Abstract
Circulating leukocytes in trafficking to the inflammatory sites, will be first tether to, and then roll on the vascular surface. This event is mediated through specific interaction of P-selectin and P-selectin glycoprotein ligand-1 (PSGL-1), and regulated by hemodynamics. Poor data were reported in understanding P-selectin-mediated rolling. With the flow chamber technique, we herein observed HL-60 cell rolling on P-selectin with or without 3% Ficoll at various wall shear stresses from 0.05 to 0.4 dyn/cm2. The results demonstrated that force rather than transport regulated the rolling, similar to rolling on L- and E-selectin. The rolling was accelerated quickly by an increasing force below the optimal shear threshold of 0.15 dyn/cm2 first and then followed by a slowly decelerating phase starting at the optimum, showing a catch-slip transition and serving as a mechanism for the rolling. The catch-slip transition was completely reflected to the tether lifetime and other rolling parameters, such as the mean and fractional stop time. The narrow catch bond regime stabilized the rolling quickly, through steeply increasing fractional stop time to a plateau of about 0.85. Data presented here suggest that the low shear stress threshold serves as a mechanism for most cell rolling events through P-selectin.
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Ley K, Bullard D C, Arbones M L, et al. Sequential contribution of L- and P-selectin to leukocyte rolling in vivo. J Exp Med, 1995, 181: 669–675
Sundd P, Pospieszalska M K, Cheung L S, et al. Biomechanics of leukocyte rolling. Biorheology, 2011, 48: 1–35
Berman C L, Yeo E L, Wencel-Drake J D, et al. A platelet alpha granule membrane protein that is associated with the plasma membrane after activation. J Clin Invest, 1986, 78: 130–137
McEver R P, Beckstead J H, Moore K L, et al. GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest, 1989, 84: 92–99
Graves B J, Crowther R L, Chandran C, et al. Insight into E-selectin/ligand interaction from the crystal structure and mutagenesis of the lec/EGF domains. Nature, 1994, 367: 532–538
Somers W S, Tang J, Shaw G D, et al. Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLex and PSGL-1. Cell, 2000, 103: 467–479
McEver R P, Zhu C. Rolling cell adhesion. Annu Rev Cell Dev Biol, 2010, 26: 363–396
Bell G I. Models for the specific adhesion of cells to cells. Science, 1978, 200: 618–627
Dembo M, Torney D C, Saxman K, et al. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc R Soc London B Biol Sci, 1988, 234: 55–83
Lou J, Yago T, Klopocki A G, et al. Flow-enhanced adhesion regulated by a selectin interdomain hinge. J Cell Biol, 2006, 174: 1107–1117
Lou J, Zhu C. A structure-based sliding-rebinding mechanism for catch bonds. Biophys J, 2007, 92: 1471–1485
Yago T, Wu J, Wey C D, et al. Catch bonds govern adhesion through L-selectin at threshold shear. J Cell Biol, 2004, 166: 913–923
Marshall B T, Long M, Piper J W, et al. Direct observation of catch bonds involving cell-adhesion molecules. Nature, 2003, 423: 190–193
Li Q, Fang Y, Ding X, et al. Force-dependent bond dissociation govern rolling of HL-60 cells through E-selectin. Exp Cell Res, 2012, 318: 1649–1658
Yago T, Lou J, Wu T, et al. Platelet glycoprotein Ibalpha forms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J Clin Invest, 2008, 118: 3195–3207
Thomas W, Forero M, Yakovenko O, et al. Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophys J, 2006, 90: 753–764
Li Z J, Mohamed N, Ross J M. Shear stress affects the kinetics of Staphylococcus aureus adhesion to collagen. Biotechnol Prog, 2000, 16: 1086–1090
Wayman A M, Chen W, McEver R P, et al. Triphasic force dependence of E-selectin/ligand dissociation governs cell rolling under flow. Biophys J, 2010, 99: 1166–1174
Sarangapani K K, Yago T, Klopocki A G, et al. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J Biol Chem, 2004, 279: 2291–2298
Edmondson K E, Denney W S, Diamond S L. Neutrophil-bead collision assay: Pharmacologically induced changes in membrane mechanics regulate the PSGL-1/P-selectin adhesion lifetime. Biophys J, 2005, 89: 3603–3614
Chen S, Alon R, Fuhlbrigge R C, et al. Rolling and transient tethering of leukocytes on antibodies reveal specializations of selectins. Proc Natl Acad Sci USA, 1997, 94: 3172–3177
Chesla S E, Selvaraj P, Zhu C. Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys J, 1998, 75: 1553–1572
Piper J W, Swerlick R A, Zhu C. Determining force dependence of two-dimensional receptor-ligand binding affinity by centrifugation. Biophys J, 1998, 74: 492–513
Shao J Y, Xu G. The adhesion between a microvillus-bearing cell and a ligand-coated substrate: A Monte Carlo study. Ann Biomed Eng, 2007, 35: 397–407
Ham A S, Goetz D J, Klibanov AL, et al. Microparticle adhesive dynamics and rolling mediated by selectin-specific antibodies under flow. Biotechnol Bioeng, 2007, 96: 596–607
Hong S, Lee D, Zhang H, et al. Covalent immobilization of P-selectin enhances cell rolling. Langmuir, 2007, 23: 12261–12268
Lee D, King M K. Microcontact printing of P-selectin increases the rate of neutrophil recruitment under shear flow. Biotechnol Prog, 2008, 24: 1052–1059
Guenther F, von zur Muhlen C, Ferrante E A, et al. An ultrasound contrast agent targeted to P-selectin detects activated platelets at supra-arterial shear flow conditions. Invest Radiol, 2010, 45: 586–591
Gee D J, Wright L K, Zimmermann J, et al. Dimethylsulfoxide exposure modulates HL-60 cell rolling interactions. Biosci Rep, 2012, 32: 375–382
Pereverzev Y V, Prezhdo O V, Forero M, et al. The two-pathway model for the catch-slip transition in biological adhesion. Biophys J, 2005, 89: 1446–1454
Pereverzev Y V, Prezhdo O V. Force-induced deformations and stability of biological bonds. Phys Rev E, 2006, 73: 050902
Klopocki A G, Yago T, Mehta P, et al. 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, 2008, 283: 11493–11500
Mehta P, Cummings R D, McEver P R. Affinity and kinetic analysis of P-selectin binding to P-selectin glycoprotein ligand-1. J Biol Chem, 1998, 273: 32506–32513
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Ling, Y., Fang, Y., Yang, X. et al. Regulation of shear stress on rolling behaviors of HL-60 cells on P-selectin. Sci. China Phys. Mech. Astron. 57, 1998–2006 (2014). https://doi.org/10.1007/s11433-013-5270-7
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DOI: https://doi.org/10.1007/s11433-013-5270-7