Cytohesin-1 regulates fMLF-mediated activation and functions of the β2 integrin Mac-1 in human neutrophils

Journal of Leukocyte Biology

Volumn 89, Issue 6, 2011, Pages 823-836

  el Azreq, Mohammed Amine ^a   Garceau, Valérie ^a   Bourgoin, Sylvain G ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Actin; Adhesion; Chemotaxis; FPRL 1; Phagocytosis

Indexed keywords

BETA2 INTEGRIN; CYTOHESIN 1; FIBRINOGEN; ZYMOSAN;

ARTICLE; CALCIUM MOBILIZATION; CELL ADHESION; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; PHAGOCYTOSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ACTINS; ADULT; ANTIGENS, CD18; BLOTTING, WESTERN; CALCIUM; CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; CHEMOTAXIS; FIBRINOGEN; FLOW CYTOMETRY; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; IMMUNOPRECIPITATION; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MACROPHAGE-1 ANTIGEN; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHIL ACTIVATION; NEUTROPHILS; PHAGOCYTOSIS; PROTEIN CONFORMATION;

EID: 79957789588     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0410222     Document Type: Article

References (71)

1. Simon, S. I., Green, C. E. (2005) Molecular mechanics and dynamics of leukocyte recruitment during inflammation. Annu. Rev. Biomed. Eng. 7, 151-185.
2. Berton, G., Lowell, C. A. (1999) Integrin signaling in neutrophils and macrophages. Cell. Signal. 11, 621-635.
3. Arnaout, M. A. (1990) Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75, 1037-1050.
4. Nakayama, H., Yoshizaki, F., Prinetti, A, Sonnino, S., Mauri, L., Taka-mori, K, Ogawa, H., Iwabuchi, K (2008) Lyn-coupled LacCer-enriched lipid rafts are required for CD11b/CD18-mediated neutrophil phagocytosis of nonopsonized microorganisms. J. Leukoc. Biol. 83, 728-741.
5. Schymeinsky, J., Mocsai, A, Walzog, B. (2007) Neutrophil activation via β2 integrins (CD11/CD18): molecular mechanisms and clinical implications. Thromb. Haemost. 98, 262-273.
6. Clark, E. A, Brugge, J. S. (1995) Integrins and signal transduction pathways: the road taken. Science 268, 233-239.
7. Giancotti, F. G., Ruoslahti, E. (1999) Integrin signaling. Science 285, 1028-1032.
8. Lowell, C. A, Berton, G. (1999) Integrin signal transduction in myeloid leukocytes. J. Leukoc. Biol. 65, 313-320.
9. Petty, H. R., Todd, R. F. (1993) Receptor-receptor interactions of complement receptor type 3 in neutrophil membranes. J. Leukoc. Biol. 54, 492-494.
10. Annenkov, A., Ortlepp, S., Hogg, N. (1996) The β 2 integrin Mac-1 but not p150,95 associates with Fc γ RIIA. Eur. J. Immunol. 26, 207-212.
11. Petty, H. R, Todd, R F. (1996) Integrins as promiscuous signal transduction devices. Immunol. Today 17, 209-212.
12. Xia, Y., Borland, G., Huang, J., Mizukami, I. F., Petty, H. R, Todd, R F., Ross, G. D. (2002) Function of the lectin domain of Mac-1/comple-ment receptor type 3 (CD11b/CD18) in regulating neutrophil adhesion. J. Immunol. 169, 6417-6426.
13. Xue, W., Kindzelskii, A. L., Todd, R F., Petty, H. R (1994) Physical association of complement receptor type 3 and urokinase-type plasminogen activator receptor in neutrophil membranes. J. Immunol. 152, 4630-4640.
14. D'Souza-Schorey, C, Chavrier, P. (2006) ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358.
15. Bourgoin, S. G., Houle, M. G., Singh, I. N., Harbour, D., Gagnon, S., Morris, A J., Brindley, D. N. (2002) ARNO but not cytohesin-1 translocation is phosphatidylinositol 3-kinase-dependent in HL-60 cells. J. Leukoc. Biol. 71, 718-728.
16. El Azreq, M. A, Garceau, V., Harbour, D., Pivot-Pajot, C, Bourgoin, S. G. (2010) Cytohesin-1 regulates the Arf6-phospholipase D signaling axis in human neutrophils: impact on superoxide anion production and secretion. J. Immunol. 184, 637-649.
17. Casanova, J. E. (2007) Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors. Traffic 8, 1476-1485.
18. Kolanus, W. (2007) Guanine nucleotide exchange factors of the cytohe-sin family and their roles in signal transduction. Immunol. Rev. 218, 102-113.
19. Kolanus, W., Nagel, W., Schiller, B., Zeitlmann, L., Godar, S., Stockinger, H., Seed, B. (1996) α L β 2 Integrin/LFA-1 binding to ICAM-1 induced by cytohesin-1, a cytoplasmic regulatory molecule. Cell 86, 233-242.
20. Geiger, C, Nagel, W., Boehm, T., van Kooyk, Y., Figdor, C. G., Kremmer, E., Hogg, N., Zeitlmann, L., Dierks, H., Weber, K S., Kolanus, W. (2000) Cytohesin-1 regulates β-2 integrin-mediated adhesion through both ARF-GEF function and interaction with LFA-1. EMBOJ. 19, 2525-2536.
21. Quast, T., Tappertzhofen, B., Schild, C, Grell, J., Czeloth, N., Forster, R, Alon, R, Fraemohs, L., Dreck, K, Weber, C, Lammermann, T., Sixt, M., Kolanus, W. (2009) Cytohesin-1 controls the activation of RhoA and modulates integrin-dependent adhesion and migration of dendritic cells. Blood 113, 5801-5810.
22. Sendide, K, Reiner, N. E., Lee, J. S., Bourgoin, S., Talal, A, Hmama, Z. (2005) Cross-talk between CD14 and complement receptor 3 promotes phagocytosis of mycobacteria: regulation by phosphatidylinositol 3-kinase and cytohesin-1. J. Immunol. 174, 4210-4219.
23. Hafner, M., Schmitz, A, Grune, I., Srivatsan, S. G., Paul, B., Kolanus, W., Quast, T., Kremmer, E., Bauer, I., Famulok, M. (2006) Inhibition of cyto-hesins by SecinH3 leads to hepatic insulin resistance. Nature 444, 941-944.
24. Garceau, V., Houle, M. G., Chouinard, F., Gagnon, S., Harbour, D., Nac-cache, P. H., Bourgoin, S. G. (2001) Characterization of cytohesin-1 monoclonal antibodies: expression in neutrophils and during granulocytic maturation of HL-60 cells.J. Immunol. Methods 249, 121-136.
25. Marcil, J., Harbour, D., Houle, M. G., Naccache, P. H., Bourgoin, S. (1999) Monosodium urate-crystal-stimulated phospholipase D in human neutrophils. Biochem. J. 337, 185-192.
26. Pivot-Pajot, C, Varoqueaux, F., de Saint Basile, G., Bourgoin, S. G (2008) Munc13-4 regulates granule secretion in human neutrophils. J. Immunol. 180, 6786-6797.
27. Thibault, N., Burelout, C, Harbour, D., Borgeat, P., Naccache, P. H., Bourgoin, S. G. (2002) Occupancy of adenosine A2a receptors promotes fMLP-induced cyclic AMP accumulation in human neutrophils: impact on phospholipase D activity and recruitment of small GTPases to membranes. J. Leukoc. Biol. 71, 367-377.
28. Thibault, N., Harbour, D., Borgeat, P., Naccache, P. H., Bourgoin, S. G. (2000) Adenosine receptor occupancy suppresses chemoattractant-in- duced phospholipase D activity by diminishing membrane recruitment of small GTPases. Blood 95, 519-527.
29. Frevert, C. W., Wong, V. A, Goodman, R B., Goodwin, R, Martin, T. R (1998) Rapid fluorescence-based measurement of neutrophil migration in vitro. J. Immunol. Methods 213, 41-52.
30. Butcher, S. K, Chahal, H., Nayak, L., Sinclair, A, Henriquez, N. V., Sapey, E., O'Mahony, D., Lord, J. M. (2001) Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans. J. Leukoc. Biol. 70, 881-886.
31. Mayer, G., Blind, M., Nagel, W., Bohm, T., Knorr, T., Jackson, C. L., Kolanus, W., Famulok, M. (2001) Controlling small guanine-nucleotide-exchange factor function through cytoplasmic RNA intramers. Proc. Natl. Acad. Sci. USA 98, 4961-4965.
32. Pivot-Pajot, C, Chouinard, F. C, Amine El Azreq, M., Harbour, D., Bourgoin, S. G. (2010) Characterization of degranulation and phagocytic capacity of a human neutrophilic cellular model, PLB-985 cells. Immunobiol-ogy 215, 38-52.
33. Gordon, D. L., Johnson, G. M., Hostetter, M. K (1987) Characteristics of iC3b binding to human polymorphonuclear leukocytes. Immunology 60, 553-558.
34. Ross, G. D., Lambris, J. D. (1982) Identification of a C3bi-specific membrane complement receptor that is expressed on lymphocytes, monocytes, neutrophils, and erythrocytes. J. Exp. Med. 155, 96-110.
35. Le Cabec, V., Cols, C, Maridonneau-Parini, I. (2000) Nonopsonic phagocytosis of zymosan and Mycobacterium kansasii by CR3 (CD11b/CD18) involves distinct molecular determinants and is or is not coupled with NA-DPH oxidase activation. Infect. Immun. 68, 4736-4745.
36. Heit, B., Colarusso, P., Kubes, P. (2005) Fundamentally different roles for LFA-1, Mac-1 and α4-integrin in neutrophil chemotaxis. J. Cell Sci. 118, 5205-5220.
37. Anderson, S. I., Hotchin, N. A, Nash, G. B. (2000) Role of the cytoskele-ton in rapid activation of CD11b/CD18 function and its subsequent downregulation in neutrophils. J. Cell Sci. 113, 2737-2745.
38. Rochon, Y P., Kavanagh, T. J., Harlan, J. M. (2000) Analysis of integrin (CD11b/CD18) movement during neutrophil adhesion and migration on endothelial cells. J. Microsc. 197, 15-24.
39. Carrigan, S. O., Pink, D. B., Stadnyk, A. W. (2007) Neutrophil transepi-thelial migration in response to the chemoattractant fMLP but not C5a is phospholipase D-dependent and related to the use of CD11b/CD18. J. Leukoc. Biol. 82, 1575-1584.
40. Li, C. C, Chiang, T. C, Wu, T. S., Pacheco-Rodriguez, G., Moss, J., Lee, F. J. (2007) ARL4D recruits cytohesin-2/ARNO to modulate actin remodeling. Mol. Biol. Cell 18, 4420-4437.
41. Bhattacharya, M., Wang, J., Ribeiro, F. M., Dixon, S. J., Feldman, R D., Hegele, R A, Ferguson, S. S. (2007) Analysis of a missense variant of the human N-formyl peptide receptor that is associated with agonist-independent β-arrestin association and indices of inflammation. Pharmacogenomics J. 7, 190-199.
42. Laroche, G., Giguere, P. M., Dupre, E., Dupuis, G., Parent, J. L. (2007) The N-terminal coiled-coil domain of the cytohesin/ARNO family of guanine nucleotide exchange factors interacts with Gaq. Mol. Cell. Biochem. 306, 141-152.
43. Phillipson, M., Heit, B., Colarusso, P., Liu, L., Ballantyne, C. M., Kubes, P. (2006) Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med. 203, 2569-2575.
44. Weber, K S., Weber, C, Ostermann, G., Dierks, H., Nagel, W., Kolanus, W. (2001) Cytohesin-1 is a dynamic regulator of distinct LFA-1 functions in leukocyte arrest and transmigration triggered by chemokines. Curr. Biol. 11, 1969-1974.
45. Sengeløv, H., Kjeldsen, L., Diamond, M. S., Springer, T. A, Borregaard, N. (1993) Subcellular localization and dynamics of Mac-1 (a m β 2) in human neutrophils. J. Clin. Invest. 92, 1467-1476.
46. Mayadas, T. N., Cullere, X. (2005) Neutrophil β2 integrins: moderators of life or death decisions. Trends Immunol. 26, 388-395.
47. Diamond, M. S., Springer, T. A. (1993) A subpopulation of Mac-1 (CD11b/CD18) molecules mediates neutrophil adhesion to ICAM-1 and fibrinogen. J. Cell Biol. 120,545-556.
48. Heit, B., Tavener, S., Raharjo, E., Kubes, P. (2002) An intracellular signaling hierarchy determines direction of migration in opposing chemot-actic gradients. J. Cell Biol. 159, 91-102.
49. Jongstra-Bilen, J., Harrison, R., Grinstein, S. (2003) Fcy-receptors induce Mac-1 (CD11b/CD18) mobilization and accumulation in the phagocytic cup for optimal phagocytosis. J. Biol. Chem. 278, 45720-45729.
50. Yan, S. R., Berton, G. (1998) Antibody-induced engagement of β2 integ-rins in human neutrophils causes a rapid redistribution of cytoskeletal proteins, Src-family tyrosine kinases, and p72syk that precedes de novo actin polymerization. J. Leukoc. Biol. 64, 401-408.
51. Vicente-Manzanares, M., Sanchez-Madrid, F. (2004) Role of the cytoskele-ton during leukocyte responses. Nat. Rev. Immunol. 4, 110-122.
52. Dierks, H., Kolanus, J., Kolanus, W. (2001) Actin cytoskeletal association of cytohesin-1 is regulated by specific phosphorylation of its carboxyl-ter-minal polybasic domain.J. Biol. Chem. 276, 37472-37481.
53. Rizoli, S. B., Rotstein, O. D., Parodo, J., Phillips, M. J., Kapus, A. (2000) Hypertonic inhibition of exocytosis in neutrophils: central role for osmotic actin skeleton remodeling. Am. J. Physiol. Cell Physiol. 279, C619-C633.
54. May, R C, Machesky, L. M. (2001) Phagocytosis and the actin cytoskele-ton. J. Cell Sci. 114, 1061-1077.
55. Ernst, S., Zobiack, N., Boecker, K, Gerke, V., Rescher, U. (2004) Agonist-induced trafficking of the low-affinity formyl peptide receptor FPRL1. Cell. Mol. Life Sci. 61, 1684-1692.
56. Huet, E., Boulay, F., Barral, S., Rabiet, M.J. (2007) The role of β-arres-tins in the formyl peptide receptor-like 1 internalization and signaling. Cell. Signal. 19, 1939-1948.
57. Claing, A., Chen, W., Miller, W. E., Vitale, N., Moss, J., Premont, R T., Lefkowitz, R J. (2001) β-Arrestin-mediated ADP-ribosylation factor 6 activation and β 2-adrenergic receptor endocytosis. J. Biol. Chem. 276, 42509-42513.
58. Bouschet, T., Martin, S., Kanamarlapudi, V., Mundell, S., Henley, J. M. (2007) The calcium-sensing receptor changes cell shape via a β-arrestin-1 ARNO ARF6 ELMO protein network. J. Cell Sci. 120, 2489-2497.
59. Oh, S.J., Santy, L.C. (2010) Differential effects of cytohesins 2 and 3 on β1 integrin recycling. J. Biol. Chem. 285, 14610-14616.
60. Hogg, N., Leitinger, B. (2001) Shape and shift changes related to the function of leukocyte integrins LFA-1 and Mac-1. J. Leukoc. Biol. 69, 893-898.
61. Walters, S. E., Tang, R H., Cheng, M., Tan, S. M., Law, S. K. (2005) Differential activation of LFA-1 and Mac-1 ligand binding domains. Biochem. Biophys. Res. Commun. 337, 142-148.
62. 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. Blood95, 911-920.
63. Prince, J. E., Brayton, C. F., Fossett, M. C, Durand, J. A., Kaplan, S. L., Smith, C. W., Ballantyne, C. M. (2001) The differential roles of LFA-1 and Mac-1 in host defense against systemic infection with Streptococcus pneumoniae. J. Immunol. 166, 7362-7369.
64. Lum, A. F., Green, C. E., Lee, G. R, Staunton, D. E., Simon, S. I. (2002) Dynamic regulation of LFA-1 activation and neutrophil arrest on intercellular adhesion molecule 1 (ICAM-1) in shear flow. J. Biol. Chem. 277, 20660-20670.
65. Sarantos, M. R, Raychaudhuri, S., Lum, A. F., Staunton, D. E., Simon, S. I. (2005) Leukocyte function-associated antigen 1-mediated adhesion stability is dynamically regulated through affinity and valency during bond formation with intercellular adhesion molecule-1. J. Biol. Chem. 280, 28290-28298.
66. Laudanna, C, Kim, J. Y., Constantin, G., Butcher, E. (2002) Rapid leukocyte integrin activation by chemokines. Immunol. Rev. 186, 37-46.
67. Ma, Y Q., Plow, E. F., Geng, J. G. (2004) P-selection binding to P-selection glycoprotein ligand-1 induces an intermediate state of αMβ2 activation and acts cooperatively with extracellular stimuli to support maximal adhesion of human neutrophils. Blood 104, 2549-2556.
68. Atarashi, K, Hirata, T., Matsumoto, M., Kanemitsu, N., Miyasaka, M. (2005) Rolling of Th1 cells via P-selectin glycoprotein ligand-1 stimulates LFA-1-mediated cell binding to ICAM-1.J. Immunol. 174, 1424-1432.
69. Chan, J. R, Hyduk, S. J., Cybulsky, M. I. (2000) α 4 β 1 Integrin/VCAM-1 interaction activates α L β 2 integrin-mediated adhesion to ICAM-1 in human T cells. J. Immunol. 164, 746-753.
70. Porter, J. C, Hogg, N. (1997) Integrin cross talk: activation of lymphocyte function-associated antigen-1 on human T cells alters α4β1- and α5β1-mediated function. J. Cell Biol. 138, 1437-1447.
71. Werr, J., Eriksson, E. E., Hedqvist, P., Lindbom, L. (2000) Engagement of β2 integrins induces surface expression of β1 integrin receptors in human neutrophils. J. Leukoc. Biol. 68, 553-560.