Regulation of receptors and transporters by ubiquitination: New insights into surprisingly similar mechanisms

Molecular Interventions

Volumn 7, Issue 3, 2007, Pages 157-167

  Miranda, Manuel ^a   Sorkin, Alexander ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE TRANSPORTER; EPIDERMAL GROWTH FACTOR; MEMBRANE PROTEIN;

CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; DNA REPAIR; DNA TRANSCRIPTION; ENDOCYTOSIS; HUMAN; MEMBRANE TRANSPORT; NEUROTRANSMISSION; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RNA INTERFERENCE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TURNOVER TIME; UBIQUITINATION;

ANIMALS; HUMANS; MEMBRANE TRANSPORT PROTEINS; RECEPTORS, CELL SURFACE; UBIQUITIN;

EID: 34347401218     PISSN: 15340384     EISSN: 15432548     Source Type: Journal    
DOI: 10.1124/mi.7.3.7     Document Type: Review

References (95)

1. Kolling, R. and Hollenberg, C.P. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13, 3261-3271 (1994). This study was the first to demonstrate the potential role of ubiquitination in endocytosis of a transporter protein.
2. Hicke, L. and Riezman, H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277-287 (1996). The data in this report represent the first definitive proof that ubiquitination of a GPCR is required for receptor internalization in yeast cells.
3. Hicke, L. and Dunn, R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172 (2003).
4. Staub, O. and Rotin, D. Role of ubiquitylation in cellular membrane transport. Physiol. Rev. 86, 669-707 (2006). A comprehensive review of the role of ubiquitination in protein trafficking.
5. Hershko, A. and Ciechanover, A. The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61, 761-807 (1992).
6. Pickart, C. M. and Fushman, D. Polyubiquitin chains: Polymeric protein signals. Curr. Opin. Chem. Biol. 8, 610-616 (2004).
7. Mukhopadhyay, D. and Riezman, H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315, 201-205 (2007).
8. Li, W., Chanda, S.K., Micik, I., and Joazeiro, C.A.P. in Methods in Enzymology (ed. Deshaies, R. J.) 280-291 (Academic Press, 2005).
9. Ma, Q. ADPF and the agonist-dependent control of diminished Ah Receptor expression: Controlling xenobiotic response by receptor degradation. Mol. Interv. 7, 133-137 (2007).
10. Millard, S.M. and Wood, S.A. Riding the DUBway: Regulation of protein trafficking by deubiquitylating enzymes. J. Cell Biol. 173, 463-468 (2006).
11. Hicke, L., Schubert, H.L., and Hill, C.P. Ubiquitin-binding domains. Nat. Rev. Mol. Cell. Biol. 6, 610-621 (2005).
12. Hurley, J.H., Lee, S., and Prag, G. Ubiquitin-binding domains. Biochem. J. 399, 361-372 (2006).
13. 63-linked di-ubiquitin chain provides clues to functional diversity of polyubiquitin signaling. J. Biol. Chem. 279, 7055-7063 (2004).
14. 48-linked polyubiquitin chain by a UBA domain. Mol. Cell 18, 687-698 (2005).
15. Raasi, S., Varadan, R., Fushman, D., and Pickart, C.M. Diverse polyubiquitin interaction properties of ubiquitin-associated domains. Nat. Struct. Mol. Biol. 12, 708-714 (2005).
16. Galcheva-Gargova, Z., Theroux, S.J., and Davis, R.J. The epidermal growth factor receptor is covalently linked to ubiquitin. Oncogene 11, 2649-2655 (1995).
17. Mori, S., Heldin, C.H., and Claesson-Welsh, L. Ligand-induced ubiquitination of the platelet-derived growth factor beta-receptor plays a negative regulatory role in its mitogenic signaling. J. Biol. Chem. 268, 577-583 (1993). References 16 and 17 are the first demonstrations of ubiquitination of RTKs.
18. Cao, Z., Wu, X., Yen, L., Sweeney, C., and Carraway, K.L., 3rd. Neuregulin-induced ErbB3 downregulation is mediated by a protein stability cascade involving the E3 ubiquitin ligase Nrdp1. Mol. Cell. Biol. 27, 2180-2188 (2007).
19. 936 of the stem cell factor receptor/c-Kit is required for ligand-induced ubiquitination, internalization and degradation. Biochem. J. 399, 59-67 (2006).
20. Geetha, T., Jiang, J., and Wooten, M.W. Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Mol. Cell 20, 301-312 (2005).
21. Arevalo, J.C., Waite, J., Rajagopal, R., Beyna, M., Chen, Z.Y., Lee, F.S., and Chao, M.V. Cell survival through Trk neurotrophin receptors is differentially regulated by ubiquitination. Neuron 50, 549-59 (2006).
22. Peschard, P., Fournier, T.M., Lamorte, L., Naujokas, M.A., Band, H., Langdon, W.Y., and Park, M. Mutation of the c-Cbl TKB domain binding site on the Met receptor tyrosine kinase converts it into a transforming protein. Mol. Cell 8, 995-1004 (2001).
23. Duval, M., Bedard-Goulet, S., Delisle, C., and Gratton, J. P. Vascular endothelial growth factor-dependent down-regulation of Flk-1/KDR involves Cbl-mediated ubiquitination. Consequences on nitric oxide production from endothelial cells. J. Biol. Chem. 278, 20091-20097 (2003).
24. Lee, P.S., Wang, Y., Dominguez, M.G., Yeung, Y.G., Murphy, M.A., Bowtell, D.D., and Stanley, E.R. The Cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation. EMBO J. 18, 3616-3628 (1999).
25. Vecchione, A., Marchese, A., Henry, P., Rotin, D., and Morrione, A. The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Mol. Cell. Biol. 23, 3363-3372 (2003).
26. Thien, C.B. and Langdon, W.Y. Cbl: Many adaptations to regulate protein tyrosine kinases. Nat. Rev. Mol. Cell Biol. 2, 294-307 (2001).
27. Levkowitz, G., Waterman, H., Ettenberg, S.A. et al. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4, 1029-1040 (1999).
28. Jiang, X. and Sorkin, A. Epidermal growth factor receptor internalization through clathrin-coated pits requires Cbl RING finger and proline-rich domains but not receptor polyubiquitylation. Traffic 4, 529-543 (2003).
29. Huang, F. and Sorkin, A. Growth factor receptor binding protein 2-mediated recruitment of the RING domain of Cbl to the epidermal growth factor receptor is essential and sufficient to support receptor endocytosis. Mol. Biol. Cell 16, 1268-1281 (2005).
30. Bao, J., Gur, G., and Yarden, Y. Src promotes destruction of c-Cbl: Implications for oncogenic synergy between Src and growth factor receptors. Proc. Natl. Acad. Sci. U.S.A. 100, 2438-2443 (2003).
31. Huang, F., Kirkpatrick, D., Jiang, X., Gygi, S., and Sorkin, A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 21, 737-748 (2006).
32. Sorkin, A. and Von Zastrow, M. Signal transduction and endocytosis: Close encounters of many kinds. Nat. Rev. Mol. Cell Biol. 3, 600-614 (2002).
33. Bonita, D.P., Miyake, S., Lupher, M.L., Jr., Langdon, W.Y. and Band, H. Phosphotyrosine binding domain-dependent upregulation of the platelet-derived growth factor receptor alpha signaling cascade by transforming mutants of Cbl: Implications for Cbl's function and oncogenicity. Mol. Cell. Biol. 17, 4597-4610 (1997).
34. Levkowitz, G., Waterman, H., Zamir, E., Kam, Z., Oved, S., Langdon, W.Y., Beguinot, L., Geiger, B., and Yarden, Y. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12, 3663-3674 (1998). These results showed that Cbl is an E3 ubiquitin ligase for the EGF receptor. This report has also established that Cbl is an important regulator of the endocytic trafficking of this receptor.
35. Miyake, S., Lupher, M.L., Jr., Druker, B., and Band, H. The tyrosine kinase regulator Cbl enhances the ubiquitination and degradation of the platelet-derived growth factor receptor alpha. Proc. Natl. Acad. Sci. U.S.A. 95, 7927-7932 (1998).
36. Jiang, X., Huang, F., Marusyk, A., and Sorkin, A. Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol. Biol. Cell 14, 858-870 (2003).
37. McKanna, J.A., Haigler, H.T., and Cohen, S. Hormone receptor topology and dynamics: Morphological analysis using ferritin-labeled epidermal growth factor. Proc. Natl. Acad. Sci. U.S.A. 76, 5689-5693 (1979).
38. Miller, K., Beardmore, J., Kanety, H., Schlessinger, J., and Hopkins, C.R. Localization of epidermal growth factor (EGF) receptor within the endosome of EGF-stimulated epidermoid carcinoma (A431) cells. J. Cell Biol. 102, 500-509 (1986).
39. Hopkins, C.R. Selective membrane protein trafficking: Vectorial flow and filter. Trends Biochem. Sci. 17, 27-32 (1992).
40. Hurley, J.H. and Emr, S.D. The ESCRT complexes: Structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35, 277-298 (2006).
41. Bache, K.G., Raiborg, C., Mehlum, A. and Stenmark, H. STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521 (2003).
42. Slagsvold, T., Pattni, K., Malerod, L., and Stenmark, H. Endosomal and non-endosomal functions of ESCRT proteins. Trends Cell Biol. 16, 317-326 (2006).
43. Babst, M., Odorizzi, G., Estepa, E.J., and Emr, S.D. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1, 248-258 (2000).
44. Bache, K.G., Stuffers, S., Malerød, L. et al. The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol Biol Cell 17, 2513-2523 (2006).
45. Bowers, K., Piper, S.C., Edeling, M.A., Gray, S.R., Owen, D.J., Lehner, P.J., and Luzio, J.P. Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class I is independent of mammalian ESCRTII. J. Biol. Chem. 281, 5094-5105 (2006).
46. Stoscheck, C.M. and Carpenter, G. "Down-regulation" of EGF receptors: Direct demonstration of receptor degradation in human fibroblasts. J. Cell Biol. 98, 1048-1053 (1984).
47. 125I-Labeled human epidermal growth factor: Binding internalization, and degradation in human fibroblasts. J. Cell Biol. 71, 159-171 (1976).
48. Longva, K.E. et al. Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J. Cell Biol. 156, 843-854 (2002).
49. Zweifel, L.S., Kuruvilla, R., and Ginty, D.D. Functions and mechanisms of retrograde neurotrophin signalling. Nat. Rev. Neurosci. 6, 615-625 (2005).
50. Shenoy, S.K. Seven-transmembrane receptors and ubiquitination. Circ. Res. 100, 1142-1154 (2007).
51. Shenoy, S.K., McDonald, P.H., Kohout, T.A., and Lefkowitz, R.J. Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science 294, 1307-1313 (2001). The first report of ubiquitination of a GPCR and β-arrestin. The data suggested that β-arrestin ubiquitination for internalization of the GPCR.
52. Marchese, A. and Benovic, J.L. Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. J. Biol. Chem. 276, 45509-45512 (2001). This study demonstrated ubiquitination of a GPCR and the essential role of this ubiquitination in the lysosomal degradation of this GPCR.
53. Jacob, C., Cottrell, G.S., Gehringer, D., Schmidlin, F., Grady, E.F., and Bunnett, N.W. c-Cbl mediates ubiquitination, degradation, and down-regulation of human protease-activated receptor 2. J. Biol. Chem. 280, 16076-16087 (2005).
54. Slagsvold, T., Marchese, A., Brech, A., and Stenmark, H. CISK attenuates degradation of the chemokine receptor CXCR4 via the ubiquitin ligase AIP4. EMBO J. 25, 3738-3749 (2006).
55. Tanowitz, M. and Von Zastrow, M. Ubiquitination-independent trafficking of G protein-coupled receptors to lysosomes. J. Biol. Chem. 277, 50219-50222 (2002).
56. Gullapalli, A., Wolfe, B.L., Griffin, C.T., Magnuson, T., and Trejo, J. An essential role for SNX1 in lysosomal sorting of protease-activated receptor-1: Evidence for retromer-, Hrs-, and Tsg101-independent functions of sorting nexins. Mol. Biol. Cell 17, 1228-1238 (2006).
57. Springael, J.-Y. and Andre, B. Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol. Biol. Cell. 9, 1253-1263 (1998).
58. +-induced down-regulation of the Saccharomyces cerevisiae Gap1p permease involves its ubiquitination with lysine-63-linked chains. J. Cell Sci. 112, 1375-1383 (1999).
59. Galan, J.M., Moreau, V., Andre, B., Volland, C., and Haguenauer-Tsapis, R. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem. 271, 10946-10952 (1996).
60. Rotin, D., Staub, O., and Haguenauer-Tsapis, R. Ubiquitination and endocytosis of plasma membrane proteins: Role of Nedd4/Rsp5p family of ubiquitin-protein ligases. J. Membr. Biol. 176, 1-17 (2000).
61. 63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J. 16, 5847-5854 (1997).
62. + channel (ENaC) by ubiquitination. EMBO J. 16, 6325-6336 (1997). This is the first demonstration of ubiquitination of a mammalian transport protein and analysis of the role of this ubiquitination in the function of this channel.
63. Abriel, H. and Staub, O. Ubiquitylation of ion channels. Physiology 20, 398-407 (2005).
64. Gainetdinov, R.R. and Caron, M.G. Monoamine transporters: From genes to behavior. Annu. Rev. Pharmacol. Toxicol. 43, 261-284 (2003).
65. Gether, U., Andersen, P.H., Larsson, O.M., and Schousboe, A. Neurotransmitter transporters: Molecular function of important drug targets. Trends Pharmacol. Sci. 27, 375-383 (2006).
66. Miranda, M., Wu, C. C., Sorkina, T., Korstjens, D. R. and Sorkin, A. Enhanced ubiquitylation and accelerated degradation of the dopamine transporter mediated by protein kinase C. J. Biol. Chem. 280, 35617-35624 (2005).
67. Kamsteeg, E.J., Hendriks, G., Boone, M., Konings, I.B., Oorschot, V., van der Sluijs, P., Klumperman, J., and Deen, P.M. Short-chain ubiquitination mediates the regulated endocytosis of the aquaporin-2 water channel. Proc. Natl. Acad. Sci. U. S. A. 103, 18344-18349 (2006).
68. Sorkina, T., Miranda, M., Dionne, K.R., Hoover, B.R., Zahniser, N.R., and Sorkin, A. RNA interference screen reveals an essential role of Nedd4-2 in dopamine transporter ubiquitination and endocytosis. J. Neurosci. 26, 8195-8205 (2006).
69. + channel deleted in Liddle's syndrome. EMBO J. 15, 2371-2380 (1996). An early report regarding the important role of the NEDD4 family of HECT domain-containing E3 ligases in regulating mammalian transport proteins.
70. Harvey, K.F., Dinudom, A., Cook, D.I., and Kumar, S. The Nedd4-like protein KIAA0439 is a potential regulator of the epithelial sodium channel. J. Biol. Chem. 276, 8597-8601 (2001).
71. Boehmer, C., Palmada, M., Rajamanickam, J., Schniepp, R., Amara, S., and Lang, F. Post-translational regulation of EAAT2 function by co-expressed ubiquitin ligase Nedd4-2 is impacted by SGK kinases. J. Neurochem. 97, 911-921 (2006).
72. Miranda, M., Dionne, K.R., Sorkina, T., and Sorkin, A. Three ubiquitin conjugation sites in the amino terminus of the dopamine transporter mediate protein kinase C-dependent endocytosis of the transporter. Mol. Biol. Cell 18, 313-323 (2007).
73. Sorkina, T., Hoover, B.R., Zahniser, N.R., and Sorkin, A. Constitutive and protein kinase C-induced internalization of the dopamine transporter is mediated by a clathrin-dependent mechanism. Traffic 6, 157-170 (2005).
74. Wang, H., Traub, L.M., Weixel, K.M. et al. Clathrin-mediated endocytosis of the epithelial sodium channel: Role of epsin. J. Biol. Chem. 281, 14129-14135 (2006).
75. Daniels, G.M. and Amara, S.G. Regulated trafficking of the human dopamine transporter. Clathrin-mediated internalization and lysosomal degradation in response to phorbol esters. J. Biol. Chem. 274, 35794-35801 (1999).
76. Sorkina, T., Doolen, S., Galperin, E., Zahniser, N.R., and Sorkin, A. Oligomerization of dopamine transporters visualized in living cells by fluorescence resonance energy transfer microscopy. J. Biol. Chem. 278, 28274-28283 (2003).
77. Hersch, S.M., Yi, H., Heilman, C.J., Edwards, R.H., and Levey, A.I. Subcellular localization and molecular topology of the dopamine transporter in the striatum and substantia nigra. J. Comp. Neurol. 388, 211-227 (1997).
78. + channel. J. Biol. Chem. 278, 20019-20028 (2003).
79. Rubin, C., Gur, G., and Yarden, Y. Negative regulation of receptor tyrosine kinases: Unexpected links to c-Cbl and receptor ubiquitylation. Cell Res. 15, 66-71 (2005).
80. Xia, X., Roundtree, M., Merikhi, A., Lu, X., Shentu, S., and Lesage, G. Degradation of the apical sodium-dependent bile acid transporter by the ubiquitin-proteasome pathway in cholangiocytes. J. Biol. Chem. 279, 44931-44937 (2004).
81. Hatanaka, T., Hatanaka, Y., and Setou, M. Regulation of amino acid transporter ATA2 by ubiquitin ligase Nedd4-2. J. Biol. Chem. 281, 35922-35930 (2006).
82. Hryciw, D.H., Ekberg, J., Lee, A., Lensink, I.L., Kumar, S., Guggino, W.B., Cook, D.I., Pollock, C.A., and Poronnik, P. Nedd4-2 Functionally Interacts with ClC-5: Involvement in constitutive albumin endocytosis in proximal tubule cells. J. Biol. Chem. 279, 54996-55007 (2004).
83. Miranda, M., Sorkina, T., Grammatopoulos, T.N., Zawada, W.M., and Sorkin, A. Multiple molecular determinants in the carboxyl terminus regulate dopamine transporter export from endoplasmic reticulum. J. Biol. Chem. 279, 30760-30770 (2004).
84. Mao, X., Kim, B.-E., Wang, F., Eide, D.J., and Petris, M.J. A Histidine-rich cluster mediates the ubiquitination and degradation of the human zinc transporter, hZIP4, and protects against zinc cytotoxicity. J. Biol. Chem. 282, 6992-7000 (2007).
85. +-ATPase α1 and α2 subunits. FEBS Letts. 405, 281-284 (1997).
86. Zhang, Z., Wu, J.-Y., Hait, W.N., and Yang, J.-M. Regulation of the stability of P-glycoprotein by ubiquitination. Mol. Pharmacol. 66, 395-403 (2004).
87. Leitch, V., Agre, P., and King, L. S. Altered ubiquitination and stability of aquaporin-1 in hypertonic stress. Proc. Natl. Acad. Sci. U.S.A. 98, 2894-2898 (2001).
88. Zheng, Y.-J., Furukawa, T., Ogura, T., Tajimi, K., and Inagaki, N. M Phase-specific expression and phosphorylation-dependent ubiquitination of the ClC-2 channel. J. Biol. Chem. 277, 32268-32273 (2002).
89. + channel by interaction of Nedd4 with a PY motif deleted in Liddle's Syndrome. J. Biol. Chem. 273, 30012-30017 (1998).
90. Büttner, C., Sadtler, S., Leyendecker, A., Laube, B., Griffon, N., Betz, H., and Schmalzing, G. Ubiquitination precedes internalization and proteolytic cleavage of plasma membrane-bound glycine receptors. J. Biol. Chem. 276, 42978-42985 (2001).
91. + channels KCNQ2/3 and KCNQ3/5 by ubiquitination: Novel role for NEDD4-2. J. Biol. Chem., in press (2007).
92. Fotia, A.B., Ekberg, J., Adams, D.J., Cook, D.I., Poronnik, P., and Kumar, S. Regulation of neuronal voltage-gated sodium channels by the ubiquitin-protein ligases Nedd4 and Nedd4-2. J. Biol. Chem. 279, 28930-28935 (2004).
93. v1.5 is regulated by Nedd4-2 mediated ubiquitination. Circ. Res. 95, 284-291 (2004).
94. Kato, A., Rouach, N., Nicoll, R.A., and Bredt, D.S. Activity-dependent NMDA receptor degradation mediated by retrotranslocation and ubiquitination. Proc. Natl. Acad. Sci. U. S. A. 102, 5600-5605 (2005).
95. Lin, D.H., Sterling, H., Wang, Z., Babilonia, E., Yang, B., Dong, K., Hebert, S.C., Giebisch, G., and Wang, W.H. ROMK1 channel activity is regulated by monoubiquitination. Proc. Natl. Acad. Sci. U. S. A. 102, 4306-4311 (2005).