The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 11649-11661

  Perez Hernandez, Daniel ^a,b   Gutiérrez Vázquez, Cristina ^b   Jorge, Inmaculada ^b   López Martín, Soraya ^c   Ursa, Angeles ^d   Sánchez Madrid, Francisco ^b,d   Vázquez, Jesús ^a,b   Yañez Mó, María ^c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^c HOSPITAL UNIVERSITARIO SANTA CRISTINA   (Spain)

^d Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASMIC REGIONS; HIGH THROUGHPUT; INTERACTION NETWORKS; INTERCELLULAR COMMUNICATIONS; POTENT MECHANISM; PROTEIN MARKERS; QUANTITATIVE PROTEOMICS; SORTING MACHINERY;

ENZYME ACTIVITY; LIGANDS; MACHINERY; MASS SPECTROMETRY; MOLECULAR BIOLOGY; MOLECULES;

PROTEINS;

CD81 ANTIGEN; RAC PROTEIN; TETRASPANIN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; EXOSOME; HUMAN; HUMAN CELL; LYMPHOBLAST; MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEOMICS;

ANIMALS; ANTIGENS, CD81; CELL LINE; EXOSOMES; HUMANS; LYMPHOCYTES; MICE; MICE, KNOCKOUT; PROTEIN STRUCTURE, TERTIARY; PROTEOME; RAC GTP-BINDING PROTEINS;

ANIMALIA;

EID: 84876915447     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.445304     Document Type: Article

References (59)

1. Yáñez-Mó, M., Barreiro, O., Gordon-Alonso, M., Sala-Valdés, M., and Sánchez-Madrid, F. (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol. 19, 434-446
2. Charrin, S., le Naour, F., Silvie, O., Milhiet, P. E., Boucheix, C., and Rubinstein, E. (2009) Lateral organization of membrane proteins: tetraspanins spin their web. Biochem. J. 420, 133-154
3. Yáñez-Mó, M., Gutiérrez-López, M. D., and Cabañas, C. (2011) Functional interplay between tetraspanins and proteases. Cell. Mol. Life Sci. 68, 3323-3335
4. Berditchevski, F., and Odintsova, E. (2007) Tetraspanins as regulators of protein trafficking. Traffic 8, 89-96
5. Mittelbrunn, M., and Sánchez-Madrid, F. (2012) Intercellular communication: diverse structures for exchange of genetic information. Nat. Rev. Mol. Cell Biol. 13, 328-335
6. Théry, C., Ostrowski, M., and Segura, E. (2009) Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581-593
7. Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., and Lötvall, J. O. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659
8. Skog, J., Würdinger, T., van Rijn, S., Meijer, D. H., Gainche, L., Sena-Esteves, M., Curry, W. T., Jr., Carter, B. S., Krichevsky, A. M., and Breakefield, X. O. (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470-1476
9. Balaj, L., Lessard, R., Dai, L., Cho, Y. J., Pomeroy, S. L., Breakefield, X. O., and Skog, J. (2011) Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun. 2, 180
10. Pegtel, D. M., Cosmopoulos, K., Thorley-Lawson, D. A., van Eijndhoven, M. A., Hopmans, E. S., Lindenberg, J. L., de Gruijl, T. D., Würdinger, T., and Middeldorp, J. M. (2010) Functional delivery of viral miRNAs via exosomes. Proc. Natl. Acad. Sci. U. S. A. 107, 6328-6333
11. Mittelbrunn, M., Gutiérrez-Vázquez, C., Villarroya-Beltri, C., González, S., Sánchez-Cabo, F., González, M. Á., Bernad, A., and Sánchez-Madrid, F. (2011) Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat. Commun. 2, 282
12. Nazarenko, I., Rana, S., Baumann, A., McAlear, J., Hellwig, A., Trendelenburg, M., Lochnit, G., Preissner, K. T., and Zöller, M. (2010) Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res. 70, 1668-1678
13. Chairoungdua, A., Smith, D. L., Pochard, P., Hull, M., and Caplan, M. J. (2010) Exosome release of β-catenin: a novel mechanism that antagonizes Wnt signaling. J. Cell Biol. 190, 1079-1091
14. Le Naour, F., Andre, M., Boucheix, C., and Rubinstein, E. (2006) Membrane microdomains and proteomics: lessons from tetraspanin microdomains and comparison with lipid rafts. Proteomics 6, 6447-6454
15. Sala-Valdes, M., Ursa, A., Charrin, S., Rubinstein, E., Hemler, M. E., Sanchez-Madrid, F., and Yañez-Mó, M. (2006) EWI-2 and EWI-F link the tetraspanin web to the actin cytoskeleton through their direct association with ezrin-radixin-moesin proteins. J. Biol. Chem. 281, 19665-19675
16. Latysheva, N., Muratov, G., Rajesh, S., Padgett, M., Hotchin, N. A., Overduin, M., and Berditchevski, F. (2006) Syntenin-1 is a new component of tetraspanin-enriched microdomains: mechanisms and consequences of the interaction of syntenin-1 with CD63. Mol. Cell. Biol. 26, 7707-7718
17. Liu, L., He, B., Liu, W. M., Zhou, D., Cox, J. V., and Zhang, X. A. (2007) Tetraspanin CD151 promotes cell migration by regulating integrin trafficking. J. Biol. Chem. 282, 31631-31642
18. Stipp, C. S., Kolesnikova, T. V., and Hemler, M. E. (2003) Functional domains in tetraspanin proteins. Trends Biochem. Sci. 28, 106-112
19. Berditchevski, F., Tolias, K. F., Wong, K., Carpenter, C. L., and Hemler, M. E. (1997) A novel link between integrins, transmembrane-4 superfamily proteins (CD63 and CD81), and phosphatidylinositol 4-kinase. J. Biol. Chem. 272, 2595-2598
20. Zhang, X. A., Bontrager, A. L., and Hemler, M. E. (2001) Transmembrane-4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific ft integrins. J. Biol. Chem. 276, 25005-25013
21. Clark, K. L., Oelke, A., Johnson, M. E., Eilert, K. D., Simpson, P. C., and Todd, S. C. (2004) CD81 associates with 14-3-3 in a redox-regulated palmitoylation-dependent manner. J. Biol. Chem. 279, 19401-19406
22. Bonzon-Kulichenko, E., Perez-Hernandez, D., Nuñez, E., Martínez-Acedo, P., Navarro, P., Trevisan-Herraz, M., Ramos Mdel, C., Sierra, S., Martínez-Martínez, S., Ruiz-Meana, M., Miro-Casas, E., García-Dorado, D., Redondo, J. M., Burgos, J. S., and Vazquez, J. (2011) A robust method for quantitative high-throughput analysis of proteomes by 18O labeling. Mol. Cell. Proteomics 10, M110.003335
23. Lopez-Ferrer, D., Martínez-Bartolome, S., Villar, M., Campillos, M., Martín-Maroto, F., and Vazquez, J. (2004) Statistical model for large-scale peptide identification in databases from tandem mass spectra using SEQUEST. Anal. Chem. 76, 6853-6860
24. Jorge, I., Casas, E. M., Villar, M., Ortega-Perez, I., Lopez-Ferrer, D., Martínez-Ruiz, A., Carrera, M., Marina, A., Martínez, P., Serrano, H., Canas, B., Were, F., Gallardo, J. M., Lamas, S., Redondo, J. M., García-Dorado, D., and Vazquez, J. (2007) High-sensitivity analysis of specific peptides in complex samples by selected MS/MS ion monitoring and linear ion trap mass spectrometry: application to biological studies. J. Mass Spectrom. 42, 1391-1403
25. Martínez-Bartolome, S., Navarro, P., Martín-Maroto, F., Lopez-Ferrer, D., Ramos-Fernandez, A., Villar, M., García-Ruiz, J. P., and Vazquez, J. (2008) Properties of average score distributions of SEQUEST: the probability ratio method. Mol. Cell. Proteomics 7, 1135-1145
26. Navarro, P., and Vazquez, J. (2009) A refined method to calculate false discovery rates for peptide identification using decoy databases. J. ProteomeRes. 8, 1792-1796
27. Ramos-Fernandez, A., Lopez-Ferrer, D., and Vazquez, J. (2007) Improved method for differential expression proteomics using trypsin-catalyzed 18O labeling with a correction for labeling efficiency. Mol. Cell. Proteomics 6, 1274-1286
28. Jorge, I., Navarro, P., Martínez-Acedo, P., Nuñez, E., Serrano, H., Alfranca, A., Redondo, J. M., and Vazquez, J. (2009) Statistical model to analyze quantitative proteomics data obtained by 18O/16O labeling and linear ion trap mass spectrometry: application to the study of vascular endothelial growth factor-induced angiogenesis in endothelial cells. Mol. Cell. Proteomics 8, 1130-1149
29. Barreiro, O., Yañez-Mó, M., Sala-Valdes, M., Gutierrez-Lopez, M. D., Ovalle, S., Higginbottom, A., Monk, P. N., Cabanas, C., and Sanchez-Madrid, F. (2005) Endothelial tetraspanin microdomains regulate leukocyte firm adhesion during extravasation. Blood 105, 2852-2861
30. Charrin, S., Le Naour, F., Labas, V., Billard, M., Le Caer, J. P., Emile, J. F., Petit, M. A., Boucheix, C., and Rubinstein, E. (2003) EWI-2 is a new component of the tetraspanin web in hepatocytes and lymphoid cells. Biochem. J. 373, 409-421
31. Stipp, C. S., Kolesnikova, T. V., and Hemler, M. E. (2001) EWI-2 is a major CD9 and CD81 partner and member of a novel Ig protein subfamily. J. Biol. Chem. 276, 40545-40554
32. Chicurel, M. E., Singer, R. H., Meyer, C. J., and Ingber, D. E. (1998) Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature 392, 730-733
33. de Hoog, C. L., Foster, L. J., and Mann, M. (2004) RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell 117, 649-662
34. Zoller, M. (2009) Tetraspanins: push and pull in suppressing and promoting metastasis. Nat. Rev. Cancer 9, 40-55
35. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J., and Mann, M. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 4, 1265-1272
36. Maecker, H. T., and Levy, S. (1997) Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J. Exp. Med. 185, 1505-1510
37. Tsitsikov, E. N., Gutierrez-Ramos, J. C., and Geha, R. S. (1997) Impaired CD19 expression and signaling, enhanced antibody response to type II T independent antigen, and reduction of B-1 cells in CD81-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 94, 10844-10849
38. Miyazaki, T., Müller, U., and Campbell, K. S. (1997) Normal development but differentially altered proliferative responses of lymphocytes in mice lacking CD81. EMBOJ. 16, 4217-4225
39. Barreiro, O., Yanez-Mo, M., Serrador, J. M., Montoya, M. C, Vicente-Manzanares, M., Tejedor, R., Furthmayr, H., and Sanchez-Madrid, F. (2002) Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J. Cell Biol. 157, 1233-1245
40. Serrador, J. M., Alonso-Lebrero, J. L., del Pozo, M. A., Furthmayr, H., Schwartz-Albiez, R., Calvo, J., Lozano, F., and Sanchez-Madrid, F. (1997) Moesin interacts with the cytoplasmic region of intercellular adhesion molecule-3 and is redistributed to the uropod of T lymphocytes during cell polarization. J. Cell Biol. 138, 1409-1423
41. Kanters, E., van Rijssel, J., Hensbergen, P. J., Hondius, D., Mul, F. P., Deelder, A. M., Sonnenberg, A., van Buul, J. D., and Hordijk, P. L. (2008) Filamin B mediates ICAM-1-driven leukocyte transendothelial migration. J. Biol. Chem. 283, 31830-31839
42. Carpen, O., Pallai, P., Staunton, D. E., and Springer, T. A. (1992) Association of intercellular adhesion molecule-1 (ICAM-1) with actin-containing cytoskeleton and α-actinin. J. Cell Biol. 118, 1223-1234
43. Mazzocca, A., Liotta, F., and Carloni, V. (2008) Tetraspanin CD81-regulated cell motility plays a critical role in intrahepatic metastasis of hepatocellular carcinoma. Gastroenterology 135, 244-256
44. Gordon-Alonso, M., Sala-Valdes, M., Rocha-Perugini, V., Perez-Hernandez, D., Lopez-Martín, S., Ursa, A., Alvarez, S., Kolesnikova, T. V., Vazquez, J., Sanchez-Madrid, F., and Yañez-Mó, M. (2012) EWI-2 association with α-actinin regulates T cell immune synapses and HIV viral infection. J. Immunol. 189, 689-700
45. Tejera, E., Rocha-Perugini, V., Lopez-Martín, S., Perez-Hernandez, D., Bachir, A. I., Horwitz, A. R., Vazquez, J., Sanchez-Madrid, F., and Yañez-Mo, M. (2013) CD81 regulates cell migration through its association with Rac GTPase. Mol. Biol. Cell 24, 261-273
46. Bassell, G. J., Powers, C. M., Taneja, K. L., and Singer, R. H. (1994) Single mRNAs visualized by ultrastructural in situ hybridization are principally localized at actin filament intersections in fibroblasts. J. Cell Biol. 126, 863-876
47. Gorrini, C., Loreni, F., Gandin, V., Sala, L. A., Sonenberg, N., Marchisio, P. C., and Biffo, S. (2005) Fibronectin controls cap-dependent translation through β1 integrin and eukaryotic initiation factors 4 and 2 coordinated pathways. Proc. Natl. Acad. Sci. U. S. A. 102, 9200-9205
48. Sanvito, F., Piatti, S., Villa, A., Bossi, M., Lucchini, G., Marchisio, P. C., and Biffo, S. (1999) The β4 integrin interactor p27BBP/eIF6 is an essential nuclear matrix protein involved in 60S ribosomal subunit assembly. J. Cell Biol. 144, 823-837
49. Schiller, H. B., Friedel, C. C., Boulegue, C., and Fassler, R. (2011) Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep. 12, 259-266
50. Humphries, J. D., Byron, A., Bass, M. D., Craig, S. E., Pinney, J. W., Knight, D., and Humphries, M. J. (2009) Proteomic analysis of integrin-associated complexes identifies RCC2 as a dual regulator of Rac1 and Arf6. Sci. Signal. 2, ra51
51. Simons, M., and Raposo, G. (2009) Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581
52. Escola, J. M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O., and Geuze, H. J. (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273, 20121-20127
53. Thery, C., Boussac, M., Veron, P., Ricciardi-Castagnoli, P., Raposo, G., Garin, J., and Amigorena, S. (2001) Proteomic analysis of dendritic cellderived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 166, 7309-7318
54. van Niel, G., Charrin, S., Simoes, S., Romao, M., Rochin, L., Saftig, P., Marks, M. S., Rubinstein, E., and Raposo, G. (2011) The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev. Cell 21, 708-721
55. Baietti, M. F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E., Zimmermann, P., and David, G. (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 14, 677-685
56. Abache, T., Le Naour, F., Planchon, S., Harper, F., Boucheix, C., and Rubinstein, E. (2007) The transferrin receptor and the tetraspanin web molecules CD9, CD81, and CD9P-1 are differentially sorted into exosomes after TPA treatment of K562 cells. J. Cell. Biochem. 102, 650-664
57. Miyado, K., Yoshida, K., Yamagata, K., Sakakibara, K., Okabe, M., Wang, X., Miyamoto, K., Akutsu, H., Kondo, T., Takahashi, Y., Ban, T., Ito, C., Toshimori, K., Nakamura, A., Ito, M., Miyado, M., Mekada, E., and Umezawa, A. (2008) The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc. Natl. Acad. Sci. U. S. A. 105, 12921-12926
58. Rubinstein, E., Ziyyat, A., Prenant, M., Wrobel, E., Wolf, J. P., Levy, S., Le Naour, F., and Boucheix, C. (2006) Reduced fertility of female mice lacking CD81. Dev. Biol. 290, 351-358
59. Kalra, H., Simpson, R. J., Ji, H., Aikawa, E., Altevogt, P., Askenase, P., Bond, V C, Borras, F. E., Breakefield, X., Budnik, V., etal. (2012) Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 10, e1001450