The functional importance of tetraspanins in exosomes

Emerging Concepts of Tumor Exosome-Mediated Cell-Cell Communication

Volumn , Issue , 2013, Pages 69-91

  Rana, Sanyukta ^a,b   Zoller, Margot ^b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84948701453     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-3697-3_4     Document Type: Chapter

References (300)

1. Abache T, Le Naour F, Planchon S, Harper F, Boucheix C, 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
2. Admyre C, Bohle B, Johansson SM, Focke-Tejkl M, Valenta R, Scheynius A, Gabrielsson S (2007) B cell-derived exosomes can present allergen peptides and activate allergen-specific T cells to proliferate and produce TH2-like cytokines. J Allergy Clin Immunol 120:1418-1424
3. Admyre C, Johansson SM, Paulie S et al (2006) Direct exosome stimulation of peripheral human T cells detected by ELISPOT. Eur J Immunol 36:1772-1781
4. Albini A, Mirisola V, Pfeffer U (2008) Metastasis signatures: genes regulating tumor- microenvironment interactions predict metastatic behavior. Cancer Metastasis Rev 27:75-83
5. André F, Schartz NE, Chaput N, Flament C, Raposo G, Amigorena S, Angevin E, Zitvogel L (2002) Tumor-derived exosomes: a new source of tumor rejection antigens. Vaccine 20(Suppl 4):A28-A31
6. André M, Le Caer JP, Greco C et al (2006) Proteomic analysis of the tetraspanin web using LC ESI MS/MS and MALDI FTICR MS. Proteomics 6:1437-1449
7. Ardôn-Alonso M, Yahez-Mô M, Barreiro O, Alvarez S, Muhoz-Fernandez MA, Valenzuela- Fernândez A, Sanchez-Madrid F (2006) Tetraspanins CD9 and CD81 modulate HIV-1-induced membrane fusion. J Immunol 177:5129-5137
8. Arduise C, Abache T, Li L, Billard M, Chabanon A, Ludwig A, Mauduit P, Boucheix C, Rubinstein E, Le Naour F (2008) Tetraspanins regulate ADAM10-mediated cleavage of TNF- alpha and epidermal growth factor. J Immunol 181:7002-7013
9. Artavanis-Tsakonas K, Kasperkovitz PV, Papa E, Cardenas ML, Khan NS, Van Der Veen AG, Ploegh HL, Vyas JM (2011) The tetraspanin CD82 is specifically recruited to fungal and bacterial phagosomes prior to acidification. Infect Immun 79:1098-1106
10. Atay S, Gercel-Taylor C, Taylor DD (2011) Human trophoblast-derived exosomal fi- bronectin induces pro-inflammatory Il-1 P production by macrophages. Am J Reprod Immunol 66:259-69
11. Barreiro O, Yâüez-Mô M, Sala-Valdés M, Gutiérrez-Lôpez MD, Ovalle S, Higginbottom A, Monk PN, Caban as C, Sânchez-Madrid F (2005) Endothelial tetraspanin microdomains regulate leukocyte firm adhesion during extravasation. Blood 105:2852-2861
12. Bartee E, Eyster CA, Viswanathan K, Mansouri M, Donaldson JG, Früh K (2010) Membrane- associated RING-CH proteins associate with Bap31 and target CD81 and CD44 to lysosomes. PLoS ONE 5:e15132
13. Bass R, Werner F, Odintsova E, Sugiura T, Berditchevski F, Ellis V (2005) Regulation of urokinase receptor proteolytic function by the tetraspanin CD82. J Biol Chem 280:1481114818
14. Bauer M, Pelkmans L (2006) A new paradigm for membrane-organizing and -shaping scaffolds. FEBS Lett 580:5559-64
15. Berckmans RJ, Neiuwland R, Boing AN, Romijn FP, Hack CE, Sturk A (2001) Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost 85:639-646
16. Berditchevski F (2001) Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci 114:4143-4151
17. Berditchevski F, Odintsova E (2007) Tetraspanins as regulators of protein trafficking. Traffic 8:89-96
18. Berditchevski F, Tolias KF, Wong K, Carpenter CL, Hemler ME (1997) A novel link between integrins, transmembrane-4 superfamily proteins (CD63 and CD81), and phosphatidylinositol 4-kinase. J Biol Chem 272:2595-2598
19. Berditchevski F, Odintsova E, Sawada S, Gilbert E (2002) Expression of the palmitoylation- deficient CD151 weakens the association of alpha 3 beta 1 integrin with the tetraspanin- enriched microdomains and affects integrin-dependent signaling. J Biol Chem 277:3699137000
20. Berthier Vergnes O, Kharbili ME, de la Fouchardière A, Pointecouteau T, Verrando P, Wierinckx A, Lachuer J, Le Naour F, Lamartine J (2011) Gene expression profiles of human melanoma cells with different invasive potential reveal TSPAN8 as a novel mediator of invasion. Br J Cancer 104:155-165
21. Bidard FC, Pierga JY, Vincent-Salomon A, Poupon MF (2008) A “class action” against the microenvironment: do cancer cells cooperate in metastasis? Cancer Metastasis Rev 27:5-10
22. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T (2005) Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer 5:744-749
23. Bradbury LE, Kansas GS, Levy S, Evans RL, Tedder TF (1992) The CD19/CD21 signal transducing complex of human B lymphocytes includes the target of antiproliferative antibody-1 and Leu-13 molecules. J Immunol 149:2841-2850
24. Brisson C, Azorsa DO, Jennings LK, Moog S, Cazenave JP, Lanza F (1997) Co-localization of CD9 and GPIIb-IIIa (alpha Ilb beta 3 integrin) on activated platelet pseudopods and alphagranule membranes. Histochemistry J 29:153-165
25. Burghoff S, Ding Z, Godecke S, Assmann A, Wirrwar A, Buchholz D, Sergeeva O, Leurs C, Hanenberg H, Müller HW, Bloch W, Schrader J (2008) Horizontal gene transfer from human endothelial cells to rat cardiomyocytes after intracoronary transplantation. Cardiovasc Res 77:534-543
26. Bussolati B, Grange C, Camussi G (2011) Tumor exploits alternative strategies to achieve vascularization. FASEB J 25:2874-82
27. Carlini MJ, De Lorenzo MS, Puricelli L (2011) Cross-talk between Tumor Cells and the Microenvironment at the Metastatic Niche. Curr Pharm Biotechnol Apr 6. (Epub ahead of print)
28. Caswell P, Norman J (2008) Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol 18:257-263
29. Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ (2010) Exosome release of P-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol 190:1079-91
30. Charrin S, Le Naour F, Oualid M, Billard M, Faure G, Hanash SM, Boucheix C, Rubinstein E (2001) The major CD9 and CD81 molecular partner. Identification and characterization of the complexes. J Biol Chem 276:14329-14337
31. Charrin S, Manié S, Oualid M, Billard M, Boucheix C, Rubinstein E (2002) Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation. FEBS Lett 516:139144
32. Charrin S, Manié S, Thiele C, Billard M, Gerlier D, Boucheix C, Rubinstein E (2003) A physical and functional link between cholesterol and tetraspanins. Eur J Immunol 33:24792489
33. Cherukuri A, Shoham T, Sohn HW, Levy S, Brooks S, Carter R, Pierce SK (2004) The tetraspanin CD81 is necessary for partitioning of coligated CD19/CD21-B cell antigen receptor complexes into signaling-active lipid rafts. J Immunol 172:370-380
34. Claas C, Seiter S, Claas A, Savelyeva L, Schwab M, Zoller M (1998) Association between the rat homologue of CO-029, a metastasis-associated tetraspanin molecule and consumption coagulopathy. J Cell Biol 141:267-280
35. Claas C, Stipp CS, Hemler ME (2001) Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts. J Biol Chem 276:7974-7984
36. Claas C, Wahl J, Orlicky DJ, Karaduman H, Schnolzer M, Kempf T, Zoller M (2005) The tetraspanin D6.1A and its molecular partners on rat carcinoma cells. Biochem J 389:99-110
37. Classen A, Lloberas J, Celada A (2009) Macrophage activation: classical versus alternative. Methods Mol Biol 531:29-43
38. De Cicco M (2004) The prothrombotic state in cancer: pathogenic mechanisms. Crit Rev Oncol Hematol 50:187-196
39. de Parseval A, Lerner DL, Borrow P, Willett BJ, Elder JH (1997) Blocking of feline immunodeficiency virus infection by a monoclonal antibody to CD9 is via inhibition of virus release rather than interference with receptor binding. J Virol 71:5742-5749
40. Delaguillaumie A, Lagaudrière-Gesbert C, Popoff MR, Conjeaud H (2002) Rho GTPases link cytoskeletal rearrangements and activation processes induced via the tetraspanin CD82 in T lymphocytes. J Cell Sci 115:433-443
41. Delcayre A, Shu H, Le Pecq JB (2005) Dendritic cell-derived exosomes in cancer immunotherapy: exploiting nature’s antigen delivery pathway. Expert Rev Anticancer Ther 5:537-547
42. Deneka M, Pelchen-Matthews A, Byland R, Ruiz-Mateos E, Marsh M (2007) In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J Cell Biol 177:329-341
43. Deng J, Yeung VP, Tsitoura D, DeKruyff RH, Umetsu DT, Levy S (2000) Allergen-induced airway hyperreactivity is diminished in CD81-deficient mice. J Immunol 165:5054-5061
44. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvodel W, Geuze HJ (2000) Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113:3365-3374
45. Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, Biancone L, Bruno S, Bussolati B, Camussi G (2007) Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110:24402448
46. Desai M, Mirzay Razzaz J, von Delft D, Sarkar S, Hamilton G, Seifalian AM (2010) Inhibition of neointimal formation and hyperplasia in vein grafts by external stent/sheath. Vasc Med 15:287-297
47. Dong LM, Potter JD, White E, Ulrich CM, Cardon LR, Peters U (2008) Genetic susceptibility to cancer: the role of polymorphisms in candidate genes. JAMA 299:2423-2436
48. Drummer HE, Boo I, Maerz AL, Poumbourios P (2006) A conserved Gly436-Trp-Leu-Ala- Gly-Leu-Phe-Tyr motif in hepatitis C virus glycoprotein E2 is a determinant of CD81 binding and viral entry. J Virol 80:7844-7853
49. Dumartin L, Quemener C, Laklai H Dumartin L, Quemener C, Laklai H (2010) Netiin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells. Gastroenterology 138:1595-1606
50. Engering A, Pieters J (2001) Association of distinct tetraspanins with MHC class II molecules at different subcellular locations in human immature dendritic cells. Int Immunol 13:127-134
51. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ (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
52. Escrevente C, Keller S, Altevogt P, Costa J (2011) Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 11:108
53. Espenel C, Margeat E, Dosset P, Arduise C, Le Grimellec C, Royer CA, Boucheix C, Rubinstein E, Milhiet PE (2008) Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web. J Cell Biol 182:765-776
54. Evergren E, Gad H, Walther K, Sundborger A, Tomilin N, Shupliakov O (2007) Intersectin is a negative regulator of dynamin recruitment to the synaptic endocytic zone in the central synapse. J Neurosci 27:379-390
55. Fanaei M, Monk PN, Partridge LJ (2011) The role of tetraspanins in fusion. Biochem Soc Trans 39:524-528
56. Fang Y, Wu N, Gan X Yan W, Morrell JC, Gould SJ (2007) Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol 5:e158
57. Farquhar MJ, Harris HJ, McKeating JA (2011) Hepatitis C virus entry and the tetraspanin CD81. Biochem Soc Trans 39:532-536
58. Fevrier B, Raposo G (2004) Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 16:415-421
59. Figdor CG, van Spriel AB (2010) Fungal pattern-recognition receptors and tetraspanins: partners on antigen-presenting cells. Trends Immunol 31:91-96
60. Fitter S, Tetaz T, Berndt MC, Ashman LK (1995) Molecular cloning of cDNA encoding a novel platelet, endothelial tetraspan antigen, PETA-3. Blood 86:1348-1355
61. Flaumenhaft R (2006) Formation and fate of platelet microparticles. Blood Cells Mol Dis 36:182-187
62. Folkman J (2004) Endogenous angiogenesis inhibitors. APMIS 112:496-507
63. Fomina AF, Deerinck TJ, Ellisman MH (2003) Regulation of membrane trafficking and subcellular organization of endocytic compartments revealed with FM1-43 in resting and activated human T cells. Exp Ceil Res 291:150-166
64. Forman JD, Klein JT, Silver RF, Liu MC, Greenlee BM, Moller DR (1994) Selective activation and accumulation of oligoclonal V beta-specific T cells in active pulmonary sarcoidosis. J Clin Invest 94:1533-1542
65. Franchini M, Montagnana M, Targher G, Lippi G (2007) Reduced von Willebrand factorcleaving protease levels in secondary thrombotic microangiopathies and other diseases. J Thromb Thrombolysis 24:29-38
66. Gambim MH, do Carmo Ade O, Marti L, Verissimo-Filho S, Lopes LR, Janiszewski M (2007) Platelet-derived exosomes induce endothelial cell apoptosis through peroxynitrite generation: experimental evidence for a novel mechanism of septic vascular dysfunction. Crit Care 11:R107
67. Garcia E, Nikolic DS, Piguet V (2008) HIV-1 replication in dendritic cells occurs through a tetraspanin-containing compartment enriched in AP-3. Traffic 9:200-214
68. Garcia-Espaba A, Chung PJ, Sarkar IN, Stiner E, Sun TT, Desalle R (2008) Appearance of new tetraspanin genes during vertebrate evolution. Genomics 91:326-334
69. Gartlan KH, Belz GT, Tarrant JM, Minigo G, Katsara M, Sheng KC, Sofi M, van Spriel AB, Apostolopoulos V, Plebanski M, Robb L, Wright MD (2010) A complementary role for the tetraspanins CD37 and Tssc6 in cellular immunity. J Immunol 185:3158-3166
70. Geiger TR, Peeper DS (2009) Metastasis mechanisms. Biochim Biophys Acta 1796:293-308
71. Gesierich S, Paret C, Hildebrand D, Weitz J, Zgraggen K, Schmitz-Winnenthal FH, Horejsi V, Yoshie O, Herlyn D, Ashman LK, Zoller M. (2005) Colocalization of the tetraspanins, CO- 029 and CD151, with integrins in human pancreatic adenocarcinoma: impact on cell motility. Clin Cancer Res 11:2840-2852
72. Gesierich S, Berezovskiy I, Ryschich E, Zoller M (2006) Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029. Cancer Res 66:7083-7094
73. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11:1143-1149
74. Gordon-Alonso M, Yanez-Mo M, Barreiro O, Alvarez S, Muiioz-Fernandez MA, Valenzuela- Fernandez A, Sanchez-Madrid F (2006) Tetraspanins CD9 and CD81 modulate HIV-1-induced membrane fusion. J Immunol 177:5129-5137
75. Goschnick MW, Lau LM, Wee JL, Liu YS, Hogarth PM, Robb LM, Hickey MJ, Wright MD, Jackson DE (2006) Impaired “outside-in” integrin alphaIIbbeta3 signaling and thrombus stability in TSSC6-deficient mice. Blood 108:1911-1918
76. Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, Tetta C, Bussolati B, Camussi G (2011) Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 71:5346-556
77. Griffith L, Slupsky J, Seehafer J, Boshkov L, Shaw AR (1991) Platelet activation by immobilized monoclonal antibody: evidence for a CD9 proximal signal. Blood 78:1753-1759
78. Grigorov B, Attuil-Audenis V, Perugi F, Nedelec M, Watson S, Pique C, Darlix JL, Conjeaud H, Muriaux D (2009) A role for CD81 on the late steps of HIV-1 replication in a chronically infected T cell line. Retrovirology 6:28
79. Gruenberg J, Stenmark H (2004) The biogenesis of multivesicular endosomes. Nat Rev Mol Cell Biol 5:317-323
80. Guo J, Wenk MR, Pellegrini L, Onofri F, Benfenati F, De Camilli P (2003) Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc Natl Acad Sci U S A 100:3995-4000
81. Hakomori SI (2010). Glycosynaptic microdomains controlling tumor cell phenotype through alteration of cell growth, adhesion, and motility. FEBS Lett 584:1901-1906
82. Hakulinen J, Sankkila L, Sugiyama N, Lehti K, Keski-Oja J (2008) Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes. J Cell Biochem 105:1211-1218
83. Hamamoto K, Ohga S, Nomura S, Yasunaga K (1994) Cellular distribution of CD63 antigen in platelets and in three megakaryocytic cell lines. Histochem J 26:367-375
84. Hasegawa M, Furuya M, Kasuya Y, Nishiyama M, Sugiura T, Nikaido T, Momota Y, Ichinose M, Kimura S (2007) CD151 dynamics in carcinoma-stroma interaction: integrin expression, adhesion strength and proteolytic activity. Lab Invest 87:882-892
85. Hashimoto A, Tarner IH, Bohle RM, Gaumann A, Manetti M, Distler O, Steinmeyer J, Ulfgren AK, Schulz A, Gay S, Muller-Ladner U, Neumann E (2007) Analysis of vascular gene expression in arthritic synovium by laser-mediated microdissection. Arthritis Rheum 56:1094-1105
86. Hassuna N, Monk PN, Moseley GW, Partridge LJ (2009) Strategies for targeting tetraspanin proteins: potential therapeutic applications in microbial infections. BioDrugs 23:341-359
87. Hasuwa H, Shishido Y, Yamazaki A, Kobayashi T, Yu X, Mekada E (2001) CD9 amino acids critical for upregulation of diphtheria toxin binding. Biochem Biophys Res Commun 289:782-790
88. He B, Liu L, Cook GA, Grgurevich S, Jennings LK, Zhang XA. (2005) Tetraspanin CD82 attenuates cellular morphogenesis through down-regulating integrin alpha6-mediated cell adhesion. J Biol Chem 280:3346-3354
89. Helle F, Dubuisson J (2008) Hepatitis C virus entry into host cells. Cell Mol Life Sci 65:100112
90. Hemler ME (2001) Specific tetraspanin functions. J Cell Biol 155:1103-1107
91. Hemler ME (2003) Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol 19:397422
92. Hemler ME (2005) Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 6:801-811
93. Hendrix A, Westbroek W, Bracke M, DeWever O (2010) An ex(o)citing machinery for invasive tumor growth. Cancer Res 70:9533-9537
94. Herlevsen M, Schmidt DS, Miyazaki K, Zoller M (2003) The association of the tetraspanin D6.1 A with the alpha6beta4 integrin supports cell motility and liver metastasis formation. J Cell Sci 116:4373-4390
95. Herrera MB, Fonsato V, Gatti S, Deregibus MC, Sordi A, Cantarella D, Calogero R, Bussolati B, Tetta C, Camussi G (2010) Human liver stem cell-derived microvesicles accelerate hepatic regeneration in hepatectomized rats. J Cell Mol Med 14:1605-1618
96. Hickey MM, Simon MC (2006) Regulation of angiogenesis by hypoxia and hypoxia-inducible factors. Curr Top Dev Biol 76:217-257
97. Hillen F, Griffioen AW (2007) Tumour vascularization: sprouting angiogenesis and beyond. Metastasis Rev 26:489-502
98. Ho SH, Martin F, Higginbottom A, Partridge LJ, Parthasarathy V, Moseley GW, Lopez P, Cheng-Mayer C, Monk PN (2006) Recombinant extracellular domains of tetraspanin proteins are potent inhibitors of the infection of macrophages by human immunodeficiency virus type 1. J Virol 80:6487-6496
99. Holderfield MT, Hughes CC (2008) Crosstalk between vascular endothelial growth factor, notch, and transforming growth factor-beta in vascular morphogenesis. CircRes 102:637-652
100. Hong IK, Jin YJ, Byun HJ, Jeoung DI, Kim YM, Lee H (2006) Homophilic interactions of Tetraspanin CD151 up-regulate motility and matrix metalloproteinase-9 expression of human melanoma cells through adhesion-dependent c-Jun activation signaling pathways. J Biol Chem 281:24279-24292
101. Hood JL, San Roman S, Wickline SA (2011) Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 71:3792-801
102. Horváth G, Serru V, Clay D, Billard M, Boucheix C, Rubinstein E (1998) CD19 is linked to the integrin-associated tetraspans CD9, CD81, and CD82. J Biol Chem 273:30537-30543
103. Huerta S, Harris DM, Jazirehi A, Bonavida B, Elashoff D, Livingston EH, Heber D (2003) Gene expression profile of metastatic colon cancer cells resistant to cisplatin-induced apoptosis. Int J Oncol 22:663-670
104. Hurley JH, Emr SD (2006) The ESCRT complexes: structure and mechanism of a membranetrafficking network. Annu Rev Biophys Biomol Struct 35:277-298
105. Hwang I, Ki D (2011) Receptor-mediated T cell absorption of antigen presenting cell-derived molecules. Front Biosci 16:411-421
106. Iero M, Valenti R, Huber V, Filipazzi P, Parmiani G, Fais S, Rivoltini L (2008) Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 15:80-88
107. Israels SJ, McMillan-Ward EM (2010) Palmitoylation supports the association of tetraspanin CD63 with CD9 and integrin alphaIIbbeta3 in activated platelets. Thromb Res 125:152-158
108. Iwai K, Ishii M, Ohshima S, Miyatake K, Saeki Y (2007) Expression and function of transmembrane-4 superfamily (tetraspanin) proteins in osteoclasts: reciprocal roles of Tspan-5 and NET-6 during osteoclastogenesis. Allergol Int 56:457-463
109. Iwamoto R, Higashiyama S, Mitamura T, Taniguchi N, Klagsbrun M, Mekada E (1994) Heparin-binding EGF-like growth factor, which acts as the diphtheria toxin receptor, forms a complex with membrane protein DRAP27/CD9, which up-regulates functional receptors and diphtheria toxin sensitivity. EMBO J 13:2322-2330
110. Izquierdo-Useros N, Naranjo-Gómez M, Erkizia I, Puertas MC, Borràs FE, Blanco J, Martinez-Picado J (2010) HIV and mature dendritic cells: Trojan exosomes riding the Trojan horse? PLoS Pathog 6:e1000740
111. Janvier K, Bonifacino JS (2005) Role of the endocytic machinery in the sorting of lysosome- associated membrane proteins. Mol Biol Cell 16:4231-4242
112. Johnstone RM (2006) Exosomes biological significance: a concise review. Blood Cells Mol Dis 36:315-321
113. Jones EL, Demaria MC, Wright MD (2011) Tetraspanins in cellular immunity. Biochem Soc Trans 39:506-511
114. Jones MC, Caswell PT, Norman JC (2006) Endocytic recycling pathways: emerging regulators of cell migration. Curr Opin Cell Biol 18:549-557
115. Jung T, Castellana D, Klingbeil P, Cuesta Hernández I, Vitacolonna M, Orlicky DJ, Roffler SR, Brodt P, Zoller M (2009) CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 11:1093-1105
116. Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J, Tada N, Miyazaki S, Kudo A (2000) The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet 24:279-282
117. Kaji K, Takeshita S, Miyake K, Takai T, Kudo A (2001) Functional association of CD9 with the Fc gamma receptors in macrophages. J Immunol 166:3256-3265
118. Kanetaka K, Sakamoto M, Yamamoto Y, Takamura M, Kanematsu T, Hirohashi S et al (2003) Possible involvement of tetraspanin CO-029 in hematogenous intrahepatic metastasis of liver cancer cells. J Gastroenterol Hepatol 18:1309-1314
119. Kaplan RN, Rafii S, Lyden D (2006) Preparing the “soil”: the premetastatic niche. Cancer Res 66:11089-11093
120. Karamatic Crew V, Burton N, Kagan A, Green CA, Levene C, Flinter F, Brady RL, Daniels G, Anstee DJ (2004) CD151, the first member of the tetraspanin (TM4) superfamily detected on erythrocytes, is essential for the correct assembly of human basement membranes in kidney and skin. Blood 104:2217-2223
121. Klein-Soyer C, Azorsa DO, Cazenave JP, Lanza F (2000) CD9 participates in endothelial cell migration during in vitro wound repair. Arterioscler Thromb Vasc Biol 20:360-369
122. Knobeloch KP, Wright MD, Ochsenbein AF, Liesenfeld O, Löhler J, Zinkernagel RM, Horak I, Orinska Z (2000) Targeted inactivation of the tetraspanin CD37 impairs T-cell-dependent B-cell response under suboptimal costimulatory conditions. Mol Cell Biol 20:5363-5369
123. Koh TW, Korolchuk VI, Wairkar YP, Jiao W, Evergren E, Pan H, Zhou Y, Venken KJ, Shupliakov O, Robinson IM, O' Kane CJ, Bellen HJ (2007) Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J Cell Biol 178:309-322
124. Koh TW, Verstreken P, Bellen HJ (2004) Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43:193-205
125. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285:17442-17452
126. Kotha J, Zhang C, Longhurst CM, Lu Y, Jacobs J, Cheng Y, Jennings LK (2009) Functional relevance of tetraspanin CD9 in vascular smooth muscle cell injury phenotypes: a novel target for the prevention of neointimal hyperplasia. Atherosclerosis 203:377-386
127. Kovalenko OV, Yang X, Kolesnikova TV, Hemler ME (2004) Evidence for specific tetraspanin homodimers: inhibition of palmitoylation makes cysteine residues available for cross-linking. Biochem J 377:407-417
128. Kovalenko OV, Yang XH, Hemler ME (2007) A novel cysteine cross-linking method reveals a direct association between claudin-1 and tetraspanin CD9. Mol Cell Proteomics 6:1855-1867
129. Krementsov DN, Rassam P, Margeat E, Roy NH, Schneider-Schaulies J, Milhiet PE, Thali M (2010) HIV-1 assembly differentially alters dynamics and partitioning of tetraspanins and raft components. Traffic 11:1401-1414
130. Kropshofer H, Spindeldreher S, Röhn TA, Platania N, Grygar C, Daniel N, Wölpl A, Langen H, Horejsi V, Vogt AB (2002) Tetraspan microdomains distinct from lipid rafts enrich select peptide-MHC class II complexes. Nat Immunol 3:61-68
131. Lafleur MA, Xu D, Hemler ME (2009) Tetraspanin proteins regulate membrane type-1 matrix metalloproteinase-dependent pericellular proteolysis. Mol Biol Cell 20:2030-2040
132. Lakkaraju A, Rodriguez-Boulan E (2008) Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol 18:199-209
133. Lan RF, Liu ZX, Liu XC, Song YE, Wang DW (2005) CD151 promotes neovascularization and improves blood perfusion in a rat hind-limb ischemia model. J Endovasc Ther 12:469-478
134. Lau LM, Wee JL, Wright MD, Moseley GW, Hogarth PM, Ashman LK, Jackson DE (2004) The tetraspanin superfamily member CD151 regulates outside-in integrin alphaIIbbeta3 signaling and platelet function. Blood 104:2368-2375
135. Le Naour F, André M, Boucheix C, Rubinstein E (2006) Membrane microdomains and proteomics: lessons from tetraspanin microdomains and comparison with lipid rafts. Proteomics 6:6447-6454
136. Le Naour F, Zöller M (2008) The tumor antigen EpCAM: tetraspanins and the tight junction protein claudin-7, new partners, new functions. Front Biosci 13:5847-5865
137. Lee TH, D'Asti E, Magnus N, Al-Nedawi K, Meehan B, Rak J (2011) Microvesicles as mediators of intercellular communication in cancer-the emerging science of cellular 'debris'. Semin Immunopathol 33:455-467
138. Lee YS, Pressman S, Andress AP, Kim K, White JL, Cassidy JJ, Li X, Lubell K, Lim do H, Cho IS, Nakahara K, Preall JB, Bellare P, Sontheimer EJ, Carthew RW (2009) Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 11:1150-1156
139. Lefèvre B, Wolf JP, Ziyyat A (2010) Sperm-egg interaction: is there a link between tetraspanin(s) and GPI-anchored protein(s)? Bioessays 32:143-152
140. Lekishvili T, Fromm E, Mujoomdar M, Berditchevski F (2008) The tumour-associated antigen L6 (L6-Ag) is recruited to the tetraspanin-enriched microdomains: implication for tumour cell motility. J Cell Sci 121:685-694
141. Lermen D, Gorjup E, Dyce PW, von Bliesen H, Müller P (2010) Neuro-muscular differentiation of adult porcine skin derived stem cell-like cells. PLoS ONE 5:e8968
142. Levental I, Grzybek M, Simons K (2010) Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49:6305-6316
143. Levy S, Shoham T (2005) Protein-protein interactions in the tetraspanin web. Physiology (Bethesda) 20:218-224
144. Li XB, Zhang ZR, Schluesener HJ, Xu SQ (2006) Role of exosomes in immune regulation. J Cell Mol Med 10:364-375
145. Lima LG, Chammas R, Monteiro RQ, Moreira ME, Barcinski MA (2009) Tumor-derived microvesicles modulate the establishment of metastatic melanoma in a phosphatidylserine- dependent manner. Cancer Lett 283:168-75
146. Little KD, Hemler ME, Stipp CS (2004) Dynamic regulation of a GPCR-tetraspanin-G protein complex on intact cells: central role of CD81 in facilitating GPR56-Galpha q/11 association. Mol Biol Cell 15:2375-2387
147. Liu L, He B, Liu WM, Zhou D, Cox JV, Zhang XA (2007) Tetraspanin CD151 promotes cell migration by regulating integrin trafficking. J Biol Chem 282:31631-31642
148. Liu WF, Zuo HJ, Chai BL, Peng D, Fei YJ, Lin JY, Yu XH, Wang DW, Liu ZX (2011) Role of tetraspanin CD151-a3/a6 integrin complex: Implication in angiogenesis CD151-integrin complex in angiogenesis. Int J Biochem Cell Biol 43:642-650
149. Loewen CJ, Moritz OL, Tam BM, Papermaster DS, Molday RS (2003) The role of subunit assembly in peripherin-2 targeting to rod photoreceptor disk membranes and retinitis pigmentosa. Mol Biol Cell 14:3400-3413
150. Longo N, Yaez-Mo M, Mittelbrunn M, de la Rosa G, Muoz ML, Sanchez-Madrid F, Sanchez- Mateos P (2001) Regulatory role of tetraspanin CD9 in tumor-endothelial cell interaction during transendothelial invasion of melanoma cells. Blood 98:3717-3726
151. Lykke-Andersen S, Brodersen DE, Jensen TH (2009) Origins and activities of the eukaryotic exosome. J Cell Sci 122:1487-1494
152. Maecker HT, Levy S (1997) Normal lymphocyte development but delayed humoral immune response in CD81-null mice. J Exp Med 185:1505-1510
153. Maecker HT, Todd SC, Levy S (1997) The tetraspanin superfamily: molecular facilitators. FASEBJ 11:428-442
154. Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, Kieu C, Papior P, Baeuerle PA, Munz M, Gires O (2009) Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol 11:162-171
155. Mallardo M, Deitinghoff A, Müller J, Goetze B, Macchi P, Peters C, Kiebler MA (2003) Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain. Proc Natl Acad Sci U S A 100:2100-2105
156. Mangin PH, Kleitz L, Boucheix C, Gachet C, Lanza F (2009) CD9 negatively regulates integrin alphaIIbbeta3 activation and could thus prevent excessive platelet recruitment at sites of vascular injury. J Thromb Haemost 7:900-902
157. Mantegazza AR, Barrio MM, Moutel S, Bover L, Weck M, Brossait P, Teillaud JL, Mordoh J (2004) CD63 tetraspanin slows down cell migration and translocates to the endosomal- lysosomal-MIICs route after extracellular stimuli in human immature dendritic cells. Blood 104:1183-1190
158. Marks MS, Ohno H, Kirchnausen T, Bonracino JS (1997) Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores. Trends Cell Biol 7:124-128
159. Marsh M, Theusner K, Pelchen-Matthews A (2009) HIV assembly and budding in macrophages. Biochem Soc Trans 37:185-189
160. Martin F, Roth DM, Jans DA, Pouton CW, Partridge LJ, Monk PN, Moseley GW (2005) Tetraspanins in viral infections: a fundamental role in viral biology? J Virol 79:10839-10851
161. Martinez FO, Helming L, Gordon S (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27:451-483
162. Masciopinto F, Giovani C, Campagnoli S, Galli-Stampino L, Colombatto P, Brunetto M, Yen TS, Houghton M, Pileri P, Abrignani S (2004) Association of hepatitis C virus envelope proteins with exosomes. Eur J Immunol 34:2834-2842
163. Mathivanan S, Lim JW, Tauro BJ, Ji H, Moritz RL, Simpson RJ (2010) Proteomic analysis of A33-immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol Cell Proteomics 9:197-208
164. Matzku S, Komitowski D, Mildenberger M, Zoller M (1983) Characterization of BSp73, a spontaneous rat tumor and its in vivo selected variants showing different metastasizing capacities. Invasion Metastasis 3:109-123
165. Mazurov D, Heidecker G, Derse D (2007) The inner loop of tetraspanins CD82 and CD81 mediates interactions with human T cell lymphotrophic virus type 1 Gag protein. J Biol Chem 282:3896-3903
166. McCready J, Sims JD, Chan D, Jay DG (2010) Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: a role for plasminogen activation. BMC Cancer 10:294
167. McGovern M, Voutev R, Maciejowski J, Corsi AK, Hubbard EJ (2009) A “latent niche” mechanism for tumor initiation. Proc Natl Acad Sci U SA 106:11617-11622
168. Meyer-Wentrup F, Figdor CG, Ansems M, Brossart P, Wright MD, Adema GJ, van Spriel AB (2007) Dectin-1 interaction with tetraspanin CD37 inhibits IL-6 production. J Immunol 178:154-162
169. Mitchell PJ, Welton J, Staffurth J, Court J, Mason MD, Tabi Z, Clayton A (2009) Can urinary exosomes act as treatment response markers in prostate cancer? J Transl Med 7:4
170. Mittelbrunn M, Yahez-Mo M, Sancho D, Ursa A, Sanchez-Madrid F (2002) Cutting edge: dynamic redistribution of tetraspanin CD81 at the central zone of the immune synapse in both T lymphocytes andAPC. J Immunol 169:6691-6695
171. Miura Y, Kainuma M, Jiang H, Velasco H, Vogt PK, Hakomori S (2004) Reversion of the Jun-induced oncogenic phenotype by enhanced synthesis of sialosyllactosylceramide (GM3 ganglioside). Proc Natl Acad Sci U S A 101:16204-16209
172. Montpellier C, Tews BA, Poitrimole J, Rocha-Perugini V, D'Arienzo V, Potel J, Zhang XA, Rubinstein E, Dubuisson J, Cocquerel L (2011) Interacting regions of CD81 and two of its partners, EWI-2 and EWI-2wint, and their effect on hepatitis C virus infection. J Biol Chem 286:13954-13965
173. Morel O, Hugel B, Jesel L, Mallat Z, Lanza F, Douchet MP, Zupan M, Chauvin M, Cazenave JP, Tedgui A, Freyssinet JM, Toti F (2004) Circulating procoagulant microparticles and soluble GPV in myocardial infarction treated by primary percutaneous transluminal coronary angioplasty. A possible role for GPIIb-IIIa antagonists. J Thromb Haemost 2:1118-1126
174. Morelli AE, Larregina AT, Shufesky WJ, Sullivan ML, Stolz DB, Papworth GD, Zahorchak AF, Logar AJ, Wang Z, Watkins SC, Falo LD Jr, Thomson AW (2004) Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 104:3257-3266
175. Murayama Y, Shinomura Y, Oritani K, Miyagawa J, Yoshida H, Nishida M, Katsube F, Shiraga M, Miyazaki T, Nakamoto T, Tsutsui S, Tamura S, Higashiyama S, Shimomura I, Hayashi N (2008) The tetraspanin CD9 modulates epidermal growth factor receptor signaling in cancer cells. J Cell Physiol 216:135-143
176. Muro Y, Okabe M (2011) Mechanisms of fertilization-a view from the study of gene- manipulated mice. J Androl 32:218-225
177. Nazarenko I, Rana S, Baumann A, McAlear J, Hellwig A, Trendelenburg M, Lochnit G, Preissner KT, Zoller M (2010) Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 70:1668-1678
178. Ng T, Shima D, Squire A et al (1999) PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J 18:3909-3923
179. Nieuwland R, Van Der Post JA, Lok CA, Kenter G, Sturk A (2010) Microparticles and exosomes in gynecologic neoplasias. Semin Thromb Hemost 36:925-929
180. Nydegger S, Khurana S, Krementsov DN, Foti M, Thali M (2006) Mapping of tetraspanin- enriched microdomains that can function as gateways for HIV-1. J Cell Biol 173:795-807
181. Obregon C, Rothen-Rutishauser B, Gerber P, Gehr P, Nicod LP (2009) Active uptake of dendritic cell-derived exovesicles by epithelial cells induces the release of inflammatory mediators through a TNF-alpha-mediated pathway. Am J Pathol 175:696-705
182. Odintsova E, Butters TD, Monti E, Sprong H, van Meer G, Berditchevski F (2006) Ganglio- sides play an important role in the organization of CD82-enriched microdomains. Biochem J 400:315-325
183. Orlowski E, Chand R, Yip J, Wong C, Goschnick MW, Wright MD, Ashman LK, Jackson, DE (2009) Platelet tetraspanin superfamily member, CD151 is required for regulation of thrombus stability in vivo. J Thrombosis Haemostasis 7:2074-2084
184. Pan BT, Teng K, Wu C, Adam M, Johnstone RM (1985) Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 101:942-948
185. Pap E, Pâllinger E, Pâsztôi M, Falus A (2009) Highlights of a new type of intercellular communication: microvesicle-based information transfer. Inflamm Res 58:1-8
186. Park JE, Tan HS, Datta A, Lai RC, Zhang H, Meng W, Lim SK, Sze SK (2010) Hypoxia modulates tumor microenvironment to enhance angiogenic and metastastic potential by secretion of proteins and exosomes. Mol Cell Proteomics 9:1985-1099
187. Parthasarathy V, Martin F, Higginbottom A, Murray H, Moseley GW, Read RC, Mal G, Hulme R, Monk PN, Partridge LJ (2009) Distinct roles for tetraspanins CD9, CD63 and CD81 in the formation of multinucleated giant cells. Immunology 127:237-248
188. Peinado H, Lavotshkin S, Lyden D (2011) The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 21:139-146
189. Percherancier Y, Planchenault T, Valenzuela-Fernandez A, Virelizier JL, Arenzana-Seisdedos F, Bachelerie F (2001) Palmitoylation-dependent control of degradation, life span, and membrane expression of the CCR5 receptor. J Biol Chem 276:31936-31944
190. Petersen SH, Odintsova E, Haigh TA, Rickinson AB, Taylor GS, Berditchevski F (2011) The role of tetraspanin CD63 in antigen presentation via MHC class II. Eur J Immunol 41:2556-2561
191. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S (1998) Binding of hepatitis C virus to CD81. Science 282:938-941
192. Pols MS, Klumperman J (2009) Trafficking and function of the tetraspanin CD63. Exp Cell Res 315:1584-1592
193. Potolicchio I, Carven GJ, Xu X, Stipp C, Riese RJ, Stern LJ, Santambrogio L (2005) Pro- teomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J Immunol 175:2237-2243
194. Qazi KR, Torregrosa Paredes P, Dahlberg B, Grunewald J, Eklund A, Gabrielsson S (2010) Proinflammatory exosomes in bronchoalveolar lavage fluid of patients with sarcoidosis. Thorax 65:1016-1024
195. Raimondo F, Morosi L, Chinello C, Magni F, Pitto M (2010) Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery. Proteomics 11:709-720
196. Rak J (2010) Microparticles in cancer. Semin Thromb Hemost 36:888-906
197. Rana S, Zoller M (2011) Exosome target cell selection and the importance of exosomal tetraspanins: a hypothesis. Biochem Soc Trans 39:559-562
198. Rana S, Claas C, Kretz CC, Nazarenko I, Zöller M (2011) Activation-induced internalization differs for the tetraspanins CD9 and Tspan8: impact on tumor cell motility. Int J Biochem Cell Biol 43:106-119
199. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ (2006) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20:847-856
200. Razmara M, Hu H, Masquelier M, Li N (2007) Glycoprotein IIb/IIIa blockade inhibits platelet aminophospholipid exposure by potentiating translocase and attenuating scramblase activity. Cell Mol Life Sci 64:999-1008
201. Re F, Belyanskaya SL, Riese RJ, Cipriani B, Fischer FR, Granucci F, Ricciardi-Castagnoli P, Brosnan C, Stern LJ, Strominger JL, Santambrogio L (2002) Granulocyte-macrophage colony-stimulating factor induces an expression program in neonatal microglia that primes them for antigen presentation. J Immunol 169:2264-2273
202. Rocha-Perugini V, Lavie M, Delgrange D, Canton J, Pillez A, Potel J, Lecoeur C, Rubinstein E, Dubuisson J, Wychowski C, Cocquerel L (2009) The association of CD81 with tetraspanin- enriched microdomains is not essential for Hepatitis C virus entry. BMC Microbiol 9:111
203. Ronquist KG, Ronquist G, Larsson A, Carlsson L (2010) Proteomic analysis of prostate cancer metastasis-derived prostasomes. Anticancer Res 30:285-290
204. Rous BA, Reaves BJ, Ihrke G, Briggs JA, Gray SR, Stephens DJ, Banting G, Luzio JP (2002) Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes. Mol Biol Cell 13:1071-1082
205. Rubinstein E (2011) The complexity of tetraspanins. Biochem Soc Trans 39:501-505
206. Rubinstein E, Ziyyat A, Wolf JP, Le Naour F, Boucheix C (2006) The molecular players of sperm-egg fusion in mammals. Semin Cell Dev Biol 17:254-263
207. Ruf W, Mueller BM (2006) Thrombin generation and the pathogenesis of cancer. Semin Thromb Hemost 32(Suppl 1):61-68
208. Runz S, Keller S, Rupp C, Stoeck A, Issa Y, Koensgen D, Mustea A, Sehouli J, Kristiansen G, Altevogt P (2007) Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol 107:563-571
209. Sachs N, Kreft M, Van Den Bergh, Weerman MA, Beynon AJ, Peters TA, Weening JJ, Sonnenberg A (2006) Kidney failure in mice lacking the tetraspanin CD151. J Cell Biol 175:33-39
210. Sala-Valdés M, Ursa A, Charrin S, Rubinstein E, Hemler ME, Sânchez-Madrid F, Yâüez- Mo 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
211. Sangaletti S, Colombo MP (2008) Matricellular proteins at the crossroad of inflammation and cancer. Cancer Lett 267:245-253
212. Sato H, Takino T (2010) Coordinate action of membrane-type matrix metalloproteinase- 1 (MT1-MMP) and MMP-2 enhances pericellular proteolysis and invasion. Cancer Sci 101:843-847
213. Saunderson SC, Schuberth PC, Dunn AC, Miller L, Hock BD, MacKay PA, Koch N, Jack RW, McLellan AD (2008) Induction of exosome release in primary B cells stimulated via CD40 and the IL-4 receptor. J Immunol 180:8146-8152
214. Sawada S, Yoshimoto M, Odintsova E, Hotchin NA, Berditchevski F (2003) The tetraspanin CD151 functions as a negative regulator in the adhesion-dependent activation of Ras. J Biol Chem 278:26323-26326
215. Scherberich A, Moog S, Haan-Archipoff G, Azorsa DO, Lanza F, Beretz A (1998) Tetraspanin CD9 is associated with very late-acting integrins in human vascular smooth muscle cells and modulates collagen matrix reorganization. Arterioscler Thromb Vasc Biol 18:1691-1697
216. Schorey JS, Bhatnagar S (2008) Exosome function: from tumor immunology to pathogen biology. Traffic 9:871-881
217. Schröder J, Lüllmann-Rauch R, Himmerkus N, Pleines I, Nieswandt B, Orinska Z, Koch- Nolte F, Schröder B, Bleich M, Saftig P (2009) Deficiency of the tetraspanin CD63 associated with kidney pathology but normal lysosomal function. Mol Cell Biol 29:1083-1094
218. Seigneuret M (2006) Complete predicted three-dimensional structure of the facilitator transmembrane protein and hepatitis C virus receptor CD81: conserved and variable structural domains in the tetraspanin superfamily. Biophys J 90:212-227
219. Sharma C, Yang XH, Hemler ME (2008) DHHC2 Affects Palmitoylation, Stability, and Functions of Tetraspanins CD9 and CD151. Mol Biol Cell 19:3415-3425
220. Sheng KC, van Spriel AB, Gartlan KH, Sofi M, Apostolopoulos V, Ashman L, Wright MD (2009) Tetraspanins CD37 and CD151 differentially regulate Ag presentation and T-cell costimulation by DC. Eur J Immunol 39:50-55
221. Shet AS, Aras O, Gupta K, Hass MJ, Rausch DJ, Saba N, Koopmeiners L, Key NS, Hebbel RP (2003) Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood 102:2678-2683
222. Shi GM, Ke AW, Zhou J, Wang XY, Xu Y, Ding ZB, Devbhandari RP, Huang XY, Qiu SJ, Shi YH, Dai Z, Yang XR, Yang GH, Fan J (2010) CD151 modulates expression of matrix metalloproteinase 9 and promotes neoangiogenesis and progression of hepatocellular carcinoma. Hepatology 52:183-196
223. Shiomi T, Inoki I, Kataoka F, Ohtsuka T, Hashimoto G, Nemoii R, Okada Y (2005) Pericellular activation of proMMP-7 (promatrilysin-1) through interaction with CD151. Lab Invest 85:1489-1506
224. Silvie O, Rubinstein E, Franetich JF, Prenant M, Belnoue E, Rénia L, Hannoun L, Eling W, Levy S, Boucheix C, Mazier D (2003) Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med 9:93-96
225. Simpson F, Hussain NK, Qualmann B, Kelly RB, Kay BK, McPherson PS Schmid SL (1999) SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nat Ceil Biol 1:119-124
226. Simpson RJ, Lim JW, Moritz RL, Mathivanan S (2009) Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics 6:267-283
227. Sincock PM, Fitter S, Parton RG, Berndt MC, Gamble JR, Ashman LK (1999) PETA- 3/CD151, a member of the transmembrane 4 superfamily, is localised to the plasma membrane and endocytic system of endothelial cells, associates with multiple integrins and modulates cell function. J Cell Sci 112:833-844
228. Singethan K, Müller N, Schubert S, Lüttge D, Krementsov DN, Khurana SR, Krohne G, Schneider-Schaulies S, Thali M, Schneider-Schaulies J (2008) CD9 clustering and formation of microvilli zippers between contacting cells regulates virus-induced cell fusion. Traffic 9:924-235
229. Smalheiser NR (2007) Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol Direct 2:35
230. Spoden G, Freitag K, Husmann M, Boller K, Sapp M, Lambert C, Florin L (2008) Clathrin- and caveolin-independent entry of human papillomavirus type 16-involvement of tetraspanin- enriched microdomains (TEMs). PLoS ONE 3:e3313
231. Sridhar SC, Miranti CK (2006) Tetraspanin KAI1/CD82 suppresses invasion by inhibiting integrin-dependent crosstalk with c-Met receptor and Src kinases. Oncogene 25:2367-2378
232. Stahl PD, Barbieri MA (2002) Multivesicular bodies and multivesicular endosomes: the “ins and outs” of endosomal traffic. Sci STKE 2002 (141):PE32
233. Sterk LM, Geuijen CA, Oomen LC, Calafat J, Janssen H, Sonnenberg A (2000) The tetraspan molecule CD151, a novel constituent of hemidesmosomes, associates with the integrin alpha6beta4 and may regulate the spatial organization of hemidesmosomes. J Cell Biol 149:969-982
234. Stipp CS, Kolesnikova TV, Hemler ME (2001a) EWI-2is a major CD9 and CD81 partner and member of a novel Ig protein subfamily. J Biol Chem 276:40545-40554
235. Stipp CS, Orlicky D, Hemler ME (2001b) FPRP, a major, highly stoichiometric, highly specific CD81- and CD9-associated protein. J Biol Chem 276:4853-4862
236. Stipp CS, Kolesnikova TV, Hemler ME (2003) Functional domains in tetraspanin proteins. Trends Biochem Sci 28:106-112
237. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G (2002) The biogenesis and functions of exosomes. Traffic 3:321-330
238. Tait JF, Smith C (1999) Phosphatidylserine receptors: role of CD36 in binding of anionic phospholipid vesicles to monocytic cells. J Biol Chem 274:3048-3054
239. Takeda Y, Kazarov AR, Butterfield CE, Hopkins BD, Benjamin LE, Kaipainen A, Hemler ME (2007) Deletion of tetraspanin Cd151 results in decreased pathologic angiogenesis in vivo and in vitro. Blood 109:1524-1532
240. Talmadge JE, Fidler IJ (2010) AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 70:5649-5669
241. Tanaka F, Hori N, Sato K (2002) Identification of differentially expressed genes in rat hepatoma cell lines using subtraction and microarray. J Biochem 131:39-44
242. Tarrant JM, Groom J, Metcalf D, Li R, Borobokas B, Wright MD, Tarlinton D, Robb L (2002) The absence of Tssc6, a member of the tetraspanin superfamily, does not affect lymphoid development but enhances in vitro T-cell proliferative responses. Mol Cell Biol 22:5006-5018
243. Taylor DD, Gercel-Taylor C (2011) Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin Immunopathol 33:441-54
244. Testa JE, Brooks PC, Lin JM, Quigley JP (1999) Eukaryotic expression cloning with an antimetastatic monoclonal antibody identifies a tetraspanin (PETA-3/CD151) as an effector of human tumor cell migration and metastasis. Cancer Res 59:3812-3820
245. Thali M (2011) Tetraspanin functions during HIV-1 and influenza virus replication. Biochem Soc Trans 39:529-531
246. Tian T, Wang Y, Wang H, Zhu Z, Xiao Z (2010) Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J Cell Biochem 111:488-496
247. Tlsty TD, Coussens LM (2006) Tumor stroma and regulation of cancer development. Annu Rev Pathol 1:119-150
248. Todeschini AR, Dos Santos JN, Handa K, Hakomori SI (2008) Ganglioside GM2/GM3 complex affixed on silica nanospheres strongly inhibits cell motility through CD82/cMet-mediated pathway. Proc Natl Acad Sci U S A 105:1925-1930
249. Todeschini RA, Hakomori SI (2008) Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochim Biophys Acta 1780:421-433
250. Tsopanoglou NE, Maragoudakis ME (2007) Inhibition of angiogenesis by small-molecule antagonists of protease-activated receptor-1. Semin Thromb Hemost 33:680-687
251. Tsukita S, Yonemura S (1999) Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J Biol Chem 274:34507-34510
252. Tsukita S, Furuse M (2000) The structure and function of claudins, cell adhesion molecules at tight junctions. Ann NY Acad Sci 915:129-135
253. Tumne A, Prasad VS, Chen Y, Stolz DB, Saha K, Ratner DM, Ding M, Watkins SC, Gupta P (2009) Noncytotoxic suppression of human immunodeficiency virus type 1 transcription by exosomes secreted from CD8+ T cells. J Virol 83:4354-4364
254. Unternaehrer JJ, Chow A, Pypaert M, Inaba K, Mellman I (2007) The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface. Proc Natl Acad Sci U S A 104:234-239
255. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654-659
256. Vallhov H, Gutzeit C, Johansson SM, Nagy N, Paul M, Li Q, Friend S, George TC, Klein E, Scheynius A, Gabrielsson S (2011) Exosomes containing glycoprotein 350 released by EBV-transformed B cells selectively target B cells through CD21 and block EBV infection in vitro. J Immunol 186:73-82
257. van Niel G, Porto-Carreiro I, Simoes S, Raposo G (2006) Exosomes: a common pathway for a specialized function. J Biochem 140:13-21
258. van Spriel AB, Figdor CG (2010) The role of tetraspanins in the pathogenesis of infectious diseases. Microbes Infect 12:106-112
259. van Spriel AB, Puls KL, Sofi M, Pouniotis D, Hochrein H, Orinska Z, Knobeloch KP, Plebanski M, Wright MD (2004) A regulatory role for CD37 in T cell proliferation. J Immunol 172:29532961
260. van Spriel AB, Sofi M, Gartlan KH, Van Der Schaaf A, Verschueren I, Torensma R, Raymakers RA, Loveland BE, Netea MG, Adema GJ, Wright MD, Figdor CG (2009) The tetraspanin protein CD37 regulates IgA responses and anti-fungal immunity. PLoS Pathog 5:e1000338
261. Veenbergen S, van Spriel AB (2011) Tetraspanins in the immune response against cancer. Immunol Lett 138:129-136
262. Vlodavsky I, Korner G, Ishai-Michaeli R, Bashkin P, Bar-Shavit R, Fuks Z (1990) Extracellular matrix-resident growth factors and enzymes: possible involvement in tumor metastasis and angiogenesis. Cancer Metastasis Rev 9:203-226
263. Vogt AB, Spindeldreher S, Kropshofer H (2002) Clustering of MHC-peptide complexes prior to their engagement in the immunological synapse: lipid raft and tetraspan microdomains. Immunol Rev 189:136-151
264. Walker JW (2008) Protein scaffolds, lipid domains and substrate recognition in protein kinase C function: implications for rational drug design. Handb Exp Pharmacol 186:185-203
265. Wang H, Min G, Glockshuber R, Sun TT, Kong XP (2009) Uropathogenic E. coli adhesin- induced host cell receptor conformational changes: implications in transmembrane signaling transduction. J Mol Biol 392:352-361
266. Wang HX, Li Q, Sharma C, Knoblich K, Hemler ME (2011) Tetraspanin protein contributions to cancer. Biochem Soc Trans 39:547-552
267. Wells A, Grandis JR (2003) Phospholipase C-gamma1 in tumor progression. Clin Exp Metastasis 20:285-290
268. Whiteside TL, Mandapathil M, Szczepanski M, Szajnik M (2011) Mechanisms of tumor escape from the immune system: Adenosine-producing Treg, exosomes and tumor-associated TLRs. Bull Cancer 98:25-31
269. Willett BJ, Picard L, Hosie MJ, Turner JD, Adema K, Clapham PR (1997) Shared usage of the chemokine receptor CXCR4 by the feline and human immunodeficiency viruses. J Virol 71:6407-6415
270. Winterwood NE, Varzavand A, Meland MN, Ashman LK, Stipp CS (2006) A critical role for tetraspanin CD151 in alpha3beta1 and alpha6beta4 integrin-dependent tumor cell functions on laminin-5. Mol Biol Cell 17:2707-2721
271. Witteveldt J, Evans MJ, Bitzegeio J, Koutsoudakis G, Owsianka AM, Angus AG, Keck ZY, Foung SK, Pietschmann T, Rice CM, Patel AH (2009) CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells. J Gen Virol 90:48-58
272. Wittmann J, Jäck HM (2010) Serum microRNAs as powerful cancer biomarkers. Biochim Biophys Acta 1806:200-207
273. Wright MD, Geary SM, Fitter S, Moseley GW, Lau LM, Sheng KC, Apostolopoulos V, Stanley EG, Jackson DE, Ashman LK (2004) Characterization of mice lacking the tetraspanin superfamily member CD151. Mol Cell Biol 24:5978-5988
274. Wright MD, Moseley GW, van Spriel AB (2004) Tetraspanin microdomains in immune cell signalling and malignant disease. Tissue Antigens 64:533-542
275. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Möbius W, Hoernschemeyer J, Slot JW, Geuze HJ, Stoorvogel W (2003) Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 278:10963-10972
276. Xie B, Zhou G, Chan SY, Shapiro E, Kong XP, Wu XR, Sun TT, Costello CE (2006) Distinct glycan structures of uroplakins Ia and Ib: structural basis for the selective binding of FimH adhesin to uroplakin Ia. J Biol Chem 281:14644-14653
277. Yalaoui S, Zougbédé S, Charrin S, Silvie O, Arduise C, Farhati K, Boucheix C, Mazier D, Rubinstein E, Froissard P (2008) Hepatocyte permissiveness to Plasmodium infection is conveyed by a short and structurally conserved region of the CD81 large extracellular domain. PLoS Pathog 4:e1000010
278. Yamabhai M, Hoffman NG, Hardison NL, McPherson PS, Castagnoli L, Cesareni G, Kay BK (1998) Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains. J Biol Chem 273:31401-31407
279. Yamamoto Y, Grubisic K, Oelgeschlâger M (2007) Xenopus Tetraspanin-1 regulates gastrulation movements and neural differentiation in the early Xenopus embryo. Differentiation 75:235-245
280. Yahez-Mo M, Alfranca A, Cabanas C, Marazuela M, Tejedor R, Ursa MA, Ashman LK, de Landâzuri MO, Sânchez-Madrid F (1998) Regulation of endothelial cell motility by complexes of tetraspan molecules CD81/TAPA-1 and CD151/PETA-3 with alpha3 beta1 integrin localized at endothelial lateral junctions. J Cell Biol 141:791-804
281. Yânez-Mo M, Barreiro O, Gonzalo P, Batista A, Megias D, Genis L, Sachs N, Sala Valdés M, Alonso MA, Montoya MC, Sonnenberg A, Arroyo AG, Sânchez Madrid F (2008) MT1-MMP collagenolytic activity is regulated through association with tetraspanin CD151 in primary endothelial cells. Blood 112:3217-3226
282. Yânez-Mo M, Barreiro O, Gordon-Alonso M, Sala-Valdés M, Sânchez-Madrid F (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 19:434-446
283. Yân ez-Mo M, Gutiérrez-Lopez MD, Cabaü as C (2011) Functional interplay between tetraspanins and proteases. Cell Mol Life Sci 68:3323-3335
284. Yang J, Weinberg RA (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14:818-829
285. Yang XH, Richardson AL, TorresArzayus MI, Zhou P, Sharma C, Kazarov AR, Andzelm MM, Strominger JL, Brown M, Hemler ME (2008) CD151 accelerates breast cancer by regulating alpha 6 integrin function, signaling, and molecular organization. Cancer Res 68:3204-3213
286. Yates AJ, Rampersaud A (1998) Sphingolipids as receptor modulators. An overview. Ann N Y Acad Sci 845:57-71
287. Yauch RL, Berditchevski F, Harler MB, Reichner J, Hemler ME (1998) Highly stoichiometric, stable, and specific association of integrin alpha3beta1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration. Mol Biol Cell 9:2751-2765
288. Yauch RL, Hemler ME (2000) Specific interactions among transmembrane 4 superfamily (TM4SF) proteins and phosphoinositide 4-kinase. Biochem J 351:629-637
289. Yunta M, Lazo PA (2003) Tetraspanin proteins as organisers of membrane microdomains and signalling complexes. Cell Signal 15:559-564
290. Zakharova L, Svetlova M, Fomina AF (2007) Tcell exosomes induce cholesterol accumulation in human monocytes via phosphatidylserine receptor. J Cell Physiol 212:174-181
291. Zhang F, Kotha J, Jennings LK, Zhang XA (2009) Tetraspanins and vascular functions. 83:7-15
292. Zhang XA, Bontrager AL, Hemler ME (2001) Transmembrane-4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific beta(1) integrins. J Biol Chem 276:25005-25013
293. Zhang XA, Kazarov AR, Yang X, Bontrager AL, Stipp CS, Hemler ME (2002) Function of the tetraspanin CD151-alpha6beta1 integrin complex during cellular morphogenesis. Mol Biol Cell 13:1-11
294. Zheng Z, Liu Z (2006) CD151 gene delivery activates PI3K/Akt pathway and promotes neovascularization after myocardial infarction in rats. Mol Med 12:214-220
295. Zheng ZZ, Liu ZX (2007) Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates CD151-induced endothelial cell proliferation and cell migration. Int J Biochem Cell Biol 39:340-348
296. Zhou B, Liu L, Reddivari M, Zhang XA (2004) The palmitoylation of metastasis suppressor KAI1/CD82 is important for its motility- and invasiveness-inhibitory activity. Cancer Res 64:7455-7463
297. Zijlstra A, Lewis J, Degryse B Stuhlmann H, Quigley JP (2008) The inhibition of tumor cell intravasation and subsequent metastasis via regulation of in vivo tumor cell motility by the tetraspanin CD151. Cancer Cell 13:221-234
298. Zoller M (2006) Gastrointestinal tumors: metastasis and tetraspanins. Z Gastroenterol 44:573-586
299. Zoller M (2009) Tetraspanins: push and pull in suppressing and promoting metastasis. Nat Rev Cancer 9:40-55
300. Zomer A, Vendrig T, Hopmans ES, van Eijndhoven M, Middeldorp JM, Pegtel DM (2010) Exosomes: fit to deliver small RNA. Commun Integr Biol 3:447-450