User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Basal ubiquitin-independent internalization of interferon alpha receptor is prevented by Tyk2-mediated masking of a linear endocytic motif

Primary tabs

Kumar, K. G. Suresh Varghese, Bentley Banerjee, Anamika Baker, Darren P. Constantinescu, Stefan N. [UCL] Fuchs, Serge Y.

Linear endocytic motifs of signaling receptors as well as their ubiquitination determine the rate of ligand-induced endocytosis that mediates down-regulation of these receptors and restricts the magnitude and duration of their respective signal transduction pathways. We previously hypothesized that, in the absence of its cognate ligand, type I interferon (IFN), the IFN alpha receptor chain 1 (IFNAR1) receptor chain is protected from basal endocytosis by a hypothetical masking complex that prevents the Tyr-based endocytic motif within IFNAR1 from interacting with components of the adaptin protein complex 2 (AP2). Here we identify a member of the Janus kinase (Jak) family, Tyk2, as a component of such a masking complex. In the absence of ligand or of receptor chain ubiquitination, binding of Janus kinase Tyk2 within the proximity of the Tyr-based linear motif of IFNAR1 is required to prevent IFNAR1 internalization and to maintain its cell surface expression. Furthermore, interaction experiments revealed that Tyk2 physically shields this Tyr-based motif from the recognition by the AP50 subunit of AP2. These data delineate a long-sought ligand- and ubiquitin-independent mechanism by which Tyk2 contributes to both the regulation of total IFNAR1 levels as well as the regulation of the cell surface density of this receptor chain.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2008
Language Anglais
Journal information "Journal of Biological Chemistry" - Vol. 283, no. 27, p. 18566-18572 (2008)
Peer reviewed yes
Publisher Amer Soc Biochemistry Molecular Biology Inc (Bethesda)
issn 0021-9258
e-issn 1083-351X
Publication status Publié
Affiliation UCL
Links
  1. Marijanovic Zrinka, Ragimbeau Josiane, Kumar K. G. Suresh, Fuchs Serge Y., Pellegrini Sandra, TYK2 activity promotes ligand-induced IFNAR1 proteolysis, 10.1042/bj20060272
  2. Jung Nadja, Haucke Volker, Clathrin-Mediated Endocytosis at Synapses, 10.1111/j.1600-0854.2007.00595.x
  3. Deng Luqin, He Kai, Wang Xiangdong, Yang Ning, Thangavel Chellappagounder, Jiang Jing, Fuchs Serge Y., Frank Stuart J., Determinants of Growth Hormone Receptor Down-Regulation, 10.1210/me.2007-0138
  4. Höller Daniela, Dikic Ivan, Receptor endocytosis via ubiquitin-dependent and -independent pathways, 10.1016/j.bcp.2004.01.003
  5. Dikic I., Mechanisms controlling EGF receptor endocytosis and degradation, 10.1042/bst0311178
  6. Haglund K, Distinct monoubiquitin signals in receptor endocytosis, 10.1016/j.tibs.2003.09.005
  7. Kumar K.G. Suresh, Barriere Hervé, Carbone Christopher J., Liu Jianghuai, Swaminathan Gayathri, Xu Ping, Li Ying, Baker Darren P., Peng Junmin, Lukacs Gergely L., Fuchs Serge Y., Site-specific ubiquitination exposes a linear motif to promote interferon-α receptor endocytosis, 10.1083/jcb.200706034
  8. Ragimbeau J., The tyrosine kinase Tyk2 controls IFNAR1 cell surface expression, 10.1093/emboj/cdg038
  9. Gauzzi M. Cristina, Velazquez Laura, McKendry Roslyn, Mogensen Knud E., Fellous Marc, Pellegrini Sandra, Interferon-α-dependent Activation of Tyk2 Requires Phosphorylation of Positive Regulatory Tyrosines by Another Kinase, 10.1074/jbc.271.34.20494
  10. Royer Yohan, Staerk Judith, Costuleanu Marcel, Courtoy Pierre J., Constantinescu Stefan N., Janus Kinases Affect Thrombopoietin Receptor Cell Surface Localization and Stability, 10.1074/jbc.m501376200
  11. Suresh Kumar K.G., SCFHOS ubiquitin ligase mediates the ligand-induced down-regulation of the interferon-  receptor, 10.1093/emboj/cdg524
  12. Rohde Gundula, Wenzel Dirk, Haucke Volker, A phosphatidylinositol (4,5)-bisphosphate binding site within μ2-adaptin regulates clathrin-mediated endocytosis, 10.1083/jcb.200203103
  13. Takei Kohji, Haucke Volker, Clathrin-mediated endocytosis: membrane factors pull the trigger, 10.1016/s0962-8924(01)02082-7
  14. Jin J., SCF -TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase, 10.1101/gad.1157503
  15. Li Y., Suresh Kumar K. G., Tang W., Spiegelman V. S., Fuchs S. Y., Negative Regulation of Prolactin Receptor Stability and Signaling Mediated by SCF -TrCP E3 Ubiquitin Ligase, 10.1128/mcb.24.9.4038-4048.2004
  16. Ragimbeau Josiane, Dondi Elisabetta, Vasserot Arnaud, Romero Pilar, Uzé Gilles, Pellegrini Sandra, The Receptor Interaction Region of Tyk2 Contains a Motif Required for Its Nuclear Localization, 10.1074/jbc.m103559200
  17. Goldman Lisa A., Zafari Mohammad, Cutrone Elizabeth Cali, Dang Anju, Brickelmeier Margot, Runkel Laura, Benjamin Christopher D., Ling Leona E., Langer Jerome A., Characterization of Antihuman IFNAR-1 Monoclonal Antibodies: Epitope Localization and Functional Analysis, 10.1089/107999099314379
  18. Fuchs Serge Y, Chen Angus, Xiong Yue, Pan Zhen-Qiang, Ronai Ze'ev, HOS, a human homolog of Slimb, forms an SCF complex with Skp1 and Cullin1 and targets the phosphorylation-dependent degradation of IκB and β-catenin, 10.1038/sj.onc.1202760
  19. Hammond D. E., Endosomal Dynamics of Met Determine Signaling Output, 10.1091/mbc.e02-09-0578
  20. Barriere Herve, Nemes Csilla, Lechardeur Delphine, Khan-Mohammad Mina, Fruh Klaus, Lukacs Gergely L., Molecular Basis of Oligoubiquitin-Dependent Internalization of Membrane Proteins in Mammalian Cells : Oligoubiquitin Recognition as Endocytic Signal, 10.1111/j.1600-0854.2006.00384.x
  21. Yan H, Krishnan K, Lim J T, Contillo L G, Krolewski J J, Molecular characterization of an alpha interferon receptor 1 subunit (IFNaR1) domain required for TYK2 binding and signal transduction., 10.1128/mcb.16.5.2074
  22. Gauzzi M. C., Barbieri G., Richter M. F., Uze G., Ling L., Fellous M., Pellegrini S., The amino-terminal region of Tyk2 sustains the level of interferon   receptor 1, a component of the interferon  /  receptor, 10.1073/pnas.94.22.11839
  23. Minegishi Yoshiyuki, Saito Masako, Morio Tomohiro, Watanabe Ken, Agematsu Kazunaga, Tsuchiya Shigeru, Takada Hidetoshi, Hara Toshiro, Kawamura Nobuaki, Ariga Tadashi, Kaneko Hideo, Kondo Naomi, Tsuge Ikuya, Yachie Akihiro, Sakiyama Yukio, Iwata Tsutomu, Bessho Fumio, Ohishi Tsutomu, Joh Kosuke, Imai Kohsuke, Kogawa Kazuhiro, Shinohara Miwa, Fujieda Mikiya, Wakiguchi Hiroshi, Pasic Srdjan, Abinun Mario, Ochs Hans D., Renner Eleonore D., Jansson Annette, Belohradsky Bernd H., Metin Ayse, Shimizu Norio, Mizutani Shuki, Miyawaki Toshio, Nonoyama Shigeaki, Karasuyama Hajime, Human Tyrosine Kinase 2 Deficiency Reveals Its Requisite Roles in Multiple Cytokine Signals Involved in Innate and Acquired Immunity, 10.1016/j.immuni.2006.09.009
  24. SMYTHE Elizabeth, WARREN Graham, The mechanism of receptor-mediated endocytosis, 10.1111/j.1432-1033.1991.tb16424.x
  25. Shimoda Kazuya, Kato Kouji, Aoki Kenichi, Matsuda Tadashi, Miyamoto Akitomo, Shibamori Masafumi, Yamashita Masakatsu, Numata Akihiko, Takase Ken, Kobayashi Shinji, Shibata Shouichirou, Asano Yoshinobu, Gondo Hisashi, Sekiguchi Kazuo, Nakayama Keiko, Nakayama Toshinori, Okamura Takashi, Okamura Seiichi, Niho Yoshiyuki, Nakayama Kei-ichi, Tyk2 Plays a Restricted Role in IFNα Signaling, Although It Is Required for IL-12-Mediated T Cell Function, 10.1016/s1074-7613(00)00055-8
  26. Karaghiosoff Marina, Neubauer Hans, Lassnig Caroline, Kovarik Pavel, Schindler Heike, Pircher Hanspeter, McCoy Barbara, Bogdan Christian, Decker Thomas, Brem Gottfried, Pfeffer Klaus, Müller Mathias, Partial Impairment of Cytokine Responses in Tyk2-Deficient Mice, 10.1016/s1074-7613(00)00054-6
  27. Sheehan Kathleen C.F., Lai Koon Siew, Dunn Gavin P., Bruce Allen T., Diamond Mark S., Heutel Jennifer D., Dungo-Arthur Corazon, Carrero Javier A., White J. Michael, Hertzog Paul J., Schreiber Robert D., Blocking Monoclonal Antibodies Specific for Mouse IFN-α/βReceptor Subunit 1 (IFNAR-1) from Mice Immunized byIn VivoHydrodynamic Transfection, 10.1089/jir.2006.26.804
  28. Biochem. Biophys. Res. Commun, 367, 388 (2007)
  29. Jabbour H., Prolactin receptor subtypes: a possible mode of tissue specific regulation of prolactin function, 10.1530/ror.0.0020014
  30. Haan Claude, Kreis Stephanie, Margue Christiane, Behrmann Iris, Jaks and cytokine receptors—An intimate relationship, 10.1016/j.bcp.2006.04.013
  31. Radtke Simone, Hermanns Heike M., Haan Claude, Schmitz-Van de Leur Hildegard, Gascan Hugues, Heinrich Peter C., Behrmann Iris, Novel Role of Janus Kinase 1 in the Regulation of Oncostatin M Receptor Surface Expression, 10.1074/jbc.m100822200
  32. Radtke S., Three Dileucine-like Motifs within the Interbox1/2 Region of the Human Oncostatin M Receptor Prevent Efficient Surface Expression in the Absence of an Associated Janus Kinase, 10.1074/jbc.m511779200
  33. Huang Lily Jun-shen, Constantinescu Stefan N., Lodish Harvey F., The N-Terminal Domain of Janus Kinase 2 Is Required for Golgi Processing and Cell Surface Expression of Erythropoietin Receptor, 10.1016/s1097-2765(01)00401-4
  34. He Kai, Loesch Kimberly, Cowan Jon W., Li Xin, Deng Luqin, Wang Xiangdong, Jiang Jing, Frank Stuart J., Janus Kinase 2 Enhances the Stability of the Mature Growth Hormone Receptor, 10.1210/en.2005-0514
  35. Bonifacino Juan S., Traub Linton M., Signals for Sorting of Transmembrane Proteins to Endosomes and Lysosomes, 10.1146/annurev.biochem.72.121801.161800
  36. Hofmann S. R., Lam A. Q., Frank S., Zhou Y.-J., Ramos H. L., Kanno Y., Agnello D., Youle R. J., O'Shea J. J., Jak3-Independent Trafficking of the Common   Chain Receptor Subunit: Chaperone Function of Jaks Revisited, 10.1128/mcb.24.11.5039-5049.2004
  37. Bonifacino Juan S., Weissman Allan M., UBIQUITIN AND THE CONTROL OF PROTEIN FATE IN THE SECRETORY AND ENDOCYTIC PATHWAYS, 10.1146/annurev.cellbio.14.1.19
  38. Weissman Allan M., 10.1038/35056563
  39. Hicke Linda, Dunn Rebecca, Regulation of Membrane Protein Transport by Ubiquitin and Ubiquitin-Binding Proteins, 10.1146/annurev.cellbio.19.110701.154617
  40. Curr. Top. Microbiol. Immunol., 286, 149 (2004)
  41. Oncogene, 11, 2649 (1995)
Bibliographic reference Kumar, K. G. Suresh ; Varghese, Bentley ; Banerjee, Anamika ; Baker, Darren P. ; Constantinescu, Stefan N. ; et. al. Basal ubiquitin-independent internalization of interferon alpha receptor is prevented by Tyk2-mediated masking of a linear endocytic motif. In: Journal of Biological Chemistry, Vol. 283, no. 27, p. 18566-18572 (2008)
Permanent URL http://hdl.handle.net/2078.1/36515