Live Cell Imaging of Paxillin in Rolling Neutrophils by Dual-Color Quantitative Dynamic Footprinting

Microcirculation

Volumn 18, Issue 5, 2011, Pages 361-372

  Sundd, Prithu ^a   Gutierrez, Edgar ^b   Petrich, Brian G ^c   Ginsberg, Mark H ^c   Groisman, Alex ^b   Ley, Klaus ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DqDF; Footprint; P selectin; TIRF

Indexed keywords

CYTOSKELETON PROTEIN; DII DYE; DIO DYE; FLUORESCENT DYE; FLUOROCHROME; HYBRID PROTEIN; PAXILLIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL MEMBRANE; CONTROLLED STUDY; DUAL COLOR QUANTITATIVE DYNAMIC FOOTPRINTING; FLUOROCHROME STAINING; LABELING INDEX; MICROVILLUS; MOLECULAR IMAGING; MOUSE; NEUTROPHIL; NONHUMAN; PERFUSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOOTPRINTING; PROTEIN LOCALIZATION;

ANIMALS; CARBOCYANINES; FLUORESCENT DYES; LEUKOCYTE ROLLING; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; NEUTROPHILS; PAXILLIN; RECOMBINANT FUSION PROTEINS;

MUS;

EID: 79959857642     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/j.1549-8719.2011.00090.x     Document Type: Article

References (60)

1. Alon R, Hammer DA, Springer TA. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 374: 539-542, 1995.
2. Alon R, Ley K. Cells on the run: shear-regulated integrin activation in leukocyte rolling and arrest on endothelial cells. Curr Opin Cell Biol 20: 525-532, 2008.
3. Bolte S, Brown S, Satiat-Jeunemaitre B. The N-myristoylated Rab-GTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells. J Cell Sci 117: 943-954, 2004.
4. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-232, 2006.
5. Brzezinska AA, Johnson JL, Munafo DB, Crozat K, Beutler B, Kiosses WB, Ellis BA, Catz SD. The Rab27a effectors JFC1/Slp1 and Munc13-4 regulate exocytosis of neutrophil granules. Traffic 9: 2151-2164, 2008.
6. Burns A, Bowden R, Abe Y, Walker D, Simon S, Entman M, Smith C. P-selectin mediates neutrophil adhesion to endothelial cell borders. J Leukoc Biol 65: 299-306, 1999.
7. Caputo KE, Hammer DA. Effect of microvillus deformability on leukocyte adhesion explored using adhesive dynamics simulations. Biophys J 89: 187-200, 2005.
8. Chiang EY, Hidalgo A, Chang J, Frenette PS. Imaging receptor microdomains on leukocyte subsets in live mice. Nat Methods 4: 219-222, 2007.
9. Chudakov DM, Verkhusha VV, Staroverov DB, Souslova EA, Lukyanov S, Lukyanov KA. Photoswitchable cyan fluorescent protein for protein tracking. Nat Biotechnol 22: 1435-1439, 2004.
10. Cohen-Hillel E, Mintz R, Meshel T, Garty BZ, Ben-Baruch A. Cell migration to the chemokine CXCL8: paxillin is activated and regulates adhesion and cell motility. Cell Mol Life Sci 66: 884-899, 2009.
11. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86: 3993-4003, 2004.
12. Damiano ER, Westheider J, Tozeren A, Ley K. Variation in the velocity, deformation, and adhesion energy density of leukocytes rolling within venules. Circ Res 79: 1122-1130, 1996.
13. Deakin NO, Turner CE. Paxillin comes of age. J Cell Sci 121: 2435-2444, 2008.
14. Dembo M, Torney DC, Saxman K, Hammer D. The reaction limited kinetics of membrane-to-surface adhesion and detachment. Proc R Soc Lond B Biol Sci 234: 55-83, 1988.
15. Erlandsen SL, Hasslen SR, Nelson RD. Detection and spatial distribution of the beta 2 integrin (Mac-1) and L-selectin (LECAM-1) adherence receptors on human neutrophils by high-resolution field emission SEM. J Histochem Cytochem 41: 327-333, 1993.
16. Fernandez R, Boxer LA, Suchard SJ. Beta2 integrins are not required for tyrosine phosphorylation of paxillin in human neutrophils. J Immunol 159: 5568-5575, 1997.
17. Finger E, Bruehl R, Bainton D, Springer T. A differential role for cell shape in neutrophil tethering and rolling on endothelial selectins under flow. J Immunol 157: 5085-5096, 1996.
18. Firrell JC, Lipowsky HH. Leukocyte margination and deformation in mesenteric venules of rat. Am J Physiol Heart Circ Physiol 256: H1667-H1674, 1989.
19. Fuortes M, Jin WW, Nathan C. Beta 2 integrin-dependent tyrosine phosphorylation of paxillin in human neutrophils treated with tumor necrosis factor. J Cell Biol 127: 1477-1483, 1994.
20. Fuortes M, Melchior M, Han H, Lyon GJ, Nathan C. Role of the tyrosine kinase pyk2 in the integrin-dependent activation of human neutrophils by TNF. J Clin Invest 104: 327-335, 1999.
21. Graham IL, Anderson DC, Holers VM, Brown EJ. Complement receptor 3 (CR3, Mac-1, integrin alpha M beta 2, CD11b/CD18) is required for tyrosine phosphorylation of paxillin in adherent and nonadherent neutrophils. J Cell Biol 127: 1139-1147, 1994.
22. Hammer DA, Apte SM. Simulation of cell rolling and adhesion on surfaces in shear flow: general results and analysis of selectin-mediated neutrophil adhesion. Biophys J 63: 35-57, 1992.
23. Hattori R, Hamilton K, Fugate R, McEver R, Sims P. Stimulated secretion of endothelial von Willebrand factor is accompanied by rapid redistribution to the cell surface of the intracellular granule membrane protein GMP-140. J Biol Chem 264: 7768-7771, 1989.
24. Hyduk SJ, Oh J, Xiao H, Chen M, Cybulsky MI. Paxillin selectively associates with constitutive and chemoattractant-induced high-affinity alpha4beta1 integrins: implications for integrin signaling. Blood 104: 2818-2824, 2004.
25. Jadhav S, Eggleton CD, Konstantopoulos K. A 3-D computational model predicts that cell deformation affects selectin-mediated leukocyte rolling. Biophys J 88: 96-104, 2005.
26. Jamieson JS, Tumbarello DA, Halle M, Brown MC, Tremblay ML, Turner CE. Paxillin is essential for PTP-PEST-dependent regulation of cell spreading and motility: a role for paxillin kinase linker. J Cell Sci 118: 5835-5847, 2005.
27. King MR, Heinrich V, Evans E, Hammer DA. Nano-to-micro scale dynamics of P-selectin detachment from leukocyte interfaces. III. Numerical simulation of tethering under flow. Biophys J 88: 1676-1683, 2005.
28. Lawrence MB, Springer TA. Leukocytes roll on a selectin at physiological flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65: 859-874, 1991.
29. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-689, 2007.
30. Lillemeier BF, Mortelmaier MA, Forstner MB, Huppa JB, Groves JT, Davis MM. TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat Immunol 11: 90-96, 2010.
31. Liu S, Ginsberg MH. Paxillin binding to a conserved sequence motif in the alpha 4 integrin cytoplasmic domain. J Biol Chem 275: 22736-22742, 2000.
32. Liu S, Thomas SM, Woodside DG, Rose DM, Kiosses WB, Pfaff M, Ginsberg MH. Binding of paxillin to alpha4 integrins modifies integrin-dependent biological responses. Nature 402: 676-681, 1999.
33. Lukyanov KA, Chudakov DM, Lukyanov S, Verkhusha VV. Innovation: photoactivatable fluorescent proteins. Nat Rev Mol Cell Biol 6: 885-891, 2005.
34. McEver RP. Rolling back neutrophil adhesion. Nat Immunol 11: 282-284, 2010.
35. Miner JJ, Xia L, Yago T, Kappelmayer J, Liu Z, Klopocki AG, Shao B, McDaniel JM, Setiadi H, Schmidtke DW, McEver RP. Separable requirements for cytoplasmic domain of PSGL-1 in leukocyte rolling and signaling under flow. Blood 112: 2035-2045, 2008.
36. Moore KL, Patel KD, Bruehl RE, Li F, Johnson DA, Lichenstein HS, Cummings RD, Bainton DF, McEver RP. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J Cell Biol 128: 661-671, 1995.
37. Norman KE, Katopodis AG, Thoma G, Kolbinger F, Hicks AE, Cotter MJ, Pockley AG, Hellewell PG. P-selectin glycoprotein ligand-1 supports rolling on E- and P-selectin in vivo. Blood 96: 3585-3591, 2000.
38. Pantazopoulou A, Penalva MA. Organization and dynamics of the Aspergillus nidulans Golgi during apical extension and mitosis. Mol Biol Cell 20: 4335-4347, 2009.
39. Pospieszalska MK, Ley K. Dynamics of microvillus extension and tether formation in rolling leukocytes. Cell Mol Bioeng 2: 207-217, 2009.
40. Pospieszalska MK, Zarbock A, Pickard JE, Ley K. Event-tracking model of adhesion identifies load-bearing bonds in rolling leukocytes. Microcirculation 16: 115-130, 2009.
41. Press WH, Flannery BP, Teukolsky SA, Vetterling WT. Numerical Recipes-The Art of Scientific Computing. New York: Cambridge University Press, 2007, 780-785
42. Ramachandran V, Williams M, Yago T, Schmidtke DW, McEver RP. Dynamic alterations of membrane tethers stabilize leukocyte rolling on P-selectin. Proc Natl Acad Sci U S A 101: 13519-13524, 2004.
43. Romanova LY, Holmes G, Bahte SK, Kovalchuk AL, Nelson PJ, Ward Y, Gueler F, Mushinski JF. Phosphorylation of paxillin at threonine 538 by PKCdelta regulates LFA1-mediated adhesion of lymphoid cells. J Cell Sci 123: 1567-1577, 2010.
44. Rossy J, Schlicht D, Engelhardt B, Niggli V. Flotillins interact with PSGL-1 in neutrophils and, upon stimulation, rapidly organize into membrane domains subsequently accumulating in the uropod. PLoS ONE 4: e5403, 2009.
45. Sachs L. Applied Statistics: A Handbook of Techniques. New York: Springer-Verlag, 1984, pp. 707
46. Schaff UY, Dixit N, Procyk E, Yamayoshi I, Tse T, Simon SI. Orai1 regulates intracellular calcium, arrest, and shape polarization during neutrophil recruitment in shear flow. Blood 115: 657-666, 2010.
47. Schmidtke DW, Diamond SL. Direct observation of membrane tethers formed during neutrophil attachment to platelets or P-selectin under physiological flow. J Cell Biol 149: 719-729, 2000.
48. Schon A, Freire E. Thermodynamics of intersubunit interactions in cholera toxin upon binding to the oligosaccharide portion of its cell surface receptor, ganglioside GM1. Biochemistry 28: 5019-5024, 1989.
49. Shroff H, Galbraith CG, Galbraith JA, White H, Gillette J, Olenych S, Davidson MW, Betzig E. Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proc Natl Acad Sci U S A 104: 20308-20313, 2007.
50. Smith ML, Sperandio M, Galkina EV, Ley K. Autoperfused mouse flow chamber reveals synergistic neutrophil accumulation through P-selectin and E-selectin. J Leukoc Biol 76: 985-993, 2004.
51. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314, 1994.
52. Stock K, Sailer R, Strauss WS, Lyttek M, Steiner R, Schneckenburger H. Variable-angle total internal reflection fluorescence microscopy (VA-TIRFM): realization and application of a compact illumination device. J Microsc 211: 19-29, 2003.
53. Sundd P, Gutierrez E, Pospieszalska MK, Zhang H, Groisman A, Ley K. Quantitative dynamic footprinting microscopy reveals mechanisms of neutrophil rolling. Nat Methods 7: 821-824, 2010.
54. Viola A, Schroeder S, Sakakibara Y, Lanzavecchia A. T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 283: 680-682, 1999.
55. Wang J, Fei B, Geahlen RL, Lu C. Quantitative analysis of protein translocations by microfluidic total internal reflection fluorescence flow cytometry. Lab Chip 10: 2673-2679, 2010.
56. Wang HB, Wang JT, Zhang L, Geng ZH, Xu WL, Xu T, Huo Y, Zhu X, Plow EF, Chen M, Geng JG. P-selectin primes leukocyte integrin activation during inflammation. Nat Immunol 8: 882-892, 2007.
57. West KA, Zhang H, Brown MC, Nikolopoulos SN, Riedy MC, Horwitz AF, Turner CE. The LD4 motif of paxillin regulates cell spreading and motility through an interaction with paxillin kinase linker (PKL). J Cell Biol 154: 161-176, 2001.
58. Wiedenmann J, Ivanchenko S, Oswald F, Schmitt F, Rocker C, Salih A, Spindler KD, Nienhaus GU. EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc Natl Acad Sci U S A 101: 15905-15910, 2004.
59. Zarbock A, Lowell CA, Ley K. Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 26: 773-783, 2007.
60. Abramoff MD, Magelhaes PJ, Ram SJ. Image Processing with ImageJ. Biophotonics International 11: 36-42, 2004.