EWI2/PGRL associates with the metastasis suppressor KAI1/CD82 and inhibits the migration of prostate cancer cells

Cancer Research

Volumn 63, Issue 10, 2003, Pages 2665-2674

  Zhang, Xin A ^a   Lane, William S ^b   Charrin, Stephanie ^c   Rubinstein, Eric ^c   Liu, Lei ^d  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HÔPITAL PAUL BROUSSE   (France)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD82 ANTIGEN; CELL SURFACE PROTEIN; PROTEIN KASP; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CANCER CELL CULTURE; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; HUMAN; HUMAN CELL; INHIBITION KINETICS; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STOICHIOMETRY; SUPPRESSOR GENE;

AMINO ACID SEQUENCE; ANTIGENS, CD; BASE SEQUENCE; CELL MOVEMENT; HUMANS; IMMUNOGLOBULINS; JURKAT CELLS; KANGAI-1 PROTEIN; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; TUMOR CELLS, CULTURED;

EID: 0038179866     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Dong, J-T., Lamb, P. W., Rinker-Schaeffer, C. W., Vukanovic, J., Ichikawa, T., Issacs, J. T., and Barrett, J. C. KAI1, a metastasis suppressor gene for prostate cancer on human chromosome 11p11.2. Science (Wash. DC), 268: 884-886, 1995.
2. Dong, J-T., Suzuki, H., Pin, S. S., Bova, S., Schalken, J. A., Isaacs, W. B., Barrett, J. C., and Isaacs, J. T. Down-regulation of the KAI1 metastasis suppressor gene during the progression of human prostate cancer infrequently involves gene mutation or allelic loss. Cancer Res., 56: 4387-4390, 1996.
3. Udea, T., Ichikawa, T., Tamura, J., Mikata, A., Akakura, K., Akimoto, S., Imai, T., Yoshie, O., Shiraishi, T., Yatani, R., Ito, H., and Shimazaki, J. Expression of KAI1 protein in benign prostatic hyperplasia and prostate cancer. Am. J. Pathol., 149: 1435-1440, 1996.
4. White, A., Lamb, P. W., and Barrett, J. C. Frequent downregulation of the KAI1(CD82) metastasis suppressor protein in human cancer cell lines. Oncogene, 16: 3143-3149, 1998.
5. Adachi, M., Taki, T., Ieki, Y., Huang, C. L., Higashiyama, M., and Miyake, M. Correlation of KAI1/CD82 gene expression with good prognosis in patients with non-small cell lung cancer. Cancer Res., 56: 1751-1755, 1996.
6. Lombardi, D. P., Geradts, J., Foley, J. F., Chiao, C., Lamb, P. W., and Barrett, J. C. Loss of KAI1 expression in the progression of colorectal cancer. Cancer Res., 59: 5724-5731, 1999.
7. Huang, C. I., Kohno, N., Ogawa, E., Adachi, M., Taki, T., and Miyake, M. Correlation of reduction in MRP-1/CD9 and KAI1/CD82 expression with recurrences in breast cancer patients. Am. J. Pathol., 153: 973-983, 1998.
8. Ono, M., Handa, K., Withers, D. A., and Hakomori, S. Motility inhibition and apoptosis are induced by metastasis-suppressing gene product CD82 and its analogue CD9, with concurrent glycosylation. Cancer Res., 59: 2335-2339, 1999.
9. Takaoka, A., Hinoda, Y., Satoh, S., Adachi, Y., Itoh, F., Adachi, M., and Imai, K. Suppression of invasive properties of colon cancer cells by a metastasis suppressor KAI1 gene. Oncogene, 16: 1443-1453, 1998.
10. Yang, X., Wei, L. L., Tang, C., Slack, R., Mueller, S., and Lippman, M. E. Overexpression of KAI1 suppresses in vitro invasiveness and in vivo metastasis in breast cancer cells. Cancer Res., 61: 5284-5288, 2001.
11. Wright, M. D., and Tomlinson, M. G. The ins and outs of the transmembrane 4 superfamily. Immunol. Today, 15: 588-594, 1994.
12. Maecker, H. T., Todd, S. C., and Levy, S. The tetraspanin superfamily: molecular facilitator. FASEB J., 11: 428-442, 1997.
13. Hemler, M. E., Mannion, B. A., and Berdichevski, F. Association of TM4SF proteins with integrins: relevance to cancer. Biochim. Biophys. Acta, 1287: 67-71, 1996.
14. Imai, T., Fukudome, K., Takagi, S., Nagira, M., Furuse, M., Fukuhara, N., Nishimura, M., Hinuma, Y., and Yoshie, O. C33 antigen recognized by monoclonal antibodies inhibitory to human T cell leukemia virus type 1-induced syncytium formation is a member of a new family of transmembrane proteins including CD9, CD37, CD53, and CD63. J. Immunol., 149: 2879-2886, 1992.
15. Gil, M. L., Vita, N., Lebel-Binay, S., Miloux, B., Chalon, P., Kaghad, M., Marchiol-Fournigault, C., Conjeaud, H., Caput, D., and Ferrara, P. A member of the tetra spans transmembrane protein superfamily is recognized by a monoclonal antibody raised against an HLA class I-deficient, lymphokine-activated killer-susceptible, B lymphocyte line. Cloning and preliminary functional studies. J. Immunol., 148: 2826-2833, 1992.
16. Nojima, Y., Hirose, T., Tachibana, K., Tanaka, T., Shi, L., Doshen, J., Freeman, G. J., Schlossman, S. F., and Morimoto, C. The 4F9 antigen is a member of the tetra spans transmembrane protein family and functions as an accessory molecule in T cell activation and adhesion. Cell. Immunol., 152: 249-260, 1993.
17. 1 and TM4SF protein CD151. J. Biol. Chem., 275: 9230-9238, 2000.
18. Kitadokoro, K., Bordo, D., Galli, G., Petracca, R., Falugi, F., Abrignani, S., Grandi, G., and Bolognesi, M. CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. EMBO J., 20: 12-18, 2001.
19. Rubinstein, E., Le Naour, F., Lagaudriere-Gesbert, C., Billard, M., Conjeaud, H., and Boucheix, C. CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur. J. Immunol., 26: 2657-2665, 1996.
20. 1 (CD49d/CD29). J. Immunol., 157: 2039-2047, 1996.
21. Imai, T., and Yoshie, O. C33 antigen and M38 antigen recognized by monoclonal antibodies inhibitory to syncytium formation by human T cell leukemia virus type 1 are both members of the transmembrane 4 superfamily and associate with each other and with CD4 or CD8 in T cells. J. Immunol., 151: 6470-6481, 1993.
22. Szollosi, J., Horejsi, V., Bene, L., Angelisova, P., and 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., 157: 2939-2946, 1996.
23. Lagaudriere-Gesbert, C., Lebel-Binay, S., Wiertz, E., Ploegh, H. L., Fradelizi, D., and Conjeaud, H. The tetraspanin protein CD82 associates with both free HLA class I heavy chain and heterodimeric β2-microglobulin complexes. J. Immunol., 158: 2790-2797, 1997.
24. Hammond, C., Denzin, L. K., Pan, M., Griffith, J. M., Geuze, H. J., and Cresswell, P. The tetraspan protein CD82 is a resident of MHC class II compartments where it associates with HLA-DR, -DM, and -DO molecules. J. Immunol., 161: 3282-3291, 1998.
25. Horvath, G., Serru, V., Clay, D., Billard, M., Boucheix, C., and Rubinstein, E. CD19 is linked to the integrin-associated tetraspans CD9, CD81, and CD82. J. Biol. Chem., 273: 30537-30543, 1998.
26. Escola, J. M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O., and Geuze, H. J. 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, 1998.
27. Berditchevski, F., and Odintsova, E. Characterization of integrin-tetraspanin adhesion complexes: roles of tetraspanins in integrin signaling. J. Cell Biol., 146: 477-492, 1999.
28. Odintsova, E., Sugiura, T., and Berditchevski, F. Attenuation of EGF receptor signaling by a metastasis suppressor, the tetraspanin CD82/KAI-1. Curr. Biol., 10: 1009-1012, 2000.
29. 1 integrins. J. Biol. Chem., 276: 25005-25013, 2001.
30. Berditchevski, F., Tolias, K. F., Wong, K., Carpenter, C. L., and Hemler, M. E. A novel link between integrins, transmembrane-4 superfamily proteins (CD63 and CD81), and phosphatidylinositol 4-kinase. J. Biol. Chem., 272: 2595-2598, 1997.
31. Lagaudriere-Gesbert, C., Lebel-Binay, S., Hubeau, C., Fradelizi, D., and 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., 28: 4332-4344, 1998.
32. Lebel-Binay, S., Lagaudriere, C., Fradelizi, D., and Conjeaud, H. CD82, member of the tetra-span-transmembrane protein family, is a costimulatory protein for T cell activation. J. Immunol., 155: 101-110, 1995.
33. Berditchevski, F., Bazzoni, G., and Hemler, M. E. Specific association of CD63 with the VLA-3 and VLA-6 integrins. J. Biol. Chem., 270: 17784-17790, 1995.
34. Fukudome, K., Furuse, M., Imai, T., Nishimura, M., Takagi, S., Hinuma, Y., and Yoshie, O. Identification of membrane antigen C33 recognized monoclonal antibodies inhibitory to HTLV-1 induced syncytium formation: altered glycosylation of C33 antigen in HTLV-1 positive cells. J. Virol., 66: 1394-1401, 1992.
35. 1 with CD151 provides a major link to phosphatidylinositol 4-kinase and may regulate cell migration. Mol. Biol. Cell, 9: 2751-2765, 1998.
36. Weitzman, J. B., Pasqualini, R., Takada, Y., and Hemler, M. E. The function and distinctive regulation of the integrin VLA-3 in cell adhesion, spreading, and homotypic cell aggregation. J. Biol. Chem., 268: 8651-8657, 1993.
37. Hemler, M. E., Huang, C., Takada, Y., Schwarz, L., Strominger, J. L., and Clabby, M. L. Characterization of the cell surface heterodimer VLA-4 and related peptides. J. Biol. Chem., 262: 11478-17485, 1987.
38. Lee, R. T., Berditchevski, F., Cheng, G. C., and Hemler, M. E. Integrin-mediated collagen matrix reorganization by cultured human vascular smooth muscle cells. Circ. Res., 76: 209-214, 1995.
39. Hemler, M. E., Sanchez-Madrid, F., Flotte, T. J., Krensky, A. M., Burakoff, S. J., Bhan, A. K., Springer, T. A., and Strominger, J. L. Glycoproteins of 210,000 and 130.000 m. w. on activated T cells: cell distribution and antigenic relation to components on resting cells and T cell lines. J. Immunol., 132: 3011-3018, 1984.
40. Mannion, B. A., Kolesnikova, T. V., Lin, S. H., Wang, S., Thompson, N. L., and Hemler, M. E. The light chain of CD98 is identified as E16/TA1 protein. J. Biol. Chem., 273: 33127-33129, 1998.
41. Barnstable, C. J., Bodmer, W. F., Brown, G., Galfre, G., Milstein, C., Williams, A. F., and Ziegler, A. Production of monoclonal antibodies to group A erythrocytes. HLA and other human cell surface antigens - new tools for genetic analysis. Cell, 14: 9-20, 1978.
42. Chittum, H. S., Lane, W. S., Carlson, B. A., Roller, P. P., Lung, F. D., Lee, B. J., and Hatfield. D. L. Rabbit β-globin is extended beyond its UGA stop codon by multiple suppressions and translational reading gaps. Biochemistry, 37: 10866-10870, 1998.
43. Eng, J. K., McCormick, A. L., and Yates, J. R. I. Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. J. Am. Soc. Mass Spectrom., 5: 976-989, 1994.
44. 1 cytoplasmic domain with ICAP-1 protein. J. Biol. Chem., 274: 11-19, 1999.
45. Kozak, M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res., 12: 857-872, 1884.
46. von Heijne, G. Signal sequences, the limits of variation. J. Mol. Biol., 184: 99-105, 1985.
47. Stipp, C. S., Kolesnikova, T. V., and Hemler, M. E. EWI-2 is a major CD9 and CD81 partner and member of a novel Ig protein subfamily. J. Biol. Chem., 276: 40545-40554, 2001.
48. Clark, K. L., Zeng, Z., Langford, A. L., Bowen, S. M., and Todd, S. C. PGRL is a major CD81-associated protein on lymphocytes and distinguishes a new family of cell surface proteins. J. Immunol., 167: 5115-5121, 2001.
49. Ruegg, C. L., Rivas, A., Madani, N. D., Zeitung, J., Laus, R., and Engleman, E. G. V7, a novel leukocyte surface protein that participates in T cell activation. II. Molecular cloning and characterization of the V7 gene. J. Immunol., 154: 4434-4443, 1995.
50. Orlicky, D. J., and Nordeen, S. K. Cloning, sequencing and proposed structure for a prostaglandin F2α receptor regulatory protein. Prostaglandins Leukotrienes Essent. Fatty Acids, 55: 261-268, 1996.
51. Stipp, C. S., Orlicky, D., and Hemler, M. E. FPRP, a major, highly stoichiometric, highly specific CD81- and CD9-associated protein. J. Biol. Chem., 276: 4853-4862, 2001.
52. Charrin, S., Le Naour, F., Oualid, M., Billard, M., Faure, G., Hanash, S. M., Boucheix, C., and Rubinstein, E. The major CD9 and CD81 molecular partner. Identification and characterization of the complexes. J. Biol. Chem., 276: 14329-14337, 2001.
53. Saupe, S., Roizes, G., Peter, M., Boyle, S., Gardiner, K., and De Sario, A. Molecular cloning of a human cDNA IGSF3 encoding an immunoglobulin-like membrane protein: expression and mapping to chromosome band Ip13. Genomics, 52: 305-311, 1998.
54. Shapiro, M. B., and Senapathy, P. RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res., 15: 7155-7174, 1987.
55. Brown, D. A., and London, E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol., 14: 111-136, 1998.
56. Simons, K., and Ikonen, E. Functional rafts in cell membranes. Nature (Lond.), 387: 569-572, 1997.
57. Claas, C., Stipp, C. S., and Hemler, M. E. Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts. J. Biol. Chem., 276: 7974-7984, 2001.
58. Yashiro-Ohtani, Y., Zhou, X. Y., Toyo-Oka, K., Tai, X. G., Park, C. S., Hamaoka, T., Abe, R., Miyake, K., and Fujiwara, H. Non-CD28 costimulatory molecules present in T cell rafts induce T cell costimulation by enhancing the association of TCR with rafts. J. Immunol., 164: 1251-1259, 2000.
59. Harder, T., Scheiffele, P., Verkade, P., and Simons, K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol., 141: 929-942, 1998.
60. Berditchevski, F., Zutter, M. M., and Hemler, M. E. Characterization of novel complexes on the cell surface between integrins and proteins with 4 transmembrane domains (TM4 proteins). Mol. Biol. Cell, 7: 193-207, 1996.
61. Levy, S., Todd, S. C., and Maecker, H. T. CD81 (TAPA-1): a molecule involved in signal transduction and cell adhesion in the immune system. Annu. Rev. Immunol., 16: 89-109, 1998.
62. 1-dependent neurite outgrowth. J. Cell Sci., 113: 1871-1882, 2000.
63. Wang, J-H., and Reinherz, E. L. Structural basis of cell-cell interactions in the immune system. Curr. Opin. Struct. Biol., 10: 656-661, 2000.
64. Davis, S. J., Ikemizu, S., Wild, M. K., and van der Merwe, P. A. CD2 and the nature of protein interactions mediating cell-cell recognition. Immunol. Rev., 163: 217-236, 1998.