B cell antigen receptor signaling enhances IFN-γ-induced Stat1 target gene expression through calcium mobilization and activation of multiple serine kinase pathways

Journal of Interferon and Cytokine Research

Volumn 25, Issue 2, 2005, Pages 113-124

  Xu, Weifeng ^a   Nair, Jayasree S ^a   Malhotra, Ajay ^a   Zhang, J Jillian ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE ANTIGEN; B LYMPHOCYTE RECEPTOR; GAMMA INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN SERINE KINASE; SERINE; STAT1 PROTEIN; T LYMPHOCYTE RECEPTOR;

ARTICLE; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVATION; GENE TARGETING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

EID: 13844270617     PISSN: 10799907     EISSN: None     Source Type: Journal    
DOI: 10.1089/jir.2005.25.113     Document Type: Article

References (50)

1. DARNELL, J.E., Jr., KERR, I.M., and STARK, G.M. (1994). Jak-Stat pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421.
2. BACH, E.A., AGUET, M., and SCHREIBER, R.D. (1997). The IFN gamma receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15, 563-591.
3. STARK, G.R., KERR, I.M., WILLIAMS, B.R., SILVERMAN, R.H., and SCHREIBER, R.D. (1998). How cells respond to interferons. Annu. Rev. Biochem. 67, 227-264.
4. BOEHM, U., KLAMP, T., GROOT, M., and HOWARD, J.C. (1997). Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15, 749-795.
5. FINKELMAN, F.D., KATONA, I.M., MOSMANN, T.R., and COFFMAN, R.L. (1988). IFN-gamma regulates the isotypes of immunoglobulin secreted during the in vivo humoral immune response. J. Immunol. 140, 1022-1032.
6. SNAPPER, C.M., PESCHEL, C., and PAUL, W.E. (1988). IFN-gamma stimulates IgG2a secretion by murine B cells stimulated with bacterial lipopolysaccharide. J. Immunol. 140, 2121-2129.
7. LU, B., EBENSPERGER, C., DEMBIC, Z., WANG, Y., KVATYUK, M., LU, T., COFFMAN, R.L., PESTKA, S., and ROTHMAN, P.B. (1998). Targeted disruption of the interferon-gamma receptor 2 gene results in severe immune defects in mice. Proc. Natl. Acad. Sci. USA 95, 8233-8238.
8. LEVY, D.E., and DARNELL, J.E., Jr. (2002). Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3, 651-662.
9. O'SHEA, J.J., GADINA, M., and SCHREIBER, R.D. (2002). Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109(Suppl.) S121-131.
10. SHUAI, K., and LIU, B. (2003). Regulation of Jak-Stat signaling in the immune system. Nat. Rev. Immunol. 3, 900-911.
11. DARNELL, J.E., Jr. (1997). Stats and gene regulation. Science 277, 1630-1635.
12. BECKER, S., GRONER, B., and MULLER, C.W. (1998). Three-dimensional structure of the Stat3beta homodimer bound to DNA. Nature 394, 145-151.
13. CHEN, X., VINKEMEIER, U., ZHAO, Y., JERUZALMI, D., DARNELL, J.E., Jr., and KURIYAN, J. (1998). Crystal structure of a tyrosine phosphorylated Stat-1 dimer bound to DNA. Cell 93, 827-839.
14. VINKEMEIER, U., MOAREFI, I., DARNELL, J.E., Jr., and KURIYAN, J. (1998). Structure of the amino-terminal protein interaction domain of Stat-4. Science 279, 1048-1052.
15. SHUAI, K., HORVATH, C.M., TSAI-HUANG, L.H., QURESHI, S., COWBURN, D., and DARNELL, J.E., Jr. (1994). Interferon activation of the transcription factor Stat91 involves dimerization through SH2-phosphotyrosyl peptide interactions. Cell 76, 821-828.
16. HEIM, M.H., KERR, I.M., STARK, G.R., and DARNELL, J.E., Jr. (1995). Stat SH2 groups contribute to specific interferon signaling by the Jak-Stat pathway. Science 267, 1347-1349.
17. SHUAI, K., STARK, G.R., KERR, I.M., and DARNELL, J.E., Jr. (1993). A single phosphotyrosine residue of Stat91 required for gene activation by interferon-γ. Science 261, 1744-1746.
18. BHATTACHARYA, S., ECKNER, R., GROSSMAN, S., OLDREAD, E., ARANY, Z., D'ANDREA, A., and LIVINGSTON, D.M. (1996). Cooperation of Stat2 and p300/CBP in signalling induced by interferon-alpha. Nature 383, 344-347.
19. LU, B., REICHEL, M., FISHER, D.A., SMITH, J.F., and ROTHMAN, P. (1997). Identification of a Stat6 domain required for IL-4-induced activation of transcription. J. Immunol. 159, 1255-1264.
20. MORIGGL, R., BERCHTOLD, S., FRIEDRICH, K., STANDKE, G.J., KAMMER, W., HEIM, M., WISSLER, M. STOCKLIN, E., GOUILLEUX, F., and GRONER, B. (1997). Comparison of the transactivation domain of Stat5 and Stat6 in lymphoid cells and mammary epithelial cells. Mol. Cell. Biol. 17, 3663-3678.
21. ZHANG, J.J., ZHAO, Y., CHAIT, B.T., LATHEM, W.W., RITZI, M., KNIPPERS, R., and DARNELL, J.R., Jr. (1998). Ser727-dependent recruitment of MCM5 by Stat1alpha in IFN-gamma-induced transcriptional activation. EMBO J. 17, 6963-6971.
22. WEN, Z., ZHONG, Z., and DARNELL, J.E., Jr. (1995). Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82, 241-250.
23. MORINOBU, A., GADINA, M., STROBER, W., VISCONTI, R., FORNACE, A., MONTAGNA, C., FELDMAN, G., NISHIKOMORI, R., and O'SHEA, J.J. (2002). Stat4 serine phosphorylation is critical for IL-12-induced IFN production but not for cell proliferation. Proc. Natl. Acad. Sci. USA 99, 12281-12286.
24. LU, B., REICHEL, M., FISHER, D.A., SMITH, J.F., and ROTHMAN, P. (1997). Identification of a Stat6 domain required for IL-4-induced activation of transcription. J. Immunol. 159, 1255-1264.
25. WICK, K.R., and BERTON, M.T. (2000). IL-4 induces serine phosphorylation of the Stat6 transactivation domain in B lymphocytes. Mol. Immunol. 37, 641-652.
26. MERAZ, M.A., WHITE, J.M., SHEEHAN, K.C.F., BACH, E.A., RODIG, S.J., DIGHE, A.S., KAPLAN, D.H., RILEY, J.K., GREENLUND, A.C., CAMPBELL, D., CARVER-MOORE, K., DUBOIS, R.N., CLARK, R., AGUET, M., and SCHREIBER, R.D. (1996). Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the Jak-Stat signaling pathway. Cell 84, 431-442.
27. DURBIN, J.E., HACKENMILLER, R., SIMON, M.C., and LEVY, D.E. (1996). Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84, 443-450.
28. VARINOU, L., RAMSAUER, K., KARAGHIOSOFF, M., KOLBE, T., PFEFFER, K., MULLER, M., and DECKER, T. (2003). Phosphorylation of the Stat1 transactivation domain is required for full-fledged IFN-gamma-dependent innate immunity. Immunity 19, 793-802.
29. KOVARIK, P., STOIBER, D., NOVY, M., and DECKER, T. (1998). Stat1 combines signals derived from IFN-gamma and LPS receptors during macrophage activation. EMBO J. 17, 3660-3668.
30. KOVARIK, P., STOIBER, D., EYERS, P.A., MENGHINI, R., NEININGER, A., GAESTEL, M., COHEN, P., and DECKER, T. (1999). Stress-induced phosphorylation of Stat1 at Ser727 requires p38 mitogen-activated protein kinase whereas IFN-gamma uses a different signaling pathway. Proc. Natl. Acad. Sci. USA 96, 13956-13961.
31. LAFONT, V., DECKER, T., and CANTRELL, D. (2000). Antigen receptor signal transduction: activating and inhibitory antigen receptors regulate Stat1 serine phosphorylation. Eur. J. Immunol. 30, 1851-1860.
32. SU, L., RICKERT, R.C., and DAVID, M. (1999). Rapid Stat phosphorylation via the B cell receptor: modulatory role of cd19. J. Biol. Chem. 274, 31770-31774.
33. GAMERO, A.M., and LARNER, A.C. (2000). Signaling via the T cell antigen receptor induces phosphorylation of Stat1 on serine 727. J. Biol. Chem. 275, 16574-16578.
34. 2+ and CaMKII for Stat1 Ser 727 phosphorylation in response to IFN-gamma. Proc. Natl. Acad. Sci. USA 99, 5971-5976.
35. KUROSAKI, T. (1999). Genetic analysis of B cell antigen receptor signaling. Annu. Rev. Immunol. 17, 555-592.
36. YANG, E., HENRIKSEN, M.A., SCHAEFER, O., ZAKHAROVA, N., and DARNELL, J.E., Jr. (2002). Dissociation time from DNA determines transcriptional function in a Stat1 linker mutant. J. Biol. Chem. 277, 13455-13462.
37. DO, R.K., HATADA, E., LEE, H., TOURIGNY, M.R., HILBERT, D., and CHEN-KIANG, S. (2000). Attenuation of apoptosis underlies B lymphocyte stimulator enhancement of humoral immune response. J. Exp. Med. 192, 953-964.
38. YANG, E., WEN, Z., HASPEL, R.L., ZHANG, J.J., and DARNELL, J.E., Jr. (1999). The linker domain of Stat1 is required for gamma interferon-driven transcription. Mol. Cell. Biol. 19, 5106-5112.
39. BOOTMAN, M.D., COLLINS, T.J., PEPPIATT, C.M., PROTHERO, L.S., MACKENZIE, L., DE SMET, P., TRAVERS, M., TOVEY, S.C., SEO, J.T., BERRIDGE, M.J., CICCOLINI, F., and LIPP, P. (2001). Calcium signalling - an overview. Semin. Cell Dev. Biol. 12, 3-10.
40. SANTELLA, L., and CARAFOLI, E. (1997). Calcium signaling in the cell nucleus. FASEB J. 11, 1091-1109.
41. MARRERO, M.B., SCHIEFFER, B., PAXTON, W.G., HEERDT, L., BERK, B.C., DELAFONTAINE, P., and BERNSTEIN, K.E. (1995). Direct stimulation of Jak/Stat pathway by the angiotensin II AT1 receptor. Nature 375, 247-250.
42. RAM, P.T., HORVATH, C.M., and IYENGAR, R. (2000). Stat3-mediated transformation of NIH-3T3 cells by the constitutively active Q205L go protein. Science 287, 142-144.
43. MELLADO, M., RODRÍGUEZ-FRADE, J.M., MAÑES, S., and MARTÍNEZ-A, C. (2001). Chemokine signaling and functional responses: the role of receptor dimerization and TK pathway activation. Annu. Rev. Immunol. 19, 397-421.
44. DAFONSECA, C.J., SHU, F., and ZHANG, J.J. (2001). Identification of two residues in MCM5 critical for the assembly of MCM complexes and Stat1-mediated transcription activation in response to IFN-gamma. Proc. Natl. Acad. Sci. USA 98, 3034-3039.
45. ZHANG, J.J., VINKEMEIER, U., GU, W., CHAKRAVARTI, D., HORVATH, C.M., and DARNELL, J.E., Jr. (1996). Two contact regions between Stat1 and CBP/p300 in interferon gamma signaling. Proc. Natl. Acad. Sci. USA 93, 15092-15096.
46. CHRIVIA, J.C., KWOK, R.P.S., LAMB, N., HAGIWARA, M., MONTMINY, M.R., and GOODMAN, R.H. (1993). Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-859.
47. ECKNER, R., EWEN, M.E., NEWSOME, D., GERDES, M., DECAPRIO, J.A., LAWRENCE, J.B., and LIVINGSTON, D.M. (1994). Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes Dev. 8, 869-884.
48. PAULSON, M., PISHARODY, S., PAN, L., GUADAGNO, S., MUI, A.L., and LEVY, D.E. (1999). Stat protein transactivation domains recruit p300/CBP through widely divergent sequences. J. Biol. Chem. 274, 25343-25349.
49. ZAKHAROVA, N., LYMAR, E.S., YANG, E., MALIK, S. ZHANG, J.J., ROEDER, R.G., and DARNELL, J.E., Jr. (2003). Distinct transcriptional activation functions of Stat1a and Stat1b on DNA and chromatin templates. J. Biol. Chem. 278, 43067-43073.
50. SHEN, Y., SCHLESSINGER, K., ZHU, X., MEFFRE, E., QUIMBY, F., LEVY, D., and DARNELL, J.E., Jr. (2004). Essential role of Stat3 in postnatal survival and growth revealed by mice lacking Stat3 serine 727 phosphorylation. Mol. Cell. Biol. 24, 407-419.