Signal transduction pathways mediated by PECAM-1: New roles for an old molecule in platelet and vascular cell biology

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 23, Issue 6, 2003, Pages 953-964

  Newman, Peter J ^a,b   Newman, Debra K ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b BLOOD RESEARCH INSTITUTE   (United States)

Author keywords

Alternative splicing; ITIM; PECAM 1; SHP 2; Signal transduction

Indexed keywords

CD31 ANTIGEN; INTEGRIN; PROTEIN TYROSINE KINASE;

CELL DEATH; CELL SURVIVAL; CYTOLOGY; HUMAN; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; THROMBOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD31; APOPTOSIS; ENDOTHELIUM, VASCULAR; HUMANS; INTEGRINS; MICE; MICE, KNOCKOUT; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PLATELET ACTIVATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0038120892     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000071347.69358.D9     Document Type: Review

References (115)

1. van Mourik JA, Leeksma OC, Reinders JH, de Groot PG, Zandbergen-Spaargaren J. Vascular endothelial cells synthesize a plasma membrane protein indistinguishable from platelet membrane glycoprotein IIa. J Biol Chem. 1985;260:11300-11306.
2. Ohto H, Maeda H, Shibata Y, Chen R-F, Qzaki Y, Higashihara M. Takeuchi A, Tohyama H. A novel leukocyte differentiation antigen: two monoclonal antibodies TM2 and TM3 define a 120-kd molecule present on neutrophils, monocytes, platelets, and activated lymphoblasts. Blood. 1985;66:873-881.
3. Goyert SM, Ferrero EM, Seremetis SV, Winchester RJ, Silver J, Mattison AC. Biochemistry and expression of myelomonocytic antigens. J Immunol. 1986;137:3909-3914.
4. McMichael AJ. White Cell Differentiation Antigens. Oxford: Oxford University Press; 1987.
5. Favaloro EJ, Moraitis N, Koutts J, Exner T, Bradstock KF. Endothelial cells and normal circulating haemopoietic cells share a number of surface antigens. Thromb Haemost. 1989;61:217-224.
6. Newman PJ, Berndt MC, Gorski J, White GC, Lyman S, Paddock C, Muller WA. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science. 1990;247:1219-1222.
7. Simmons DL, Walker C, Power C, Pigott R. Molecular cloning of CD31, a putative intercellular adhesion molecule closely related to carcinoembryonic antigen. J Exp Med. 1990;171:2147-2152.
8. Stockinger H, Gadd SJ, Eher R, Majdic O, Schreiber W, Kasinrerk W, Strass B, Schnabl E, Knapp W. Molecular characterization and functional analysis of the leukocyte surface protein CD31. J Immunol. 1990;145:3889-3897.
9. Horak ER, Leek R, Klenk N, LeJeune S, Smith K, Stuart N, Greenall M, Stepniewska K, Harris AL. Angiogenesis, assessed by platelet/endothelial cell adhesion molecule antibodies, as indicator of node metastases and survival in breast cancer. Lancet. 1992;340:1120-1124.
10. DeLisser HM, Baldwin HS, Albelda SM. Platelet endothelial cell adhesion molecule 1 (PECAM-1/CD31): a multifunctional vascular cell adhesion molecule. Trends Cardiovasc Med. 1997;7:203-210.
11. Newman PJ. The biology of PECAM-1. J Clin Invest. 1997;99:3-8.
12. Sun Q-H, DeLisser HM, Zukowski MM, Paddock C, Albelda SM, Newman PJ. Individually distinct Ig homology domains in PECAM-1 regulate homophilic binding and modulate receptor affinity. J Biol Chem. 1996;271:11090-11098.
13. Sun J, Williams J, Yan H-C, Amin KM, Albelda SM, DeLisser HM. Platelet endothelial cell adhesion molecule-1 (PECAM-1) homophilic adhesion is mediated by immunoglobulin-like domains 1 and 2 and depends on the cytoplasmic domain and the level of surface expression. J Biol Chem. 1996;271:18561-18570.
14. Newton JP, Buckley CD, Jones EY, Simmons DL. Residues on both faces of the first immunoglobulin fold contribute to homophilic binding sites on PECAM-1/CD31. J Biol Chem. 1997;272:20555-20563.
15. Vaporciyan AA, DeLisser HM, Yan H-C, Mendiguren II, Thom SR. Jones ML, Ward PA, Albelda SM. Involvement of platelet endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science. 1993;262:1580-1582.
16. Muller WA, Weigl SA, Deng X, Phillips DM. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med. 1993;178:449-460.
17. Bogen S, Pak J, Garifallou M, Deng X, Muller WA. Monoclonal antibody to murine PECAM-1 (CD31) blocks acute inflammation in vivo. J Exp Med. 1994;179:1059-1064.
18. Liao F, Huynh HK, Eiroa A, Greene T, Polizzi E, Muller WA. Migration of monocytes across endothelium and passage through extracellular matrix involve separate molecular domains of PECAM-1. J Exp Med. 1995;182:1337-1343.
19. Yong KL, Watts M, Shaun TN, Sullivan A, Ings S, Linch DC. Transmigration of CD34+ cells across specialized and nonspecialized endothelium requires prior activation by growth factors and is mediated by PECAM-1 (CD31). Blood. 1998;91:1196-1205.
20. Treutiger CJ, Heddini A, Fernandez V, Muller WA, Wahlgren M. PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nat Med. 1997;3:1405-1408.
21. Zhou Z, Christofidou-Solomidou M, Garlanda C, DeLisser HM. Antibody against murine PECAM-1 inhibits tumor angiogenesis in mice. Angiogenesis. 1999;3:181-188.
22. Kirschbaum NE, Gumina RJ, Newman PJ. Organization of the gene for human platelet/endothelial cell adhesion molecule-1 (PECAM-1) reveals alternatively spliced isoforms and a functionally complex cytoplasmic domain. Blood. 1994;84:4028-4037.
23. Goldberger A, Middleton KA, Oliver JA, Paddock C, Yan H-C, DeLisser HM, Albelda SM, Newman PJ. Biosynthesis and processing of the cell adhesion molecule PECAM-1 includes production of a soluble form. J Biol Chem. 1994;269:17183-17191.
24. Newman PJ, Doers MP, Gorski J. Molecular cloning of a 130 kD membrane glycoprotein expressed on human platelets, umbilical vein endothelial cells, and human erythroleukemia (HEL) cells. J Cell Biol. 105;53a:1987.
25. Baldwin HS, Shen HM, Yan H-C, DeLisser HM, Chung A, Mickanin C, Trask T, Kirschbaum N, Newman PJ, Albelda SM, Buck CA. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during early mammalian cardiovascular development. Development. 1994;120:2539-2553.
26. Yan H-C, Baldwin HS, Sun J, Buck CA, Albelda SM, DeLisser HM. Alternative splicing of a specific cytoplasmic exon alters the binding characteristics of murine platelet/endothelial cell adhesion molecule-1 (PECAM-1). J Biol Chem. 1995;270:23672-23680.
27. Sheibani N, Sorenson CM, Frazier WA. Tissue specific expression of alternatively spliced murine PECAM-1 isoforms. Dev Dyn. 1999;214:44-54.
28. Aroca F, Renaud W, Bartoli C, Bouvier-Labit C, Figarella-Branger D. Expression of PECAM-1/CD31 isoforms in human brain gliomas. J Neurooncol. 1999;43:19-25.
29. Robson P, Stein P, Zhou B, Schultz RM, Baldwin HS. Inner cell mass-specific expression of a cell adhesion molecule (PECAM-1/CD31) in the mouse blastocyst. Dev Biol. 2001;234:317-329.
30. Wang Y, Su X, Sorenson CM, Sheibani N. The tissue specific distribution of alternatively spliced human PECAM-1 isoforms. Am J Physiol Heart Circ Physiol. 2003;284:H1008-H1017.
31. Wang Y, Sheibani N. Expression pattern of alternatively spliced PECAM-1 isoforms in hematopoietic cells and platelets. J Cell Biochem. 2002;87:424-438.
32. c-src. Biochem J. 1994;299:613-621.
33. Lu TT, Yan LG, Madri JA. Integrin engagement mediates tyrosine dephosphorylation on platelet-endothelial cell adhesion molecule 1. Proc Natl Acad Sci U S A. 1996:93:11808-11813.
34. Cicmil M, Thomas JM, Sage T, Barry FA, Leduc M, Bon C, Gibbins JM. Collagen, convulxin, and thrombin stimulate aggregation-independent tyrosine phosphorylation of CD31 in platelets: evidence for the involvement of Src family kinases. J Biol Chem. 2000;275:27339-27347.
35. Ohmori T, Yatomi Y, Wu Y, Osada M, Satoh K, Ozaki Y. Wheat germ agglutinin-induced platelet activation via platelet endothelial cell adhesion molecule-1: involvement of rapid phospholipase C gamma 2 activation by Src family kinases. Biochemistry. 2001;40:12992-13001.
36. Jones KL, Hughan SC, Dopheide SM, Farndale RW, Jackson SP, Jackson DE. Platelet endothelial cell adhesion molecule-1 is a negative regulator of platelet-collagen interactions. Blood. 2001;98:1456-1463.
37. Jackson DE, Ward CM, Wang R, Newman PJ. The protein-tyrosine phosphatase SHP-2 binds PECAM-1 and forms a distinct signaling complex during platelet aggregation: evidence for a mechanistic link between PECAM-1 and integrin-mediated cellular signaling. J Biol Chem. 1997;272:6986-6993.
38. Edmead CE, Crosby DA, Southcott M, Poole AW. Thrombin-induced association of SHP-2 with multiple tyrosine-phosphorylated proteins in human platelets. FEBS Lett. 1999;459:27-32.
39. Varon D, Jackson DE, Shenkman B, Dardik R, Tamarin I, Savion N, Newman PJ. Platelet/endothelial cell adhesion molecule-1 serves as a co-stimulatory agonist receptor that modulates integrin-dependent adhesion and aggregation of human platelets. Blood. 1998;91:500-507.
40. Cicmil M, Thomas JM, Leduc M, Bon C, Gibbins JM. Platelet endothelial cell adhesion molecule-1 signaling inhibits the activation of human platelets. Blood. 2002;99:137-144.
41. Osawa M, Masuda M, Kusano K, Fujiwara K. Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J Cell Biol. 2002;158:773-785.
42. Bird IN, Taylor V, Newton JP, Spragg JH, Simmons DL, Salmon M, Buckley CD. Homophilic PECAM-1(CD31) interactions prevent endothelial cell apoptosis but do not support cell spreading or migration. J Cell Sci. 1999;112:1989-1997.
43. Osawa M, Masuda M, Harada N, Lopes RB, Fujiwara K. Tyrosine phosphorylation of platelet endothelial cell adhesion molecule-1 (PECAM-1, CD31) in mechanically stimulated vascular endothelial cells. Eur J Cell Biol. 1997;72:229-237.
44. Harada N, Masuda M, Fujiwara K. Fluid flow and osmotic stress induce tyrosine phosphorylation of an endothelial cell 128 kDa surface glycoprotein. Biochem Biophys Res Commun. 1995;214:69-74.
45. Newton-Nash DK, Newman PJ, A new role for platelet-endothelial cell adhesion molecule-1 (CD31): Inhibition of TCR-mediated signal transduction. J Immunol. 1999;163:682-688.
46. Sagawa K, Kimura T, Swieter M, Siraganian RP. The protein-tyrosine phosphatase SHP-2 associates with tyrosine-phosphorylated adhesion molecule PECAM-1 (CD31). J Biol Chem. 1997;272:31086-31091.
47. Sagawa K, Swaim W, Zhang J, Unsworth E, Siraganian RP. Aggregation of the high affinity IgE receptor results in the tyrosine phosphorylation of the surface adhesion protein PECAM-1 (CD31). J Biol Chem. 1997;272:13412-13418.
48. Masuda M, Osawa M, Shigematsu H, Harada N, Fujiwara K. Platelet endothelial cell adhesion molecule-1 is a major SH-PTP2 binding protein in vascular endothelial cells. FEBS Lett. 1997;408:331-336.
49. Lu TT, Barreuther M, Davis S, Madri JA. Platelet endothelial cell adhesion molecule-1 is phosphorylatable by c-Src, binds Src-Src homology 2 domain, and exhibits immunoreceptor tyrosine-based activation motif-like properties. J Biol Chem. 1997;272:14442-14446.
50. Cao MY, Huber M, Beauchemin N, Famiglietti J, Albelda SM, Veillette A. Regulation of mouse PECAM-1 tyrosine phosphorylation by the Src and Csk families of protein-tyrosine kinases. J Biol Chem. 1998;273:15765-15772.
51. lck. Blood. 2001;97:2351-2357.
52. Xie Y, Muller WA. Molecular cloning and adhesive properties of murine platelet/endothelial cell adhesion molecule 1. Proc Natl Acad Sci U S A. 1993;90:5569-5573.
53. Stewart RJ, Kashour TS, Marsden PA. Vascular endothelial platelet endothelial adhesion molecule-1 (PECAM-1) expression is decreased by TNF-alpha and IFN-gamma: evidence for cytokine-induced destabilization of messenger ribonucleic acid transcripts in bovine endothelial cells. J Immunol. 1996;156:1221-1228.
54. Jackson DE, Kupcho KR, Newman PJ. Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of platelet/endothelial cell adhesion molecule-1 (PECAM-1) that are required for the cellular association and activation of the protein-tyrosine phosphatase, SHP-2. J Biol Chem. 1997;272:24868-24875.
55. Newman PJ. Switched at birth: a new family for PECAM-1. J Clin Invest. 1999;103:5-9.
56. Newman DK, Hoffman S, Kotamraju S, Zhao T, Wakim B, Kalyanaraman B, Newman PJ. Nitration of PECAM-1 ITIM tyrosines abrogates phosphorylation and SHP-2 binding. Biochem Biophys Res Commun. 2002;296:1171-1179.
57. Hua CT, Gamble JR, Vadas MA, Jackson DE. Recruitment and activation of SHP-1 protein-tyrosine phosphatase by human platelet endothelial cell adhesion molecule-1 (PECAM-1). J Biol Chem. 1998;273:28332-28340.
58. Pumphrey NJ, Taylor V, Freeman S, Douglas MR, Bradfield PF, Young SP, Lord JM, Wakelam MJ, Bird IN, Salmon M, Buckley CD. Differential association of cytoplasmic signalling molecules SHP-1, SHP-2, SHIP and phospholipase C-gamma1 with PECAM-1/CD31. FEBS Lett. 1999;450:77-83.
59. Henshall TL, Jones KL, Wilkinson R, Jackson DE. Src homology 2 domain-containing protein-tyrosine phosphatases, SHP-1 and SHP-2, are required for platelet endothelial cell adhesion molecule-1/CD31-mediated inhibitory signaling. J Immunol. 2001;166:3098-3106.
60. Cochrane D, Webster C, Masih G, McCafferty J. Identification of natural ligands for SH2 domains from a phage display cDNA library. J Mol Biol. 2000;297:89-97.
61. Shlapatska LM, Mikhalap SV, Berdova AG, Zelensky OM, Yun TJ, Nichols KE, Clark EA, Sidorenko SP. CD150 association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A. J Immunol. 2001;166:5480-5487.
62. Poy F, Yaffe MB, Sayos J, Saxena K, Morra M, Sumegi J, Cantley LC, Terhorst C, Eck MJ. Crystal structures of the XLP protein SAP reveal a class of SH2 domains with extended, phosphotyrosine-independent sequence recognition. Mol Cell. 1999;4:555-561.
63. Ilan N, Cheung L, Miller S, Mohsenin A, Tucker A, Madri JA. Pecam-1 is a modulator of stat family member phosphorylation and localization: lessons from a transgenic mouse. Dev Biol. 2001;232:219-232.
64. Pellegatta F, Chierchia SL, Zocchi MR. Functional association of platelet endothelial cell adhesion molecule-1 and phosphoinositide 3-kinase in human neutrophils. J Biol Chem. 1998;273:27768-27771.
65. Li W, Nishimura R, Kashishian A, Batzer AG, Kim WJH, Cooper JA, Schlessinger J. A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol Cell Biol. 1994;14:509-517.
66. Bennett AM, Tang TL, Sugimoto S, Walsh CT, Neel BG. Protein-tyrosine-phosphatase SHPTP2 couples platelet-derived growth factor receptor β to Ras. Proc Natl Acad Sci U S A. 1994;91:7335-7339.
67. Cunnick JM, Dorsey JF, Munoz-Antonia T, Mei L, Wu J. Requirement of SHP2 binding to Grb2-associated binder-1 for mitogen-activated protein kinase activation in response to lysophosphatidic acid and epidermal growth factor. J Biol Chem. 2000;275:13842-13848.
68. Zehnder JL, Hirai K, Shatsky M, McGregor JL, Levitt LJ, Leung LLK. The cell adhesion molecule CD31 is phosphorylated after cell activation: down-regulation of CD31 in activated T lymphocytes. J Biol Chem. 1992;267:5243-5249.
69. Newman PJ, Hillery CA, Albrecht R, Parise LV, Berndt MC, Mazurov AV, Dunlop LC, Zhang J, Rittenhouse SE. Activation-dependent changes in human platelet PECAM-1: phosphorylation, cytoskeletal association, and surface membrane redistribution. J Cell Biol. 1992;119:239-246.
70. Rattan V, Shen Y, Sultana C, Kumar D, Kalra VK. Glucose-induced transmigration of monocytes is linked to phosphorylation of PECAM-1 in cultured endothelial cells. Am J Physiol. 1996;271:E711-E717.
71. Sultana C, Shen Y, Johnson C, Kalra VK. Cobalt chloride-induced signaling in endothelium leading to the augmented adherence of sickle red blood cells and transendothelial migration of monocyte-like HL-60 cells is blocked by PAF-receptor antagonist. J Cell Physiol. 1999;179:67-78.
72. Lastres P, Almendro N, Bellon T, Lopez-Guerrero JA, Eritja R, Bernabeu C. Functional regulation of platelet/endothelial cell adhesion molecule-1 by TGF-β1 in promonocytic U-937 cells. J Immunol. 1994;153:4206-4218.
73. Ilan N, Cheung L, Pinter E, Madri JA. Platelet-endothelial cell adhesion molecule-1 (CD31), a scaffolding molecule for selected catenin family members whose binding is mediated by different tyrosine and serine/threonine phosphorylation. J Biol Chem. 2000;275:21435-21443.
74. Ayalon O, Sabanai H, Lampugnani MG, Dejana E, Geiger B. Spatial and temporal relationships between cadherins and PECAM-1 in cell-cell junctions of human endothelial cells. J Cell Biol. 1994;126:247-258.
75. Poggi A, Panzeri MC, Moretta L, Zocchi MR. CD31-triggered rearrangement of the actin cytoskeleton in human natural killer cells. Eur J Immunol. 1996;26:817-824.
76. Matsumura T, Wolff K, Petzelbauer P. Endothelial cell tube formation depends on cadherin 5 and CD31 interactions with filamentous actin. J Immunol. 1997;158:3408-3416.
77. Lampugnani MG, Corada M, Caveda L, Breviario F, Ayalon O, Geiger B, Dejana E. The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin). J Cell Biol. 1995;129:203-217.
78. Sheibani N, Newman PJ, Frazier WA. Thrombospondin-1, a natural inhibitor of angiogenesis, regulates Platelet-Endothelial Cell Adhesion Molecule-1 expression and endothelial cell morphogenesis. Mol Biol Cell. 1997;8:1329-1341.
79. Ilan N, Mahooti S, Rimm DL, Madri JA. PECAM-1 (CD31) functions as a reservoir for and a modulator of tyrosine-phosphorylated β-catenin. J Cell Sci. 1999;112:3005-3014.
80. Ravetch JV, Lanier LL. Immune inhibitory receptors. Science. 2000;290:84-89.
81. Stein-Gerlach M, Wallasch C, Ullrich A. SHP-2, SH2-containing protein tyrosine phosphatase-2. Int J Biochem Cell Biol. 1998;30:559-566.
82. Watson SP, Gibbins J. Collagen receptor signalling in platelets: extending the role of the ITAM. Immunol Today. 1998;19:260-264.
83. Wu XW, Lian EC. Binding properties and inhibition of platelet aggregation by a monoclonal antibody to CD31 (PECAM-1). Arterioscler Thromb Vasc Biol. 1997;17:3154-3158.
84. Wilkinson R, Lyons AB, Roberts D, Wong MX, Bartley PA, Jackson DE. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) acts as a regulator of B-cell development, B-cell antigen receptor (BCR)-mediated activation, and autoimmune disease. Blood. 2002;100:184-193.
85. Wong MX, Roberts D, Bartley PA, Jackson DE. Absence of platelet endothelial cell adhesion molecule-1 (CD31) leads to increased severity of local and systemic IgE-mediated anaphylaxis and modulation of mast cell activation. J Immunol. 2002;168:6455-6462.
86. Patil S, Newman DK, Newman PJ. Platelet endothelial cell adhesion molecule-1 serves as an inhibitory receptor that modulates platelet responses to collagen. Blood. 2001;97:1727-1732.
87. Duncan GS, Andrew DP, Takimoto H, Kaufman SA, Yoshida H, Spellberg J, Luis de la Pompa J, Elia A, Wakeham A, Karan-Tamir B, Muller WA, Senaldi G, Zukowski MM, Mak TW. Genetic evidence for functional redundancy of platelet/endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. J Immunol. 1999;162:3022-3030.
88. Vollmar B, Schmits R, Kunz D, Menger MD. Lack of in vivo function of CD31 in vascular thrombosis. Thromb Haemost. 2001;85:160-164.
89. Rosenblum WI, Murata S, Nelson GH, Werner PK, Ranken R, Harmon RC. Anti-CD31 delays platelet adhesion/aggregation at sites of endothelial injury in mouse cerebral arterioles. Am J Clin Pathol. 1994;145:33-36.
90. Rosenblum WI, Nelson GH, Wormley B, Werner P, Wang J, Shih CC-Y. Role of Platelet-endothelial cell adhesion molecule (PECAM) in platelet adhesion/aggregation over injured but not denuded endothelium in vivo and ex vivo. Stroke. 1996;27:709-711.
91. Bennett AM, Hausdorff SF, O'Reilly AM, Freeman RM, Neel BG. Multiple requirements for SHPTP2 in epidermal growth factor-mediated cell cycle progression. Mol Cell Biol. 1996;16:1189-1202.
92. Tanaka Y, Albelda SM, Horgan KJ, Van Seventer GA, Shimizu Y, Newman W, Hallam J, Newman PJ, Buck CA, Shaw S. CD31 expressed on distinctive T cell subsets is a preferential amplifier of β1 integrinmediated adhesion. J Exp Med. 1992;176:245-253.
93. + hemopoietic progenitor cells. J Immunol. 1994;153:4673-4683.
94. Piali L, Albelda SM, Baldwin HS, Hammel P, Gisler RH, Imhof BA. Murine platelet endothelial cell adhesion molecule (PECAM-1/CD31) modulates β2 integrins on lymphokine-activated killer cells. Eur J Immunol. 1993;23:2464-2471.
95. Berman ME, Muller WA. Ligation of Platelet/endothelial cell adhesion molecule 1 (PECAM-1/CD31) on monocytes and neutrophils increases binding capacity of leukocyte CR3 (CD11b/CD18). J Immunol. 1995;154:299-307.
96. 2 integrin activation. J Immunol. 1996;156:1515-1524.
97. Chiba R, Nakagawa N, Kurasawa K, Tanaka Y, Saito Y, Iwamoto I. Ligation of CD31 (PECAM-1) on endothelial cells increases adhesive function of αvβ3 integrin and enhances β1 integrin-mediated adhesion of eosinophils to endothelial cells. Blood. 1999;94:1319-1329.
98. Reedquist KA, Ross E, Koop EA, Wolthuis RM, Zwartkruis FJ, Kooyk YV, Salmon M, Buckley CD, Bos JL. The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J Cell Biol. 2000;148:1151-1158.
99. Zhao T, Newman PJ. Integrin activation by regulated dimerization and oligomerization of platelet endothelial cell adhesion molecule (PECAM)-1 from within the cell. J Cell Biol. 2001;152:65-73.
100. Bertoni A, Tadokoro S, Eto K, Pampori N, Parise LV, White GC, Shattil SJ. Relationships between Rap1b, affinity modulation of integrin αIIbβ3, and the actin cytoskeleton. J Biol Chem. 2002;277:25715-25721.
101. Eto K, Murphy R, Kerrigan SW, Bertom A, Stuhlmann H, Nakano T, Leavitt AD, Shattil SJ. Megakaryocytes derived from embryonic stem cells implicate Ca1DAG-GEFI in integrin signaling. Proc Natl Acad Sci U S A. 2002;99:12819-12824.
102. 3. J Biol Chem. 1996;271:16416-16421.
103. Calderwood DA, Zent R, Grant R, Rees DJ, Hynes RO, Ginsberg MH. The talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J Biol Chem. 1999;274:28071-28074.
104. Dangerfield J, Larbi KY, Huang MT, Dewar A, Nourshargh S. PECAM-1 (CD31) homophilic interaction up-regulates α6β1 on transmigrated neutrophils in vivo and plays a functional role in the ability of a6 Integrins to mediate leukocyte migration through the perivascular basement membrane. J Exp Med. 2002;196:1201-1212.
105. Roussel E, Gingras MC. Transendothelial migration induces rapid expression on neutrophils of granule-release VLA6 used for tissue infiltration. J Leukoc Biol. 1997;62:356-362.
106. O'Brien CD, Lim P, Sun J, Albelda SM. PECAM-1-dependent neutrophil transmigration is independent of monolayer PECAM-1 signaling or localization. Blood. 2003;101:2816-2825.
107. Seabra MC, Hume AN, Mules EH. Rab GTPases, intracellular traffic and disease. Trends Mol Med. 2002;8:23-30.
108. Noble KE, Wickremasinghe RG, DeCornet C, Panayiotidis P, Yong KL. Monocytes stimulate expression of the Bcl-2 family member, A1, in endothelial cells and confer protection against apoptosis. J Immunol. 1999;162:1376-1383.
109. Evans PC, Taylor ER, Kilshaw PJ. Signaling through CD31 protects endothelial cells from apoptosis. Transplantation. 2001;71:457-460.
110. Gao C, Sun W, Matsuyama S, Newman PJ. PECAM-1 is a specific and potent inhibitor of Bax-induced apoptosis. Blood. 2001;98:796a.
111. Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407:770-776.
112. Sheibani N, Sorenson CM, Frazier WA. Differential modulation of cadherin-mediated cell-cell adhesion by platelet endothelial cell adhesion molecule-1 isoforms through activation of extracellular regulated kinases. Mol Biol Cell. 2000;11:2793-2802.
113. Takahashi-Tezuka M, Yoshida Y, Fukada T, Ohtani T, Yamanaka Y, Nishida K, Nakajima K, Hibi M, Hirano T. Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Mol Cell Biol. 1998;18:4109-4117.
114. Zhang S, Broxmeyer HE. Flt3 ligand induces tyrosine phosphorylation of gab1 and gab2 and their association with shp-2, grb2, and PI3 kinase. Biochem Biophys Res Commun. 2000;277:195-199.
115. Brown S, Heinisch I, Ross E, Shaw K, Buckley CD, Savill J. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature. 2002;418:200-203.