STAT1, STAT3 and p38MAPK are involved in the apoptotic effect induced by a chimeric cyclic interferon-α2b peptide

Experimental Cell Research

Volumn 316, Issue 4, 2010, Pages 603-614

  Blank, Viviana C ^a   Peña, Clara ^a   Roguin, Leonor P ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Apoptosis; Cyclic peptide; IFN 2b; p38 MAPK; STATs

Indexed keywords

ALPHA2B INTERFERON; CHIMERIC PROTEIN; CYCLOPEPTIDE; JANUS KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE TYK2; STAT1 PROTEIN; STAT3 PROTEIN; RECOMBINANT PROTEIN; STAT1 PROTEIN, HUMAN;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL GROWTH; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RNA INTERFERENCE; TUMOR CELL LINE; WISH CELL LINE; CELL CULTURE; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; FLOW CYTOMETRY; HUMANS; INTERFERON ALFA-2B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDES, CYCLIC; PHOSPHORYLATION; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR;

EID: 77449128739     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.11.016     Document Type: Article

References (57)

1. [1] Pestka, S., Langer, J.A., Zoon, K.C., Samuel, C.E., Interferons and their actions. Annu. Rev. Biochem. 56 (1987), 727–777.
2. [2] Langer, J.A., Pestka, S., Interferon receptors. Immunol. Today 9 (1988), 393–400.
3. [3] Viscomi, G.C., Grimaldi, M., Palazzini, E., Silvestri, S., Human leukocyte interferon alpha: structure, pharmacology, and therapeutic applications. Med. Res. Rev. 15 (1995), 445–478.
4. [4] Brierley, M.M., Fish, E.N., Review: IFN-alpha/beta receptor interactions to biologic outcomes: understanding the circuitry. J. Interferon Cytokine Res. 22 (2002), 835–845.
5. [5] Parmar, S., Platanias, L.C., Interferons: mechanisms of action and clinical applications. Curr. Opin. Oncol. 15 (2003), 431–439.
6. [6] Uzé, G., Lutfalla, G., Gresser, I., Genetic transfer of a functional human interferon α receptor into mouse cells: cloning and expression of its cDNA. Cell 60 (1990), 225–234.
7. [7] Novick, D., Cohen, B., Rubinstein, M., The human interferon α/β receptor: characterization and molecular cloning. Cell 77 (1994), 391–400.
8. [8] Domanski, P., Colamonici, O.R., The type-I interferon receptor. The long and short of it. Cytokine Growth Factor Rev. 7 (1996), 143–151.
9. [9] Cutrone, E.C., Langer, L.A., Contributions of cloned type I interferon receptor subunits to differential ligand binding. FEBS Lett. 404 (1997), 197–202.
10. [10] Owczarek, C.M., Hwang, S.Y., Holland, K.A., Gulluyan, L.M., Tavaria, M., Weaver, B., Reich, N.C., Kola, I., Hertzog, P.J., Cloning and characterization of soluble and transmembrane isoforms of a novel component of the murine type I interferon receptor, IFNAR 2. J. Biol. Chem. 272 (1997), 23865–23870.
11. [11] Uddin, S., Platanias, L.C., Mechanisms of type-I interferon signal transduction. J. Biochem. Mol. Biol. 37 (2004), 635–641.
12. [12] Brierley, M.M., Fish, E.N., Stats: multifaceted regulators of transcription. J. Interferon. Cytokine Res. 25 (2005), 733–744.
13. [13] Caraglia, M., Marra, M., Pelaia, G., Maselli, R., Caputi, M., Marisco, S.A., Abbruzzese, A., Alpha-interferon and its effects on signal transduction pathways. J. Cell Physiol. 202 (2005), 323–335.
14. [14] Platanias, L.C., Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 5 (2005), 375–386.
15. [15] Schindler, C., Levy, D.E., Decker, T., JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282 (2007), 20059–20063.
16. [16] Platanias, L.C., The p38 mitogen-activated protein kinase pathway and its role in interferon signalling. Pharmacol. Ther. 98 (2003), 129–142.
17. [17] Kaur, S., Uddin, S., Platanias, L.C., The PI3′ kinase pathway in interferon signalling. J. Interferon. Cytokine Res. 25 (2005), 780–787.
18. [18] Pokrovskaja, K., Panaretakis, T., Grandér, D., Alternative signaling pathways regulating type I interferon-induced apoptosis. J. Interferon Cytokine Res. 25 (2005), 799–810.
19. [19] Hjortsberg, L., Lindvall, C., Corcoran, M., Arulampalam, V., Chan, D., Thyrell, L., Nordenskjold, M., Grandér, D., Pokrovskaja, K., Phosphoinositide 3-kinase regulates a subset of interferon-alpha-stimulated genes. Exp. Cell Res. 313 (2007), 404–414.
20. [20] Mayer, I.A., Verma, A., Grumbach, I.M., Uddin, S., Lekmine, F., Ravandi, F., Majchrzak, B., Fujita, S., Fish, E.N., Platanias, L.C., The p38 MAPK pathway mediates the growth inhibitory effects of interferon-alpha in BCR-ABL-expressing cells. J. Biol. Chem. 276 (2001), 28570–28577.
21. [21] Verma, A., Deb, D.K., Sassano, A., Uddin, S., Varga, J., Wickrema, A., Platanias, L.C., Activation of the p38 mitogen-activated protein kinase mediates the suppressive effects of type I interferons and transforming growth factor-beta on normal hematopoiesis. J. Biol. Chem. 277 (2002), 7726–7735.
22. [22] Peña, C., Blank, V.C., Marino, V.J., Roguin, L.P., Synthesis and biological properties of chimeric interferon-alpha 2b peptides. Peptides 26 (2005), 1144–1149.
23. [23] Blank, V.C., Peña, C., Roguin, L.P., cyclic chimeric, A, interferon-α2b peptide induces apoptosis in tumor cells. Cancer Biol. Ther. 6 (2007), 1787–1793.
24. [24] Blank, V.C., Peña, C., Roguin, L.P., Suitable experimental conditions are required to characterize IFN-α2b synthetic peptides. Eur. J. Biochem. 267 (2000), 5711–5716.
25. [25] Landegren, U., Measurement of cell numbers by means of the endogenous enzyme hexosaminidase. Applications to detection of lymphokines and cell surface antigens. J. Immunol. Methods 67 (1984), 379–388.
26. [26] Wen, Z., Zhong, Z., Darnell, J.E. Jr, Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82 (1995), 241–250.
27. [27] Wen, Z., Darnell, J.E. Jr, Mapping of Stat3 serine phosphorylation to a single residue (727) and evidence that serine phosphorylation has no influence on DNA binding of Stat1 and Stat3. Nucleic Acids Res. 25 (1997), 2062–2067.
28. [28] Horvath, C.M., STAT proteins and transcriptional responses to extracellular signals. Trends Biochem. Sci. 25 (2000), 496–502.
29. [29] Panaretakis, T., Hjortsberg, L., Tamm, K.P., Björklund, A.C., Joseph, B., Grandér, D., Interferon alpha induces nucleus-independent apoptosis by activating extracellular signal-regulated kinase 1/2 and c-Jun NH2-terminal kinase downstream of phosphatidylinositol 3-kinase and mammalian target of rapamycin. Mol. Biol. Cell 19 (2008), 41–50.
30. [30] Young, P.R., McLaughlin, M.M., Kumar, S., Kassis, S., Doyle, M.L., McNulty, D., Gallagher, T.F., Fisher, S., McDonnell, P.C., Carr, S.A., Huddleston, M.J., Seibel, G., Porter, T.G., Livi, G.P., Adams, J.L., Lee, J.C., Pyridinyl imidazole inhibitors of p38 mitogen-activated protein kinase bind in the ATP site. J. Biol. Chem. 272 (1997), 12116–12121.
31. [31] Fish, E.N., Definition of receptor binding domains in interferon-α. J. Interferon Res. 12 (1992), 257–266.
32. [32] Uzé, G., Di Marco, S., Mouchel-Vielh, E., Monneron, D., Bandu, M.T., Horisberger, M.A., Dorques, A., Lutfalla, G., Mogensen, K.E., Domains of interaction between alpha interferon and its receptor components. J. Mol. Biol. 243 (1994), 245–257.
33. [33] Klaus, W., Gsell, B., Labhardt, A.M., Wipf, B., Senn, H., The three-dimensional high resolution structure of human interferon α-2a determined by heteronuclear NMR spectroscopy in solution. J. Mol. Biol. 274 (1997), 661–675.
34. [34] Piehler, J., Roisman, L.C., Schreiber, G., New structural and functional aspects of the type I interferon-receptor interaction revealed by comprehensive mutational analysis of the binding interface. J. Biol. Chem. 275 (2000), 40425–40433.
35. [35] Chill, J.H., Quadt, S.R., Levy, R., Schreiber, G., Anglister, J., The human type, I, interferon receptor: NMR structure reveals the molecular basis of ligand binding. Structure 11 (2003), 791–802.
36. [36] Quadt-Akabayov, S.R., Chill, J.H., Levy, R., Kessler, N., Anglister, J., Determination of the human type I interferon receptor binding site on human interferon-alpha2 by cross saturation and an NMR-based model of the complex. Protein Sci. 15 (2006), 2656–2668.
37. [37] Kumaran, J., Wei, L., Kotra, L.P., Fish, E.N., A structural basis for interferon-alpha-receptor interactions. FASEB J. 21 (2007), 3288–3296.
38. [38] Cajean-Feroldi, C., Nosal, F., Nardeux, P.C., Gallet, X., Guymarho, J., Baychelier, F., Sempé, P., Tovey, M.G., Escary, J.L., Eid, P., Identification of residues of the IFNAR1 chain of the type I human interferon receptor critical for ligand binding and biological activity. Biochemistry 43 (2004), 12498–12512.
39. [39] Pan, M., Kalie, E., Scaglione, B.J., Raveche, E.S., Schreiber, G., Langer, J.A., Mutation of the IFNAR-1 receptor binding site of human IFN-alpha2 generates type I IFN competitive antagonists. Biochemistry 47 (2008), 12018–12027.
40. [40] Velichko, S., Wagner, T.C., Turkson, J., Jove, R., Croze, E., STAT3 activation by type I interferons is dependent on specific tyrosines located in the cytoplasmic domain of interferon receptor chain 2c. Activation of multiple STATS proceeds through the redundant usage of two tyrosine residues. J. Biol. Chem. 277 (2002), 35635–35641.
41. [41] Nguyen, V.P., Saleh, A.Z., Arch, A.E., Yan, H., Piazza, F., Kim, J., Krolewski, J.J., Stat2 binding to the interferon-alpha receptor 2 subunit is not required for interferon-alpha signaling. J. Biol. Chem. 277 (2002), 9713–9721.
42. [42] Yan, H., Krishnan, K., Greenlund, A.C., Gupta, S., Lim, J.T., Schreiber, R.D., Schindler, C.W., Krolewski, J.J., Phosphorylated interferon-alpha receptor 1 subunit (IFNaR1) acts as a docking site for the latent form of the 113 kDa STAT2 protein. EMBO J. 15 (1996), 1064–1074.
43. [43] Leung, S., Qureshi, S.A., Kerr, I.M., Darnell, J.E. Jr., Stark, G.R., Role of STAT2 in the alpha interferon signaling pathway. Mol. Cell. Biol. 15 (1995), 1312–1317.
44. [44] Qureshi, S.A., Leung, S., Kerr, I.M., Stark, G.R., Darnell, J.E. Jr., Function of Stat2 protein in transcriptional activation by alpha interferon. Mol. Cell. Biol. 16 (1996), 288–293.
45. [45] Goh, K.C., Haque, S.J., Williams, B.R., p38 MAP kinase is required for STAT1 serine phosphorylation and transcriptional activation induced by interferons. EMBO J. 18 (1999), 5601–5608.
46. [46] Uddin, S., Lekmine, F., Sharma, N., Majchrzak, B., Mayer, I., Young, P.R., Bokoch, G.M., Fish, E.N., Platanias, L.C., The Rac1/p38 mitogen-activated protein kinase pathway is required for interferon alpha-dependent transcriptional activation but not serine phosphorylation of Stat proteins. J. Biol. Chem. 275 (2000), 27634–27640.
47. [47] Ramsauer, K., Sadzak, I., Porras, A., Pilz, A., Nebreda, A.R., Decker, T., Kovarik, P., p38 MAPK enhances STAT1-dependent transcription independently of Ser-727 phosphorylation. Proc. Natl. Acad. Sci. U. S. A 99 (2002), 12859–12864.
48. [48] Uddin, S., Sassano, A., Deb, D.K., Verma, A., Majchrzak, B., Rahman, A., Malik, A.B., Fish, E.N., Platanias, L.C., Protein kinase C-delta (PKC-delta) is activated by type I interferons and mediates phosphorylation of Stat1 on serine 727. J. Biol. Chem. 277 (2002), 14408–14416.
49. [49] Kaur, S., Parmar, S., Smith, J., Katsoulidis, E., Li, Y., Sassano, A., Majchrzak, B., Uddin, S., Tallman, M.S., Fish, E.N., Platanias, L.C., Role of protein kinase C-delta (PKC-delta) in the generation of the effects of IFN-alpha in chronic myelogenous leukemia cells. Exp. Hematol. 33 (2005), 550–557.
50. [50] Bromberg, J.F., Horvath, C.M., Wen, Z., Schreiber, R.D., Darnell, J.E. Jr., Transcriptionally active Stat1 is required for the antiproliferative effects of both interferon alpha and interferon gamma. Proc. Natl. Acad. Sci. U.S.A. 93 (1996), 7673–7678.
51. [51] Bromberg, J.F., Darnell, J.E. Jr, The role of STATs in transcriptional control and their impact on cellular function. Oncogene 19 (2000), 2468–2473.
52. [52] Shen, Y., Devgan, G., Darnell, J.E. Jr., Bromberg, J.F., Constitutively activated Stat3 protects fibroblasts from serum withdrawal and UV-induced apoptosis and antagonizes the proapoptotic effects of activated Stat1. Proc. Natl. Acad. Sci. U.S.A. 98 (2001), 1543–1548.
53. [53] Thyrell, L., Arulampalam, V., Hjortsberg, L., Farnebo, M., Grandér, D., Pokrovskaja Tamm, K., Interferon alpha induces cell death through interference with interleukin 6 signaling and inhibition of STAT3 activity. Exp. Cell. Res. 313 (2007), 4015–4024.
54. [54] 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.
55. [55] Eriksen, K.W., Søndergaard, H., Woetmann, A., Krejsgaard, T., Skak, K., Geisler, C., Wasik, M.A., Odum, N., The combination of IL-21 and IFN-alpha boosts STAT3 activation, cytotoxicity and experimental tumor therapy. Mol. Immunol. 46 (2009), 812–820.
56. [56] Caraglia, M., Abbruzzese, A., Leardi, A., Pepe, S., Budillon, A., Baldassare, G., Selleri, C., Lorenzo, S.D., Fabbrocini, A., Giuberti, G., Vitale, G., Lupoli, G., Bianco, A.R., Tagliaferri, P., Interferon-alpha induces apoptosis in human KB cells through a stress-dependent mitogen activated protein kinase pathway that is antagonized by epidermal growth factor. Cell. Death Differ. 6 (1999), 773–780.
57. [57] Li, C., Chi, S., He, N., Zhang, X., Guicherit, O., Wagner, R., Tyring, S., Xie, J., IFNalpha induces Fas expression and apoptosis in hedgehog pathway activated BCC cells through inhibiting Ras-Erk signalling. Oncogene 23 (2004), 1608–1617.