Tetraspanins and vascular functions

Cardiovascular Research

Volumn 83, Issue 1, 2009, Pages 7-15

  Zhang, Feng ^a   Kotha, Jayaprakash ^a   Jennings, Lisa K ^a   Zhang, Xin A ^a  

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

Author keywords

CD151; CD63; CD9; Endothelial cells; Platelets; Smooth muscle cells; Tetraspanins; Vascular system

Indexed keywords

CELL ADHESION MOLECULE; GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN; TETRASPANIN;

ANGIOGENESIS; BLOOD VESSEL INJURY; CELL ADHESION; CELL FUSION; CELL MIGRATION; HEMATOPOIETIC CELL; HEMOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; THROMBOSIS; VASCULAR DISEASE;

BLOOD VESSELS; ENDOTHELIUM, VASCULAR; HUMANS; MEMBRANE PROTEINS; MUSCLE, SMOOTH, VASCULAR; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; VASCULAR DISEASES;

EID: 67649317253     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvp080     Document Type: Review

References (117)

1. Boucheix C, Rubinstein E. Tetraspanins. Cell Mol Life Sci 2001;58:1189-1205.
2. Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 2005;6:801-811.
3. Horejsi V, Vlcek C. Novel structurally distinct family of leucocyte surface glycoproteins including CD9, CD37, CD53 and CD63. FEBS Lett 1991;288:1-4.
4. Maecker HT, Todd SC, Levy S. The tetraspanin superfamily: molecular facilitators. FASEB J 1997;11:428-442.
5. Wright MD, Tomlinson MG. The ins and outs of the transmembrane 4 superfamily. Immunol Today 1994;15:588-594.
6. 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;276:40545-40554.
7. 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;26:2657-2665.
8. Levy S, Shoham T. Protein-protein interactions in the tetraspanin web. Physiology (Bethesda) 2005;20:218-224.
9. Zoller M. Tetraspanins: push and pull in suppressing and promoting metastasis. Nat Rev Cancer 2009;9:40-55.
10. Lazo PA. Functional implications of tetraspanin proteins in cancer biology. Cancer Sci 2007;98:1666-1677.
11. Goschnick MW, Jackson DE. Tetraspanins-structural and signalling scaffolds that regulate platelet function. Mini Rev Med Chem 2007;7:1248-1254.
12. Wright MD, Moseley GW, van Spriel AB. Tetraspanin microdomains in immune cell signalling and malignant disease. Tissue Antigens 2004;64:533-542.
13. Martin F, Roth DM, Jans DA, Pouton CW, Partridge LJ, Monk PN et al. Tetraspanins in viral infections: a fundamental role in viral biology? J Virol 2005;79:10839-10851.
14. Berditchevski F, Odintsova E. Tetraspanins as regulators of protein traf-ficking. Traffic 2007;8:89-96.
15. Liu L, He B, Liu WM, Zhou D, Cox JV, Zhang XA. Tetraspanin CD151 promotes cell migration by regulating integrin trafficking. J Biol Chem 2007;282:31631-31642.
16. Sugiura T, Berditchevski F. Function of alpha3beta1-tetraspanin protein complexes in tumor cell invasion. Evidence for the role of the complexes in production of matrix metalloproteinase 2 (MMP-2). J Cell Biol 1999;146:1375-1389.
17. Saito Y, Tachibana I, Takeda Y, Yamane H, He P, Suzuki M et al. Absence of CD9 enhances adhesion-dependent morphologic differentiation, survival, and matrix metalloproteinase-2 production in small cell lung cancer cells. Cancer Res 2006;66:9557-9565.
18. Arduise C, Abache T, Li L, Billard M, Chabanon A, Ludwig A et al. Tetraspanins regulate ADAM10-mediated cleavage of TNF-alpha and epidermal growth factor. J Immunol 2008;181:7002-7013.
19. Yanez-Mo M, Barreiro O, Gonzalo P, Batista A, Megias D, Genis L et al. MT1-MMP collagenolytic activity is regulated through association with tetraspanin CD151 in primary endothelial cells. Blood 2008;112:3217-3226.
20. Kersey JH, LeBien TW, Abramson CS, Newman R, Sutherland R, Greaves M. P-24: a human leukemia-associated and lymphohemopoietic progenitor cell surface structure identified with monoclonal antibody. J Exp Med 1981;153:726-731.
21. Benoit P, Gross MS, Frachet P, Frezal J, Uzan G, Boucheix C et al. Assignment of the human CD9 gene to chromosome 12 (region P13) by use of human specific DNA probes. Hum Genet 1991;86:268-272.
22. Lanza F, Wolf D, Fox CF, Kieffer N, Seyer JM, Fried VA et al. cDNA cloning and expression of platelet p24/CD9. Evidence for a new family of multiple membrane-spanning proteins. J Biol Chem 1991;266:10638- 10645.
23. Kotha J, Longhurst C, Appling W, Jennings LK. Tetraspanin CD9 regulates beta 1 integrin activation and enhances cell motility to fibronectin via a PI-3 kinase-dependent pathway. Exp Cell Res 2008;314:1811-1822.
24. Boucheix C, Duc GH, Jasmin C, Rubinstein E. Tetraspanins and malignancy. Expert Rev Mol Med 2001;2001:1-17.
25. Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J et al. The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet 2000;24:279-282.
26. Longhurst CM, White MM, Wilkinson DA, Jennings LK. A CD9, alphaIIbbeta3, integrin-associated protein, and GPIb/V/IX complex on the surface of human platelets is influenced by alphaIIbbeta3 conformational states. Eur J Biochem 1999;263:104-111.
27. Rubinstein E, Le Naour F, Billard M, Prenant M, Boucheix C. CD9 antigen is an accessory subunit of the VLA integrin complexes. Eur J Immunol 1994;24:3005-3013.
28. Higashiyama S, Iwamoto R, Goishi K, Raab G, Taniguchi N, Klagsbrun M et al. The membrane protein CD9/DRAP 27 potentiates the juxtacrine growth factor activity of the membrane-anchored heparin-binding EGF-like growth factor. J Cell Biol 1995;128:929-938.
29. De Meyer GR, Bult H. Mechanisms of neointima formation-lessons from experimental models. Vasc Med 1997;2:179-189.
30. Kotha J, Zhang C, Longhurst CM, Lu Y, Jacobs J, Cheng Y et al. Functional relevance of tetraspanin CD9 in vascular smooth muscle cell injury phenotypes: A novel target for the prevention of neointimal hyperplasia. Atherosclerosis 2008; Published online ahead of print on August 8.
31. Scherberich A, Moog S, Haan-Archipoff G, Azorsa DO, Lanza F, Beretz A. Tetraspanin CD9 is associated with very late-acting integrins in human vascular smooth muscle cells and modulates collagen matrix reorganization. Arterioscler Thromb Vasc Biol 1998;18:1691-1697.
32. Lijnen HR, Lupu F, Collen D, Le Naour F, Boucheix C. CD9 gene deficiency does not affect smooth muscle cell migration and neointima formation after vascular injury in mice. Thromb Haemost 2000;83:956-961.
33. Scherberich A, Giannone G, Perennou E, Takeda K, Boucheix C, Rubinstein E et al. FAK-mediated inhibition of vascular smooth muscle cell migration by the tetraspanin CD9. Thromb Haemost 2002;87:1043-1050.
34. Goncharova EA, Ammit AJ, Irani C, Carroll RG, Eszterhas AJ, Panettieri RA et al. PI3K is required for proliferation and migration of human pulmonary vascular smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2002;283:L354-L363.
35. Oudit GY, Sun H, Kerfant BG, Crackower MA, Penninger JM, Backx PH. The role of phosphoinositide-3 kinase and PTEN in cardiovascular physiology and disease. J Mol Cell Cardiol 2004;37:449-471.
36. Deissler H, Kuhn EM, Lang GE, Deissler H. Tetraspanin CD9 is involved in the migration of retinal microvascular endothelial cells. Int J Mol Med 2007;20:643-652.
37. Favaloro EJ. Differential expression of surface antigens on activated endothelium. Immunol Cell Biol 1993;71:571-581.
38. Barreiro O, Yanez-Mo M, Sala-Valdes M, Gutierrez-Lopez MD, Ovalle S, Higginbottom A et al. Endothelial tetraspanin microdomains regulate leukocyte firm adhesion during extravasation. Blood 2005;105:2852- 2861.
39. Klein-Soyer C, Azorsa DO, Cazenave JP, Lanza F. CD9 participates in endothelial cell migration during in vitro wound repair. Arterioscler Thromb Vasc Biol 2000;20:360-369.
40. Erovic BM, Neuchrist C, Kandutsch S, Woegerbauer M, Pammer J. CD9 expression on lymphatic vessels in head and neck mucosa. Mod Pathol 2003;16:1028-1034.
41. Yanez-Mo M, Alfranca A, Cabanas C, Marazuela M, Tejedor R, Ursa MA et al. 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 1998;141:791-804.
42. Ko EM, Lee IY, Cheon IS, Kim J, Choi JS, Hwang JY et al. Monoclonal antibody to CD9 inhibits platelet-induced human endothelial cell proliferation. Mol Cells 2006;22:70-77.
43. Forsyth KD. Anti-CD9 antibodies augment neutrophil adherence to endothelium. Immunology 1991;72:292-296.
44. Longo N, Yanez-Mo M, Mittelbrunn M, de la Rosa G, Munoz ML, Sanchez-Madrid F et al. Regulatory role of tetraspanin CD9 in tumorendothelial cell interaction during transendothelial invasion of melanoma cells. Blood 2001;98:3717-3726.
45. Barreiro O, Zamai M, Yanez-Mo M, Tejera E, Lopez-Romero P, Monk PN et al. Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. J Cell Biol 2008;183:527-542.
46. Ushikoshi HTT, Takemura G, Li Y, Esaki M, Khai NC, Kawai T et al. CD9 gene therapy inhibits cardiac hypertrophy and tachycardia, and attenuates the remodeling after myocardial infarction in mice. Mol Ther 2005;11(Suppl. 1):S359.
47. Hannah MJ, Williams R, Kaur J, Hewlett LJ, Cutler DF. Biogenesis of Weibel-Palade bodies. Semin Cell Dev Biol 2002;13:313-324.
48. Vischer UM, Wagner DD. CD63 is a component of Weibel-Palade bodies of human endothelial cells. Blood 1993;82:1184-1191.
49. Bonfanti R, Furie BC, Furie B, Wagner DD. PADGEM (GMP140) is a component of Weibel-Palade bodies of human endothelial cells. Blood 1989;73:1109-1112.
50. Schnyder-Candrian S, Borsig L, Moser R, Berger EG. Localization of alpha 1,3-fucosyltransferase VI in Weibel-Palade bodies of human endothelial cells. Proc Natl Acad Sci USA 2000;97:8369-8374.
51. Kobayashi T, Vischer UM, Rosnoblet C, Lebrand C, Lindsay M, Parton RG et al. The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol Biol Cell 2000;11:1829-1843.
52. Michaux G, Cutler DF. How to roll an endothelial cigar: the biogenesis of Weibel-Palade bodies. Traffic 2004;5:69-78.
53. Smith DA, Monk PN, Partridge LJ. Antibodies against human CD63 activate transfected rat basophilic leukemia (RBL-2H3) cells. Mol Immunol 1995;32:1339-1344.
54. Toothill VJ, Van Mourik JA, Niewenhuis HK, Metzelaar MJ, Pearson JD. Characterization of the enhanced adhesion of neutrophil leukocytes to thrombin-stimulated endothelial cells. J Immunol 1990;145:283-291.
55. Berditchevski F, Bazzoni G, Hemler ME. Specific association of CD63 with the VLA-3 and VLA-6 integrins. J Biol Chem 1995;270:17784-17790.
56. Skubitz KM, Campbell KD, Iida J, Skubitz AP. CD63 associates with tyrosine kinase activity and CD11/CD18, and transmits an activation signal in neutrophils. J Immunol 1996;157:3617-3626.
57. Mantegazza AR, Barrio MM, Moutel S, Bover L, Weck M, Brossart P et al. CD63 tetraspanin slows down cell migration and translocates to the endosomal-lysosomal-MIICs route after extracellular stimuli in human immature dendritic cells. Blood 2004;104:1183-1190.
58. Radford KJ, Thorne RF, Hersey P. Regulation of tumor cell motility and migration by CD63 in a human melanoma cell line. J Immunol 1997;158:3353-3358.
59. Kitani S, Berenstein E, Mergenhagen S, Tempst P, Siraganian RP. A cell surface glycoprotein of rat basophilic leukemia cells close to the high affinity IgE receptor (Fc epsilon RI). Similarity to human melanoma differentiation antigen ME491. J Biol Chem 1991;266:1903-1909.
60. Carmo AM, Wright MD. Association of the transmembrane 4 superfamily molecule CD53 with a tyrosine phosphatase activity. Eur J Immunol 1995;25:2090-2095.
61. Iida J, Skubitz AP, McCarthy JB, Skubitz KM. Protein kinase activity is associated with CD63 in melanoma cells. J Transl Med 2005;3:42.
62. Lin D, Kamsteeg EJ, Zhang Y, Jin Y, Sterling H, Yue P et al. Expression of tetraspan protein CD63 activates protein-tyrosine kinase (PTK) and enhances the PTK-induced inhibition of ROMK channels. J Biol Chem 2008;283:7674-7681.
63. Latysheva N, Muratov G, Rajesh S, Padgett M, Hotchin NA, Overduin M 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 Biol 2006;26:7707-7718.
64. Takino T, Miyamori H, Kawaguchi N, Uekita T, Seiki M, Sato H. Tetraspanin CD63 promotes targeting and lysosomal proteolysis of membranetype 1 matrix metalloproteinase. Biochem Biophys Res Commun 2003;304:160-166.
65. Jung KK, Liu XW, Chirco R, Fridman R, Kim HR. Identification of CD63 as a tissue inhibitor of metalloproteinase-1 interacting cell surface protein. EMBO J 2006;25:3934-3942.
66. Duffield A, Kamsteeg EJ, Brown AN, Pagel P, Caplan MJ. The tetraspanin CD63 enhances the internalization of the H,K-ATPase beta-subunit. Proc Natl Acad Sci USA 2003;100:15560-15565.
67. Fitter S, Seldin MF, Ashman LK. Characterisation of the mouse homologue of CD151 (PETA-3/SFA-1); genomic structure, chromosomal localisation and identification of 2 novel splice forms. Biochim Biophys Acta 1998;1398:75-85.
68. Fitter S, Tetaz TJ, Berndt MC, Ashman LK. Molecular cloning of cDNA encoding a novel platelet-endothelial cell tetra-span antigen, PETA-3. Blood 1995;86:1348-1355.
69. Geary SM, Cambareri AC, Sincock PM, Fitter S, Ashman LK. Differential tissue expression of epitopes of the tetraspanin CD151 recognised by monoclonal antibodies. Tissue Antigens 2001;58:141-153.
70. Berditchevski F, Gilbert E, Griffiths MR, Fitter S, Ashman L, Jenner SJ. Analysis of the CD151-alpha3beta1 integrin and CD151-tetraspanin interactions by mutagenesis. J Biol Chem 2001;276:41165-41174.
71. Sterk LM, Geuijen CA, van den Berg JG, Claessen N, Weening JJ, Sonnenberg A. Association of the tetraspanin CD151 with the laminin-binding integrins alpha3beta1, alpha6beta1, alpha6beta4 and alpha7-beta1 in cells in culture and in vivo. J Cell Sci 2002;115:1161-1173.
72. 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;275:9230-9238.
73. Gesierich S, Paret C, Hildebrand D, Weitz J, Zgraggen K, Schmitz-Winnenthal FH et al. Colocalization of the tetraspanins, CO-029 and CD151, with integrins in human pancreatic adenocarcinoma: impact on cell motility. Clin Cancer Res 2005;11:2840-2852.
74. Testa JE, Brooks PC, Lin JM, Quigley JP. 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 1999;59:3812-3820.
75. Winterwood NE, Varzavand A, Meland MN, Ashman LK, Stipp CS. A critical role for tetraspanin CD151 in alpha3beta1 and alpha6beta4 integrin-dependent tumor cell functions on laminin-5. Mol Biol Cell 2006;17:2707- 2721.
76. Chattopadhyay N, Wang Z, Ashman LK, Brady-Kalnay SM, Kreidberg JA. Alpha3beta1 integrin-CD151, a component of the cadherin-catenin complex, regulates PTPmu expression and cell-cell adhesion. J Cell Biol 2003;163:1351-1362.
77. 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;163:165-176.
78. 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 alpha6beta4 and may regulate the spatial organization of hemidesmosomes. J Cell Biol 2000;149:969-982.
79. Lammerding J, Kazarov AR, Huang H, Lee RT, Hemler ME. Tetraspanin CD151 regulates alpha6beta1 integrin adhesion strengthening. Proc Natl Acad Sci USA 2003;100:7616-7621.
80. Zijlstra A, Lewis J, Degryse B, Stuhlmann H, Quigley JP. The inhibition of tumor cell intravasation and subsequent metastasis via regulation of in vivo tumor cell motility by the tetraspanin CD151. Cancer Cell 2008;13:221-234.
81. Yang J, Liu Z, Shen X, Yao W, Qu H, Yang M et al. Expression of CD151 in human atherosclerotic artery and its implication. J Huazhong Univ Sci Technolog Med Sci 2005;25:629-631.
82. Sincock PM, Fitter S, Parton RG, Berndt MC, Gamble JR, Ashman LK. 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 1999;112:833-844.
83. Takeda Y, Kazarov AR, Butterfield CE, Hopkins BD, Benjamin LE, Kaipainen A et al. Deletion of tetraspanin Cd151 results in decreased pathologic angiogenesis in vivo and in vitro. Blood 2007;109:1524-1532.
84. Zhang XA, Kazarov AR, Yang X, Bontrager AL, Stipp CS, Hemler ME. Function of the tetraspanin CD151-alpha6beta1 integrin complex during cellular morphogenesis. Mol Biol Cell 2002;13:1-11.
85. Zheng Z, Liu Z. CD151 gene delivery activates PI3K/Akt pathway and promotes neovascularization after myocardial infarction in rats. Mol Med 2006;12:214-220.
86. Nishiuchi R, Sanzen N, Nada S, Sumida Y, Wada Y, Okada M et al. Potentiation of the ligand-binding activity of integrin alpha3beta1 via association with tetraspanin CD151. Proc Natl Acad Sci USA 2005;102:1939-1944.
87. Fitter S, Sincock PM, Jolliffe CN, Ashman LK. Transmembrane 4 superfamily protein CD151 (PETA-3) associates with beta 1 and alpha IIb beta 3 integrins in haemopoietic cell lines and modulates cell-cell adhesion. Biochem J 1999;338:61-70.
88. Sincock PM, Mayrhofer G, Ashman LK. Localization of the transmembrane 4 superfamily (TM4SF) member PETA-3 (CD151) in normal human tissues: comparison with CD9, CD63, and alpha5beta1 integrin. J Histochem Cytochem 1997;45:515-525.
89. Karamatic Crew V, Burton N, Kagan A, Green CA, Levene C, Flinter F 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;104:2217-2223.
90. 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;126:680-689.
91. Lau LM, Wee JL, Wright MD, Moseley GW, Hogarth PM, Ashman LK et al. The tetraspanin superfamily member CD151 regulates outside-in integrin alphaIIbbeta3 signaling and platelet function. Blood 2004;104: 2368-2375.
92. Wright MD, Geary SM, Fitter S, Moseley GW, Lau LM, Sheng KC et al. Characterization of mice lacking the tetraspanin superfamily member CD151. Mol Cell Biol 2004;24:5978-5988.
93. Hasegawa H, Nomura T, Kishimoto K, Yanagisawa K, Fujita S. SFA-1/PETA-3 (CD151), a member of the transmembrane 4 superfamily, associates preferentially with alpha 5 beta 1 integrin and regulates adhesion of human T cell leukemia virus type 1-infected T cells to fibronectin. J Immunol 1998;161:3087-3095.
94. Hasegawa H, Utsunomiya Y, Kishimoto K, Yanagisawa K, Fujita S. 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 1996;70:3258-3263.
95. Ho SH, Martin F, Higginbottom A, Partridge LJ, Parthasarathy V, Moseley GW et al. Recombinant extracellular domains of tetraspanin proteins are potent inhibitors of the infection of macrophages by human immunodeficiency virus type 1. J Virol 2006;80:6487-6496.
96. Protty MB, Watkins NA, Colombo D, Thomas SG, Heath VL, Herbert J et al. Identification of Tspan9 as a novel platelet tetraspanin and the collagen receptor GPVI as a component of tetraspanin microdomains. Biochem J 2009;417:391-400.
97. Miller JL, Kupinski JM, Hustad KO. Characterization of a platelet membrane protein of low molecular weight associated with platelet activation following binding by monoclonal antibody AG-1. Blood 1986;68:743- 751.
98. Miao WM, Vasile E, Lane WS, Lawler J. CD36 associates with CD9 and integrins on human blood platelets. Blood 2001;97:1689-1696.
99. Israels SJ, McMillan-Ward EM. CD63 modulates spreading and tyrosine phosphorylation of platelets on immobilized fibrinogen. Thromb Haemost 2005;93:311-318.
100. Jennings LK, Fox CF, Kouns WC, McKay CP, Ballou LR, Schultz HE. The activation of human platelets mediated by anti-human platelet p24/CD9 monoclonal antibodies. J Biol Chem 1990;265:3815-3822.
101. Rubinstein E, Boucheix C, Worthington RE, Carroll RC. Anti-platelet antibody interactions with Fc gamma receptor. Semin Thromb Hemost 1995;21:10-22.
102. Worthington RE, Carroll RC, Boucheix C. Platelet activation by CD9 monoclonal antibodies is mediated by the Fc gamma II receptor. Br J Haematol 1990;74:216-222.
103. Carroll RC, Worthington RE, Boucheix C. Stimulus-response coupling in human platelets activated by monoclonal antibodies to the CD9 antigen, a 24 kDa surface-membrane glycoprotein. Biochem J 1990;266:527-535.
104. Griffith L, Slupsky J, Seehafer J, Boshkov L, Shaw AR. Platelet activation by immobilized monoclonal antibody: evidence for a CD9 proximal signal. Blood 1991;78:1753-1759.
105. Hill SK. The tetraspanin CD9 localizes to platelet-platelet contacts and regulates thrombus stability. PhD Thesis, University of Tennessee Health Science Center, Memphis.
106. Brisson C, Azorsa DO, Jennings LK, Moog S, Cazenave JP, Lanza F. Co-localization of CD9 and GPIIb-IIIa (alpha IIb beta 3 integrin) on activated platelet pseudopods and alpha-granule membranes. Histochem J 1997;29:153-165.
107. Hamamoto K, Ohga S, Nomura S, Yasunaga K. Cellular distribution of CD63 antigen in platelets and in three megakaryocytic cell lines. Histochem J 1994;26:367-375.
108. Nishibori M, Cham B, McNicol A, Shalev A, Jain N, Gerrard JM. The protein CD63 is in platelet dense granules, is deficient in a patient with Hermansky-Pudlak syndrome, and appears identical to granulophysin. J Clin Invest 1993;91:1775-1782.
109. Israels SJ, McMillan-Ward EM, Easton J, Robertson C, McNicol A. CD63 associates with the alphaIIb beta3 integrin-CD9 complex on the surface of activated platelets. Thromb Haemost 2001;85:134-141.
110. Israels SJ, McMillan-Ward EM. Platelet tetraspanin complexes and their association with lipid rafts. Thromb Haemost 2007;98:1081-1087.
111. Schroder JL-RR, Himmerkus N, Pleines I, Nieswandt B, Orinska Z, Koch-Nolte F et al. Deficiency of the tetraspanin CD63 associated with kidney pathology but normal lysosomal function. Mol Cell Biol 2009;29:1083-1094.
112. Ashman LK, Aylett GW, Mehrabani PA, Bendall LJ, Niutta S, Cambareri AC et al. The murine monoclonal antibody, 14A2.H1, identifies a novel platelet surface antigen. Br J Haematol 1991;79:263-270.
113. Goschnick MW, Lau LM, Wee JL, Liu YS, Hogarth PM, Robb LM et al. Impaired 'outside-in' integrin alphaIIbbeta3 signaling and thrombus stability in TSSC6-deficient mice. Blood 2006;108:1911-1918.
114. Garcia-Espana A, Chung PJ, Sarkar IN, Stiner E, Sun TT, Desalle R. Appearance of new tetraspanin genes during vertebrate evolution. Genomics 2008;91:326-334.
115. Huang S, Yuan S, Dong M, Su J, Yu C, Shen Y et al. The phylogenetic analysis of tetraspanins projects the evolution of cell-cell interactions from unicellular to multicellular organisms. Genomics 2005;86:674-684.
116. Clergeot PH, Gourgues M, Cots J, Laurans F, Latorse MP, Pepin R et al. PLS1, a gene encoding a tetraspanin-like protein, is required for penetration of rice leaf by the fungal pathogen Magnaporthe grisea. Proc Natl Acad Sci USA 2001;98:6963-6968.
117. Kaji K, Oda S, Miyazaki S, Kudo A. Infertility of CD9-deficient mouse eggs is reversed by mouse CD9, human CD9, or mouse CD81; polyadenylated mRNA injection developed for molecular analysis of sperm-egg fusion. Dev Biol 2002;247:327-334.