Inhibition of spontaneous neutrophil apoptosis by parabutoporin acts independently of NADPH oxidase inhibition but by lipid raft-dependent stimulation of Akt

Journal of Leukocyte Biology

Volumn 85, Issue 3, 2009, Pages 497-507

  Remijsen, Quinten ^a   Berghe, Tom Vanden ^b,c   Parthoens, Eef ^c   Asselbergh, Bob ^c   Vandenabeele, Peter ^b,c   Willems, Jean ^a,d  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d Laboratory of Biochemistry   (Belgium)

Author keywords

Chronic granulomatous disease; Granulocyte; Scorpion; Superoxide

Indexed keywords

OXIDOREDUCTASE INHIBITOR; PARABUTOPORIN; PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL SURVIVAL; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INHIBITION KINETICS; LIPID RAFT; NEUTROPHIL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANTIMICROBIAL CATIONIC PEPTIDES; APOPTOSIS; CELLS, CULTURED; HUMANS; KINETICS; MEMBRANE MICRODOMAINS; NADPH OXIDASE; NEUTROPHILS; PROTO-ONCOGENE PROTEINS C-AKT; SCORPION VENOMS;

SCORPIONES;

EID: 61449111932     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0908525     Document Type: Article

References (46)

1. Luo, H. R., Loison, F. (2008) Constitutive neutrophil apoptosis: mechanisms and regulation. Am. J. Hematol. 83, 288-295.
2. Maianski, N. A., Maianski, A. N., Kuijpers, T. W., Roos, D. (2004) Apoptosis of neutrophils. Acta Haematol. 111, 56-66.
3. Weiss, S. J. (1989) Tissue destruction by neutrophils. N. Engl. J. Med. 320, 365-376.
4. Segal, A. W. (2005) How neutrophils kill microbes. Annu. Rev. Immunol. 23, 197-223.
5. Blomgran, R., Zheng, L., Stendahl, O. (2007) Cathepsin-cleaved Bid promotes apoptosis in human neutrophils via oxidative stress-induced lysosomal membrane permeabilization. J. Leukoc. Biol. 81, 1213-1223.
6. Hampton, M. B., Vissers, M. C., Keenan, J. I., Winterbourn, C. C. (2002) Oxidant-mediated phosphatidylserine exposure and macrophage uptake of activated neutrophils: possible impairment in chronic granulomatous disease. J. Leukoc. Biol. 71, 775-781.
7. Romani, L., Fallarino, F., De Luca, A., Montagnoli, C., D'Angelo, C., Zelante, T., Vacca, C., Bistoni, F., Fioretti, M. C., Grohmann, U., Segal, B. H., Puccetti, P. (2008) Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451, 211-215.
8. Babior, B. M. (1999) NADPH oxidase: an update. Blood 93, 1464-1476.
9. Seger, R. A. (2008) Modern management of chronic granulomatous disease. Br. J. Haematol. 140, 255-266.
10. Morgenstern, D. E., Gifford, M. A., Li, L. L., Doerschuk, C. M., Dinauer, M. C. (1997) Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus. J. Exp. Med. 185, 207-218.
11. Bylund, J., Macdonald, K. L., Brown, K. L., Mydel, P., Collins, L. V., Hancock, R. E., Speert, D. P. (2007) Enhanced inflammatory responses of chronic granulomatous disease leukocytes involve ROS-independent activation of NF-κ B. Eur. J. Immunol. 37, 1087-1096.
12. Hatanaka, E., Carvalho, B. T., Condino-Neto, A., Campa, A. (2004) Hyperresponsiveness of neutrophils from gp 91phox deficient patients to lipopolysaccharide and serum amyloid A. Immunol. Lett. 94, 43-46.
13. Kasahara, Y., Iwai, K., Yachie, A., Ohta, K., Konno, A., Seki, H., Miyawaki, T., Taniguchi, N. (1997) Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. Blood 89, 1748-1753.
14. Fadeel, B., Ahlin, A., Henter, J. I., Orrenius, S., Hampton, M. B. (1998) Involvement of caspases in neutrophil apoptosis: regulation by reactive oxygen species. Blood 92, 4808-4818.
15. Wilkie, R. P., Vissers, M. C., Dragunow, M., Hampton, M. B. (2007) A functional NADPH oxidase prevents caspase involvement in the clearance of phagocytic neutrophils. Infect. Immun. 75, 3256-3263.
16. Fay, A. J., Qian, X., Jan, Y. N., Jan, L. Y. (2006) SK channels mediate NADPH oxidase-independent reactive oxygen species production and apoptosis in granulocytes. Proc. Natl. Acad. Sci. USA 103, 17548-17553.
17. Pullar, J. M., Hampton, M. B. (2002) Diphenyleneiodonium triggers the efflux of glutathione from cultured cells. J. Biol. Chem. 277, 19402-19407.
18. Willems, J., Moerman, L., Bosteels, S., Bruyneel, E., Ryniers, F., Ver- donck, F. (2004) Parabutoporin-an antibiotic peptide from scorpion venom-can both induce activation and inhibition of granulocyte cell functions. Peptides 25, 1079-1084.
19. Moerman, L., Bosteels, S., Noppe, W., Willems, J., Clynen, E., Schoofs, L., Thevissen, K., Tytgat, J., Van Eldere, J., van der Walt, J., Verdonck, F. (2002) Antibacterial and antifungal properties of α-helical, cationic pep-tides in the venom of scorpions from southern Africa. Eur. J Biochem. 269, 4799-4810.
20. Remijsen, Q. F. M., Fontayne, A., Verdonck, F., Clynen, E., Schoofs, L., Willems, J. (2006) The antimicrobial peptide parabutoporin competes with p47(phox) as a PKC-substrate and inhibits NADPH oxidase in human neutrophils. FEBS Lett. 580, 6206-6210.
21. Zhu, D., Hattori, H., Jo, H., Jia, Y., Subramanian, K. K., Loison, F., You, J., Le, Y., Honczarenko, M., Silberstein, L., Luo, H. R. (2006) Deactivation of phosphatidylinositol 3,4,5-trisphosphate/Akt signaling mediates neutrophil spontaneous death. Proc. Natl. Acad. Sci. USA 103, 14836-14841.
22. Vanden Berghe, T., Kalai, M., van Loo, G., Declercq, W., Vandenabeele, P. (2003) Disruption of HSP90 function reverts tumor necrosis factor- induced necrosis to apoptosis. J. Biol. Chem. 278, 5622-5629.
23. Pongracz, J., Webb, P., Wang, K., Deacon, E., Lunn, O. J., Lord, J. M. (1999) Spontaneous neutrophil apoptosis involves caspase 3-mediated activation of protein kinase C-§. J. Biol. Chem. 274, 37329-37334.
24. Francois, S., El Benna, J., Dang, P. M., Pedruzzi, E., Gougerot-Pocidalo, M. A., Elbim, C. (2005)Inhibition ofneutrophil apoptosis byTLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-κB signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J. Immunol. 174, 3633-3642.
25. Ward, C., Chilvers, E. R., Lawson, M. F., Pryde, J. G., Fujihara, S., Farrow, S. N., Haslett, C., Rossi, A. G. (1999) NF-κB activation is a critical regulator of human granulocyte apoptosis in vitro. J. Biol. Chem. 274, 4309-4318.
26. Mackay, H. J., Twelves, C. J. (2007) Targeting the protein kinase C family: are we there yet? Nat. Rev. Cancer 7, 554-562.
27. Pryde, J. G., Walker, A., Rossi, A. G., Hannah, S., Haslett, C. (2000) Temperature-dependent arrest of neutrophil apoptosis. Failure of Bax insertion into mitochondria at 15 degrees C prevents the release of cytochrome c. J. Biol. Chem. 275, 33574-33584.
28. Davies, S. P., Reddy, H., Caivano, M., Cohen, P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105.
29. Weinmann, P., Gaehtgens, P., Walzog, B. (1999) Bcl-Xl- and Bax-α- mediated regulation of apoptosis of human neutrophils via caspase-3. Blood 93, 3106-3115.
30. Liles, W. C., Kiener, P. A., Ledbetter, J. A., Aruffo, A., Klebanoff, S. J. (1996) Differential expression of Fas (CD95) and Fas ligand on normal human phagocytes: implications for the regulation of apoptosis in neutro-phils. J. Exp. Med. 184, 429-440.
31. Brown, S. B., Savill, J. (1999) Phagocytosis triggers macrophage release of Fas ligand and induces apoptosis of bystander leukocytes. J. Immunol. 162, 480-485.
32. Daigle, I., Simon, H. U. (2001) Critical role for caspases 3 and 8 in neutrophil but not eosinophil apoptosis. Int. Arch. Allergy Immunol. 126, 147-156.
33. Fecho, K., Cohen, P. L. (1998) Fas ligand (gld)- and Fas (lpr)-deficient mice do not show alterations in the extravasation or apoptosis of inflammatory neutrophils. J. Leukoc. Biol. 64, 373-383.
34. Hannah, S., Nadra, I., Dransfield, I., Pryde, J. G., Rossi, A. G., Haslett, C. (1998) Constitutive neutrophil apoptosis in culture is modulated by cell density independently of β2 integrin-mediated adhesion. FEBS Lett. 421, 141-146.
35. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V., Zychlinsky, A. (2007) Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241.
36. Hannah, S., Mecklenburgh, K., Rahman, I., Bellingan, G. J., Greening, A., Haslett, C., Chilvers, E. R. (1995) Hypoxia prolongs neutrophil survival in vitro. FEBS Lett. 372, 233-237.
37. Rollet-Labelle, E., Grange, M. J., Elbim, C., Marquetty, C., Gougerot- Pocidalo, M. A., Pasquier, C. (1998) Hydroxyl radical as a potential intracellular mediator of polymorphonuclear neutrophil apoptosis. Free Radic. Biol. Med. 24, 563-572.
38. Janssen-Heininger, Y. M., Poynter, M. E., Baeuerle, P. A. (2000) Recent advances towards understanding redox mechanisms in the activation of nuclear factor κB. Free Radic. Biol. Med. 28, 1317-1327.
39. Oishi, K., Machida, K. (1997) Inhibition of neutrophil apoptosis by antioxidants in culture medium. Scand. J. Immunol. 45, 21-27.
40. Katsumata, O., Hara-Yokoyama, M., Sautes-Fridman, C., Nagatsuka, Y., Katada, T., Hirabayashi, Y., Shimizu, K., Fujita-Yoshigaki, J., Sugiya, H., Furuyama, S. (2001) Association of FcγRII with low-density detergent- resistant membranes is important for cross-linking-dependent initiation of the tyrosine phosphorylation pathway and superoxide generation. J. Immunol. 167, 5814-5823.
41. Wang, X., Chen, W., Zeng, W., Bai, L., Tesfaigzi, Y., Belinsky, S. A., Lin, Y. (2008) Akt-mediated eminent expression of c-FLIP and Mcl-1 confers acquired resistance to TRAIL-induced cytotoxicity to lung cancer cells. Mol. Cancer Ther. 7, 1156-1163.
42. Derouet, M., Thomas, L., Cross, A., Moots, R. J., Edwards, S. W. (2004) Granulocyte macrophage colony-stimulating factor signaling and protea- some inhibition delay neutrophil apoptosis by increasing the stability of Mcl-1. J. Biol. Chem. 279, 26915-26921.
43. (1991) A controlled trial of interferon γ to prevent infection in chronic granulomatous disease. The International Chronic Granulomatous Disease Cooperative Study Group. N. Engl. J. Med. 324, 509-516.
44. Sakamoto, E., Hato, F., Kato, T., Sakamoto, C., Akahori, M., Hino, M., Kitagawa, S. (2005) Type I and type II interferons delay human neutrophil apoptosis via activation of STAT3 and up-regulation of cellular inhibitor of apoptosis 2. J. Leukoc. Biol. 78, 301-309.
45. Maianski, N. A., Geissler, J., Srinivasula, S. M., Alnemri, E. S., Roos, D., Kuijpers, T. W. (2004) Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis. Cell Death Differ. 11, 143-153.
46. Narayanan, P. K., Ragheb, K., Lawler, G., Robinson, J. P. (1997) Defects in intracellular oxidative metabolism of neutrophils undergoing apoptosis. J. Leukoc. Biol. 61, 481-488.