Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule-1

Eric R. Hentzen, Sriram Neelamegham, Geoffrey S. Kansas, Jennifer A. Benanti, Larry V. McIntire, C. Wayne Smith, Scott I. Simon

Research output: Contribution to journalArticle

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Abstract

The relative contributions of CD11a/CD18 and CD11b/CD18 to the dynamics and strength of neutrophil adhesion to intercellular adhesion molecule (ICAM)-1-transfected cells were examined over the time course of chemotactic stimulation. Suspensions of neutrophils and transfectants were sheared in a cone-plate viscometer, and formation of heterotypic aggregates was measured by 2-color flow cytometry. The 2-body collision theory was used to compute adhesion efficiency, defined as the proportion of collisions between neutrophils and target cells that resulted in capture. ICAM-1 surface density and shear rate both regulated adhesion efficiency. Target cells expressing approximately 1000 ICAM-1 sites/μm 2 (I(low)) were captured with an efficiency of 0.15 at 100 s -1, which decreased to zero at 300 s -1. At 8- fold higher ICAM-1 expression (I(high)) corresponding to levels measured on interleukin-1-stimulated endothelium, efficiency was 0.3 at 100 s -1 and remained above background to 900 s -1. Shear alone was sufficient for CD11a/18-mediated adhesion to ICAM-1, and stimulation with formyl-methionyl- leucyl-phenylalanine boosted capture efficiency through CD11a/CD18 by 4-fold. In comparison, CD11b/CD18 supported one third of this efficiency, but was necessary for aggregate stability over several minutes of shear and at shear stresses exceeding 5 dyne/cm 2. Hydrodynamics influenced capture efficiency predominantly through the collisional contact duration, predicted to be approximately 9 milliseconds for successful capture of I(low) and 4 milliseconds for I(high). The implication is that an increase in ICAM-1 from resting levels to those on inflamed endothelium effectively increases the permissible shear in which capture through β 2-integrins may occur. Neutrophil adhesion to ICAM-1 appears to be a cooperative and sequential process of CD11a-dependent capture followed by CD11b-mediated stabilization.

Original languageEnglish (US)
Pages (from-to)911-920
Number of pages10
JournalBlood
Volume95
Issue number3
StatePublished - Feb 1 2000

Fingerprint

Intercellular Adhesion Molecule-1
Neutrophils
Adhesion
Endothelium
methionyl-leucyl-phenylalanine
Flow cytometry
Viscometers
Hydrodynamics
Interleukin-1
Integrins
Contacts (fluid mechanics)
Shear deformation
Cones
Shear stress
Suspensions
Flow Cytometry
Stabilization
Color
Cells

ASJC Scopus subject areas

  • Hematology

Cite this

Hentzen, E. R., Neelamegham, S., Kansas, G. S., Benanti, J. A., McIntire, L. V., Smith, C. W., & Simon, S. I. (2000). Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule-1. Blood, 95(3), 911-920.

Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule-1. / Hentzen, Eric R.; Neelamegham, Sriram; Kansas, Geoffrey S.; Benanti, Jennifer A.; McIntire, Larry V.; Smith, C. Wayne; Simon, Scott I.

In: Blood, Vol. 95, No. 3, 01.02.2000, p. 911-920.

Research output: Contribution to journalArticle

Hentzen, ER, Neelamegham, S, Kansas, GS, Benanti, JA, McIntire, LV, Smith, CW & Simon, SI 2000, 'Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule-1', Blood, vol. 95, no. 3, pp. 911-920.
Hentzen ER, Neelamegham S, Kansas GS, Benanti JA, McIntire LV, Smith CW et al. Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule-1. Blood. 2000 Feb 1;95(3):911-920.
Hentzen, Eric R. ; Neelamegham, Sriram ; Kansas, Geoffrey S. ; Benanti, Jennifer A. ; McIntire, Larry V. ; Smith, C. Wayne ; Simon, Scott I. / Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule-1. In: Blood. 2000 ; Vol. 95, No. 3. pp. 911-920.
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abstract = "The relative contributions of CD11a/CD18 and CD11b/CD18 to the dynamics and strength of neutrophil adhesion to intercellular adhesion molecule (ICAM)-1-transfected cells were examined over the time course of chemotactic stimulation. Suspensions of neutrophils and transfectants were sheared in a cone-plate viscometer, and formation of heterotypic aggregates was measured by 2-color flow cytometry. The 2-body collision theory was used to compute adhesion efficiency, defined as the proportion of collisions between neutrophils and target cells that resulted in capture. ICAM-1 surface density and shear rate both regulated adhesion efficiency. Target cells expressing approximately 1000 ICAM-1 sites/μm 2 (I(low)) were captured with an efficiency of 0.15 at 100 s -1, which decreased to zero at 300 s -1. At 8- fold higher ICAM-1 expression (I(high)) corresponding to levels measured on interleukin-1-stimulated endothelium, efficiency was 0.3 at 100 s -1 and remained above background to 900 s -1. Shear alone was sufficient for CD11a/18-mediated adhesion to ICAM-1, and stimulation with formyl-methionyl- leucyl-phenylalanine boosted capture efficiency through CD11a/CD18 by 4-fold. In comparison, CD11b/CD18 supported one third of this efficiency, but was necessary for aggregate stability over several minutes of shear and at shear stresses exceeding 5 dyne/cm 2. Hydrodynamics influenced capture efficiency predominantly through the collisional contact duration, predicted to be approximately 9 milliseconds for successful capture of I(low) and 4 milliseconds for I(high). The implication is that an increase in ICAM-1 from resting levels to those on inflamed endothelium effectively increases the permissible shear in which capture through β 2-integrins may occur. Neutrophil adhesion to ICAM-1 appears to be a cooperative and sequential process of CD11a-dependent capture followed by CD11b-mediated stabilization.",
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AU - Kansas, Geoffrey S.

AU - Benanti, Jennifer A.

AU - McIntire, Larry V.

AU - Smith, C. Wayne

AU - Simon, Scott I.

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