Ubiquitylation is required for degradation of transmembrane surface proteins in Trypanosomes

Traffic

Volumn 9, Issue 10, 2008, Pages 1681-1697

  Chung, Wei Lian ^a   Leung, Ka Fai ^a   Carrington, Mark ^a   Field, Mark C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Endocytosis; Intracellular transport; Targeting; Trypanosomes; Ubiquitin; Vesicle transport

Indexed keywords

CBL PROTEIN; CLATHRIN; GENE PRODUCT; GLYCOPROTEIN; LYSINE; MEMBRANE PROTEIN; NEDD8 PROTEIN; PROTEASOME; PROTEIN RSP5P; PROTEIN UBA 1; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ACIDITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LINEAGE; CELL TRANSPORT; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; EUKARYOTIC CELL; GENETIC CONSERVATION; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TRYPANOSOMA BRUCEI; UBIQUITINATION;

ANIMALS; CLATHRIN; CYTOSOL; ENDOCYTOSIS; ENDOSOMES; GLYCOSYLPHOSPHATIDYLINOSITOLS; MEMBRANE PROTEINS; MUCOPROTEINS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; TRANSFECTION; TRYPANOSOMA BRUCEI BRUCEI; UBIQUITIN;

EID: 47149099160     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00785.x     Document Type: Article

References (56)

1. Mayor S, Riezman H. Sorting GPI-anchored proteins. Nat Rev Mol Cell Biol 2004;5:110-120.
2. Robinson MS. Adaptable adaptors for coated vesicles. Trends Cell Biol 2004;14:167-174.
3. Hicke L, Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 2003;19:141-172.
4. Bonifacino JS, Weissman AM. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu Rev Cell Dev Biol 1998;14:19-57.
5. Kerscher O, Felberbaum R, Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 2006;22:159-180.
6. de Melker AA, van der Horst G, Calafat J, Jansen H, Borst J. c-Cbl ubiquitinates the EGF receptor at the plasma membrane and remains receptor associated throughout the endocytic route. J Cell Sci 2001;114:2167-2178.
7. Huang F, Goh LK, Sorkin A. EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci U S A 2007;104:16904-16909.
8. Hawryluk MJ, Keyel PA, Mishra SK, Watkins SC, Heuser JE, Traub LM. Epsin 1 is a polyubiquitin-selective clathrin-associated sorting protein. Traffic 2006;7:262-281.
9. Fisher RD, Wang B, Alam SL, Higginson DS, Robinson H, Sundquist WI, Hill CP. Structure and ubiquitin binding of the ubiquitin-interacting motif. J Biol Chem 2003;278:28976-28984.
10. Katz M, Shtiegman K, Tal-Or P, Yakir L, Mosesson Y, Harari D, Machluf Y, Asao H, Jovin T, Sugamura K, Yarden Y. Ligand-independent degradation of epidermal growth factor receptor involves receptor ubiquitylation and Hgs, an adaptor whose ubiquitin-interacting motif targets ubiquitylation by Nedd4. Traffic 2002;3:740-751.
11. Klapisz E, Sorokina I, Lemeer S, Pijnenburg M, Verkleij AJ, van Bergen en Henegouwen PM. A ubiquitin-interacting motif (UIM) is essential for Eps15 and Eps15R ubiquitination. J Biol Chem 2002;277:30746-30753.
12. Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, Bossi G, Chen H, De Camilli P, Di Fiore PP. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 2002;416:451-455.
13. Miller SL, Malotky E, O'Bryan JP. Analysis of the role of ubiquitin-interacting motifs in ubiquitin binding and ubiquitylation. J Biol Chem 2004;279:33528-33537.
14. Oved S, Mosesson Y, Zwang Y, Santonico E, Shtiegman K, Marmor MD, Kochupurakkal BS, Katz M, Lavi S, Cesareni G, Yarden Y. Conjugation to Nedd8 instigates ubiquitylation and down-regulation of activated receptor tyrosine kinases. J Biol Chem 2006;281:21640-21651.
15. Hurley JH, Emr SD. The ESCRT complexes: Structure and mechanism of a membrane-trafficking network. Annu Rev Biophys Biomol Struct 2006;35:277-298.
16. Williams RL, Urbe S. The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol 2007;8:355-368.
17. Field MC, Gabernet-Castello C, Dacks JB. 'Reconstructing the evolution of the endocytic system: Insights from genomics and molecular cell biology'. Adv Exp Med Biol 2007;607:84-96.
18. Dacks JB, Field MC. Evolution of the eukaryotic membrane-trafficking system: Origin, tempo and mode. J Cell Sci 2007;120:2977-2985.
19. Ferguson MA. The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J Cell Sci 1999;112:2799-2809.
20. Field MC, Carrington M. Intracellular membrane transport systems in Trypanosoma brucei. Traffic 2004;5:905-913.
21. Tazeh NN, Bangs JD. Multiple motifs regulate trafficking of the LAMP-like protein p67 in the ancient eukaryote Trypanosoma brucei. Traffic 2007;8:1007-1017.
22. Allen CL, Goulding D, Field MC. Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J 2003;22:4991-5002.
23. Allen CL, Liao D, Chung WL, Field MC. Dileucine signal-dependent and AP-1-independent targeting of a lysosomal glycoprotein in Trypanosoma brucei. Mol Biochem Parasitol 2007;156:175-190.
24. Morgan GW, Goulding D, Field MC. The single dynamin-like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. J Biol Chem 2004;279:10692-10701.
25. Denny PW, Field MC, Smith DF. GPI-anchored proteins and glycoconjugates segregate into lipid rafts in Kinetoplastida. FEBS Lett 2001;491:148-153.
26. Grunfelder CG, Engstler M, Weise F, Schwarz H, Stierhof YD, Morgan GW, Field MC, Overath P. Endocytosis of a glycosylphosphatidylinositol-anchored protein via clathrin-coated vesicles, sorting by default in endosomes, and exocytosis via RAB11-positive carriers. Mol Biol Cell 2003;14:2029-2040.
27. Ziegelbauer K, Overath P. Identification of invariant surface glycoproteins in the bloodstream stage of Trypanosoma brucei. J Biol Chem 1992;267:10791-10796.
28. Chung WL, Carrington M, Field MC. Cytoplasmic targeting signals in transmembrane invariant surface glycoproteins of trypanosomes. J Biol Chem 2004;279:54887-54895.
29. Hua S, To WY, Nguyen TT, Wong ML, Wang CC. Purification and characterization of proteasomes from Trypanosoma brucei. Mol Biochem Parasitol 1996;78:33-46.
30. Li Z, Wang CC. Functional characterization of the 11 non-ATPase subunit proteins in the trypanosome 19 S proteasomal regulatory complex. J Biol Chem 2002;277:42686-42693.
31. Hein C, Springael JY, Volland C, Haguenauer-Tsapis R, Andre B. NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol Microbiol 1995;18:77-87.
32. Galan JM, Moreau V, Andre B, Volland C, Haguenauer-Tsapis R. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J Biol Chem 1996;271:10946-10952.
33. Morvan J, Froissard M, Haguenauer-Tsapis R, Urban-Grimal D. The ubiquitin ligase Rsp5p is required for modification and sorting of membrane proteins into multivesicular bodies. Traffic 2004;5:383-392.
34. Wang G, McCaffery JM, Wendland B, Dupre S, Haguenauer-Tsapis R, Huibregtse JM. Localization of the Rsp5p ubiquitin-protein ligase at multiple sites within the endocytic pathway. Mol Cell Biol 2001;21:3564-3575.
35. Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, Dikic I. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 2003;5:461-466.
36. Rubin C, Gur G, Yarden Y. Negative regulation of receptor tyrosine kinases: Unexpected links to c-Cbl and receptor ubiquitylation. Cell Res 2005;15:66-71.
37. Thien CB, Langdon WY. Cbl: Many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol 2001;2:294-307.
38. Ingham RJ, Gish G, Pawson T. The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture. Oncogene 2004;23:1972-1984.
39. Leung KF, Dacks JB, Field MC. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 2008; doi: 10.1111/j.1600-0854.2008.00797.x
40. McGrath JP, Jentsch S, Varshavsky A. UBA 1: An essential yeast gene encoding ubiquitin-activating enzyme. EMBO J 1991;10:227-236.
41. Handley PM, Mueckler M, Siegel NR, Ciechanover A, Schwartz AL. Molecular cloning, sequence, and tissue distribution of the human ubiquitin-activating enzyme E1. Proc Natl Acad Sci U S A 1991;1:258-262.
42. Jin J, Li X, Gygi SP, Harper JW. Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 2007;447:1135-1138.
43. Pelzer C, Kassner I, Matentzoglu K, Singh RK, Wollscheid HP, Scheffner M, Schmidtke G, Groettrup M. UBE1L2, a novel E1 enzyme specific for ubiquitin. J Biol Chem 2007;282:23010-23014.
44. Nolan DP, Geuskens M, Pays E. N-linked glycans containing linear poly-N-acetyllactosamine as sorting signals in endocytosis in Trypanosoma brucei. Curr Biol 1999;9:1169-1172.
45. Pal A, Hall BS, Nesbeth DN, Field HI, Field MC. Differential endocytic functions of Trypanosoma brucei Rab5 isoforms reveal a glycosylphosphatidylinositol-specific endosomal pathway. J Biol Chem 2002;277:9529-9539.
46. Pal A, Hall BS, Jeffries TR, Field MC. Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein antibody recycling in Trypanosoma brucei. Biochem J 2003;374:443-451.
47. Ackers JP, Dhir V, Field MC. A bioinformatic analysis of the RAB genes of Trypanosoma brucei. Mol Biochem Parasitol 2005;141:89-97.
48. Seyfang A, Mecke D, Duszenko M. Degradation, recycling, and shedding of Trypanosoma brucei variant surface glycoprotein. J Protozool 1990;37:546-552.
49. Terrell J, Shih S, Dunn R, Hicke L. A function for monoubiquitination in the internalization of a G protein-coupled receptor. Mol Cell 1998;1:193-202.
50. Barriere H, Nemes C, Lechardeur D, Khan-Mohammad M, Fruh K, Lukacs GL. Molecular basis of oligoubiquitin-dependent internalization of membrane proteins in mammalian cells. Traffic 2006;7:282-297.
51. Urbe S, Sachse M, Row PE, Preisinger C, Barr FA, Strous G, Klumperman J, Clague MJ. The UIM domain of Hrs couples receptor sorting to vesicle formation. J Cell Sci 2003;116:4169-4179.
52. Hirumi H, Hirumi K. Axenic culture of African trypanosome bloodstream forms. Parasitol Today 1994;10:80-84.
53. Wirtz E, Leal S, Ochatt C, Cross GA. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 1999;99:89-101.
54. Redmond S, Vadivelu J, Field MC. RNAit: An automated web-based tool for the selection of RNAi targets in Trypanosoma brucei. Mol Biochem Parasitol 2003;128:115-118.
55. Nolan DP, Jackson DG, Biggs MJ, Brabazon ED, Pays A, Van Laethem F, Paturiaux-Hanocq F, Elliott JF, Voorheis HP, Pays E. Characterization of a novel alanine-rich protein located in surface microdomains in Trypanosoma brucei. J Biol Chem 2000;275:4072-4080.
56. Subramaniam C, Veazey P, Redmond S, Hayes-Sinclair J, Chambers E, Carrington M, Gull K, Matthews K, Horn D, Field MC. Chromosome-wide analysis of gene function by RNA interference in the African trypanosome. Eukaryot Cell 2006;5:1539-1549.