Involvement of JAK2, but not PI 3-kinase/Akt and MAP kinase pathways, in anti-apoptotic signals of GM-CSF in human eosinophils

Journal of Leukocyte Biology

Volumn 65, Issue 5, 1999, Pages 700-706

  Miike, Satoshi ^b   Nakao, Atsuhito ^b   Hiraguri, Masaki ^b   Kurasawa, Kazuhiro ^b   Saito, Yasushi ^b   Iwamoto, Itsuo ^a  

^a CHIBA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NONE

Author keywords

AG 490; Allergy; Apoptosis; Signal transduction

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; WORTMANNIN;

ALLERGY; APOPTOSIS; ARTICLE; CELL SURVIVAL; DNA SYNTHESIS INHIBITION; ENZYME ACTIVATION; EOSINOPHIL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STEM CELL; TRANSCRIPTION REGULATION;

EID: 0032934674     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1002/jlb.65.5.700     Document Type: Article

References (49)

1. Lopez, A. F., Williamson, D. J., Gamble, J. R., Begley, C. G, Harlan, J. M., Klebanoff, S. J., Waltersdorph, A., Wong, G., Clark, S. C., Vadas, M. A. (1986) Recombinant human granulocyte-macrophage colony-stimulating factor stimulates in vitro human mature neutrophil and eosinophil function, surface receptor expression, and survival. J. Clin. Invest. 78, 1220-1228.
2. Owen, W. F., Jr., Rothenherg, M. E., Silberstein, D. S., Gasson, J. C., Stevens, R. L., Austen, K. F., Soberman, R. J. (1987) Regulation of human eosinophil viability, density, and function by granulocyte/macrophage colony-stimulating factor in the presence of 3T3 fibroblasts. J. Exp. Med. 166, 129-141.
3. Rothenberg, M. E., Petersen, J., Stevens, R. L., Silberstein, D. S., McKenzie, D. T., Austen, K. F., Owen, W. F., Jr. (1989) Interleukin-5-dependent conversion of normodense human eosinophils to the hypodense phenotype uses 3T3 fibroblasts for enhanced viability, accelerated hypodensity, and sustained antibody-dependent cytotoxicity. J. Immunol. 143, 2311-2316.
4. Drazen, J. M., Arm, J. P., Austen, K. F. (1996) Sorting out the cytokines of asthma. J. Exp. Med. 183, 1-5.
5. Simon, H.-U., Yousefi, S., Schranz, C., Schapowal, A., Bachert, C., Blase, K. (1997) Direct demonstration of delayed eosinophil apoptosis as a mechanism causing tissue eosinophilia. J. Immunol. 158, 3902-3908.
6. Gleich, G. J. (1990) The eosinophil and bronchial asthma: Current understanding. J. Allergy Clin. Immunol. 85, 422-436.
7. Pazdrak, K., Schreiber, D., Forsythe, P., Justement, L., Alam, R. (1995) The intracellular signal transduction mechanism of interleukin-5 in eosinophils: The involvement of Lyn tyrosine kinase and the Ras-Raf-1-MEK-microtubule-associated protein kinase pathway. J. Exp. Med. 181, 1827-1834.
8. Pazdrak, K., Stafford, S., Alam, R. (1995) The activation of the Jak-STAT1 signaling pathway by IL-5 in eosinophils. J. Immunol. 155, 397-402.
9. Bates, M. E., Bertics, P. J., Busse, W. W. (1996) IL-5 activates a 45-kilodalton mitogen-activated protein (MAP) kinase and Jak2 tyrosine kinase in human eosinophils. J. Immunol. 156, 711-718.
10. van der Bruggen, T., Caldenhoven, E., Kanters, D., Coffer, P., Raaijmakers, J. A. M., Lammers, J.-W. J., Koenderman, L. (1995) Interleukin-5 signaling in human eosinophils involves JAK2 tyrosine kinase and Statla. Blood 85, 1442-1448.
11. Hiraguri, M., Miike, S., Sano, H., Kurasawa, K., Saito, Y., Iwamoto, I. (1997) Granulocyte-macrophage colony-stimulating factor and interleukin-5 activate mitogen-activated protein kinase through Jak2 kinase and phosphatidylinositol 3-kinase in human eosinophils. J. Allergy Clin. Immunol. 100, S45-S51.
12. Yousefi, S., Hoessli, D. C., Blaser, K., Mills, G. B., Simon, H.-U. (1996) Requirement of Lyn and Syk tyrosine kinases for the prevention of apoptosis by cytokines in human eosinophils. J. Exp. Med. 83, 1407-1414.
13. Yao, R., Cooper, G. M. (1995) Requirement for phosphatidylinositol 3-kinase in the prevention of apoptosis by nerve growth factor. Science 270, 1326-1331.
14. Minshall, C., Arkins, S., Freund, G. G., Kelley, K. W. (1996) Requirement for phosphatidylinositol 3′-kinase to protect hemopoietic progenitors against apoptosis depends upon the extracellular survival factor. J. Immunol. 156, 939-947.
15. Kauffmann-Zeh, A., Rodriguez-Viciana, P., Ulrich, E., Gilbert, C., Coffer, P., Downward, J., Evan, G. (1997) Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature 385, 544-548.
16. Ahmed, N. N., Grimes, H. L., Bellacosa, A., Chan, T. O., Tsichlis. P. N. (1997) Transduction of interleukin-2 anti-apoptotic and proliferative signals via Akt protein kinase. Proc. Natl. Acad. Sci. USA. 94, 3627-3632.
17. Songyang, Z., Baltimore, D., Cantley, L. C., Kaplan, D. R., Franke, T. F. (1997) Interleukin 3-dependent survival by the Akt protein kinase. Proc. Natl. Acad. Sci. USA. 94, 11345-11350.
18. Parrizas, M., Saltiel, A. R., LeRoith, D. (1997) Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3′-kinase and mitogen-activated protein kinase pathways. J. Biol. Chem. 272, 154-161.
19. Villalba, M., Bockaert, J., Journot, L. (1997) Pituitary adenylate cyclase-activating polypeptide (PACAP-38) protects cerebellar granule neurons from apoptosis by activating the mitogen-activated protein kinase (MAP kinase) pathway. J. Neurosci. 17, 83-90.
20. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J., Greenberg, M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.
21. Sato, N., Sakamaki, K., Terada, N., Arai, K., Miyajima, A. (1993) Signal transduction by the high-affinity GM-CSF receptor: two distinct cytoplasmic regions of the common β subunit responsible for different signaling. EMBO J. 12, 4181-4189.
22. Kinoshita, T., Yokota, T., Arai, K., Miyajima, A. (1995) Suppression of apoptotic death in hematopoietic cells by signalling through the IL-3/GM-CSF receptors. EMBO J. 14, 266-275.
23. Pang, L., Sawada, T., Decker, S. J., Saltiel, A. R. (1995) Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem. 270, 13585-13588.
24. Alessi, D. R., Cuenda, A., Cohen, P., Dudley, D. T., Saltiel, A. R. (1995) PD98059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270, 27489-27494.
25. Dudley, D. T., Pang, L., Decker, S. J., Bridges, A. J., Saltiel, A. R. (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 92, 7686-7689.
26. Franke, T. F., Yang, S.-I., Chan, T. O., Datta, K., Kazlauskas, A., Morrison, D. K., Kaplan, D. R., Tsichlis, P. N. (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81, 727-736.
27. Burgering, B. M. T., Coffer, P. J. (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376, 599-602.
28. Meydan, N., Grunberger, T., Dadih, H., Shahar, M., Arpaia, E., Lapidot, Z., Leeder, J. S., Freedman, M., Cohen, A., Gazit, A., Levitzki, A., Roifman, C. M. (1996) Inhibition of acute lymphoblastic leukemia by a Jak-2 inhibitor. Nature 379, 645-648.
29. cdc2. Biochim. Biophys. Acta 1135, 335-342.
30. Torres, M., Hall, F. L., O'Neill, K. (1993) Stimulation of human neutrophils with formyl-methionyl-leucyl-phenylalanine induces tyrosine phosphorylation and activation of two distinct mitogen-activated protein-kinases. J. Immunol. 150, 1563-1578.
31. Hansel, T. T., De Vries, I. J. M., Iff, T., Rihs, S., Wandzilak, M., Betz, S., Blaser, K., Walker, C. (1991) An improved immunomagnetic procedure for the isolation of highly purified human blood eosinophils. J. Immunol. Meth. 145, 105-110.
32. Yano, H., Nakanishi, S., Kimura, K., Hanai, N., Saitoh, Y., Fukui, Y., Nonomura, Y., Matsuda, Y. (1993) Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268, 25846-25856.
33. Okada, T., Sakuma, L., Fukui, Y., Hazeki, O., Ui, M. (1994) Blockade of chemotactic peptide-induced stimulation of neutrophils by wortmannin as a result of selective inhibition of phosphatidylinositol 3-kinase. J. Biol. Chem. 269, 3563-3567.
34. Thelen, M., Wymann, M. P., Langen, H. (1994) Wortmannin binds specifically to 1-phosphatidylinositol 3-kinase while inhibiting guanine nucleotide-binding protein-coupled receptor signaling in neutrophil leukocytes. Proc. Natl. Acad. Sci. USA 91, 4960-4964.
35. Vlahos, C. J., Matter, W. F., Hui, K. Y., Brown, R. F. (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
36. Kimura, K., Hattori, S., Kabuyama, Y., Shizawa, Y., Takayanagi, J., Nakamura, S., Toki, S., Matsuda, Y., Onodera, K., Fukui, Y. (1994) Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J. Biol. Chem. 269, 18961-18967.
37. Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F., Riccardi, C. (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Meth. 139, 271-279.
38. Quelle, F. W., Sato, N., Witthuhn, B. A., Inhorn, R. C., Eder, M., Miyajima, A., Griffin, J. D., Ihle, J. N. (1994) JAK2 associates with the βc chain of the receptor for granulocyte-macrophage colony-stimulating factor, and its activation requires the membrane-proximal region. Mol. Cell. Biol. 14, 4335-4341.
39. O'Shea J. J. (1997) Jaks, STATs, cytokine signal transduction, and immunoregulation: Are we there yet? Immunity 7, 1-11.
40. del Peso, L., González-García, M., Page, C., Herrera, R., Nuñez, G. (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278, 687-689.
41. Datta, S. R., Dudek, H., Tao, X., Masters, S., Fu, H., Gotoh, Y., Greenberg, M. E. (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91, 231-241.
42. Simon, H.-U., Yousefi, S., Fibbert, B., Levi-Schaffer, F., Blaser, K. (1997) Anti-apoptotic signals of granulocyte-macrophage colony-stimulating factor are transduced via Jak2 tyrosine kinase in eosinophils. Eur. J. Immunol. 27, 3536-3539.
43. Friedman, M. C., Migone, T. S., Russel, S. M., Leonard, W. J. (1996) Different interleukin-2 receptor β-chain tyrosines couple to at least two signaling pathways and synergistically mediate interleukin-2-induced proliferation. Proc. Natl. Acad. Sci. USA 93, 2077-2082.
44. Mui, A. L-F., Wakao, H., Kinoshita, T., Kitamura, T., Miyajima, A. (1996) Suppression of interleukin-3-induced gene expression by a C-terminal truncated Stat5: role of Stat5 in proliferation. EMBO J. 15, 2425-2433.
45. Takeshita, T., Arita, T., Higuchi, M., Asao, H., Endo, K., Kuroda, H., Tanaka, N., Murata, K., Ishii, N., Sugamura, K. (1997) STAM, signal transducing adaptor molecule is associated with Janus kinases and involved in signaling for cell growth and c-myc induction. Immunity 6, 449-457.
46. Pazdrak, K., Olszewska-Pazdrak, B., Stafford, S., Garofalo, R. P., Alam, R. (1998) Lyn, Jak2, and Raf-1 kinases are critical for the antiapoptotic effect of interleukin 5, whereas only Raf-1 kinase is essential for eosinophil activation and degranulation. J. Exp. Med. 188, 421-429.
47. Pulverer, B. J., Kyriakis, J. M., Avruch, J., Nikolakaki, E. Woodgett, J. R. (1991) Phosphorylalion of c-jun mediated by MAP kinase. Nature 353, 670-672.
48. Zha, J., Harada, H., Yang, E., Jockel, J., Korsmeyer, S. J. (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-XL. Cell 87, 619-628.
49. Li, S., Sedivy, J. M. (1993) Raf-1 protein kinase activates the NF-κB transcription factor by dissociating the cytoplasmic NF-κB-IκB complex. Proc. Natl. Acad. Sci. USA 90, 9247-9251.