PECAM-1 functions as a specific and potent inhibitor of mitochondrial-dependent apoptosis

Blood

Volumn 102, Issue 1, 2003, Pages 169-179

  Gao, Cunji ^b   Sun, Weiyong ^b   Christofidou Solomidou, Melpo ^b   Sawada, Motoshi ^b   Newman, Debra K ^b   Bergom, Carmen ^b   Albelda, Steven M ^b   Matsuyama, Shigemi ^b   Newman, Peter J ^a  

^a BLOOD RESEARCH INSTITUTE   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CD31 ANTIGEN; CYTOCHROME C; MONOCLONAL ANTIBODY; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL ADHESION; CELL DEATH; CELL FRACTIONATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; THROMBOCYTE; X IRRADIATION;

EID: 0038508862     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2003-01-0003     Document Type: Article

References (77)

1. Newman PJ, Bemdt MC, Gorski J, et al. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science. 1990;247:1219-1222.
2. Muller WA, Ratti CM, McDonnell SL, Cohn ZA. A human endothelial cell-restricted externally disposed plasmalemmal protein enriched in intercellular junctions. J Exp Med. 1989;170:399-414.
3. Albelda SM, Oliver PD, Romer LH, Buck CA. EndoCAM: a novel endothelial cell-cell adhesion molecule. J Cell Biol. 1990;110:1227-1237.
4. Sun Q-H, DeLisser HM, Zukowski MM, et al. Individually distinct Ig homology domains in PECAM-1 regulate homophilic binding and modulate receptor affinity. J Biol Chem. 1996;271:11090-11098.
5. 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.
6. Muller WA, Weigl SA, Deng X, Phillips DM. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med. 1993;178:449-460.
7. Vaporciyan AA, DeLisser HM, Yan H-C, et al. Involvement of platelet endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science. 1993;262:1580-1582.
8. Zhou Z, Christofidou-Solomidou M, Garlanda C, DeLisser HM. Antibody against murine PECAM-1 inhibits tumor angiogenesis in mice. Angiogenesis. 1999;3:181-188.
9. lck. Blood. 2001;97:2351-2357.
10. 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.
11. Jones KL, Hughan SC, Dopheide SM, et al. Platelet endothelial cell adhesion molecule-1 is a negative regulator of platelet-collagen interactions. Blood. 2001;98:1456-1463.
12. 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.
13. 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.
14. 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.
15. Newman PJ. Switched at birth: a new family for PECAM-1. J Clin Invest. 1999;103:5-9.
16. 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.
17. Sun J, Williams J, Yan H-C, et al. 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.
18. Bird IN, Taylor V, Newton JP, et al. Homophilic PECAM-1 (CD31) interactions prevent endothelial cell apoptosis but do not support cell spreading or migration. J Cell Sci. 1999;112:1989-1997.
19. Evans PC, Taylor ER, Kilshaw PJ. Signaling through CD31 protects endothelial cells from apoptosis. Transplantation. 2001;71:457-460.
20. Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407:770-776.
21. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science. 1998;281:1305-1308.
22. Finkel E. The mitochondrion: is it central to apoptosis? Science. 2001;292:624-626.
23. Cheng EH, Wei MC, Weiler S, et al. BCL-2, BCL-XL sequester BH3 domain-only molecules preventing Bax- and Bak-mediated mitochondrial apoptosis. Mol Cell. 2001;8:705-711.
24. Wolter KG, Hsu YT, Smith CL, et al. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol. 1997;139:1281-1292.
25. Gross A, Jockel J, Wei MC, Korsmeyer SJ. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 1998;17:3878-3885.
26. Acehan D, Jiang X, Morgan DG, et al. Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol Cell. 2002;9:423-432.
27. Rodriguez J, Lazebnik Y, Caspase-9 and APAF-1 form an active holoenzyme. Genes Dev. 1999;13:3179-3184.
28. Deveraux QL, Reed JC. IAP family proteins suppressors of apoptosis. Genes Dev. 1999;13:239-252.
29. Suh SH, Vennekens R, Manolopoulos VG, et al. Characterisation of explanted endothelial cells from mouse aorta: electrophysiology and Ca2+ signalling. Pflugers Arch. 1999;438:612-620.
30. Picciano PT, Johnson B, Walenga RW, et al. Effects of D-valine on pulmonary artery endothelial cell morphology and function in cell culture. Exp Cell Res. 1984;151:134-147.
31. Gilmore AP, Metcalfe AD, Romer LH, Streuli CH. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. J Cell Biol. 2000;149:431-446.
32. Zhang H, Xu Q, Krajewski S, et al. BAR: an apoptosis regulator at the intersection of caspases and Bcl-2 family proteins. Proc Natl Acad Sci U S A. 2000;97:2597-2602.
33. Jurgensmeier JM, Xie Z, Deveraux Q, et al. Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci U S A. 1998;95:4997-5002.
34. Xu Q, Reed JC. Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell. 1998;1:337-346.
35. 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.
36. Yang J, Liu X, Bhalla K, et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 1997;275:1129-1132.
37. Harrington EO, Smeglin A, Newton J, Ballard G, Rounds S. Protein tyrosine phosphatase-dependent proteolysis of focal adhesion complexes in endothelial cell apoptosis. Am J Physiol Lung Cell Mol Physiol. 2001;280:L342-L353.
38. Wei MC, Zong WX, Cheng EH, et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 2001;292:727-730.
39. Hsu YT, Wolter KG, Youle RJ. Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci U S A. 1997;94:3668-3672.
40. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281:1309-1312.
41. Goyal L. Cell death inhibition: keeping caspases in check. Cell. 2001;104:805-808.
42. 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.
43. Ferrero E, Belloni D, Contini P, et al. Transendothelial migration leads to protection from starvation-induced apoptosis in CD34+CD14+ circulating precursors: evidence for PECAM-1 involvement through Akt/PKB activation. Blood. 2003;101:186-193.
44. Dudek H, Datta SR, Franke TF, et al. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science. 1997;275:661-665.
45. Wu CJ, O'Rourke DM, Feng GS, et al. The tyrosine phosphatase SHP-2 is required for mediating phosphatidylinositol 3-kinase/Akt activation by growth factors. Oncogene. 2001;20:6018-6025.
46. Sun J, Paddock C, Shubert J, et al. Contributions of the extracelluiar and cytoplasmic domains of platelet-endothelial cell adhesion molecule-1 (PECAM-1/CD31) in regulating cell-cell localization. J Cell Sci. 2000;113:1459-1469.
47. Meredith J, Fazeli B, Schwartz MA. The extracellular matrix as a cell survival factor. Mol Biol Cell. 1993;4:953-961.
48. Frisch SM, Ruoslahti E. Integrins and anoikis. Curr Opin Cell Biol. 1997;9:701-706.
49. Tanaka Y, Albelda SM, Horgan KJ, et al. CD31 expressed on distinctive T cell subsets is a preferential amplifier of β1 integrin-mediated adhesion. J Exp Med. 1992;176:245-253.
50. Piali L, Albeida SM, Baldwin HS, et al. Murine platelet endothelial cell adhesion molecule (PECAM-1/CD31) modulates β2 integrins on lymphokine-activated killer cells. Eur J Immunol. 1993;23:2464-2471.
51. Leavesley DI, Oliver JM, Swart BW, et al. Signals from platelet/endothelial cell adhesion molecule enhance the adhesive activity of the very late antigen-4 integrin of human CD34+ hemopoietic progenitor cells. J Immunol. 1994;153:4673-4683.
52. 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.
53. 2 integrin activation. J Immunol. 1996;156:1515-1524.
54. Varon D, Jackson DE, Shenkman B, et al. Platelet/endothelial cell adhesion molecule-1 serves as a co-stimulatory agonist receptor that modulates integrin-dependent adhesion and aggregation ofihuman platelets. Blood. 1998;91:500-507.
55. Chiba R, Nakagawa N, Kurasawa K, et al. 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.
56. 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.
57. 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 α6 integrins to mediate leukocyte migration through the perivascular basement membrane. J Exp Med. 2002;196:1201-1212.
58. Stupack DG, Puente XS, Boutsaboualoy S, Storgard CM, Cheresh DA. Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins. J Cell Biol. 2001;155:459-470.
59. Daigle I, Yousefi S, Colonna M, Green DR, Simon HU. Death receptors bind SHP-1 and block cytokine-induced anti-apoptotic signaling in neutrophils. Nat Med. 2002;8:61-67.
60. Cao MY, Huber M, Beauchemin N, et al. Regulation of mouse PECAM-1 tyrosine phosphorylation by the Src and Csk families of protein-tyrosine kinases. J Biol Chem. 1998;273:15765-15772.
61. 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.
62. Cunnick JM, Meng S, Ren Y, et al. Regulation of the mitogen-activated protein kinase signaling pathway by SHP2. J Biol Chem. 2002;277:9498-9504.
63. Zhang SQ, Tsiaras WG, Araki T, et al. Receptor-specific regulation of phosphatidylinositol 3′-kinase activation by the protein tyrosine phosphatase Shp2. Mol Cell Biol. 2002;22:4062-4072.
64. Suzuki M, Youle RJ, Tjandra N. Structure of Bax: coregulation of dimer formation and intracellular localization. Cell. 2000;103:645-654.
65. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 1998;94:481-490.
66. Wei MC, Lindsten T, Mootha VK, et al. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 2000;14:2060-2071.
67. Eskes R, Desagher S, Antonsson B, Martinou JC. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol. 2000;20:929-935.
68. Ruffolo SC, Breckenridge DG, Nguyen M, et al. BID-dependent and BID-independent pathways for BAX insertion into mitochondria. Cell Death Differ. 2000;7:1101-1108.
69. Pumphrey NJ, Taylor V, Freeman S, et al. 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.
70. 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.
71. 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.
72. 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.
73. Ilan N, Cheung L, Miller S, et al. Pecam-1 is a modulator of stat family member phosphorylation and localization: lessons from a transgenic mouse. Dev Biol. 2001;232:219-232.
74. 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.
75. 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.
76. Paris F, Fuks Z, Kang A, et al. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science. 2001;293:293-297.
77. Yerebakan O, Ciftcioglu MA, Akkaya BK, Yilmaz E. Prognostic value of Ki-67, CD31 and epidermal growth factor receptor expression in basal cell carcinoma. J Dermatol. 2003;30:33-41.