Damage-associated molecular pattern S100A9 increases bactericidal activity of human neutrophils by enhancing phagocytosis

Journal of Immunology

Volumn 186, Issue 6, 2011, Pages 3622-3631

  Simard, Jean Christophe ^a   Simon, Marie Michelle ^a   Tessier, Philippe A ^b,c   Girard, Denis ^a  

^a INSTITUT NATIONAL DE LA RECHERCHE SCIENTIFIQUE   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN B; CD16 ANTIGEN; CD32 ANTIGEN; CD64 ANTIGEN; FC RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; PROTEIN KINASE SYK; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANTIBACTERIAL ACTIVITY; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ESCHERICHIA COLI; HUMAN; HUMAN CELL; INFECTION CONTROL; NEUTROPHIL; NONHUMAN; NORMAL HUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION;

BLOOD BACTERICIDAL ACTIVITY; CALGRANULIN B; ENZYME ACTIVATION; ESCHERICHIA COLI; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEUTROPHILS; PHAGOCYTOSIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; RECEPTORS, PATTERN RECOGNITION;

EID: 79953167848     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002956     Document Type: Article

References (68)

1. Nathan, C. 2006. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6: 173-182.
2. Nimmerjahn, F., and J. V. Ravetch. 2008. Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 8: 34-47.
3. Brown, E. J. 1992. Complement receptors, adhesion, and phagocytosis. Infect. Agents Dis. 1: 63-70.
4. May, R. C., and L. M. Machesky. 2001. Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114: 1061-1077.
5. García-García, E., and C. Rosales. 2002. Signal transduction during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 72: 1092-1108.
6. Turrens, J. F. 2003. Mitochondrial formation of reactive oxygen species. J. Physiol. 552: 335-344. (Pubitemid 37321833)
7. Edgeworth, J., M. Gorman, R. Bennett, P. Freemont, and N. Hogg. 1991. Identification of p8,14 as a highly abundant heterodimeric calcium binding protein complex of myeloid cells. J. Biol. Chem. 266: 7706-7713.
8. Berntzen, H. B., and M. K. Fagerhol. 1990. L1, a major granulocyte protein; isolation of high quantities of its subunits. Scand. J. Clin. Lab. Invest. 50: 769-774.
9. Endoh, Y., Y. M. Chung, I. A. Clark, C. L. Geczy, and K. Hsu. 2009. IL-10-dependent S100A8 gene induction in monocytes/macrophages by double-stranded RNA. J. Immunol. 182: 2258-2268.
10. Yen, T., C. A. Harrison, J. M. Devery, S. Leong, S. E. Iismaa, T. Yoshimura, and C. L. Geczy. 1997. Induction of the S100 chemotactic protein, CP-10, in murine microvascular endothelial cells by proinflammatory stimuli. Blood 90: 4812-4821.
11. Foell, D., H. Wittkowski, T. Vogl, and J. Roth. 2007. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J. Leukoc. Biol. 81: 28-37.
12. Urban, C. F., D. Ermert, M. Schmid, U. Abu-Abed, C. Goosmann, W. Nacken, V. Brinkmann, P. R. Jungblut, and A. Zychlinsky. 2009. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5: e1000639.
13. Vogl, T., K. Tenbrock, S. Ludwig, N. Leukert, C. Ehrhardt, M. A. van Zoelen, W. Nacken, D. Foell, T. van der Poll, C. Sorg, and J. Roth. 2007. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 13: 1042-1049.
14. Hofmann, M. A., S. Drury, C. Fu, W. Qu, A. Taguchi, Y. Lu, C. Avila, N. Kambham, A. Bierhaus, P. Nawroth, et al. 1999. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 97: 889-901. (Pubitemid 29375048)
15. 2+-binding proteins MRP8, MRP14 and their heterodimeric form MRP8/14 in Crohn's disease. Digestion 56: 406-414.
16. van Lent, P. L., L. Grevers, A. B. Blom, A. Sloetjes, J. S. Mort, T. Vogl, W. Nacken, W. B. van den Berg, and J. Roth. 2008. Myeloid-related proteins S100A8/S100A9 regulate joint inflammation and cartilage destruction during antigen-induced arthritis. Ann. Rheum. Dis. 67: 1750-1758.
17. + T cells. Nat. Med. 16: 713-717.
18. Newton, R. A., and N. Hogg. 1998. The human S100 protein MRP-14 is a novel activator of the b2 integrin Mac-1 on neutrophils. J. Immunol. 160: 1427-1435. (Pubitemid 28093444)
19. Anceriz, N., K. Vandal, and P. A. Tessier. 2007. S100A9 mediates neutrophil adhesion to fibronectin through activation of β2 integrins. Biochem. Biophys. Res. Commun. 354: 84-89. (Pubitemid 46123204)
20. Ryckman, C., K. Vandal, P. Rouleau, M. Talbot, and P. A. Tessier. 2003. Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J. Immunol. 170: 3233-3242.
21. Vandal, K., P. Rouleau, A. Boivin, C. Ryckman, M. Talbot, and P. A. Tessier. 2003. Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J. Immunol. 171: 2602-2609.
22. Simard, J. C., D. Girard, and P. A. Tessier. 2010. Induction of neutrophil degranulation by S100A9 via a MAPK-dependent mechanism. J. Leukoc. Biol. 87: 905-914.
23. Pechkovsky, D. V., O. M. Zalutskaya, G. I. Ivanov, and N. I. Misuno. 2000. Calprotectin (MRP8/14 protein complex) release during mycobacterial infection in vitro and in vivo. FEMS Immunol. Med. Microbiol. 29: 27-33.
24. Corbin, B. D., E. H. Seeley, A. Raab, J. Feldmann, M. R. Miller, V. J. Torres, K. L. Anderson, B. M. Dattilo, P. M. Dunman, R. Gerads, et al. 2008. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319: 962-965. (Pubitemid 351263768)
25. Herndon, B. L., S. Abbasi, D. Bennett, and D. Bamberger. 2003. Calcium-binding proteins MRP 8 and 14 in a Staphylococcus aureus infection model: role of therapy, inflammation, and infection persistence. J. Lab. Clin. Med. 141: 110-120.
26. Kocher, M., P. A. Kenny, E. Farram, K. B. Abdul Majid, J. J. Finlay-Jones, and L. Geczy C. 1996. Functional chemotactic factor CP-10 and MRP-14 are abundant in murine abscesses. Infect. Immun. 64: 1342-1350.
27. Leach, S. T., H. M. Mitchell, C. L. Geczy, P. M. Sherman, and A. S. Day. 2008. S100 calgranulin proteins S100A8, S100A9 and S100A12 are expressed in the inflamed gastric mucosa of Helicobacter pylori-infected children. Can. J. Gastroenterol. 22: 461-464.
28. Sohnle, P. G., M. J. Hunter, B. Hahn, and W. J. Chazin. 2000. Zinc-reversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J. Infect. Dis. 182: 1272-1275.
29. Raquil, M. A., N. Anceriz, P. Rouleau, and P. A. Tessier. 2008. Blockade of antimicrobial proteins S100A8 and S100A9 inhibits phagocyte migration to the alveoli in streptococcal pneumonia. J. Immunol. 180: 3366-3374.
30. Rouleau, P., K. Vandal, C. Ryckman, P. E. Poubelle, A. Boivin, M. Talbot, and P. A. Tessier. 2003. The calcium-binding protein S100A12 induces neutrophil adhesion, migration, and release from bone marrow in mouse at concentrations similar to those found in human inflammatory arthritis. Clin. Immunol. 107: 46-54.
31. Ennaciri, J., and D. Girard. 2009. IL-4Rα, a new member that associates with Syk kinase: implication in IL-4-induced human neutrophil functions. J. Immunol. 183: 5261-5269.
32. Williamson, D. J., and T. C. Brown. 1987. Enhancement of neutrophil-mediated phagocytosis by human granulocyte-macrophage colony-stimulating factor demonstrated using a novel mathematical model. Immunol. Cell Biol. 65: 329-335.
33. Lemarie, A., C. Morzadec, E. Bourdonnay, O. Fardel, and L. Vernhet. 2006. Human macrophages constitute targets for immunotoxic inorganic arsenic. J. Immunol. 177: 3019-3027. (Pubitemid 44277818)
34. Green, J. N., C. C. Winterbourn, and M. B. Hampton. 2007. Analysis of neutrophil bactericidal activity. In Neutrophil Methods and Protocols. M. T. Quinn, F. R. DeLeo, and G. M. Bokoch, eds. Humana Press, Totawa, NJ, p. 319-332.
35. Pelletier, M., C. J. Roberge, M. Gauthier, K. Vandal, P. A. Tessier, and D. Girard. 2001. Activation of human neutrophils in vitro and dieldrin-induced neutrophilic inflammation in vivo. J. Leukoc. Biol. 70: 367-373.
36. Gauthier, M., C. J. Roberge, M. Pelletier, P. A. Tessier, and D. Girard. 2001. Activation of human neutrophils by technical toxaphene. Clin. Immunol. 98: 46-53.
37. Ghavami, S., M. Eshragi, S. R. Ande, W. J. Chazin, T. Klonisch, A. J. Halayko, K. D. McNeill, M. Hashemi, C. Kerkhoff, and M. Los. 2010. S100A8/A9 induces autophagy and apoptosis via ROS-mediated cross-talk between mitochondria and lysosomes that involves BNIP3. Cell Res. 20: 314-331.
38. Babior, B. M., R. S. Kipnes, and J. T. Curnutte. 1973. Biological defense mechanisms: the production by leukocytes of superoxide, a potential bactericidal agent. J. Clin. Invest. 52: 741-744.
39. Roos, D., R. van Bruggen, and C. Meischl. 2003. Oxidative killing of microbes by neutrophils. Microbes Infect. 5: 1307-1315. (Pubitemid 37410244)
40. Good, R. A., P. G. Quie, D. B. Windhorst, A. R. Page, G. E. Rodey, J. White, J. J. Wolfson, and B. H. Holmes. 1968. Fatal (chronic) granulomatous disease of childhood: a hereditary defect of leukocyte function. Semin. Hematol. 5: 215-254.
41. Steinbakk, M., C. F. Naess-Andresen, E. Lingaas, I. Dale, P. Brandtzaeg, and M. K. Fagerhol. 1990. Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet 336: 763-765.
42. W. E. Paul, ed. 2008. Fundamental Immunology. Lippincott Williams & Wilkins, Philadelphia.
43. Kedzierska, K., N. J. Vardaxis, A. Jaworowski, and S. M. Crowe. 2001. FcγR-mediated phagocytosis by human macrophages involves Hck, Syk, and Pyk2 and is augmented by GM-CSF. J. Leukoc. Biol. 70: 322-328.
44. Borregaard, N., O. E. Sørensen, and K. Theilgaard-Mönch. 2007. Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 28: 340-345. (Pubitemid 47077924)
45. Greenberg, S., P. Chang, and S. C. Silverstein. 1994. Tyrosine phosphorylation of the γ subunit of Fcγ receptors, p72syk, and paxillin during Fc receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 269: 3897-3902.
46. García-García, E., R. Rosales, and C. Rosales. 2002. Phosphatidylinositol 3-kinase and extracellular signal-regulated kinase are recruited for Fc receptor-mediated phagocytosis during monocyte-to-macrophage differentiation. J. Leukoc. Biol. 72: 107-114.
47. C. N. Serhan, P. A. Ward, and D. W. Gilroy, eds. 2010. Fundamentals of Inflammation. Cambridge University Press, New York.
48. Sohnle, P. G., B. L. Hahn, and V. Santhanagopalan. 1996. Inhibition of Candida albicans growth by calprotectin in the absence of direct contact with the organisms. J. Infect. Dis. 174: 1369-1372.
49. Ravetch, J. V., and S. Bolland. 2001. IgG Fc receptors. Annu. Rev. Immunol. 19: 275-290.
50. Pelletier, M., V. Lavastre, A. Savoie, C. Ratthé, R. Saller, K. Hostanska, and D. Girard. 2001. Modulation of interleukin-15-induced human neutrophil responses by the plant lectin Viscum album agglutinin-I. Clin. Immunol. 101: 229-236.
51. Korade-Mirnics, Z., and S. J. Corey. 2000. Src kinase-mediated signaling in leukocytes. J. Leukoc. Biol. 68: 603-613.
52. Turner, M., E. Schweighoffer, F. Colucci, J. P. Di Santo, and V. L. Tybulewicz. 2000. Tyrosine kinase SYK: essential functions for immunoreceptor signalling. Immunol. Today 21: 148-154.
53. Coxon, P. Y., M. J. Rane, D. W. Powell, J. B. Klein, and K. R. McLeish. 2000. Differential mitogen-activated protein kinase stimulation by Fcγ receptor IIa and Fcγ receptor IIIb determines the activation phenotype of human neutrophils. J. Immunol. 164: 6530-6537.
54. May, R. C., E. Caron, A. Hall, and L. M. Machesky. 2000. Involvement of the Arp2/3 complex in phagocytosis mediated by FcγR or CR3. Nat. Cell Biol. 2: 246-248.
55. Caron, E., and A. Hall. 1998. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282: 1717-1721. (Pubitemid 28549289)
56. Greenberg, S., P. Chang, and S. C. Silverstein. 1993. Tyrosine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med. 177: 529-534.
57. Gaudry, M., A. C. Caon, C. Gilbert, S. Lille, and P. H. Naccache. 1992. Evidence for the involvement of tyrosine kinases in the locomotory responses of human neutrophils. J. Leukoc. Biol. 51: 103-108.
58. Melamed, I., G. P. Downey, and C. M. Roifman. 1991. Tyrosine phosphorylation is essential for microfilament assembly in B lymphocytes. Biochem. Biophys. Res. Commun. 176: 1424-1429.
59. Van Ziffle, J. A., and C. A. Lowell. 2009. Neutrophil-specific deletion of Syk kinase results in reduced host defense to bacterial infection. Blood 114: 4871-4882.
60. Kerkhoff, C., W. Nacken, M. Benedyk, M. C. Dagher, C. Sopalla, and J. Doussiere. 2005. The arachidonic acid-binding protein S100A8/A9 promotes NADPH oxidase activation by interaction with p67phox and Rac-2. FASEB J. 19: 467-469. (Pubitemid 40316552)
61. Sroussi, H. Y., Y. Lu, Q. L. Zhang, D. Villines, and P. T. Marucha. 2010. S100A8 and S100A9 inhibit neutrophil oxidative metabolism in-vitro: involvement of adenosine metabolites. Free Radic. Res. 44: 389-396.
62. Sroussi, H. Y., J. Berline, and J. M. Palefsky. 2007. Oxidation of methionine 63 and 83 regulates the effect of S100A9 on the migration of neutrophils in vitro. J. Leukoc. Biol. 81: 818-824.
63. Lim, S. Y., M. J. Raftery, J. Goyette, and C. L. Geczy. 2010. S-glutathionylation regulates inflammatory activities of S100A9. J. Biol. Chem. 285: 14377-14388.
64. Lim, S. Y., M. J. Raftery, J. Goyette, K. Hsu, and C. L. Geczy. 2009. Oxidative modifications of S100 proteins: functional regulation by redox. J. Leukoc. Biol. 86: 577-587.
65. Fialkow, L., Y. Wang, and G. P. Downey. 2007. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic. Biol. Med. 42: 153-164.
66. Waddell, T. K., L. Fialkow, C. K. Chan, T. K. Kishimoto, and G. P. Downey. 1994. Potentiation of the oxidative burst of human neutrophils: a signaling role for L-selectin. J. Biol. Chem. 269: 18485-18491.
67. Fuortes, M., W. W. Jin, and C. Nathan. 1993. Adhesion-dependent protein tyrosine phosphorylation in neutrophils treated with tumor necrosis factor. J. Cell Biol. 120: 777-784. (Pubitemid 23035146)
68. Brumell, J. H., A. L. Burkhardt, J. B. Bolen, and S. Grinstein. 1996. Endogenous reactive oxygen intermediates activate tyrosine kinases in human neutrophils. J. Biol. Chem. 271: 1455-1461.