Regulation of endothelial cell motility by complexes of retraspan molecules CD81/TAPA-1 and CD151/PETA-3 with α3β1 integrin localized at endothelial lateral junctions

Journal of Cell Biology

Volumn 141, Issue 3, 1998, Pages 791-804

  Yáñez Mó, María ^a   Alfranca, Arántzazu ^a   Cabañas, Carlos ^b   Marazuela, Monica ^a   Tejedor, Reyes ^a   Ursa, M Angeles ^a   Ashman, Leonie K ^c   De Landázuri, Manuel O ^a   Sánchez Madrid, Francisco ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; FIBRONECTIN; INTEGRIN; LAMININ;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; CELL JUNCTION; CELL MIGRATION; CELL MOTILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; IMMUNOFLUORESCENCE; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; CELL LINE; CELL MOVEMENT; CELLS, CULTURED; COLLAGEN; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; GELS; HUMANS; INTEGRIN ALPHA3BETA1; INTEGRINS; INTERCELLULAR JUNCTIONS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C;

EID: 0032482216     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.3.791     Document Type: Article

References (92)

1. Ades, E.W., F.J. Candal, R.A. Swerlick, V.G. George, S. Summers, D.C. Bosse, and T.J. Lawley. 1992. HMEC-1: Establishment of an immortalized human microvascular endothelial cell line. J. Invest. Dermatol. 99:683-690.
2. Anderson, J.M., M.S. Balda, and A.S. Fanning. 1993. The structure and regulation of tight junctions. Curr. Opin. Cell Biol. 5:772-778.
3. Angelisová, P., I. Hilgert, and V. Horejsi. 1994. Association of four antigens of the tetraspan family (CD37, CD53, TAPA-1, and R2/C33) with MHC class II glycoproteins. Immunogenetics. 39:249-256.
4. Arroyo, A.G., P. Sánchez-Mateos, M.R. Campanero, I. Martín-Padura, E. Dejana, and F. Sánchez-Madrid. 1992. Regulation of the VLA integrin-ligand interactions through the β1 subunit. J. Cell Biol. 117:659-670.
5. Ashman, L.K., S. Fitter, P.M. Sincock, L. Nguyen, and A.C. Cambareri. 1997. Summary report: CD151. In Leucocyte Typing VI. Ed by T. Kishimoto, M. Miyasaka, D. Mason, K. Sugamura, T. Springer, S. Shaw, S.M. Goyert, L. Moretta, H. Zola, A.E.-G.Kr. von dem Borne. K. Okumura, and K. Kikutani. Garland Publishing, New York.
6. Behr, S., and F. Schriever. 1995. 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 α4/β1 and fibronectin. J. Exp. Med. 182:1191-1199.
7. Bell, G.M., W.E. Seaman, E.C. Niemi, and J.B. Imboden. 1992. The OX-44 molecule couples to signaling pathways and is associated with CD2 on rat T lymphocytes and in a Natural Killer cell line. J. Exp. Med. 175:527-536.
8. Berditchevski, F., M.M. Zutter, and M.E. Hemler. 1996. Characterization of novel complexes on the cell surface between integrins and proteins with 4 transmembrane domains (TM4 proteins). Mol. Biol. Cell. 7:193-207.
9. Berditchevski, F., K.F. Tolias, K. Wong, C.L. Carpenter, and M.E. Hemler. 1997. A novel link between integrins, transmembrane-4 superfamily proteins (CD63 and CD81) and phosphatidylinositol 4-kinase. J. Biol. Chem. 272: 2585-2598.
10. Bradbury, L.E., V.S. Goldmacher, and T.F. Tedder. 1993. The CD19 signal transduction complex of B lymphocytes. J. Immunol. 151:2915-2927.
11. Breviario, F., L. Caveda, M. Corada, I. Martín-Padura, P. Navarro, J. Golay, M. Introna, D. Gulino, M.G. Lampugnani, and E. Dejana. 1995. Functional properties of human vascular endothelial cadherin (7B4/Cadherin-5), an endothelium-specific cadherin. Arterioscler. Thromb. Vasc. Biol. 15:1229-1239.
12. Brooks, P.C., S. Stromblad, L.C. Sanders, T.L. von Schalscha, R.T. Aimes, W.G. Stetler-Stevenson, J.P. Quigley, and D.A.Cheresh. 1996. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin αvβ3. Cell. 85:683-693.
13. Campanero, M.R., A.G. Arroyo, R. Pulido, A. Ursa, M.S. de Matías, P. Sánchez-Mateos, P.D. Kassner, B.M.C. Chan, M.E. Hemler, A.L. Corbí, M.O. de Landázuri, and F. Sánchez-Madrid. 1992. Functional role of α2/β1 and α4/β1 integrins in leukocyte intercellular adhesion induced through the common β1 subunit. Ear. J. Immunol. 22:3111-3119.
14. Carmo, A.M., and M.D. Wright. 1995. Association of the transmembrane 4 superfamily molecule CD53 with a tyrosine phosphatase activity. Eur. J. Immunol. 25:2090-2095.
15. Caveda, L., I. Martín-Padura, P. Navarro, F. Breviario, M. Corada, D. Gulino, M.G. Lampugnani, and E. Dejana. 1996. Inhibition of cultured cell growth by vascular endothelial cadherin (Cadherin-5/VE-Cadherin). J. Clin. Invest. 98:886-893.
16. Citi, S. 1993. The molecular organization of tight junctions. J. Cell Biol. 121: 485-489.
17. Cowin, P., and B. Burke. 1996. Cytoskeleton-membrane interactions. Curr. Opin. Cell Biol. 8:56-65.
18. Dejana, E. 1996. Endothelial adherens junctions: implications in the control of vascular permeability and angiogenesis. J. Clin. Invest. 98:1949-1953.
19. Domanico S.Z., A.J. Pelletier, W.L. Havran, and V. Quaranta. 1997. Integrin α6Aβ1 induces CD81-dependent cell motility without engaging the extracellular matrix migration substrate. Mol. Biol. Cell. 8:2253-2265.
20. Drubin, D.O., and W.J. Nelson. 1996. Origins of cell polarity. Cell. 84:335-344.
21. Fearon, D.T. 1993. The CD19-CR2-TAPA-1 complex. CD45 and signaling by the antigen receptor of B lymphocytes. Curr. Opin. Immunol. 5:341-348.
22. Fitter, S., T.J. Tetaz, M.C. Berndt, and L.K. Ashman. 1995. Molecular cloning of a cDNA encoding a novel platelet-endothelial cell tetra-span antigen, PETA-3. Blood. 4:1348-1355.
23. Forsyth, K.D. 1991. Anti-CD9 antibodies augment neutrophil adherence to endothelium. Immunology. 72:292-296.
24. Furuse, M., T. Hirase, M. Itoh, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1993. Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 123:1777-1788.
25. Gamble, J.R., L.J. Matthias, G. Meyer, P. Kaur, G. Russ, R. Faull, M.C. Berndt, and M.A. Vadas. 1993. Regulation of in vitro capillary tube formation by anti-integrin antibodies. J. Cell Biol. 121:931-943.
26. García-Monzón, C., F. Sánchez-Madrid, L. García-Buey, A.G. Arroyo, A. García-Sánchez, and R. Moreno-Otero. 1995. Vascular adhesion molecule expression in viral chronic hepatitis: evidence of neoangiogenesis in portal tracts. Gastroenterology. 108:231-241.
27. Geiger, B., and O. Ayalon. 1992. Cadherins. Annu. Rev. Cell Biol. 8:307-332.
28. Gil, M.L., N. Vita, S. Lebel-Binay, B. Miloux, P. Chalon, M. Kaghad, C. Marchiol-Fournigault, H. Conjeaud, D. Caput, P. Ferrara, et al. 1992. 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. J. Immunol. 148:2826-2833.
29. Gómez, M., A. Luque, M.A. del Pozo, N. Hogg, F. Sánchez-Madrid and C. Cabañas. 1997. Functional relevance during lymphocyte migration and cellular localization of activated β1 integrins. Eur. J. Immunol. 27:8-16.
30. Goodenough, D.A., J.A. Goliger, and D.L. Paul. 1996. Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65:475-502.
31. Gumbiner, B., B. Stevenson, and A. Grimaldi. 1988. The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J. Cell Biol. 107:1575-1587.
32. Hanahan, D., and J. Folkman. 1996. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:353-364.
33. Hasegawa, H., Y. Utsunomiya, K. Kishimoto, and K. Yanagisawa. 1996. SFA-1, a novel cellular gene induced by human T-cell leukemia virus type 1, is a member of the transmembrane 4 superfamily. J. Virol. 70:3258-3263.
34. Hemler, M.E., B.A. Mannion, F. Berditchevski. 1996. Association of TM4SF proteins with integrins: relevance to cancer. Biochim. Biophys. Acta. 1287: 67-71.
35. Imai, T., and O. Yoshie. 1993. C33 antigen and M38 antigen recognized by monoclonal antibodies inhibitory to syncitium formation in 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.
36. Iwamoto, R., S. Higashiyama, T. Mitamura, N. Taniguchi, M. Klagsbrun, and E. Mekada. 1994. Heparin-binding EGF-like growth factor, which acts as the diphteria toxin receptor, forms a complex with membrane protein DRAP27/ CD9, which up-regulates functional receptors and diphteria toxin sensitivity. EMBO (Eur. Mol. Biol. Organ.) J. 13:2322-2330.
37. Jaffe, E.A., R.I. Nachman, C.G. Becker, and R.C. Minick. 1972. Culture of human endothelial cells derived from umbilical veins. Circulation. 46:211-253.
38. Jain, R.K., K. Schlenger, M. Höckel, and F. Yuan. 1997. Quantitative angiogenesis assays: progress and problems. Nat. Med. 3:1203-1208.
39. Jockusch, B.M., P. Bubeck, K. Giehl, M. Kroemer, J. Moschner, M. Rothkegel, M. Rüdiger, K. Schlüter, G. Stanke, and J. Winkler. 1995. The molecular architecture of focal adhesions. Annu. Rev. Cell Dev. Biol. 11:379-416.
40. Jones, P.H., L.A. Bishop, and F.M. Watt. 1996. Functional significance of CD9 association with beta-1 integrins in human epidermal keratinocytes. Cell Adhes. Commun. 4:297-305.
41. Kallin, B., R. de Martin, T. Etzold, V. Sorrentino, and L. Philipson. 1991. Cloning of a growth arrest-specific and transforming growth factor β-regulated gene, TI 1, from an epithelial cell line. Mol. Cell. Biol. 11:5338-5345.
42. Kemler, R. 1993. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 9:317-321.
43. Keon, B.H., S. Shäfer, C. Kuhn, C. Grund, and W.W. Franke. 1996. Symplekin, a novel type of tight junction plaque protein. J. Cell Biol. 134:1003-1018.
44. Kitani, S., E. Berenstein, S. Mergenhagen, P. Tempst, and R.P. Siraganian. 1991. A cell surface glycoprotein of rat basophilic leukemia cells close to the high affinity IgE receptor (Fc∈RI). J. Biol. Chem. 266:1903-1909.
45. Lampugnani, M.G., M. Resnati, E. Dejana, and P.C. Marchisio. 1991. The role of integrins in the maintenance of endothelial monolayer integrity. J. Cell Biol. 112:479-490.
46. Lampugnani, M.G., M. Resnati, M. Raiteri, R. Pigott, A. Pisacane, G. Houen, L.P. Ruco, and E. Dejana. 1992. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118:1511-1522.
47. Lampugnani, M.G., M. Corada, L. Caveda, F. Breviario, O. Ayalon, B. Geiger, and E. Dejana. 1995. The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, β-catenin, and α-catenin with vascular endothelial cadherin (VE-cadherin). J. Cell Biol. 129:203-217.
48. Langholz, O., D. Röckel, C. Mauch, E. Kozlowska, I. Bank, T. Krieg, and B. Eckes. 1995. Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by α1β1 and α2β1 integrins. J. Cell Biol. 131:1903-1915.
49. Larjava, H., J. Peltonen, S.K. Akiyama, S.S. Yamada, H.R. Gralnick, J. Uitto, and K.M. Yamada. 1990. Novel function for β1 integrins in keratinocyte cell-cell interactions. J. Cell Biol. 110:803-815.
50. Larjava, H., J.G. Lyons, T Salo, M. Mäkelä, L. Koivisto, H. Birkedal-Hansen, S.K. Akiyama, K.M. Yamada, and J. Heino. 1993. Anti-integrin antibodies induce type IV collagenase expression in keratinocytes. J. Cell. Physiol. 157: 190-200.
51. Leach, L., P. Clark, M.G. Lampugnani, A.G. Arroyo, E. Dejana, and J.A. Firth. 1993. Immunoelectron characterization of the inter-endothelial junctions in human term placenta. J. Cell. Sci. 104:1073-1081.
52. Lebel-Binay, S., C. Lagaudrière, D. Fradelizi, and H. Conjeaud. 1995. CD82, member of the tetra-span-transmembrane protein family, is a costimulatory protein for T cell activation. J. Immunol. 155:101-110.
53. Ledbetter, J.A., G. Shu, and E.A. Clark. 1987, Monoclonal antibodies to a new gp40-45 (CD37) B-cell-associated cluster growth modulate B-cell proliferation. In Leukocyte Typing III. A.J. McMichael, P.C.L. Beverley, S. Cobbold, M.J. Crumpton, W. Gilks, F.M. Gotch, N. Hogg, M. Horton, N. Ling, J.C.M. MacLennan, D.Y. Mason, C. Milstein, D. Spiegelhalter, and H. Waldmann, editors. Oxford University Press. Oxford. 339 pp.
54. Maecker, H.T., S.C. Todd, and S. Levy. 1997. The tetraspanin superfamily: molecular facilitators. FASEB J. 11:428-442.
55. Marrs, J.A., C. Andersson-Fisone, M.C. Jeong, L. Cohen-Gould, C. Zurzolo, I.R. Nabi, E. Rodriguez-Boulan, and W.J. Nelson. 1995. Plasticity in epithelial cell phenotype: modulation by expression of different cadherin cell adhesion molecules. J. Cell Biol. 129:507-519.
56. Masellis-Smith, A., and A.R.E. Shaw. 1994. CD9-regulated adhesion. Anti-CD9 monoclonal antibody induce pre-B cell adhesion to bone marrow fibroblasts through de novo recognition of fibronectin. J. Immunol. 152:2768-2777.
57. McNeill, H., M. Ozawa, R. Kemler, and W.J. Nelson. 1990. Novel function of the cell adhesion molecule uvomorulin as an inducer of cell surface polarity. Cell. 62:309-316.
58. Melchiori, A., R. Mortarini, S. Carlone, P.C. Marchisio, A. Anichini, D.M. Noonan, and A. Albini. 1995. The α3β1 integrin is involved in melanoma cell migration and invasion. Exp. Cell Res. 219:233-242.
59. Metzelaar, M.J., P.L.J. Wijngaard, P.J. Peters, J.J. Sixma, H.K. Nieuwenhuis, and H.C. Clevers. 1991. CD63 antigen. A novel lysosomal membrane glycoprotein, cloned by a screening procedure for intracellular antigens in eukaryotic cells. J. Biol. Chem. 266:3239-3245.
60. Miyake, M., M. Koyama, M. Seno, and S. Ikeyama. 1991. Identification of the motility-related protein (MRP-1), recognized by monoclonal antibody M31-15, which inhibits cell motility. J. Exp. Med. 174:1347-1354.
61. Montesano, R., and L. Orci. 1985. Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell. 42:469-477.
62. Montesano, R., and L. Orci. 1986. Phorbol esters induce angiogenesis in vitro from large-vessel endothelial cells. J. Cell Physiol. 130:284-291.
63. Nakamura, K., R. Iwamoto, and E. Mekada. 1995. Membrane-anchored heparin-binding EGF-like growth factor (HB-EGF) and diphteria toxin receptor-associated protein (DRAP27)/CD9 form a complex with integrin α3β1 at cell-cell contact sites. J. Cell Biol. 129:1691-1705.
64. Newman, P.J. 1997. The biology of PECAM-1. J. Clin. Invest. 99:3-8.
65. Olweus, J., F. Lund-Johansen, and V. Horejsi. 1993. CD53, a protein with four membrane-spanning domains, mediates signal transduction in human monocytes and B cells. J. Immunol. 151:707-716.
66. Oren, R., S. Takahashi, C. Doss. R. Levy, and S. Levy. 1990. TAPA-1, the target of an antiproliferative antibody, defines a new family of transmembrane proteins. Mol. Cell. Biol. 10:4007-4015.
67. Radford, K.J., R.F. Thorne, and P. Hersey. 1996. CD63 associates with transmembrane 4 superfamily members. CD9 and CD81, and with β1 integrins in human melanoma. Biochem. Biophys. Res. Commun. 222:13-18.
68. Radford, K.J., R.F. Thorne, and P. Hersey. 1997. Regulation of tumor cell motility and migration by CD63 in a human melanoma cell line. J. Immunol. 158:3353-3358.
69. Rubinstein, E., F.L. Naour, C. Lagaudrière-Gesbert, M. Billard, H. Conjeaud, and C. Boucheix. 1996. 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.
70. Schneeberger, E.E., and R.D. Lynch. 1992. Structure, function and regulation of cellular tight junctions. Am. J. Physiol. 262:L647-L661.
71. Shaw, A.R., A. Domanska, A. Mak, A. Gilchrist, K. Dobler, L. Visser, S. Poppema, L. Fliegel, M. Letarte, and B.J. Willet. 1995. Ectopic expression of human and feline CD9 in a human B cell line confers beta 1 integrin-dependent motility on fibronectin and laminin substrates and enhanced tyrosine phosphorylation. J. Biol. Chem. 270:24092-24099.
72. Sincock, P.M., G. Mayrhofer, and L.K. Ashman. 1997. Localization of the transmembrane 4 superfamily (TM4SF) member PETA-3 (CD151) in normal human tissues: comparison with CD9, CD63 and α5β1 integrin. J. Histochem. Cytochem. 45:515-525.
73. Skubitz, K.M., K.D. Campbell, J. Iida, and A.P.N. Skubitz. 1996. CD63 associates with tyrosine kinase activity and CD11/CD18, and transmits an activation signal in neutrophils. J. Immunol. 157:3617-3626.
74. Slupsky, J.R., J.G. Seehafer, S. Tang, A. Masellis-Smith, and A.R.E. Shaw. 1989. Evidence that monoclonal antibodies against CD9 antigen induce specific association between CD9 and the platelet glycoprotein IIb/IIIa complex. J. Biol. Chem. 264:12289-12293.
75. Sriramarao, P., P. Steffner, and K.R. Gehlsen. 1993. Biochemical evidence for a homophilic interaction of the α3β1 integrin. J. Biol. Chem. 268:22036-22041.
76. Symington, B.E., Y. Takada, and W.G. Carter. 1993. Interaction of integrins α3β1 and α2β1: potential role in keratinocyte intercellular adhesion. 1993. J. Cell Biol. 120:523-535.
77. Tai, X.G., Y. Yashiro, R. Abe, K. Toyooka, C.R. Wood, J. Morris, A. Long, S. Ono, M. Kobayashi, T. Hamaoka, et al. 1996. A role for CD9 molecules in T cell activation. J. Exp. Med. 184:753-758.
78. Takeichi, M. 1990. Cadherins: a molecular family important in selective cell-cell adhesion. Annu. Rev. Biochem. 59:237-252.
79. Takeuchi, K., T. Tsuji, S. Hakomori, and T. Irimura. 1994. Intercellular adhesion induced by anti-α3 integrin (VLA-3) antibodies. Exp. Cell Res. 211: 133-141.
80. Toothil, V.J., J.A. van Mourik, H.R. Niewenhuis, M.J. Metzelaar, and J.D.Pearson. 1990. Characterization of the enhanced adhesion of neutrophil leukocytes to thrombin-stimulated endothelial cells. J. Immunol. 145:283-291.
81. Tsukita, S., S. Tsukita, A. Nagafuchi, and S. Yonemura. 1992. Molecular linkage between cadherins and actin filaments in cell-cell adherens junctions. Curr. Opin. Cell Biol. 4:834-839.
82. Vischer, U.M., and D.D. Wagner. 1993. CD63 is a component of Weibel-Palade bodies of human endothelial cells. Blood. 82:1184-1191.
83. Wary, K.K., F. Miniero, S.J. Isakoff, E.E. Marcantonio, and F.G. Giancotti. 1996. The adaptor protein She couples a class of integrins to the control of cell cycle progression. Cell. 87:733-743.
84. Wayner, E., and W.G. Carter. 1987. Identification of multiple cell adhesion receptors for collagen and fibronectin in human fibrosarcoma cells possessing unique α and common β subunits. J. Cell Biol. 105:1873-1884.
85. Weber, C., R. Alon, B. Moser, and T.A. Springer. 1996. Sequential regulation of α4β1 and α5β1 integrin avidity by CC chemokines in monocytes: implications for transendothelial chemotaxis. J. Cell Biol. 134:1063-1073.
86. Weitzman, J.B., R. Pasqualini, Y. Takada, and M.E. Hemler. 1994. The function and distinctive regulation of the integrin VLA-3 in cell adhesion, spreading and homotypic cell aggregation. J. Biol. Chem. 12:8651-8657.
87. Weitzman, J.B., A. Chen, and M.E. Hemler. 1995. Investigation of the role of β1 integrins in cell-cell adhesion. J. Cell Sci. 108:3635-3644.
88. Werb, Z., P.M. Tremble, O. Behrendtsen, E. Crowly, and C.H. Damsky.1989. Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J. Cell. Biol. 109: 877-889.
89. Wice, B.M., and J.I. Gordon. 1995. A tetraspan membrane glycoprotein produced in the human intestinal epithelium and liver that can regulate cell density-dependent proliferation. J. Biol. Chem. 270:21907-21918.
90. Wright, M.D., and M.G. Tomlinson. 1994. The ins and outs of the transmembrane 4 superfamily. Immunol. Today. 15:588-594.
91. Wu, C., A.E. Chung, and J.A. Mc.Donald. 1995. A novel role for α3β1 integrins in extracellular matrix assembly. J. Cell Sci. 108:2511-2523.
92. Yu, J., J.H. Lin, X.R. Wu, and T.T. Sun. 1994. Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins. J. Cell Biol. 125:171-182.