Janus kinases promote cell-surface expression and provoke autonomous signalling from routing-defective G-CSF receptors

Biochemical Journal

Volumn 417, Issue 3, 2009, Pages 737-746

  Meenhuis, Annemarie ^a   Irandoust, Mahban ^a   Wölfer, Albert ^a   Roovers, Onno ^a   Valkhof, Marijke ^a   Touw, Ivo P ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Endocytosis; Granulocyte colony stimulating factor (G CSF) receptor; Janus kinase (JAK); Signal transducer and activator of transcription 3 (STAT3); Signal transduction

Indexed keywords

BIOSYNTHETIC PATHWAY; CELL SURFACE EXPRESSION; CELL SURVIVAL; CYTOKINE RECEPTOR; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; GRANULOCYTE COLONY-STIMULATING FACTOR (G-CSF) RECEPTOR; GRANULOCYTE-COLONY STIMULATING FACTOR; HAEMATOPOIETIC CELLS; JANUS KINASE; JANUS KINASE (JAK); LYSOSOMAL DEGRADATION; PROGENITOR CELL; PROTEIN STABILITY; SIGNAL TRANSDUCER AND ACTIVATOR OF TRANSCRIPTION 3 (STAT3); SIGNAL TRANSDUCERS; TYROSINE KINASE; TYROSINE RESIDUES;

AMINO ACIDS; BACTERIOPHAGES; CHEMICAL ACTIVATION; PIEZOELECTRIC TRANSDUCERS; TRANSCRIPTION;

SIGNAL TRANSDUCTION;

GRANULOCYTE COLONY STIMULATING FACTOR RECEPTOR; JANUS KINASE; JANUS KINASE 1; JANUS KINASE 2; LYSINE; MUTANT PROTEIN; PROTEIN KINASE TYK2; STAT3 PROTEIN; COLONY STIMULATING FACTOR RECEPTOR; CSF3R PROTEIN, HUMAN; LIGAND;

ANIMAL CELL; ARTICLE; CELL SURFACE; CELL SURVIVAL; CELL TRANSFORMATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME BINDING; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STABILITY; SIGNAL TRANSDUCTION; STEADY STATE; TRANSCRIPTION INITIATION; UBIQUITINATION; ANIMAL; CELL MEMBRANE; GENETIC TRANSFECTION; GENETICS; HELA CELL; METABOLISM; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; ENDOCYTOSIS; HELA CELLS; HUMANS; JANUS KINASES; LIGANDS; LYSOSOMES; MICE; RECEPTORS, COLONY-STIMULATING FACTOR; RECEPTORS, GRANULOCYTE COLONY-STIMULATING FACTOR; SIGNAL TRANSDUCTION; TRANSFECTION; UBIQUITINATION;

EID: 59849094269     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081153     Document Type: Article

References (37)

1. Avalos, B. R., Gasson, J. C., Hedvat, C., Quan, S. G., Baldwin, G. C., Weisbart, R. H., Williams, R. E., Golde, D. W. and DiPersio, J. F. (1990) Human granulocyte colony-stimulating factor: biologic activities and receptor characterization on hematopoietic cells and small cell lung cancer cell lines. Blood 75, 851-857
2. Touw, I. P. and Bontenbal, M. (2007) Granulocyte colony-stimulating factor: key factor or innocent bystander in the development of secondary myeloid malignancy? J. Natl. Cancer. Inst. 99, 183-186
3. Aarts, L. H., Roovers, O., Ward, A. C. and Touw, I. P. (2004) Receptor activation and 2 distinct COOH-terminal motifs control G-CSF receptor distribution and internalization kinetics. Blood 103, 571-579
4. Irandoust, M. I., Aarts, L. H., Roovers, O., Gits, J., Erkeland, S. J. and Touw, I. P. (2007) Suppressor of cytokine signaling 3 controls lysosomal routing of G-CSF receptor. EMBO J. 26, 1782-1793
5. Erratum (2007) EMBO J. 26, 2822
6. Touw, I. P. and van de Geijn, G. J. (2007) Granulocyte colony-stimulating factor and its receptor in normal myeloid cell development, leukemia and related blood cell disorders. Front. Biosci. 12, 800-815
7. Ward, A. C., van Aesch, Y. M., Schelen, A. M. and Touw, I. P. (1999) Defective internalization and sustained activation of truncated granulocyte colony-stimulating factor receptor found in severe congenital neutropenia/acute myeloid leukemia. Blood 93, 447-458
8. Radtke, S., Jorissen, A., de Leur, H. S., Heinrich, P. C. and Behrmann, I. (2006) Three dileucine-like motifs within the interbox1/2 region of the human oncostatin M receptor prevent efficient surface expression in the absence of an associated Janus kinase. J. Biol. Chem. 281, 4024-4034
9. Royer, Y., Staerk, J., Costuleanu, M., Courtoy, P. J. and Constantinescu, S. N. (2005) Janus kinases affect thrombopoietin receptor cell surface localization and stability. J. Biol. Chem. 280, 27251-27261
10. Tong, W., Sulahian, R., Gross, A. W., Hendon, N., Lodish, H. F. and Huang, L. J. (2006) The membrane-proximal region of the thrombopoietin receptor confers its high surface expression by JAK2-dependent and -independent mechanisms. J. Biol. Chem. 281, 38930-38940
11. Ragimbeau, J., Dondi, E., Alcover, A., Eid, P., Uze, G. and Pellegrini, S. (2003) The tyrosine kinase Tyk2 controls IFNAR1 cell surface expression. EMBO J. 22, 537-547
12. Kumar, K. G., Varghese, B., Banerjee, A., Baker, D. P., Constantinescu, S. N., Pellegrini, S. and Fuchs, S. Y. (2008) Basal ubiquitin-independent internalization of interferon α receptor is prevented by Tyk2-mediated masking of a linear endocytic motif. J. Biol. Chem. 283, 18566-18572
13. Huang, L. J., Constantinescu, S. N. and Lodish, H. F. (2001) The N-terminal domain of Janus kinase 2 is required for Golgi processing and cell surface expression of erythropoietin receptor. Mol. Cell 8, 1327-1338
14. Joos, S., Kupper, M., Ohl, S., von Bonin, F., Mechtersheimer, G., Bentz, M., Marynen, P., Moller, P., Pfreundschuh, M., Trumper, L. and Lichter, P. (2000) Genomic imbalances including amplification of the tyrosine kinase gene JAK2 in CD30+ Hodgkin cells. Cancer Res. 60, 549-552
15. Rucker, F. G., Bullinger, L., Schwaenen, C., Lipka, D. B., Wessendorf, S., Frohling, S., Bentz, M., Miller, S., Scholl, C., Schlenk, R. F. et al. (2006) Disclosure of candidate genes in acute myeloid leukemia with complex karyotypes using microarray-based molecular characterization. J. Clin. Oncol. 24, 3887-3894
16. Barge, R. M., de Koning, J. P., Pouwels, K., Dong, F., Lowenberg, B. and Touw, I. P. (1996) Tryptophan 650 of human granulocyte colony-stimulating factor (G-CSF) receptor, implicated in the activation of JAK2, is also required for G-CSF-mediated activation of signaling complexes of the p21ras route. Blood 87, 2148-2153
17. Dong, F., van Buitenen, C., Pouwels, K., Hoefsloot, L. H., Lowenberg, B. and Touw, I. P. (1993) Distinct cytoplasmic regions of the human granulocyte colony-stimulating factor receptor involved in induction of proliferation and maturation. Mol. Cell. Biol. 13, 7774-7781
18. van den Akker, E., van Dijk, T., Parren-van Amelsvoort, M., Grossmann, K. S., Schaeper, U., Toney-Earley, K., Waltz, S. E., Lowenberg, B. and von Lindern, M. (2004) Tyrosine kinase receptor RON functions downstream of the erythropoietin receptor to induce expansion of erythroid progenitors. Blood 103, 4457-4465
19. Greenberger, J. S., Eckner, R. J., Sakakeeny, M., Marks, P., Reid, D., Nabel, G., Hapel, A., Ihle, J. N. and Humphries, K. C. (1983) Interleukin 3-dependent hematopoietic progenitor cell lines. Fed. Proc. 42, 2762-2771
20. Palacios, R. and Steinmetz, M. (1985) IL-3-dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes in vivo. Cell 41, 727-734
21. Watling, D., Guschin, D., Muller, M., Silvennoinen, O., Witthuhn, B. A., Quelle, F. W., Rogers, N. C., Schindler, C., Stark, G. R., Ihle, J. N. et al. (1993) Complementation by the protein tyrosine kinase JAK2 of a mutant cell line defective in the interferon-γ signal transduction pathway. Nature 366, 166-170
22. Muller, M., Briscoe, J., Laxton, C., Guschin, D., Ziemiecki, A., Silvennoinen, O., Harpur, A. G., Barbieri, G., Witthuhn, B. A., Schindler, C. et al. (1993) The protein tyrosine kinase JAK1 complements defects in interferon-α/β and -γ signal transduction. Nature 366, 129-135
23. Velazquez, L., Fellous, M., Stark, G. R. and Pellegrini, S. (1992) A protein tyrosine kinase in the interferon α/β signaling pathway. Cell 70, 313-322
24. Ward, A. C., Smith, L., de Koning, J. P., van Aesch, Y. and Touw, I. P. (1999) Multiple signals mediate proliferation, differentiation, and survival from the granulocyte colony-stimulating factor receptor in myeloid 32D cells. J. Biol. Chem. 274, 14956-14962
25. Lu, X., Levine, R., Tong, W., Wernig, G., Pikman, Y., Zarnegar, S., Gilliland, D. G. and Lodish, H. (2005) Expression of a homodimeric type I cytokine receptor is required for JAK2V617F-mediated transformation. Proc. Natl. Acad. Sci. U.S.A. 102, 18962-18967
26. Weston, C. R., Lambright, D. G. and Davis, R. J. (2002) Signal transduction. MAP kinase signaling specificity. Science 296, 2345-2347
27. McLemore, M. L., Grewal, S., Liu, F., Archambault, A., Poursine-Laurent, J., Haug, J. and Link, D. C. (2001) STAT-3 activation is required for normal G-CSF-dependent proliferation and granulocytic differentiation. Immunity 14, 193-204
28. Dong, F., Liu, X., de Koning, J. P., Touw, I. P., Hennighausen, L., Larner, A. and Grimley, P. M. (1998) Stimulation of Stat5 by granulocyte colony-stimulating factor (G-CSF) is modulated by two distinct cytoplasmic regions of the G-CSF receptor. J. Immunol. 161, 6503-6509
29. Radtke, S., Hermanns, H. M., Haan, C., Schmitz-Van De Leur, H., Gascan, H., Heinrich, P. C. and Behrmann, I. (2002) Novel role of Janus kinase 1 in the regulation of oncostatin M receptor surface expression. J. Biol. Chem. 277, 11297-11305
30. Pelletier, S., Gingras, S., Funakoshi-Tago, M., Howell, S. and Ihle, J. N. (2006) Two domains of the erythropoietin receptor are sufficient for Jak2 binding/activation and function. Mol. Cell. Biol. 26, 8527-8538
31. Belouzard, S. and Rouille, Y. (2006) Ubiquitylation of leptin receptor OB-Ra regulates its clathrin-mediated endocytosis. EMBO J. 25, 932-942
32. Hurley, J. H., Lee, S. and Prag, G. (2006) Ubiquitin-binding domains. Biochem. J. 399, 361-372
33. Wang, J., Sun, H. Q., Macia, E., Kirchhausen, T., Watson, H., Bonifacino, J. S. and Yin, H. L. (2007) PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal. Mol. Biol. Cell 18, 2646-2655
34. Hurley, J. H. (2008) ESCRT complexes and the biogenesis of multivesicular bodies. Curr. Opin. Cell Biol. 20, 4-11
35. Lowenberg, B. and Touw, I. P. (1993) Hematopoietic growth factors and their receptors in acute leukemia. Blood 81, 281-292
36. Freedman, M. H., Bonilla, M. A., Fier, C., Bolyard, A. A., Scarlata, D., Boxer, L. A., Brown, S., Cham, B., Kannourakis, G., Kinsey, S. E. et al. (2000) Myelodysplasia syndrome and acute myeloid leukemia in patients with congenital neutropenia receiving G-CSF therapy. Blood 96, 429-436
37. Migone, T. S., Humbert, M., Rascle, A., Sanden, D., D'Andrea, A. and Johnston, J. A. (2001) The deubiquitinating enzyme DUB-2 prolongs cytokine-induced signal transducers and activators of transcription activation and suppresses apoptosis following cytokine withdrawal. Blood 98, 1935-1941