Mitochondrial ascorbic acid is responsible for enhanced susceptibility of U937 cells to the toxic effects of peroxynitrite

BioFactors

Volumn 40, Issue 2, 2014, Pages 236-246

  Guidarelli, Andrea ^a   Cerioni, Liana ^a   Fiorani, Mara ^a   Azzolini, Catia ^a   Cantoni, Orazio ^a  

^a UNIVERSITY OF URBINO   (Italy)

Author keywords

Ascorbic acid; Dehydroascorbic acid; Mitochondrial uptake; Peroxynitrite; Toxicity

Indexed keywords

ANTINEOPLASTIC AGENT; ASCORBIC ACID; DEHYDROASCORBIC ACID; PEROXYNITROUS ACID; SUPEROXIDE;

CELL SURVIVAL; DRUG EFFECTS; DRUG SCREENING; HUMAN; METABOLISM; MITOCHONDRION; SINGLE STRANDED DNA BREAK; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; ASCORBIC ACID; CELL LINE, TUMOR; CELL SURVIVAL; DEHYDROASCORBIC ACID; DNA BREAKS, SINGLE-STRANDED; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; MITOCHONDRIA; PEROXYNITROUS ACID; SUPEROXIDES;

EID: 84899066041     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1139     Document Type: Article

References (50)

1. Daruwala, R., Song, J., Koh, W. S., Rumsey, S. C., and Levine, M. (1999) Cloning and functional characterization of the human sodium-dependent vitamin C transporters hSVCT1 and hSVCT2. FEBS Lett. 460, 480-484.
2. +-dependent l-ascorbic acid transporters. Nature 399, 70-75.
3. Liang, W. J., Johnson, D., and Jarvis, S. M. (2001) Vitamin C transport systems of mammalian cells. Mol. Membr. Biol. 18, 87-95.
4. Wilson, J. X. (2005) Regulation of vitamin C transport. Annu. Rev. Nutr. 25, 105-125.
5. Traber, M. G. and Stevens, J. F. (2011) Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic. Biol. Med. 51, 1000-1013.
6. Frei, B., England, L., and Ames, B. N. (1989) Ascorbate is an outstanding antioxidant in human blood plasma. Proc. Natl. Acad. Sci. USA 86, 6377-6381.
7. Halliwell, B. (1996) Vitamin C: antioxidant or pro-oxidant in vivo? Free Radic. Res. 25, 439-454.
8. Verrax, J., Cadrobbi, J., Marques, C., Taper, H., Habraken, Y., et al. (2004) Ascorbate potentiates the cytotoxicity of menadione leading to an oxidative stress that kills cancer cells by a non-apoptotic caspase-3 independent form of cell death. Apoptosis 9, 223-233.
9. 2-induced damage and iron homeostasis in human cells. Free Radic. Biol. Med. 43, 1165-1175.
10. Fiorani, M., Azzolini, C., Cerioni, L., Guidarelli, A., and Cantoni, O. (2013) Superoxide dictates the mode of U937 cell ascorbic acid uptake and prevents the enhancing effects of the vitamin to otherwise nontoxic levels of reactive oxygen/nitrogen species. J. Nutr. Biochem. 24, 467-474.
11. Azzolini, C., Fiorani, M., Guidarelli, A., and Cantoni, O. (2011) Studies with low micromolar levels of ascorbic and dehydroascorbic acid fail to unravel a preferential route for vitamin C uptake and accumulation in U937 cells. Br. J. Nutr. 28, 1-6.
12. Tommasini, I., Sestili, P., and Cantoni, O. (2002) Delayed formation of hydrogen peroxide mediates the lethal response evoked by peroxynitrite in U937 cells. Mol. Pharmacol. 61, 870-878.
13. Guidarelli, A., Tommasini, I., Fiorani, M., and Cantoni, O. (2000) Essential role of the mitochondrial respiratory chain in peroxynitrite-induced strand scission of genomic DNA. IUBMB Life 50, 195-201.
14. Fiskum, G., Craig, S. W., Decker, G. L., and Lehninger, A. L. (1980) The cytoskeleton of digitonin-treated rat hepatocytes. Proc. Natl. Acad. Sci. USA 77, 3430-3434.
15. Savini, I., Duflot, S., and Avigliano, L. (2000) Dehydroascorbic acid uptake in a human keratinocyte cell line (HaCaT) is glutathione-independent. Biochem. J. 345, 665-672.
16. 2. Biochem. J. 366, 307-314.
17. Perez-Cruz, I., Carcamo, J. M., and Golde, D. W. (2003) Vitamin C inhibits FAS-induced apoptosis in monocytes and U937 cells. Blood 102, 336-343.
18. Li, X., Cobb, C. E., Hill, K. E., Burk, R. F., and May, J. M. (2001) Mitochondrial uptake and recycling of ascorbic acid. Arch. Biochem. Biophys. 387, 143-153.
19. Cantoni, O. and Guidarelli, A. (2008) Indirect mechanisms of DNA strand scission by peroxynitrite. Methods Enzymol. 440, 111-120.
20. Gardner, P. R. (2002) Aconitase: sensitive target and measure of superoxide. Methods Enzymol. 349, 9-23.
21. Brand, K. A. and Hermfisse, U. (1997) Aerobic glycolysis by proliferating cells: a protective strategy against reactive oxygen species. FASEB J. 11, 388-395.
22. Beckman, J. S. and Crow, J. P. (1993) Pathological implications of nitric oxide, superoxide and peroxynitrite formation. Biochem. Soc. Trans. 21, 330-334.
23. Kooy, N. W., Royall, J. A., Ischiropoulos, H., and Beckman, J. S. (1994) Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Radic. Biol. Med. 16, 149-156.
24. Mukhopadhyay, P., Rajesh, M., Hasko, G., Hawkins, B. J., Madesh, M., et al. (2007) Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat. Protoc. 2, 2295-2301.
25. Guidarelli, A., Fiorani, M., Azzolini, C., and Cantoni, O. (2010) A novel mechanism, uniquely dependent on mitochondrial calcium accumulation, whereby peroxynitrite promotes formation of superoxide/hydrogen peroxide and the ensuing strand scission of genomic DNA. Antioxid. Redox. Signal. 13, 745-756.
26. Lane, D. J. and Lawen, A. (2009) Ascorbate and plasma membrane electron transport-enzymes vs efflux. Free Radic. Biol. Med. 47, 485-495.
27. Azzolini, C., Fiorani, M., Cerioni, L., Guidarelli, A., and Cantoni, O. (2013) Sodium-dependent transport of ascorbic acid in U937 cell mitochondria. IUBMB Life 65, 149-153.
28. Sagun, K., Carcamo, J. M., and Golde, D. W. (2005) Vitamin C enters mitochondria via facilitative glucose transporter 1 (Glut1) and confers mitochondrial protection against oxidative injury. FASEB J. 19, 1657-1667.
29. Lee, Y. C., Huang, H. Y., Chang, C. J., Cheng, C. H., and Chen, Y. T. (2010) Mitochondrial GLUT10 facilitates dehydroascorbic acid import and protects cells against oxidative stress: mechanistic insight into arterial tortuosity syndrome. Hum. Mol. Genet. 19, 3721-3733.
30. 2. Cell Death Differ. 11, 974-984.
31. Tommasini, I., Guidarelli, A., Palomba, L., Cerioni, L., and Cantoni, O. (2006) 5-Hydroxyeicosatetraenoic acid is a key intermediate of the arachidonate-dependent protective signaling in monocytes/macrophages exposed to peroxynitrite. J. Leukoc. Biol. 80, 929-938.
32. Guidarelli, A., Sciorati, C., Clementi, E., and Cantoni, O. (2006) Peroxynitrite mobilizes calcium ions from ryanodine-sensitive stores, a process associated with the mitochondrial accumulation of the cation and the enforced formation of species mediating cleavage of genomic DNA. Free Radic. Biol. Med. 41, 154-164.
33. 2 limits U937 cell survival to peroxynitrite by promoting ERK1/2 dephosphorylation. Biochim. Biophys. Acta 1783, 492-502.
34. 2+ dependence for mitochondrial superoxide formation and permeability transition evoked by peroxynitrite. J. Cell Sci. 120, 1908-1914.
35. Guidarelli, A., De Sanctis, R., Cellini, B., Fiorani, M., Dacha, M., et al. (2001) Intracellular ascorbic acid enhances the DNA single-strand breakage and toxicity induced by peroxynitrite in U937 cells. Biochem. J. 356, 509-513.
36. Guidarelli, A., Fiorani, M., and Cantoni, O. (2004) Enhancing effects of intracellular ascorbic acid on peroxynitrite-induced U937 cell death are mediated by mitochondrial events resulting in enhanced sensitivity to peroxynitrite-dependent inhibition of complex III and formation of hydrogen peroxide. Biochem J. 378, 959-966.
37. Berenson, J. R., Matous, J., Swift, R. A., Mapes, R., Morrison, B., et al. (2007) A phase I/II study of arsenic trioxide/bortezomib/ascorbic acid combination therapy for the treatment of relapsed or refractory multiple myeloma. Clin. Cancer Res. 13, 1762-1768.
38. Grad, J. M., Bahlis, N. J., Reis, I., Oshiro, M. M., Dalton, W. S., et al. (2001) Ascorbic acid enhances arsenic trioxide-induced cytotoxicity in multiple myeloma cells. Blood 98, 805-813.
39. Rollig, C. and Illmer, T. (2009) The efficacy of arsenic trioxide for the treatment of relapsed and refractory multiple myeloma: a systematic review. Cancer Treat. Rev. 35, 425-430.
40. Cerioni, L. and Cantoni O. (2007) ERK1/2 regulates two sequential steps promoting monocyte survival to peroxynitrite. J. Cell Physiol. 210, 177-182.
41. 2 signals monocyte/macrophage survival to peroxynitrite via protein kinase A converging in bad phosphorylation with the protein kinase C α-dependent pathway driven by 5-hydroxyeicosatetraenoic acid. J. Immunol. 181, 5637-5645.
42. Tommasini, I., Guidarelli, A., Cerioni, L., and Cantoni O. (2004) The arachidonate-dependent cytoprotective signaling evoked by peroxynitrite is a general response of the monocyte/macrophage lineage. Biochem. Biophys. Res. Commun. 316, 1191-1195.
43. Di Virgilio, F. (2004) New pathways for reactive oxygen species generation in inflammation and potential novel pharmacological targets. Curr. Pharm. Des. 10, 1647-1652.
44. Mandl, J., Szarka, A., and Banhegyi, G. (2009) Vitamin C: update on physiology and pharmacology. Br. J. Pharmacol. 157, 1097-1110.
45. McLaran, C. J., Bett, J. H., Nye, J. A., and Halliday, J. W. (1982) Congestive cardiomyopathy and haemochromatosis-rapid progression possibly accelerated by excessive ingestion of ascorbic acid. Aust. NZ J. Med. 12, 187-188.
46. Gerster, H. (1999) High-dose vitamin C: a risk for persons with high iron stores? Int. J. Vitam. Nutr. Res. 69, 67-82.
47. Rees, D. C., Kelsey, H., and Richards, J. D. (1993) Acute haemolysis induced by high dose ascorbic acid in glucose-6-phosphate dehydrogenase deficiency. BMJ 306, 841-842.
48. Galley, H. F., Davies, M. J., and Webster, N. R. (1996) Ascorbyl radical formation in patients with sepsis: effect of ascorbate loading. Free Radic. Biol. Med. 20, 139-143.
49. Childs, A., Jacobs, C., Kaminski, T., Halliwell, B., and Leeuwenburgh, C. (2001) Supplementation with vitamin C and N-acetyl-cysteine increases oxidative stress in humans after an acute muscle injury induced by eccentric exercise. Free Radic. Biol. Med. 31, 745-753.
50. Bryer, S. C. and Goldfarb, A. H. (2006) Effect of high dose vitamin C supplementation on muscle soreness, damage, function, and oxidative stress to eccentric exercise. Int. J. Sport. Nutr. Exerc. Metab. 16, 270-280.