Mac-1, but Not LFA-1, Uses Intercellular Adhesion Molecule-1 to Mediate Slow Leukocyte Rolling in TNF-α-Induced Inflammation

Journal of Immunology - Tập 171 Số 11 - Trang 6105-6111 - 2003
Jessica L. Dunne1, Robert G. Collins2, Arthur L. Beaudet3, Christie M. Ballantyne4, Klaus Ley1,5,6
1Department of Biomedical Engineering, and
2Pediatrics
3Medicine, and
4¶Human Genetics, Baylor College of Medicine, Houston, TX 77030
5Departments of
6†Cardiovascular Research Center, University of Virginia Health Sciences Center, Charlottesville, VA 22908; and Departments of

Tóm tắt

AbstractWe have previously shown that Mac-1 and LFA-1 play a cooperative role in slow leukocyte rolling in inflamed vessels, and that, although both have a role in leukocyte adhesion, the contribution from LFA-1 exceeds that of Mac-1. In this study, we used mice deficient in ICAM-1 (ICAM-1null) to study the function of ICAM-1 as an endothelial ligand for Mac-1 and LFA-1. The cremaster muscles of these mice were treated with TNF-α and prepared for intravital microscopy. We found that the average rolling velocity in venules was not different in ICAM-1null mice (4.7 μm/s) compared with wild-type mice (5.1 μm/s). Similarly, leukocyte adhesion efficiency in ICAM-1null mice (0.11 ± 0.01 mm) was similar to that in Mac-1−/− (0.12 ± 0.03 mm) mice but significantly increased compared with that in LFA-1−/− (0.08 ± 0.01 mm) mice and significantly reduced from that in wild type (0.26 ± 0.04 mm). When both LFA-1 and ICAM-1 were blocked, rolling velocity increased, and adhesion efficiency and arrest decreased. However, blocking both Mac-1 and ICAM-1 had no greater effect than either blockade alone. We conclude that endothelial ICAM-1 is the main ligand responsible for slow leukocyte rolling mediated by Mac-1, but not LFA-1.

Từ khóa


Tài liệu tham khảo

Butcher, E. C.. 1991. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67:1033.

Jung, U., K. E. Norman, K. Scharffetter-Kochanek, A. L. Beaudet, K. Ley. 1998. Transit time of leukocytes rolling through venules controls cytokine-induced inflammatory cell recruitment in vivo. J. Clin. Invest. 102:1526.

Ley, K., M. Allietta, D. C. Bullard, S. Morgan. 1998. Importance of E-selectin for firm leukocyte adhesion in vivo. Circ. Res. 83:287.

Milstone, D. S., D. Fukumura, R. C. Padgett, P. E. O’Donnell, V. M. Davis, O. J. Benavidez, W. L. Monsky, R. J. Melder, R. K. Jain, M. A. Gimbrone, Jr. 1998. Mice lacking E-selectin show normal numbers of rolling leukocytes but reduced leukocyte stable arrest on cytokine-activated microvascular endothelium. Microcirculation 5:153.

Kunkel, E. J., J. L. Dunne, K. Ley. 2000. Leukocyte arrest during cytokine-dependent inflammation in vivo. J. Immunol. 164:3301.

Forlow, S. B., E. J. White, S. C. Barlow, S. H. Feldman, H. Lu, G. J. Bagby, A. L. Beaudet, D. C. Bullard, K. Ley. 2000. Severe inflammatory defect and reduced viability in CD18 and E-selectin double-mutant mice. J. Clin. Invest. 106:1457.

Dunne, J. L., C. M. Ballantyne, A. L. Beaudet, K. Ley. 2002. Control of leukocyte rolling velocity in TNF-α-induced inflammation by LFA-1 and Mac-1. Blood 99:336.

Simon, S. I., Y. Hu, D. Vestweber, C. W. Smith. 2000. Neutrophil tethering on E-selectin activates β2 integrin binding to ICAM-1 through a mitogen-activated protein kinase signal transduction pathway. J. Immunol. 164:4348.

Ding, Z. M., J. E. Babensee, S. I. Simon, H. Lu, J. L. Perrard, D. C. Bullard, X. Y. Dai, S. K. Bromley, M. L. Dustin, M. L. Entman, et al 1999. Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration. J. Immunol. 163:5029.

Staunton, D. E., M. L. Dustin, H. P. Erickson, T. A. Springer. 1990. The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovirus. [Published errata appear in 1990 Cell 61:1157 and 1991 Cell 66:1311.]. Cell 61:243.

Diamond, M. S., D. E. Staunton, A. R. de Fougerolles, S. A. Stacker, J. Garcia-Aguilar, M. L. Hibbs, T. A. Springer. 1990. ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18). J. Cell Biol. 111:3129.

Steeber, D. A., M. A. Campbell, A. Basit, K. Ley, T. F. Tedder. 1998. Optimal selectin-mediated rolling of leukocytes during inflammation in vivo requires intercellular adhesion molecule-1 expression. Proc. Natl. Acad. Sci. USA 95:7562.

Bullard, D. C., L. Qin, I. Lorenzo, W. M. Quinlin, N. A. Doyle, R. Bosse, D. Vestweber, C. M. Doerschuk, A. L. Beaudet. 1995. P-selectin/ICAM-1 double mutant mice: acute emigration of neutrophils into the peritoneum is completely absent but is normal into pulmonary alveoli. J. Clin. Invest. 95:1782.

de Fougerolles, A. R., S. A. Stacker, R. Schwarting, T. A. Springer. 1991. Characterization of ICAM-2 and evidence for a third counter-receptor for LFA-1. J. Exp. Med. 174:253.

Ostermann, G., K. S. Weber, A. Zernecke, A. Schroder, C. Weber. 2002. JAM-1 is a ligand of the β2 integrin LFA-1 involved in transendothelial migration of leukocytes. Nat. Immunol. 3:151.

Ley, K.. 2002. Integration of inflammatory signals by rolling neutrophils. Immunol. Rev. 186:8.

Hidari, K. I., A. S. Weyrich, G. A. Zimmerman, R. P. McEver. 1997. Engagement of P-selectin glycoprotein ligand-1 enhances tyrosine phosphorylation and activates mitogen-activated protein kinases in human neutrophils. J. Biol. Chem. 272:28750.

Sligh, J. E. J., C. M. Ballantyne, S. S. Rich, H. K. Hawkins, C. W. Smith, A. Bradley, A. L. Beaudet. 1993. Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. Proc. Natl. Acad. Sci. USA 90:8529.

Xu, H., J. A. Gonzalo, Y. St. Pierre, I. R. Williams, T. S. Kupper, R. S. Cotran, T. A. Springer, J. C. Gutierrez-Ramos. 1994. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J. Exp. Med. 180:95.

van Den Engel, N. K., E. Heidenthal, A. Vinke, H. Kolb, S. Martin. 2000. Circulating forms of intercellular adhesion molecule (ICAM)-1 in mice lacking membranous ICAM-1. Blood 95:1350.

Lu, H., C. W. Smith, J. Perrard, D. Bullard, L. Tang, S. B. Shappell, M. L. Entman, A. L. Beaudet, C. M. Ballantyne. 1997. LFA-1 is sufficient in mediating neutrophil emigration in Mac-1-deficient mice. J. Clin. Invest. 99:1340.

Springer, T., G. Galfre, D. S. Secher, C. Milstein. 1978. Monoclonal xenogeneic antibodies to murine cell surface antigens: identification of novel leukocyte differentiation antigens. Eur. J. Immunol. 8:539.

Xu, H., J. K. Bickford, E. Luther, C. Carpenito, F. Takei, T. A. Springer. 1996. Characterization of murine intercellular adhesion molecule-2. J. Immunol. 156:4909.

Sanchez-Madrid, F., A. M. Krensky, C. F. Ware, E. Robbins, J. L. Strominger, S. J. Burakoff, T. A. Springer. 1982. Three distinct antigens associated with human T-lymphocyte-mediated cytolysis: LFA-1, LFA-2, and LFA-3. Proc. Natl. Acad. Sci. USA 79:7489.

Takei, F.. 1985. Inhibition of mixed lymphocyte response by a rat monoclonal antibody to a novel murine lymphocyte activation antigen (MALA-2). J. Immunol. 134:1403.

Pries, A. R.. 1988. A versatile video image analysis system for microcirculatory research. Int. J. Microcirc. Clin. Exp. 7:327.

Lipowsky, H. H., B. W. Zweifach. 1978. Application of the “two-slit” photometric technique to the measurement of microvascular volumetric flow rates. Microvasc. Res. 15:93.

Reneman, R. S., B. Woldhuis, M. G. A. oudeEgbrink, D. W. Slaaf, G. J. Tangelder. 1992. Concentration and velocity profiles of blood cells in the microcirculation. N. H. C. Hwang, Jr, and V. T. Turitto, Jr, and M. R. T. Yen, Jr, eds. Advances in Cardiovascular Engineering 25. Plenum, New York.

Norman, K. E.. 2001. An effective and economical solution for digitizing and analyzing video recordings of the microcirculation. Microcirculation 8:243.

Forlow, S. B., J. R. Schurr, J. K. Kolls, G. J. Bagby, P. O. Schwarzenberger, K. Ley. 2001. Increased granulopoiesis through interleukin-17 and granulocyte colony-stimulating factor in leukocyte adhesion molecule-deficient mice. Blood 98:3309.

Natsuka, S., K. M. Gersten, K. Zenita, R. Kannagi, J. B. Lowe. 1994. Molecular cloning of a cDNA encoding a novel human leukocyte α-1,3-fucosyltransferase capable of synthesizing the sialyl LewisX determinant. [Published erratum appears in 1994 J. Biol. Chem. 269:20806.]. J. Biol. Chem. 269:16789.

Kadono, T., G. M. Venturi, D. A. Steeber, T. F. Tedder. 2002. Leukocyte rolling velocities and migration are optimized by cooperative L-selectin and intercellular adhesion molecule-1 functions. J. Immunol. 169:4542.

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

Shimaoka, M., C. Lu, R. T. Palframan, U. H. von Andrian, A. McCormack, J. Takagi, T. A. Springer. 2001. Reversibly locking a protein fold in an active conformation with a disulfide bond: integrin αL I domains with high affinity and antagonist activity in vivo. Proc. Natl. Acad. Sci. USA 98:6009.

Bazzoni, G., M. E. Hemler. 1998. Are changes in integrin affinity and conformation overemphasized?. Trends Biochem. Sci. 23:30.

Grabovsky, V., S. Feigelson, C. Chen, D. A. Bleijs, A. Peled, G. Cinamon, F. Baleux, F. Arenzana-Seisdedos, T. Lapidot, Y. Van Kooyk, et al 2000. Subsecond induction of α4 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.

Laudanna, C., J. Y. Kim, G. Constantin, E. Butcher. 2002. Rapid leukocyte integrin activation by chemokines. Immunol. Rev. 186:37.

Lum, A. F., C. E. Green, G. R. Lee, D. E. Staunton, S. I. Simon. 2002. Dynamic regulation of LFA-1 activation and neutrophil arrest on intercellular adhesion molecule 1 (ICAM-1) in shear flow. J. Biol. Chem. 277:20660.

van Kooyk, Y., P. Weder, K. Heije, C. G. Figdor. 1994. Extracellular Ca2+ modulates leukocyte function-associated antigen-1 cell surface distribution on T lymphocytes and consequently affects cell adhesion. J. Cell Biol. 124:1061.

Shimaoka, M., T. Xiao, J. H. Liu, Y. Yang, Y. Dong, C. D. Jun, A. McCormack, R. Zhang, A. Joachimiak, J. Takagi, et al 2003. Structures of the αL I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112:99.

Beals, C. R., A. C. Edwards, R. J. Gottschalk, T. W. Kuijpers, D. E. Staunton. 2001. CD18 activation epitopes induced by leukocyte activation. J. Immunol. 167:6113.

Beglova, N., S. C. Blacklow, J. Takagi, T. A. Springer. 2002. Cysteine-rich module structure reveals a fulcrum for integrin rearrangement upon activation. Nat. Struct. Biol. 9:282.

Lupher, M. L., Jr, E. A. Harris, C. R. Beals, L. M. Sui, R. C. Liddington, D. E. Staunton. 2001. Cellular activation of leukocyte function-associated antigen-1 and its affinity are regulated at the I domain allosteric site. J. Immunol. 167:1431.

Salas, A., M. Shimaoka, S. Chen, C. V. Carman, T. Springer. 2002. Transition from rolling to firm adhesion is regulated by the conformation of the I domain of the integrin lymphocyte function-associated antigen-1. J. Biol. Chem. 277:50255.

Shimaoka, M., J. Takagi, T. A. Springer. 2002. Conformational regulation of integrin structure and function. Ann. Rev. Biophys. Biomol. Struct. 31:485.

Takagi, J., H. P. Erickson, T. A. Springer. 2001. C-terminal opening mimics “inside-out” activation of integrin α5β1. Nat. Struct. Biol. 8:412.

Takagi, J., T. A. Springer. 2002. Integrin activation and structural rearrangement. Immunol. Rev. 186:141.

Takagi, J., B. M. Petre, T. Walz, T. A. Springer. 2002. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 110:599.

DiVietro, J. A., M. J. Smith, B. R. Smith, L. Petruzzelli, R. S. Larson, M. B. Lawrence. 2001. Immobilized IL-8 triggers progressive activation of neutrophils rolling in vitro on P-selectin and intercellular adhesion molecule-1. J. Immunol. 167:4017.

Thông tin
Thông tin xuất bản

Journal of Immunology

Tập 171 Số 11

6105-6111

Thông tin tác giả