Pathogen recognition receptor signaling accelerates phosphorylation-dependent degradation of IFNAR1

PLoS Pathogens

Volumn 7, Issue 6, 2011, Pages

  Qian, Juan ^a   Zheng, Hui ^a   HuangFu, Wei Chun ^a   Liu, Jianghuai ^a   Carbone, Christopher J ^a   Leu, N Adrian ^a   Baker, Darren P ^b   Fuchs, Serge Y ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; DNA; INTERFERON RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; TYPE 1 INTERFERON RECEPTOR; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; IFNAR1 PROTEIN, HUMAN; IFNAR1 PROTEIN, MOUSE; INTERFERON;

ARTICLE; CYTOTOXICITY; DENDRITIC CELL; DOWN REGULATION; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; INNATE IMMUNITY; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; UBIQUITINATION; VIRUS; VIRUS INFECTION; ANIMAL; CELL LINE; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 79959855146     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002065     Document Type: Article

References (60)

1. O'Neill LA, Bowie AG, (2010) Sensing and signaling in antiviral innate immunity. Curr Biol 20: R328-333.
2. Blasius AL, Beutler B, (2010) Intracellular toll-like receptors. Immunity 32: 305-315.
3. Takeuchi O, Akira S, (2009) Innate immunity to virus infection. Immunol Rev 227: 75-86.
4. Coccia EM, (2008) IFN regulation and functions in myeloid dendritic cells. Cytokine Growth Factor Rev 19: 21-32.
5. Iwasaki A, Medzhitov R, (2010) Regulation of adaptive immunity by the innate immune system. Science 327: 291-295.
6. Brodsky IE, Medzhitov R, (2009) Targeting of immune signalling networks by bacterial pathogens. Nat Cell Biol 11: 521-526.
7. Palm NW, Medzhitov R, (2009) Pattern recognition receptors and control of adaptive immunity. Immunol Rev 227: 221-233.
8. Stark GR, (2007) How cells respond to interferons revisited: from early history to current complexity. Cytokine Growth Factor Rev 18: 419-423.
9. Aaronson DS, Horvath CM, (2002) A road map for those who don't know JAK-STAT. Science 296: 1653-1655.
10. Platanias LC, (2005) Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5: 375-386.
11. Hasan UA, Caux C, Perrot I, Doffin AC, Menetrier-Caux C, et al. (2007) Cell proliferation and survival induced by Toll-like receptors is antagonized by type I IFNs. Proc Natl Acad Sci U S A 104: 8047-8052.
12. Yen JH, Ganea D, (2009) Interferon beta induces mature dendritic cell apoptosis through caspase-11/caspase-3 activation. Blood 114: 1344-1354.
13. Longhi MP, Trumpfheller C, Idoyaga J, Caskey M, Matos I, et al. (2009) Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J Exp Med 206: 1589-1602.
14. Longman RS, Braun D, Pellegrini S, Rice CM, Darnell RB, et al. (2007) Dendritic-cell maturation alters intracellular signaling networks, enabling differential effects of IFN-alpha/beta on antigen cross-presentation. Blood 109: 1113-1122.
15. Gao Y, Majchrzak-Kita B, Fish EN, Gommerman JL, (2009) Dynamic accumulation of plasmacytoid dendritic cells in lymph nodes is regulated by interferon-beta. Blood 114: 2623-2631.
16. Mattei F, Bracci L, Tough DF, Belardelli F, Schiavoni G, (2009) Type I IFN regulate DC turnover in vivo. Eur J Immunol 39: 1807-1818.
17. Delgado-Vega AM, Alarcon-Riquelme ME, Kozyrev SV, (2010) Genetic associations in type I interferon related pathways with autoimmunity. Arthritis Res Ther 12 (Suppl 1): S2.
18. Hall JC, Rosen A, (2010) Type I interferons: crucial participants in disease amplification in autoimmunity. Nat Rev Rheumatol 6: 40-49.
19. Kunz M, Ibrahim SM, (2009) Cytokines and cytokine profiles in human autoimmune diseases and animal models of autoimmunity. Mediators Inflamm 2009: 979258.
20. Finke D, Eloranta ML, Ronnblom L, (2009) Endogenous type I interferon inducers in autoimmune diseases. Autoimmunity 42: 349-352.
21. Uze G, Schreiber G, Piehler J, Pellegrini S, (2007) The receptor of the type I interferon family. Curr Top Microbiol Immunol 316: 71-95.
22. Coccia EM, Uze G, Pellegrini S, (2006) Negative regulation of type I interferon signaling: facts and mechanisms. Cell Mol Biol (Noisy-le-grand) 52: 77-87.
23. Huangfu WC, Fuchs SY, (2010) Ubiquitination-dependent regulation of signaling receptors in cancer. Genes Cancer 1: 725-734.
24. Kumar KG, Barriere H, Carbone CJ, Liu J, Swaminathan G, et al. (2007) Site-specific ubiquitination exposes a linear motif to promote interferon-alpha receptor endocytosis. J Cell Biol 179: 935-950.
25. Kumar KG, Tang W, Ravindranath AK, Clark WA, Croze E, et al. (2003) SCF(HOS) ubiquitin ligase mediates the ligand-induced down-regulation of the interferon-alpha receptor. EMBO J 22: 5480-5490.
26. Kumar KG, Krolewski JJ, Fuchs SY, (2004) Phosphorylation and specific ubiquitin acceptor sites are required for ubiquitination and degradation of the IFNAR1 subunit of type I interferon receptor. J Biol Chem 279: 46614-46620.
27. Marijanovic Z, Ragimbeau J, Kumar KG, Fuchs SY, Pellegrini S, (2006) TYK2 activity promotes ligand-induced IFNAR1 proteolysis. Biochem J 397: 31-38.
28. Zheng H, Qian J, Varghese B, Baker DP, Fuchs S, (2011) Ligand-stimulated downregulation of the alpha interferon receptor: role of protein kinase d2. Mol Cell Biol 31: 710-720.
29. Liu J, Plotnikov A, Banerjee A, Suresh Kumar KG, Ragimbeau J, et al. (2008) Ligand-independent pathway that controls stability of interferon alpha receptor. Biochem Biophys Res Commun 367: 388-393.
30. Wek RC, Cavener DR, (2007) Translational control and the unfolded protein response. Antioxid Redox Signal 9: 2357-2371.
31. Ron D, Walter P, (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529.
32. He B, (2006) Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 13: 393-403.
33. Liu J, HuangFu WC, Kumar KG, Qian J, Casey JP, et al. (2009) Virus-induced unfolded protein response attenuates antiviral defenses via phosphorylation-dependent degradation of the type I interferon receptor. Cell Host Microbe 5: 72-83.
34. Liu J, Carvalho LP, Bhattacharya S, Carbone CJ, Kumar KG, et al. (2009) Mammalian casein kinase 1alpha and its leishmanial ortholog regulate stability of IFNAR1 and type I interferon signaling. Mol Cell Biol 29: 6401-6412.
35. Bhattacharya S, HuangFu WC, Liu J, Veeranki S, Baker DP, et al. (2010) Inducible priming phosphorylation promotes ligand-independent degradation of the IFNAR1 chain of type I interferon receptor. J Biol Chem 285: 2318-2325.
36. Kirchner H, Engler H, Schroder CH, Zawatzky R, Storch E, (1983) Herpes simplex virus type 1-induced interferon production and activation of natural killer cells in mice. J Gen Virol 64 (Pt 2): 437-441.
37. Gauzzi MC, Velazquez L, McKendry R, Mogensen KE, Fellous M, et al. (1996) Interferon-alpha-dependent activation of Tyk2 requires phosphorylation of positive regulatory tyrosines by another kinase. J Biol Chem 271: 20494-20500.
38. Rani MR, Gauzzi C, Pellegrini S, Fish EN, Wei T, et al. (1999) Induction of beta-R1/I-TAC by interferon-beta requires catalytically active TYK2. J Biol Chem 274: 1891-1897.
39. Lutfalla G, Holland SJ, Cinato E, Monneron D, Reboul J, 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.
40. Cheng G, Feng Z, He B, (2005) Herpes simplex virus 1 infection activates the endoplasmic reticulum resident kinase PERK and mediates eIF-2alpha dephosphorylation by the gamma(1)34.5 protein. J Virol 79: 1379-1388.
41. Mulvey M, Arias C, Mohr I, (2007) Maintenance of endoplasmic reticulum (ER) homeostasis in herpes simplex virus type 1-infected cells through the association of a viral glycoprotein with PERK, a cellular ER stress sensor. J Virol 81: 3377-3390.
42. Zhang P, McGrath B, Li S, Frank A, Zambito F, et al. (2002) The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol Cell Biol 22: 3864-3874.
43. Lund J, Sato A, Akira S, Medzhitov R, Iwasaki A, (2003) Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J Exp Med 198: 513-520.
44. Krug A, Luker GD, Barchet W, Leib DA, Akira S, et al. (2004) Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 103: 1433-1437.
45. Kurt-Jones EA, Chan M, Zhou S, Wang J, Reed G, et al. (2004) Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc Natl Acad Sci U S A 101: 1315-1320.
46. Yang K, Puel A, Zhang S, Eidenschenk C, Ku CL, et al. (2005) Human TLR-7-,-8-, and-9-mediated induction of IFN-alpha/beta and-lambda Is IRAK-4 dependent and redundant for protective immunity to viruses. Immunity 23: 465-478.
47. Osterlund PI, Pietila TE, Veckman V, Kotenko SV, Julkunen I, (2007) IFN regulatory factor family members differentially regulate the expression of type III IFN (IFN-lambda) genes. J Immunol 179: 3434-3442.
48. Coccia EM, Severa M, Giacomini E, Monneron D, Remoli ME, et al. (2004) Viral infection and Toll-like receptor agonists induce a differential expression of type I and lambda interferons in human plasmacytoid and monocyte-derived dendritic cells. Eur J Immunol 34: 796-805.
49. Severa M, Remoli ME, Giacomini E, Ragimbeau J, Lande R, et al. (2006) Differential responsiveness to IFN-alpha and IFN-beta of human mature DC through modulation of IFNAR expression. J Leukoc Biol 79: 1286-1294.
50. Gauzzi MC, Canini I, Eid P, Belardelli F, Gessani S, (2002) Loss of type I IFN receptors and impaired IFN responsiveness during terminal maturation of monocyte-derived human dendritic cells. J Immunol 169: 3038-3045.
51. Moraga I, Harari D, Schreiber G, Uze G, Pellegrini S, (2009) Receptor density is key to the alpha2/beta interferon differential activities. Mol Cell Biol 29: 4778-4787.
52. Roux PP, Blenis J, (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68: 320-344.
53. Katsoulidis E, Li Y, Mears H, Platanias LC, (2005) The p38 mitogen-activated protein kinase pathway in interferon signal transduction. J Interferon Cytokine Res 25: 749-756.
54. Platanias LC, (2003) The p38 mitogen-activated protein kinase pathway and its role in interferon signaling. Pharmacol Ther 98: 129-142.
55. Uddin S, Majchrzak B, Woodson J, Arunkumar P, Alsayed Y, et al. (1999) Activation of the p38 mitogen-activated protein kinase by type I interferons. J Biol Chem 274: 30127-30131.
56. Verma A, Deb DK, Sassano A, Kambhampati S, Wickrema A, et al. (2002) Cutting edge: activation of the p38 mitogen-activated protein kinase signaling pathway mediates cytokine-induced hemopoietic suppression in aplastic anemia. J Immunol 168: 5984-5988.
57. Uddin S, Lekmine F, Sharma N, Majchrzak B, Mayer I, et al. (2000) 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: 27634-27640.
58. Soloff AC, Barratt-Boyes SM, (2010) Enemy at the gates: dendritic cells and immunity to mucosal pathogens. Cell Res 20: 872-885.
59. Alsharifi M, Mullbacher A, Regner M, (2008) Interferon type I responses in primary and secondary infections. Immunol Cell Biol 86: 239-245.
60. Goldman LA, Zafari M, Cutrone EC, Dang A, Brickelmeier M, et al. (1999) Characterization of antihuman IFNAR-1 monoclonal antibodies: epitope localization and functional analysis. J Interferon Cytokine Res 19: 15-26.