Relative contribution of PECAM-1 adhesion and signaling to the maintenance of vascular integrity

Journal of Cell Science

Volumn 124, Issue 9, 2011, Pages 1477-1485

  Privratsky, Jamie R ^a,b   Paddock, Cathy M ^a   Florey, Oliver ^c   Newman, Debra K ^a,b   Muller, William A ^c   Newman, Peter J ^a,b  

^a BLOOD RESEARCH INSTITUTE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Adhesion molecules; CD31; PECAM 1; Vascular permeability

Indexed keywords

CD31 ANTIGEN;

ARTICLE; CELL JUNCTION; ENDOTHELIUM CELL; MUTANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEADY STATE;

ANTIGENS, CD31; CELL ADHESION; CELL LINE; ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR JUNCTIONS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 79955525883     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.082271     Document Type: Article

References (72)

1. Albelda, S. M., Oliver, P. D., Romer, L. H. and Buck, C. A. (1990). EndoCAM: a novel endothelial cell-cell adhesion molecule. J. Cell Biol. 110, 1227-1237.
2. Bergom, C., Goel, R., Paddock, C., Gao, C., Newman, D. K., Matsuyama, S. and Newman, P. J. (2006). The cell-adhesion and signaling molecule PECAM-1 is a molecular mediator of resistance to genotoxic chemotherapy. Cancer Biol. Ther. 5, 1699-1707.
3. Bergom, C., Paddock, C., Gao, C., Holyst, T., Newman, D. K. and Newman, P. J. (2008). An alternatively spliced isoform of PECAM-1 is expressed at high levels in human and murine tissues, and suggests a novel role for the C-terminus of PECAM-1 in cytoprotective signaling. J. Cell Sci. 121, 1235-1242.
4. Berman, M. E. and Muller, W. A. (1995). 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. 154, 299-307.
5. Berman, M. E., Xie, Y. and Muller, W. A. (1996). Roles of platelet/endothelial cell adhesion molecule-1 (PECAM-1, CD31) in natural killer cell transendothelial migration and beta 2 integrin activation. J. Immunol. 156, 1515-1524.
6. Biswas, P., Zhang, J., Schoenfeld, J. D., Schoenfeld, D., Gratzinger, D., Canosa, S. and Madri, J. A. (2005). Identification of the regions of PECAM-1 involved in β-and γ-catenin associations. Biochem. Biophys. Res. Commun. 329, 1225-1233.
7. Biswas, P., Canosa, S., Schoenfeld, D., Schoenfeld, J., Li, P., Cheas, L. C., Zhang, J., Cordova, A., Sumpio, B. and Madri, J. A. (2006). PECAM-1 affects GSK-3β-mediated β-catenin phosphorylation and degradation. Am. J. Pathol. 169, 314-324.
8. Cao, M. Y., Huber, M., Beauchemin, N., Famiglietti, J., Albelda, S. M. and Veillette, A. (1998). Regulation of mouse PECAM-1 tyrosine phosphorylation by the Src and Csk families of protein-tyrosine kinases. J. Biol. Chem. 273, 15765-15772.
9. Carrithers, M., Tandon, S., Canosa, S., Michaud, M., Graesser, D. and Madri, J. A. (2005). Enhanced susceptibility to endotoxic shock and impaired STAT3 signaling in CD31-deficient mice. Am. J. Pathol. 166, 185-196.
10. Chiba, R., Nakagawa, N., Kurasawa, K., Tanaka, Y., Saito, Y. and Iwamoto, I. (1999). Ligation of CD31 (PECAM-1) on endothelial cells increases adhesive function of alphavbeta3 integrin and enhances beta1 integrin-mediated adhesion of eosinophils to endothelial cells. Blood 94, 1319-1329.
11. Cohen, J. (2002). The immunopathogenesis of sepsis. Nature 420, 885-891.
12. Dangerfield, J., Larbi, K. Y., Huang, M. T., Dewar, A. and Nourshargh, S. (2002). 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. 196, 1201-1211.
13. Dasgupta, B., Dufour, E., Mamdouh, Z. and Muller, W. A. (2009). A novel and critical role for tyrosine 663 in platelet endothelial cell adhesion molecule-1 trafficking and transendothelial migration. J. Immunol. 182, 5041-5051.
14. Duncan, G. S., Andrew, D. P., Takimoto, H., Kaufman, S. A., Yoshida, H., Spellberg, J., de la Pompa, J. L., Elia, A., Wakeham, A., Karan-Tamir, B. et al. (1999). 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. 162, 3022-3030.
15. Falati, S., Patil, S., Gross, P. L., Stapleton, M., Merrill-Skoloff, G., Barrett, N. E., Pixton, K. L., Weiler, H., Cooley, B., Newman, D. K. et al. (2006). Platelet PECAM-1 inhibits thrombus formation in vivo. Blood 107, 535-541.
16. Ferrero, E., Ferrero, M. E., Pardi, R. and Zocchi, M. R. (1995). The platelet endothelial cell adhesion molecule-1 (PECAM1) contributes to endothelial barrier function. FEBS Lett. 374, 323-326.
17. Florey, O., Durgan, J. and Muller, W. (2010). Phosphorylation of leukocyte PECAM and its association with detergent-resistant membranes regulate transendothelial migration. J. Immunol. 185, 1878-1886.
18. Fukuda, Y., Aoyama, Y., Wada, A. and Igarashi, Y. (2004). Identification of PECAM-1 association with sphingosine kinase 1 and its regulation by agonist-induced phosphorylation. Biochim. Biophys. Acta 1636, 12-21.
19. Giaever, I. and Keese, C. R. (1991). Micromotion of mammalian cells measured electrically. Proc. Natl. Acad. Sci. USA 88, 7896-7900.
20. Goel, R., Boylan, B., Gruman, L., Newman, P. J., North, P. E. and Newman, D. K. (2007). The proinflammatory phenotype of PECAM-1-deficient mice results in atherogenic diet-induced steatohepatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 293, G1205-G1214.
21. Goel, R., Schrank, B. R., Arora, S., Boylan, B., Fleming, B., Miura, H., Newman, P. J., Molthen, R. C. and Newman, D. K. (2008). Site-specific effects of PECAM-1 on atherosclerosis in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28, 1996-2002.
22. Graesser, D., Solowiej, A., Bruckner, M., Osterweil, E., Juedes, A., Davis, S., Ruddle, N. H., Engelhardt, B. and Madri, J. A. (2002). Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice. J. Clin. Invest. 109, 383-392.
23. Gratzinger, D., Canosa, S., Engelhardt, B. and Madri, J. A. (2003). Platelet endothelial cell adhesion molecule-1 modulates endothelial cell motility through the small G-protein Rho. FASEB J. 17, 1458-1469.
24. Harry, B. L., Sanders, J. M., Feaver, R. E., Lansey, M., Deem, T. L., Zarbock, A., Bruce, A. C., Pryor, A. W., Gelfand, B. D., Blackman, B. R. et al. (2008). Endothelial cell PECAM-1 promotes atherosclerotic lesions in areas of disturbed flow in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28, 2003-2008.
25. Henshall, T. L., Jones, K. L., Wilkinson, R. and Jackson, D. E. (2001). 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. 166, 3098-3106.
26. Hua, C. T., Gamble, J. R., Vadas, M. A. and Jackson, D. E. (1998). Recruitment and activation of SHP-1 protein-tyrosine phosphatase by human platelet endothelial cell adhesion molecule-1 (PECAM-1). Identification of immunoreceptor tyrosine-based inhibitory motif-like binding motifs and substrates. J. Biol. Chem. 273, 28332-28340.
27. Huang, Y. T., Chen, S. U., Chou, C. H. and Lee, H. (2008). Sphingosine 1-phosphate induces platelet/endothelial cell adhesion molecule-1 phosphorylation in human endothelial cells through cSrc and Fyn. Cell. Signal. 20, 1521-1527.
28. Komarova, Y. A., Mehta, D. and Malik, A. B. (2007). Dual regulation of endothelial junctional permeability. Sci. STKE 2007, re8.
29. Kumar, V., Abbas, A. and Fausto, N. (2004). Robbins and Cotran Pathologic Basis of Disease. Philadelphia: Saunders.
30. Lee, F. A., van Lier, M., Relou, I. A., Foley, L., Akkerman, J. W., Heijnen, H. F. and Farndale, R. W. (2006). Lipid rafts facilitate the interaction of PECAM-1 with the glycoprotein VI-FcR gamma-chain complex in human platelets. J. Biol. Chem. 281, 39330-39338.
31. Limaye, V., Li, X., Hahn, C., Xia, P., Berndt, M. C., Vadas, M. A. and Gamble, J. R. (2005). Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1-dependent activation of PI-3K/Akt and regulation of Bcl-2 family members. Blood 105, 3169-3177.
32. Lu, T. T., Barreuther, M., Davis, S. and Madri, J. A. (1997). 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. 272, 14442-14446.
33. Maas, M., Stapleton, M., Bergom, C., Mattson, D. L., Newman, D. K. and Newman, P. J. (2005). Endothelial cell PECAM-1 confers protection against endotoxic shock. Am. J. Physiol. Heart Circ. Physiol. 288, H159-H164.
34. Mahooti, S., Graesser, D., Patil, S., Newman, P., Duncan, G., Mak, T. and Madri, J. A. (2000). PECAM-1 (CD31) expression modulates bleeding time in vivo. Am. J. Pathol. 157, 75-81.
35. Masuda, M., Osawa, M., Shigematsu, H., Harada, N. and Fujiwara, K. (1997). Platelet endothelial cell adhesion molecule-1 is a major SH-PTP2 binding protein in vascular endothelial cells. FEBS Lett. 408, 331-336.
36. Mehta, D. and Malik, A. B. (2006). Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 86, 279-367.
37. Moses, A. V., Fish, K. N., Ruhl, R., Smith, P. P., Strussenberg, J. G., Zhu, L., Chandran, B. and Nelson, J. A. (1999). Long-term infection and transformation of dermal microvascular endothelial cells by human herpesvirus 8. J. Virol. 73, 6892-6902.
38. Muller, W. A., Ratti, C. M., McDonnell, S. L. and Cohn, Z. A. (1989). A human endothelial cell-restricted, externally disposed plasmalemmal protein enriched in intercellular junctions. J. Exp. Med. 170, 399-414.
39. Muller, W. A., Weigl, S. A., Deng, X. and Phillips, D. M. (1993). PECAM-1 is required for transendothelial migration of leukocytes. J. Exp. Med. 178, 449-460.
40. Newman, D. K., Hamilton, C. and Newman, P. J. (2001). Inhibition of antigen-receptor signaling by platelet endothelial cell adhesion molecule-1 (CD31) requires functional ITIMs, SHP-2, and p56(lck). Blood 97, 2351-2357.
41. Newman, P. J. (1994). The role of PECAM-1 in vascular cell biology. Ann. N. Y. Acad. Sci. 714, 165-174.
42. Newman, P. J. (1997). The biology of PECAM-1. J. Clin. Invest. 100, S25-S29.
43. Newman, P. J. (1999). Switched at birth: a new family for PECAM-1. J. Clin. Invest. 103, 5-9.
44. Newman, P. J. and Newman, D. K. (2003). Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler. Thromb. Vasc. Biol. 23, 953-964.
45. Newman, P. J., Berndt, M. C., Gorski, J., White, G. C., Lyman, S., Paddock, C. and Muller, W. A. (1990). PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247, 1219-1222.
46. Newton, J. P., Buckley, C. D., Jones, E. Y. and Simmons, D. L. (1997). Residues on both faces of the first immunoglobulin fold contribute to homophilic binding sites of PECAM-1/CD31. J. Biol. Chem. 272, 20555-20563.
47. Newton-Nash, D. K. and Newman, P. J. (1999). A new role for platelet-endothelial cell adhesion molecule-1 (CD31): inhibition of TCR-mediated signal transduction. J. Immunol. 163, 682-688.
48. O'Brien, C. D., Lim, P., Sun, J. and Albelda, S. M. (2003). PECAM-1-dependent neutrophil transmigration is independent of monolayer PECAM-1 signaling or localization. Blood 101, 2816-2825.
49. Osawa, M., Masuda, M., Harada, N., Lopes, R. B. and Fujiwara, K. (1997). Tyrosine phosphorylation of platelet endothelial cell adhesion molecule-1 (PECAM-1, CD31) in mechanically stimulated vascular endothelial cells. Eur. J. Cell Biol. 72, 229-237.
50. Patil, S., Newman, D. K. and Newman, P. J. (2001). Platelet endothelial cell adhesion molecule-1 serves as an inhibitory receptor that modulates platelet responses to collagen. Blood 97, 1727-1732.
51. Privratsky, J. R., Newman, D. K. and Newman, P. J. (2010). PECAM-1: conflicts of interest in inflammation. Life Sci. 87, 69-82.
52. Pumphrey, N. J., Taylor, V., Freeman, S., Douglas, M. R., Bradfield, P. F., Young, S. P., Lord, J. M., Wakelam, M. J., Bird, I. N., Salmon, M. et al. (1999). Differential association of cytoplasmic signalling molecules SHP-1, SHP-2, SHIP and phospholipase C-gamma1 with PECAM-1/CD31. FEBS Lett. 450, 77-83.
53. Rosen, H. and Goetzl, E. J. (2005). Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nat. Rev. Immunol. 5, 560-570.
54. Rui, Y., Liu, X., Li, N., Jiang, Y., Chen, G., Cao, X. and Wang, J. (2007). PECAM-1 ligation negatively regulates TLR4 signaling in macrophages. J. Immunol. 179, 7344-7351.
55. Sagawa, K., Kimura, T., Swieter, M. and Siraganian, R. P. (1997). The protein-tyrosine phosphatase SHP-2 associates with tyrosine-phosphorylated adhesion molecule PECAM-1 (CD31). J. Biol. Chem. 272, 31086-31091.
56. Sardjono, C. T., Harbour, S. N., Yip, J. C., Paddock, C., Tridandapani, S., Newman, P. J. and Jackson, D. E. (2006). Palmitoylation at Cys595 is essential for PECAM-1 localisation into membrane microdomains and for efficient PECAM-1-mediated cytoprotection. Thromb. Haemost. 96, 756-766.
57. Sima, A. V., Stancu, C. S. and Simionescu, M. (2009). Vascular endothelium in atherosclerosis. Cell Tissue Res. 335, 191-203.
58. Smythe, W. R., Hwang, H. C., Amin, K. M., Eck, S. L., Davidson, B. L., Wilson, J. M., Kaiser, L. R. and Albelda, S. M. (1994). Use of recombinant adenovirus to transfer the herpes simplex virus thymidine kinase (HSVtk) gene to thoracic neoplasms: an effective in vitro drug sensitization system. Cancer Res. 54, 2055-2059.
59. Sun, J., Paddock, C., Shubert, J., Zhang, H. B., Amin, K., Newman, P. J. and Albelda, S. M. (2000). Contributions of the extracellular and cytoplasmic domains of platelet-endothelial cell adhesion molecule-1 (PECAM-1/CD31) in regulating cell-cell localization. J. Cell Sci. 113, 1459-1469.
60. Sun, Q. H., Delisser, H. M., Zukowski, M. M., Paddock, C., Albelda, S. M. and Newman, P. J. (1996). Individually distinct Ig homology domains in PECAM-1 regulate homophilic binding and modulate receptor affinity. J. Biol. Chem. 271, 11090-11098.
61. Tada, Y., Koarada, S., Morito, F., Ushiyama, O., Haruta, Y., Kanegae, F., Ohta, A., Ho, A., Mak, T. W. and Nagasawa, K. (2003). Acceleration of the onset of collagen-induced arthritis by a deficiency of platelet endothelial cell adhesion molecule 1. Arthritis Rheum. 48, 3280-3290.
62. Tanaka, Y., Albelda, S. M., Horgan, K. J., van Seventer, G. A., Shimizu, Y., Newman, W., Hallam, J., Newman, P. J., Buck, C. A. and Shaw, S. (1992). CD31 expressed on distinctive T cell subsets is a preferential amplifier of β-1 integrin-mediated adhesion. J. Exp. Med. 176, 245-253.
63. Tiruppathi, C., Malik, A. B., Del Vecchio, P. J., Keese, C. R. and Giaever, I. (1992). Electrical method for detection of endothelial cell shape change in real time: assessment of endothelial barrier function. Proc. Natl. Acad. Sci. USA 89, 7919-7923.
64. Tzima, E., Irani-Tehrani, M., Kiosses, W. B., Dejana, E., Schultz, D. A., Engelhardt, B., Cao, G., DeLisser, H. and Schwartz, M. A. (2005). A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426-431.
65. Vandenbroucke, E., Mehta, D., Minshall, R. and Malik, A. B. (2008). Regulation of endothelial junctional permeability. Ann. N. Y. Acad. Sci. 1123, 134-145.
66. Vaporciyan, A. A., Delisser, H. M., Yan, H. C., Mendiguren, I. I., Thom, S. R., Jones, M. L., Ward, P. A. and Albelda, S. M. (1993). Involvement of platelet-endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science 262, 1580-1582.
67. Varon, D., Jackson, D. E., Shenkman, B., Dardik, R., Tamarin, I., Savion, N. and Newman, P. J. (1998). Platelet/endothelial cell adhesion molecule-1 serves as a costimulatory agonist receptor that modulates integrin-dependent adhesion and aggregation of human platelets. Blood 91, 500-507.
68. Vernon-Wilson, E. F., Aurade, F. and Brown, S. B. (2006). CD31 promotes beta1 integrin-dependent engulfment of apoptotic Jurkat T lymphocytes opsonized for phagocytosis by fibronectin. J. Leukoc. Biol. 79, 1260-1267.
69. Vernon-Wilson, E. F., Aurade, F., Tian, L., Rowe, I. C., Shipston, M. J., Savill, J. and Brown, S. B. (2007). CD31 delays phagocyte membrane repolarization to promote efficient binding of apoptotic cells. J. Leukoc. Biol. 82, 1278-1288.
70. Wakelin, M. W., Sanz, M. J., Dewar, A., Albelda, S. M., Larkin, S. W., Boughton-Smith, N., Williams, T. J. and Nourshargh, S. (1996). An anti-platelet-endothelial cell adhesion molecule-1 antibody inhibits leukocyte extravasation from mesenteric microvessels in vivo by blocking the passage through the basement membrane. J. Exp. Med. 184, 229-239.
71. Wilkinson, R., Lyons, A. B., Roberts, D., Wong, M. X., Bartley, P. A. and Jackson, D. E. (2002). 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 100, 184-193.
72. Wong, M. X., Roberts, D., Bartley, P. A. and Jackson, D. E. (2002). 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. 168, 6455-6462.