Relationship between Extracellular ATP and Intracellular ATP and Its Role in Regulating the Cell Death under Oligomycin Treatment

doi:10.7525/j.issn.1673-5102.2016.06.017

Abstract

Abstract: In BY-2 tobacco suspension cells, the effect of intracellular ATP(iATP) production on extracellular ATP(eATP) levels was studied by using oligomycin(Inhibitors of F_oF₁-ATPase). The results showed that with the increase of the concentrations of oligomycin(from 5-50 μmol·L^-1), the level of iATP and eATP were decreased, and the level of cell death were increased under higher concentration of oligomycin. With the increase of the times of oligomycin treatment(0.5, 1, 3 and 5 h), the levels of both iATP and eATP were decreased in different extents, while the level of cell death were increased. Treatment with exogenous ATP alleviated the decrease in iATP and the increase in cell death level that were caused by oligomycin, The level of eATP can be affected by iATP, and eATP can regulate the iATP production and cell death under the condition of mitochondrial oxidative phosphorylation being inhibited.

Key words: intracellular ATP, extracellular ATP, oligomycin, cell death

CLC Number:

Q945.79

WANG Qing-Wen, BAI Jing-Yue, SHI Dai-Long, JIA Ling-Yun, FENG Han-Qing. Relationship between Extracellular ATP and Intracellular ATP and Its Role in Regulating the Cell Death under Oligomycin Treatment[J]. Bulletin of Botanical Research, 2016, 36(6): 925-930.

References

1. Winkler H H,Neuhaus H E.Non-mitochondrial ATP transport[J].Trends in Biochemical Sciences,1999,24(2):64-68.
2. Goh C H,Jung K H,Roberts S K,et al.Mitochondria provide the main source of cytosolic ATP for activation of outward-rectifying K⁺ channels in mesophyll protoplast of chlorophyll-deficient mutant rice(OsCHLH) Seedlings[J].The Journal of Biological Chemistry,2004,279(8):6874-6882.
3. Khakh B S,Burnstock G.The double life of ATP[J].Scientific American,2009,301(6):84-92.
4. Choi J,Tanaka K,Cao Y,et al.Identification of a plant receptor for extracellular ATP[J].Science,2014,343(6168):290-294.
5. Chivasa S,Simon W J,Murphy A M,et al.The effects of extracellular adenosine 5'-triphosphate on the tobacco proteome[J].Proteomics,2010,10(2):235-244.
6. Sun J,Zhang C L,Deng S R,et al.An ATP signalling pathway in plant cells:extracellular ATP triggers programmed cell death in Populus euphratica[J].Plant,Cell & Environment,2012,35(5):893-916.
7. Dichmann S,Idzko M,Zimpfer U,et al.Adenosine triphosphate-induced oxygen radical production and CD11b up-regulation:Ca⁺⁺ mobilization and actin reorganization in human eosinophils[J].Blood,2000,95(3):973-978.
8. Silva G,Beierwaltes W H,Garvin J L.Extracellular ATP stimulates NO production in rat thick ascending limb[J].Hypertension,2006,47(3):563-567.
9. Chivasa S,Murphy A M,Hamilton J M,et al.Extracellular ATP is a regulator of pathogen defence in plants[J].The Plant Journal,2009,60(3):436-448.
10. Chivasa S,Tome D F,Murphy A M,et al.Extracellular ATP:a modulator of cell death and pathogen defense in plants[J].Journal Plant Signaling & Behavior,2009,4(11):1078-1080.
11. Chivasa S,Ndimba B K,Simon W J,et al.Extracellular ATP functions as an endogenous external metabolite regulating plant cell viability[J].The Plant Cell,2005,17(11):3019-3034.
12. Ramirez F,Marecek J F,Kantor T V,et al.Effects of borohydride-treated oligomycins on processes of energy transduction in mitochondria[J].European Journal of Biochemistry,1982,121(2):275-279.
13. Murashige T,Skoog F.A revised medium for rapid growth and bio assays with tobacco tissue cultures[J].Physiologia Plantarum,1962,15(3):473-497.
14. Yang S W,Kim S K,Kim W T.Perturbation of NgTRF1 expression induces apoptosis-like cell death in tobacco BY-2 cells and implicates NgTRF1 in the control of telomere length and stability[J].The Plant Cell,2004,16(12):3370-3385.
15. Mcelroy W D.The energy source for bioluminescence in an isolated system[J].Proceedings of the National Academy of Sciences of the United States of America,1947,33(33):342-345.
16. Yokota A,Henmi M,Takaokao N,et al.Enhancement of glucose metabolism in a pyruvic acid-hyperproducing E.coli mutant defective in F1-ATPase activity[J].Journal of Fermentation and Bioengineering,1997,83(2):132-138.
17. Keobmann B J,Westerhoff H V,Snoep J L,et al.The glycolytic flux in E.coli is controlled by the demand for ATP[J].Journal of Bacteriology,2002,184(14):3909-3916.
18. Kim S Y,Sivaguru M,Stacey G.Extracellular ATP in plants.Visualization,localization,and analysis of physiological significance in growth and signaling[J].Plant Physiology,2006,142(3):984-992.
19. Thomas C,Rajagopal A,Windsor B,et al.A role for ectophosphatase in xenobiotic resistance[J].The Plant Cell,2000,12(4):519-533.
20. Azad A K,Ishikawa T,Ishikawa T,et al.Intracellular energy depletion triggers programmed cell death during petal senescence in tulip[J].Journal of Experimental Botany,2008,59(8):2085-2095.
21. Comelli M,Pancrazio F D,Mavelli I.Apoptosis is induced by decline of mitochondrial ATP synthesis in erythroleukemia cells[J].Free Radical Biology and Medicine,2003,34(9):1190-1199.
22. Foresi N P,Laxalt A M,Tonón C V,et al.Extracellular ATP induces nitric oxide production in tomato cell suspensions[J].Plant Physiology,2007,145(3):589-592.
23. Demidchik V,Nichols C,Oliynyk M,et al.Is ATP a signaling agent in plants[J].Plant Physiology,2003,133(2):456-461.
24. Burkeen J F,Womac A D,Earnest D J,et al.Mitochondrial calcium signaling mediates rhythmic extracellular ATP accumulation in suprachiasmatic nucleus astrocytes[J].Journal of Neuroscience,2011,31(23):8432-8440.
25. Jeter C R,Tang W Q,Henaff E,et al.Evidence of a novel cell signaling role for extracellular adenosine triphosphates and diphosphates in Arabidopsis[J].The Plant Cell,2004,16(10):2652-2664.
26. Griffiths E J,Rutter G A.Mitochondrial calcium as a key regulator of mitochondrial ATP production in mammalian cells[J].Biochimica et Biophysica Acta(BBA)-Bioenergetics,2009,1787(11):1324-1333.

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