Flavones induce neutrophil apoptosis by down-regulation of Mcl-1 via a proteasomal-dependent pathway

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1084-1094

  Lucas, Christopher D ^a   Allen, Keith C ^a   Dorward, David A ^a   Hoodless, Laura J ^a   Melrose, Lauren A ^a   Marwick, John A ^a   Tucker, Carl S ^a   Haslett, Christopher ^a   Duffin, Rodger ^a,b   Rossi, Adriano G ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b CXR Biosciences Ltd   (United Kingdom)

Author keywords

Inflammation; Polyphenols; Resolution

Indexed keywords

APIGENIN; CASPASE 3; CASPASE 9; CASPASE INHIBITOR; DEXAMETHASONE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; LIPOTEICHOIC ACID; LUTEOLIN; PEPTIDOGLYCAN; PROTEASOME; PROTEIN MCL 1; WOGONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INCUBATION TIME; INFLAMMATION; MEDIATOR; MORPHOLOGY; NEUTROPHIL; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; TISSUE INJURY; ZEBRA FISH;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; ANTI-INFLAMMATORY AGENTS; APOPTOSIS; CASPASE 3; CASPASE 9; CASPASE INHIBITORS; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; FEMALE; FLAVONES; HUMANS; MALE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-BCL-2; QUINOLINES; ZEBRAFISH;

EID: 84874587994     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-218990     Document Type: Article

References (70)

1. Nathan, C. (2006) Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173-182 (Pubitemid 43290987)
2. Duffin, R., Leitch, A. E., Fox, S., Haslett, C., and Rossi, A. G. (2010) Targeting granulocyte apoptosis: mechanisms, models, and therapies. Immunol. Rev. 236, 28-40
3. Serhan, C. N., Brain, S. D., Buckley, C. D., Gilroy, D. W., Haslett, C., O'Neill, L. A., Perretti, M., Rossi, A. G., and Wallace, J. L. (2007) Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21, 325-332 (Pubitemid 46213480)
4. Fox, S., Leitch, A. E., Duffin, R., Haslett, C., and Rossi, A. G. (2010) Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J. Innate Immun. 2, 216-227
5. Michlewska, S., Dransfield, I., Megson, I. L., and Rossi, A. G. (2009) Macrophage phagocytosis of apoptotic neutrophils is critically regulated by the opposing actions of pro-inflammatory and anti-inflammatory agents: key role for TNF-alpha. FASEB J. 23, 844-854
6. Raza, K., Scheel-Toellner, D., Lee, C. Y., Pilling, D., Curnow, S. J., Falciani, F., Trevino, V., Kumar, K., Assi, L. K., Lord, J. M., Gordon, C., Buckley, C. D., and Salmon, M. (2006) Synovial fluid leukocyte apoptosis is inhibited in patients with very early rheumatoid arthritis. Arthritis Res. Ther. 8, R120
7. Fialkow, L., Fochesatto Filho, L., Bozzetti, M. C., Milani, A. R., Rodrigues Filho, E. M., Ladniuk, R. M., Pierozan, P., de Moura, R. M., Prolla, J. C., Vachon, E., and Downey, G. P. (2006) Neutrophil apoptosis: a marker of disease severity in sepsis and sepsis-induced acute respiratory distress syndrome. Crit. Care 10, R155
8. Munoz, L. E., Lauber, K., Schiller, M., Manfredi, A. A., and Herrmann, M. (2010) The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol. 6, 280-289
9. Fitzpatrick, A. M., Holguin, F., Teague, W. G., and Brown, L. A. (2008) Alveolar macrophage phagocytosis is impaired in children with poorly controlled asthma. J. Allergy Clin. Immunol. 121, 1372-1378
10. Rossi, A. G., Sawatzky, D. A., Walker, A., Ward, C., Sheldrake, T. A., Riley, N. A., Caldicott, A., Martinez-Losa, M., Walker, T. R., Duffin, R., Gray, M., Crescenzi, E., Martin, M. C., Brady, H. J., Savill, J. S., Dransfield, I., and Haslett, C. (2006) Cyclindependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis. Nat. Med. 12, 1056-1064 (Pubitemid 44353387)
11. Leitch, A. E., Lucas, C. D., Marwick, J. A., Duffin, R., Haslett, C., and Rossi, A. G. (2012) Cyclin-dependent kinases 7 and 9 specifically regulate neutrophil transcription and their inhibition drives apoptosis to promote resolution of inflammation. Cell Death Differ. 29, 80
12. Koedel, U., Frankenberg, T., Kirschnek, S., Obermaier, B., Hacker, H., Paul, R., and Hacker, G. (2009) Apoptosis is essential for neutrophil functional shutdown and determines tissue damage in experimental pneumococcal meningitis. PLoS Pathog. 5, e1000461
13. McGrath, E. E., Marriott, H. M., Lawrie, A., Francis, S. E., Sabroe, I., Renshaw, S. A., Dockrell, D. H., and Whyte, M. K. (2011) TNF-related apoptosis-inducing ligand (TRAIL) regulates inflammatory neutrophil apoptosis and enhances resolution of inflammation. J. Leukoc. Biol. 2011, 855-865
14. Leitch, A. E., Lucas, C. D., and Rossi, A. G. (2011) Neutrophil apoptosis: hot on the TRAIL of inflammatory resolution. J. Leukoc. Biol. 90, 841-843
15. El Kebir, D., Jozsef, L., Pan, W., Wang, L., Petasis, N. A., Serhan, C. N., and Filep, J. G. (2009) 15-epi-lipoxin A4 inhibits myeloperoxidase signaling and enhances resolution of acute lung injury. Am. J. Respir. Crit. Care Med. 180, 311-319
16. Chiang, N., Fredman, G., Backhed, F., Oh, S. F., Vickery, T., Schmidt, B. A., and Serhan, C. N. (2012) Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484, 524-528
17. Seki, H., Fukunaga, K., Arita, M., Arai, H., Nakanishi, H., Taguchi, R., Miyasho, T., Takamiya, R., Asano, K., Ishizaka, A., Takeda, J., and Levy, B. D. (2010) The anti-inflammatory and proresolving mediator resolvin E1 protects mice from bacterial pneumonia and acute lung injury. J. Immunol. 184, 836-843
18. Fischer, C. D., Beatty, J. K., Zvaigzne, C. G., Morck, D. W., Lucas, M. J., and Buret, A. G. (2011) Anti-Inflammatory benefits of antibiotic-induced neutrophil apoptosis: tulathromycin induces caspase-3-dependent neutrophil programmed cell death and inhibits NF-kappaB signaling and CXCL8 transcription. Antimicrob. Agents Chemother. 55, 338-348
19. Sawatzky, D. A., Willoughby, D. A., Colville-Nash, P. R., and Rossi, A. G. (2006) The involvement of the apoptosis-modulating proteins ERK 1/2, Bcl-xL and Bax in the resolution of acute inflammation in vivo. Am. J. Pathol. 168, 33-41 (Pubitemid 43062557)
20. Havsteen, B. H. (2002) The biochemistry and medical significance of the flavonoids. Pharmacol. Ther. 96, 67-202 (Pubitemid 35356564)
21. McCullough, M. L., Peterson, J. J., Patel, R., Jacques, P. F., Shah, R., and Dwyer, J. T. (2012) Flavonoid intake and cardiovascular disease mortality in a prospective cohort of US adults. Am. J. Clin. Nutr. 95, 454-464
22. Rossi, L., Mazzitelli, S., Arciello, M., Capo, C. R., and Rotilio, G. (2008) Benefits from dietary polyphenols for brain aging and Alzheimer's disease. Neurochem. Res. 33, 2390-2400
23. Serafini, M., Peluso, I., and Raguzzini, A. (2010) Flavonoids as anti-inflammatory agents. Proc. Nutr. Soc. 69, 273-278
24. Huang, C. H., Jan, R. L., Kuo, C. H., Chu, Y. T., Wang, W. L., Lee, M. S., Chen, H. N., and Hung, C. H. (2010) Natural flavone kaempferol suppresses chemokines expression in human monocyte THP-1 cells through MAPK pathways. J. Food Sci. 75, H254-259
25. Yi Lau, G. T., and Leung, L. K. (2010) The dietary flavonoid apigenin blocks phorbol 12-myristate 13-acetate-induced COX-2 transcriptional activity in breast cell lines. Food Chem. Toxicol. 48, 3022-3027
26. Chen, S. R., Xu, X. Z., Wang, Y. H., Chen, J. W., Xu, S. W., Gu, L. Q., and Liu, P. Q. (2010) Icariin derivative inhibits inflammation through suppression of p38 mitogen-activated protein kinase and nuclear factor-kappaB pathways. Biol. Pharm. Bull. 33, 1307-1313
27. Mann, G. E., Rowlands, D. J., Li, F. Y., de Winter, P., and Siow, R. C. (2007) Activation of endothelial nitric oxide synthase by dietary isoflavones: role of NO in Nrf2-mediated antioxidant gene expression. Cardiovasc. Res. 75, 261-274 (Pubitemid 46964821)
28. Leitch, A. E., Riley, N. A., Sheldrake, T. A., Festa, M., Fox, S., Duffin, R., Haslett, C., and Rossi, A. G. (2010) The cyclindependent kinase inhibitor R-roscovitine down-regulates Mcl-1 to override pro-inflammatory signalling and drive neutrophil apoptosis. Eur. J. Immunol. 40, 1127-1138
29. Haslett, C., Guthrie, L. A., Kopaniak, M. M., Johnston, R. B., Jr., and Henson, P. M. (1985) Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide. Am. J. Pathol. 119, 101-110 (Pubitemid 15088729)
30. Savill, J. S., Wyllie, A. H., Henson, J. E., Walport, M. J., Henson, P. M., and Haslett, C. (1989) Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83, 865-875 (Pubitemid 19080618)
31. O'Flaherty, J. T., and Rossi, A. G. (1993) 5-hydroxyicosatetraenoate stimulates neutrophils by a stereospecific, G proteinlinked mechanism. J. Biol. Chem. 268, 14708-14714 (Pubitemid 23206610)
32. Ward, C., Chilvers, E. R., Lawson, M. F., Pryde, J. G., Fujihara, S., Farrow, S. N., Haslett, C., and Rossi, A. G. (1999) NF-kappaB activation is a critical regulator of human granulocyte apoptosis in vitro. J. Biol. Chem. 274, 4309-4318
33. Renshaw, S. A., Loynes, C. A., Trushell, D. M., Elworthy, S., Ingham, P. W., and Whyte, M. K. (2006) A transgenic zebrafish model of neutrophilic inflammation. Blood 108, 3976-3978 (Pubitemid 44913264)
34. Loynes, C. A., Martin, J. S., Robertson, A., Trushell, D. M., Ingham, P. W., Whyte, M. K., and Renshaw, S. A. (2010) Pivotal Advance: Pharmacological manipulation of inflammation resolution during spontaneously resolving tissue neutrophilia in the zebrafish. J. Leukoc. Biol. 87, 203-212
35. Westerfield, M. (2007) The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio), University of Oregon Press, Eugene, OR, USA
36. Wardle, D. J., Burgon, J., Sabroe, I., Bingle, C. D., Whyte, M. K., and Renshaw, S. A. (2011) Effective caspase inhibition blocks neutrophil apoptosis and reveals Mcl-1 as both a regulator and a target of neutrophil caspase activation PLoS One 6, e15768
37. Hideshima, T., Richardson, P., Chauhan, D., Palombella, V. J., Elliott, P. J., Adams, J., and Anderson, K. C. (2001) The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res. 61, 3071-3076 (Pubitemid 32691956)
38. Bannenberg, G. L., Chiang, N., Ariel, A., Arita, M., Tjonahen, E., Gotlinger, K. H., Hong, S., and Serhan, C. N. (2005) Molecular circuits of resolution: formation and actions of resolvins and protectins. J. Immunol. 174, 4345-4355 (Pubitemid 40396017)
39. Schwab, J. M., Chiang, N., Arita, M., and Serhan, C. N. (2007) Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447, 869-874 (Pubitemid 46920139)
40. Dorward, D. A., Lucas, C. D., Rossi, A. G., Haslett, C., and Dhaliwal, K. (2012) Imaging inflammation: molecular strategies to visualize key components of the inflammatory cascade, from initiation to resolution. Pharmacol. Ther. 135, 182-199
41. Woolley, K. L., Gibson, P. G., Carty, K., Wilson, A. J., Twaddell, S. H., and Woolley, M. J. (1996) Eosinophil apoptosis and the resolution of airway inflammation in asthma. Am. J. Respir. Crit. Care Med. 154, 237-243 (Pubitemid 26255795)
42. Meagher, L. C., Cousin, J. M., Seckl, J. R., and Haslett, C. (1996) Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J. Immunol. 156, 4422-4428 (Pubitemid 26165843)
43. Qi, L., Pan, H., Li, D., Fang, F., Chen, D., and Sun, H. (2011) Luteolin improves contractile function and attenuates apoptosis following ischemia-reperfusion in adult rat cardiomyocytes. Eur. J. Pharmacol. 668, 201-207
44. Yamamoto, Y., Shioda, N., Han, F., Moriguchi, S., Nakajima, A., Yokosuka, A., Mimaki, Y., Sashida, Y., Yamakuni, T., Ohizumi, Y., and Fukunaga, K. (2009) Nobiletin improves brain ischemiainduced learning and memory deficits through stimulation of CaMKII and CREB phosphorylation. Brain Res. 1295, 218-229
45. Zhu, J., Wang, J., Sheng, Y., Zou, Y., Bo, L., Wang, F., Lou, J., Fan, X., Bao, R., Wu, Y., Chen, F., Deng, X., and Li, J. (2012) Baicalin improves survival in a murine model of polymicrobial sepsis via suppressing inflammatory response and lymphocyte apoptosis. PLoS One 7, e35523
46. Lin, C. L., Tseng, H. C., Chen, R. F., Chen, W. P., Su, M. J., Fang, K. M., and Wu, M. L. (2011) Intracellular zinc release-activated ERK-dependent GSK-3beta-p53 and Noxa-Mcl-1 signaling are both involved in cardiac ischemic-reperfusion injury. Cell Death Differ. 18, 1651-1663
47. Jacquemin, G., Shirley, S., and Micheau, O. (2010) Combining naturally occurring polyphenols with TNF-related apoptosisinducing ligand: a promising approach to kill resistant cancer cells? Cell. Mol. Life Sci. 67, 3115-3130
48. Brizuela, L., Dayon, A., Doumerc, N., Ader, I., Golzio, M., Izard, J. C., Hara, Y., Malavaud, B., and Cuvillier, O. (2010) The sphingosine kinase-1 survival pathway is a molecular target for the tumor-suppressive tea and wine polyphenols in prostate cancer. FASEB J. 24, 3882-3894
49. Walter, A., Etienne-Selloum, N., Brasse, D., Khallouf, H., Bronner, C., Rio, M. C., Beretz, A., and Schini-Kerth, V. B. (2010) Intake of grape-derived polyphenols reduces C26 tumor growth by inhibiting angiogenesis and inducing apoptosis. FASEB J. 24, 3360-3369
50. Akgul, C., and Edwards, S. W. (2003) Regulation of neutrophil apoptosis via death receptors. Cell. Mol. Life Sci. 60, 2402-2408 (Pubitemid 37487260)
51. Dibbert, B., Weber, M., Nikolaizik, W. H., Vogt, P., Schoni, M. H., Blaser, K., and Simon, H. U. (1999) Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc. Natl. Acad. Sci. U. S. A. 96, 13330-13335
52. Moulding, D. A., Akgul, C., Derouet, M., White, M. R., and Edwards, S. W. (2001) BCL-2 family expression in human neutrophils during delayed and accelerated apoptosis. J. Leukoc. Biol. 70, 783-792 (Pubitemid 33127013)
53. Derouet, M., Thomas, L., Moulding, D. A., Akgul, C., Cross, A., Moots, R. J., and Edwards, S. W. (2006) Sodium salicylate promotes neutrophil apoptosis by stimulating caspase-dependent turnover of Mcl-1. J. Immunol. 176, 957-965 (Pubitemid 43099694)
54. Dzhagalov, I., St John, A., and He, Y. W. (2007) The antiapoptotic protein Mcl-1 is essential for the survival of neutrophils but not macrophages. Blood 109, 1620-1626 (Pubitemid 46239596)
55. Derouet, M., Thomas, L., Cross, A., Moots, R. J., and Edwards, S. W. (2004) Granulocyte macrophage colony-stimulating factor signaling and proteasome inhibition delay neutrophil apoptosis by increasing the stability of Mcl-1. J. Biol. Chem. 279, 26915-26921 (Pubitemid 38812526)
56. Leuenroth, S. J., Grutkoski, P. S., Ayala, A., and Simms, H. H. (2000) Suppression of PMN apoptosis by hypoxia is dependent on Mcl-1 and MAPK activity. Surgery 128, 171-177 (Pubitemid 30622480)
57. Kato, T., Kutsuna, H., Oshitani, N., and Kitagawa, S. (2006) Cyclic AMP delays neutrophil apoptosis via stabilization of Mcl-1. FEBS Lett. 580, 4582-4586 (Pubitemid 44189375)
58. Akgul, C., Turner, P. C., White, M. R., and Edwards, S. W. (2000) Functional analysis of the human MCL-1 gene. Cell. Mol. Life. Sci. 57, 684-691 (Pubitemid 30311437)
59. Oishi, K., and Machida, K. (1997) Inhibition of neutrophil apoptosis by antioxidants in culture medium. Scand. J. Immunol. 45, 21-27 (Pubitemid 27013963)
60. Watson, R. W., Redmond, H. P., Wang, J. H., Condron, C., and Bouchier-Hayes, D. (1996) Neutrophils undergo apoptosis following ingestion of Escherichia coli. J. Immunol. 156, 3986-3992 (Pubitemid 26137686)
61. Simon, H. U., Haj-Yehia, A., and Levi-Schaffer, F. (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415-418 (Pubitemid 32162623)
62. Lee, J. P., Li, Y. C., Chen, H. Y., Lin, R. H., Huang, S. S., Chen, H. L., Kuan, P. C., Liao, M. F., Chen, C. J., and Kuan, Y. H. (2010) Protective effects of luteolin against lipopolysaccharideinduced acute lung injury involves inhibition of MEK/ERK and PI3K/Akt pathways in neutrophils. Acta Pharmacol. Sin. 31, 831-838
63. Kuo, M. Y., Liao, M. F., Chen, F. L., Li, Y. C., Yang, M. L., Lin, R. H., and Kuan, Y. H. (2011) Luteolin attenuates the pulmonary inflammatory response involves abilities of antioxidation and inhibition of MAPK and NFkappaB pathways in mice with endotoxin-induced acute lung injury. Food Chem. Toxicol. 49, 2660-2666
64. Chen, C. Y., Peng, W. H., Wu, L. C., Wu, C. C., and Hsu, S. L. (2010) Luteolin ameliorates experimental lung fibrosis both in vivo and in vitro: implications for therapy of lung fibrosis. J. Agric. Food Chem. 58, 11653-11661
65. Tang, Y. J., Zhou, F. W., Luo, Z. Q., Li, X. Z., Yan, H. M., Wang, M. J., Huang, F. R., and Yue, S. J. (2010) Multiple therapeutic effects of adjunctive baicalin therapy in experimental bacterial meningitis. Inflammation 33, 180-188
66. Birrell, M. A., McCluskie, K., Wong, S., Donnelly, L. E., Barnes, P. J., and Belvisi, M. G. (2005) Resveratrol, an extract of red wine, inhibits lipopolysaccharide induced airway neutrophilia and inflammatory mediators through an NF-kappaB-independent mechanism. FASEB J. 19, 840-841 (Pubitemid 40617402)
67. Milan, D. J., Peterson, T. A., Ruskin, J. N., Peterson, R. T., and MacRae, C. A. (2003) Drugs that induce repolarization abnormalities cause bradycardia in zebrafish. Circulation 107, 1355-1358 (Pubitemid 36350731)
68. Tobin, D. M., Roca, F. J., Oh, S. F., McFarland, R., Vickery, T. W., Ray, J. P., Ko, D. C., Zou, Y., Bang, N. D., Chau, T. T., Vary, J. C., Hawn, T. R., Dunstan, S. J., Farrar, J. J., Thwaites, G. E., King, M. C., Serhan, C. N., and Ramakrishnan, L. (2012) Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 148, 434-446
69. Rithidech, K. N., Tungjai, M., Reungpatthanaphong, P., Honikel, L., and Simon, S. R. (2012) Attenuation of oxidative damage and inflammatory responses by apigenin given to mice after irradiation. Mutat. Res. 15, 00268-00269
70. Garrison, S. P., Thornton, J. A., Hacker, H., Webby, R., Rehg, J. E., Parganas, E., Zambetti, G. P., and Tuomanen, E. I. (2010) The p53-target gene puma drives neutrophil-mediated protection against lethal bacterial sepsis. PLoS Pathog. 6, e1001240