Signaling via IL-2 and IL-4 in JAK3-deficient severe combined immunodeficiency lymphocytes: JAK3-dependent and independent pathways

Immunity

Volumn 5, Issue 6, 1996, Pages 605-615

  Oakes, Scott A ^d   Candotti, Fabio ^d   Johnston, James A ^d   Chen, Yi Qing ^d   Ryan, John J ^d   Taylor, Naomi ^b   Liu, Xiuwen ^a   Hennighausen, Lothar ^a   Notarangelo, Luigi D ^c   Paul, William E ^d   Blaese, R Michael ^d   O'Shea, John J ^d  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b CHILDREN S HOSPITAL LOS ANGELES   (United States)

^c UNIVERSITY OF BRESCIA   (Italy)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; INTERLEUKIN 2; INTERLEUKIN 4; PROTEIN TYROSINE KINASE;

ARTICLE; B LYMPHOCYTE; CELL LINE; COMBINED IMMUNODEFICIENCY; HUMAN; MUTATION; PRIORITY JOURNAL;

EID: 0030497506     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80274-5     Document Type: Article

References (52)

1. Asao, H., Takeshita, T., Ishii, N., Kumaki, S., Nakamura, M., and Sugamura, K. (1993). Reconstitution of functional interleukin 2 receptor complexes on fibroblastoid cells: involvement of the cytoplasmic domain of the γ chain in two distinct signaling pathways. Proc. Natl. Acad. Sci. USA 90, 4127-4131.
2. Boussiotis, V.A., Barber, D.L., Nakarai, T., Freeman, G.J., Gribben, J.G., Bernstein, G.M., D'Andrea, A.D., Ritz, J., and Nadler, L.M. (1994). Prevention of T cell anergy by signaling through the γc chain of the IL-2 receptor. Science 266, 1039-1042.
3. Callard, R.E., Matthews, D.J., and Hibbert, L. (1996). IL-4 and IL-13 receptors: are they one and the same? Immunol. Today 17, 108-110.
4. Candotti, F., Oakes, S.A., Johnston, J.A., Notarangelo, L.D., O'Shea, J.J., and Blaese, R.M. (1996). In vitro correction of JAK3-deficient severe combined immunodeficiency by retroviral-mediated gene transduction. J. Exp. Med. 183, 2687-2692.
5. Caput, D., Laurent, P., Kaghad, M., Lelias, J.-M., Lefort, S, Vita, N., Ferrara, P. (1996). Cloning and characterization of a specific interleukin (IL)-13 binding protein structurally related to the IL-5 receptor α chain. J. Biol. Chem. 271, 16921-16926.
6. Coffman, R.L., Lebman, D.A., and Rothman, P. (1993). Mechanism and regulation of immunoglobulin isotype switching. Adv. Immunol. 54, 229-270.
7. Conrad, D.H., Waldschmidt, T.J., Lee, W.T., Rao, M., Keegan, A.D., Noelle, R.J., Lynch, R.G., and Kehry, M.R. (1987). Effect of B cell stimulatory factor-1 (interleukin 4) on Fc∈ and Fcγ receptor expression on murine B lymphocytes and B cell lines. J. Immunol. 139, 2290-2296.
8. Fenghao, X., Saxon, A., Nguyen, A., Ke, Z., Diaz-Sanchez, D., and Nel, A. (1995). Interleukin 4 activates a signal transducer and activator of transcription (Stat) protein which interacts with an Interferon-γ activation site-like sequence upstream of the I∈ exon in a human B cell line: evidence for the involvement of Janus kinase 3 and interleukin-4 Stat. J. Clin. Invest. 96, 907-914.
9. Friedmann, M.C., Migone, T.S., Russell, S.M., and 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.
10. Fujii, H., Nakagawa, Y., Schindler, U., Kawahara, A., Mori, H., Bouilleux, F., Groner, B., Ihle, J.N., Minami, Y., Miyazaki, T.,and Taniguchi, T. (1995). Activation of Stat5 by interleukin 2 requires a carboxyl-terminal region of the interleukin 2 receptor β chain but is not essential for the proliferative signal transmission. Proc. Natl. Acad. Sci. USA 92, 5482-5486.
11. Giri, J.G., Ahdieh, M., Eisenman, J., Shanebeck, K., Grabstein, K., Kumaki, S., Namen, A., Park, L.S., Cosman, D., and Anderson, D. (1994). Utilization of the β and γ chains of the IL-2 receptor by the novel cytokine IL-15. EMBO J. 13, 2822-2830.
12. Hilton, D.J., Zhang, J.G., Metcalf, D., Alexander, W.S., Nicola, N.A., and Willson, T.A. (1996). Cloning and characterization of a binding subunit of the interleukin 13 receptor that is also a component of the interleukin 4 receptor. Proc. Natl. Acad. Sci. USA 93, 497-501.
13. Hou, J., Schindler, U., Henzel, W.J., Ho, T.C., Brasseur, M., and McKnight, S.L. (1994). An interleukin-4-induced transcription factor: IL-4 Stat. Science 265, 1701-1706.
14. Hou, J., Schindler, U., Henzel, W.J., Wong, S.C., and McKnight, S.L. (1995). Identification and purification of human Stat proteins activated in response to interleukin-2. Immunity 2, 321-329.
15. Ihle, J. (1995). Cytokine receptor signaling. Nature 377, 591-594.
16. Izuhara, K., Heike, T., Otsuka, T., Yamaoka, K., Mayumi, M., Imamura, T., Nibo, Y., and Harada, N. (1996). Signal transduction pathway of interleukin-4 and interleukin-13 in human B cells derived from X-linked severe combined immunodeficiency patients. J. Biol. Chem. 271, 619-622.
17. Johnston, J.A., Kawamura, M., Kirken, R.A., Chen, Y.Q., Blake, T.B., Shibuya, K., Ortaldo, J.R., McVicar, D.W., and O'Shea, J.J. (1994). Phosphorylation and activation of the Jak-3 Janus kinase in response to interleukin-2. Nature 370, 151-153.
18. Johnston, J.A., Bacon, C.M., Finbloom, D.S., Rees, R.C., Kaplan, D., Shibuya, K., Ortaldo, J.R., Gupta, S., Chen, Y.Q., Giri, J.D., and O'Shea, J.J. (1995a). Tyrosine phosphorylation and activation of STAT5, STAT3, and Janus kinases by interleukins 2 and 15. Proc. Natl. Acad. Sci. USA 92, 8705-8709.
19. Johnston, J.A., Wang, L.M., Hanson, E.P., Sun, X.J., White, M.F., Oakes, S.A., Pierce, J.H., and O'Shea, J.J. (1995b). Interleukins 2, 4, 7, and 15 stimulate tyrosine phosphorylation of insulin receptor substrates 1 and 2 in T cells: potential role of JAK kinases. J. Biol. Chem. 270, 28527-28530.
20. Kawamura, M., McVicar, D.W., Johnston, J.A., Blake, T.B., Chen, Y.Q., Lal, B.K., Lloyd, A.R., Kelvin, D.J., Staples, J.E., Ortaldo, J.R., and O'Shea, J.J. (1994). Molecular cloning of L-JAK, a Janus family protein-tyrosine kinase expressed in natural killer cells and activated leukocytes. Proc. Natl. Acad. Sci. USA 97, 6374-6378.
21. Keegan, A.D., Nelms, K., White, M., Wang, L.-M., Pierce, J.H., and Paul, W.E. (1994). An IL-4 receptor region containing an insulin receptor motif is important for IL-4-mediated IRS-1 phosphorylation and cell growth. Cell 76, 811-820.
22. Keegan, A.D., Johnston, J.A., Tortolani, P.J., McReynolds, L.J., Kinzer, C., O'Shea, J.J., and Paul, W.E. (1995). Similarities and differences in signal transduction by interleukin 4 and interleukin 13: analysis of janus kinase activation. Proc. Natl. Acad. Sci. USA 92, 7681-7685.
23. Kimura, Y., Takeshita, T., Kondo, M., Ishii, N., Nakamura, M., Van Snick, J., and Sugamura, K. (1995). Sharing of the IL-2 receptor γ chain with the functional IL-9 receptor complex. Int. Immunol. 7, 115-120.
24. Kondo, M., Takeshita, T., Ishii, N., Nakamura, M., Watanabe, S., Arai, K., and Sugamura, K. (1993). Sharing of the interleukin-2 (IL-2) receptor γ chain between receptors for IL-2 and IL-4. Science 262, 1874-1877.
25. Kondo, M., Takeshita, T., Higuchi, M., Nakamura, M., Sudo, T., Nishikawa, S., and Sugamura, K. (1994). Functional participation of the IL-2 receptor γ chain in IL-7 receptor complexes. Science 263, 1453-1454.
26. Kuhn, R., Rajewsky, K., and Miller, W. (1991). Generation and analysis of interleukin-4 deficient mice. Science 254, 707-710.
27. Lin, J.X., Migone, T.S., Tsang, M., Friedmann, M., Weatherbee, J.A., Zhou, L., Yamauchi, A., Bloom, E.T., Mietz, J., John, S., and Leonard, W.J. (1995). The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15. Immunity 2, 331-339.
28. Liu, X., Robinson, G.W., Gouilleux, F., Groner, B., and Hennighausen, L. (1995). Cloning and expression of Stat5 and an additional homologue (Stat5b) involved in prolactin signal transduction in mouse mammary tissue. Proc. Natl. Acad. Sci. USA 92, 8831-8835.
29. Macchi, P., Villa, A., Gillani, S., Sacco, M.G., Frattini, A., Porta, F., Ugazio, A.G., Johnston, J.A., Candotti, F., O'Shea, J.J., Vezzoni, P., and Notarangelo, L.D. (1995). Mutations of Jak-3 gene in patients with autosomal severe combined immune deficiency (SCID). Nature 377, 65-68.
30. Matthews, D.J., Clark, P.A., Herbert, J., Morgan, G., Armitage, R.J., Kinnon, C., Minty, A., Grabstein, K.H., Caput, D., Ferrara, P., and Callard, R. (1995). Function of the interleukin-2 (IL-2) receptor γ-chain in biologic responses of X-linked severe combined immunodeficient B cells to IL-2, IL-4, IL-13, and IL-15. Blood 85, 38-42.
31. Miyazaki, T., Kawahara, A., Fujii, H., Nakagawa, Y., Minami, Y., Liu, Z.-J., Oishi, I., Silvennoinen, O., Witthuhn, B.A., Ihle, J.N., and Taniguchi, T. (1994). Functional activation of Jak1 and Jak3 by selective association with IL-2 receptor subunits. Science 266, 1045-1047.
32. Murata, T., Noguchi, P.D., and Puri, R.K. (1996). Receptors for interleukin (IL)-4 do not associate with the common γ chain, and IL-4 induces the phosphorylation of JAK2 tyrosine kinase in human colon carcinoma cells. J. Biol. Chem. 270, 30829-30836.
33. Musso, T., Johnston, J.A., Linnekin, D., Varesio, L., Rowe, T.K., O'Shea, J.J., and McVicar, D.W. (1995). Regulation of JAK3 expression in human monocytes: phosphorylation in response to interleukins 2, 4, and 7. J. Exp. Med. 181, 1425-1431.
34. Noelle, R., Krammer, P.M., Ohara, J., Uhr, J.W., and Vitetta, E.S. (1984). Increased expression of Ia antigens on resting B cells: an additional role for B-cell growth factor. Proc. Natl. Acad. Sci. USA 81, 6149-6153.
35. Noguchi, M., Nakamura, Y., Russell, S.M., Ziegler, S.F., Tsang, M., Cao, X., and Leonard, W.J. (1993a). Interleukin-2 receptor γ chain: a functional component of the interleukin-7 receptor. Science 262, 1877-1880.
36. Noguchi, M., Yi, H., Rosenblatt, H.M., Filipovich, A.H., Adelstein, S., Modi, W.S., McBride, O.W., and Leonard, W.J.(1993b). Interleukin-2 receptor γ chain mutation results in X-linked severe combined immunodeficiency in humans. Cell 73, 147-157.
37. Obiri, N.I., Debinski, W., Leonard, W.J., and Puri, R.K. (1995). Receptor for interleukin 13: interaction with interleukin 4 by a mechanism that does not involve the common γ chain shared by receptors for interleukins 2, 4, 7, 9, and 15. J. Biol. Chem. 270, 8797-8804.
38. Paul, W.E., and Seder, R.A. (1994). Lymphocyte responses and cytokines. Cell 76, 241-251.
39. Puck, J.M., Deschenes, S.M., Porter, J.C., Dutra, A.S., Brown, C.J., Willard, H.F., and Henthorn, P.S. (1993). The interleukin-2 receptor γ chain maps to Xq13.1 and is mutated in X-linked severe combined immunodeficiency, SCIDX1. Hum. Mol. Genet. 2, 1099-1104.
40. Russell, S.M., Keegan, A.D., Harada, N., Nakamura, Y., Noguchi, M., Leland, P., Friedmann, M.C., Miyajima, A., Puri, R.K., Paul, W.E., and Leonard, W.J. (1993). Interleukin-2 receptor γ chain: a functional component of the interleukin-4 receptor. Science 262, 1880-1883.
41. Russell, S.M., Johnston, J.A., Noguchi, M., Kawamura, M., Bacon, C.M., Friedmann, M., Berg, M., McVicar, D.W., Witthuhn, B.A., Silvennoinen, O., Goldman, A.S., Schmalsteig, F.C., Ihle, J.N., O'Shea, J.J., and Leonard, W.J. (1994). Interaction of IL-2R β and γc chains with Jak1 and Jak3: implications for XSCID and XCID. Science 266, 1042-1045.
42. Russell, S.M., Tayebi, N., Nakajima, H., Riedy, M.C., Roberts, J.L., Aman, M.J., Migone, T.S., Noguchi, M., Markert, M.L., Buckley, R.H., O'Shea, J.J., and Leonard, W.J. (1995). Mutation of Jak3 in a patient with SCID: essential role of Jak3 in lymphoid development. Science 270, 797-800.
43. Schindler, C., and Darnell, J.E. (1995). Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64, 621-651.
44. Schnyder, B., Lugli, S., Feng, N., Etter, H., Lutz, R.A., Ryffel, B., Sugamura, K., Wunderli-Allenspach, H., and Moser, R. (1996). Interleukin-4 (IL-4) and IL-13 bind to a shared heterodimeric complex on endothelial cells mediating vascular cell adhesion molecule-1 induction in the absence of the common γ chain. Blood 87, 4286-4295.
45. Sun, X.J., Wang, L.M., Zhanf, Y., Yenush, L., Meyers, M.G., Glasheen, E., Wolf, G., Shoelson, S.E., Lane, W.S., Pierce, J.H., and White, M.F. (1995). Role of IRS-2 in insulin and cytokine signaling. Nature 377, 173-177.
46. Takeshita, T., Asao, H., Ohtani, K., Ishii, N., Kumaki, S., Tanaka, N., Munakata, H., Nakamura, M., and Sugamura, K. (1992). Cloning of the γ chain of the human IL-2 receptor. Science 257, 379-382.
47. Tortolani, P.J., Lal, B.K., Riva, A., Johnston, J.A., Chen, Y.-Q., Reaman, G.H., Beckwith, M., Longo, D., Ortaldo, J.R., Bhatia, K., McGrath, I., Kehrl, J., Tuscano, J., McVicar, D.W., and O'Shea, J.J. (1995). Regulation of JAK3 expression and activation in human B cells and B cell malignancies. J. Immunol. 155, 5220-5226.
48. Wang, L.M., Keegan, A.D., Paul, W.E., Heidaran, M.A., Gutkind, J.S., and Pierce, J.H. (1992). IL-4 activates a distinct signal transduction cascade from IL-3 in factor-dependent myeloid cells. EMBO J. 11, 4899-4908.
49. Wang, L.M., Keegan, A.D., Frankel, M., Paul, W.E., and Pierce, J.H. (1995). Signal transduction through the IL-4 and insulin receptor families. Stem Cells 13, 360-368.
50. Welham, M.J., Learmonth, L., Bone, H., and Schrader, J.W. (1995). Interleukin-13 signal transduction in lymphohemopoietic cells: similarities and differences in signal transduction with interleukin-4 and insulin. J. Biol. Chem. 270, 12286-12296.
51. White, M.F., and Kahn, C.R. (1994). The insulin signaling system. J. Biol. Chem. 269, 1-4.
52. Witthuhn, B.A., Silvennoinen, O., Miura, O., Lai, K.S., Cwik, C., Liu, E.T., and Ihle, J.N. (1994). Involvement of the Jak-3 Janus kinase in signaling by interleukins 2 and 4 in lymphoid and myeloid cells. Nature 370, 153-157.