Post-translational modifications of exosomal proteins

Frontiers in Immunology

Volumn 5, Issue AUG, 2014, Pages

  Moreno Gonzalo, Olga ^a,b   Villarroya Beltri, Carolina ^a,b   Sánchez Madrid, Francisco ^a,b  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

Author keywords

Exosomes; Multivesicular bodies; Post translational modifications; Sorting; Ubiquitination

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPITHELIAL GROWTH FACTOR RECEPTOR; ESCRT PROTEIN; EXOSOMAL PROTEIN; FAS LIGAND; GROWTH FACTOR RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ACETYLATION; EXOSOME; HUMAN; MAJOR HISTOCOMPATIBILITY COMPLEX; MASS SPECTROMETRY; MULTIVESICULAR BODY; MYRISTYLATION; NITROSYLATION; OXIDATION; PALMITOYLATION; POLYGLUTAMYLATION; PROTEIN GLYCOSYLATION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PRENYLATION; PROTEIN PROCESSING; SHORT SURVEY; SUMOYLATION; UBIQUITINATION;

EID: 84919499685     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00383     Document Type: Short Survey

References (56)

1. Uy R, Wold R Posttranslational covalent modification of proteins. Science (1977) 198(4320):890-6. doi:10.1126/science.337487
2. Xin F, Radivojac P. Post-translational modifications induce significant yet not extreme changes to protein structure. Bioinformatics (2012) 28(22):2905-13. doi:10.1093/bioinformatics/bts541bts541
3. Bode AM, Dong Z. Post-translational modification of p53 in tumorigenesis. Nat Rev Cancer (2004) 4(10):793-805. doi:10.1038/nrcl455
4. Gong CX, Liu F, Grundke-Iqbal I, Iqbal K. Post-translational modifications of tau protein in Alzheimer's disease. J Neural Transm (2005) 112(6):813-38. doi:10.1007/s00702-004-0221-0
5. Martin L, Latypova X, Terro F. Post-translational modifications of tau protein: implications for Alzheimer's disease. Neurochem Int (2011) 58(4):458-71. doi:10.1016/j.neuint.2010.12.023S0197-0186(10)00401-8
6. Toh KL, Jones CR, He Y, Eide EJ, Hinz WA, Virshup DM, et al. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science (2001) 291(5506):1040-3. doi:10.1126/science.l057499
7. Van Eyk JE. Overview: the maturing of proteomics in cardiovascular research. Circ Res (2011) 108(4):490-8. doi:10.1161/CIRCRESAHA.110.226894108/4/ 490
8. Zuccato E, Blott EJ, Holt O, Sigismund S, Shaw M, Bossi G, et al. Sorting of Fas ligand to secretory lysosomes is regulated by mono-ubiquitylation and phosphorylation. / Cell Sci (2007) 120(Pt 1):191-9. doi:10.1242/jcs.03315
9. Valapala M, Vishwanatha JK. Lipid raft endocytosis and exosomal transport facilitate extracellular trafficking of annexin A2. / Biol Chetn (2011) 286(35):30911-25. doi:10.1074/jbc.M111.271155
10. SamanS,KimW, RayaM,VisnickY, Miro S, Jackson B, et al. Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. / Biol Chem (2012) 287(6):3842-9. doi:10.1074/jbc.Ml 11.277061
11. Surgucheva I, SharovVS, Surguchov A. Gamma-Synuclein: seeding of alphasynuclein aggregation and transmission between cells. Biochemistry (2012) 51(23):4743-54. doi:10.1021/bi300478w
12. Escrevente C, Grammel N, Kandzia S, Zeiser J, Tranfield EM, Conradt HS, et al. Sialoglycoproteins and N-glycans from secreted exosomes of ovarian carcinoma cells. PLoS One (2013) 8(10):e78631. doi:10.1371/journal.pone.0078631
13. Batista BS, Eng WS, Pilobello KT, Hendricks-Munoz KD, Mahal LK. Identification of a conserved glycan signature for microvesicles. J Proteome Res (2011) 10(10):4624-33. doi:10.1021/pr200434y
14. Marimpietri D, Petretto A, Raffaghello L, Pezzolo A, Gagliani C, Tacchetti C, et al. Proteome profiling of neuroblastoma-derived exosomes reveal the expression of proteins potentially involved in tumor progression. PLoS One (2013) 8(9):e75054. doi:10.1371/joumal.pone.0075054
15. Shen B, Wu N, Yang JM, Gould SJ. Protein targeting to exosomes/microvesicles by plasma membrane anchors. J Biol Chem (2011) 286(16): 14383-14395. doi:10. 1074/jbc.Ml 10.208660
16. Ikeda M, Longnecker R. Cholesterol is critical for Epstein-Barr virus latent membrane protein 2A trafficking and protein stability. Virology (2007) 360(2):461-8. doi:10.1016/j.virol.2006.10.046
17. Putz U, Howitt J, Doan A, Goh CP, Low LH, Silke J, et al. The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Sci Signal (2012) 5(243):ra70. doi:10.1126/scisignal.2003084
18. Zhu H, Guariglia S, Yu RY, Li W, Brancho D, Peinado H, et al. Mutation of SIMPLE in Charcot-Marie-Tooth 1C alters production of exosomes. Mol Biol Cell (2013) 24(11):1619-37. doi:10.1091/mbc.E12-07-0544
19. Liu Y, Shah SV, Xiang X, Wang J, Deng ZB, Liu C, et al. COP9-associated CSN5 regulates exosomal protein deubiquitination and sorting. Am J Pathol (2009) 174(4):1415-25. doi:10.2353/ajpath.2009.080861
20. Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q. Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. ProcNatl Acad Sci USA (2012) 109(11):4146-51.doi:10.1073/pnas.l200448109
21. Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, et al. Sumoylated hnRNPA2Bl controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun (2013) 4:2980. doi:10.1038/ncomms3980
22. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol (2009) 9(8):581-93. doi:10.1038/nri2567nri2567
23. Tanno H, Komada M. The ubiquitin code and its decoding machinery in the endocytic pathway. / Biochem (2013) 153(6):497-504. doi:10.1093/jb/ mvtO28mvtO28
24. Peng DJ, Zeng M, Muromoto R, Matsuda T, Shimoda K, Subramaniam M, etal. Noncanonical K27-linked polyubiquitination of TIEG1 regulates Foxp3 expression and tumor growth. JImmunol (2011) 186(10):5638-47. doi:10.4049/ jimmunol.1003801
25. Arimoto K, Funami K, Saeki Y, Tanaka K, Okawa K, Takeuchi O, et al. Polyubiquitin conjugation to NEMO by triparite motif protein 23 (TRIM23) is critical in antiviral defense. Proc Natl Acad Sci USA (2010) 107(36):15856-61. doi:10.1073/pnas.l004621107
26. Chastagner P, Israel A, Brou C. Itch/AIP4 mediates Deltex degradation through the formation of K29-linked polyubiquitin chains. EMBO Rep (2006) 7(11):1147-53. doi:10.1038/sj.embor.7400822
27. Wu-Baer F, Lagrazon K, Yuan W, Baer R. The BRCA1/BARD1 heterodimer assembles polyubiquitin chains through an unconventional linkage involving lysine residue K6 of ubiquitin. / Biol Chem (2003) 278(37):34743-6. doi:10.1074/jbc.C300249200
28. Matsumoto ML, Wickliffe KE, Dong KC, Yu C, Bosanac I, Bustos D, et al. Kl 1- linked polyubiquitination in cell cycle control revealed by a K l l linkage-specific antibody. Mol Cell (2010) 39(3):477-84. doi:10.1016/j.molcel.2010.07.001
29. Huang H, Jeon MS, Liao L, Yang C, Elly C, Yates JR III, et al. K33-linked polyubiquitination of T cell receptor-zeta regulates proteolysis-independent T cell signaling. Immunity (2010) 33(1):60-70. doi:10.1016/j.immuni.2010.07.002
30. Bagola K, von Delbruck M, Dittmar G, Scheffner M, Ziv I, Glickman MH, et al. Ubiquitin binding by a CUE domain regulates ubiquitin chain formation by ERAD E3 ligases. Mol Cell (2013) 50(4):528-39. doi:10.1016/j.molcel.2013. 04.005
31. Nathan JA, Kim HT, Ting L, Gygi SP, Goldberg AL. Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes? EMBO J (2013) 32(4):552-65. doi:10.1038/emboj.2012.354
32. Ori D, Kato H, Sanjo H, Tartey S, Mino T, Akira S, et al. Essential roles of K63- linked polyubiquitin-binding proteins TAB2 and TAB3 in B cell activation via MAPKs. /Immunol (2013) 190(8):4037-45. doi:10.4049/jimmunol.l300173
33. Erpapazoglou Z, Dhaoui M, Pantazopoulou M, Giordano F, Mari M, Leon S, et al. A dual role for K63-linked ubiquitin chains in multivesicular body biogenesis and cargo sorting. Mol Biol Cell (2012) 23(11):2170-83. doi:10.1091/mbc. Ell-10-0891
34. McDowell GS, Philpott A. Non-canonical ubiquitylation: mechanisms and consequences. Int! Biochem Cell Biol (2013) 45(8):1833-42. doi:10.1016/j.biocel. 2013.05.026
35. Li H, Wittwer T, Weber A, Schneider H, Moreno R, Maine GN, et al. Regulation of NF-kappaB activity by competition between RelA acetylation and ubiquitination. Oncogene (2012) 31(5):611-23. doi:10.1038/onc.2011.253
36. Lang V, Janzen J, Fischer GZ, Soneji Y, Beinke S, Salmeron A, et al. betaTrCPmediated proteolysis of NF-kappaBl plO5 requires phosphorylation of plO5 serines 927 and 932. Mol Cell Biol (2003) 23(1):402-13. doi:10.1128/MCB.23.1. 402-413.2003
37. Bies J, Markus J, Wolff L. Covalent attachment of the SUMO-1 protein to the negative regulatory domain of the c-Myb transcription factor modifies its stability and transactivation capacity. J Biol Chem (2002) 277(11):8999-9009. doi:10.1074/jbc.Ml 10453200
38. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science (2008) 319(5867):1244-7. doi:10.1126/science.H53124319/5867/1244
39. Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature (2009) 458(7237):445-52. doi:10.1038/ natureO7961
40. Komada M, Kitamura N. Growth factor-induced tyrosine phosphorylation of Hrs, a novel 115-kilodalton protein with a structurally conserved putative zinc finger domain. Mol Cell Biol (1995) 15(11):6213-21.
41. Takeshita T, Arita T, Asao H, Tanaka N, Higuchi M, Kuroda H, et al. Cloning of a novel signal-transducing adaptor molecule containing an SH3 domain and ITAM. Biochem Biophys Res Commun (1996) 225(3):1035-9. doi:10.1006/bbrc. 1996.1290
42. Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, Bossi G, et al. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature (2002) 416(6879):451-5. doi:10.1038/416451a
43. Hoeller D, Crosetto N,BlagoevB,RaiborgC,TikkanenR,Wagner S,et al. Regulation of ubiquitin-binding proteins by monoubiquitination. Nat Cell Biol (2006) 8(2):163-9. doi:10.1038/ncbl354
44. Kim BY, Olzmann JA, Barsh GS, Chin LS, Li L. Spongiform neurodegenerationassociated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol Biol Cell (2007) 18(4):1129-42. doi:10.1091/mbc.E06-09-0787
45. Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C, Sanchez-Madrid F, Mittelbrunn M. Sorting it out: regulation of exosome loading. Semin Cancer Biol (2014). doi:10.1016/j.semcancer.2014.04.009
46. Putz U, Howitt J, Lackovic J, Foot N, Kumar S, Silke J, et al. Nedd4 familyinteracting protein 1 (Ndfipl) is required for the exosomal secretion of Nedd4 family proteins. / Biol Chem (2008) 283(47):32621-7. doi:10.1074/jbc. M804120200
47. Gauvreau ME, Cote MH, Bourgeois-Daigneault MC, Rivard LD, Xiu F, Brunet A, et al. Sorting of MHC class II molecules into exosomes through a ubiquitinindependent pathway. Traffic (2009) 10(10):1518-27. doi:10.1111/j. 1600-0854. 2009.00948.x
48. Buschow SI, Nolte-'t Hoen EN, van Niel G, Pols MS, ten Broeke T, Lauwen M, et al. MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic (2009) 10(10):1528-42. doi:10.1111/J.1600-0854.2009.00963.X
49. Lee HS, Jeong J, Lee KJ. Characterization of vesicles secreted from insulinoma NIT-1 cells. JProteomeRes (2009) 8(6):2851-62. doi:10.1021/pr900009y
50. Buschow SI, Liefhebber JM,Wubbolts R, Stoorvogel W. Exosomes contain ubiquitinated proteins. Blood Cells Mol Dis (2005) 35(3):398-403. doi:10.1016/j. bcmd.2005.08.005
51. Rapoport EM, Kurmyshkina OV, Bovin NV. Mammalian galectins: structure, carbohydrate specificity, and functions. Biochemistry (Mosc) (2008) 73(4):393-405. doi:10.1134/S0006297908040032
52. Delacour D, Gouyer V, Zanetta JP, Drobecq H, Leteurtre E, Grard G, et al. Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. JCellBiol (2005) 169(3):491-501. doi:10.1083/jcb.200407073
53. Delacour D, Cramm-Behrens CI, Drobecq H, Le Bivic A, Nairn HY, Jacob R. Requirement for galectin-3 in apical protein sorting. Curr Biol (2006) 16(4):408-14.doi:10.1016/j.cub.2005.12.046
54. Delacour D, Greb C, Koch A, Salomonsson E, Leffler H, Le Bivic A, et al. Apical sorting by galectin-3-dependent glycoprotein clustering. Traffic (2007) 8(4):379-88. doi:10.1111/J.1600-0854.2007.00539.X
55. Mishra R, Grzybek M, Niki T, Hirashima M, Simons K. Galectin-9 trafficking regulates apical-basal polarity in Madin-Darby canine kidney epithelial cells. ProcNatlAcadSci USA (2010) 107(41):17633-8. doi:10.1073/pnas.l012424107
56. Fang Y, Wu N, Gan X, Yan W, Morrell JC, Gould SJ. Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol (2007) 5(6):el58. doi:10.1371/joumal.pbio.0050158