Proteinase-activated receptor-2 up-regulation by Fcγ-receptor activation in human neutrophils

FASEB Journal

Volumn 24, Issue 6, 2010, Pages 2116-2125

  St Onge, Mireille ^a   Lagarde, Stéphanie ^a   Laflamme, Cynthia ^a   Rollet Labelle, Emmanuelle ^a   Marois, Louis ^a   Naccache, Paul H ^a   Pouliot, Marc ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

Inflammation; PARs; Polymorphonuclear leukocytes; Primary granules

Indexed keywords

BINDING PROTEIN; FCGAMMA RECEPTOR; IMMUNOGLOBULIN BINDING RECEPTOR; IMMUNOGLOBULIN RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; UNCLASSIFIED DRUG;

ARTICLE; FLOW CYTOMETRY; GRANULOCYTE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; NEUTROPHIL; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

BLOTTING, WESTERN; CALCIUM SIGNALING; CELLS, CULTURED; GRANULOCYTES; HUMANS; NEUTROPHILS; RECEPTOR, PAR-2; RECEPTORS, IGG; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 77953505270     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-146167     Document Type: Article

References (55)

1. Coughlin, S. R. (2000) Thrombin signalling and protease-activated receptors. Nature 407, 258-264
2. Ossovskaya, V. S., and Bunnett, N. W. (2004) Protease-activated receptors: contribution to physiology and disease. Physiol. Rev. 84, 579-621
3. Uehara, A., Sugawara, Y., Sasano, T., Takada, H., and Sugawara, S. (2004) Proinflammatory cytokines induce proteinase 3 as membrane-bound and secretory forms in human oral epithelial cells and antibodies to proteinase 3 activate the cells through protease-activated receptor-2. J. Immunol. 173, 4179-4189 (Pubitemid 39280784)
4. Sekiguchi, F. (2005) Development of agonists/antagonists for protease-activated receptors (PARs) and the possible therapeutic application to gastrointestinal diseases. Yakugaku Zasshi 125, 491-498
5. Nakanishi-Matsui, M., Zheng, Y. W., Sulciner, D. J., Weiss, E. J., Ludeman, M. J., and Coughlin, S. R. (2000) PAR3 is a cofactor for PAR4 activation by thrombin. Nature 404, 609-613
6. Steinhoff, M., Buddenkotte, J., Shpacovitch, V., Rattenholl, A., Moormann, C., Vergnolle, N., Luger, T. A., and Hollenberg, M. D. (2005) Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr. Rev. 26, 1-43
7. Coughlin, S. R., and Camerer, E. (2003) PARticipation in inflammation. J. Clin. Invest. 111, 25-27
8. Vergnolle, N., Wallace, J. L., Bunnett, N. W., and Hollenberg, M. D. (2001) Protease-activated receptors in inflammation, neuronal signaling and pain. Trends Pharmacol. Sci. 22, 146-152
9. Houle, S., Papez, M. D., Ferazzini, M., Hollenberg, M. D., and Vergnolle, N. (2005) Neutrophils and the kallikrein-kinin system in proteinase-activated receptor 4-mediated inflammation in rodents. Brit. J. Pharmacol. 146, 670-678
10. Vergnolle, N. (1999) Proteinase-activated receptor-2-activating peptides induce leukocyte rolling, adhesion, and extravasation in vivo. J. Immunol. 163, 5064-5069
11. Garcia, J. G., Patterson, C., Bahler, C., Aschner, J., Hart, C. M., and English, D. (1993) Thrombin receptor activating peptides induce Ca2+ mobilization, barrier dysfunction, prostaglandin synthesis, and platelet-derived growth factor mRNA expression in cultured endothelium. J. Cell. Physiol. 156, 541-549
12. Ferrell, W. R., Lockhart, J. C., Kelso, E. B., Dunning, L., Plevin, R., Meek, S. E., Smith, A. J., Hunter, G. D., McLean, J. S., McGarry, F., Ramage, R., Jiang, L., Kanke, T., and Kawagoe, J. (2003) Essential role for proteinase-activated receptor-2 in arthritis. J. Clin. Invest. 111, 35-41
13. Seeliger, S., Derian, C. K., Vergnolle, N., Bunnett, N. W., Nawroth, R., Schmelz, M., Von Der Weid, P. Y., Buddenkotte, J., Sunderkotter, C., Metze, D., Andrade-Gordon, P., Harms, E., Vestweber, D., Luger, T. A., and Steinhoff, M. (2003) Proinflammatory role of proteinase-activated receptor-2 in humans and mice during cutaneous inflammation in vivo. FASEB J. 17, 1871-1885
14. Hyun, E., Andrade-Gordon, P., Steinhoff, M., and Vergnolle, N. (2008) Protease-activated receptor-2 activation: a major actor in intestinal inflammation. Gut 57, 1222-1229
15. De Boer, W. I., Yao, H., and Rahman, I. (2007) Future therapeutic treatment of COPD: struggle between oxidants and cytokines. Int. J. Chron. Obstruct. Pulmon. Dis.2, 205-228 (Pubitemid 350110895)
16. Lynch, J. P., 3rd, Flint, A., Miller, D. M., and Fantone, J. C. (1985) Noncaseating pulmonary granulomas associated with small cell carcinoma of the lung. Amer. J. Med. 78, 691-696
17. Sawyer, D. W., Donowitz, G. R., and Mandell, G. L. (1989) Polymorphonuclear neutrophils: an effective antimicrobial force. Rev. Infect. Dis. 11(Suppl. 7), S1532-S1544
18. Howells, G. L., Macey, M. G., Chinni, C., Hou, L., Fox, M. T., Harriott, P., and Stone, S. R. (1997) Proteinase-activated receptor-2: expression by human neutrophils. J. Cell Sci. 110(Pt. 7), 881-887 (Pubitemid 27196787)
19. Wang, H., and He, S. (2006) Induction of lactoferrin and IL-8 release from human neutrophils by tryptic enzymes via proteinase activated receptor-2. Cell Biol. Int. 30, 688-697
20. Shpacovitch, V. M., Varga, G., Strey, A., Gunzer, M., Mooren, F., Buddenkotte, J., Vergnolle, N., Sommerhoff, C. P., Grabbe, S., Gerke, V., Homey, B., Hollenberg, M., Luger, T. A., and Steinhoff, M. (2004) Agonists of proteinase-activated receptor-2 modulate human neutrophil cytokine secretion, expression of cell adhesion molecules, and migration within 3-D collagen lattices. J. Leuk. Biol. 76, 388-398
21. Shpacovitch, V. M., Seeliger, S., Huber-Lang, M., Balkow, S., Feld, M., Hollenberg, M. D., Sarma, V. J., Ward, P. A., Strey, A., Gerke, V., Sommerhoff, C. P., Vergnolle, N., and Steinhoff, M. (2007) Agonists of proteinase-activated receptor-2 affect transendothelial migration and apoptosis of human neutrophils. Exp. Dermatol. 16, 799-806
22. Pouliot, M., Fiset, M. E., Masse, M., Naccache, P. H., and Borgeat, P. (2002) Adenosine up-regulates cyclooxygenase-2 in human granulocytes: impact on the balance of eicosanoid generation. J. Immunol. 169, 5279-5286 (Pubitemid 35217200)
23. Rosales, C., and Brown, E. J. (1991) Two mechanisms for IgG Fc-receptor-mediated phagocytosis by human neutrophils. J. Immunol. 146, 3937-3944
24. Dussault, A. A., and Pouliot, M. (2006) Rapid and simple comparison of messenger RNA levels using real-time PCR. Biol. Proced. Online 8, 1-10
25. Beaulieu, A. D., Paquin, R., Rathanaswami, P., and McColl, S. R. (1992) Nuclear signaling in human neutrophils. Stimulation of RNA synthesis is a response to a limited number of proinflammatory agonists. J. Biol. Chem. 267, 426-432
26. Pouliot, M., McDonald, P. P., Borgeat, P., and McColl, S. R. (1994) Granulocyte/macrophage colony-stimulating factor stimulates the expression of the 5-lipoxygenase-activating protein (FLAP) in human neutrophils. J. Exp. Med. 179, 1225-1232 (Pubitemid 24091781)
27. Fujishima, S., Hoffman, A. R., Vu, T., Kim, K. J., Zheng, H., Daniel, D., Kim, Y., Wallace, E. F., Larrick, J. W., and Raffin, T. A. (1993) Regulation of neutrophil interleukin 8 gene expression and protein secretion by LPS, TNF-alpha, and IL-1 beta. J. Cell. Physiol. 154, 478-485
28. Williams, C., Mehrian Shai, R., Wu, Y., Hsu, Y. H., Sitzer, T., Spann, B., McCleary, C., Mo, Y., and Miller, C. A. (2009) Transcriptome analysis of synaptoneurosomes identifies neuroplasticity genes overexpressed in incipient Alzheimer's disease. PloS One 4, e4936
29. Movat, H. Z., Cybulsky, M. I., Colditz, I. G., Chan, M. K., and Dinarello, C. A. (1987) Acute inflammation in gram-negative infection: endotoxin, interleukin 1, tumor necrosis factor, and neutrophils. Fed. Proc. 46, 97-104
30. Shanley, T. P., Warner, R. L., and Ward, P. A. (1995) The role of cytokines and adhesion molecules in the development of inflammatory injury. Mol. Med. Today 1, 40-45
31. Selvatici, R., Falzarano, S., Mollica, A., and Spisani, S. (2006) Signal transduction pathways triggered by selective formylpeptide analogues in human neutrophils. Eur. J. Pharmacol. 534, 1-11
32. Kato, T., and Kitagawa, S. (2006) Regulation of neutrophil functions by proinflammatory cytokines. Int. J. Hematol. 84, 205-209
33. St-Onge, M., Dumas, A., Michaud, A., Laflamme, C., Dussault, A. A., and Pouliot, M. (2009) Impact of anti-inflammatory agents on the gene expression profile of stimulated human neutrophils: unraveling endogenous resolution pathways. PloS One 4, e4902
34. Gilbert, C., Poubelle, P. E., Borgeat, P., Pouliot, M., and Naccache, P. H. (2003) Crystal-induced neutrophil activation: VIII. Immediate production of prostaglandin E2 mediated by constitutive cyclooxygenase 2 in human neutrophils stimulated by urate crystals. Arthritis Rheum. 48, 1137-1148
35. Foster, P. S., Rosenberg, H. F., Asquith, K. L., and Kumar, R. K. (2008) Targeting eosinophils in asthma. Curr. Mol. Med. 8, 585-590
36. Gopinath, R., and Nutman, T. B. (1997) Identification of eosinophils in lysed whole blood using side scatter and CD16 negativity. Cytometry 30, 313-316 (Pubitemid 127473350)
37. Nanda, A., Brumell, J. H., Nordstrom, T., Kjeldsen, L., Sengelov, H., Borregaard, N., Rotstein, O. D., and Grinstein, S. (1996) Activation of proton pumping in human neutrophils occurs by exocytosis of vesicles bearing vacuolar-type H+-ATPases. J. Biol. Chem. 271, 15963-15970
38. Barabe, F., Rollet-Labelle, E., Gilbert, C., Fernandes, M. J., Naccache, S. N., and Naccache, P. H. (2002) Early events in the activation of Fc gamma RIIA in human neutrophils: stimulated insolubilization, translocation to detergent-resistant domains, and degradation of Fc gamma RIIA. J. Immunol. 168, 4042-4049 (Pubitemid 34298410)
39. Fernandes, M. J., Lachance, G., Pare, G., Rollet-Labelle, E., and Naccache, P. H. (2005) Signaling through CD16b in human neutrophils involves the Tec family of tyrosine kinases. J. Leuk. Biol. 78, 524-532
40. Borregaard, N., Kjeldsen, L., Lollike, K., and Sengelov, H. (1995) Granules and secretory vesicles of the human neutrophil. Clin. Exper. Immunol. 101(Suppl. 1), 6-9
41. Borregaard, N., Sorensen, O. E., and Theilgaard-Monch, K. (2007) Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 28, 340-345 (Pubitemid 47077924)
42. Suzuki, T., Yanai, M., Kubo, H., Kanda, A., Sasaki, H., and Butler, J. P. (2006) Interaction of non-adherent suspended neutrophils to complement opsonized pathogens: a new assay using optical traps. Cell. Res. 16, 887-894
43. O'Shea, J. J., Brown, E. J., Seligmann, B. E., Metcalf, J. A., Frank, M. M., and Gallin, J. I. (1985) Evidence for distinct intracellular pools of receptors for C3b and C3bi in human neutrophils. J. Immunol. 134, 2580-2587
44. Berger, M., Sorensen, R. U., Tosi, M. F., Dearborn, D. G., and Doring, G. (1989) Complement receptor expression on neutrophils at an inflammatory site, the Pseudomonas-infected lung in cystic fibrosis. J. Clin. Invest. 84, 1302-1313 (Pubitemid 19247604)
45. Monk, P. N., Scola, A. M., Madala, P., and Fairlie, D. P. (2007) Function, structure and therapeutic potential of complement C5a receptors. Brit. J. Pharmacol. 152, 429-448
46. Terkeltaub, R., Tenner, A. J., Kozin, F., and Ginsberg, M. H. (1983) Plasma protein binding by monosodium urate crystals. Analysis by two-dimensional gel electrophoresis. Arthritis Rheum. 26, 775-783 (Pubitemid 13099998)
47. Daeron, M. (1997) Fc receptor biology. Annu. Rev. Immunol. 15, 203-234
48. Indik, Z. K., Park, J. G., Hunter, S., and Schreiber, A. D. (1995) The molecular dissection of Fc gamma receptor mediated phagocytosis. Blood 86, 4389-4399
49. Oikonomopoulou, K., Hansen, K. K., Saifeddine, M., Tea, I., Blaber, M., Blaber, S. I., Scarisbrick, I., Andrade-Gordon, P., Cottrell, G. S., Bunnett, N. W., Diamandis, E. P., and Hollenberg, M. D. (2006) Proteinase-activated receptors, targets for kallikrein signaling. J. Biol. Chem. 281, 32095-32112
50. Dulon, S., Leduc, D., Cottrell, G. S., D'Alayer, J., Hansen, K. K., Bunnett, N. W., Hollenberg, M. D., Pidard, D., and Chignard, M. (2005) Pseudomonas aeruginosa elastase disables proteinase-activated receptor 2 in respiratory epithelial cells. Amer. J. Resp. Cell Mol. Biol. 32, 411-419
51. Roche, N., Stirling, R. G., Lim, S., Oliver, B. G., and Chung, K. F. (2003) Regulation of protease-activated receptor-1 in mononuclear cells by neutrophil proteases. Resp. Med. 97, 228-233
52. Chin, A. C., Lee, W. Y., Nusrat, A., Vergnolle, N., and Parkos, C. A. (2008) Neutrophil-mediated activation of epithelial protease-activated receptors-1 and -2 regulates barrier function and transepithelial migration. J. Immunol. 181, 5702-5710
53. Dulon, S., Cande, C., Bunnett, N. W., Hollenberg, M. D., Chignard, M., and Pidard, D. (2003) Proteinase-activated receptor-2 and human lung epithelial cells: disarming by neutrophil serine proteinases. Amer. J. Respir. Cell Mol. Biol. 28, 339-346
54. Pham, C. T. (2006) Neutrophil serine proteases: specific regulators of inflammation. Nat. Rev. 6, 541-550
55. Knecht, W., Cottrell, G. S., Amadesi, S., Mohlin, J., Skaregarde, A., Gedda, K., Peterson, A., Chapman, K., Hollenberg, M. D., Vergnolle, N., and Bunnett, N. W. (2007) Trypsin IV or mesotrypsin and p23 cleave protease-activated receptors 1 and 2 to induce inflammation and hyperalgesia. J. Biol. Chem. 282, 26089-26100