Skip to main content
PMC home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1989 Jun;83(6):2008–2017. doi: 10.1172/JCI114111

Cooperative interactions of LFA-1 and Mac-1 with intercellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophils in vitro.

C W Smith 1, S D Marlin 1, R Rothlein 1, C Toman 1, D C Anderson 1
PMCID: PMC303925  PMID: 2566624

Abstract

The adherence of human neutrophils to human umbilical vein endothelial cells (HUVEC) is partially dependent on the CD11/CD18 family of glycoproteins on the neutrophil and ICAM-1 on the HUVEC. The CD18 heterodimer involved in this adherence was evaluated in vitro using subunit-specific monoclonal antibodies (MAbs). The adherence of unstimulated neutrophils to IL-1-stimulated HUVEC was significantly inhibited by anti-CD11a but not CD11b MAbs, while the adherence of fMLP-stimulated neutrophils was significantly inhibited by both anti-CD11a and -CD11b. Anti-CD11a, but not anti-CD11b MAbs, reduced the adherence of unstimulated neutrophils on purified ICAM-1 to the same low level untreated neutrophils exhibited on a control protein, glycophorin. Stimulation with fMLP significantly increased neutrophil attachment to purified ICAM-1, but not to the control protein. Anti-CD11b MAbs reduced this chemotactically augmented adherence to that of unstimulated neutrophils, and in combination with anti-CD11a MAbs reduced adherence to that on the control protein. The results in this report indicate that unstimulated neutrophils exhibit LFA-1-dependent attachment to ICAM-1, and chemotactic stimulation enhances the attachment of human neutrophils to ICAM-1 by a Mac-1-dependent process.

Full text

PDF
2008

Images in this article

2011Image
on p.2011
2012Image
on p.2012
2012Image
on p.2012
2012Image
on p.2012
2013Image
on p.2013
2013Image
on p.2013

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altieri D. C., Edgington T. S. The saturable high affinity association of factor X to ADP-stimulated monocytes defines a novel function of the Mac-1 receptor. J Biol Chem. 1988 May 25;263(15):7007–7015. [PubMed] [Google Scholar]
  2. Anderson D. C., Krishna G. S., Hughes B. J., Mace M. L., Mintz A. A., Smith C. W., Nichols B. L. Impaired polymorphonuclear leukocyte motility in malnourished infants: relationship to functional abnormalities of cell adherence. J Lab Clin Med. 1983 Jun;101(6):881–895. [PubMed] [Google Scholar]
  3. Anderson D. C., Mace M. L., Brinkley B. R., Martin R. R., Smith C. W. Recurrent infection in glycogenosis type Ib: abnormal neutrophil motility related to impaired redistribution of adhesion sites. J Infect Dis. 1981 Mar;143(3):447–459. doi: 10.1093/infdis/143.3.447. [DOI] [PubMed] [Google Scholar]
  4. Anderson D. C., Miller L. J., Schmalstieg F. C., Rothlein R., Springer T. A. Contributions of the Mac-1 glycoprotein family to adherence-dependent granulocyte functions: structure-function assessments employing subunit-specific monoclonal antibodies. J Immunol. 1986 Jul 1;137(1):15–27. [PubMed] [Google Scholar]
  5. Anderson D. C., Schmalsteig F. C., Finegold M. J., Hughes B. J., Rothlein R., Miller L. J., Kohl S., Tosi M. F., Jacobs R. L., Waldrop T. C. The severe and moderate phenotypes of heritable Mac-1, LFA-1 deficiency: their quantitative definition and relation to leukocyte dysfunction and clinical features. J Infect Dis. 1985 Oct;152(4):668–689. doi: 10.1093/infdis/152.4.668. [DOI] [PubMed] [Google Scholar]
  6. Anderson D. C., Schmalstieg F. C., Arnaout M. A., Kohl S., Tosi M. F., Dana N., Buffone G. J., Hughes B. J., Brinkley B. R., Dickey W. D. Abnormalities of polymorphonuclear leukocyte function associated with a heritable deficiency of high molecular weight surface glycoproteins (GP138): common relationship to diminished cell adherence. J Clin Invest. 1984 Aug;74(2):536–551. doi: 10.1172/JCI111451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Arnaout M. A., Wang E. A., Clark S. C., Sieff C. A. Human recombinant granulocyte-macrophage colony-stimulating factor increases cell-to-cell adhesion and surface expression of adhesion-promoting surface glycoproteins on mature granulocytes. J Clin Invest. 1986 Aug;78(2):597–601. doi: 10.1172/JCI112615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Barnstable C. J., Bodmer W. F., Brown G., Galfre G., Milstein C., Williams A. F., Ziegler A. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens-new tools for genetic analysis. Cell. 1978 May;14(1):9–20. doi: 10.1016/0092-8674(78)90296-9. [DOI] [PubMed] [Google Scholar]
  9. Beesley J. E., Pearson J. D., Hutchings A., Carleton J. S., Gordon J. L. Granulocyte migration through endothelium in culture. J Cell Sci. 1979 Aug;38:237–248. doi: 10.1242/jcs.38.1.237. [DOI] [PubMed] [Google Scholar]
  10. Bevilacqua M. P., Pober J. S., Mendrick D. L., Cotran R. S., Gimbrone M. A., Jr Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9238–9242. doi: 10.1073/pnas.84.24.9238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bierer B. E., Burakoff S. J. T cell adhesion molecules. FASEB J. 1988 Jul;2(10):2584–2590. doi: 10.1096/fasebj.2.10.2838364. [DOI] [PubMed] [Google Scholar]
  12. Boyd A. W., Wawryk S. O., Burns G. F., Fecondo J. V. Intercellular adhesion molecule 1 (ICAM-1) has a central role in cell-cell contact-mediated immune mechanisms. Proc Natl Acad Sci U S A. 1988 May;85(9):3095–3099. doi: 10.1073/pnas.85.9.3095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Broudy V. C., Harlan J. M., Adamson J. W. Disparate effects of tumor necrosis factor-alpha/cachectin and tumor necrosis factor-beta/lymphotoxin on hematopoietic growth factor production and neutrophil adhesion molecule expression by cultured human endothelial cells. J Immunol. 1987 Jun 15;138(12):4298–4302. [PubMed] [Google Scholar]
  14. Buchanan M. R., Crowley C. A., Rosin R. E., Gimbrone M. A., Jr, Babior B. M. Studies on the interaction between GP-18-0-deficient neutrophils and vascular endothelium. Blood. 1982 Jul;60(1):160–165. [PubMed] [Google Scholar]
  15. Charo I. F., Yuen C., Perez H. D., Goldstein I. M. Chemotactic peptides modulate adherence of human polymorphonuclear leukocytes to monolayers of cultured endothelial cells. J Immunol. 1986 May 1;136(9):3412–3419. [PubMed] [Google Scholar]
  16. Dana N., Styrt B., Griffin J. D., Todd R. F., 3rd, Klempner M. S., Arnaout M. A. Two functional domains in the phagocyte membrane glycoprotein Mo1 identified with monoclonal antibodies. J Immunol. 1986 Nov 15;137(10):3259–3263. [PubMed] [Google Scholar]
  17. Detmers P. A., Wright S. D., Olsen E., Kimball B., Cohn Z. A. Aggregation of complement receptors on human neutrophils in the absence of ligand. J Cell Biol. 1987 Sep;105(3):1137–1145. doi: 10.1083/jcb.105.3.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dougherty G. J., Murdoch S., Hogg N. The function of human intercellular adhesion molecule-1 (ICAM-1) in the generation of an immune response. Eur J Immunol. 1988 Jan;18(1):35–39. doi: 10.1002/eji.1830180107. [DOI] [PubMed] [Google Scholar]
  19. Dunn C. J., Fleming W. E. Increased adhesion of polymorphonuclear leukocytes to vascular endothelium by specific interaction of endogenous (interleukin-1) and exogenous (lipopolysaccharide) substances with endothelial cells 'in vitro'. Eur J Rheumatol Inflamm. 1984;7(3):80–86. [PubMed] [Google Scholar]
  20. Dustin M. L., Rothlein R., Bhan A. K., Dinarello C. A., Springer T. A. Induction by IL 1 and interferon-gamma: tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). J Immunol. 1986 Jul 1;137(1):245–254. [PubMed] [Google Scholar]
  21. Forrester J. V., Lackie J. M. Adhesion of neutrophil leucocytes under conditions of flow. J Cell Sci. 1984 Aug;70:93–110. doi: 10.1242/jcs.70.1.93. [DOI] [PubMed] [Google Scholar]
  22. Gamble J. R., Harlan J. M., Klebanoff S. J., Vadas M. A. Stimulation of the adherence of neutrophils to umbilical vein endothelium by human recombinant tumor necrosis factor. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8667–8671. doi: 10.1073/pnas.82.24.8667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gimbrone M. A., Jr, Brock A. F., Schafer A. I. Leukotriene B4 stimulates polymorphonuclear leukocyte adhesion to cultured vascular endothelial cells. J Clin Invest. 1984 Oct;74(4):1552–1555. doi: 10.1172/JCI111570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gimbrone M. A., Jr Culture of vascular endothelium. Prog Hemost Thromb. 1976;3:1–28. [PubMed] [Google Scholar]
  25. Gudewicz P. W., Odekon L. E., Del Vecchio P. J., Saba T. M. Generation of neutrophil chemotactic activity by phorbol ester-stimulated calf pulmonary artery endothelial cells. J Leukoc Biol. 1988 Jul;44(1):1–7. doi: 10.1002/jlb.44.1.1. [DOI] [PubMed] [Google Scholar]
  26. Harlan J. M., Killen P. D., Senecal F. M., Schwartz B. R., Yee E. K., Taylor R. F., Beatty P. G., Price T. H., Ochs H. D. The role of neutrophil membrane glycoprotein GP-150 in neutrophil adherence to endothelium in vitro. Blood. 1985 Jul;66(1):167–178. [PubMed] [Google Scholar]
  27. Hoover R. L., Robinson J. M., Karnovsky M. J. Adhesion of polymorphonuclear leukocytes to endothelium enhances the efficiency of detoxification of oxygen-free radicals. Am J Pathol. 1987 Feb;126(2):258–268. [PMC free article] [PubMed] [Google Scholar]
  28. Jaffe E. A., Nachman R. L., Becker C. G., Minick C. R. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest. 1973 Nov;52(11):2745–2756. doi: 10.1172/JCI107470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lawrence M. B., McIntire L. V., Eskin S. G. Effect of flow on polymorphonuclear leukocyte/endothelial cell adhesion. Blood. 1987 Nov;70(5):1284–1290. [PubMed] [Google Scholar]
  30. Makgoba M. W., Sanders M. E., Ginther Luce G. E., Dustin M. L., Springer T. A., Clark E. A., Mannoni P., Shaw S. ICAM-1 a ligand for LFA-1-dependent adhesion of B, T and myeloid cells. Nature. 1988 Jan 7;331(6151):86–88. doi: 10.1038/331086a0. [DOI] [PubMed] [Google Scholar]
  31. Marlin S. D., Morton C. C., Anderson D. C., Springer T. A. LFA-1 immunodeficiency disease. Definition of the genetic defect and chromosomal mapping of alpha and beta subunits of the lymphocyte function-associated antigen 1 (LFA-1) by complementation in hybrid cells. J Exp Med. 1986 Sep 1;164(3):855–867. doi: 10.1084/jem.164.3.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Marlin S. D., Springer T. A. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell. 1987 Dec 4;51(5):813–819. doi: 10.1016/0092-8674(87)90104-8. [DOI] [PubMed] [Google Scholar]
  33. McFall T. L., Zimmerman G. A., Augustine N. H., Hill H. R. Effect of group B streptococcal type-specific antigen on polymorphonuclear leukocyte function and polymorphonuclear leukocyte-endothelial cell interaction. Pediatr Res. 1987 Jun;21(6):517–523. doi: 10.1203/00006450-198706000-00001. [DOI] [PubMed] [Google Scholar]
  34. Mercandetti A. J., Lane T. A., Colmerauer M. E. Cultured human endothelial cells elaborate neutrophil chemoattractants. J Lab Clin Med. 1984 Sep;104(3):370–380. [PubMed] [Google Scholar]
  35. Miller L. J., Bainton D. F., Borregaard N., Springer T. A. Stimulated mobilization of monocyte Mac-1 and p150,95 adhesion proteins from an intracellular vesicular compartment to the cell surface. J Clin Invest. 1987 Aug;80(2):535–544. doi: 10.1172/JCI113102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Miller L. J., Schwarting R., Springer T. A. Regulated expression of the Mac-1, LFA-1, p150,95 glycoprotein family during leukocyte differentiation. J Immunol. 1986 Nov 1;137(9):2891–2900. [PubMed] [Google Scholar]
  37. O'Brien R. F., Seton M. P., Makarski J. S., Center D. M., Rounds S. Thiourea causes endothelial cells in tissue culture to produce neutrophil chemoattractant activity. Am Rev Respir Dis. 1984 Jul;130(1):103–109. doi: 10.1164/arrd.1984.130.1.103. [DOI] [PubMed] [Google Scholar]
  38. O'Shea J. J., Brown E. J., Seligmann B. E., Metcalf J. A., Frank M. M., Gallin J. I. Evidence for distinct intracellular pools of receptors for C3b and C3bi in human neutrophils. J Immunol. 1985 Apr;134(4):2580–2587. [PubMed] [Google Scholar]
  39. Petty H. R., Francis J. W., Todd R. F., 3rd, Petrequin P., Boxer L. A. Neutrophil C3bi receptors: formation of membrane clusters during cell triggering requires intracellular granules. J Cell Physiol. 1987 Nov;133(2):235-42, 256. doi: 10.1002/jcp.1041330206. [DOI] [PubMed] [Google Scholar]
  40. Philips M. R., Buyon J. P., Winchester R., Weissmann G., Abramson S. B. Up-regulation of the iC3b receptor (CR3) is neither necessary nor sufficient to promote neutrophil aggregation. J Clin Invest. 1988 Aug;82(2):495–501. doi: 10.1172/JCI113623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Pober J. S., Gimbrone M. A., Jr, Lapierre L. A., Mendrick D. L., Fiers W., Rothlein R., Springer T. A. Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon. J Immunol. 1986 Sep 15;137(6):1893–1896. [PubMed] [Google Scholar]
  42. Pober J. S., Lapierre L. A., Stolpen A. H., Brock T. A., Springer T. A., Fiers W., Bevilacqua M. P., Mendrick D. L., Gimbrone M. A., Jr Activation of cultured human endothelial cells by recombinant lymphotoxin: comparison with tumor necrosis factor and interleukin 1 species. J Immunol. 1987 May 15;138(10):3319–3324. [PubMed] [Google Scholar]
  43. Pohlman T. H., Munford R. S., Harlan J. M. Deacylated lipopolysaccharide inhibits neutrophil adherence to endothelium induced by lipopolysaccharide in vitro. J Exp Med. 1987 May 1;165(5):1393–1402. doi: 10.1084/jem.165.5.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pohlman T. H., Stanness K. A., Beatty P. G., Ochs H. D., Harlan J. M. An endothelial cell surface factor(s) induced in vitro by lipopolysaccharide, interleukin 1, and tumor necrosis factor-alpha increases neutrophil adherence by a CDw18-dependent mechanism. J Immunol. 1986 Jun 15;136(12):4548–4553. [PubMed] [Google Scholar]
  45. Ross G. D., Thompson R. A., Walport M. J., Springer T. A., Watson J. V., Ward R. H., Lida J., Newman S. L., Harrison R. A., Lachmann P. J. Characterization of patients with an increased susceptibility to bacterial infections and a genetic deficiency of leukocyte membrane complement receptor type 3 and the related membrane antigen LFA-1. Blood. 1985 Oct;66(4):882–890. [PubMed] [Google Scholar]
  46. Rothlein R., Dustin M. L., Marlin S. D., Springer T. A. A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J Immunol. 1986 Aug 15;137(4):1270–1274. [PubMed] [Google Scholar]
  47. Sanchez-Madrid F., Nagy J. A., Robbins E., Simon P., Springer T. A. A human leukocyte differentiation antigen family with distinct alpha-subunits and a common beta-subunit: the lymphocyte function-associated antigen (LFA-1), the C3bi complement receptor (OKM1/Mac-1), and the p150,95 molecule. J Exp Med. 1983 Dec 1;158(6):1785–1803. doi: 10.1084/jem.158.6.1785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Schmalstieg F. C., Rudloff H. E., Hillman G. R., Anderson D. C. Two-dimensional and three-dimensional movement of human polymorphonuclear leukocytes: two fundamentally different mechanisms of locomotion [corrected]. J Leukoc Biol. 1986 Dec;40(6):677–691. doi: 10.1002/jlb.40.6.677. [DOI] [PubMed] [Google Scholar]
  49. Smith C. W., Hollers J. C. Motility and adhesiveness in human neutrophils. Redistribution of chemotactic factor-induced adhesion sites. J Clin Invest. 1980 Apr;65(4):804–812. doi: 10.1172/JCI109731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Smith C. W., Hollers J. C., Patrick R. A., Hassett C. Motility and adhesiveness in human neutrophils. Effects of chemotactic factors. J Clin Invest. 1979 Feb;63(2):221–229. doi: 10.1172/JCI109293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Smith C. W., Rothlein R., Hughes B. J., Mariscalco M. M., Rudloff H. E., Schmalstieg F. C., Anderson D. C. Recognition of an endothelial determinant for CD 18-dependent human neutrophil adherence and transendothelial migration. J Clin Invest. 1988 Nov;82(5):1746–1756. doi: 10.1172/JCI113788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Springer T., Galfré G., Secher D. S., Milstein C. Mac-1: a macrophage differentiation antigen identified by monoclonal antibody. Eur J Immunol. 1979 Apr;9(4):301–306. doi: 10.1002/eji.1830090410. [DOI] [PubMed] [Google Scholar]
  53. Todd R. F., 3rd, Van Agthoven A., Schlossman S. F., Terhorst C. Structural analysis of differentiation antigens Mo1 and Mo2 on human monocytes. Hybridoma. 1982;1(3):329–337. doi: 10.1089/hyb.1.1982.1.329. [DOI] [PubMed] [Google Scholar]
  54. Tonnesen M. G., Smedly L. A., Henson P. M. Neutrophil-endothelial cell interactions. Modulation of neutrophil adhesiveness induced by complement fragments C5a and C5a des arg and formyl-methionyl-leucyl-phenylalanine in vitro. J Clin Invest. 1984 Nov;74(5):1581–1592. doi: 10.1172/JCI111574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Vedder N. B., Harlan J. M. Increased surface expression of CD11b/CD18 (Mac-1) is not required for stimulated neutrophil adherence to cultured endothelium. J Clin Invest. 1988 Mar;81(3):676–682. doi: 10.1172/JCI113372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Voyta J. C., Via D. P., Butterfield C. E., Zetter B. R. Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein. J Cell Biol. 1984 Dec;99(6):2034–2040. doi: 10.1083/jcb.99.6.2034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Wallis W. J., Beatty P. G., Ochs H. D., Harlan J. M. Human monocyte adherence to cultured vascular endothelium: monoclonal antibody-defined mechanisms. J Immunol. 1985 Oct;135(4):2323–2330. [PubMed] [Google Scholar]
  58. Wright S. D., Jong M. T. Adhesion-promoting receptors on human macrophages recognize Escherichia coli by binding to lipopolysaccharide. J Exp Med. 1986 Dec 1;164(6):1876–1888. doi: 10.1084/jem.164.6.1876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Zigmond S. H., Levitsky H. I., Kreel B. J. Cell polarity: an examination of its behavioral expression and its consequences for polymorphonuclear leukocyte chemotaxis. J Cell Biol. 1981 Jun;89(3):585–592. doi: 10.1083/jcb.89.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Zimmerman G. A., McIntyre T. M. Neutrophil adherence to human endothelium in vitro occurs by CDw18 (Mo1, MAC-1/LFA-1/GP 150,95) glycoprotein-dependent and -independent mechanisms. J Clin Invest. 1988 Feb;81(2):531–537. doi: 10.1172/JCI113351. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES