CD31 delays phagocyte membrane repolarization to promote efficient binding of apoptotic cells

Journal of Leukocyte Biology

Volumn 82, Issue 5, 2007, Pages 1278-1288

  Vernon Wilson, Elizabeth F ^a   Auradé, Frédéric ^a   Tian, Lijun ^a   Rowe, Iain C M ^a   Shipston, Michael J ^a   Savill, John ^a   Brown, Simon B ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Apoptosis; Ether a go go related gene (ERG); Integrins; Phagocytosis

Indexed keywords

BETA1 INTEGRIN; BIOTIN; CD31 ANTIGEN; FIBRONECTIN; IMMUNOGLOBULIN F(AB) FRAGMENT; LATEX; POTASSIUM CHANNEL HERG;

APOPTOSIS; ARTICLE; CELL STRAIN K 562; CONTROLLED STUDY; CYTOPLASM; ENZYME INHIBITION; HUMAN; HUMAN CELL; MEMBRANE STEADY POTENTIAL; MUSCLE FIBER MEMBRANE RESISTANCE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; REPOLARIZATION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD29; ANTIGENS, CD31; APOPTOSIS; CROSS-LINKING REAGENTS; ELECTROPHYSIOLOGY; ETHER-A-GO-GO POTASSIUM CHANNELS; FIBRONECTINS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; K562 CELLS; MACROPHAGE ACTIVATION; MACROPHAGES; MEMBRANE POTENTIALS; MONOCYTES; PHAGOCYTES; PHAGOCYTOSIS;

EID: 36248948570     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0507283     Document Type: Article

References (62)

1. Muller, W. A., Weigl, S. A., Deng, X., Phillips, D. M. (1993) PECAM-1 is required for transendothelial migration of leukocytes. J. Exp. Med. 178, 449-460.
2. Muller, W. A. (2003) Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 24, 327-334.
3. Nourshargh, S., Marelli-Berg, F. M. (2005) Transmigration through venular walls: a key regulator of leukocyte phenotype and function. Trends Immunol. 26, 157-165.
4. Liao, F., Huynh, H. K., Eiroa, A., Greene, T., Polizzi, E., Muller, W. A. (1995) Migration of monocytes across endothelium and passage through extracellular matrix involve separate molecular domains of PECAM-1. J. Exp. Med. 182, 1337-1343.
5. Dangerfield, J., Larbi, K. Y., Huang, M. T., Dewar, A., 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.
6. Newman, P. J., 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.
7. O'Brien, C. D., Lim, P., Sun, J., Albelda, S. M. (2003) PECAM-1-dependent neutrophil transmigration is independent of monolayer PECAM-1 signaling or localization. Blood 101, 2816-2825.
8. Luu, N. T., Rainger, G. E., Buckley, C. D., Nash, G. B. (2003) CD31 regulates direction and rate of neutrophil migration over and under endothelial cells. J. Vasc. Res. 40, 467-479.
9. Chiba, R., Nakagawa, N., Kurasawa, K., Tanaka, Y., Saito, Y., Iwamoto, I. (1999) 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 94, 1319-1329.
10. Bogen, S., Pak, J., Garifallou, M., Deng, X., Muller, W. A. (1994) Monoclonal antibody to murine PECAM-1 (CD31) blocks acute inflammation in vivo. J. Exp. Med. 179, 1059-1064.
11. Schenkel, A. R., Chew, T. W., Muller, W. A. (2004) Platelet endothelial cell adhesion molecule deficiency or blockade significantly reduces leukocyte emigration in a majority of mouse strains. J. Immunol. 173, 6403-6408.
12. Liao, F., Ali, J., Greene, T., Muller, W. A. (1997) Soluble domain 1 of platelet-endothelial cell adhesion molecule (PECAM) is sufficient to block transendothelial migration in vitro and in vivo. J. Exp. Med. 185, 1349-1357.
13. Reedquist, K. A., Ross, E., Koop, E. A., Wolthuis, R. M., Zwartkruis, F. J., van Kooyk, Y., Salmon, M., Buckley, C. D., Bos, J. L. (2000) The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J. Cell Biol. 148, 1151-1158.
14. Zhao, T., Newman, P. J. (2001) Integrin activation by regulated dimerization and oligomerization of platelet endothelial cell adhesion molecule (PECAM)-1 from within the cell. J. Cell Biol. 152, 65-73.
15. Buckley, C. D., Doyonnas, R., Newton, J. P., Blystone, S. D., Brown, E. J., Watt, S. M., Simmons, D. L. (1996) Identification of α v β 3 as a heterotypic ligand for CD31/PECAM-1. J. Cell Sci. 109, 437-445.
16. Wong, C. W., Wiedle, G., Ballestrem, C., Wehrle-Haller, B., Etteldorf, S., Bruckner, M., Engelhardt, B., Gisler, R. H., Imhof, B. A. (2000) PECAM-1/CD31 trans-homophilic binding at the intercellular junctions is independent of its cytoplasmic domain; evidence for heterophilic interaction with integrin αvβ3 in cis. Mol. Biol. Cell 11, 3109-3121.
17. Brown, S., Heinisch, I., Ross, E., Shaw, K., Buckley, C. D., Savill, J. (2002) Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature 418, 200-203.
18. Dogusan, Z., Montecino-Rodriguez, E., Dorshkind, K. (2004) Macrophages and stromal cells phagocytose apoptotic bone marrow-derived B lineage cells. J. Immunol. 172, 4717-4723.
19. Vernon-Wilson, E. F., Aurade, F., Brown, S. B. (2006) CD31 promotes β-1 integrin-dependent binding of apoptotic leukocytes opsonized for phagocytosis by fibronectin. J. Leukoc. Biol. 79, 1260-1267.
20. Potter, P. K., Larbi, K. Y., Nourshargh, S., Botto, M. (2007) Efficient clearance of opsonized apoptotic cells in the absence of PECAM-1. Mol. Immunol. 44, 1135-1140.
21. Savill, J., Dransfield, I., Gregory, C., Haslett, C. (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975.
22. Oldenborg, P. A., Zheleznyak, A., Fang, Y. F., Lagenaur, C. F., Gresham, H. D., Lindberg, F. P. (2000) Role of CD47 as a marker of self on red blood cells. Science 288, 2051-2054.
23. Oldenborg, P. A., Gresham, H. D., Lindberg, F. P. (2001) CD47-signal regulatory protein α (SIRPα) regulates Fcγ and complement receptor-mediated phagocytosis. J. Exp. Med. 193, 855-862.
24. Gardai, S. J., McPhillips, K., Frasch, C., Janssen, J., Starefeldt, A., Murphy-Ullrich, J. E., Bratton, D. L., Oldenborg, P. A., Michalak, M., Henson, P. M. (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321-334.
25. Newman, P. J. (1999) Switched at birth: a new family for PECAM-1. J. Clin. Invest. 103, 5-9.
26. Jackson, D. E. (2003) The unfolding tale of PECAM-1. FEBS Lett. 540, 7-14.
27. Gratzinger, D., Barreuther, M., Madri, J. A. (2003) Platelet-endothelial cell adhesion molecule-1 modulates endothelial migration through its immunoreceptor tyrosine-based inhibitory motif. Biochem. Biophys. Res. Commun. 301, 243-249.
28. Gratzinger, D., Canosa, S., Engelhardt, B., 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.
29. O'Brien, C. D., Cao, G., Makrigiannakis, A., DeLisser, H. M. (2004) Role of immunoreceptor tyrosine-based inhibitory motifs of PECAM-1 in PECAM-1-dependent cell migration. Am. J. Physiol. Cell Physiol. 287, C1103-C1113.
30. Mitcheson, J. S., Sanguinetti, M. C. (1999) Biophysical properties and molecular basis of cardiac rapid and slow delayed rectifier potassium channels. Cell. Physiol. Biochem. 9, 201-216.
31. Zhou, W., Cayabyab, F. S., Pennefather, P. S., Schlichter, L. C., DeCoursey, T. E. (1998) HERG-like K+ channels in microglia. J. Gen. Physiol. 111, 781-794.
32. Smith, G. A., Tsui, H. W., Newell, E. W., Jiang, X., Zhu, X. P., Tsui, F. W., Schlichter, L. C. (2002) Functional up-regulation of HERG K+ channels in neoplastic hematopoietic cells. J. Biol. Chem. 277, 18528-18534.
33. Pillozzi, S., Brizzi, M. F., Balzi, M., Crociani, O., Cherubini, A., Guasti, L., Bartolozzi, B., Becchetti, A., Wanke, E., Bernabei, P. A., Olivotto, M., Pegoraro, L., Arcangeli, A. (2002) HERG potassium channels are constitutively expressed in primary human acute myeloid leukemias and regulate cell proliferation of normal and leukemic hemopoietic progenitors. Leukemia 16, 1791-1798.
34. Crociani, O., Guasti, L., Balzi, M., Becchetti, A., Wanke, E., Olivotto, M., Wymore, R. S., Arcangeli, A. (2003) Cell cycle-dependent expression of HERG1 and HERG1B isoforms in tumor cells. J. Biol. Chem. 278, 2947-2955.
35. Brown, S. B., Tucker, C. S., Ford, C., Lee, Y., Dunbar, D. R., Mullins, J. J. (2007) Class III anti-arrhythmic methanesulfonanilides inhibit leukocyte recruitment in Zebrafish. J. Leukoc. Biol. 82, 79-84.
36. Savill, J. S., Henson, P. M., Haslett, C. (1989) Phagocytosis of aged human neutrophils by macrophages is mediated by a novel "charge- sensitive" recognition mechanism. J. Clin. Invest. 84, 1518-1527.
37. Blystone, S. D., Graham, I. L., Lindberg, F. P., Brown, E. J. (1994) Integrin α v β 3 differentially regulates adhesive and phagocytic functions of the fibronectin receptor α 5 β 1. J. Cell Biol. 127, 1129-1137.
38. Baxter, D. F., Kirk, M., Garcia, A. F., Raimondi, A., Holmqvist, M. H., Flint, K. K., Bojanic, D., Distefano, P. S., Curtis, R., Xie, Y. (2002) A novel membrane potential-sensitive fluorescent dye improves cell-based assays for ion channels. J. Biomol. Screen. 7, 79-85.
39. Newton, J. P., Buckley, C. D., Jones, E. Y., 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.
40. Hofmann, G., Bernabei, P. A., Crociani, O., Cherubini, A., Guasti, L., Pillozzi, S., Lastraioli, E., Polvani, S., Bartolozzi, B., Solazzo, V., Gragnani, L., Defilippi, P., Rosati, B., Wanke, E., Olivotto, M., Arcangeli, A. (2001) HERG K+ channels activation during β(1) integrin-mediated adhesion to fibronectin induces an up-regulation of α(v)β(3) integrin in the preosteoclastic leukemia cell line FLG29.1. J. Biol. Chem. 276, 4923-4931.
41. + current with a cell-cycle dependence governs the resting potential of mammalian neuroblastoma cells. J. Physiol. 489, 455-471.
42. Gregory, C. D., Devitt, A. (2004) The macrophage and the apoptotic cell: an innate immune interaction viewed simplistically? Immunology 113, 1-14.
43. O'Shea, P. (2005) Physical landscapes in biological membranes: physicochemical terrains for spatio-temporal control of biomolecular interactions and behavior. Philos. Transact. A Math Phys. Eng. Sci. 363, 575-588.
44. McCaig, C. D., Rajnicek, A. M., Song, B., Zhao, M. (2005) Controlling cell behavior electrically: current views and future potential. Physiol. Rev. 85, 943-978.
45. Ben-Chaim, Y., Chanda, B., Dascal, N., Bezanilla, F., Parnas, I., Parnas, H. (2006) Movement of 'gating charge' is coupled to ligand binding in a G-protein-coupled receptor. Nature 444, 106-109.
46. Cherubini, A., Hofmann, G., Pillozzi, S., Guasti, L., Crociani, O., Cilia, E., Di Stefano, P., Degani, S., Balzi, M., Olivotto, M., Wanke, E., Becchetti, A., Defilippi, P., Wymore, R., Arcangeli, A. (2005) Human ether-a-go-go-related gene 1 channels are physically linked to β-1 integrins and modulate adhesion-dependent signaling. Mol. Biol. Cell 16, 2972-2983.
47. Levite, M., Cahalon, L., Peretz, A., Hershkoviz, R., Sobko, A., Ariel, A., Desai, R., Attali, B., Lider, O. (2000) Extracellular K(+) and opening of voltage-gated potassium channels activate T cell integrin function: physical and functional association between Kv1.3 channels and β1 integrins. J. Exp. Med. 191, 1167-1176.
48. Artym, V. V., Petty, H. R. (2002) Molecular proximity of Kv1.3 voltage-gated potassium channels and β(1)-integrins on the plasma membrane of melanoma cells: effects of cell adherence and channel blockers. J. Gen. Physiol. 120, 29-37.
49. Murata, Y., Iwasaki, H., Sasaki, M., Inaba, K., Okamura, Y. (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435, 1239-1243.
50. Zhao, M., Song, B., Pu, J., Wada, T., Reid, B., Tai, G., Wang, F., Guo, A., Walczysko, P., Gu, Y., Sasaki, T., Suzuki, A., Forrester, J. V., Bourne, H. R., Devreotes, P. N., McCaig, C. D., Penninger, J. M. (2006) Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-γ and PTEN. Nature 442, 457-460.
51. Scott, C. C., Dobson, W., Botelho, R. J., Coady-Osberg, N., Chavrier, P., Knecht, D. A., Heath, C., Stahl, P., Grinstein, S. (2005) Phosphatidylinositol- 4,5-bisphosphate hydrolysis directs actin remodeling during phagocytosis. J. Cell Biol. 169, 139-149.
52. Yeung, T., Terebiznik, M., Yu, L., Silvius, J., Abidi, W. M., Philips, M., Levine, T., Kapus, A., Grinstein, S. (2006) Receptor activation alters inner surface potential during phagocytosis. Science 313, 347-351.
53. Rainger, G. E., Buckley, C., Simmons, D. L., Nash, G. B. (1997) Cross-talk between cell adhesion molecules regulates the migration velocity of neutrophils. Curr. Biol. 7, 316-325.
54. Hartmann, T., Verkman, A. S. (1990) Model of ion transport in chloride-secreting airway epithelial cells. Biophys. J. 58, 391-401.
55. Vu, C. C., Bortner, C. D., Cidlowski, J. A. (2001) Differential involvement of initiator caspases in apoptotic volume decrease and potassium efflux during Fas- and UV-induced cell death. J. Biol. Chem. 276, 37602-37611.
56. Koizumi, S., Shigemoto-Mogami, Y., Nasu-Tada, K., Shinozaki, Y., Ohsawa, K., Tsuda, M., Joshi, B. V., Jacobson, K. A., Kohsaka, S., Inoue, K. (2007) UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446, 1091-1095.
57. Lauber, K., Bohn, E., Kröber, S. M., Xiao, Y. J., Blumenthal, S. G., Lindemann, R. K., Marini, P., Wiedig, C., Zobywalski, A., Baksh, S., Xu, Y., Autenrieth, I. B., Schulze-Osthoff, K., Belka, C., Stuhler, G., Wesselborg, S. (2003) Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113, 717-730.
58. Hart, S. P., Smith, J. R., Dransfield, I. (2004) Phagocytosis of opsonized apoptotic cells: roles for 'old-fashioned' receptors for antibody and complement. Clin. Exp. Immunol. 135, 181-185.
59. Young, J. D., Unkeless, J. C., Kaback, H. R., Cohn, Z. A. (1983) Macrophage membrane potential changes associated with γ 2b/γ 1 Fc receptor-ligand binding. Proc. Natl. Acad. Sci. USA 80, 1357-1361.
60. Holevinsky, K. O., Nelson, D. J. (1995) Simultaneous detection of free radical release and membrane current during phagocytosis. J. Biol. Chem. 270, 8328-8336.
61. Floto, R. A., Somasundaram, B., Allen, J. M., Mahaut-Smith, M. P. (1997) Fcγ receptor I activation triggers a novel Ca2+-activated current selective for monovalent cations in the human monocytic cell line, U937. J. Biol. Chem. 272, 4753-4758.
62. Campo, B., Surprenant, A., North, R. A. (2003) Sustained depolarization and ADP-ribose activate a common ionic current in rat peritoneal macrophages. J. Immunol. 170, 1167-1173.