A possible involvement of plasma membrane NAD(P)H oxidase in the switch mechanism of the cell death mode from apoptosis to necrosis in menadione-induced cell injury.

• Authors: Edyta Niemczyk , Anna Majczak , Anna Hallmann , Jakub Kędzior , Michał Woźniak , Takashi Wakabayashi
• Languages of publication: EN

Abstracts

EN

The effects of inhibitors of plasma membrane NADPH oxidase on menadione-induced cell injury processes were studied using human osteosarcoma 143B cells. The intracellular level of superoxide in the cells treated with menadione for 6 h reached a maximum followed by an abrupt decrease. The population of apoptotic cells detected by Annexin V and propidium iodide double staining also reached its maximum at 6 h of menadione-treatment while that of necrotic cells increased continuously reaching 90% of the total population at 9 h of the treatment. Pretreatment of the cells with inhibitors of NADPH oxidase, including diphenyliodonium chloride, apocynin, N-vanillylnonanamide and staurosporine was effective in lowering the menadione-induced elevations of superoxide, and also in the suppression of the switch of the cell death mode from apoptosis to necrosis in menadione-treated cells except for the case of staurosporine. These results strongly suggest that superoxide generated by NADPH oxidase, besides that generated by the mitochondria, may contribute to the remarkable increase in the intracellular level of superoxide in the cells treated with menadione for 6 h resulting in the switch from apoptosis to necrosis, although a direct evidence of the presence of active and inactive forms of NADPH oxidase in control and menadione-treated 143B cells is lacking at present.

Keywords

EN

menadione; NADPH oxidase; necrosis; superoxide; apoptosis

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2004
• Volume: 51
• Issue: 4
• Pages: 1015-1022

Dates

published

2004

received

2004-05-24

accepted

2004-06-07

revised

2004-06-07

Contributors

author

Edyta Niemczyk

• Department of Cell Biology and Molecular Pathology, Medical University of Gdańsk, Gdańsk, Poland

author

Anna Majczak

• Department of Cell Biology and Molecular Pathology, Medical University of Gdańsk, Gdańsk, Poland

author

Anna Hallmann

• Department of Pharmaceutical Biochemistry, Medical University of Gdańsk, Gdańsk, Poland

author

Jakub Kędzior

• Department of Cell Biology and Molecular Pathology, Medical University of Gdańsk, Gdańsk, Poland

author

Michał Woźniak

• Department of Medical Chemistry, Medical University of Gdańsk, Gdańsk, Poland

author

Takashi Wakabayashi

• Department of Cell Biology and Molecular Pathology, Medical University of Gdańsk, Gdańsk, Poland

References

• Arroyo A, Modriancy M, Serinkan FB, Bello RI, Matsura T, Jiang J, Tyurin VA, Tyurina YY, Fadeel B, Kagan VE. (2002) NADPH oxidase-dependent oxidation and externalization of phosphatidylserine during apoptosis in Me2SO-differentiated HL-60 cells. J Biol Chem.; 277: 49965-75.
• Benchoua A, Guégan C, Couriaud C, Hosseini H, Sampaïo N, Morin D, Onténiente B. (2001) Specific caspase pathways are activated in the two stages of cerebral infarction. J Neurosci.; 21: 7127-34.
• Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. (1995) Apoptosis and necrosis: Two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA.; 92: 7162-6.
• Chandra J, Samali A, Orrenius S. (2004) Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med.; 29: 323-33
• Dive C, Hickman JA. (1991) Drug-target interactions: only the first step in the commitment to a programmed cell death? Brit J Cancer.; 64: 192-6.
• Eastman A. (1993) Apoptosis: a product of programmed and unprogrammed cell death. Toxicol Appl Pharmacol.; 121: 160-4.
• Eguchi Y, Shimizu S, Tsujimoto Y. (1997) Intracellular levels of ATP determine cell death fate by apoptosis or necrosis. Cancer Res.; 57: 1835-40.
• Ehleben W, Porwol T, Fandrey J, Kummer W, Acker H. (1997) Cobalt and desferroxamine reveal crucial numbers of the oxygen sensing pathway in HepG2 cells. Kidney Int.; 51: 483-91.
• Gerasimenko JA, Gerasimenko OV, Palejwale A, Tepiki AV, Petersen OH, Watson AM. (2002) Menadione-induced apoptosis: role of cytosolic Ca2+ elevations and the mitochondrial permeability transition pore. J Cell Sci.; 115: 485-97.
• Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. (1994) Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res.; 74: 1141-8.
• Griendling KK, Sorescu D, Ushio-Fukai M. (2000) NAD(P)H oxidase, role in cardiovascular biology and disease. Circ Res.; 86: 494-501.
• Ha HC, Synder SH. (1999) Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA.; 96: 13978-82.
• Hampton MB, Orrenius S. (1997) Dual regulation of caspase activity by hydrogen peroxide: implication for apoptosis. FEBS Lett.; 414: 552-6.
• Hohler B, Holzapfel B, Kummer W. (2000) NADPH oxidase subunits and superoxide production in porcine pulmonary artery endothelial cells. Histochem Cell Biol.; 114: 29-37.
• Hu Q, Yu Z-X, Ferrans VJ, Takeda K, Irani K, Ziegelstein C. (2002) Critical role of NADPH oxidase-derived reactive oxygen species in generating Ca2+ oscillations in human aortic endothelial cells stimulated by histamine. J Biol Chem.; 277: 32546-51.
• Jones SA, Hancock JT, Jones OTG, Neubauer A, Topley N. (1995) The expression of NADPH oxidase components in human glomerular messangial cells: detection of protein and mRNA for p47-phos, p67-phos. J Am Soc Nephrol.; 5: 1483-91.
• Kaminski M, Masaoka M, Karbowski M, Kedzior J, Nishizawa Y, Usukura J, Wakabayashi T. (2003) Ultrastructural basis for the transition of cell death mode from apoptosis to necrosis in menadione-treated osteosarcoma 143B cells. J Electron Microsc (Tokyo).; 52: 313-25.
• Kim SH, Won SJ, Sohn S, Kwon HJ, Lee JY, Park JH, Gwag BJ. (2002) Brain-derived neurotrophic factor can act as a pronecrotic factor through transcriptional and translational activation of NADPH oxidase. J Cell Biol.; 159: 821-31.
• Leist M, Single B, Castaldi AF, Kuhle S, Nicotera P. (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med.; 185: 1481-6.
• Lemaire C, Andreau K, Souvannavong V, Adam A. (1998) Inhibition of caspase activity induces a switch from apoptosis to necrosis. FEBS Lett.; 425: 266-70.
• Lieberthal W, Triaca V, Levine J. (1996) Mechanism of death induced by cisplatin in proximal tubular epithelial cells: apoptosis vs necrosis. Am J Physiol.; 270: F700-8.
• Mancini M, Anderson BO, Caldwell E, Sedghinasab M, Paty PB, Hockenbery DM. (1997) Mitochondrial proliferation and paradoxical membrane depolarization during terminal differentiation and apoptosis in human colon carcinoma cell line. J Cell Biol.; 138: 449-69.
• Matsubara S, Sato I. (2001) Enzyme histochemically detectable NAD(P)H oxidase in human placental trophoblasts: normal, preeclamptic, and fetal growth restriction-complicated pregnancy. Histochem Cell Biol.; 116: 1-7.
• Melino G, Bernassola F, Knight RA, Corasaniti MT, Mistico G, Finazzi-Agro A. (1997) S-nitrosylation regulates apoptosis. Nature.; 388: 432-3.
• Nobel CS, Burgess DH, Zhivotovsky B, Burkitt MJ, Orrenius S, Slater AF. (1997) Mechanism of dithiocarbamate inhibition of apoptosis: thiol oxidation by dithiocarbamate disulfides directly inhibits processing of the caspase-3 proenzyme. Chem Res Toxicol.; 10: 636-43.
• Samali A, Nordgren H, Zhivotovsky B, Peterson E, Orrenius S. (1999) A comparative study of apoptosis and necrosis in HepG2 cells: oxidant-induced caspase inactivation leads to necrosis. Biochem Biophys Res Commun.; 255: 6-11.
• Sun Y-L, Zhao Y, Hong X, Zhai Z-H. (1999) Cytochrome c release and caspase activation by menadione-induced apoptosis in plants. FEBS Lett.; 462: 317-21.
• Spodnik JH, Wozniak M, Budzko D, Teranishi M, Karbowki M, Nishizawa Y, Usukura J, Wakabayashi T. (2002) Mechanism of leflunomide-induced proliferation of mitochondria in mammalian cells. Mitochondrion.; 2: 163-79.
• Suzuki Y, Ono Y. (1999) Involvement of reactive oxygen species produced via NADPH oxidase in tyrosine phosphorylation in human B- and T-lineage lymphoid cells. Biochem Biophys Res Commun.; 255: 262-7.
• Thor H, Smith MT, Hartzell P, Bellomo G, Jewell SA, Orrenius S. (1982) The metabolism of menadione (2-methyl-1,4-naphthoquinone) by isolated hepatocytes. J Biol Chem.; 257: 12419-25.
• Yamashoji S, Ikedo T, Yamashoji K. (1991) Extracellular generation of active oxygen species catalyzed by exogenous menadione in yeast cell suspension. Biochim Biophys Acta.; 1059: 99-105.