Functional implications of tetraspanin proteins in cancer biology

Cancer Science

Volumn 98, Issue 11, 2007, Pages 1666-1677

  Lazo, Pedro A ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD53 ANTIGEN; CD63 ANTIGEN; CD82 ANTIGEN; CD9 ANTIGEN; GANGLIOSIDE; GROWTH FACTOR; GROWTH FACTOR RECEPTOR; HLA ANTIGEN; TETRASPANIN;

ANTIGEN EXPRESSION; APOPTOSIS; B CELL LYMPHOMA; CANCER; CANCER CELL; CANCER INHIBITION; CANCER RESISTANCE; CARCINOMA; CELL ADHESION; CELL INTERACTION; CELL MOTILITY; CELL PROTECTION; CELL SURVIVAL; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC CODE; HUMAN; LIPID RAFT; METASTASIS; NONHUMAN; ONCOGENE; OXIDATION REDUCTION REACTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEFICIENCY; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

ANTIGENS, CD; CHOLESTEROL; GANGLIOSIDES; HLA ANTIGENS; HUMANS; INTEGRINS; MEMBRANE LIPIDS; MEMBRANE PROTEINS; NEOPLASM PROTEINS; NEOPLASMS; PROTEOME; RECEPTORS, GROWTH FACTOR;

EID: 34748886142     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2007.00584.x     Document Type: Review

References (159)

1. Hemler ME. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol 2003; 19: 397-422.
2. Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 2005; 6: 801-11.
3. Boucheix C, Duc GHT, Jasmin C, Rubinstein E. Tetraspanins and malignancy. Expert Rev Mol Med 2001; 2001: 1-17.
4. Tarrant JM, Robb L, van Spriel AB, Wright MD. Tetraspanins: Molecular organisers of the leukocyte surface. Trends Immunol 2003; 24: 610-17.
5. Shoham T, Rajapaksa R, Kuo CC, Haimovich J, Levy S. Building of the tetraspanin web: Distinct structural domains of CD81 function in different cellular compartments. Mol Cell Biol 2006; 26: 1373-85.
6. Seigneuret M, Delaguillaumie A, Lagaudriere-Gesbert C, Conjeaud H. Structure of the tetraspanin main extracellular domain. A partially conserved fold with a structurally variable domain insertion. J Biol Chem 2001; 276: 40 055-64.
7. Stipp CS, Kolesnikova TV, Hemler ME. Functional domains in tetraspanin proteins. Trends Biochem Sci 2003; 28: 106-12.
8. Yunta M, Lazo PA. Tetraspanin proteins as organisers of membrane microdomains and signalling complexes. Cell Signal 2003; 15: 559-64.
9. Wright MD, Moseley GW, van Spriel AB. Tetraspanin microdomains in immune cell signalling and malignant disease. Tissue Antigens 2004; 64: 533-42.
10. Maecker HT, Todd SC, Levy S. The tetraspanin superfamily: Molecular facilitators. FASEB J 1997; 11: 428-42.
11. Min G, Wang H, Sun TT, Kong XP. Structural basis for tetraspanin functions as revealed by the cryo-EM structure of uroplakin complexes at 6-A resolution. J Cell Biol 2006; 173: 975-83.
12. Ritter LM, Boesze-Battaglia K, Tam BM et al. Uncoupling of photoreceptor peripherin/rds fusogenic activity from biosynthesis, subunit assembly, and targeting: A potential mechanism for pathogenic effects. J Biol Chem 2004; 279:39 958-67.
13. Charrin S, Manie S, Thiele C et al. A physical and functional link between cholesterol and tetraspanins. European J Immunol 2003; 33: 2479-89.
14. Levy S, Shoham T. Protein-protein interactions in the tetraspanin web. Physiology (Bethesda) 2005; 20: 218-24.
15. Recio JA, Merlino G. Hepatocyte growth factor/scatter factor activates proliferation in melanoma cells through p38 MAPK, ATF-2 and cyclin D1. Oncogene 2002; 21: 1000-8.
16. Andre M, Le Caer JP, Greco C et al. Proteomic analysis of the tetraspanin web using LC-ESI-MS/MS and MALDI-FTICR-MS. Proteomics 2006; 6: 1437-49.
17. Le Naour F, Andre M, Greco C et al. Profiling of the tetraspanin web of human colon cancer cells. Mol Cell Proteomics 2006; 5: 845-57.
18. Watt FM. Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J 2002; 21: 3919-26.
19. Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer 2002; 2: 91-100.
20. Ridley AJ, Schwartz MA, Burridge K et al. Cell migration: Integrating signals from front to back. Science 2003; 302: 1704-9.
21. Janes SM, Watt FM. New roles for integrins in squamous-cell carcinoma. Nat Rev Cancer 2006; 6: 175-83.
22. Hemler ME, Lobb RR. The leukocyte beta 1 integrins. Curr Opin Hematol 1995; 2: 61-7.
23. Berditchevski F. Complexes of tetraspanins with integrins: More than meets the eye. J Cell Sci 2001; 114: 4143-51.
24. Yauch RL, Kazarov AR, Desai B, Lee RT, Hemler ME. Direct extracellular contact between integrin alpha (3) beta (1) and TM4SF protein CD151. J Biol Chem 2000; 275: 9230-8.
25. Kawakami Y, Kawakami K, Steelant WF et al. Tetraspanin CD9 is a 'proteolipid', and its interaction with alpha3 integrin in microdomain is promoted by GM3 ganglioside, leading to inhibition of laminin-5-dependent cell motility. J Biol Chem 2002; 277: 34 349-58.
26. Ono M, Handa K, Sonnino S, Withers DA, Nagai H, Hakomori S. GM3 ganglioside inhibits CD9-facilitated haptotactic cell motility: coexpression of GM3 and CD9 is essential in the downregulation of tumor cell motility and malignancy. Biochemistry 2001; 40: 6414-21.
27. Berditchevski F, Zutter MM, Hemler ME. Characterization of novel complexes on the cell surface between integrins and proteins with 4 transmembrane domains (TM4 proteins). Mol Biol Cell 1996; 7: 193-207.
28. Nishiuchi R, Sanzen N, Nada S et al. Potentiation of the ligand-binding activity of integrin α3β1 via association with tetraspanin CD151. Proc Natl Acad Sci USA 2005; 102: 1939-44.
29. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L et al. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996; 379: 91-6.
30. Dedhar S. Cell-substrate interactions and signaling through ILK. Curr Opin Cell Biol 2000; 12: 250-6.
31. Yanez-Mo M, Tejedor R, Rousselle P, Sanchez-Madrid F. Tetraspanins in intercellular adhesion of polarized epithelial cells: Spatial and functional relationship to integrins and cadherins. J Cell Sci 2001; 114: 577-87.
32. Stipp CS, Kolesnikova TV, Hemler ME. EWI-2 is a major CD9 and CD81 partner and member of a novel Ig protein subfamily. J Biol Chem 2001; 276: 40 545-54.
33. Zhang XA, Lane WS, Charrin S, Rubinstein E, Liu L. EWI2/PGRL associates with the metastasis suppressor KAI1/CD82 and inhibits the migration of prostate cancer cells. Cancer Res 2003; 63: 2665-74.
34. Kolesnikova TV, Stipp CS, Rao RM, Lane WS, Luscinskas FW, Hemler ME. EWI-2 modulates lymphocyte integrin α4β1 functions. Blood 2004; 103: 3013-19.
35. Sridhar SC, Miranti CK. Tetraspanin KAI1/CD82 suppresses invasion by inhibiting integrin-dependent crosstalk with c-Met receptor and Src kinases. Oncogene 2006; 25: 2367-78.
36. Todeschini AR, Dos Santos JN, Handa K, Hakomori SI. Ganglioside GM2/ tetraspanin CD82 complex inhibits Met activation, and its cross-talk with integrins: Basis for control of cell motility through glycosynapse. J Biol Chem 2007; 282: 8123-33.
37. Trusolino L, Comoglio PM. Scatter-factor and semaphorin receptors: Cell signalling for invasive growth. Nature Rev Cancer 2002; 2: 289-300.
38. Shi W, Fan H, Shum L, Derynck R. The tetraspanin CD9 associates with transmembrane TGF-α and regulates TGF-α-induced EGF receptor activation and cell proliferation. J Cell Biol 2000; 148: 591-602.
39. Meyer-Wentrup F, Figdor CG, Ansems M et al. Dectin-1 interaction with tetraspanin CD37 inhibits IL-6 production. J Immunol 2007; 178: 154-62.
40. Szollosi J, Horejsi V, Bene L, Angelisova P, Damjanovich S. Supramolecular complexes of MHC class I, MHC class II, CD20, and tetraspan molecules (CD53, CD81, and CD82) at the surface of a B cell line JY. J Immunol 1996; 157: 2939-46.
41. Berditchevski F, Odintsova E. Tetraspanins as regulators of protein trafficking. Traffic 2007; 8: 89-96.
42. Unternaehrer JJ, Chow A, Pypaert M, Inaba K, Mellman I. The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface. Proc Natl Acad Sci USA 2007; 104: 234-9.
43. Boucheix C, Rubinstein E. Tetraspanins. Cell Mol Life Sci 2001; 58: 1189-205.
44. Berditchevski F, Tolias KF, Wong K, Carpenter CL, Hemler ME. A novel link between integrins, transmembrane-4-superfamily proteins (CD63 and CD81), and phosphatidylinositol 4-kinase. J Biol Chem 1997; 272: 2595-8.
45. Claas C, Stipp CS, Hemler ME. Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts. J Biol Chem 2001; 276: 7974-84.
46. Bosca L, Lazo PA. Induction of nitric oxide release by MRC OX-44 (anti-CD53) through a protein kinase C-dependent pathway in rat macrophages. J Exp Med 1994; 179: 1119-26.
47. Barcia R, Garcia-Vargas S, Bosca L, Lazo PA. CD53 antigen and epidermal growth factor induce similar changes in the pattern of phorbol ester binding in a B cell lymphoma. Cell Immunol 1996; 169: 107-12.
48. Lazo PA, Cuevas L, Gutierrez del Arroyo A, Orue E. Ligation of CD53/ OX44, a tetraspan antigen, induces homotypic adhesion mediated by specific cell-cell interactions. Cell Immunol 1997; 178: 132-40.
49. Zhang XA, Bontrager AL, Hemler ME. Transmembrane-4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific beta (1) integrins. J Biol Chem 2001; 276: 25 005-13.
50. Yunta M, Oliva JL, Barcia R, Horejsi V, Angelisova P, Lazo PA. Transient activation of the c-Jun N-terminal kinase (JNK) activity by ligation of the tetraspan CD53 antigen in different cell types. Eur J Biochem 2002; 269: 1012-21.
51. Yunta M, Rodriguez-Barbero A, Arevalo MA, Lopez-Novoa JM, Lazo PA. Induction of DNA synthesis by ligation of the CD53 tetraspanin antigen in primary cultures of mesangial cells. Kidney Int 2003; 63: 534-42.
52. Carmo AM, Wright MD. Association of the transmembrane 4 superfamily molecule CD53 with a tyrosine phosphatase activity. Eur J Immunol 1995; 25: 2090-5.
53. Penninger JM, Wallace VA, Kishihara K, Mak TW. The role of p56lck and p59fyn tyrosine kinases and CD45 protein tyrosine phosphatase in T-cell development and clonal selection. Immunol Rev 1993; 135: 183-214.
54. Sefton BM, Taddie JA. Role of tyrosine kinases in lymphocyte activation. Curr Opin Immunol 1994; 6: 372-9.
55. Charrin S, Manie S, Oualid M, Billard M, Boucheix C, Rubinstein E. Differential stability of tetraspanin/tetraspanin interactions: Role of palmitoylation. FEBS Lett 2002; 516: 139-44.
56. Kovalenko OV, Yang X, Kolesnikova TV, Hemler ME. Evidence for specific tetraspanin homodimers: Inhibition of palmitoylation makes cysteine residues available for cross-linking. Biochem J 2004; 377: 407-17.
57. Berditchevski F, Odintsova E, Sawada S, Gilbert E. Expression of the palmitoylation-deficient CD151 weakens the association of α3β1 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signaling. J Biol Chem 2002; 277: 36 991-7000.
58. Yang X, Claas C, Kraeft SK et al. Palmitoylation of tetraspanin proteins: Modulation of CD151 lateral interacts, subcellular distribution, and integrin-dependent cell morphology. Mol Biol Cell 2002; 13: 767-81.
59. Yang XH, Kovalenko OV, Kolesnikova TV et al. Contrasting effects of EWI proteins, integrins and protein palmitoylation on cell surface CD9 organization. J Biol Chem 2006; 281: 12 976-85.
60. Clark KL, Oelke A, Johnson ME, Eilert KD, Simpson PC, Todd SC. CD81 associates with 14-3-3 in a redox-regulated palmitoylation-dependent manner. J Biol Chem 2004; 279: 19 401-6.
61. Cherukuri A, Carter RH, Brooks S et al. B cell signaling is regulated by induced palmitoylation of CD81. J Biol Chem 2004; 279: 31 973-82.
62. Zhou B, Liu L, Reddivari M, Zhang XA. The palmitoylation of metastasis suppressor KAI1/CD82 is important for its motility- and invasiveness-inhibitory activity. Cancer Res 2004; 64: 7455-63.
63. Yang X, Kovalenko OV, Tang W, Claas C, Stipp CS, Hemler ME. Palmitoylation supports assembly and function of integrin-tetraspanin complexes. J Cell Biol 2004; 167: 1231-40.
64. Mitsuzuka K, Handa K, Satoh M, Arai Y, Hakomori S. A specific microdomain ('glycosynapse 3') controls phenotypic conversion and reversion of bladder cancer cells through GM3-mediated interaction of α3β1 integrin with CD9. J Biol Chem 2005; 280: 35 545-53.
65. Toledo MS, Suzuki E, Handa K, Hakomori S. Cell growth regulation through GM3-enriched microdomain (glycosynapse) in human lung embryonal fibroblast WI38 and its oncogenic transformant VA13. J Biol Chem 2004; 279: 34 655-64.
66. Odintsova E, Butters TD, Monti E, Sprong H, van Meer G, Berditchevski F. Gangliosides play an important role in the organisation of CD82-enriched microdomains. Biochem J 2006; 400: 315-25.
67. Thorne RF, Mhaidat NM, Ralston KJ, Burns GF. Shed gangliosides provide detergent-independent evidence for type-3 glycosynapses. Biochem Biophys Res Commun 2007; 356: 306-11.
68. Miura Y, Kainuma M, Jiang H, Velasco H, Vogt PK, Hakomori S. Reversion of the Jun-induced oncogenic phenotype by enhanced synthesis of sialosyllactosylceramide (GM3 ganglioside). Proc Natl Acad Sci USA 2004; 101: 16 204-9.
69. Yauch RL, Hemler ME. Specific interactions among transmembrane 4 superfamily (TM4SF) proteins and phosphoinositide 4-kinase. Biochem J 2000; 351: 629-37.
70. Karamatic Crew V, Burton N, Kagan A et al. 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 2004; 104: 2217-23.
71. Sachs N, Kreft M, van den Bergh Weerman MA et al. Kidney failure in mice lacking the tetraspanin CD151. J Cell Biol 2006; 175: 33-9.
72. Zemni R, Bienvenu T, Vinet MC et al. A new gene involved in X-linked mental retardation identified by analysis of an X;2 balanced translocation. Nat Genet 2000; 24: 167-70.
73. van Soest S, Westerveld A, de Jong PT, Bleeker-Wagemakers EM, Bergen AA. Retinitis pigmentosa: Defined from a molecular point of view. Surv Ophthalmol 1999; 43: 321-34.
74. Mollinedo F, Fontan G, Barasoain I, Lazo PA. Recurrent infectious diseases in human CD53 deficiency. Clin Diagn Lab Immunol 1997; 4: 229-31.
75. Le Naour F, Rubinstein E, Jasmin C, Prenant M, Boucheix C. Severely reduced female fertility in CD9-deficient mice. Science 2000; 287: 319-21.
76. Rubinstein E, Ziyyat A, Prenant M et al. Reduced fertility of female mice lacking CD81. Dev Biol 2006; 290: 351-8.
77. Takeda Y, Kazarov AR, Butterfield CE et al. Deletion of tetraspanin CD151 results in decreased pathological angiogenesis in vivo and in vitro. Blood 2006; 109: 1524-32.
78. Cowin AJ, Adams D, Geary SM, Wright MD, Jones JC, Ashman LK. Wound healing is defective in mice lacking tetraspanin CD151. J Invest Dermatol 2006; 126: 680-9.
79. Knobeloch KP, Wright MD, Ochsenbein AF et al. Targeted inactivation of the tetraspanin CD37 impairs T-cell-dependent B-cell response under suboptimal costimulatory conditions. Mol Cell Biol 2000; 20: 5363-9.
80. Fradkin LG, Kamphorst JT, DiAntonio A, Goodman CS, Noordermeer JN. Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar function in the formation of the embryonic synapse. Proc Natl Acad Sci USA 2002; 99: 13 663-8.
81. Moribe H, Yochem J, Yamada H, Tabuse Y, Fujimoto T, Mekada E. Tetraspanin protein (TSP-15) is required for epidermal integrity in Caenorhabditis elegans. J Cell Sci 2004; 22: 5209-20.
82. Berditchevski F, Odintsova E. Characterization of integrin-tetraspanin adhesion complexes: Role of tetraspanins in integrin signaling. J Cell Biol 1999; 146: 477-92.
83. Yanez-Mo M, Alfranca A, Cabanas C et al. Regulation of endothelial cell motility by complexes of tetraspan molecules CD81/TAPA-1 and CD151/ PETA-3 with α3β1 integrin localized at endothelial lateral junctions. J Cell Biol 1998; 141: 791-804.
84. Penas PF, Garcia-Diez A, Sanchez-Madrid F, Yanez-Mo M. Tetraspanins are localized at motility-related structures and involved in normal human keratinocyte wound healing migration. J Invest Dermatol 2000; 114: 1126-35.
85. Sterk LM, Geuijen CA, Oomen LC, Calafat J, Janssen H, Sonnenberg A. The tetraspan molecule CD151, a novel constituent of hemidesmosomes, associates with the integrin α6β4 and may regulate the spatial organization of hemidesmosomes. J Cell Biol 2000; 149: 969-82.
86. Longo N, Yanez-Mo M, Mittelbrunn M et al. Regulatory role of tetraspanin CD9 in tumor-endothelial cell interaction during transendothelial invasion of melanoma cells. Blood 2001; 98: 3717-26.
87. Hong I-K, Jin Y-J, Byun H-J, Jeoung D-I, Kim Y-M, Lee H. 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 2006; 281: 24 279-92.
88. Shigeta M, Sanzen N, Ozawa M, Gu J, Hasegawa H, Sekiguchi K. CD151 regulates epithelial cell-cell adhesion through PKC- and Cdc42-dependent actin cytoskeletal reorganization. J Cell Biol 2003; 163: 165-76.
89. Garcia-Lopez MA, Barreiro O, Garcia-Diez A, Sanchez-Madrid F, Penas PF. Role of tetraspanins CD9 and CD151 in primary melanocyte motility. J Invest Dermatol 2005; 125: 1001-9.
90. Winterwood NE, Varzavand A, Meland MN, Ashman LK, Stipp CS. A critical role for tetraspanin CD151 in α3β1 and α6β4 integrin-dependent tumor cell functions on laminin-5. Mol Biol Cell 2006; 17: 2707-21.
91. Chometon G, Zhang ZG, Rubinstein E, Boucheix C, Mauch C, Aumailley M. Dissociation of the complex between CD151 and laminin-binding integrins permits migration of epithelial cells. Exp Cell Res 2006; 312: 983-95.
92. Delaguillaumie A, Harriague J, Kohanna S et al. Tetraspanin CD82 controls the association of cholesterol-dependent microdomains with the actin cytoskeleton in T lymphocytes: Relevance to co-stimulation. J Cell Sci 2004; 117: 5269-82.
93. Lagaudriere-Gesbert C, Lebel-Binay S, Hubeau C, Fradelizi D, Conjeaud H. Signaling through the tetraspanin CD82 triggers its association with the cytoskeleton leading to sustained morphological changes and T cell activation. Eur J Immunol 1998; 28: 4332-44.
94. Delaguillaumie A, Lagaudriere-Gesbert C, Popoff MR, Conjeaud H. Rho GTPases link cytoskeletal rearrangements and activation processes induced via the tetraspanin CD82 in T lymphocytes. J Cell Sci 2002; 115: 433-43.
95. Ono M, Handa K, Withers DA, Hakomori S. Motility inhibition and apoptosis are induced by metastasis-suppressing gene product CD82 and its analogue CD9, with concurrent glycosylation. Cancer Res 1999; 59: 2335-9.
96. Zhang XA, He B, Zhou B, Liu L. Requirement of the p130CAS-Crk coupling for metastasis suppressor KAI1/CD82-mediated inhibition of cell migration. J Biol Chem 2003; 278: 27 319-28.
97. Adachi M, Taki T, Ieki Y, Huang CL, Higashiyama M, Miyake M. Correlation of KAI1/CD82 gene expression with good prognosis in patients with non-small cell lung cancer. Cancer Res 1996; 56: 1751-5.
98. Uchida S, Shimada Y, Watanabe G et al. Motility-related protein (MRP-1/ CD9) and KAI1/CD82 expression inversely correlate with lymph node metastasis in oesophageal squamous cell carcinoma. Br J Cancer 1999; 79: 1168-73.
99. Tohami T, Drucker L, Shapiro H, Radnay J, Lishner M. Overexpression of tetraspanins affects multiple myeloma cell survival and invasive potential. FASEB J 2007; 21: 691-9.
100. Lebel-Binay S, Lagaudriere C, Fradelizi D, Conjeaud H. CD82, tetra-span-transmembrane protein, is a regulated transducing molecule on U937 monocytic cell line. J Leukoc Biol 1995; 57: 956-63.
101. Iwata S, Kobayashi H, Miyake-Nishijima R et al. Distinctive signaling pathways through CD82 and beta1 integrins in human T cells. Eur J Immunol 2002; 32: 1328-37.
102. Lebel-Binay S, Lagaudriere C, Fradelizi D, Conjeaud H. CD82, member of the tetra-span-transmembrane protein family, is a costimulatory protein for T cell activation. J Immunol 1995; 155: 101-10.
103. Bandyopadhyay S, Zhan R, Chaudhuri A et al. Interaction of KAI1 on tumor cells with DARC on vascular endothelium leads to metastasis suppression. Nat Med 2006; 12: 933-8.
104. Iiizumi M, Bandyopadhyay S, Watabe K. Interaction of Duffy antigen receptor for chemokines and KAI1: A critical step in metastasis suppression. Cancer Res 2007; 67: 1411-14.
105. Lowe SW, Cepero E, Evan G. Intrinsic tumour suppression. Nature 2004; 432: 307-15.
106. Yan Y, Shirakabe K, Werb Z. The metalloprotease Kuzbanian (ADAM10) mediates the transactivation of EGF receptor by G protein-coupled receptors. J Cell Biol 2002; 158: 221-6.
107. Saito Y, Tachibana I, Takeda Y et al. Absence of CD9 enhances adhesion-dependent morph differentiation, survival, matrix metalloproteinase-2 production in small cell lung cancer cells. Cancer Res 2006; 66: 9557-65.
108. Si Z, Hersey P. Expression of the neuroglandular antigen and analogues in melanoma. CD9 expression appears inversely related to metastatic potential of melanoma. Int J Cancer 1993; 54: 37-43.
109. Huang CI, Kohno N, Ogawa E, Adachi M, Taki T, Miyake M. Correlation of reduction in MRP-1/CD9 and KAI1/CD82 expression with recurrences in breast cancer patients. Am J Pathol 1998; 153: 973-83.
110. Kusukawa J, Ryu F, Kameyama T, Mekada E. Reduced expression of CD9 in oral squamous cell carcinoma: CD9 expression inversely related to high prevalence of lymph node metastasis. J Oral Pathol Med 2001; 30: 73-9.
111. Houle CD, Ding XY, Foley JF, Afshari CA, Barrett JC, Davis BJ. Loss of expression and altered localization of KAI1 and CD9 protein are associated with epithelial ovarian cancer progression. Gynecol Oncol 2002; 86: 69-78.
112. Sauer G, Windisch J, Kurzeder C, Heilmann V, Kreienberg R, Deissler H. Progression of cervical carcinomas is associated with down-regulation of CD9 but strong local re-expression at sites of transendothelial invasion. Clin Cancer Res 2003; 9: 6426-31.
113. Waterhouse R, Ha C, Dveksler GS. Murine CD9 is the receptor for pregnancy-specific glycoprotein 17. J Exp Med 2002; 195: 277-82.
114. Ellerman DA, Ha C, Primakoff P, Myles DG, Dveksler GS. Direct binding of the ligand PSG17 to CD9 requires a CD9 site essential for sperm-egg fusion. Mol Biol Cell 2003; 14: 5090-103.
115. Snyder SK, Wessner DH, Wessells JL et al. Pregnancy-specific glycoproteins function as immunomodulators by inducing secretion of IL-10, IL-6 and TGF-β1 by human monocytes. Am J Reprod Immunol 2001; 45: 205-16.
116. Ha CT, Waterhouse R, Wessells J, Wu JA, Dveksler GS. Binding of pregnancy-specific glycoprotein 17 to CD9 on macrophages induces secretion of IL-10, IL-6, PGE2, and TGF-β1. J Leukoc Biol 2005; 77: 948-57.
117. Schick MR, Nguyen VQ, Levy S. Anti-TAPA-1 antibodies induce protein tyrosine phosphorylation that is prevented by increasing intracellular thiol levels. J Immunol 1993; 151: 1918-25.
118. Schick MR, Levy S. The TAPA-1 molecule is associated on the surface of B cells with HLA-DR molecules. J Immunol 1993; 151: 4090-7.
119. Mannion BA, Berditchevski F, Kraeft SK, Chen LB, Hemler ME. Transmembrane-4 superfamily proteins CD81 (TAPA-1), CD82, CD63, and CD53 specifically associated with integrin alpha 4 beta 1 (CD49d/CD29). J Immunol 1996; 157: 2039-47.
120. Rubinstein E, Le Naour F, Lagaudriere-Gesbert C, Billard M, Conjeaud H, Boucheix C. CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur J Immunol 1996; 26: 2657-65.
121. Behr S, Schriever F. Engaging CD19 or target of an antiproliferative antibody 1 on human B lymphocytes induces binding of B cells to the interfollicular stroma of human tonsils via integrin a4/b1 and fibronectin. J Exp Med 1995; 182: 1191-9.
122. Levy S, Todd SC, Maecker HT. CD81 (TAPA-1): A molecule involved in signal transduction and cell adhesion in the immune system. Annu Rev Immunol 1998; 16: 89-109.
123. Sala-Valdes M, Ursa A, Charrin S et al. 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 2006; 281: 19 665-75.
124. Latysheva N, Muratov G, Rajesh S et al. Syntenin-1 is a new component of tetraspanin-enriched microdomains: Mechanisms and consequences of the interaction of syntenin-1 with CD63. Mol Cell Bio 2006; 24: 7707-18.
125. Hotta H, Takahashi N, Homma M. Transcriptional enhancement of the human gene encoding for a melanoma-associated antigen (ME491) in association with malignant transformation. Jpn J Cancer Res 1989; 80: 1186-91.
126. Hotta H, Ross AH, Huebner K et al. Molecular cloning and characterization of an antigen associated with early stages of melanoma tumor progression. Cancer Res 1988; 48: 2955-62.
127. Radford KJ, Mallesch J, Hersey P. Suppression of human melanoma cell growth and metastasis by the melanoma-associated antigen CD63 (ME491). Int J Cancer 1995; 62: 631-5.
128. Sordat I, Decraene C, Silvestre T et al. Complementary DNA arrays identify CD63 tetraspanin and α3 integrin chain as differentially expressed in low and high metastatic human colon carcinoma cells. Lab Invest 2002; 82: 1715-24.
129. Yunta M, Lazo PA. Apoptosis protection and survival signal by the CD53 tetraspanin antigen. Oncogene 2003; 22: 1219-24.
130. Nichols TC, Guthridge JM, Karp DR, Molina H, Fletcher DR, Holers VM. Gamma-glutamyl transpeptidase, an ecto-enzyme regulator of intracellular redox potential, is a component of TM4 signal transduction complexes. Eur J Immunol 1998; 28: 4123-9.
131. Voehringer DW, Hirschberg DL, Xiao J et al. Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proc Natl Acad Sci USA 2000; 97: 2680-5.
132. Barrena S, Almeida J, Yunta M et al. Aberrant expression of tetraspanin molecules in B-cell chronic lymphoproliferative disorders and its correlation with normal B-cell maturation. Leukemia 2005; 19: 1376-83.
133. Slupsky JR, Seehafer JG, Tang S-C, Masellis-Smith A, Shaw ARE. Evidence that monoclonal antibodies against CD9 antigen induce specific association between CD9 and the platelet glycoprotein IIb-IIIa complex. Jbiolchem 1989; 264: 12 289-93.
134. Masellis-Smith A, Jensen GS, Seehafer JG, Slupsky JR, Shaw AR. Anti-CD9 monoclonal antibodies induce homotypic adhesion of pre-B cell lines by a novel mechanism. J Immunol 1990; 144: 1607-13.
135. Takahashi S, Doss C, Levy S, Levy R. TAPA-1, the target of an antiproliferative antibody, is associated on the cell surface with the Leu-13 antigen. J Immunol 1990; 145: 2207-13.
136. Horejsi V, Vlcek C. Novel structurally distinct family of leucocyte surface glycoproteins including CD9, CD37, CD53 and CD63. FEBS Lett 1991; 288: 1-4.
137. Beckmann J, Scheitza S, Wernet P, Fischer JC, Giebel B. Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: Identification of asymmetrically segregating proteins. Blood 2007; 109: 5494-501.
138. Okochi H, Mine T, Nashiro K, Suzuki J, Fujita T, Furue M. Expression of tetraspans transmembrane family in the epithelium of the gastrointestinal tract. J Clin Gastroenterol 1999; 29: 63-7.
139. Szala S, Kasai Y, Steplewski Z, Rodeck U, Koprowski H, Linnenbach AJ. Molecular cloning of cDNA for the human tumor-associated antigen CO-029 and identification of related transmembrane antigens. Proc Natl Acad Sci USA 1990; 87: 6833-7.
140. Hajj R, Baranek T, Le Naour R, Lesimple P, Puchelle E, Coraux C. Basal cells of the human adult airway surface epithelium retain transit-amplifying cell properties. Stem Cells 2006; 25: 139-48.
141. Whitfield ML, Finlay DR, Murray JI et al. Systemic and cell type-specific gene expression patterns in scleroderma skin. Proc Natl Acad Sci USA 2003; 100: 12 319-24.
142. Okochi H, Kato M, Nashiro K, Yoshie O, Miyazono K, Furue M. Expression of tetra-spans transmembrane family (CD9, CD37, CD53, CD63, CD81 and CD82) in normal and neoplastic human keratinocytes: An association of CD9 with alpha 3 beta 1 integrin. Br J Dermatol 1997; 137: 856-63.
143. Le Naour F, Prenant M, Francastel C, Rubinstein E, Uzan G, Boucheix C. Transcriptional regulation of the human CD9 gene: Characterization of the 5′-flanking region. Oncogene 1996; 13: 481-6.
144. Hernandez-Torres J, Yunta M, Lazo PA. Differential cooperation between regulatory sequences required for human CD53 gene expression. J Biol Chem 2001; 276: 35 405-13.
145. Davidson EH. The Regulatory Genome. Gene Regulatory Networks in Development and Evolution. San Diego, CA: Academic Press, 2006.
146. Ferrer M, Yunta M, Lazo PA. Tetraspan transmembrane antigen levels in Burkitt lymphoma cell lines. Leukemia 1998; 12: 773.
147. Ferrer M, Yunta M, Lazo PA. Pattern of expression of tetraspanin antigen genes in Burkitt lymphoma cell lines. Clin Exp Immunol 1998; 113: 346-52.
148. Barrena S, Almeida J, Yunta M et al. Discrimination of biclonal B-cell chronic lymphoproliferative neoplasias by tetraspanin antigen expression. Leukemia 2005; 19: 1708-9.
149. Higgins JP, Shinghal R, Gill H et al. Gene expression patterns in renal cell carcinoma assessed by complementary DNA microarray. Am J Pathol 2003; 162: 925-32.
150. Higashiyama M, Taki T, Ieki Y et al. Reduced motility related protein-1 (MRP1/CD9) gene expression as a factor of poor prognosis in non-small cell lung cancer. Cancer Res 1995; 55: 6040-4.
151. Hori H, Yano S, Koufuji K, Takeda J, Shirouzu K. CD9 expression in gastric cancer and its significance. J Surg Res 2004; 117: 208-15.
152. Hotta H, Hara I, Miyamoto H, Homma M. Overexpression of the human melanoma-associated antigen ME491 partially suppresses in vivo malignant phenotypes of H-ras-transformed NIH3T3 cells in athymic nude mice. Melanoma Res 1991; 1: 125-32.
153. Sauer G, Kurzeder C, Grundmann R, Kreienberg R, Zeillinger R, Deissler H. Expression of tetraspanin adaptor proteins below defined threshold values is associated with in vitro invasiveness of mammary carcinoma cells. Oncol Report 2003; 10: 405-10.
154. Gesierich S, Berezovskiy I, Ryschich E, Zoller M. Systemic induction of the angiogenesis switch by the tetraspanin D6.1a/CO-029. Cancer Res 2006; 66: 7083-94.
155. Chen Z, Mustafa T, Trojanowicz B et al. CD82, and CD63 in thyroid cancer. Int J Mol Med 2004; 14: 517-27.
156. Lapointe J, Li C, Higgins JP et al. Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc Natl Acad Sci USA 2004; 101: 811-16.
157. Ang J, Lijovic M, Ashman LK, Kan K, Frauman AG. CD151 protein expression predicts the clinical outcome of low-grade primary prostate cancer better than histologic grading: A new prognostic indicator? Cancer Epidemiol Biomarkers Prev 2004; 13: 1717-21.
158. Yuasa T, Yoshiki T, Isono T, Tanaka T, Hayashida H, Okada Y. Expression of transitional cell-specific genes, uroplakin Ia and II, in bladder cancer: Detection of circulating cancer cells in the peripheral blood of metastatic patients. Int J Urol 1999; 6: 286-92.
159. Olsburgh J, Harnden P, Weeks R et al. Uroplakin gene expression in normal human tissues and locally advanced bladder cancer. J Pathol 2003; 199: 41-9.