The adhesion mediated by the P-selectin P-selectin glycoprotein ligand-1 (PSGL-1) couple is stronger for shorter PSGL-1 variants

Journal of Leukocyte Biology

Volumn 87, Issue 4, 2010, Pages 727-734

  Barbaux, Sandrine ^a,b   Poirier, Odette ^a,b   Pincet, Frédéric ^c   Hermand, Patricia ^a,b   Tiret, Laurence ^a,b   Deterre, Philippe ^a,b  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Biomembrane force probe; Catch bond; Ligand

Indexed keywords

P SELECTIN GLYCOPROTEIN LIGAND 1; PADGEM PROTEIN;

ADHESION; ARTICLE; BINDING SITE; CONTROLLED STUDY; DISSOCIATION; HAPLOTYPE; HUMAN; HUMAN CELL; MUTATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN VARIANT;

EID: 77950562407     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0609408     Document Type: Article

References (60)

1. Frenette, P. S., Denis, C. V., Weiss, L., Jurk, K., Subbarao, S., Kehrel, B., Hartwig, J. H., Vestweber, D., Wagner, D. D. (2000) P-selectin glycoprotein ligand 1 (PSGL-1) is expressed on platelets and can mediate platelet-endothelial interactions in vivo. J. Exp. Med. 191, 1413-1422. (Pubitemid 30227127)
2. Da Costa Martins, P., Garcia-Vallejo, J. J., van Thienen, J. V., Fernandez-Borja, M., van Gils, J. M., Beckers, C., Horrevoets, A. J., Hordijk, P. L., Zwaginga, J. J. (2007) P-selectin glycoprotein ligand-1 is expressed on endothelial cells and mediates monocyte adhesion to activated endothelium. Arterioscler. Thromb. Vasc. Biol. 27, 1023-1029. (Pubitemid 46641987)
3. Sako, D., Chang, X. J., Barone, K. M., Vachino, G., White, H. M., Shaw, G., Veldman, G. M., Bean, K. M., Ahern, T. J., Furie, B., et al. (1993) Expression cloning of a functional glycoprotein ligand for P-selectin. Cell 75, 1179-1186. (Pubitemid 24006114)
4. Spertini, O., Cordey, A. S., Monai, N., Giuffre, L., Schapira, M. (1996) P-selectin glycoprotein ligand 1 is a ligand for L-selectin on neutrophils, monocytes, and CD34+ hematopoietic progenitor cells. J. Cell Biol. 135, 523-531. (Pubitemid 26359344)
5. Norman, K. E., Katopodis, A. G., Thoma, G., Kolbinger, F., Hicks, A. E., Cotter, M. J., Pockley, A. G., Hellewell, P. G. (2000) P-selectin glycoprotein ligand-1 supports rolling on E- and P-selectin in vivo. Blood 96, 3585-3591.
6. Rinko, L. J., Lawrence, M. B., Guilford, W. H. (2004) The molecular mechanics of P- and L-selectin lectin domains binding to PSGL-1. Biophys. J. 86, 544-554.
7. Martinez, M., Joffraud, M., Giraud, S., Baisse, B., Bernimoulin, M. P., Schapira, M., Spertini, O. (2005) Regulation of PSGL-1 interactions with L-selectin, P-selectin, and E-selectin: role of human fucosyltransferase-IV and -VII. J. Biol. Chem. 280, 5378-5390. (Pubitemid 40280012)
8. Cummings, R. D. (1999) Structure and function of the selectin ligand PSGL-1. Braz. J. Med. Biol. Res. 32, 519-528. (Pubitemid 129540413)
9. Snapp, K. R., Heitzig, C. E., Ellies, L. G., Marth, J. D., Kansas, G. S. (2001) Differential requirements for the O-linked branching enzyme core 2 β1-6-N-glucosaminyltransferase in biosynthesis of ligands for E-selectin and P-selectin. Blood 97, 3806-3811.
10. Rodgers, S. D., Camphausen, R. T., Hammer, D. A. (2001) Tyrosine sulfation enhances but is not required for PSGL-1 rolling adhesion on P-selectin. Biophys. J. 81, 2001-2009.
11. Bernimoulin, M. P., Zeng, X. L., Abbal, C., Giraud, S., Martinez, M., Michielin, O., Schapira, M., Spertini, O. (2003) Molecular basis of leukocyte rolling on PSGL-1. Predominant role of core-2 O-glycans and of tyrosine sulfate residue 51. J. Biol. Chem. 278, 37-47. (Pubitemid 36043541)
12. Croce, K., Freedman, S. J., Furie, B. C., Furie, B. (1998) Interaction between soluble P-selectin and soluble P-selectin glycoprotein ligand 1: equilibrium binding analysis. Biochemistry 37, 16472-16480. (Pubitemid 28543905)
13. Lichtenthaler, S. F., Dominguez, D. I., Westmeyer, G. G., Reiss, K., Haass, C., Saftig, P., De Strooper, B., Seed, B. (2003) The cell adhesion protein P-selectin glycoprotein ligand-1 is a substrate for the aspartyl protease BACE1. J. Biol. Chem. 278, 48713-48719. (Pubitemid 41079512)
14. Wang, K., Zhou, Z., Zhou, X., Tarakji, K., Topol, E. J., Lincoff, A. M. (2001) Prevention of intimal hyperplasia with recombinant soluble P-selectin glycoprotein ligand-immunoglobulin in the porcine coronary artery balloon injury model. J. Am. Coll. Cardiol. 38, 577-582. (Pubitemid 32721791)
15. Theoret, J. F., Bienvenu, J. G., Kumar, A., Merhi, Y. (2001) P-selectin antagonism with recombinant P-selectin glycoprotein ligand-1 (rPSGL-Ig) inhibits circulating activated platelet binding to neutrophils induced by damaged arterial surfaces. J. Pharmacol. Exp. Ther. 298, 658-664. (Pubitemid 32673417)
16. Yang, J., Hirata, T., Croce, K., Merrill-Skoloff, G., Tchernychev, B., Williams, E., Flaumenhaft, R., Furie, B. C., Furie, B. (1999) Targeted gene disruption demonstrates that P-selectin glycoprotein ligand 1 (PSGL-1) is required for P-selectin-mediated but not E-selectin-mediated neutrophil rolling and migration. J. Exp. Med. 190, 1769-1782. (Pubitemid 30013843)
17. Xia, L., Sperandio, M., Yago, T., McDaniel, J. M., Cummings, R. D., Pearson-White, S., Ley, K., McEver, R. P. (2002) P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J. Clin. Invest. 109, 939-950. (Pubitemid 34275115)
18. Veldman, G. M., Bean, K. M., Cumming, D. A., Eddy, R. L., Sait, S. N., Shows, T. B. (1995) Genomic organization and chromosomal localization of the gene encoding human P-selectin glycoprotein ligand. J. Biol. Chem. 270, 16470-16475.
19. Afshar-Kharghan, V., Diz-Kucukkaya, R., Ludwig, E. H., Marian, A. J., Lopez, J. A. (2001) Human polymorphism of P-selectin glycoprotein ligand 1 attributable to variable numbers of tandem decameric repeats in the mucinlike region. Blood 97, 3306-3307.
20. Tregouet, D. A., Barbaux, S., Poirier, O., Blankenberg, S., Bickel, C., Escolano, S., Rupprecht, H. J., Meyer, J., Cambien, F., Tiret, L. (2003) SELPLG gene polymorphisms in relation to plasma SELPLG levels and coronary artery disease. Ann. Hum. Genet. 67, 504-511. (Pubitemid 38016711)
21. Lozano, M. L., Gonzalez-Conejero, R., Corral, J., Rivera, J., Iniesta, J. A., Martinez, C., Vicente, V. (2001) Polymorphisms of P-selectin glycoprotein ligand-1 are associated with neutrophil-platelet adhesion and with ischemic cerebrovascular disease. Br. J. Haematol. 115, 969-976. (Pubitemid 34042918)
22. Bugert, P., Hoffmann, M. M., Winkelmann, B. R., Vosberg, M., Jahn, J., Entelmann, M., Katus, H. A., Marz, W., Mansmann, U., Boehm, B. O., Goerg, S., Kluter, H. (2003) The variable number of tandem repeat polymorphism in the P-selectin glycoprotein ligand-1 gene is not associated with coronary heart disease. J. Mol. Med. 81, 495-501. (Pubitemid 37070202)
23. Bugert, P., Vosberg, M., Entelmann, M., Jahn, J., Katus, H. A., Kluter, H. (2004) Polymorphisms in the P-selectin (CD62P) and P-selectin glycoprotein ligand-1 (PSGL-1) genes and coronary heart disease. Clin. Chem. Lab. Med. 42, 997-1004. (Pubitemid 39307388)
24. Roldan, V., Gonzalez-Conejero, R., Marin, F., Pineda, J., Vicente, V., Corral, J. (2004) Short alleles of P-selectin glycoprotein ligand-1 protect against premature myocardial infarction. Am. Heart J. 148, 602-605. (Pubitemid 39349378)
25. Scalabrini, D., Galimberti, D., Fenoglio, C., Comi, C., De Riz, M., Venturelli, E., Castelli, L., Piccio, L., Ronzoni, M., Lovati, C., Mariani, C., Monaco, F., Bresolin, N., Scarpini, E. (2005) P-selectin glycoprotein ligand-1 variable number of tandem repeats (VNTR) polymorphism in patients with multiple sclerosis. Neurosci. Lett. 388, 149-152. (Pubitemid 41208210)
26. Diz-Kucukkaya, R., Inanc, M., Afshar-Kharghan, V., Zhang, Q. E., Lopez, J. A., Pekcelen, Y. (2007) P-selectin glycoprotein ligand-1 VNTR polymorphisms and risk of thrombosis in the antiphospholipid syndrome. Ann. Rheum. Dis. 66, 1378-1380. (Pubitemid 47492485)
27. Ozben, B., Diz-Kucukkaya, R., Bilge, A. K., Hancer, V. S., Oncul, A. (2007) The association of P-selectin glycoprotein ligand-1 VNTR polymorphisms with coronary stent restenosis. J. Thromb. Thrombolysis 23, 181-187. (Pubitemid 46564117)
28. Volcik, K. A., Ballantyne, C. M., Coresh, J., Folsom, A. R., Boerwinkle, E. (2007) Specific P-selectin and P-selectin glycoprotein ligand-1 genotypes/haplotypes are associated with risk of incident CHD and ischemic stroke: the Atherosclerosis Risk in Communities (ARIC) study. Atherosclerosis 195, e76-e82. (Pubitemid 47561962)
29. Zhu, C., Yago, T., Lou, J., Zarnitsyna, V. I., McEver, R. P. (2008) Mechanisms for flow-enhanced cell adhesion. Ann. Biomed. Eng. 36, 604-621.
30. Thomas, W. E., Vogel, V., Sokurenko, E. (2008) Biophysics of catch bonds. Annu. Rev. Biophys. 37, 399-416.
31. Dembo, M., Torney, D. C., Saxman, K., Hammer, D. (1988) The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. R. Soc. Lond. B Biol. Sci. 234, 55-83.
32. Marshall, B. T., Long, M., Piper, J. W., Yago, T., McEver, R. P., Zhu, C. (2003) Direct observation of catch bonds involving cell-adhesion molecules. Nature 423, 190-193. (Pubitemid 36569544)
33. Sarangapani, K. K., Yago, T., Klopocki, A. G., Lawrence, M. B., Fieger, C. B., Rosen, S. D., McEver, R. P., Zhu, C. (2004) Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J. Biol. Chem. 279, 2291-2298. (Pubitemid 38084502)
34. Evans, E., Leung, A., Heinrich, V., Zhu, C. (2004) Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Natl. Acad. Sci. USA 101, 11281-11286. (Pubitemid 39038338)
35. Heinrich, V., Leung, A., Evans, E. (2005) Nano-to-microscale mechanical switches and fuses mediate adhesive contacts between leukocytes and the endothelium. J. Chem. Inf. Model. 45, 1482-1490. (Pubitemid 41784713)
36. Evans, E., Ritchie, K., Merkel, R. (1995) Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. Biophys. J. 68, 2580-2587.
37. Pincet, F., Husson, J. (2005) The solution to the streptavidin-biotin paradox: the influence of history on the strength of single molecular bonds. Biophys. J. 89, 4374-4381. (Pubitemid 41725655)
38. Merkel, R., Nassoy, P., Leung, A., Ritchie, K., Evans, E. (1999) Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397, 50-53. (Pubitemid 29038244)
39. Evans, E., Williams, P. M. (2002) Dynamic Force Spectroscopy. In: Physics of Biol-Molecules and Cells (F. Julicher, P. Ormos, F. David, H. Flyvbjerg, eds.), Berlin, Springer-Verlag, 145.
40. Husson, J., Pincet, F. (2008) Analyzing single-bond experiments: influence of the shape of the energy landscape and universal law between the width, depth, and force spectrum of the bond. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 77, 026108. (Pubitemid 351366273)
41. Perret, E., Leung, A., Feracci, H., Evans, E. (2004) Trans-bonded pairs of E-cadherin exhibit a remarkable hierarchy of mechanical strengths. Proc. Natl. Acad. Sci. USA 101, 16472-16477. (Pubitemid 39557737)
42. Gao, J. M., Xiang, R. L., Jiang, L., Li, W. H., Feng, Q. P., Guo, Z. J., Sun, Q., Zeng, Z. P., Fang, F. D. (2009) Sulfated tyrosines 27 and 29 in the N-terminus of human CXCR3 participate in binding native IP-10. Acta Pharmacol. Sin. 30, 193-201.
43. Yun, H. Y., Keutmann, H. T., Eipper, B. A. (1994) Alternative splicing governs sulfation of tyrosine or oligosaccharide on peptidylglycine α-amidating monooxygenase. J. Biol. Chem. 269, 10946-10955.
44. Wilkins, P. P., Moore, K. L., McEver, R. P., Cummings, R. D. (1995) Tyrosine sulfation of P-selectin glycoprotein ligand-1 is required for high affinity binding to P-selectin. J. Biol. Chem. 270, 22677-22680.
45. Sako, D., Comess, K. M., Barone, K. M., Camphausen, R. T., Cumming, D. A., Shaw, G. D. (1995) A sulfated peptide segment at the amino terminus of PSGL-1 is critical for P-selectin binding. Cell 83, 323-331.
46. Leppanen, A., White, S. P., Helin, J., McEver, R. P., Cummings, R. D. (2000) Binding of glycosulfopeptides to P-selectin requires stereospecific contributions of individual tyrosine sulfate and sugar residues. J. Biol. Chem. 275, 39569-39578. (Pubitemid 32058983)
47. Walcheck, B., Leppanen, A., Cummings, R. D., Knibbs, R. N., Stoolman, L. M., Alexander, S. R., Mattila, P. E., McEver, R. P. (2002) The monoclonal antibody CHO-131 binds to a core 2 O-glycan terminated with sialyl-Lewis x, which is a functional glycan ligand for P-selectin. Blood 99, 4063-4069. (Pubitemid 35332048)
48. Epperson, T. K., Patel, K. D., McEver, R. P., Cummings, R. D. (2000) Noncovalent association of P-selectin glycoprotein ligand-1 and minimal determinants for binding to P-selectin. J. Biol. Chem. 275, 7839-7853.
49. Snapp, K. R., Craig, R., Herron, M., Nelson, R. D., Stoolman, L. M., Kansas, G. S. (1998) Dimerization of P-selectin glycoprotein ligand-1 (PSGL-1) required for optimal recognition of P-selectin. J. Cell Biol. 142, 263-270. (Pubitemid 28341156)
50. Ramachandran, V., Yago, T., Epperson, T. K., Kobzdej, M. M., Nollert, M. U., Cummings, R. D., Zhu, C., McEver, R. P. (2001) Dimerization of a selectin and its ligand stabilizes cell rolling and enhances tether strength in shear flow. Proc. Natl. Acad. Sci. USA 98, 10166-10171. (Pubitemid 32802992)
51. Evans, E., Heinrich, V., Leung, A., Kinoshita, K. (2005) Nano- to microscale dynamics of P-selectin detachment from leukocyte interfaces. I. Membrane separation from the cytoskeleton. Biophys. J. 88, 2288-2298. (Pubitemid 40976235)
52. Snapp, K. R., Heitzig, C. E., Kansas, G. S. (2002) Attachment of the PSGL-1 cytoplasmic domain to the actin cytoskeleton is essential for leukocyte rolling on P-selectin. Blood 99, 4494-4502.
53. Miner, J. J., Xia, L., Yago, T., Kappelmayer, J., Liu, Z., Klopocki, A. G., Shao, B., McDaniel, J. M., Setiadi, H., Schmidtke, D. W., McEver, R. P. (2008) Separable requirements for cytoplasmic domain of PSGL-1 in leukocyte rolling and signaling under flow. Blood 112, 2035-2045.
54. Bruehl, R. E., Moore, K. L., Lorant, D. E., Borregaard, N., Zimmerman, G. A., McEver, R. P., Bainton, D. F. (1997) Leukocyte activation induces surface redistribution of P-selectin glycoprotein ligand-1. J. Leukoc. Biol. 61, 489-499. (Pubitemid 27219843)
55. Itoh, S., Susuki, C., Takeshita, K., Nagata, K., Tsuji, T. (2007) Redistribution of P-selectin glycoprotein ligand-1 (PSGL-1) in chemokine-treated neutrophils: a role of lipid microdomains. J. Leukoc. Biol. 81, 1414-1421. (Pubitemid 46827964)
56. Liu, W., Ramachandran, V., Kang, J., Kishimoto, T. K., Cummings, R. D., McEver, R. P. (1998) Identification of N-terminal residues on P-selectin glycoprotein ligand-1 required for binding to P-selectin. J. Biol. Chem. 273, 7078-7087. (Pubitemid 28160377)
57. Lou, J., Yago, T., Klopocki, A. G., Mehta, P., Chen, W., Zarnitsyna, V. I., Bovin, N. V., Zhu, C., McEver, R. P. (2006) Flow-enhanced adhesion regulated by a selectin interdomain hinge. J. Cell Biol. 174, 1107-1117. (Pubitemid 44455197)
58. Phan, U. T., Waldron, T. T., Springer, T. A. (2006) Remodeling of the lectin-EGF-like domain interface in P- and L-selectin increases adhesiveness and shear resistance under hydrodynamic force. Nat. Immunol. 7, 883-889.
59. Klopocki, A. G., Yago, T., Mehta, P., Yang, J., Wu, T., Leppanen, A., Bovin, N. V., Cummings, R. D., Zhu, C., McEver, R. P. (2008) Replacing a lectin domain residue in L-selectin enhances binding to P-selectin glycoprotein ligand-1 but not to 6-sulfo-sialyl Lewis x. J. Biol. Chem. 283, 11493-11500.
60. Tregouet, D. A., Barbaux, S., Escolano, S., Tahri, N., Golmard, J. L., Tiret, L., Cambien, F. (2002) Specific haplotypes of the P-selectin gene are associated with myocardial infarction. Hum. Mol. Genet. 11, 2015-2023. (Pubitemid 34919276)