Endocytosis of the IFNAR1 chain of Type 1 interferon receptor is regulated by diverse E2 ubiquitin conjugation enzymes
Аннотация
Ubiquitination of signaling receptors triggers their endocytosis to restrict the extent of cell signaling. Type 1 interferon (IFN1) eliminates its receptor from cell surface via stimulating the ubiquitination of its IFNAR1 chain. While it was suggested that this ubiquitination aids IFNAR1
internalization via relieving a steric hindrance of a linear motif within IFNAR1 from the endocytic machinery, the mechanisms involved remain poorly understood. Here we describe a specific role for two disparate ubiquitin acceptor sites within this receptor. These sites, Lys501 and Lys525 / 526, exhibit a preference for polyubiquitination via either Lys63- or Lys48‑linked chains (K63‑Ub and K48‑Ub, respectively). Whereas the SCFβTrcp E3 ubiquitin ligase controls either type of ubiquitination-dependent IFNAR1 endocytosis, the specificity of these processes is determined by two different E2 ubiquitin conjugating enzymes, Ubc13 and Cdc34. These enzymes can be directly used by SCFβTrcp E3 ubiquitin ligase to generate either K63‑Ub or K48‑Ub in vitro. Ubc13 is involved in IFNAR1 endocytosis driven by the K63‑Ub modification of Lys501, whereas the K48‑Ub-specific Cdc34 affects receptor endocytosis via ubiquitin conjugation that occurs on Lys525 / 526. Both types of linkages combine to maximize IFNAR1 endocytosis otherwise suppressed by unfavorable conformation dependent on the presence of a conserved Pro470 within the intracellular domain of IFNAR1. We propose a model where alternate utilization of both E2s to assemble diverse polyubiquitin linkages cooperates to achieve IFNAR1 intracellular domain conformations and spatial arrangements that favor a maximal rate of receptor endocytosis.
Об авторах
Christopher J. Carbone
Department of Animal Biology and Mari Lowe Center for Comparative Oncology, School of Veterinary Medicine, University of Pennsylvania, 380 S. University Avenue, Hill 316, Philadelphia, PA 19104, USA
Россия
Россия
Hui Zheng
Department of Animal Biology and Mari Lowe Center for Comparative Oncology, School of Veterinary Medicine, University of Pennsylvania, 380 S. University Avenue, Hill 316, Philadelphia, PA 19104, USA
Россия
Россия
Serge Y. Fuchs
Department of Animal Biology and Mari Lowe Center for Comparative Oncology, School of Veterinary Medicine, University of Pennsylvania, 380 S. University Avenue, Hill 316, Philadelphia, PA 19104, USA
Россия
Россия
Список литературы
1. Ciechanover A. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J 1998;17(24):7151–60.
2. Bonifacino J. S., Weissman A. M. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu Rev Cell Dev Biol 1998;14: 19–57.
3. Holler D., Dikic I. Receptor endocytosis via ubiquitin-dependent and -independent pathways. Biochem Pharmacol 2004;67(6):1013–7.
4. Huangfu W. C., Fuchs S. Y. Ubiquitination-dependent regulation of signaling receptors in cancer. Genes Cancer 2010;1(7):725–34.
5. Galan J. M., Haguenauer-Tsapis R. Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J 1997;16(19):5847–54.
6. Geetha T., Jiang J., Wooten M. W. Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Mol Cell 2005;20(2):301–12.
7. Duncan L. M., Piper S., Dodd R. B. et al. Lysine-63‑linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J 2006;25(8):1635–45.
8. Varghese B., Barriere H., Carbone C. J. et al. Polyubiquitination of prolactin receptor stimulates its internalization, postinternalization sorting, and degradation via the lysosomal pathway. Mol Cell Biol 2008;28(17):5275–87.
9. Barriere H., Nemes C., Lechardeur D. et al. Molecular basis of oligoubiquitindependent internalization of membrane proteins in Mammalian cells. Traffic 2006;7(3):282–97.
10. Kumar K. G., Barriere H., Carbone C. J. et al. Site-specific ubiquitination exposes a linear motif to promote interferon-alpha receptor endocytosis. J Cell Biol 2007;179(5):935–50.
11. Constantinescu S. N., Croze E., Wang C. et al. Role of interferon alpha / beta receptor chain 1 in the structure and transmembrane ignaling of the interferon alpha / beta receptor complex. Proc Natl Acad Sci USA 1994;91(20):9602–6.
12. Colamonici O. R., Porterfield B., Domanski P. et al. Complementation of the interferon alpha response in resistant cells by expression of the cloned subunit of the interferon alpha receptor. A central role of this subunit in interferon alpha signaling. J Biol Chem 1994;269(13):9598–602.
13. Muller U., Steinhoff U., Reis L. F. et al. Functional role of type I and type II interferons in antiviral defense. Science 1994;264(5167):1918–21.
14. Kumar K. G., Krolewski J. J., Fuchs S. Y. Phosphorylation and specific ubiquitin acceptor sites are required for ubiquitination and degradation of the IFNAR1 subunit of type I interferon receptor. J Biol Chem 2004;279(45):46614–20.
15. Kumar K. G., Tang W., Ravindranath A. K. et al. SCF(HOS) ubiquitin ligase mediates the ligand-induced down-regulation of the interferon-alpha receptor. EMBO J 2003;22(20):5480–90.
16. Kumar K. G., Varghese B., Banerjee A. et al. Basal ubiquitin-independent internalization of interferon alpha receptor is prevented by Tyk2‑mediated masking of a linear endocytic motif. J Biol Chem 2008;283(27):18566–72.
17. Fuchs S. Y. Hope and fear for interferon: the receptor-centric outlook on the future of interferon therapy. J Interferon Cytokine Res 2013;33(4):211–25.
18. Fuchs S. Y. Ubiquitination-mediated regulation of interferon responses. Growth Factors 2012;30(3):141–8.
19. Mosesson Y., Shtiegman K., Katz M. et al. Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem 2003;278(24):21323–6.
20. Parisien J. P., Lau J. F., Rodriguez J. J. et al. Selective STAT protein degradation induced by paramyxoviruses requires both STAT1 and STAT2 but is independent of alpha / beta interferon signal transduction. J Virol 2002;76(9):4190–8.
21. Li Y., Kumar K. G., Tang W. et al. Negative regulation of prolactin receptor stability and signaling mediated by SCF (beta-TrCP) E3 ubiquitin ligase. Mol Cell Biol 2004;24(9):4038–48.
22. Xu M., Skaug B., Zeng W., Chen Z. J. A ubiquitin replacement strategy in human cells reveals distinct mechanisms of IKK activation by TNFalpha and IL-1beta. Mol Cell 2009;36(2):302–14.
23. Soldatenkov V. A., Dritschilo A., Ronai Z., Fuchs S. Y. Inhibition of homologue of Slimb (HOS) function sensitizes human melanoma cells for apoptosis. Cancer Res 1999;59(20):5085–8.
24. Li Y., Gazdoiu S., Pan Z. Q., Fuchs S. Y. Stability of homologue of Slimb F-box protein is regulated by availability of its substrate. J Biol Chem 2004;279(12):11074–80.
25. Liu J., HuangFu W. C., Kumar K. G. et al. Virus-induced unfolded protein response attenuates antiviral defenses via phosphorylation-dependent degradation of the type I interferon receptor. Cell Host Microbe 2009;5(1):72–83.
26. Tan P., Fuchs S. Y., Chen A. et al. Recruitment of a ROC1‑CUL1 ubiquitinligase by Skp1 and HOS to catalyze the ubiquitination of I kappa B alpha. Mol Cell 1999;3(4):527–33.
27. Wu K., Kovacev J., Pan Z. Q. Priming and extending: a UbcH5 / Cdc34 E2 handoff mechanism for polyubiquitination on a SCF substrate. Mol Cell 2010;37(6):784–96.
28. Topisirovic I., Gutierrez G. J., Chen M. et al. Control of p53 multimerization by Ubc13 is JNK-regulated. Proc Natl Acad Sci USA 2009;106(31):12676–81.
29. Laine A., Topisirovic I., Zhai D. et al. Regulation of p53 localization and activity by Ubc13. Mol Cell Biol 2006;26(23):8901–13.
30. Goldman L. A., Zafari M., Cutrone E. C. et al. Characterization of antihuman IFNAR-1 monoclonal antibodies: epitope localization and functional analysis. J Interferon Cytokine Res 1999;19(1):15–26.
31. Zhao G. Y., Sonoda E., Barber L. J. et al. A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination. Mol Cell 2007;25(5):663–75.
32. Hofmann R. M., Pickart C. M. Noncanonical MMS2‑encoded ubiquitinconjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 1999;96(5):645–53.
33. Karin M., Gallagher E. TNFR signaling: ubiquitin-conjugated TRAFfic signals control stop-and-go for MAPK signaling complexes. Immunol Rev 2009;228(1):225–40.
34. Laine A., Ronai Z. Ubiquitin chains in the ladder of MAPK signaling. Sci STKE 2005;2005(281):re5.
35. Chen Z. J. Ubiquitin signalling in the NF-kappaB pathway. Nat Cell Biol 2005;7(8):758–65.
36. Fuchs S. Y., Spiegelman V. S., Kumar K. G. The many faces of beta-TrCP E3 ubiquitin ligases: reflections in the magic mirror of cancer. Oncogene 2004;23(11):2028–36.
37. Zeng W., Sun L., Jiang X. et al. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 2010;141(2):315–30.
38. Ragimbeau J., Dondi E., Alcover A. et al. The tyrosine kinase Tyk2 controls IFNAR1 cell surface expression. EMBO J 2003;22(3):537–47.
39. Marijanovic Z., Ragimbeau J., Kumar K. G. et al. TYK2 activity promotes ligand-induced IFNAR1 proteolysis. Biochem J 2006;397(1):31–8.
40. Liu J., Plotnikov A., Banerjee A. et al. Ligand-independent pathway that controls stability of interferon alpha receptor. Biochem Biophys Res Commun 2008;367(2):388–93.
41. Carbone C. J., Zheng H., Bhattacharya S. et al. Protein tyrosine phosphatase 1B is a key regulator of IFNAR1 endocytosis and a target for antiviral therapies. Proc Natl Acad Sci USA
42. ;109(47):19226–31.
43. Payelle-Brogard B., Pellegrini S. Biochemical monitoring of the early endocytic traffic of the type I interferon receptor. J Interferon Cytokine Res 2010;30(2):89–98.
44. Wu G., Xu G., Schulman B. A. et al. Structure of a beta-TrCP1‑Skp1‑beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase. Mol Cell 2003; 11(6):1445–56.
45. Tang W., Pavlish O. A., Spiegelman V. S. et al. Interaction of Epstein-Barr virus latent membrane protein 1 with SCFHOS / beta- TrCP E3 ubiquitin ligase regulates extent of NF-kappaB activation. J Biol Chem 2003;278(49):48942–9.
46. Karin M., Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol 2000;18:621–63.
47. Windheim M., Peggie M., Cohen P. Two different classes of E2 ubiquitin-conjugating enzymes are required for the monoubiquitination of proteins and elongation by polyubiquitin chains with a specific topology. Biochem J 2008;409(3):723–9.
48. Tenno T., Fujiwara K., Tochio H. et al. Structural basis for distinct roles of Lys63- and Lys48‑linked polyubiquitin chains. Genes Cells 2004;9(10):865–75.
Для цитирования:
J. Carbone C., Zheng H., Y. Fuchs S. Endocytosis of the IFNAR1 chain of Type 1 interferon receptor is regulated by diverse E2 ubiquitin conjugation enzymes. Успехи молекулярной онкологии. 2014;1(2):50-60. https://doi.org/10.17650/2313-805X.2014.1.2.50-60
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