Natural iron chelators: Protective role in A549 cells of flavonoids-rich extracts of Citrus juices in Fe3+-induced oxidative stress

Environmental Toxicology and Pharmacology

Volumn 43, Issue , 2016, Pages 248-256

  Ferlazzo, Nadia ^a   Visalli, Giuseppa ^a   Cirmi, Santa ^a   Lombardo, Giovanni Enrico ^a   Laganà, Pasqualina ^a   Di Pietro, Angela ^a   Navarra, Michele ^a  

^a UNIVERSITY OF MESSINA   (Italy)

Author keywords

A549 cells; Bergamot and orange Citrus extracts; Flavonoids; Iron chelating activity; Oxidative stress

Indexed keywords

BIOFLAVONOID; CATALASE; FERROUS SULFATE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; ANTIOXIDANT; IRON; IRON CHELATING AGENT; PLANT EXTRACT;

A549 CELL LINE; ANTIOXIDANT ACTIVITY; ARTICLE; BERGAMOT JUICE; CELL VIABILITY; CHEMICAL COMPOSITION; CONTROLLED STUDY; FRUIT JUICE; GENE EXPRESSION; HUMAN; HUMAN CELL; IRON CHELATION; IRON OVERLOAD; LIPID PEROXIDATION; ORANGE JUICE; OXIDATIVE STRESS; PRIORITY JOURNAL; A-549 CELL LINE; CITRUS; DRUG EFFECTS;

A549 CELLS; ANTIOXIDANTS; CITRUS; HUMANS; IRON; IRON CHELATING AGENTS; OXIDATIVE STRESS; PLANT EXTRACTS;

EID: 84962257846     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2016.03.005     Document Type: Article

References (48)

1. Ak T., Gülçin I. Antioxidant and radical scavenging properties of curcumin. Chem. Biol. Interact. 2008, 174:27-37.
2. Batra P., Sharma A.K. Anti-cancer potential of flavonoids: recent trends and future perspectives. 3 Biotech. 2013, 3:439-459.
3. Brunekreef B., Holgate S.T. Air pollution and health. Lancet 2002, 360:1233-1242.
4. Cabantchik Z.I. Labile iron in cells and body fluids: physiology, pathology, and pharmacology. Front. Pharmacol. 2014, 5:45.
5. Calabrese V., Cornelius C., Dinkova-Kostova A.T., Iavicoli I., Di Paola R., Koverech A., Cuzzocrea S., Rizzarelli E., Calabrese E.J. Cellular stress responses, hormetic phytochemicals and vitagenes in aging and longevity. Biochim. Biophys. Acta 2012, 1822:753-783.
6. Celano M., Maggisano V., De rose R.F., Bulotta S., Maiuolo J., Navarra M., Russo D. Flavonoid fraction of Citrus reticulata juice reduces proliferation and migration of anaplastic thyroid carcinoma cells. Nutr. Cancer 2015, 67:1183-1190.
7. Chen C., Kong A.N. Dietary cancer-chemopreventive compounds: from signaling and gene expression to pharmacological effects. Trends Pharmacol. Sci. 2005, 26:318-326.
8. Chowdhury S.R., Sengupta S., Biswas S., Sen R., Sinha T.K., Basak R.K., Adhikari B., Bhattacharyya A. Low fucose containing bacterial polysaccharide facilitate mitochondria-dependent ROS-induced apoptosis of human lung epithelial carcinoma via controlled regulation of MAPKs-mediated Nrf2/Keap1 homeostasis signaling. Mol. Carcinog. 2015, 54:1636-1655.
9. Costa D.L., Dreher K.L. Bioavailable transition metals in particulate matter mediate cardiopulmonary injury in healthy and compromised animal models. Environ. Health Perspect. 1997, 105:1053-1060.
10. Currò M., Risitano R., Ferlazzo N., Cirmi S., Gangemi C., Caccamo D., Ientile R., Navarra M. Citrus bergamia juice extract attenuates ò-amyloid-induced pro-inflammatory activation of THP -1 cells through MAPK and AP -1 pathways. Sci. Rep. 2016, 6:20809.
11. Day A.J., Mellon F., Barron D., Sarrazin G., Morgan M.R., Williamson G. Human metabolism of dietary flavonoids: identification of plasma metabolites of quercetin. Free Radic. Res. 2001, 35:941-952.
12. Delle Monache S., Sanita P., Trapasso E., Ursino M.R., Dugo P., Russo M., Ferlazzo N., Calapai G., Angelucci A., Navarra M. Mechanisms underlying the anti-tumoral effects of Citrus bergamia juice. PLoS One 2013, 8:e61484.
13. Di Majo D., Giammanco M., La Guardia M., Tripoli E., Giammanco S., Finotti E. Flavanones in Citrus fruit: structure-antioxidant activity relationships. Food Res. Int. 2005, 38:1161-1166.
14. Di Pietro A., Visalli G., Munaò F., Baluce B., La Maestra S., Primerano P., Corigliano F., De Flora S. Oxidative damage in human epithelial alveolar cells exposed in vitro to oil fly ash transition metals. Int. J. Hyg. Environ. Health 2009, 212:196-208.
15. Di Pietro A., Visalli G., Baluce B., Micale R.T., La Maestra S., Spataro P., De Flora S. Multigenerational mitochondrial alterations in pneumocytes exposed to oil fly ash metals. Int. J. Hyg. Environ. Health 2011, 214:138-144.
16. Esposito B.P., Breuer W., Sirankapracha P., Pootrakul P., Hershko C., Cabantchik Z.I. Labile plasma iron in iron overload: redox activity and susceptibility to chelation. Blood 2003, 102:2670-2677.
17. Farina M., Avila D.S., da Rocha J.B., Aschner M. Metals, oxidative stress and neurodegeneration: a focus on iron manganese and mercury. Neurochem. Int. 2013, 62:575-594.
18. Ferlazzo N., Visalli G., Smeriglio A., Cirmi S., Lombardo G.E., Campiglia P., Di Pietro A., Navarra M. Flavonoid fraction of orange and bergamot juices protect human lung epithelial cells from hydrogen peroxide-Induced oxidative stress. Evid. Based Complement. Altern. Med. 2015, 2015:957031.
19. Ferlazzo N., Cirmi S., Russo M., Trapasso E., Ursino M.R., Lombardo G.E., Gangemi S., Calapai G., Navarra M. NF-κB mediates the antiproliferative and proapoptotic effects of bergamot juice in HepG2 cells. Life Sci. 2016, 146:81-91.
20. Ferro E., Visalli G., Currò M., La Rosa M.A., Piraino B., Salpietro C., Di Pietro A. HIF1alpha and Glut1 receptor in transfused and untransfused thalassemic patients. Br. J. Haematol. 2015.
21. Filocamo A., Bisignano C., Ferlazzo N., Cirmi S., Mandalari G., Navarra M. In vitro effect of bergamot (Citrus bergamia) juice against cagA-positive and-negative clinical isolates of Helicobacter pylori. BMC Complement Altern. Med. 2015, 15:256.
22. Gülçin I. Antioxidant activity of food constituents: an overview. Arch. Toxicol. 2012, 86:345-391.
23. Ghio A.J., Silbajoris R., Carson J.L., Samet J.M. Biologic effects of oil fly ash. Environ. Health Perspect. 2002, 110:89-94.
24. Grosso G., Galvano F., Mistretta A., Marventano S., Nolfo F., Calabrese G., Buscemi S., Drago F., Veronesi U., Scuderi A. Red orange: experimental models and epidemiological evidence of its benefits on human health. Oxid. Med. Cell. Longev. 2013, 2013:157240.
25. Hatcher H.C., Singh R.N., Torti F.M., Torti S.V. Synthetic and natural iron chelators: therapeutic potential and clinical use. Future Med. Chem. 2009, 1:1643-1670.
26. Impellizzeri D., Bruschetta G., Di Paola R., Ahmad A., Campolo M., Cuzzocrea S., Esposito E., Navarra M. The anti-inflammatory and antioxidant effects of bergamot juice extract (BJe) in an experimental model of inflammatory bowel disease. Clin. Nutr. 2014, 34:1146-1154.
27. Kalinowski D.S., Richardson D.R. The evolution of iron chelators for the treatment of iron overload disease and cancer. Pharmacol. Rev. 2005, 57:547-583.
28. Knaapen A.M., Shi T.M., Borm P.J.A., Schins R.P.F. Soluble metals as well as the insoluble particle fraction are involved in cellular DNA damage induced by particulate matter. Mol. Cell. Biochem. 2002, 234:317-326.
29. Kode A., Rajendrasozhan S., Caito S., Yang S.R., Megson I.L., Rahman I. Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294:L478-88.
30. Lieu P.T., Heiskala M., Peterson P.A., Yang Y. The roles of iron in health and disease. Mol. Aspects Med. 2001, 22:1-87.
31. Lodovici M., Bigagli E. Oxidative stress and air pollution exposure. J. Toxicol. 2011, 2011:487074.
32. Malesev D., Kuntic V. Investigation of metal-flavonoid chelates and the determination of flavonoids via metal-flavonoid complexing reactions. J. Serb. Chem. Soc. 2007, 72:921-939.
33. Navarra M., Ursino M.R., Ferlazzo N., Russo M., Schumacher U., Valentiner U. Effect of Citrus bergamia juice on human neuroblastoma cells in vitro and in metastatic xenograft models. Fitoterapia 2014, 95:83-92.
34. Navarra M., Mannucci C., Delbo M., Calapai G. Citrus bergamia essential oil: from basic research to clinical application. Front. Pharmacol. 2015, 6:36.
35. Picerno I., Chirico C., Condello S., Visalli G., Ferlazzo N., Gorgone G., Caccamo D., Ientile R. Homocysteine induces DNA damage and alterations in proliferative capacity of T-lymphocytes: a model for immunosenescence?. Biogerontology 2007, 8:111-119.
36. Podder B., Kim Y.S., Song H.Y. Cytoprotective effect of bioactive sea buckthorn extract on paraquat-exposed A549 cells via induction of Nrf2 and its downstream genes. Mol. Med. Rep. 2013, 8:1852-1860.
37. Risitano R., Currò M., Cirmi S., Ferlazzo N., Campiglia P., Caccamo D., Ientile R., Navarra M. Flavonoid fraction of Bergamot juice reduces LPS-induced inflammatory response through SIRT1-mediated NF-kappaB inhibition in THP-1 monocytes. PLoS One 2014, 9:e107431.
38. Scapagnini G., Colombrita C., Amadio M., D'Agata V., Arcelli E., Sapienza M., Quattrone A., Calabrese V. Curcumin activates defensive genes and protects neurons against oxidative stress. Antioxid. Redox Signal. 2006, 8:395-403.
39. Singh A., Misra V., Thimmulappa R.K., Lee H., Ames S., Hoque M.O., Herman J.G., Baylin S.B., Sidransky D., Gabrielson E., Brock M.V., Biswal S. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med. 2006, 3:e420.
40. Stefanson A.L., Bakovic M. Dietary regulation of Keap1/Nrf2/ARE pathway: focus on plant-derived compounds and trace minerals. Nutrients 2014, 6:3777-3801.
41. Suhaimi N.F., Jalaludin J. Biomarker as a research tool in linking exposure to air particles and respiratory health. Biomed. Res. Int. 2015, 962853.
42. Visalli G., Ferlazzo N., Cirmi S., Campiglia P., Gangemi S., Di Pietro A., Calapai G., Navarra M. Bergamot juice extract inhibits proliferation by inducing apoptosis in human colon cancer cells. Anticancer Agents Med. Chem. 2014, 14:1402-1413.
43. Visalli G., Bertuccio M.P., Picerno I., Spataro P., Di Pietro A. Mitochondrial dysfunction by pro-oxidant vanadium: ex vivo assessment of individual susceptibility. Environ. Toxicol. Pharmacol. 2015, 39:93-101.
44. Visalli G., Baluce B., Bertuccio M., Picerno I., Di Pietro A. Mitochondrial-mediated apoptosis pathway in alveolar epithelial cells exposed to the metals in combustion-generated particulate matter. J. Toxicol. Environ. Health A 2015, 78:697-709.
45. Wallace D.C., Fan W.W. The pathophysiology of mitochondrial disease as modeled in the mouse. Genes Dev. 2009, 23:1714-1736.
46. Youdim K.A., Dobbie M.S., Kuhnle G., Proteggente A.R., Abbott N.J., Rice-Evans C. Interaction between flavonoids and the blood-brain barrier: in vitro studies. J. Neurochem. 2003, 85:180-192.
47. Yuan X.M., Li W. Iron involvement in multiple signaling pathways of atherosclerosis: a revisited hypothesis. Curr. Med. Chem. 2008, 15:2157-2172.
48. Zhang P., Omaye S.T. Antioxidant and prooxidant roles for beta-carotene, alpha-tocopherol and ascorbic acid in human lung cells. Toxicol. In Vitro 2001, 15:13-24.