Tumor necrosis factor α inhibits erythroid differentiation in human erythropoietin-dependent cells involving p38 MAPK pathway, GATA-1 and FOG-1 downregulation and GATA-2 upregulation

Biochemical Pharmacology

Volumn 76, Issue 10, 2008, Pages 1229-1239

  Buck, Isabelle ^a   Morceau, Franck ^a   Cristofanon, Silvia ^a   Heintz, Caroline ^a   Chateauvieux, Sébastien ^a   Reuter, Simone ^a   Dicato, Mario ^a   Diederich, Marc ^a  

^a LABORATOIRE DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE DU CANCER   (Luxembourg)

Author keywords

Erythropoiesis; FOG 1; GATA 1 2; p38; Tumor necrosis factor

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ALPHA GLOBIN; ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; GAMMA GLOBIN; GLYCOPHORIN A; MITOGEN ACTIVATED PROTEIN KINASE P38; PORPHOBILINOGEN DEAMINASE; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR NRF1; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL DIFFERENTIATION; ENZYME ACTIVATION; ERYTHROID CELL; ERYTHROPOIESIS; GENE EXPRESSION; HEMOGLOBIN SYNTHESIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

CELL DIFFERENTIATION; CELL LINE, TUMOR; DOWN-REGULATION; ERYTHROPOIESIS; ERYTHROPOIETIN; GATA1 TRANSCRIPTION FACTOR; GATA2 TRANSCRIPTION FACTOR; HUMANS; LEUKEMIA, ERYTHROBLASTIC, ACUTE; MAP KINASE SIGNALING SYSTEM; NUCLEAR PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 54049113367     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.08.025     Document Type: Article

References (49)

1. Knight K., Wade S., and Balducci L. Prevalence and outcomes of anemia in cancer: a systematic review of the literature. Am J Med 116 Suppl. 7A (2004) 11S-26S
2. Tas F., Eralp Y., Basaran M., Sakar B., Alici S., Argon A., et al. Anemia in oncology practice: relation to diseases and their therapies. Am J Clin Oncol 25 (2002) 371-379
3. Caro J.J., Salas M., Ward A., and Goss G. Anemia as an independent prognostic factor for survival in patients with cancer: a systemic, quantitative review. Cancer 91 (2001) 2214-2221
4. Andrews N.C. Anemia of inflammation: the cytokine-hepcidin link. J Clin Invest 113 (2004) 1251-1253
5. Rizzo J.D., Somerfield M.R., Hagerty K.L., Seidenfeld J., Bohlius J., Bennett C.L., et al. Use of epoetin and darbepoetin in patients with cancer: 2007 American Society of Hematology/American Society of Clinical Oncology clinical practice guideline update. Blood 111 (2008) 25-41
6. Bokemeyer C., Oechsle K., and Hartmann J.T. Anaemia in cancer patients: pathophysiology, incidence and treatment. Eur J Clin Invest 35 Suppl. 3 (2005) 26-31
7. Kurzrock R. The role of cytokines in cancer-related fatigue. Cancer 92 (2001) 1684-1688
8. Allen D.A., Breen C., Yaqoob M.M., and Macdougall I.C. Inhibition of CFU-E colony formation in uremic patients with inflammatory disease: role of IFN-gamma and TNF-alpha. J Investig Med 47 (1999) 204-211
9. Means Jr. R.T. Pathogenesis of the anemia of chronic disease: a cytokine-mediated anemia. Stem Cells 13 (1995) 32-37
10. Papadaki H.A., Kritikos H.D., Valatas V., Boumpas D.T., and Eliopoulos G.D. Anemia of chronic disease in rheumatoid arthritis is associated with increased apoptosis of bone marrow erythroid cells: improvement following anti-tumor necrosis factor-alpha antibody therapy. Blood 100 (2002) 474-482
11. Aggarwal B.B. Signalling pathways of the TNF superfamily: a double-edged sword. Nat Rev Immunol 3 (2003) 745-756
12. Szlosarek P.W., and Balkwill F.R. Tumour necrosis factor alpha: a potential target for the therapy of solid tumours. Lancet Oncol 4 (2003) 565-573
13. Szlosarek P., Charles K.A., and Balkwill F.R. Tumour necrosis factor-alpha as a tumour promoter. Eur J Cancer 42 (2006) 745-750
14. Dufour C., Corcione A., Svahn J., Haupt R., Poggi V., Beka'ssy A.N., et al. TNF-alpha and IFN-gamma are overexpressed in the bone marrow of Fanconi anemia patients and TNF-alpha suppresses erythropoiesis in vitro. Blood 102 (2003) 2053-2059
15. Xiao W., Koizumi K., Nishio M., Endo T., Osawa M., Fujimoto K., et al. Tumor necrosis factor-alpha inhibits generation of glycophorin A+ cells by CD34+ cells. Exp Hematol 30 (2002) 1238-1247
16. Hodges V.M., Rainey S., Lappin T.R., and Maxwell A.P. Pathophysiology of anemia and erythrocytosis. Crit Rev Oncol Hematol 64 (2007) 139-158
17. Wang H., Zhang Y., Cheng Y., Zhou Y., King D.C., Taylor J., et al. Experimental validation of predicted mammalian erythroid cis-regulatory modules. Genome Res 16 (2006) 1480-1492
18. Pevny L., Simon M.C., Robertson E., Klein W.H., Tsai S.F., D'Agati V., et al. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349 (1991) 257-260
19. Morceau F., Schnekenburger M., Dicato M., and Diederich M. GATA-1: friends, brothers, and coworkers. Ann NY Acad Sci 1030 (2004) 537-554
20. Leonard M., Brice M., Engel J.D., and Papayannopoulou T. Dynamics of GATA transcription factor expression during erythroid differentiation. Blood 82 (1993) 1071-1079
21. Tsai F.Y., and Orkin S.H. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 89 (1997) 3636-3643
22. Ferreira R., Ohneda K., Yamamoto M., and Philipsen S. GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol Cell Biol 25 (2005) 1215-1227
23. Lu S.J., Rowan S., Bani M.R., and Ben-David Y. Retroviral integration within the Fli-2 locus results in inactivation of the erythroid transcription factor NF-E2 in friend erythroleukemias: evidence that NF-E2 is essential for globin expression. Proc Natl Acad Sci USA 91 (1994) 8398-8402
24. Perkins A.C., Peterson K.R., Stamatoyannopoulos G., Witkowska H.E., and Orkin S.H. Fetal expression of a human Agamma globin transgene rescues globin chain imbalance but not hemolysis in EKLF null mouse embryos. Blood 95 (2000) 1827-1833
25. Swiers G., Patient R., and Loose M. Genetic regulatory networks programming hematopoietic stem cells and erythroid lineage specification. Dev Biol 294 (2006) 525-540
26. Morceau F., Schnekenburger M., Blasius R., Buck I., Dicato M., and Diederich M. Tumor necrosis factor alpha inhibits aclacinomycin A-induced erythroid differentiation of K562 cells via GATA-1. Cancer Lett 240 (2006) 203-212
27. Ribeil J.A., Zermati Y., Vandekerckhove J., Cathelin S., Kersual J., Dussiot M., et al. Hsp70 regulates erythropoiesis by preventing caspase-3-mediated cleavage of GATA-1. Nature 445 (2007) 102-105
28. Johnson R.A., Waddelow T.A., Caro J., Oliff A., and Roodman G.D. Chronic exposure to tumor necrosis factor in vivo preferentially inhibits erythropoiesis in nude mice. Blood 74 (1989) 130-138
29. Zon L.I., Youssoufian H., Mather C., Lodish H.F., and Orkin S.H. Activation of the erythropoietin receptor promoter by transcription factor GATA-1. Proc Natl Acad Sci USA 88 (1991) 10638-10641
30. Mignotte V., Eleouet J.F., Raich N., and Romeo P.H. Cis- and trans-acting elements involved in the regulation of the erythroid promoter of the human porphobilinogen deaminase gene. Proc Natl Acad Sci USA 86 (1989) 6548-6552
31. Grass J.A., Boyer M.E., Pal S., Wu J., Weiss M.J., and Bresnick E.H. GATA-1-dependent transcriptional repression of GATA-2 via disruption of positive autoregulation and domain-wide chromatin remodelling. Proc Natl Acad Sci USA 100 (2003) 8811-8816
32. La Ferla K., Reimann C., Jelkmann W., and Hellwig-Burgel T. Inhibition of erythropoietin gene expression signaling involves the transcription factors GATA-2 and NF-kappaB. FASEB J 16 (2002) 1811-1813
33. Nakano Y., Imagawa S., Matsumoto K., Stockmann C., Obara N., Suzuki N., et al. Oral administration of K-11706 inhibits GATA binding activity, enhances hypoxia-inducible factor 1 binding activity, and restores indicators in an in vivo mouse model of anemia of chronic disease. Blood 104 (2004) 4300-4307
34. Tsang A.P., Fujiwara Y., Hom D.B., and Orkin S.H. Failure of megakaryopoiesis and arrested erythropoiesis in mice lacking the GATA-1 transcriptional cofactor FOG. Genes Dev 12 (1998) 1176-1188
35. Cantor A.B., Iwasaki H., Arinobu Y., Moran T.B., Shigematsu H., Sullivan M.R., et al. Antagonism of FOG-1 and GATA factors in fate choice for the mast cell lineage. J Exp Med 205 (2008) 611-624
36. Pal S., Cantor A.B., Johnson K.D., Moran T.B., Boyer M.E., Orkin S.H., et al. Coregulator-dependent facilitation of chromatin occupancy by GATA-1. Proc Natl Acad Sci USA 101 (2004) 980-985
37. Uddin S., Ah-Kang J., Ulaszek J., Mahmud D., and Wickrema A. Differentiation stage-specific activation of p38 mitogen-activated protein kinase isoforms in primary human erythroid cells. Proc Natl Acad Sci USA 101 (2004) 147-152
38. Jacobs-Helber S.M., Ryan J.J., and Sawyer S.T. JNK and p38 are activated by erythropoietin (EPO) but are not induced in apoptosis following EPO withdrawal in EPO-dependent HCD57 cells. Blood 96 (2000) 933-940
39. Nagata Y., Takahashi N., Davis R.J., and Todokoro K. Activation of p38 MAP kinase and JNK but not ERK is required for erythropoietin-induced erythroid differentiation. Blood 92 (1998) 1859-1869
40. Tamura K., Sudo T., Senftleben U., Dadak A.M., Johnson R., and Karin M. Requirement for p38alpha in erythropoietin expression: a role for stress kinases in erythropoiesis. Cell 102 (2000) 221-231
41. Yuasa T., Ohno S., Kehrl J.H., and Kyriakis J.M. Tumor necrosis factor signaling to stress-activated protein kinase (SAPK)/Jun NH2-terminal kinase (JNK) and p38. Germinal center kinase couples TRAF2 to mitogen-activated protein kinase/ERK kinase kinase 1 and SAPK while receptor interacting protein associates with a mitogen-activated protein kinase kinase kinase upstream of MKK6 and p38. J Biol Chem 273 (1998) 22681-22692
42. Wei G.H., Zhao G.W., Song W., Hao D.L., Lv X., Liu D.P., et al. Mechanisms of human gamma-globin transcriptional induction by apicidin involves p38 signaling to chromatin. Biochem Biophys Res Commun 363 (2007) 889-894
43. Stassen M., Klein M., Becker M., Bopp T., Neudorfl C., Richter C., et al. p38 MAP kinase drives the expression of mast cell-derived IL-9 via activation of the transcription factor GATA-1. Mol Immunol 44 (2007) 926-933
44. Towatari M., Ciro M., Ottolenghi S., Tsuzuki S., and Enver T. Involvement of mitogen-activated protein kinase in the cytokine-regulated phosphorylation of transcription factor GATA-1. Hematol J 5 (2004) 262-272
45. Crossley M., and Orkin S.H. Phosphorylation of the erythroid transcription factor GATA-1. J Biol Chem 269 (1994) 16589-16596
46. Partington G.A., and Patient R.K. Phosphorylation of GATA-1 increases its DNA-binding affinity and is correlated with induction of human K562 erythroleukaemia cells. Nucleic Acids Res 27 (1999) 1168-1175
47. Hernandez-Hernandez A., Ray P., Litos G., Ciro M., Ottolenghi S., Beug H., et al. Acetylation and MAPK phosphorylation cooperate to regulate the degradation of active GATA-1. EMBO J 25 (2006) 3264-3274
48. De Maria R., Zeuner A., Eramo A., Domenichelli C., Bonci D., Grignani F., et al. Negative regulation of erythropoiesis by caspase-mediated cleavage of GATA-1. Nature 401 (1999) 489-493
49. Miwatashi S., Arikawa Y., Kotani E., Miyamoto M., Naruo K., Kimura H., et al. Novel inhibitor of p38 MAP kinase as an anti-TNF-alpha drug: discovery of N-[4-[2-ethyl-4-(3-methylphenyl)-1,3-thiazol-5-yl]-2-pyridyl]benzamide (TAK-715) as a potent and orally active anti-rheumatoid arthritis agent. J Med Chem 48 (2005) 5966-5979