ALIX regulates the ubiquitin-independent lysosomal sorting of the P2Y1 purinergic receptor via a YPX3 L motif

PLoS ONE

Volumn 11, Issue 6, 2016, Pages

  Dores, Michael R ^a,b   Grimsey, Neil J ^a   Mendez, Francisco ^a   Trejo, JoAnn ^a  

^a San Diego   (United States)

^b HOFSTRA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN ALIX; PURINERGIC P2Y1 RECEPTOR; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; CELL CYCLE PROTEIN; ESCRT PROTEIN; PDCD6IP PROTEIN, HUMAN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UBIQUITIN; VPS4A PROTEIN, HUMAN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; LYSOSOME; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; UBIQUITINATION; ANIMAL; HELA CELL LINE; METABOLISM; PROTEIN DENATURATION;

AMINO ACID MOTIFS; ANIMALS; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HELA CELLS; HUMANS; LYSOSOMES; PROTEIN DENATURATION; RECEPTORS, PURINERGIC P2Y1; UBIQUITIN; UBIQUITINATION; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84976385658     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0157587     Document Type: Article

References (56)

1. Stevens RC, Cherezov V, Katritch V, Abagyan R, Kuhn P, Rosen H, et al. The GPCR Network: a largescale collaboration to determine human GPCR structure and function. Nat Rev Drug Discov. 2013; 12 (1):25-34. doi: 10.1038/nrd3859 PMID: 23237917; PubMed Central PMCID: PMCPMC3723354.
2. O'Hayre M, Degese MS, Gutkind JS. Novel insights into G protein and G protein-coupled receptor signaling in cancer. Curr Opin Cell Biol. 2014; 27:126-35. doi: 10.1016/j.ceb.2014.01.005 PMID: 24508914; PubMed Central PMCID: PMC4021379.
3. Mason JS, Bortolato A, Congreve M, Marshall FH. New insights from structural biology into the druggability of G protein-coupled receptors. Trends Pharmacol Sci. 2012; 33(5):249-60. doi: 10.1016/j.tips. 2012.02.005 PMID: 22465153.
4. Dores MR, Chen B, Lin H, Soh UJK, Paing MM, Montagne WA, et al. ALIX binds a YPX3L motif of the GPCR PAR1 and mediates ubiquitin-independent ESCRT-III/MVB sorting. J Cell Biol. 2012; 197 (3):407-19. doi: 10.1083/jcb.201110031 PMID: 22547407
5. Marchese A, Paing MM, Temple BRS, Trejo J. G protein-coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol. 2008; 48(1):601-29. doi: 10.1146/annurev.pharmtox.48. 113006.094646
6. Arora P, Ricks TK, Trejo J. Protease-activated receptor signalling, endocytic sorting and dysregulation in cancer. J Cell Sci. 2007; 120(6):921-8. doi: 10.1242/jcs.03409
7. Shen J, DiCorleto PE. ADP stimulates human endothelial cell migration via P2Y1 nucleotide receptormediated mitogen-activated protein kinase pathways. Circ Res. 2008; 102(4):448-56. doi: 10.1161/ CIRCRESAHA.107.165795 PMID: 18174464.
8. Govindan S, Taylor EJ, Taylor CW. Ca(2+) signalling by P2Y receptors in cultured rat aortic smooth muscle cells. Br J Pharmacol. 2010; 160(8):1953-62. doi: 10.1111/j.1476-5381.2010.00763.x PMID: 20649593; PubMed Central PMCID: PMCPMC2913105.
9. Hardy AR, Jones ML, Mundell SJ, Poole AW. Reciprocal cross-talk between P2Y1 and P2Y12 receptors at the level of calcium signaling in human platelets. Blood. 2004; 104(6):1745-52. doi: 10.1182/ blood-2004-02-0534 PMID: 15187029.
10. Shinozaki Y, Koizumi S, Ohno Y, Nagao T, Inoue K. Extracellular ATP counteracts the ERK1/2-mediated death-promoting signaling cascades in astrocytes. Glia. 2006; 54(6):606-18. doi: 10.1002/glia. 20408 PMID: 16944453.
11. Wei Q, Costanzi S, Liu QZ, Gao ZG, Jacobson KA. Activation of the P2Y1 receptor induces apoptosis and inhibits proliferation of prostate cancer cells. Biochemical Pharmacology. 2011; 82(4):418-25. Epub 2011/06/03. doi: 10.1016/j.bcp.2011.05.013 PMID: 21632028; PubMed Central PMCID: PMC3140712.
12. Ko T, An HJ, Ji YG, Kim OJ, Lee DH. P2Y Receptors Regulate Proliferation of Human Pancreatic Duct Epithelial Cells. Pancreas. 2012; 41(5):797-803. doi: 10.1097/MPA.0b013e31823ba3b3 PMID: 22249129
13. Reiner S, Ziegler N, Leon C, Lorenz K, von Hayn K, Gachet C, et al. beta-Arrestin-2 interaction and internalization of the human P2Y1 receptor are dependent on C-terminal phosphorylation sites. Mol Pharmacol. 2009; 76(6):1162-71. Epub 2009/09/11. doi: 10.1124/mol.109.060467 PMID: 19741005.
14. Nisar S, Kelly E, Cullen PJ, Mundell SJ. Regulation of P2Y1 receptor traffic by sorting Nexin 1 is retromer independent. Traffic. 2010; 11(4):508-19. Epub 2010/01/15. doi: 10.1111/j.1600-0854.2010. 01035.x PMID: 20070609.
15. Kanazawa C, Morita E, Yamada M, Ishii N, Miura S, Asao H, et al. Effects of deficiencies of STAMs and Hrs, mammalian class E Vps proteins, on receptor downregulation. Biochemical and Biophysical Research Communications. 2003; 309(4):848-56. doi: 10.1016/j.bbrc.2003.08.078 PMID: 13679051
16. Hierro A, Sun J, Rusnak AS, Kim J, Prag G, Emr SD, et al. Structure of the ESCRT-II endosomal trafficking complex. Nature. 2004; 431(7005):221-5. PMID: 15329733.
17. Im YJ, Wollert T, Boura E, Hurley JH. Structure and Function of the ESCRT-II-III Interface in Multivesicular Body Biogenesis. Developmental Cell. 2009; 17(2):234-43. doi: 10.1016/j.devcel.2009.07.008 PMID: 19686684
18. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH. Membrane scission by the ESCRT-III complex. Nature. 2009; 458(7235):172-7. doi: 10.1038/nature07836 PMID: 19234443
19. Sachse M, Strous GJ, Klumperman J. ATPase-deficient hVPS4 impairs formation of internal endosomal vesicles and stabilizes bilayered clathrin coats on endosomal vacuoles. Journal of Cell Science. 2004; 117(Pt 9):1699-708. Epub 2004/04/13. doi: 10.1242/jcs.00998 PMID: 15075231.
20. Merrill S, Hanson PI. Activation of Human Vps4A by ESCRT-III Proteins Reveals Ability of Substrates to Relieve Enzyme Autoinhibition. Journal of Biological Chemistry. 2010; 285(46):35428-38. doi: 10. 1074/jbc.M110.126318 PMID: 20805225
21. Carlton JG, Agromayor M, Martin-Serrano J. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc Nat Acad Sci USA. 2008; 105(30):10541-6. doi: 10.1073/pnas. 0802008105 PMID: 18641129
22. Bissig C, Gruenberg J. ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell Biol. 2014; 24(1):19-25. Epub 2013/11/30. doi: 10.1016/j.tcb.2013.10.009 PMID: 24287454.
23. Grimsey NJ, Aguilar B, Smith TH, Le P, Soohoo AL, Puthenveedu MA, et al. Ubiquitin plays an atypical role in GPCR-induced p38 MAP kinase activation on endosomes. J Cell Biol. 2015; 210(7):1117-31. doi: 10.1083/jcb.201504007 PMID: 26391660; PubMed Central PMCID: PMCPMC4586747.
24. Fairn GD, Schieber NL, Ariotti N, Murphy S, Kuerschner L, Webb RI, et al. High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J Cell Biol. 2011; 194(2):257-75. doi: 10.1083/jcb.201012028 PMID: 21788369; PubMed Central PMCID: PMCPMC3144401.
25. Malerod L, Stuffers S, Brech A, Stenmark H. Vps22/EAP30 in ESCRT-II Mediates Endosomal Sorting of Growth Factor and Chemokine Receptors Destined for Lysosomal Degradation. Traffic. 2007; 8 (11):1617-29. PMID: 17714434
26. Dores MR, Trejo J. GPCR sorting at multivesicular endosomes. Methods Cell Biol. 2015; 130:319-32. doi: 10.1016/bs.mcb.2015.05.006 PMID: 26360043.
27. Hasdemir B, Bunnett NW, Cottrell GS. Hepatocyte Growth Factor-regulated Tyrosine Kinase Substrate (HRS) Mediates Post-endocytic Trafficking of Protease-activated Receptor 2 and Calcitonin Receptorlike Receptor. J Biol Chem. 2007; 282(40):29646-57. doi: 10.1074/jbc.M702974200 PMID: 17675298
28. Marchese A, Raiborg C, Santini F, Keen JH, Stenmark H, Benovic JL. The E3 ubiquitin ligase AIP4 mediates ubiquitination and sorting of the G protein-coupled receptor CXCR4. Dev Cell. 2003; 5 (5):709-22. PMID: 14602072.
29. Shenoy SK, McDonald PH, Kohout TA, Lefkowitz RJ. Regulation of receptor fate by ubiquitination of activated b2 - adrenergic receptor and b-arrestin. Science. 2001; 294(5545):1307-13. PMID: 11588219
30. Bache KG, Raiborg C, Mehlum A, Stenmark H. STAM and Hrs are subunits of a multivalent ubiquitinbinding complex on early endosomes. J Biol Chem. 2003; 278:12513-21. PMID: 12551915.
31. Gullapalli A, Wolfe BL, Griffin CT, Magnuson T, 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. 2006; 17(3):1228-38. doi: 10.1091/mbc.E05-09-0899 PMID: 16407403
32. Lu Q, Hope LW, Brasch M, Reinhard C, Cohen SN. TSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation. Proc Natl Acad Sci U S A. 2003. PMID: 12802020.
33. Chin LS, Raynor MC, Wei X, Chen HQ, Li L. Hrs interacts with sorting nexin 1 and regulates degradation of epidermal growth factor receptor. J Biol Chem. 2001; 276(10):7069-78. PMID: 11110793
34. Scheuring S, Rohricht RA, Schoning-Burkhardt B, Beyer A, Muller S, Abts HF, et al. Mammalian cells express two VPS4 proteins both of which are involved in intracellular protein trafficking. Journal of molecular biology. 2001; 312(3):469-80. doi: 10.1006/jmbi.2001.4917 PMID: 11563910.
35. Pols MS, Klumperman J. Trafficking and function of the tetraspanin CD63. Exp Cell Res. 2009; 315 (9):1584-92. doi: 10.1016/j.yexcr.2008.09.020 PMID: 18930046.
36. Xiao K, Shenoy SK. Beta2-adrenergic receptor lysosomal trafficking is regulated by ubiquitination of lysyl residues in two distinct receptor domains. The Journal of biological chemistry. 2011; 286 (14):12785-95. Epub 2011/02/19. doi: 10.1074/jbc.M110.203091 PMID: 21330366; PubMed Central PMCID: PMC3069478.
37. Jacob C, Cottrell GS, Gehringer D, Schmidlin F, Grady EF, Bunnett NW. c-Cbl Mediates Ubiquitination, Degradation, and Down-regulation of Human Protease-activated Receptor 2. J Biol Chem. 2005; 280 (16):16076-87. doi: 10.1074/jbc.M500109200 PMID: 15708858
38. Hislop JN, Marley A, von Zastrow M. Role of Mammalian Vacuolar Protein-sorting Proteins in Endocytic Trafficking of a Non-ubiquitinated G Protein-coupled Receptor to Lysosomes. J Biol Chem. 2004; 279 (21):22522-31. doi: 10.1074/jbc.M311062200 PMID: 15024011
39. Tanowitz M, von Zastrow M. Ubiquitination-independent trafficking of G protein-coupled receptors to lysosomes. J Biol Chem. 2002; 277(52):50219-22. PMID: 12401797.
40. Wolfe BL, Marchese A, Trejo J. Ubiquitination differentially regulates clathrin-dependent internalization of protease-activated receptor-1. J Cell Biol. 2007; 177(5):905-16. doi: 10.1083/jcb.200610154 PMID: 17535965
41. Whistler JL, Enquist J, Marley A, Fong J, Gladher F, Tsuruda P, et al. Modulation of postendocytic sorting of G protein-coupled receptors. Science. 2002; 297(5581):615-20. PMID: 12142540.
42. Heydorn A, Sondergaard BP, Ersboll B, Holst B, Nielsen FC, Haft CR, et al. A library of 7TM receptor C-terminal tails. Interactions with the proposed post-endocytic sorting proteins ERM-binding phosphoprotein 50 (EBP50), N-ethylmaleimide-sensitive factor (NSF), sorting nexin 1 (SNX1), and G protein-coupled receptor-associated sorting protein (GASP). The Journal of biological chemistry. 2004; 279 (52):54291-303. Epub 2004/09/29. doi: 10.1074/jbc.M406169200 PMID: 15452121.
43. Marley A, von Zastrow M. Dysbindin promotes the post-endocytic sorting of G protein-coupled receptors to lysosomes. PLoS One. 2010; 5(2):e9325. doi: 10.1371/journal.pone.0009325 PMID: 20174469; PubMed Central PMCID: PMC2824829.
44. Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD. ESCRT-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev Cell. 2002; 3(2):271-82. PMID: 12194857
45. Babst M, Wendland B, Estepa EJ, Emr SD. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 1998; 17(11):2982-93. PMID: 9606181
46. Lata S, Schoehn G, Jain A, Pires R, Piehler J, Gëttlinger HG, et al. Helical Structures of ESCRT-III Are Disassembled by VPS4. Science. 2008; 321(5894):1354-7. doi: 10.1126/science.1161070 PMID: 18687924
47. van Weering JR, Sessions RB, Traer CJ, Kloer DP, Bhatia VK, Stamou D, et al. Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO J. 2012; 31(23):4466-80. doi: 10.1038/emboj.2012.283 PMID: 23085988; PubMed Central PMCID: PMCPMC3512392.
48. Freeman CL, Hesketh G, Seaman MN. RME-8 coordinates the activity of the WASH complex with the function of the retromer SNX dimer to control endosomal tubulation. J Cell Sci. 2014; 127(Pt 9):2053-70. doi: 10.1242/jcs.144659 PMID: 24643499; PubMed Central PMCID: PMCPMC4004978.
49. McCullough J, Fisher RD, Whitby FG, Sundquist WI, Hill CP. ALIX-CHMP4 interactions in the human ESCRT pathway. Proceedings of the National Academy of Sciences. 2008; 105(22):7687-91. doi: 10. 1073/pnas.0801567105
50. Bissig C, Lenoir M, Velluz MC, Kufareva I, Abagyan R, Overduin M, et al. Viral infection controlled by a calcium-dependent lipid-binding module in ALIX. Dev Cell. 2013; 25(4):364-73. doi: 10.1016/j.devcel. 2013.04.003 PMID: 23664863; PubMed Central PMCID: PMCPMC4129370.
51. Zhai Q, Fisher RD, Chung H-Y, Myszka DG, Sundquist WI, Hill CP. Structural and functional studies of ALIX interactions with YPXnL late domains of HIV-1 and EIAV. Nat Struct Mol Biol. 2008; 15(1):43-9. http://www.nature.com/nsmb/journal/v15/n1/suppinfo/nsmb1319-S1.html. PMID: 18066081
52. Dores MR, Lin H, Grimsey N, Mendez F, Trejo J. The alpha arrestin ARRDC3 regulates ALIX ubiquitination and G protein-coupled receptor lysosomal sorting. Mol Biol Cell. 2015;In Press.
53. Pashkova N, Gakhar L, Winistorfer SC, Sunshine AB, Rich M, Dunham MJ, et al. The Yeast Alix Homolog Bro1 Functions as a Ubiquitin Receptor for Protein Sorting into Multivesicular Endosomes. Developmental Cell. 2013. Epub 2013/06/04. doi: 10.1016/j.devcel.2013.04.007 PMID: 23726974.
54. Keren-Kaplan T, Attali I, Estrin M, Kuo LS, Farkash E, Jerabek-Willemsen M, et al. Structure-based in silico identification of ubiquitin-binding domains provides insights into the ALIX-V:ubiquitin complex and retrovirus budding. EMBO J. 2013; 32(4):538-51. Epub 2013/01/31. doi: 10.1038/emboj.2013.4 PMID: 23361315; PubMed Central PMCID: PMC3579145.
55. Pires R, Hartlieb B, Signor L, Schoehn G, Lata S, Roessle M, et al. A crescent-shaped ALIX dimer targets ESCRT-III CHMP4 filaments. Structure. 2009; 17(6):843-56. Epub 2009/06/16. doi: 10.1016/j.str. 2009.04.007 PMID: 19523902; PubMed Central PMCID: PMC2699623.
56. Tsvetanova NG, Irannejad R, von Zastrow M. G protein-coupled receptor (GPCR) signaling via heterotrimeric G proteins from endosomes. J Biol Chem. 2015; 290(11):6689-96. doi: 10.1074/jbc.R114. 617951 PMID: 25605726; PubMed Central PMCID: PMCPMC4358092.