The E3 Ubiquitin Ligase Atrophin Interacting Protein 4 Binds Directly To The Chemokine Receptor CXCR4 Via a Novel WW Domain-mediated Interaction

Molecular Biology of the Cell - Tập 20 Số 5 - Trang 1324-1339 - 2009
Deepali Bhandari1, Seth L. Robia2, Adriano Marchese3,4
1Program in Molecular Biology, Stritch School of Medicine, Loyola University Chicago, Maywood, IL 60153, USA.
2Cell and Molecular Physiology and
3*Program in Molecular Biology, Stritch School of Medicine, Loyola University Chicago, Maywood, IL 60153
4Departments of Pharmacology and Experimental Therapeutics and

Tóm tắt

The E3 ubiquitin ligase atrophin interacting protein 4 (AIP4) mediates ubiquitination and down-regulation of the chemokine receptor CXCR4. AIP4 belongs to the Nedd4-like homologous to E6-AP carboxy terminus domain family of E3 ubiquitin ligases, which typically bind proline-rich motifs within target proteins via the WW domains. The intracellular domains of CXCR4 lack canonical WW domain binding motifs; thus, whether AIP4 is targeted to CXCR4 directly or indirectly via an adaptor protein remains unknown. Here, we show that AIP4 can interact directly with CXCR4 via a novel noncanonical WW domain-mediated interaction involving serine residues 324 and 325 within the carboxy-terminal tail of CXCR4. These serine residues are critical for mediating agonist-promoted binding of AIP4 and subsequent ubiquitination and degradation of CXCR4. These residues are phosphorylated upon agonist activation and phosphomimetic mutants show enhanced binding to AIP4, suggesting a mechanism whereby phosphorylation mediates the interaction between CXCR4 and AIP4. Our data reveal a novel noncanonical WW domain-mediated interaction involving phosphorylated serine residues in the absence of any proline residues and suggest a novel mechanism whereby an E3 ubiquitin ligase is targeted directly to an activated G protein-coupled receptor.

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Tài liệu tham khảo

Angers A., 2004, J. Biol. Chem, 279, 11471, 10.1074/jbc.M309934200

Balkwill F., 2004, Semin. Cancer Biol, 14, 171, 10.1016/j.semcancer.2003.10.003

Bhandari D., 2007, J. Biol. Chem, 282, 36971, 10.1074/jbc.M705085200

Bleul C. C., 1996, Nature, 382, 829, 10.1038/382829a0

Busillo J. M., 2007, Biochim. Biophys. Acta, 1768, 952, 10.1016/j.bbamem.2006.11.002

Cheng Z. J., 2000, J. Biol. Chem, 275, 2479, 10.1074/jbc.275.4.2479

Cho W., 2006, Biochim. Biophys. Acta, 1761, 838, 10.1016/j.bbalip.2006.06.014

Damas J. K., 2000, Cardiovasc. Res, 47, 778, 10.1016/S0008-6363(00)00142-5

Diaz G. A., 2005, Curr Allergy Asthma Rep, 5, 350, 10.1007/s11882-005-0005-0

10.1091/mbc.12.2.421

Hu H., 2004, Proteomics, 4, 643, 10.1002/pmic.200300632

Huibregtse J. M., 1995, Proc. Natl. Acad. Sci. USA, 92, 2563, 10.1073/pnas.92.7.2563

Ingham R. J., 2005, Mol. Cell. Biol, 25, 7092, 10.1128/MCB.25.16.7092-7106.2005

Ingham R. J., 2004, Oncogene, 23, 1972, 10.1038/sj.onc.1207436

Ingham R. J., 2005, J. Biol. Chem, 280, 34133, 10.1074/jbc.M507831200

Janz J. M., 2007, J. Biol. Chem, 282, 28893, 10.1074/jbc.M702678200

Kasanov J., 2001, Chem. Biol, 8, 231, 10.1016/S1074-5521(01)00005-9

Kelly E. M., 2008, J. Biol. Chem

Kenworthy A. K., 2001, Methods, 24, 289, 10.1006/meth.2001.1189

Lu M., 2002, Proc. Natl. Acad. Sci. USA, 99, 7090, 10.1073/pnas.092013799

Macias M. J., 2002, FEBS Lett, 513, 30, 10.1016/S0014-5793(01)03290-2

Marchese A., 2001, J. Biol. Chem, 276, 45509, 10.1074/jbc.C100527200

Marchese A., 2004, Methods Mol. Biol, 259, 299

Marchese A., 2008, Annu. Rev. Pharmacol. Toxicol, 48, 601, 10.1146/annurev.pharmtox.48.113006.094646

Marchese A., 2003, Dev. Cell, 5, 709, 10.1016/S1534-5807(03)00321-6

Muller A., 2001, Nature, 410, 50, 10.1038/35065016

Murphy P. M., 2002, Pharmacol. Rev, 54, 227, 10.1124/pr.54.2.227

Nagasawa T., 1996, Nature, 382, 635, 10.1038/382635a0

Oberlin E., 1996, Nature, 382, 833, 10.1038/382833a0

Orsini M. J., 1999, J. Biol. Chem, 274, 31076, 10.1074/jbc.274.43.31076

Otte L., 2003, Protein Sci, 12, 491, 10.1110/ps.0233203

Pickart C. M., 2004, Biochim. Biophys. Acta, 1695, 55, 10.1016/j.bbamcr.2004.09.019

Pierce K. L., 2002, Nat. Rev, 3, 639, 10.1038/nrm908

Piston D. W., 2007, Trends Biochem. Sci, 32, 407, 10.1016/j.tibs.2007.08.003

Shearwin-Whyatt L., 2006, Bioessays, 28, 617, 10.1002/bies.20422

Shenoy S. K., 2001, Science, 294, 1307, 10.1126/science.1063866

Shenoy S. K., 2008, J. Biol. Chem, 283, 22166, 10.1074/jbc.M709668200

Tachibana K., 1998, Nature, 393, 591, 10.1038/31261

Verdecia M. A., 2000, Nat. Struct. Biol, 7, 639, 10.1038/77929

Walter D. H., 2005, Circ. Res, 97, 1142, 10.1161/01.RES.0000193596.94936.2c

Winberg G., 2000, Mol. Cel. Biol, 20, 8526, 10.1128/MCB.20.22.8526-8535.2000

Woelk T., 2006, Nat. Cell Biol, 8, 1246, 10.1038/ncb1484

Zarrinpar A., 2000, Nat. Struct. Biol, 7, 611, 10.1038/77891

Zou Y. R., 1998, Nature, 393, 595, 10.1038/31269