Interferon induces the interaction of prothymosin-α with STAT3 and results in the nuclear translocation of the complex

Experimental Cell Research

Volumn 298, Issue 1, 2004, Pages 197-206

  Yang, Chuan He ^a   Murti, Aruna ^a   Baker, Suzanne J ^b   Frangou Lazaridis, Maria ^c   Vartapetian, Andrey B ^d   Murti, K Gopal ^b   Pfeffer, Lawrence M ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF IOANNINA   (Greece)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Gene transcription; Interferon; Nuclear localization signal; Prothymosin ; STAT; STAT3; Tyrosine phosphorylation; Yeast two hybrid

Indexed keywords

INTERFERON; PROTEIN TYROSINE KINASE; PROTHYMOSIN ALPHA; STAT3 PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL SURVIVAL; CHROMATIN; CONTROLLED STUDY; CYTOPLASM; FIBROBLAST; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENE TRANSLOCATION; GROWTH REGULATION; HOST RESISTANCE; HYBRID; IMMUNOMODULATION; MAMMAL CELL; MONKEY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; YEAST CELL;

MAMMALIA;

EID: 3042823705     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.04.008     Document Type: Article

References (43)

1. Friedman R.L., Stark G.R. α-Interferon-induced transcription of HLA and metallothionein genes containing homologous upstream sequences. Nature. 314:1985;637-639
2. Larner A.C., Chaudhuri A., Darnell J.E.J. Transcriptional induction by interferon: new protein(s) determine the length and extent of induction. J. Biol. Chem. 261:1986;453-459
3. Darnell J.E.J., Kerr I.M., Stark G.R. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science. 264:1994;1415-1421
4. Boulton T., Zhong Z., Wen Z., Darnell J.E.J., Stahl N., Yancopoulos G.D. STAT3 activation by cytokines utilizing gp130 and related transducers involves a secondary modification requiring a H7-sensitive kinase. Proc. Natl. Acad. Sci. U. S. A. 92:1995;6915-6919
5. Campbell G.S., Meyer D.J., Raz R., Levy D.E., Schwartz J., Carter-Su C. Activation of the acute phase response factor (APRF)/STAT3 transcription factor by growth hormone. J. Biol. Chem. 270:1995;3974-3979
6. Yang C.H., Shi W., Basu L., Murti A., Constantinescu S.N., Blatt L., Croze E., Mullersman J.E., Pfeffer L.M. Direct association of STAT3 with the IFNAR1 signal transducing chain of the type I IFN receptor. J. Biol. Chem. 271:1996;8057-8061
7. Pfeffer L.M., Mullersman J.E., Pfeffer S.R., Murti A., Shi W., Yang C.H. STAT3 as an adapter to couple phosphatidylinositol-3 kinase to the IFNAR-1 chain of the type I IFN receptor. Science. 276:1997;1418-1420
8. Yang C.H., Murti A., Pfeffer L.M. STAT3 complements defects in an interferon-resistant cell line: evidence for an essential role for STAT3 in interferon signaling and biological activities. Proc. Natl. Acad. Sci. U. S. A. 95:1998;5568-5572
9. Haritos A.A., Blacher R., Stein S., Caldarella J., Horecker B.L. Primary structure of rat thymus prothymosin alpha. Proc. Natl. Acad. Sci. U. S. A. 82:1985;343-346
10. Manrow R.E., Sburlati A.R., Hanover J.A., Berger S.L. Nuclear targeting of prothymosin alpha. J. Biol. Chem. 266:1991;3916-3924
11. Gomez-Marquez J., Rodriguez P. Prothymosin alpha is a chromatin-remodelling protein in mammalian cells. Biochem. J. 333:1998;1-3
12. Orre R.S., Cotter M.A. II, Subramanian C., Robertson E.S. Prothymosin alpha functions as a cellular oncoprotein by inducing transformation of rodent fibroblasts in vitro. J. Biol. Chem. 276:2001;1794-1799
13. Ausable F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. Current protocols in molecular biology. 2003;5.8.1-5.8.8 Wiley, Hoboken, NJ
14. Vidal M., Brachmann R.K., Fattaey A., Harlow E., Boeke J.D. Reverse two-hybrid and one-hybrid systems to detect dissociation of protein-protein and DNA-protein interactions. Proc. Natl. Acad. Sci. U. S. A. 93:1996;10315-10320
15. Keegan K., Cooper J.A. Use of the two hybrid system to detect the association of the protein-tyrosine-phosphatase, SHPTP2, with another SH2-containing protein, Grb7. Oncogene. 12:1996;1537-1544
16. Chevray P.M., Nathans D. Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun. Proc. Natl. Acad. Sci. U. S. A. 89:1992;5789-5793
17. Trumbore M.W., Wang R.H., Enkelmann S.A., Berger S.L. Prothymosin. J. Biol. Chem. 272:1997;26394-26404
18. Guan K., Dixon J.E. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192:1991;262-267
19. Smith D.B., Johnson K.S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 67:1988;31-40
20. Evstafieva A.G., Belov G.A., Rubtsov Y.P., Kalkum M., Joseph B., Chichkova N.V., Sukhacheva E.A., Bogdanov A.A., Pettersson R.F., Agol V.I., Vartapetian A.B. Apoptosis-related fragmentation, translocation, and properties of human prothymosin alpha. Exp. Cell Res. 284:2003;211-223
21. Murti K.G., Brown P.S., Kumagai M., Campana D. Molecular interactions between human B-cell progenitors and the bone marrow microenvironment. Exp. Cell Res. 226:1996;47-58
22. Vareli K., Frangou-Lazaridis M., van der Kraan I., Tsolas O., van Driel R. Nuclear distribution of prothymosin alpha and parathymosin: evidence that prothymosin alpha is associated with RNA synthesis processing and parathymosin with early DNA replication. Exp. Cell Res. 257:2000;152-161
23. Pfeffer L.M., Yang C.H., Pfeffer S.R., Murti A., McCormack S.A., Johnson L.R. Inhibition of ornithine decarboxylase induces STAT3 tyrosine phosphorylation and DNA-binding in IEC-6 cells. Am. J. Physiol.: Cell Physiol. 278:2000;C331-C335
24. Becker S., Groner B., Muller C.W. Three-dimensional structure of the Stat3beta homodimer bound to DNA. Nature. 394:1998;145-151
25. Chen X., Vinkemeier U., Zhao Y., Jeruzalmi D., Darnell J.E. Jr., Kuriyan J. Crystal structure of a tyrosine phosphorylated STAT-1 dimer bound to DNA. Cell. 93:1998;827-839
26. Vinkemeier U., Cohen S.L., Moarefi I., Chait B.T., Kuriyan J., Darnell J.E. Jr. DNA binding of in vitro activated Stat1 alpha, Stat1 beta and truncated Stat1: interaction between NH2-terminal domains stabilizes binding of two dimers to tandem DNA sites. EMBO J. 15:1996;5616-5626
27. Xu X., Sun Y.L., Hoey T. Cooperative DNA binding and sequence-selective recognition conferred by the STAT amino-terminal domain. Science. 273:1996;794-797
28. Zhang T., Kee W.H., Seow K.T., Fung W., Cao X. The coiled-coil domain of Stat3 is essential for its SH2 domain-mediated receptor binding and subsequent activation induced by epidermal growth factor and interleukin-6. Mol. Cell. Biol. 20:2000;7132-7139
29. Sburlati A.R., De La Rosa A., Batey D.W., Kurys G.L., Manrow R.E., Pannell L.K., Martin B.M., Sheeley D.M., Berger S.L. Phosphorylation of human and bovine prothymosin alpha in vivo. Biochemistry. 32:1993;4587-4596
30. Sburlati A.R., Manrow R.E., Berger S.L. Human prothymosin alpha: purification of a highly acidic nuclear protein by means of a phenol extraction. Protein Expression Purif. 1:1990;184-190
31. Enkemann S.A., Ward R.D., Berger S.L. Mobility within the nucleus and neighboring cytosol is a key feature of prothymosin-alpha. J. Histochem. Cytochem. 48:2000;1341-1355
32. Rubtsov Y.P., Zolotukhin A.S., Vorobjev I.A., Chichkova N.V., Pavlov N.A., Karger E.M., Evstafieva A.G., Felber B.K., Vartapetian A.B. Mutational analysis of human prothymosin alpha reveals a bipartite nuclear localization signal. FEBS Lett. 413:1997;135-141
33. Gomez-Marquez J., Segade F., Dosil M., Pichel J.G., Bustelo X.R., Freire M. The expression of prothymosin alpha gene in T lymphocytes and leukemic lymphoid cells is tied to lymphocyte proliferation. J. Biol. Chem. 264:1989;8451-8454
34. Silverman A.L., Smith M.R., Sasaki D., Mutchnick M.G., Diehl A.M. Altered levels of prothymosin immunoreactive peptide, a growth-related gene product, during liver regeneration after chronic ethanol feeding. Alcohol. Clin. Exp. Res. 18:1994;616-619
35. Sburlati A.R., Manrow R.E., Berger S.L. Prothymosin alpha antisense oligomers inhibit myeloma cell division. Proc. Natl. Acad. Sci. U. S. A. 88:1991;253-257
36. Rodriguez P., Vinuela J.E., Alvarez-Fernandez L., Gomez-Marquez J. Prothymosin alpha antisense oligonucleotides induce apoptosis in HL-60 cells. Cell Death Differ. 6:1999;3-5
37. Jiang X., Kim H.E., Shu H., Zhao Y., Zhang H., Kofron J., Donnelly J., Burns D., Ng S.C., Rosenberg S., Wang X. Distinctive roles of PHAP proteins and prothymosin-alpha in a death regulatory pathway. Science. 299:2003;223-226
38. Rodriguez P., Vinuela J.E., Alvarez-Fernandez L., Buceta M., Vidal A., Dominguez F., Gomez-Marquez J. Overexpression of prothymosin alpha accelerates proliferation and retards differentiation in HL-60 cells. Biochem. J. 1998;753-761
39. Subramanian C., Hasan S., Rowe M., Hottiger M., Orre R., Robertson E.S. Epstein-Barr virus nuclear antigen 3C and prothymosin alpha interact with the p300 transcriptional coactivator at the CH1 and CH3/HAT domains and cooperate in regulation of transcription and histone acetylation. J. Virol. 76:2002;4699-4708
40. Karetsou Z., Kretsovali A., Murphy C., Tsolas O., Papamarcaki T. Prothymosin alpha interacts with the CREB-binding protein and potentiates transcription. EMBO Rep. 3:2002;361-366
41. Yang C.H., Murti A., Pfeffer S.R., Kim J.G., Donner D.B., Pfeffer L.M. Interferon α/β promotes cell survival by activating NF-kB through phosphatidylinositol-3 kinase and Akt. J. Biol. Chem. 276:2001;13756-13761
42. Bhattacharya S., Eckner R., Grossman S., Oldread E., Arany Z., D'Andrea A., Livingston D.M. Cooperation of Stat2 and p300/CBP in signalling induced by interferon-alpha. Nature. 383:1996;344-347
43. Yang C.H., Murti A., Basu L., Kim J.G., Pfeffer L.M. IFNα/β promotes cell survival by activating NF-κB. Proc. Natl. Acad. Sci. U. S. A. 97:2000;13631-13636