Elongated Membrane Tethers, Individually Anchored by High Affinity α4β1/VCAM-1 Complexes, Are the Quantal Units of Monocyte Arrests

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Chu, Calvin ^a   Celik, Emrah ^a   Rico, Felix ^a   Moy, Vincent T ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCYTE CHEMOTACTIC PROTEIN 1; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4; MULTIPROTEIN COMPLEX;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; CELL MEMBRANE; CELL POPULATION; CELL STIMULATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; MONOCYTE; PROTEIN BINDING; PROTEIN EXPRESSION; CELL ADHESION; METABOLISM; NONPARAMETRIC TEST; PHYSIOLOGY; TUMOR CELL LINE; VASCULAR ENDOTHELIUM;

CELL ADHESION; CELL LINE, TUMOR; CELL MEMBRANE; ENDOTHELIUM, VASCULAR; HUMANS; INTEGRIN ALPHA4BETA1; MICROSCOPY, ATOMIC FORCE; MONOCYTES; MULTIPROTEIN COMPLEXES; STATISTICS, NONPARAMETRIC; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84877872228     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064187     Document Type: Article

References (52)

1. Grabovsky V, Feigelson S, Chen C, Bleijs DA, Peled A, et al. (2000) Subsecond induction of alpha4 integrin clustering by immobilized chemokines stimulates leukocyte tethering and rolling on endothelial vascular cell adhesion molecule 1 under flow conditions. J Exp Med 192: 495-506.
2. McEver RP, Cummings RD, (1997) Perspectives series: cell adhesion in vascular biology. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 100: 485-491.
3. Marshall BT, Long M, Piper JW, Yago T, McEver RP, et al. (2003) Direct observation of catch bonds involving cell-adhesion molecules. Nature 423: 190-193.
4. Sundd P, Gutierrez E, Pospieszalska MK, Zhang H, Groisman A, et al. (2010) Quantitative dynamic footprinting microscopy reveals mechanisms of neutrophil rolling. Nat Methods 7: 821-824.
5. McEver RP, Zhu C, (2010) Rolling cell adhesion. Annu Rev Cell Dev Biol 26: 363-396.
6. Sundd P, Gutierrez E, Koltsova EK, Kuwano Y, Fukuda S, et al. (2012) 'Slings' enable neutrophil rolling at high shear. Nature 488 (7411) (): 399-403.
7. Takagi J, Petre BM, Walz T, Springer TA, (2002) Global Conformational Rearrangements in Integrin Extracellular Domains in Outside-In and Inside-Out Signaling. Cell 110: 599-611.
8. Simon SI, Green CE, (2005) Molecular mechanics and dynamics of leukocyte recruitment during inflammation. Annual Review of Biomedical Engineering 7: 151-185.
9. Chigaev A, Buranda T, Dwyer DC, Prossnitz ER, Sklar LA, (2003) FRET detection of cellular alpha4-integrin conformational activation. Biophys J 85: 3951-3962.
10. Chan JR, Hyduk SJ, Cybulsky MI, (2003) Detecting rapid and transient upregulation of leukocyte integrin affinity induced by chemokines and chemoattractants. J Immunol Methods 273: 43-52.
11. DiVietro JA, Brown DC, Sklar LA, Larson RS, Lawrence MB, (2007) Immobilized stromal cell-derived factor-1alpha triggers rapid VLA-4 affinity increases to stabilize lymphocyte tethers on VCAM-1 and subsequently initiate firm adhesion. J Immunol 178: 3903-3911.
12. Alon R, Feigelson SW, Manevich E, Rose DM, Schmitz J, et al. (2005) Alpha4beta1-dependent adhesion strengthening under mechanical strain is regulated by paxillin association with the alpha4-cytoplasmic domain. J Cell Biol 171: 1073-1084.
13. Rullo J, Becker H, Hyduk SJ, Wong JC, Digby G, et al. (2012) Actin polymerization stabilizes alpha4beta1 integrin anchors that mediate monocyte adhesion. J Cell Biol 197: 115-129.
14. Boring L, Gosling J, Cleary M, Charo IF, (1998) Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394: 894-897.
15. Chow F, Ozols E, Nikolic-Paterson DJ, Atkins RC, Tesch GH, (2004) Macrophages in mouse type 2 diabetic nephropathy: correlation with diabetic state and progressive renal injury. Kidney Int 65: 116-128.
16. Alam R, York J, Boyars M, Stafford S, Grant JA, et al. (1996) Increased MCP-1, RANTES, and MIP-1alpha in bronchoalveolar lavage fluid of allergic asthmatic patients. Am J Respir Crit Care Med 153: 1398-1404.
17. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, et al. (2003) Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci U S A 100: 7947-7952.
18. Kim JS, Gautam SC, Chopp M, Zaloga C, Jones ML, et al. (1995) Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat. J Neuroimmunol 56: 127-134.
19. Ferreira AM, Isaacs H, Hayflick JS, Rogers KA, Sandig M, (2006) The p110delta isoform of PI3K differentially regulates beta1 and beta2 integrin-mediated monocyte adhesion and spreading and modulates diapedesis. Microcirculation 13: 439-456.
20. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, et al. (1980) Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 26: 171-176.
21. Ashida N, Arai H, Yamasaki M, Kita T, (2001) Distinct signaling pathways for MCP-1-dependent integrin activation and chemotaxis. J Biol Chem 276: 16555-16560.
22. Florin EL, Moy VT, Gaub HE, (1994) Adhesion Forces Between Individual Ligand-Receptor Pairs. Science 264: 415-417.
23. Hutter J, Bechhoefer J, (1993) Calibration of atomic-force microscope tips. Rev Sci Instrum 64: 1868-1873.
24. Zhang X, Wojcikiewicz E, Moy VT, (2002) Force spectroscopy of the leukocyte function-associated antigen- 1/intercellular adhesion molecule-1 interaction. Biophys J 83: 2270-2279.
25. Rico F, Chu C, Abdulreda MH, Qin Y, Moy VT, (2010) Temperature modulation of integrin-mediated cell adhesion. Biophysical Journal 99: 1387-1396.
26. Tees DF, Waugh RE, Hammer DA, (2001) A microcantilever device to assess the effect of force on the lifetime of selectin-carbohydrate bonds. Biophys J 80: 668-682.
27. Krieg M, Helenius J, Heisenberg CP, Muller DJ, (2008) A Bond for a Lifetime: Employing Membrane Nanotubes from Living Cells to Determine Receptor-Ligand Kinetics. Angewandte Chemie-International Edition 47: 9775-9777.
28. Bell GI, (1978) Models for the specific adhesion of cells to cells. Science 200: 618-627.
29. Evans E, Ritchie K, (1997) Dynamic strength of molecular adhesion bonds. Biophysical Journal 72: 1541-1555.
30. Hyduk SJ, Chan JR, Duffy ST, Chen M, Peterson MD, et al. (2007) Phospholipase C, calcium, and calmodulin are critical for alpha4beta1 integrin affinity up-regulation and monocyte arrest triggered by chemoattractants. Blood 109: 176-184.
31. Jing Q, Xin SM, Zhang WB, Wang P, Qin YW, et al. (2000) Lysophosphatidylcholine activates p38 and p42/44 mitogen-activated protein kinases in monocytic THP-1 cells, but only p38 activation is involved in its stimulated chemotaxis. Circ Res 87: 52-59.
32. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE, (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276: 1109-1112.
33. Afrin R, Arakawa H, Osada T, Ikai A, (2003) Extraction of membrane proteins from a living cell surface using the atomic force microscope and covalent crosslinkers. Cell Biochem Biophys 39: 101-117.
34. Zhang X, Craig SE, Kirby H, Humphries MJ, Moy VT, (2004) Molecular basis for the dynamic strength of the integrin alpha4beta1/VCAM-1 interaction. Biophys J 87: 3470-3478.
35. Hochmuth FM, Shao JY, Dai J, Sheetz MP, (1996) Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys J 70: 358-369.
36. Sun M, Graham JS, Hegedus B, Marga F, Zhang Y, et al. (2005) Multiple membrane tethers probed by atomic force microscopy. Biophysical Journal 89: 4320-4329.
37. Brochard-Wyart F, Borghi N, Cuvelier D, Nassoy P, (2006) Hydrodynamic narrowing of tubes extruded from cells. Proc Natl Acad Sci U S A 103: 7660-7663.
38. Afrin R, Ikai A, (2006) Force profiles of protein pulling with or without cytoskeletal links studied by AFM. Biochemical and Biophysical Research Communications 348: 238-244.
39. Hosu BG, Sun M, Marga F, Grandbois M, Forgacs G, (2007) Eukaryotic membrane tethers revisited using magnetic tweezers. Phys Biol 4: 67-78.
40. Sun M, Northup N, Marga F, Huber T, Byfield FJ, et al. (2007) The effect of cellular cholesterol on membranecytoskeleton adhesion. Journal of Cell Science 120: 2223-2231.
41. Kong F, Garcia AJ, Mould AP, Humphries MJ, Zhu C, (2009) Demonstration of catch bonds between an integrin and its ligand. J Cell Biol 185: 1275-1284.
42. Dembo M, Torney DC, 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.
43. Williams PM, (2003) Analytical descriptions of dynamic force spectroscopy: behaviour of multiple connections. Analytica Chimica Acta 479: 107-115.
44. Berlin C, Bargatze RF, Campbell JJ, von Andrian UH, Szabo MC, et al. (1995) alpha 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell 80: 413-422.
45. Wojcikiewicz EP, Zhang X, Chen A, Moy VT, (2003) Contributions of molecular binding events and cellular compliance to the modulation of leukocyte adhesion. Journal of Cell Science 116: 2531-2539.
46. van Kooyk Y, Figdor CG, (2000) Avidity regulation of integrins: the driving force in leukocyte adhesion. Curr Opin Cell Biol 12: 542-547.
47. Carman CV, Springer TA, (2003) Integrin avidity regulation: are changes in affinity and conformation underemphasized? Curr Opin Cell Biol 15: 547-556.
48. Brown MJ, Nijhara R, Hallam JA, Gignac M, Yamada KM, et al. (2003) Chemokine stimulation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization. Blood 102: 3890-3899.
49. Hao JJ, Liu Y, Kruhlak M, Debell KE, Rellahan BL, et al. (2009) Phospholipase C-mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane. J Cell Biol 184: 451-462.
50. Fu GH, (2007) An extension of Hertz's theory in contact mechanics. J Appl Mech 74: 373-374.
51. Goldman AJ, Cox RG, Brenner H, (1967) Slow viscous motion of a sphere parallel to a plane wall-II Couette flow. Chem Eng Sci 22: 653-660.
52. Tissot O, Pierres A, Foa C, Delaage M, Bongrand P, (1992) Motion of cells sedimenting on a solid surface in a laminar shear flow. Biophys J 61: 204-215.