Interleukin-15 delays human neutrophil apoptosis by intracellular events and not via extracellular factors: Role of Mcl-1 and decreased activity of caspase-3 and caspase-8

Journal of Leukocyte Biology

Volumn 75, Issue 5, 2004, Pages 893-900

  Bouchard, Amélie ^a   Ratthé, Claude ^a   Girard, Denis ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

Cytokine; De novo protein synthesis; Inflammation

Indexed keywords

CASPASE 3; CASPASE 8; CYCLOHEXIMIDE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 15; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; PROTEIN MCL 1; VIMENTIN;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN SYNTHESIS; SUPERNATANT; WESTERN BLOTTING;

APOPTOSIS; CASPASE 3; CASPASE 8; CASPASES; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; INTERLEUKIN-15; KINETICS; NEOPLASM PROTEINS; NEUTROPHILS; PROTO-ONCOGENE PROTEINS C-BCL-2; SIALOGLYCOPROTEINS;

EID: 2342644148     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1103585     Document Type: Article

References (48)

1. Al-Mohanna, F., Saleh, S., Parhar, R. S., Collison, K. (2002) IL-12-dependent nuclear factor-κB activation leads to de novo synthesis and release of IL-8 and TNF-α in human neutrophils. J. Leukoc. Biol. 72, 995-1002.
2. Wagner, C., Pioch, M., Meyer, C., Iking-Konert, C., Andrassy, K., Hansch, G. M. (2000) Differentiation of polymorphonuclear neutrophils in patients with systemic infections and chronic inflammatory diseases: evidence of prolonged life span and de novo synthesis of fibronectin. J. Mol. Med. 78, 337-345.
3. Crepaldi, L., Silveri, L., Calzetti, F., Pinardi, C., Cassatella, M. A. (2002) Molecular basis of the synergistic production of IL-1 receptor antagonist by human neutrophils stimulated with IL-4 and IL-10. Int. Immunol. 14, 1145-1153.
4. Zhou, Z., Richard, C., Menard, H. A. (2000) De novo synthesis of proteinase 3 by cytokine -rimed circulating human polymorphonuclear neutrophils and mononuclear cells. J. Rheumatol. 27, 2406-2411.
5. Savill, J. (1997) Apoptosis in resolution of inflammation. J. Leukoc. Biol. 61, 375-380.
6. Ward, C., Dransfield, I., Chilvers, E. R., Haslett, C., Rossi, A. G. (1999) Pharmacological manipulation of gGranulocyte apoptosis: potential therapeutic targets. Trends Phamacol. Sci. 20, 503-509.
7. Akgul, C., Moulding, D. A., Edwards, S. W. (2001) Molecular control of neutrophil apoptosis. FEBS Lett. 487, 318-322.
8. Fehniger, T. A., Caligiuri, M. A. (2001) Interleukin 15: biology and relevance to human disease. Blood 97, 14-32.
9. McInnes, I. B., Liew, F. Y. (1998) Interleukin 15: a proinflammatory role in rheumatoid arthritis synovitis. Immunol. Today 19, 75-79.
10. McInnes, I. B., Leung, B. P., Sturrock, R. D., Field, M., Liew, F. Y. (1997) Interleukin-15 mediates T cell-dependent regulation of tumor necrosis factor-α production in rheumatoid arthritis. Nat. Med. 3, 189-195.
11. McInnes, I. B., al-Mughales, J., Field, M., Leung, B. P., Huang, F. P., Dixon, R., Sturrock, R. D., Wilkinson, P. C., Liew, F. Y. (1996) The role of interleukin-15 in T-cell migration and activation in rheumatoid arthritis. Nat. Med. 2, 175-182.
12. Thurkow, E. W., van der Heijden, I. M., Breedveld, F. C., Smeets, T. J., Daha, M. R., Kluin, P. M., Meinders, A. E., Tak, P. P. (1997) Increased expression of IL-15 in the synovium of patients with rheumatoid arthritis compared with patients with Yersinia-induced arthritis and osteoarthritis. J. Pathol. 181, 444-450.
13. Girard, D., Boiani, N., Beaulieu, A. D. (1998) Human neutrophils express the interleukin-15 receptor α chain (IL-15Rα) but not the IL-9Rα component. Clin. Immunol. Immunopathol. 88, 232-240.
14. Musso, T., Calosso, L., Zucca, M., Millesimo, M., Puliti, M., Bulfone-Paus, S., Merlino, C., Savoia, D., Cavallo, R., Ponzi, A. N., Badolato, R. (1998) Interleukin-15 activates proinflammatory and antimicrobial functions in polymorphonuclear cells. Infect. Immun. 66, 2640-2647.
15. Girard, D., Paquet, M. E., Paquin, R., Beaulieu, A. D. (1996) Differential effects of interleukin-15 (IL-15) and IL-2 on human neutrophils: modulation of phagocytosis, cytoskeleton rearrangement, gene expression, and apoptosis by IL-15. Blood 88, 3176-3184.
16. McDonald, P. P., Russo, M. P., Ferrini, S., Cassatella, M. A. (1998) Interleukin-15 (IL-15) induces NF-κB activation and IL-8 production in human neutrophils. Blood 92, 4828-4835.
17. Pelletier, M., Lavastre, V., Savoie, A., Ratthe, C., Saller, R., Hostanska, K., Girard, D. (2001) Modulation of interleukin-15-induced human neutrophil responses by the plant lectin Viscum album agglutinin-I. Clin. Immunol. 101, 229-236.
18. Pelletier, M., Ratthé, C., Girard, D. (2002) Mechanisms involved in interleukin-15-induced suppression of human neutrophil apoptosis: role of the antiapoptotic Mcl-1 protein and several kinases including Janus kinase-2, p38 mitogen-activated protein kinase and extracellular signal-regulated kinases-1/2. FEBS Lett. 532, 164-170.
19. Ottonello, L., Frumento, G., Arduino, N., Bertolotto, M., Dapino, P., Mancini, M., Dallegri, F. (2002) Differential regulation of spontaneous and immune complex-induced neutrophil apoptosis by proinflammatory cytokines. Role of oxidants, Bax and caspase-3. J. Leukoc. Biol. 72, 125-132.
20. Jablonska, E., Piotrowski, L., Kiluk, M., Jablonski, J., Grabowska, Z., Markiewicz, W. (2001) Effect of IL-15 on the secretion of IL-1β, IL-1Ra and sIL-1RII by PMN from cancer patients. Cytokine 16, 173-177.
21. Lavastre, V., Pelletier, M., Sailer, R., Hostanska, K., Girard, D. (2002) Mechanisms involved in spontaneous and Viscum album agglutinin-I-induced human neutrophil apoptosis: viscum album agglutinin-I accelerates the loss of antiapoptotic Mcl-1 expression and the degradation of cytoskeletal paxillin and vimentin proteins via caspases. J. Immunol. 168, 1419-1427.
22. Ratthe, C., Pelletier, M., Roberge, C. J., Girard, D. (2002) Activation of human neutrophils by the pollutant sodium sulfite: effect on cytokine production, chemotaxis, and cell surface expression of cell adhesion molecules. Clin. Immunol. 105, 169-175.
23. 3 is a neutrophil but not a HL-60 cell agonist. Clin. Immunol. 96, 131-139.
24. Dransfield, I., Buckle, A. M., Savill, J. S., McDowall, A., Haslett, C., Hogg, N. (1994) Neutrophil apoptosis is associated with a reduction in CD16 (Fc γ RIII) expression. J. Immunol. 153, 1254-1263.
25. McColl, S. R., Paquin, R., Menard, C., Beaulieu, A. D. (1992) Human neutrophils produce high levels of the interleukin 1 receptor antagonist in response to granulocyte/macrophage colony-stimulating factor and tumor necrosis factor α. J. Exp. Med. 176, 593-598.
26. Arend, W. P. (2002) The balance between IL-1 and IL-1Ra in disease. Cytokine Growth Factor Rev. 13, 323-340.
27. Leuenroth, S. J., Grutkoski, P. S., Ayala, A., Simms, H. H. (2000) The loss of Mcl-1 expression in human polymorphonuclear leukocytes promotes apoptosis. J. Leukoc. Biol. 68, 158-166.
28. Morishima, N. (1999) Changes in nuclear morphology during apoptosis correlate with vimentin cleavage by different caspases located either upstream or downstream of Bcl-2 action. Genes Cells 4, 401-414.
29. Anderson, D. M., Kumaki, S., Ahdieh, M., Bertles, J., Tometsko, M., Loomis, A., Giri, J., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Valentine, V., Shapiro, D. N., Morris, S. W., Park, L. S., Cosman, D. (1995) Functional characterization of the human interleukin-15 receptor α chain and close linkage of IL15RA and IL2RA genes. J. Biol. Chem. 270, 29862-29869.
30. Pereno, R., Giron-Michel, J., Gaggero, A., Cazes, E., Meazza, R., Monetti, M., Monaco, E., Mishal, Z., Jasmin, C., Indiveri, F., Ferrini, S., Azzrone, B. (2000) IL-15/IL-15Rα intracellular trafficking in human melanoma cells and signal transduction through the IL-15Rα. Oncogene 19, 5153-5162.
31. Pereno, R., Gaggero, A., Scudeletti, M., Lanza, L., Meazza, R., Mishal, Z., Jasmin, C., Indiveri, F., Ferrini, S., Azzarone, B. (1999) IL-15/IL-15R α intracellular trafficking in human cells and protection from apoptosis. Ann. N. Y. Acad. Sci. 876, 236-245.
32. Cox, G., Austin, R. C. (1997). Dexamethasone-induced suppression of apoptosis in human neutrophils requires continuous stimulation of new protein synthesis. J. Leukoc. Biol. 61, 224-230.
33. Maianski, N. A., Mul, F. P., van Buul, J. D., Roos, D., Kuijpers, T. W. (2002) Granulocyte colony-stimulating factor inhibits the mitochondria-dependent activation of caspase-3 in neutrophils. Blood 99, 672-679.
34. Sakamoto, C., Suzuki, K., Hato, F., Akahori, M., Hasegawa, T., Hino, M., Kitagawa, S. (2003) Antiapoptotic effect of granulocyte colony-stimulating factor, granulocyte-macrophage colony-stimulating factor, and cyclic AMP on human neutrophils: protein synthesis-dependent and protein synthesis-independent mechanisms and the role of the Janus kinase-STAT pathway. Int. J. Hematol. 77, 60-70.
35. Kilpatrick, L. E., Lee, J. Y., Haines, K. M., Campbell, D. E., Sullivan, K. E., Korchak, H. M. (2002) A role for PKC-δ and PI 3-kinase in TNF-α-mediated antiapoptotic signaling in the human neutrophil. Am. J. Physiol. Cell Physiol. 283, C48-C57.
36. Kato, T., Takeda, Y., Nakada, T., Sendo, F. (1995) Inhibition by dexamethasone of human neutrophil apoptosis in vitro. Nat. Immun. 14, 198-208.
37. Brach, M. A., deVos, S., Gruss, H. J., Herrmann, F. (1992) Prolongation of survival of human polymorphonuclear neutrophils by granulocyte-macrophage colony-stimulating factor is caused by inhibition of programmed cell death. Blood 80, 2920-2924.
38. Mikami, M., Yamazaki, M., Yui, S. (1998) Kinetical analysis of tumor cell death-inducing mechanism by polymorphonuclear leukocyte-derived calprotectin: involvement of protein synthesis and generation of reactive oxygen species in target cells. Microbiol. Immunol. 42, 211-221.
39. Watson, R. W., Rotstein, O. D., Parodo, J., Bitar, R., Marshall, J. C. (1998) The IL-1 β-converting enzyme (caspase-1) inhibits apoptosis of inflammatory neutrophils through activation of IL-1 β. J. Immunol. 161, 957-962.
40. Moulding, D. A., Akgul, C., Derouet, M., White, M. R., Edwards, S. W. (2001) BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J. Leukoc. Biol. 70, 783-792.
41. Epling-Burnette, P. K., Zhong, B., Bai, F., Jiang, K., Bailey, R. D., Garcia, R., Jove, R., Djeu, J. Y., Loughran Jr., T. P., Wei, S. (2001) Cooperative regulation of Mcl-1 by Janus kinase/STAT and phosphatidylinositol 3-kinase contribute to granulocyte-macrophage colony-stimulating factor-delayed apoptosis in human neutrophils. J. Immunol. 166, 7486-7495.
42. Mor-Vaknin, N., Punturieri, A., Sitwala, K., Markovitz, D. M. (2003) Vimentin is secreted by activated macrophages. Nat. Cell Biol. 5, 59-63.
43. Kothakota, S., Azuma, T., Reinhard, C., Klippel, A., Tang, J., Chu, K., McGarry, T. J., Kirschner, M. W., Koths, K., Kwiatkowski, D. J., Williams, L. T. (1997) Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278, 294-298.
44. Girard, D., Paquin, R., Beaulieu, A. D. (1997) Responsiveness of human neutrophils to interleukin-4: induction of cytoskeletal rearrangements, de novo protein synthesis and delay of apoptosis. Biochem. J. 325, 147-153.
45. Grenier, A., Dehoux, M., Boutten, A., Arce-Vicioso, M., Durand, G., Gougerot-Pocidalo, M. A., Chollet-Martin, S. (1999) Oncostatin M production and regulation by human polymorphonuclear neutrophils. Blood 93, 1413-1421.
46. McCain, R. W., Holden, E. P., Blackwell, T. R., Christman, J. W. (1994) Leukotriene B4 stimulates human polymorphonuclear leukocytes to synthesize and release interleukin-8 in vitro. Am. J. Respir. Cell Mol. Biol. 10, 651-657.
47. Scapini, P., Laudanna, C., Pinardi, C., Allavena, P., Mantovani, A., Sozzani, S., Cassatella, M. A. (2001) Neutrophils produce biologically active macrophage inflammatory protein-3α (MIP-3α)/CCL20 and MIP-3β/CCL19. Eur. J. Immunol. 31, 1981-1988.
48. Cassatella, M. A. (1995) The production of cytokines by polymorphonuclear neutrophils. Immunol. Today 16, 21-26.