Stochastic receptor expression determines cell fate upon interferon treatment

Molecular and Cellular Biology

Volumn 31, Issue 16, 2011, Pages 3252-3266

  Levin, Doron ^a   Harari, Daniel ^a   Schreiber, Gideon ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; ALPHA INTERFERON RECEPTOR 1; ALPHA INTERFERON RECEPTOR 2; INTERFERON; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; CELL FATE; CONTROLLED STUDY; GENE INDUCTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING;

CELL LINE, TUMOR; CELL LINEAGE; CELL PROLIFERATION; HUMANS; INTERFERON TYPE I; RECEPTOR, INTERFERON ALPHA-BETA; RNA, SMALL INTERFERING; STAT TRANSCRIPTION FACTORS; STOCHASTIC PROCESSES; TRANSCRIPTIONAL ACTIVATION;

EID: 79961163823     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05251-11     Document Type: Article

References (50)

1. Brierley, M. M., and E. N. Fish. 2002. Review: IFN-alpha/beta receptor interactions to biologic outcomes: understanding the circuitry. J. Interferon Cytokine Res. 22:835-845.
2. Cai, L., N. Friedman, and X. S. Xie. 2006. Stochastic protein expression in individual cells at the single molecule level. Nature 440:358-362.
3. Cajean-Feroldi, C., et al. 2004. Identification of residues of the IFNAR1 chain of the type I human interferon receptor critical for ligand binding and biological activity. Biochemistry 43:12498-12512.
4. Chawla-Sarkar, M., D. W. Leaman, and E. C. Borden. 2001. Preferential induction of apoptosis by interferon (IFN)-beta compared with IFN-alpha2: correlation with TRAIL/Apo2L induction in melanoma cell lines. Clin. Cancer Res. 7:1821-1831.
5. Claudinon, J., M.-N. Monier, and C. Lamaze. 2007. Interfering with interferon receptor sorting and trafficking: impact on signaling. Biochimie 89: 735-743.
6. Cohen, B., D. Novick, S. Barak, and M. Rubinstein. 1995. Ligand-induced association of the type I interferon receptor components. Mol. Cell. Biol. 15:4208-4214.
7. Damdinsuren, B., et al. 2007. Interferon alpha receptors are important for antiproliferative effect of interferon-alpha against human hepatocellular carcinoma cells. Hepatol. Res. 37:77-83.
8. da Silva, A. J., et al. 2002. Comparison of gene expression patterns induced by treatment of human umbilical vein endothelial cells with IFN-alpha 2b versus IFN-beta 1a: understanding the functional relationship between distinct type I interferons that act through a common receptor. J. Interferon Cytokine Res. 22:173-188.
9. Grumbach, I. M., et al. 1999. Activation of the Jak-Stat pathway in cells that exhibit selective sensitivity to the antiviral effects of IFN-beta compared with IFN-alpha. J. Interferon Cytokine Res. 19:797-801.
10. Haller, O., G. Kochs, and F. Weber. 2006. The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344:119-130.
11. Hilkens, C. M. U., J. F. Schlaak, and I. M. Kerr. 2003. Differential responses to IFN-alpha subtypes in human T cells and dendritic cells. J. Immunol. 171:5255-5263.
12. Ito, K., et al. 2004. Initial expression of interferon alpha receptor 2 (IFNAR2) on CD34-positive cells and its down-regulation correlate with clinical response to interferon therapy in chronic myelogenous leukemia. Eur. J. Haematol. 73:191-205.
13. Jacobs, S., E. Hazum, Y. Shechter, and P. Cuatrecasas. 1979. Insulin receptor: covalent labeling and identification of subunits. Proc. Natl. Acad. Sci. U. S. A. 76:4918-4921.
14. Jaitin, D. A., et al. 2006. Inquiring into the differential action of interferons (IFNs): an IFN-alpha2 mutant with enhanced affinity to IFNAR1 is functionally similar to IFN-beta. Mol. Cell. Biol. 26:1888-1897.
15. Jaitin, D. A., and G. Schreiber. 2007. Upregulation of a small subset of genes drives type I interferon-induced antiviral memory. J. Interferon Cytokine Res. 27:653-664.
16. Jaks, E., M. Gavutis, G. Uzé, J. Martal, and J. Piehler. 2007. Differential receptor subunit affinities of type I interferons govern differential signal activation. J. Mol. Biol. 366:525-539.
17. Kalie, E., D. A. Jaitin, R. Abramovich, and G. Schreiber. 2007. An interferon alpha2 mutant optimized by phage display for IFNAR1 binding confers specifically enhanced antitumor activities. J. Biol. Chem. 282:11602-11611.
18. Kalie, E., D. A. Jaitin, Y. Podoplelova, J. Piehler, and G. Schreiber. 2008. The stability of the ternary interferon-receptor complex rather than the affinity to the individual subunits dictates differential biological activities. J. Biol. Chem. 283:32925-32936.
19. Lamken, P., S. Lata, M. Gavutis, and J. Piehler. 2004. Ligand-induced assembling of the type I interferon receptor on supported lipid bilayers. J. Mol. Biol. 341:303-318.
20. Laude, H., and C. La Bonnardiere. 1984. Cytocidal effect of interferons on porcine renal cells. J. Interferon Res. 4:101-110.
21. Leaman, D. W., et al. 2003. Novel growth and death related interferonstimulated genes (ISGs) in melanoma: greater potency of IFN-beta compared with IFN-alpha2. J. Interferon Cytokine Res. 23:745-756.
22. Lemaire, P. A., E. Anderson, J. Lary, and J. L. Cole. 2008. Mechanism of PKR activation by dsRNA. J. Mol. Biol. 381:351-360.
23. Lutfalla, G., et al. 1995. Mutant U5A cells are complemented by an interferon-alpha beta receptor subunit generated by alternative processing of a new member of a cytokine receptor gene cluster. EMBO J. 14:5100-5108.
24. Manche, L., S. R. Green, C. Schmedt, and M. B. Mathews. 1992. Interactions between double-stranded RNA regulators and the protein kinase DAI. Mol. Cell. Biol. 12:5238-5248.
25. Marchetti, M., et al. 2006. Stat-mediated signaling induced by type I and type II interferons (IFNs) is differentially controlled through lipid microdomain association and clathrin-dependent endocytosis of IFN receptors. Mol. Biol. Cell 17:2896-2909.
26. Marijanovic, Z., J. Ragimbeau, J. van der Heyden, G. Uzé, and S. Pellegrini. 2007. Comparable potency of IFNalpha2 and IFNbeta on immediate JAK/STAT activation but differential down-regulation of IFNAR2. Biochem. J. 407:141-151.
27. Meng, F., et al. 2011. Alteration of interferon-α/β receptors in chronic hepatitis B patients. J. Clin. Immunol. [Epub ahead of print.] doi:10.1007/s10875-011-9518-6.
28. Mitsui, Y., and T. Senda. 1997. Elucidation of the basic three-dimensional structure of type I interferons and its functional and evolutionary implications. J. Interferon Cytokine Res. 17:319-326.
29. Moraga, I., D. Harari, G. Schreiber, G. Uzé, and S. Pellegrini. 2009. Recep-tor density is key to the alpha2/beta interferon differential activities. Mol. Cell. Biol. 29:4778-4787.
30. Newman, J. R. S., et al. 2006. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441:840-846.
31. Pearce, K. H., Jr., B. C. Cunningham, G. Fuh, T. Teeri, and J. A. Wells. 1999. Growth hormone binding affinity for its receptor surpasses the requirements for cellular activity. Biochemistry 38:81-89.
32. Pestka, S., C. D. Krause, and M. R. Walter. 2004. Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 202:8-32.
33. Pfeffer, L. M. 1997. Biologic activities of natural and synthetic type I interferons. Semin. Oncol. 24:S9-63-S9-69.
34. Piehler, J., L. C. Roisman, and G. Schreiber. 2000. New structural and functional aspects of the type I interferon-receptor interaction revealed by comprehensive mutational analysis of the binding interface. J. Biol. Chem. 275:40425-40433.
35. Piehler, J., and G. Schreiber. 1999. Biophysical analysis of the interaction of human ifnar2 expressed in E. coli with IFNalpha2. J. Mol. Biol. 289: 57-67.
36. Platanias, L. C. 2005. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 5:375-386.
37. Raj, A., and A. van Oudenaarden. 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:216-226.
38. Rani, M. R., et al. 1996. Characterization of beta-R1, a gene that is selectively induced by interferon beta (IFN-beta) compared with IFN-alpha. J. Biol. Chem. 271:22878-22884.
39. Roisman, L. C., J. Piehler, J. Y. Trosset, H. A. Scheraga, and G. Schreiber. 2001. Structure of the interferon-receptor complex determined by distance constraints from double-mutant cycles and flexible docking. Proc. Natl. Acad. Sci. U. S. A. 98:13231-13236.
40. Roos, G., T. Leanderson, and E. Lundgren. 1984. Interferon-induced cell cycle changes in human hematopoietic cell lines and fresh leukemic cells. Cancer Res. 44:2358-2362.
41. Rosenblum, M. G., et al. 1990. Growth inhibitory effects of interferon-beta but not interferon-alpha on human glioma cells: correlation of receptor binding, ',5'-oligoadenylate synthetase and protein kinase activity. J. Interferon Res. 10:141-151.
42. Rubinstein, M., and S. Pestka. 1981. Purification and characterization of human leukocyte interferons by high-performance liquid chromatography. Methods Enzymol. 78:464-472.
43. Severa, M., et al. 2006. Differential responsiveness to IFN-alpha and IFNbeta of human mature DC through modulation of IFNAR expression. J. Leukoc. Biol. 79:1286-1294.
44. Slutzki, M., D. A. Jaitin, T. B. Yehezkel, and G. Schreiber. 2006. Variations in the unstructured C-terminal tail of interferons contribute to differential receptor binding and biological activity. J. Mol. Biol. 360:1019-1030.
45. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67:227-264.
46. Theofilopoulos, A. N., R. Baccala, B. Beutler, and D. H. Kono. 2005. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 23:307-336.
47. Uzé, G., et al. 1994. Domains of interaction between alpha interferon and its receptor components. J. Mol. Biol. 243:245-257.
48. Velazquez, L., M. Fellous, G. R. Stark, and S. Pellegrini. 1992. A protein tyrosine kinase in the interferon alpha/beta signaling pathway. Cell 70:313-322.
49. Wagner, T. C., et al. 2004. Interferon receptor expression regulates the antiproliferative effects of interferons on cancer cells and solid tumors. Int. J. Cancer 111:32-42.
50. Zheng, L., U. Baumann, and J.-L. Reymond. 2004. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32:e115.