin ML, Chen SS, et al. Expression of C/EBPbeta from the C/ebpalpha gene locus is sufficient for normal hematopoiesis in vivo. Blood. 2002;99:2032–2036
  45. Natsuka S, Akira S, Nishio Y, et al. Macrophage differentiation-specific expression of NF-IL6, a transcription factor for interleukin-6. Blood. 1992;79:460–466
  46. Radomska HS, Huettner CS, Zhang P, Cheng T, Scadden DT, Tenen DG. CCAAT/enhancer binding protein alpha is a regulatory switch sufficient for induction of granulocytic development from bipotential myeloid progenitors. Mol Cell Biol. 1998;18:4301–4314
  47. Scott LM, Civin CI, Rorth P, Friedman AD. A novel temporal expression pattern of three C/EBP family members in differentiating myelomonocytic cells. Blood. 1992;80:1725–1735
  48. Hohaus S, Petrovick MS, Voso MT, Sun Z, Zhang DE, Tenen DG. PU.1 (Spi-1) and C/EBP alpha regulate expression of the granulocyte-macrophage colony-stimulating factor receptor alpha gene. Mol Cell Biol. 1995;15:5830–5845
  49. Aperlo C, Pognonec P, Stanley ER, Boulukos KE. Constitutive c-ets2 expression in M1D+ myeloblast leukemic cells induces their differentiation to macrophages. Mol Cell Biol. 1996;16:6851–6858
  50. Brocke-Heidrich K, Ge B, Cvijic H, et al. BCL3 is induced by IL-6 via STAT3 binding to intronic enhancer HS4 and represses its own transcription. Oncogene. 2006;25:7297–7304
  51. Bohmann D, Bos TJ, Admon A, Nishimura T, Vogt PK, Tjian R. Human proto-oncogene c-jun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1. Science. 1987;238:1386–1392
  52. Rauscher FJ, Sambucetti LC, Curran T, Distel RJ, Spiegelman BM. Common DNA binding site for Fos protein complexes and transcription factor AP-1. Cell. 1988;52:471–480
  53. Franza BR, Rauscher FJ, Josephs SF, Curran T. The Fos complex and Fos-related antigens recognize sequence elements that contain AP-1 binding sites. Science. 1988;239:1150–1153
  54. Rauscher FJ, Cohen DR, Curran T, et al. Fos-associated protein p39 is the product of the jun proto-oncogene. Science. 1988;240:1010–1016
  55. Chiu R, Boyle WJ, Meek J, Smeal T, Hunter T, Karin M. The c-Fos protein interacts with c-Jun/AP-1 to stimulate transcription of AP-1 responsive genes. Cell. 1988;54:541–552
  56. Sassone-Corsi P, Lamph WW, Kamps M, Verma IM. Fos-associated cellular p39 is related to nuclear transcription factor AP-1. Cell. 1988;54:553–560
  57. Schuringa JJ, Timmer H, Luttickhuizen D, Vellenga E, Kruijer W. c-Jun and c-Fos cooperate with STAT3 in IL-6-induced transactivation of the IL-6 response element (IRE). Cytokine. 2001;14:78–87
  58. Higashi N, Kunimoto H, Kaneko S, et al. Cytoplasmic c-Fos induced by the YXXQ-derived STAT3 signal requires the co-operative MEK/ERK signal for its nuclear translocation. Genes Cells. 2004;9:233–242
  59. Clarkson RW, Boland MP, Kritikou EA, et al. The genes induced by signal transducer and activators of transcription (STAT)3 and STAT5 in mammary epithelial cells define the roles of these STATs in mammary development. Mol Endocrinol. 2006;20:675–685

PII: S0301-472X(08)00074-X

doi: 10.1016/j.exphem.2008.02.008

Experimental Hematology
Volume 36, Issue 7 , Pages 786-798 , July 2008

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