Btk Is Required for an Efficient Response to Erythropoietin and for SCF-controlled Protection against TRAIL in Erythroid Progenitors

Journal of Experimental Medicine

Volumn 199, Issue 6, 2004, Pages 785-795

  Schmidt, Uwe ^a,c   Van Den Akker, Emile ^b   Parren Van Amelsvoort, Martine ^b   Litos, Gabi ^a   De Bruijn, Marella ^b,d   Gutiérrez, Laura ^b   Hendriks, Rudi W ^b   Ellmeier, Wilfried ^c   Löwenberg, Bob ^b   Beug, Hartmut ^a   Von Lindern, Marieke ^b  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF VIENNA   (Austria)

^d Med Res Cncl Molec Haematol U   (United Kingdom)

Author keywords

Hematopoiesis; Jak2; Signal transduction; Stat5

Indexed keywords

BRUTON TYROSINE KINASE; DEATH RECEPTOR 4; ERYTHROPOIETIN; ERYTHROPOIETIN RECEPTOR; JANUS KINASE 2; LIGAND; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA1; REGULATOR PROTEIN; STAT5 PROTEIN; STEM CELL FACTOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BLOOD CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; ERYTHROID PRECURSOR CELL; ERYTHROPOIESIS; FLOW CYTOMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; BLOTTING, WESTERN; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; ERYTHROID PROGENITOR CELLS; ERYTHROPOIETIN; FLOW CYTOMETRY; HEMOGLOBINS; JANUS KINASE 2; PLASMIDS; PRECIPITIN TESTS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RECEPTORS, ERYTHROPOIETIN; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; STEM CELL FACTOR; TRANSFECTION;

EID: 12144288611     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20031109     Document Type: Article

References (53)

1. Wu, H., X. Liu, R. Jaenisch, and H.F. Lodish. 1995. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell. 83:59-67.
2. Flanagan, J.G., D.C. Chan, and P. Leder. 1991. Transmembrane form of the kit ligand growth factor is determined by alternative splicing and is missing in the Sld mutant. Cell. 64:1025-1035.
3. Shetty, V., S. Hussaini, L. Broady-Robinson, K. Allampallam, S. Mundle, R. Borok, E. Broderick, L. Mazzoran, F. Zorat, and A. Raza. 2000. Intramedullary apoptosis of hematopoietic cells in myelodysplastic syndrome patients can be massive: apoptotic cells recovered from high-density fraction of bone marrow aspirates. Blood. 96:1388-1392.
4. De Maria, R., A. Zeuner, A. Eramo, C. Domenichelli, D. Bonci, F. Grignani, S.M. Srinivasula, E.S. Alnemri, U. Testa, and C. Peschle. 1999. Negative regulation of erythropoiesis by caspase-mediated cleavage of GATA-1. Nature. 401:489-493.
5. Dai, C.H., J.O. Price, T. Brunner, and S.B. Krantz. 1998. Fas ligand is present in human erythroid colony-forming cells and interacts with Fas induced by interferon gamma to produce erythroid cell apoptosis. Blood. 91:1235-1242.
6. Zamai, L., P. Secchiero, S. Pierpaoli, A. Bassini, S. Papa, E.S. Alnemri, L. Guidotti, M. Vitale, and G. Zauli. 2000. TNF-related apoptosis-inducing ligand (TRAIL) as a negative regulator of normal human erythropoiesis. Blood. 95:3716-3724.
7. Rusten, L.S., and S.E. Jacobsen. 1995. Tumor necrosis factor (TNF)-alpha directly inhibits human erythropoiesis in vitro: role of p55 and p75 TNF receptors. Blood. 85:989-996.
8. Hoefsloot, L.H., M.P. van Amelsvoort, L.C. Broeders, D.C. van der Plas, K. van Lom, H. Hoogerbrugge, I.P. Touw, and B. Lowenberg. 1997. Erythropoietin-induced activation of STAT5 is impaired in the myelodysplastic syndrome. Blood. 89:1690-1700.
9. Claessens, Y.E., D. Bouscary, J.M. Dupont, F. Picard, J. Melle, S. Gisselbrecht, C. Lacombe, F. Dreyfus, P. Mayeux, and M. Fontenay-Roupie. 2002. In vitro proliferation and differentiation of erythroid progenitors from patients with myelodysplastic syndromes: evidence for Fas-dependent apoptosis. Blood. 99:1594-1601.
10. von Lindern, M., W. Zauner, G. Mellitzer, P. Steinlein, G. Fritsch, K. Huber, B. Lowenberg, and H. Beug. 1999. The glucocorticoid receptor cooperates with the erythropoietin receptor and c-Kit to enhance and sustain proliferation of erythroid progenitors in vitro. Blood. 94:550-559.
11. Wessely, O., A. Bauer, C.T. Quang, E.M. Deiner, M. von Lindern, G. Mellitzer, P. Steinlein, J. Ghysdael, and H. Beug. 1999. A novel way to induce erythroid progenitor self renewal: cooperation of c-Kit with the erythropoietin receptor. Biol. Chem. 380:187-202.
12. Wessely, O., E.M. Deiner, H. Beug, and M. von Lindern. 1997. The glucocorticoid receptor is a key regulator of the decision between self-renewal and differentiation in erythroid progenitors. EMBO J. 16:267-280.
13. Smith, M.A., E.L. Court, and J.G. Smith. 2001. Stem cell factor: laboratory and clinical aspects. Blood Rev. 15:191-197.
14. Damen, J.E., and G. Krystal. 1996. Early events in erythropoietin-induced signaling. Exp. Hematol. 24:1455-1459.
15. Klingmuller, U., H. Wu, J.G. Hsiao, A. Toker, B.C. Duckworth, L.C. Cantley, and H.F. Lodish. 1997. Identification of a novel pathway important for proliferation and differentiation of primary erythroid progenitors. Proc. Natl. Acad. Sci. USA. 94:3016-3021.
16. Taylor, M.L., and D.D. Metcalfe. 2000. Kit signal transduction. Hematol. Oncol. Clin. North Am. 14:517-535.
17. Wojchowski, D.M., R.C. Gregory, C.P. Miller, A.K. Pandit, and T.J. Pircher. 1999. Signal transduction in the erythropoietin receptor system. Exp. Cell Res. 253:143-156.
18. Qiu, Y., and H.J. Kung. 2000. Signaling network of the Btk family kinases. Oncogene. 19:5651-5661.
19. Yang, W.C., Y. Collette, J.A. Nunes, and D. Olive. 2000. Tec kinases: a family with multiple roles in immunity. Immunity. 12:373-382.
20. Khan, W.N., F.W. Alt, R.M. Gerstein, B.A. Malynn, I. Larsson, G. Rathbun, L. Davidson, S. Muller, A.B. Kantor, L.A. Herzenberg, et al. 1995. Defective B cell development and function in Btk-deficient mice. Immunity. 3:283-299.
21. Conley, M.E., J. Rohrer, and Y. Minegishi. 2000. X-linked agammaglobulinemia. Clin. Rev. Allergy Immunol. 19:183-204.
22. Hendriks, R.W., M.F. de Bruijn, A. Maas, G.M. Dingjan, A. Karis, and F. Grosveld. 1996. Inactivation of Btk by insertion of lacZ reveals defects in B cell development only past the pre-B cell stage. EMBO J. 15:4862-4872.
23. Vassilev, A., Z. Ozer, C. Navara, S. Mahajan, and F.M. Uckun. 1999. Bruton's tyrosine kinase as an inhibitor of the Fas/CD95 death-inducing signaling complex. J. Biol. Chem. 274:1646-1656.
24. Uckun, F.M., K.G. Waddick, S. Mahajan, X. Jun, M. Takata, J. Bolen, and T. Kurosaki. 1996. BTK as a mediator of radiation-induced apoptosis in DT-40 lymphoma B cells. Science. 273:1096-1100.
25. Li, Z., M.I. Wahl, A. Eguinoa, L.R. Stephens, P.T. Hawkins, and O.N. Witte. 1997. Phosphatidylinositol 3-kinase-gamma activates Bruton's tyrosine kinase in concert with Src family kinases. Proc. Natl. Acad. Sci. USA. 94:13820-13825.
26. Suzuki, H., S. Matsuda, Y. Terauchi, M. Fujiwara, T. Ohteki, T. Asano, T.W. Behrens, T. Kouro, K. Takatsu, T. Kadowaki, and S. Koyasu. 2003. PI3K and Btk differentially regulate B cell antigen receptor-mediated signal transduction. Nat. Immunol. 4:280-286.
27. Saito, K., A.M. Scharenberg, and J.P. Kinet. 2001. Interaction between the Btk PH domain and phosphatidylinositol-3,4,5-trisphosphate directly regulates Btk. J. Biol. Chem. 276: 16201-16206.
28. Hansson, H., M.P. Okoh, C.I. Smith, M. Vihinen, and T. Hard. 2001. Intermolecular interactions between the SH3 domain and the proline-rich TH region of Bruton's tyrosine kinase. FEBS Lett. 489:67-70.
29. Laederach, A., K.W. Cradic, K.N. Brazin, J. Zamoon, D.B. Fulton, X.Y. Huang, and A.H. Andreotti. 2002. Competing modes of self-association in the regulatory domains of Bruton's tyrosine kinase: intramolecular contact versus asymmetric homodimerization. Protein Sci. 11:36-45.
30. Pursglove, S.E., T.D. Mulhern, J.P. Mackay, M.G. Hinds, and G.W. Booker. 2002. The solution structure and intramolecular associations of the Tec kinase SRC homology 3 domain. J. Biol. Chem. 277:755-762.
31. Takahashi-Tezuka, M., M. Hibi, Y. Fujitani, T. Fukada, T. Yamaguchi, and T. Hirano. 1997. Tec tyrosine kinase links the cytokine receptors to PI-3 kinase probably through JAK. Oncogene. 14:2273-2282.
32. Yamashita, Y., S. Watanabe, A. Miyazato, K. Ohya, U. Ikeda, K. Shimada, N. Komatsu, K. Hatake, Y. Miura, K. Ozawa, and H. Mano. 1998. Tec and Jak2 kinases cooperate to mediate cytokine-driven activation of c-fos transcription. Blood. 91:1496-1507.
33. Baba, Y., S. Hashimoto, M. Matsushita, D. Watanabe, T. Kishimoto, T. Kurosaki, and S. Tsukada. 2001. BLNK mediates Syk-dependent Btk activation. Proc. Natl. Acad. Sci. USA. 98:2582-2586.
34. Robinson, D., H.C. Chen, D. Li, J.T. Yustein, F. He, W.C. Lin, M.J. Hayman, and H.J. Kung. 1998. Tyrosine kinase expression profiles of chicken erythro-progenitor cells and oncogene-transformed erythroblasts. J. Biomed. Sci. 5:93-100.
35. Whyatt, D., F. Lindeboom, A. Karis, R. Ferreira, E. Milot, R. Hendriks, M. de Bruijn, A. Langeveld, J. Gribnau, F. Grosveld, and S. Philipsen. 2000. An intrinsic but cell-non-autonomous defect in GATA-1-overexpressing mouse erythroid cells. Nature. 406:519-524.
36. van Dijk, T.B., E. van Den Akker, M.P. Amelsvoort, H. Mano, B. Lowenberg, and M. von Lindern. 2000. Stem cell factor induces phosphatidylinositol 3′-kinase-dependent Lyn/Tec/Dok-1 complex formation in hematopoietic cells. Blood. 96:3406-3413.
37. von Lindern, M., E.M. Deiner, H. Dolznig, M. Parren-Van Amelsvoort, M.J. Hayman, E.W. Mullner, and H. Beug. 2001. Leukemic transformation of normal murine erythroid progenitors: v- and c-ErbB act through signaling pathways activated by the EpoR and c-Kit in stress erythropoiesis. Oncogene. 20:3651-3664.
38. Kowenz, E., A. Leutz, G. Doderlein, T. Graf, and H. Beug. 1987. ts-oncogene-transformed erythroleukemic cells: a novel test system for purifying and characterizing avian erythroid growth factors. Hamatol. Bluttransfus. 31:199-209.
39. Beug, H., S. Palmieri, C. Freudenstein, H. Zentgraf, and T. Graf. 1982. Hormone-dependent terminal differentiation in vitro of chicken erythroleukemia cells transformed by ts mutants of avian erythroblastosis virus. Cell. 28:907-919.
40. Tatton, L., G.M. Morley, R. Chopra, and A. Khwaja. 2003. The Src-selective kinase inhibitor PP1 also inhibits Kit and Bcr-Abl tyrosine kinases. J. Biol. Chem. 278:4847-4853.
41. Tumang, J.R., R.S. Negm, L.A. Solt, T.J. Schneider, T.P. Colarusso, W.D. Hastings, R.T. Woodland, and T.L. Rothstein. 2002. BCR engagement induces Fas resistance in primary B cells in the absence of functional Bruton's tyrosine kinase. J. Immunol. 168:2712-2719.
42. Pan, S., P. An, R. Zhang, X. He, G. Yin, and W. Min. 2002. Etk/Bmx as a tumor necrosis factor receptor type 2-specific kinase: role in endothelial cell migration and angiogenesis. Mol. Cell. Biol. 22:7512-7523.
43. von Lindern, M., M. Parren-van Amelsvoort, T. van Dijk, E. Deiner, E. van den Akker, S. van Emst-de Vries, P. Willems, H. Beug, and B. Lowenberg. 2000. Protein kinase C alpha controls erythropoietin receptor signaling. J. Biol. Chem. 275: 34719-34727.
44. Saharinen, P., and O. Silvennoinen. 2002. The pseudokinase domain is required for suppression of basal activity of Jak2 and Jak3 tyrosine kinases and for cytokine-inducible activation of signal transduction. J. Biol. Chem. 277:47954-47963.
45. Silvestris, F., P. Cafforio, M. Tucci, and F. Dammacco. 2002. Negative regulation of erythroblast maturation by Fas-L(+)/TRAIL(+) highly malignant plasma cells: a major pathogenetic mechanism of anemia in multiple myeloma. Blood. 99: 1305-1313.
46. Tsushima, H., Y. Imaizumi, D. Imanishi, K. Fuchigami, and M. Tomonaga. 1999. Fas antigen (CD95) in pure erythroid cell line AS-E2 is induced by interferon-gamma and tumor necrosis factor-alpha and potentiates apoptotic death. Exp. Hematol. 27:433-440.
47. Chung, I.J., C. Dai, and S.B. Krantz. 2003. Stem cell factor increases the expression of FLIP that inhibits IFNgamma-induced apoptosis in human erythroid progenitor cells. Blood. 101:1324-1328.
48. De Maria, R., U. Testa, L. Luchetti, A. Zeuner, G. Stassi, E. Pelosi, R. Riccioni, N. Felli, P. Samoggia, and C. Peschle. 1999. Apoptotic role of Fas/ Fas ligand system in the regulation of erythropoiesis. Blood. 93:796-803.
49. Kolbus, A., S. Pilat, Z. Husak, E.M. Deiner, G. Stengl, H. Beug, and M. Baccarini. 2002. Raf-1 antagonizes erythroid differentiation by restraining caspase activation. J. Exp. Med. 196:1347-1353.
50. Zermati, Y., C. Garrido, S. Amsellem, S. Fishelson, D. Bouscary, F. Valensi, B. Varet, E. Solary, and O. Hermine. 2001. Caspase activation is required for terminal erythroid differentiation. J. Exp. Med. 193:247-254.
51. Dolznig, H., B. Habermann, K. Stangl, E.M. Deiner, R. Moriggl, H. Beug, and E.W. Müllner. 2002. Apoptosis protection by the Epo target Bcl-XL allows factor-independent differentiation of primary erythroblasts. Curr. Biol. 12:1076-1085.
52. Socolovsky, M., H. Nam, M.D. Fleming, V.H. Haase, C. Brugnara, and H.F. Lodish. 2001. Ineffective erythropoiesis in Stat5a(-/-)5b(-/-) mice due to decreased survival of early erythroblasts. Blood. 98:3261-3273.
53. Gersuk, G.M., C. Beckham, M.R. Loken, P. Kiener, J.E. Anderson, A. Farrand, A.B. Troutt, J.A. Ledbetter, and H.J. Deeg. 1998. A role for tumour necrosis factor-alpha, Fas and Fas-Ligand in marrow failure associated with myelodysplastic syndrome. Br. J. Haematol. 103:176-188.